Steroid‐dependent switch of OvoL/Shavenbaby controls self‐renewal versus differentiation of intestinal stem cells

Adult stem cells must continuously fine‐tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell‐intrinsic role for the OvoL fami...

Full description

Saved in:
Bibliographic Details
Published inThe EMBO journal Vol. 40; no. 4; pp. e104347 - n/a
Main Authors Al Hayek, Sandy, Alsawadi, Ahmad, Kambris, Zakaria, Boquete, Jean‐Philippe, Bohère, Jérôme, Immarigeon, Clément, Ronsin, Brice, Plaza, Serge, Lemaitre, Bruno, Payre, François, Osman, Dani
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 15.02.2021
Springer Nature B.V
EMBO Press
John Wiley and Sons Inc
Subjects
Animals
Cell Differentiation
Cell interactions
Cell proliferation
Cell Self Renewal
Cell survival
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
Drosophila
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
EMBO03
EMBO34
EMBO37
enterocyte differentiation
Enterocytes
Epidermal growth factor receptors
Female
Fruit flies
Gene Expression Regulation, Developmental
Hormones
Insects
intestinal stem cells
Intestine
Intestines - physiology
Life Sciences
Male
Organs
Ovaries
OvoL transcription factors
Proteasomes
Signal transduction
Signaling
Stem cells
Stem Cells - cytology
Stem Cells - metabolism
Steroid hormones
Steroids
Steroids - pharmacology
Survival
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
Tumors
Wnt and EFGR pathways
Wnt protein
Wnt and EFGR pathways
intestinal stem cells
enterocyte differentiation
OvoL transcription factors
Drosophila
OvoL
Signal Transduction
Stem Cells & Regenerative Medicine
Wnt and EFGR pathways Subject Categories Cancer
Online AccessGet full text
ISSN0261-4189
1460-2075
1460-2075
DOI10.15252/embj.2019104347

Cover

Abstract Adult stem cells must continuously fine‐tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell‐intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self‐renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post‐translational processing of Svb into a transcriptional activator, whose upregulation induces tumor‐like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and inter‐organ communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells. SYNOPSIS How somatic stem cells integrate cell‐intrinsic and extrinsic cues to fine‐tune their output remains unclear. Here, the OvoL‐family transcription factor Shavenbaby (Svb) is shown to balance Drosophila intestinal stem cell (ISCs) fate decisions in response to systemic hormones. Svb is a direct target of EGFR and Wnt signaling in ISCs. Svb is switched from transcriptional repressor into activator by limited proteasomal degradation. Repressor Svb induces differentiation into enterocytes. Activator Svb promotes survival and proliferation of stem cells. The Svb repressor‐to‐activator switch is remotely induced by ovarian steroids. Graphical Abstract Post‐translational processing of the transcription factor Shavenbaby defines its dichotomous function in fly midgut homeostasis.
AbstractList Adult stem cells must continuously fine‐tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell‐intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self‐renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post‐translational processing of Svb into a transcriptional activator, whose upregulation induces tumor‐like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and inter‐organ communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells.
Adult stem cells must continuously fine‐tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell‐intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self‐renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post‐translational processing of Svb into a transcriptional activator, whose upregulation induces tumor‐like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and inter‐organ communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells. SYNOPSIS How somatic stem cells integrate cell‐intrinsic and extrinsic cues to fine‐tune their output remains unclear. Here, the OvoL‐family transcription factor Shavenbaby (Svb) is shown to balance Drosophila intestinal stem cell (ISCs) fate decisions in response to systemic hormones. Svb is a direct target of EGFR and Wnt signaling in ISCs. Svb is switched from transcriptional repressor into activator by limited proteasomal degradation. Repressor Svb induces differentiation into enterocytes. Activator Svb promotes survival and proliferation of stem cells. The Svb repressor‐to‐activator switch is remotely induced by ovarian steroids. Graphical Abstract Post‐translational processing of the transcription factor Shavenbaby defines its dichotomous function in fly midgut homeostasis.
Adult stem cells must continuously fine‐tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell‐intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self‐renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post‐translational processing of Svb into a transcriptional activator, whose upregulation induces tumor‐like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and inter‐organ communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells. Post‐translational processing of the transcription factor Shavenbaby defines its dichotomous function in fly midgut homeostasis.
Adult stem cells must continuously fine‐tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell‐intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self‐renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post‐translational processing of Svb into a transcriptional activator, whose upregulation induces tumor‐like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and inter‐organ communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells. SYNOPSIS How somatic stem cells integrate cell‐intrinsic and extrinsic cues to fine‐tune their output remains unclear. Here, the OvoL‐family transcription factor Shavenbaby (Svb) is shown to balance Drosophila intestinal stem cell (ISCs) fate decisions in response to systemic hormones. Svb is a direct target of EGFR and Wnt signaling in ISCs. Svb is switched from transcriptional repressor into activator by limited proteasomal degradation. Repressor Svb induces differentiation into enterocytes. Activator Svb promotes survival and proliferation of stem cells. The Svb repressor‐to‐activator switch is remotely induced by ovarian steroids. Post‐translational processing of the transcription factor Shavenbaby defines its dichotomous function in fly midgut homeostasis.
Adult stem cells must continuously fine‐tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell‐intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self‐renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post‐translational processing of Svb into a transcriptional activator, whose upregulation induces tumor‐like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and inter‐organ communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells. image How somatic stem cells integrate cell‐intrinsic and extrinsic cues to fine‐tune their output remains unclear. Here, the OvoL‐family transcription factor Shavenbaby (Svb) is shown to balance Drosophila intestinal stem cell (ISCs) fate decisions in response to systemic hormones. Svb is a direct target of EGFR and Wnt signaling in ISCs. Svb is switched from transcriptional repressor into activator by limited proteasomal degradation. Repressor Svb induces differentiation into enterocytes. Activator Svb promotes survival and proliferation of stem cells. The Svb repressor‐to‐activator switch is remotely induced by ovarian steroids.
Adult stem cells must continuously fine-tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell-intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self-renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post-translational processing of Svb into a transcriptional activator, whose upregulation induces tumor-like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and inter-organ communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells.Adult stem cells must continuously fine-tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell-intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self-renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post-translational processing of Svb into a transcriptional activator, whose upregulation induces tumor-like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and inter-organ communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells.
Adult stem cells must continuously fine-tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to regulate somatic stem cells, the underlying mechanisms remain largely unexplored. Here, we demonstrate a cell-intrinsic role for the OvoL family transcription factor, Shavenbaby (Svb), in balancing self-renewal and differentiation of Drosophila intestinal stem cells. We find that svb is a downstream target of Wnt and EGFR pathways, mediating their activity for stem cell survival and proliferation. This requires post-translational processing of Svb into a transcriptional activator, whose upregulation induces tumor-like stem cell hyperproliferation. In contrast, the unprocessed form of Svb acts as a repressor that imposes differentiation into enterocytes, and suppresses tumors induced by altered signaling. We show that the switch between Svb repressor and activator is triggered in response to systemic steroid hormone, which is produced by ovaries. Therefore, the Svb axis allows intrinsic integration of local signaling cues and interorgan communication to adjust stem cell proliferation versus differentiation, suggesting a broad role of OvoL/Svb in adult and cancer stem cells.
Author Lemaitre, Bruno
Boquete, Jean‐Philippe
Alsawadi, Ahmad
Immarigeon, Clément
Al Hayek, Sandy
Kambris, Zakaria
Bohère, Jérôme
Ronsin, Brice
Payre, François
Plaza, Serge
Osman, Dani
AuthorAffiliation 2 Azm Center for Research in Biotechnology and its Applications LBA3B, EDST, Lebanese University Tripoli Lebanon
6 Present address: Laboratoire de Recherche en Sciences Végétales (LSRV) CNRS UPS Castanet‐Tolosan France
3 Centre de Biologie du Développement (CBD) Centre de Biologie Intégrative (CBI) Université de Toulouse CNRS Toulouse France
4 Biology Department Faculty of Arts and Sciences American University of Beirut Beirut Lebanon
1 Faculty of Sciences III Lebanese University Tripoli Lebanon
5 Global Health Institute, School of Life Sciences Lausanne Switzerland
AuthorAffiliation_xml – name: 4 Biology Department Faculty of Arts and Sciences American University of Beirut Beirut Lebanon
– name: 2 Azm Center for Research in Biotechnology and its Applications LBA3B, EDST, Lebanese University Tripoli Lebanon
– name: 3 Centre de Biologie du Développement (CBD) Centre de Biologie Intégrative (CBI) Université de Toulouse CNRS Toulouse France
– name: 5 Global Health Institute, School of Life Sciences Lausanne Switzerland
– name: 1 Faculty of Sciences III Lebanese University Tripoli Lebanon
– name: 6 Present address: Laboratoire de Recherche en Sciences Végétales (LSRV) CNRS UPS Castanet‐Tolosan France
Author_xml – sequence: 1
  givenname: Sandy
  orcidid: 0000-0003-4623-9626
  surname: Al Hayek
  fullname: Al Hayek, Sandy
  organization: Faculty of Sciences III, Lebanese University, Azm Center for Research in Biotechnology and its Applications, LBA3B, EDST, Lebanese University, Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS
– sequence: 2
  givenname: Ahmad
  surname: Alsawadi
  fullname: Alsawadi, Ahmad
  organization: Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS
– sequence: 3
  givenname: Zakaria
  orcidid: 0000-0002-7377-1899
  surname: Kambris
  fullname: Kambris, Zakaria
  organization: Biology Department, Faculty of Arts and Sciences, American University of Beirut
– sequence: 4
  givenname: Jean‐Philippe
  surname: Boquete
  fullname: Boquete, Jean‐Philippe
  organization: Global Health Institute, School of Life Sciences
– sequence: 5
  givenname: Jérôme
  orcidid: 0000-0001-8305-129X
  surname: Bohère
  fullname: Bohère, Jérôme
  organization: Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS
– sequence: 6
  givenname: Clément
  surname: Immarigeon
  fullname: Immarigeon, Clément
  organization: Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS
– sequence: 7
  givenname: Brice
  surname: Ronsin
  fullname: Ronsin, Brice
  organization: Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS
– sequence: 8
  givenname: Serge
  surname: Plaza
  fullname: Plaza, Serge
  organization: Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS, Laboratoire de Recherche en Sciences Végétales (LSRV), CNRS, UPS
– sequence: 9
  givenname: Bruno
  orcidid: 0000-0001-7970-1667
  surname: Lemaitre
  fullname: Lemaitre, Bruno
  organization: Global Health Institute, School of Life Sciences
– sequence: 10
  givenname: François
  orcidid: 0000-0002-8144-6711
  surname: Payre
  fullname: Payre, François
  email: francois.payre@univ-tlse3.fr
  organization: Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS
– sequence: 11
  givenname: Dani
  orcidid: 0000-0003-3880-3098
  surname: Osman
  fullname: Osman, Dani
  email: dani.osman@ul.edu.lb
  organization: Faculty of Sciences III, Lebanese University, Azm Center for Research in Biotechnology and its Applications, LBA3B, EDST, Lebanese University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33372708$$D View this record in MEDLINE/PubMed
https://hal.science/hal-03065225$$DView record in HAL
BookMark eNqFks1u1DAURi1URKeFPSsUiQ0s0vonjh0JIZWqUNCgLgpry0luOh5l7MFOMpodj9Bn7JPgNKWlIwErS_Y59_qz7wHas84CQi8JPiKccnoMq3J5RDEpCM5YJp6gGclynFIs-B6aYZqTNCOy2EcHISwxxlwK8gztM8YEFVjOUH_ZgXemvvl5XcMabA22S8LGdNUicU1yMbj58eVCD2BLXW6TytnOuzYkAdomOh4sbHSbDOBDH5LaNA3Evc7ozjg7VjC2g9AZG6HQwSqpoG3Dc_S00W2AF3frIfr-8ezb6Xk6v_j0-fRknlacM5GWOZGiJlnJc503BHPOJWVS1nkhZTMeNjWPmfJGFKWudMV4WWFCRIGB5aVkh-j9VHfdlyuoq3gzr1u19mal_VY5bdTjE2sW6soNSkjJMM9igbdTgcWOdn4yV-MeZjjnlPKBRvbNXTPvfvQxtFqZMMbVFlwfFM0EE5xKyiP6egddut7HNxopWRDGKS4i9erP29_3__17EcATUHkXgofmHiFY3Q6IGgdEPQxIVPIdpTLd7WfF_Kb9l_huEjemhe1_G6mzrx--PNLJpIdo2ivwD4n_2vIXq6nj1A
CitedBy_id crossref_primary_10_1016_j_ibmb_2024_104154
crossref_primary_10_1038_s41467_024_55255_1
crossref_primary_10_1016_j_biopha_2023_114350
crossref_primary_10_1096_fj_202400827R
crossref_primary_10_3389_fgene_2021_714152
crossref_primary_10_1371_journal_pgen_1011004
crossref_primary_10_1126_sciadv_adg8816
crossref_primary_10_1016_j_isci_2023_108624
crossref_primary_10_1093_g3journal_jkae204
crossref_primary_10_1016_j_jinsphys_2022_104472
crossref_primary_10_3390_cells13191645
crossref_primary_10_1111_febs_16463
Cites_doi 10.1016/j.gene.2016.11.034
10.1242/jcs.180448
10.1371/journal.pgen.1005634
10.7554/eLife.39748
10.1016/j.devcel.2014.03.006
10.1242/dev.056671
10.1038/nature04333
10.1038/onc.2016.304
10.1016/j.ydbio.2009.10.045
10.1101/gad.1827009
10.1016/j.cell.2014.11.041
10.1016/S0166-2236(00)01791-4
10.1523/JNEUROSCI.18-11-04335.1998
10.1038/nature07329
10.1387/ijdb.15272387
10.1016/j.ydbio.2011.03.033
10.1371/journal.pone.0076773
10.1016/j.celrep.2016.04.020
10.1038/nature05988
10.7554/eLife.55795
10.1242/dev.113357
10.1371/journal.pgen.1004568
10.1186/gb-2013-14-8-r86
10.7554/eLife.33934
10.1126/science.aac5677
10.1186/s40851-015-0031-2
10.1038/s41598-019-43021-z
10.1038/nature10200
10.1016/j.celrep.2012.06.018
10.1016/j.celrep.2013.04.001
10.1038/nature09158
10.1038/srep40056
10.1242/dev.026955
10.15252/embj.201591517
10.15252/embj.201489050
10.3390/genes9030138
10.1053/j.gastro.2015.11.041
10.1038/22330
10.1016/j.gene.2005.10.018
10.1016/S0960-9822(00)00044-0
10.1016/j.celrep.2018.02.073
10.1242/dev.039404
10.1016/0925-4773(94)00305-7
10.1038/nature04371
10.15252/embr.201846273
10.1016/j.ajhg.2015.11.018
10.1016/j.celrep.2014.05.024
10.1016/j.stem.2008.07.024
10.1371/journal.pgen.1001159
10.1038/s41467-018-07569-0
10.1016/j.devcel.2016.10.010
10.1126/science.aab0988
10.1016/j.stemcr.2018.12.008
10.1242/dmm.024232
10.1126/science.1136606
10.1038/nchembio.1964
10.1371/journal.pbio.0040290
10.1016/j.cell.2009.05.014
10.1038/s41586-020-2462-y
10.1038/nature01768
10.1016/j.stemcr.2018.03.014
10.1016/S0925-4773(03)00081-9
10.18632/oncotarget.4629
10.15252/embj.201489072
10.1242/dev.127.4.881
10.1002/dvg.20661
10.1016/j.devcel.2009.11.009
10.1016/S0960-9822(00)00826-5
10.1371/journal.pbio.3000041
10.2147/OTT.S110409
10.1126/science.1188158
10.1242/dev.119.3.897
10.1242/dev.065292
10.1146/annurev-cellbio-100616-060516
10.1038/ncb3052
10.1016/j.stem.2010.11.026
10.1371/journal.pbio.0050106
10.1016/j.celrep.2018.12.079
10.1016/j.cell.2016.06.028
ContentType Journal Article
Copyright The Author(s) 2020
2020 The Authors. Published under the terms of the CC BY 4.0 license
2020 The Authors. Published under the terms of the CC BY 4.0 license.
2020. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Distributed under a Creative Commons Attribution 4.0 International License
Copyright_xml – notice: The Author(s) 2020
– notice: 2020 The Authors. Published under the terms of the CC BY 4.0 license
– notice: 2020 The Authors. Published under the terms of the CC BY 4.0 license.
– notice: 2020. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: Distributed under a Creative Commons Attribution 4.0 International License
DBID C6C
24P
AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7QG
7QL
7QP
7T5
7TK
7TM
7TO
7U9
8FD
C1K
FR3
H94
K9.
M7N
P64
RC3
7X8
1XC
VOOES
5PM
DOI 10.15252/embj.2019104347
DatabaseName Springer Nature OA Free Journals
Wiley Online Library Open Access
CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Animal Behavior Abstracts
Bacteriology Abstracts (Microbiology B)
Calcium & Calcified Tissue Abstracts
Immunology Abstracts
Neurosciences Abstracts
Nucleic Acids Abstracts
Oncogenes and Growth Factors Abstracts
Virology and AIDS Abstracts
Technology Research Database
Environmental Sciences and Pollution Management
Engineering Research Database
AIDS and Cancer Research Abstracts
ProQuest Health & Medical Complete (Alumni)
Algology Mycology and Protozoology Abstracts (Microbiology C)
Biotechnology and BioEngineering Abstracts
Genetics Abstracts
MEDLINE - Academic
Hyper Article en Ligne (HAL)
Hyper Article en Ligne (HAL) (Open Access)
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Virology and AIDS Abstracts
Oncogenes and Growth Factors Abstracts
Technology Research Database
Nucleic Acids Abstracts
ProQuest Health & Medical Complete (Alumni)
Neurosciences Abstracts
Biotechnology and BioEngineering Abstracts
Environmental Sciences and Pollution Management
Genetics Abstracts
Animal Behavior Abstracts
Bacteriology Abstracts (Microbiology B)
Algology Mycology and Protozoology Abstracts (Microbiology C)
AIDS and Cancer Research Abstracts
Immunology Abstracts
Engineering Research Database
Calcium & Calcified Tissue Abstracts
MEDLINE - Academic
DatabaseTitleList Virology and AIDS Abstracts



MEDLINE
CrossRef
MEDLINE - Academic
Database_xml – sequence: 1
  dbid: C6C
  name: Springer Nature OA Free Journals
  url: http://www.springeropen.com/
  sourceTypes: Publisher
– sequence: 2
  dbid: 24P
  name: Wiley Online Library Open Access
  url: https://authorservices.wiley.com/open-science/open-access/browse-journals.html
  sourceTypes: Publisher
– sequence: 3
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 4
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Chemistry
Biology
DocumentTitleAlternate Sandy Al Hayek et al
EISSN 1460-2075
EndPage n/a
ExternalDocumentID PMC7883054
oai_HAL_hal_03065225v2
33372708
10_15252_embj_2019104347
EMBJ2019104347
Genre article
Research Support, Non-U.S. Gov't
Journal Article
GrantInformation_xml – fundername: Federation of European Biochemical Societies (FEBS)
  grantid: Long‐Term Fellowship
  funderid: 10.13039/100012623
– fundername: Agence Nationale de la Recherche (ANR)
  grantid: ChronoNet
  funderid: 10.13039/501100001665
– fundername: American University of Beirut
  grantid: 103782‐24683
  funderid: 10.13039/100007688
– fundername: Agence Universitaire de la Francophonie (AUF)
  grantid: PCSI AUF‐BMO
  funderid: 10.13039/501100002708
– fundername: Fondation pour la Recherche Médicale (FRM)
  grantid: DEQ20170336739
  funderid: 10.13039/501100002915
– fundername: Agence Nationale de la Recherche (ANR)
  funderid: ChronoNet
– fundername: Federation of European Biochemical Societies (FEBS)
  funderid: Long‐Term Fellowship
– fundername: Agence Universitaire de la Francophonie (AUF)
  funderid: PCSI AUF‐BMO
– fundername: Fondation pour la Recherche Médicale (FRM)
  funderid: DEQ20170336739
– fundername: American University of Beirut
  funderid: 103782‐24683
– fundername: ;
  grantid: Long‐Term Fellowship
– fundername: ;
  grantid: PCSI AUF‐BMO
– fundername: ;
  grantid: ChronoNet
– fundername: ;
  grantid: DEQ20170336739
– fundername: ;
  grantid: 103782‐24683
GroupedDBID ---
-DZ
-~X
0R~
123
1OC
24P
29G
2WC
33P
36B
39C
53G
5VS
70F
8R4
8R5
A8Z
AAESR
AAEVG
AAHBH
AAHHS
AAIHA
AAJSJ
AANLZ
AAONW
AAXRX
AAYCA
AAZKR
ABCUV
ABLJU
ACAHQ
ACCFJ
ACCZN
ACGFO
ACGFS
ACNCT
ACPOU
ACPRK
ACXBN
ACXQS
ADBBV
ADEOM
ADKYN
ADMGS
ADOZA
ADXAS
ADZMN
AEEZP
AEGXH
AEIGN
AENEX
AEQDE
AEUYR
AFBPY
AFFNX
AFGKR
AFPWT
AFRAH
AFWVQ
AFZJQ
AHMBA
AIAGR
AIURR
AIWBW
AJBDE
ALAGY
ALIPV
ALMA_UNASSIGNED_HOLDINGS
ALUQN
AMBMR
AMYDB
AOIJS
AUFTA
AZBYB
AZFZN
AZVAB
BAWUL
BDRZF
BENPR
BFHJK
BMNLL
BMXJE
BRXPI
BTFSW
C6C
CS3
DCZOG
DIK
DPXWK
DRFUL
DRSTM
DU5
E3Z
EBD
EBLON
EBS
EMB
EMOBN
F5P
G-S
GROUPED_DOAJ
GX1
HH5
HK~
HYE
KQ8
LATKE
LEEKS
LITHE
LOXES
LUTES
LYRES
MEWTI
MRFUL
MRSTM
MSFUL
MSSTM
MVM
MXFUL
MXSTM
MY~
O9-
OK1
P2P
P2W
Q2X
R.K
RHF
RHI
RNS
ROL
RPM
SV3
TN5
TR2
WBKPD
WH7
WIH
WIK
WIN
WOHZO
WXSBR
WYJ
YSK
ZCA
ZZTAW
~KM
ABJNI
AAMMB
AASML
AAYXX
ABZEH
AEFGJ
AGXDD
AIDQK
AIDYY
AJAOE
CITATION
ESTFP
NAO
CGR
CUY
CVF
ECM
EIF
NPM
7QG
7QL
7QP
7T5
7TK
7TM
7TO
7U9
8FD
C1K
FR3
H94
K9.
M7N
P64
RC3
7X8
1XC
VOOES
5PM
AASGY
ID FETCH-LOGICAL-c5537-b6187d14b56a6f1055582388d6988f6187fd50586f79bacac35bc011790e36b83
IEDL.DBID 24P
ISSN 0261-4189
1460-2075
IngestDate Tue Sep 30 15:41:43 EDT 2025
Fri Sep 12 12:49:53 EDT 2025
Sun Sep 28 01:37:37 EDT 2025
Sat Aug 23 13:21:15 EDT 2025
Mon Jul 21 06:07:08 EDT 2025
Thu Apr 24 22:52:05 EDT 2025
Wed Oct 01 02:30:16 EDT 2025
Wed Jan 22 16:30:21 EST 2025
Fri Feb 21 02:37:18 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 4
Keywords Wnt and EFGR pathways
intestinal stem cells
enterocyte differentiation
OvoL transcription factors
Drosophila
OvoL
Signal Transduction
Stem Cells & Regenerative Medicine
Wnt and EFGR pathways Subject Categories Cancer
Language English
License Attribution
2020 The Authors. Published under the terms of the CC BY 4.0 license.
Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c5537-b6187d14b56a6f1055582388d6988f6187fd50586f79bacac35bc011790e36b83
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
PMCID: PMC7883054
ORCID 0000-0001-8305-129X
0000-0002-8144-6711
0000-0003-4623-9626
0000-0002-7377-1899
0000-0003-3880-3098
0000-0001-7970-1667
0000-0002-3492-109X
OpenAccessLink https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.2019104347
PMID 33372708
PQID 2489135209
PQPubID 35985
PageCount 23
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_7883054
hal_primary_oai_HAL_hal_03065225v2
proquest_miscellaneous_2473752825
proquest_journals_2489135209
pubmed_primary_33372708
crossref_primary_10_15252_embj_2019104347
crossref_citationtrail_10_15252_embj_2019104347
wiley_primary_10_15252_embj_2019104347_EMBJ2019104347
springer_journals_10_15252_embj_2019104347
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 15 February 2021
PublicationDateYYYYMMDD 2021-02-15
PublicationDate_xml – month: 02
  year: 2021
  text: 15 February 2021
  day: 15
PublicationDecade 2020
PublicationPlace London
PublicationPlace_xml – name: London
– name: England
– name: New York
– name: Hoboken
PublicationTitle The EMBO journal
PublicationTitleAbbrev EMBO J
PublicationTitleAlternate EMBO J
PublicationYear 2021
Publisher Nature Publishing Group UK
Springer Nature B.V
EMBO Press
John Wiley and Sons Inc
Publisher_xml – name: Nature Publishing Group UK
– name: Springer Nature B.V
– name: EMBO Press
– name: John Wiley and Sons Inc
References Kitazawa, Hikichi, Nakamura, Mitsunaga, Tanaka, Nakamura, Yamakawa, Furukawa, Takasaka, Goshima (CR32) 2016; 15
Frankel, Davis, Vargas, Wang, Payre, Stern (CR19) 2010; 466
Jin, Ha, Fores, Xiang, Glasser, Maldera, Jimenez, Edgar (CR29) 2015; 11
Roca, Hernandez, Weidner, McEachin, Fuller, Sud, Schumann, Wilkinson, Zaslavsky, Li (CR58) 2013; 8
Zeng, Chauhan, Hou (CR70) 2010; 48
Normanno, De Luca, Bianco, Strizzi, Mancino, Maiello, Carotenuto, De Feo, Caponigro, Salomon (CR45) 2006; 366
Furriols, Bray (CR203) 2001; 11
Preger‐Ben Noon, Sabaris, Ortiz, Sager, Liebowitz, Stern, Frankel (CR55) 2018; 22
Ray, Rosenberg, Chanut‐Delalande, Decaras, Schwertner, Toubiana, Auman, Schnellhammer, Teuscher, Valenti (CR57) 2019; 8
Micchelli, Perrimon (CR43) 2006; 439
Antonello, Reiff, Ballesta‐Illan, Dominguez (CR3) 2015; 34
Wang, Zeng, Ryoo, Jasper (CR205) 2014; 10
Buchon, Osman, David, Fang, Boquete, Deplancke, Lemaitre (CR12) 2013; 3
Cooper, Bray (CR202) 2000; 10
Menoret, Santolini, Fernandes, Spokony, Zanet, Gonzalez, Latapie, Ferrer, Rouault, White (CR41) 2013; 14
Ahmed, Maldera, Krunic, Paiva‐Silva, Penalva, Teleman, Edgar (CR1) 2020; 584
Crocker, Abe, Rinaldi, McGregor, Frankel, Wang, Alsawadi, Valenti, Plaza, Payre (CR15) 2015; 160
Nieto, Huang, Jackson, Thiery (CR44) 2016; 166
Bohere, Mancheno‐Ferris, Al Hayek, Zanet, Valenti, Akino, Yamabe, Inagaki, Chanut‐Delalande, Plaza (CR10) 2018; 9
Haensel, Sun, MacLean, Ma, Zhou, Stemmler, Brabletz, Berx, Plikus, Nie (CR24) 2019; 20
Jiang, Edgar (CR26) 2009; 136
Saghatelian, Couso (CR59) 2015; 11
Biteau, Karpac, Supoyo, Degennaro, Lehmann, Jasper (CR9) 2010; 6
Uryu, Ameku, Niwa (CR62) 2015; 1
Pueyo, Couso (CR56) 2011; 355
Kondo, Plaza, Zanet, Benrabah, Valenti, Hashimoto, Kobayashi, Payre, Kageyama (CR33) 2010; 329
Payre, Vincent, Carreno (CR50) 1999; 400
Lee, Luo (CR36) 2001; 24
Fernandes, Chanut‐Delalande, Ferrer, Latapie, Waltzer, Affolter, Payre, Plaza (CR18) 2010; 18
Delon, Chanut‐Delalande, Payre (CR17) 2003; 120
Loza‐Coll, Southall, Sandall, Brand, Jones (CR39) 2014; 33
Biteau, Hochmuth, Jasper (CR6) 2008; 3
Ohlstein, Spradling (CR46) 2006; 439
Fu, Qi, Chen, He, Zhang, Guo (CR21) 2016; 9
Lapan, Reddien (CR35) 2012; 2
Oliver, Kim, Baker (CR48) 1993; 119
Plaza, Menschaert, Payre (CR53) 2017; 33
Mevel‐Ninio, Terracol, Salles, Vincent, Payre (CR42) 1995; 49
Xu, Tang, Hung, Hu, Ni, Housden, Perrimon (CR66) 2019; 26
Lin, Xu, Xi (CR38) 2008; 455
Watanabe, Liu, Noguchi, Murray, Chang, Kishima, Nishimura, Hashimoto, Minoda, Suzuki (CR64) 2019; 9
Jolly, Jia, Boareto, Mani, Pienta, Ben‐Jacob, Levine (CR30) 2015; 6
Izumi, Motoishi, Furuse, Furuse (CR204) 2016; 129
Sucena, Delon, Jones, Payre, Stern (CR60) 2003; 424
Frankel, Erezyilmaz, McGregor, Wang, Payre, Stern (CR20) 2011; 474
Perdigoto, Schweisguth, Bardin (CR51) 2011; 138
Zanet, Benrabah, Li, Pelissier‐Monier, Chanut‐Delalande, Ronsin, Bellen, Payre, Plaza (CR69) 2015; 349
Bardin, Perdigoto, Southall, Brand, Schweisguth (CR4) 2010; 137
Li, Jasper (CR37) 2016; 9
Ohlstein, Spradling (CR47) 2007; 315
Zeng, Hou (CR71) 2015; 142
Zipper, Jassmann, Burgmer, Gorlich, Reiff (CR73) 2020; 9
Guo, Ohlstein (CR23) 2015; 350
Payre (CR49) 2004; 48
Andrews, Garcia‐Estefania, Delon, Lu, Mevel‐Ninio, Spierer, Payre, Pauli, Oliver (CR2) 2000; 127
Tang, Zhao, Buchon, Engstrom (CR61) 2018; 10
Biteau, Jasper (CR7) 2011; 138
Preger‐Ben Noon, Davis, Stern (CR54) 2016; 39
Chen, Sayadian, Lowe, Lovegrove, St Johnston (CR201) 2018; 16
Kagawa, Shimamoto, Kim, Oceguera‐Yanez, Yamamoto, Schroeder, Woltjen (CR31) 2019; 12
Davidson, Liskova, Evans, Dudakova, Noskova, Pontikos, Hartmannova, Hodanova, Stranecky, Kozmik (CR16) 2016; 98
Chanut‐Delalande, Fernandes, Roch, Payre, Plaza (CR13) 2006; 4
Beebe, Lee, Micchelli (CR5) 2010; 338
Chanut‐Delalande, Hashimoto, Pelissier‐Monier, Spokony, Dib, Kondo, Bohere, Niimi, Latapie, Inagaki (CR14) 2014; 16
Buchon, Broderick, Chakrabarti, Lemaitre (CR11) 2009; 23
Ye, Sun, Jiao, Chen, Liu, Huang, Zhang, Cai, Li, Wu (CR68) 2016; 150
Jiang, Patel, Kohlmaier, Grenley, McEwen, Edgar (CR28) 2009; 137
Zhan, Rindtorff, Boutros (CR72) 2017; 36
Korzelius, Naumann, Loza‐Coll, Chan, Dutta, Oberheim, Glasser, Southall, Brand, Jones (CR34) 2014; 33
Xu, Liu, Wang, Wong, Song (CR67) 2018; 7
Hayashi, Shinozuka, Shigenobu, Sato, Sugimoto, Ito, Abe, Kobayashi (CR25) 2017; 7
Galindo, Pueyo, Fouix, Bishop, Couso (CR22) 2007; 5
Jiang, Grenley, Bravo, Blumhagen, Edgar (CR27) 2011; 8
Balakireva, Stocker, Gendre, Ferveur (CR200) 1998; 18
McGregor, Orgogozo, Delon, Zanet, Srinivasan, Payre, Stern (CR40) 2007; 448
Watanabe, Villarreal‐Ponce, Sun, Salmans, Fallahi, Andersen, Dai (CR65) 2014; 29
Wang, Li, Hu, Yang, Yan, Wu, Li, Guo (CR63) 2017; 600
Biteau, Jasper (CR8) 2014; 7
Perochon, Carroll, Cordero (CR52) 2018; 9
2015; 34
2017; 7
2011; 355
2013; 3
2010; 18
2010; 466
2019; 12
2015; 142
1999; 400
2008; 3
2014; 29
2015; 349
2016; 39
2013; 8
2011; 474
2018; 7
1998; 18
2018; 9
2013; 14
2019; 20
2017; 36
2000; 127
2000; 10
2017; 33
2019; 26
2020; 9
2014; 16
2007; 5
2001; 11
2014; 7
2010; 6
2017; 600
2003; 120
2014; 10
2006; 366
2016; 150
2011; 138
2009; 23
2019; 8
2015; 1
2015; 160
2019; 9
2015; 6
2007; 448
2006; 439
2010; 329
2016; 129
2004; 48
2015; 11
2016; 98
2016; 166
2020; 584
2006; 4
2018; 22
2001; 24
2016; 15
2009; 136
2011; 8
2009; 137
2015; 350
2012; 2
2010; 48
2007; 315
1993; 119
2003; 424
2010; 338
1995; 49
2010; 137
2008; 455
2018; 10
2018; 16
2016; 9
2014; 33
e_1_2_8_28_1
e_1_2_8_24_1
e_1_2_8_47_1
e_1_2_8_26_1
e_1_2_8_49_1
e_1_2_8_68_1
e_1_2_8_3_1
e_1_2_8_5_1
e_1_2_8_7_1
e_1_2_8_9_1
e_1_2_8_20_1
e_1_2_8_43_1
e_1_2_8_66_1
e_1_2_8_22_1
e_1_2_8_45_1
e_1_2_8_64_1
e_1_2_8_62_1
e_1_2_8_41_1
e_1_2_8_60_1
e_1_2_8_17_1
e_1_2_8_19_1
e_1_2_8_13_1
e_1_2_8_36_1
e_1_2_8_59_1
e_1_2_8_15_1
e_1_2_8_38_1
e_1_2_8_57_1
e_1_2_8_70_1
e_1_2_8_32_1
e_1_2_8_55_1
e_1_2_8_78_1
e_1_2_8_11_1
e_1_2_8_34_1
e_1_2_8_53_1
e_1_2_8_76_1
e_1_2_8_51_1
e_1_2_8_74_1
e_1_2_8_30_1
e_1_2_8_72_1
e_1_2_8_29_1
e_1_2_8_25_1
e_1_2_8_46_1
e_1_2_8_27_1
e_1_2_8_48_1
e_1_2_8_69_1
e_1_2_8_2_1
e_1_2_8_80_1
e_1_2_8_4_1
e_1_2_8_6_1
e_1_2_8_8_1
e_1_2_8_21_1
e_1_2_8_42_1
e_1_2_8_67_1
e_1_2_8_23_1
e_1_2_8_44_1
e_1_2_8_65_1
e_1_2_8_63_1
e_1_2_8_40_1
e_1_2_8_61_1
e_1_2_8_18_1
e_1_2_8_39_1
e_1_2_8_14_1
e_1_2_8_35_1
e_1_2_8_16_1
e_1_2_8_37_1
e_1_2_8_58_1
e_1_2_8_79_1
e_1_2_8_10_1
e_1_2_8_31_1
e_1_2_8_56_1
e_1_2_8_77_1
e_1_2_8_12_1
e_1_2_8_33_1
e_1_2_8_54_1
e_1_2_8_75_1
e_1_2_8_52_1
e_1_2_8_73_1
e_1_2_8_50_1
e_1_2_8_71_1
References_xml – volume: 7
  year: 2018
  ident: CR67
  article-title: Temporospatial induction of homeodomain gene cut dictates natural lineage reprogramming
  publication-title: Elife
– volume: 3
  start-page: 442
  year: 2008
  end-page: 455
  ident: CR6
  article-title: JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging gut
  publication-title: Cell Stem Cell
– volume: 138
  start-page: 1045
  year: 2011
  end-page: 1055
  ident: CR7
  article-title: EGF signaling regulates the proliferation of intestinal stem cells in
  publication-title: Development
– volume: 7
  start-page: 1867
  year: 2014
  end-page: 1875
  ident: CR8
  article-title: Slit/Robo signaling regulates cell fate decisions in the intestinal stem cell lineage of
  publication-title: Cell Rep
– volume: 166
  start-page: 21
  year: 2016
  end-page: 45
  ident: CR44
  article-title: Emt: 2016
  publication-title: Cell
– volume: 29
  start-page: 59
  year: 2014
  end-page: 74
  ident: CR65
  article-title: Mammary morphogenesis and regeneration require the inhibition of EMT at terminal end buds by Ovol2 transcriptional repressor
  publication-title: Dev Cell
– volume: 98
  start-page: 75
  year: 2016
  end-page: 89
  ident: CR16
  article-title: Autosomal‐dominant corneal endothelial dystrophies CHED1 and PPCD1 are allelic disorders caused by non‐coding mutations in the promoter of OVOL2
  publication-title: Am J Hum Genet
– volume: 136
  start-page: 483
  year: 2009
  end-page: 493
  ident: CR26
  article-title: EGFR signaling regulates the proliferation of adult midgut progenitors
  publication-title: Development
– volume: 6
  start-page: 25161
  year: 2015
  end-page: 25174
  ident: CR30
  article-title: Coupling the modules of EMT and stemness: a tunable “stemness window” model
  publication-title: Oncotarget
– volume: 329
  start-page: 336
  year: 2010
  end-page: 339
  ident: CR33
  article-title: Small peptides switch the transcriptional activity of Shavenbaby during embryogenesis
  publication-title: Science
– volume: 11
  year: 2015
  ident: CR29
  article-title: EGFR/Ras signaling controls intestinal stem cell proliferation via capicua‐regulated genes
  publication-title: PLoS Genet
– volume: 400
  start-page: 271
  year: 1999
  end-page: 275
  ident: CR50
  article-title: ovo/svb integrates Wingless and DER pathways to control epidermis differentiation
  publication-title: Nature
– volume: 4
  start-page: e290
  year: 2006
  ident: CR13
  article-title: Shavenbaby couples patterning to epidermal cell shape control
  publication-title: PLoS Biol
– volume: 8
  year: 2019
  ident: CR57
  article-title: The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning
  publication-title: Elife
– volume: 22
  start-page: 3021
  year: 2018
  end-page: 3031
  ident: CR55
  article-title: Comprehensive analysis of a cis‐regulatory region reveals pleiotropy in enhancer function
  publication-title: Cell Rep
– volume: 142
  start-page: 644
  year: 2015
  end-page: 653
  ident: CR71
  article-title: Enteroendocrine cells are generated from stem cells through a distinct progenitor in the adult posterior midgut
  publication-title: Development
– volume: 15
  start-page: 1359
  year: 2016
  end-page: 1368
  ident: CR32
  article-title: OVOL2 maintains the transcriptional program of human corneal epithelium by suppressing epithelial‐to‐mesenchymal transition
  publication-title: Cell Rep
– volume: 137
  start-page: 705
  year: 2010
  end-page: 714
  ident: CR4
  article-title: Transcriptional control of stem cell maintenance in the intestine
  publication-title: Development
– volume: 9
  start-page: 6490
  year: 2019
  ident: CR64
  article-title: OVOL2 induces mesenchymal‐to‐epithelial transition in fibroblasts and enhances cell‐state reprogramming towards epithelial lineages
  publication-title: Sci Rep
– volume: 7
  start-page: 40056
  year: 2017
  ident: CR25
  article-title: Conserved role of Ovo in germline development in mouse and
  publication-title: Sci Rep
– volume: 600
  start-page: 1
  year: 2017
  end-page: 8
  ident: CR63
  article-title: Ovol2 gene inhibits the Epithelial‐to‐Mesenchymal Transition in lung adenocarcinoma by transcriptionally repressing Twist1
  publication-title: Gene
– volume: 127
  start-page: 881
  year: 2000
  end-page: 892
  ident: CR2
  article-title: OVO transcription factors function antagonistically in the female germline
  publication-title: Development
– volume: 33
  start-page: 2967
  year: 2014
  end-page: 2982
  ident: CR34
  article-title: Escargot maintains stemness and suppresses differentiation in intestinal stem cells
  publication-title: EMBO J
– volume: 34
  start-page: 2025
  year: 2015
  end-page: 2041
  ident: CR3
  article-title: Robust intestinal homeostasis relies on cellular plasticity in enteroblasts mediated by miR‐8‐Escargot switch
  publication-title: EMBO J
– volume: 474
  start-page: 598
  year: 2011
  end-page: 603
  ident: CR20
  article-title: Morphological evolution caused by many subtle‐effect substitutions in regulatory DNA
  publication-title: Nature
– volume: 5
  start-page: e106
  year: 2007
  ident: CR22
  article-title: Peptides encoded by short ORFs control development and define a new eukaryotic gene family
  publication-title: PLoS Biol
– volume: 12
  start-page: 319
  year: 2019
  end-page: 332
  ident: CR31
  article-title: OVOL1 Influences the determination and expansion of iPSC reprogramming intermediates
  publication-title: Stem Cell Rep
– volume: 11
  start-page: 60
  year: 2001
  end-page: 64
  ident: CR203
  article-title: A model Notch response element detects Suppressor of Hairless‐dependent molecular switch
  publication-title: Curr Biol
– volume: 3
  start-page: 1725
  year: 2013
  end-page: 1738
  ident: CR12
  article-title: Morphological and molecular characterization of adult midgut compartmentalization in
  publication-title: Cell Rep
– volume: 16
  year: 2018
  ident: CR201
  article-title: An alternative mode of epithelial polarity in the Drosophila midgut
  publication-title: PLoS Biol
– volume: 439
  start-page: 475
  year: 2006
  end-page: 479
  ident: CR43
  article-title: Evidence that stem cells reside in the adult midgut epithelium
  publication-title: Nature
– volume: 129
  start-page: 1155
  year: 2016
  end-page: 1164
  ident: CR204
  article-title: A tetraspanin regulates septate junction formation in Drosophila midgut
  publication-title: J Cell Sci
– volume: 119
  start-page: 897
  year: 1993
  end-page: 908
  ident: CR48
  article-title: Sex‐lethal, master and slave: a hierarchy of germ‐line sex determination in
  publication-title: Development
– volume: 33
  start-page: 2983
  year: 2014
  end-page: 2996
  ident: CR39
  article-title: Regulation of intestinal stem cell maintenance and differentiation by the transcription factor Escargot
  publication-title: EMBO J
– volume: 350
  start-page: aab0988
  year: 2015
  ident: CR23
  article-title: Stem cell regulation. Bidirectional Notch signaling regulates intestinal stem cell multipotency
  publication-title: Science
– volume: 315
  start-page: 988
  year: 2007
  end-page: 992
  ident: CR47
  article-title: Multipotent intestinal stem cells specify daughter cell fates by differential notch signaling
  publication-title: Science
– volume: 160
  start-page: 191
  year: 2015
  end-page: 203
  ident: CR15
  article-title: Low affinity binding site clusters confer hox specificity and regulatory robustness
  publication-title: Cell
– volume: 20
  year: 2019
  ident: CR24
  article-title: An Ovol2‐Zeb1 transcriptional circuit regulates epithelial directional migration and proliferation
  publication-title: EMBO Rep
– volume: 138
  start-page: 4585
  year: 2011
  end-page: 4595
  ident: CR51
  article-title: Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine
  publication-title: Development
– volume: 48
  start-page: 207
  year: 2004
  end-page: 215
  ident: CR49
  article-title: Genetic control of epidermis differentiation in
  publication-title: Int J Dev Biol
– volume: 49
  start-page: 83
  year: 1995
  end-page: 95
  ident: CR42
  article-title: ovo, a gene required for ovarian development, is specifically expressed in the germline and shares most of its coding sequences with shavenbaby, a gene involved in embryo patterning
  publication-title: Mech Dev
– volume: 355
  start-page: 183
  year: 2011
  end-page: 193
  ident: CR56
  article-title: Tarsal‐less peptides control Notch signalling through the Shavenbaby transcription factor
  publication-title: Dev Biol
– volume: 448
  start-page: 587
  year: 2007
  end-page: 590
  ident: CR40
  article-title: Morphological evolution through multiple cis‐regulatory mutations at a single gene
  publication-title: Nature
– volume: 14
  start-page: R86
  year: 2013
  ident: CR41
  article-title: Genome‐wide analyses of Shavenbaby target genes reveals distinct features of enhancer organization
  publication-title: Genome Biol
– volume: 424
  start-page: 935
  year: 2003
  end-page: 938
  ident: CR60
  article-title: Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism
  publication-title: Nature
– volume: 338
  start-page: 28
  year: 2010
  end-page: 37
  ident: CR5
  article-title: JAK/STAT signaling coordinates stem cell proliferation and multilineage differentiation in the intestinal stem cell lineage
  publication-title: Dev Biol
– volume: 9
  start-page: 5963
  year: 2016
  end-page: 5973
  ident: CR21
  article-title: Expression of Ovol2 is related to epithelial characteristics and shows a favorable clinical outcome in hepatocellular carcinoma
  publication-title: Onco Targets Ther
– volume: 366
  start-page: 2
  year: 2006
  end-page: 16
  ident: CR45
  article-title: Epidermal growth factor receptor (EGFR) signaling in cancer
  publication-title: Gene
– volume: 10
  year: 2014
  ident: CR205
  article-title: Integration of UPRER and oxidative stress signaling in the control of intestinal stem cell proliferation
  publication-title: PLoS Genet
– volume: 10
  start-page: 1507
  year: 2000
  end-page: 1510
  ident: CR202
  article-title: R7 photoreceptor specification requires Notch activity
  publication-title: Curr Biol
– volume: 466
  start-page: 490
  year: 2010
  end-page: 493
  ident: CR19
  article-title: Phenotypic robustness conferred by apparently redundant transcriptional enhancers
  publication-title: Nature
– volume: 24
  start-page: 251
  year: 2001
  end-page: 254
  ident: CR36
  article-title: Mosaic analysis with a repressible cell marker (MARCM) for neural development
  publication-title: Trends Neurosci
– volume: 48
  start-page: 607
  year: 2010
  end-page: 611
  ident: CR70
  article-title: Characterization of midgut stem cell‐ and enteroblast‐specific Gal4 lines in
  publication-title: Genesis
– volume: 137
  start-page: 1343
  year: 2009
  end-page: 1355
  ident: CR28
  article-title: Cytokine/Jak/Stat Signaling Mediates Regeneration and Homeostasis in the Midgut
  publication-title: Cell
– volume: 349
  start-page: 1356
  year: 2015
  end-page: 1358
  ident: CR69
  article-title: Pri sORF peptides induce selective proteasome‐mediated protein processing
  publication-title: Science
– volume: 18
  start-page: 4335
  year: 1998
  end-page: 4343
  ident: CR200
  article-title: Voila, a new Drosophila courtship variant that affects the nervous system: behavioral, neural, and genetic characterization
  publication-title: J Neurosci
– volume: 18
  start-page: 64
  year: 2010
  end-page: 76
  ident: CR18
  article-title: Zona pellucida domain proteins remodel the apical compartment for localized cell shape changes
  publication-title: Dev Cell
– volume: 8
  start-page: 84
  year: 2011
  end-page: 95
  ident: CR27
  article-title: EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in
  publication-title: Cell Stem Cell
– volume: 26
  start-page: 670
  year: 2019
  end-page: 688 e6
  ident: CR66
  article-title: The septate junction protein Tsp2A restricts intestinal stem cell activity via endocytic regulation of aPKC and hippo signaling
  publication-title: Cell Rep
– volume: 9
  start-page: 5123
  year: 2018
  ident: CR10
  article-title: Shavenbaby and Yorkie mediate Hippo signaling to protect adult stem cells from apoptosis
  publication-title: Nat Commun
– volume: 8
  year: 2013
  ident: CR58
  article-title: Transcription factors OVOL1 and OVOL2 induce the mesenchymal to epithelial transition in human cancer
  publication-title: PLoS One
– volume: 36
  start-page: 1461
  year: 2017
  end-page: 1473
  ident: CR72
  article-title: Wnt signaling in cancer
  publication-title: Oncogene
– volume: 120
  start-page: 747
  year: 2003
  end-page: 758
  ident: CR17
  article-title: The Ovo/Shavenbaby transcription factor specifies actin remodelling during epidermal differentiation in
  publication-title: Mech Dev
– volume: 455
  start-page: 1119
  year: 2008
  end-page: 1123
  ident: CR38
  article-title: Paracrine Wingless signalling controls self‐renewal of intestinal stem cells
  publication-title: Nature
– volume: 33
  start-page: 391
  year: 2017
  end-page: 416
  ident: CR53
  article-title: In search of lost small peptides
  publication-title: Annu Rev Cell Dev Biol
– volume: 584
  start-page: 415
  year: 2020
  end-page: 419
  ident: CR1
  article-title: Fitness trade‐offs incurred by ovary‐to‐gut steroid signalling in
  publication-title: Nature
– volume: 23
  start-page: 2333
  year: 2009
  end-page: 2344
  ident: CR11
  article-title: Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in
  publication-title: Genes Dev
– volume: 150
  start-page: 659
  year: 2016
  end-page: 671
  ident: CR68
  article-title: OVOL2, an inhibitor of WNT signaling, reduces invasive activities of human and mouse cancer cells and is down‐regulated in human colorectal tumors
  publication-title: Gastroenterology
– volume: 11
  start-page: 909
  year: 2015
  end-page: 916
  ident: CR59
  article-title: Discovery and characterization of smORF‐encoded bioactive polypeptides
  publication-title: Nat Chem Biol
– volume: 2
  start-page: 294
  year: 2012
  end-page: 307
  ident: CR35
  article-title: Transcriptome analysis of the planarian eye identifies ovo as a specific regulator of eye regeneration
  publication-title: Cell Rep
– volume: 6
  year: 2010
  ident: CR9
  article-title: Lifespan extension by preserving proliferative homeostasis in
  publication-title: PLoS Genet
– volume: 39
  start-page: 572
  year: 2016
  end-page: 584
  ident: CR54
  article-title: Evolved Repression Overcomes Enhancer Robustness
  publication-title: Dev Cell
– volume: 10
  start-page: 1565
  year: 2018
  end-page: 1578
  ident: CR61
  article-title: The POU/Oct transcription factor nubbin controls the balance of intestinal stem cell maintenance and differentiation by isoform‐specific regulation
  publication-title: Stem Cell Rep
– volume: 1
  start-page: 32
  year: 2015
  ident: CR62
  article-title: Recent progress in understanding the role of ecdysteroids in adult insects: Germline development and circadian clock in the fruit fly
  publication-title: Zoological Lett
– volume: 16
  start-page: 1035
  year: 2014
  end-page: 1044
  ident: CR14
  article-title: Pri peptides are mediators of ecdysone for the temporal control of development
  publication-title: Nat Cell Biol
– volume: 439
  start-page: 470
  year: 2006
  end-page: 474
  ident: CR46
  article-title: The adult posterior midgut is maintained by pluripotent stem cells
  publication-title: Nature
– volume: 9
  start-page: 138
  year: 2018
  ident: CR52
  article-title: Wnt signalling in intestinal stem cells: lessons from mice and flies
  publication-title: Genes
– volume: 9
  year: 2020
  ident: CR73
  article-title: Ecdysone steroid hormone remote controls intestinal stem cell fate decisions via the PPARgamma‐homolog Eip75B in
  publication-title: Elife
– volume: 9
  start-page: 487
  year: 2016
  end-page: 499
  ident: CR37
  article-title: Gastrointestinal stem cells in health and disease: from flies to humans
  publication-title: Dis Model Mech
– volume: 4
  start-page: e290
  year: 2006
  article-title: Shavenbaby couples patterning to epidermal cell shape control
  publication-title: PLoS Biol
– volume: 39
  start-page: 572
  year: 2016
  end-page: 584
  article-title: Evolved Repression Overcomes Enhancer Robustness
  publication-title: Dev Cell
– volume: 9
  start-page: 6490
  year: 2019
  article-title: OVOL2 induces mesenchymal‐to‐epithelial transition in fibroblasts and enhances cell‐state reprogramming towards epithelial lineages
  publication-title: Sci Rep
– volume: 6
  year: 2010
  article-title: Lifespan extension by preserving proliferative homeostasis in
  publication-title: PLoS Genet
– volume: 448
  start-page: 587
  year: 2007
  end-page: 590
  article-title: Morphological evolution through multiple cis‐regulatory mutations at a single gene
  publication-title: Nature
– volume: 9
  year: 2020
  article-title: Ecdysone steroid hormone remote controls intestinal stem cell fate decisions via the PPARgamma‐homolog Eip75B in
  publication-title: Elife
– volume: 2
  start-page: 294
  year: 2012
  end-page: 307
  article-title: Transcriptome analysis of the planarian eye identifies ovo as a specific regulator of eye regeneration
  publication-title: Cell Rep
– volume: 15
  start-page: 1359
  year: 2016
  end-page: 1368
  article-title: OVOL2 maintains the transcriptional program of human corneal epithelium by suppressing epithelial‐to‐mesenchymal transition
  publication-title: Cell Rep
– volume: 26
  start-page: 670
  year: 2019
  end-page: 688 e6
  article-title: The septate junction protein Tsp2A restricts intestinal stem cell activity via endocytic regulation of aPKC and hippo signaling
  publication-title: Cell Rep
– volume: 6
  start-page: 25161
  year: 2015
  end-page: 25174
  article-title: Coupling the modules of EMT and stemness: a tunable “stemness window” model
  publication-title: Oncotarget
– volume: 338
  start-page: 28
  year: 2010
  end-page: 37
  article-title: JAK/STAT signaling coordinates stem cell proliferation and multilineage differentiation in the intestinal stem cell lineage
  publication-title: Dev Biol
– volume: 16
  start-page: 1035
  year: 2014
  end-page: 1044
  article-title: Pri peptides are mediators of ecdysone for the temporal control of development
  publication-title: Nat Cell Biol
– volume: 18
  start-page: 4335
  year: 1998
  end-page: 4343
  article-title: Voila, a new Drosophila courtship variant that affects the nervous system: behavioral, neural, and genetic characterization
  publication-title: J Neurosci
– volume: 23
  start-page: 2333
  year: 2009
  end-page: 2344
  article-title: Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in
  publication-title: Genes Dev
– volume: 9
  start-page: 138
  year: 2018
  article-title: Wnt signalling in intestinal stem cells: lessons from mice and flies
  publication-title: Genes
– volume: 142
  start-page: 644
  year: 2015
  end-page: 653
  article-title: Enteroendocrine cells are generated from stem cells through a distinct progenitor in the adult posterior midgut
  publication-title: Development
– volume: 129
  start-page: 1155
  year: 2016
  end-page: 1164
  article-title: A tetraspanin regulates septate junction formation in Drosophila midgut
  publication-title: J Cell Sci
– volume: 166
  start-page: 21
  year: 2016
  end-page: 45
  article-title: Emt: 2016
  publication-title: Cell
– volume: 12
  start-page: 319
  year: 2019
  end-page: 332
  article-title: OVOL1 Influences the determination and expansion of iPSC reprogramming intermediates
  publication-title: Stem Cell Rep
– volume: 600
  start-page: 1
  year: 2017
  end-page: 8
  article-title: Ovol2 gene inhibits the Epithelial‐to‐Mesenchymal Transition in lung adenocarcinoma by transcriptionally repressing Twist1
  publication-title: Gene
– volume: 14
  start-page: R86
  year: 2013
  article-title: Genome‐wide analyses of Shavenbaby target genes reveals distinct features of enhancer organization
  publication-title: Genome Biol
– volume: 439
  start-page: 470
  year: 2006
  end-page: 474
  article-title: The adult posterior midgut is maintained by pluripotent stem cells
  publication-title: Nature
– volume: 7
  start-page: 1867
  year: 2014
  end-page: 1875
  article-title: Slit/Robo signaling regulates cell fate decisions in the intestinal stem cell lineage of
  publication-title: Cell Rep
– volume: 474
  start-page: 598
  year: 2011
  end-page: 603
  article-title: Morphological evolution caused by many subtle‐effect substitutions in regulatory DNA
  publication-title: Nature
– volume: 350
  start-page: aab0988
  year: 2015
  article-title: Stem cell regulation. Bidirectional Notch signaling regulates intestinal stem cell multipotency
  publication-title: Science
– volume: 10
  year: 2014
  article-title: Integration of UPRER and oxidative stress signaling in the control of intestinal stem cell proliferation
  publication-title: PLoS Genet
– volume: 9
  start-page: 487
  year: 2016
  end-page: 499
  article-title: Gastrointestinal stem cells in health and disease: from flies to humans
  publication-title: Dis Model Mech
– volume: 1
  start-page: 32
  year: 2015
  article-title: Recent progress in understanding the role of ecdysteroids in adult insects: Germline development and circadian clock in the fruit fly
  publication-title: Zoological Lett
– volume: 9
  start-page: 5123
  year: 2018
  article-title: Shavenbaby and Yorkie mediate Hippo signaling to protect adult stem cells from apoptosis
  publication-title: Nat Commun
– volume: 584
  start-page: 415
  year: 2020
  end-page: 419
  article-title: Fitness trade‐offs incurred by ovary‐to‐gut steroid signalling in
  publication-title: Nature
– volume: 136
  start-page: 483
  year: 2009
  end-page: 493
  article-title: EGFR signaling regulates the proliferation of adult midgut progenitors
  publication-title: Development
– volume: 5
  start-page: e106
  year: 2007
  article-title: Peptides encoded by short ORFs control development and define a new eukaryotic gene family
  publication-title: PLoS Biol
– volume: 349
  start-page: 1356
  year: 2015
  end-page: 1358
  article-title: Pri sORF peptides induce selective proteasome‐mediated protein processing
  publication-title: Science
– volume: 16
  year: 2018
  article-title: An alternative mode of epithelial polarity in the Drosophila midgut
  publication-title: PLoS Biol
– volume: 366
  start-page: 2
  year: 2006
  end-page: 16
  article-title: Epidermal growth factor receptor (EGFR) signaling in cancer
  publication-title: Gene
– volume: 120
  start-page: 747
  year: 2003
  end-page: 758
  article-title: The Ovo/Shavenbaby transcription factor specifies actin remodelling during epidermal differentiation in
  publication-title: Mech Dev
– volume: 49
  start-page: 83
  year: 1995
  end-page: 95
  article-title: ovo, a gene required for ovarian development, is specifically expressed in the germline and shares most of its coding sequences with shavenbaby, a gene involved in embryo patterning
  publication-title: Mech Dev
– volume: 7
  start-page: 40056
  year: 2017
  article-title: Conserved role of Ovo in germline development in mouse and
  publication-title: Sci Rep
– volume: 160
  start-page: 191
  year: 2015
  end-page: 203
  article-title: Low affinity binding site clusters confer hox specificity and regulatory robustness
  publication-title: Cell
– volume: 36
  start-page: 1461
  year: 2017
  end-page: 1473
  article-title: Wnt signaling in cancer
  publication-title: Oncogene
– volume: 24
  start-page: 251
  year: 2001
  end-page: 254
  article-title: Mosaic analysis with a repressible cell marker (MARCM) for neural development
  publication-title: Trends Neurosci
– volume: 10
  start-page: 1507
  year: 2000
  end-page: 1510
  article-title: R7 photoreceptor specification requires Notch activity
  publication-title: Curr Biol
– volume: 355
  start-page: 183
  year: 2011
  end-page: 193
  article-title: Tarsal‐less peptides control Notch signalling through the Shavenbaby transcription factor
  publication-title: Dev Biol
– volume: 138
  start-page: 1045
  year: 2011
  end-page: 1055
  article-title: EGF signaling regulates the proliferation of intestinal stem cells in
  publication-title: Development
– volume: 8
  start-page: 84
  year: 2011
  end-page: 95
  article-title: EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in
  publication-title: Cell Stem Cell
– volume: 11
  start-page: 60
  year: 2001
  end-page: 64
  article-title: A model Notch response element detects Suppressor of Hairless‐dependent molecular switch
  publication-title: Curr Biol
– volume: 8
  year: 2013
  article-title: Transcription factors OVOL1 and OVOL2 induce the mesenchymal to epithelial transition in human cancer
  publication-title: PLoS One
– volume: 3
  start-page: 442
  year: 2008
  end-page: 455
  article-title: JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging gut
  publication-title: Cell Stem Cell
– volume: 455
  start-page: 1119
  year: 2008
  end-page: 1123
  article-title: Paracrine Wingless signalling controls self‐renewal of intestinal stem cells
  publication-title: Nature
– volume: 119
  start-page: 897
  year: 1993
  end-page: 908
  article-title: Sex‐lethal, master and slave: a hierarchy of germ‐line sex determination in
  publication-title: Development
– volume: 48
  start-page: 207
  year: 2004
  end-page: 215
  article-title: Genetic control of epidermis differentiation in
  publication-title: Int J Dev Biol
– volume: 29
  start-page: 59
  year: 2014
  end-page: 74
  article-title: Mammary morphogenesis and regeneration require the inhibition of EMT at terminal end buds by Ovol2 transcriptional repressor
  publication-title: Dev Cell
– volume: 466
  start-page: 490
  year: 2010
  end-page: 493
  article-title: Phenotypic robustness conferred by apparently redundant transcriptional enhancers
  publication-title: Nature
– volume: 34
  start-page: 2025
  year: 2015
  end-page: 2041
  article-title: Robust intestinal homeostasis relies on cellular plasticity in enteroblasts mediated by miR‐8‐Escargot switch
  publication-title: EMBO J
– volume: 33
  start-page: 2967
  year: 2014
  end-page: 2982
  article-title: Escargot maintains stemness and suppresses differentiation in intestinal stem cells
  publication-title: EMBO J
– volume: 137
  start-page: 1343
  year: 2009
  end-page: 1355
  article-title: Cytokine/Jak/Stat Signaling Mediates Regeneration and Homeostasis in the Midgut
  publication-title: Cell
– volume: 33
  start-page: 2983
  year: 2014
  end-page: 2996
  article-title: Regulation of intestinal stem cell maintenance and differentiation by the transcription factor Escargot
  publication-title: EMBO J
– volume: 8
  year: 2019
  article-title: The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning
  publication-title: Elife
– volume: 439
  start-page: 475
  year: 2006
  end-page: 479
  article-title: Evidence that stem cells reside in the adult midgut epithelium
  publication-title: Nature
– volume: 48
  start-page: 607
  year: 2010
  end-page: 611
  article-title: Characterization of midgut stem cell‐ and enteroblast‐specific Gal4 lines in
  publication-title: Genesis
– volume: 3
  start-page: 1725
  year: 2013
  end-page: 1738
  article-title: Morphological and molecular characterization of adult midgut compartmentalization in
  publication-title: Cell Rep
– volume: 10
  start-page: 1565
  year: 2018
  end-page: 1578
  article-title: The POU/Oct transcription factor nubbin controls the balance of intestinal stem cell maintenance and differentiation by isoform‐specific regulation
  publication-title: Stem Cell Rep
– volume: 424
  start-page: 935
  year: 2003
  end-page: 938
  article-title: Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism
  publication-title: Nature
– volume: 138
  start-page: 4585
  year: 2011
  end-page: 4595
  article-title: Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine
  publication-title: Development
– volume: 137
  start-page: 705
  year: 2010
  end-page: 714
  article-title: Transcriptional control of stem cell maintenance in the intestine
  publication-title: Development
– volume: 315
  start-page: 988
  year: 2007
  end-page: 992
  article-title: Multipotent intestinal stem cells specify daughter cell fates by differential notch signaling
  publication-title: Science
– volume: 400
  start-page: 271
  year: 1999
  end-page: 275
  article-title: ovo/svb integrates Wingless and DER pathways to control epidermis differentiation
  publication-title: Nature
– volume: 18
  start-page: 64
  year: 2010
  end-page: 76
  article-title: Zona pellucida domain proteins remodel the apical compartment for localized cell shape changes
  publication-title: Dev Cell
– volume: 20
  year: 2019
  article-title: An Ovol2‐Zeb1 transcriptional circuit regulates epithelial directional migration and proliferation
  publication-title: EMBO Rep
– volume: 127
  start-page: 881
  year: 2000
  end-page: 892
  article-title: OVO transcription factors function antagonistically in the female germline
  publication-title: Development
– volume: 11
  year: 2015
  article-title: EGFR/Ras signaling controls intestinal stem cell proliferation via capicua‐regulated genes
  publication-title: PLoS Genet
– volume: 9
  start-page: 5963
  year: 2016
  end-page: 5973
  article-title: Expression of Ovol2 is related to epithelial characteristics and shows a favorable clinical outcome in hepatocellular carcinoma
  publication-title: Onco Targets Ther
– volume: 150
  start-page: 659
  year: 2016
  end-page: 671
  article-title: OVOL2, an inhibitor of WNT signaling, reduces invasive activities of human and mouse cancer cells and is down‐regulated in human colorectal tumors
  publication-title: Gastroenterology
– volume: 329
  start-page: 336
  year: 2010
  end-page: 339
  article-title: Small peptides switch the transcriptional activity of Shavenbaby during embryogenesis
  publication-title: Science
– volume: 7
  year: 2018
  article-title: Temporospatial induction of homeodomain gene cut dictates natural lineage reprogramming
  publication-title: Elife
– volume: 98
  start-page: 75
  year: 2016
  end-page: 89
  article-title: Autosomal‐dominant corneal endothelial dystrophies CHED1 and PPCD1 are allelic disorders caused by non‐coding mutations in the promoter of OVOL2
  publication-title: Am J Hum Genet
– volume: 33
  start-page: 391
  year: 2017
  end-page: 416
  article-title: In search of lost small peptides
  publication-title: Annu Rev Cell Dev Biol
– volume: 22
  start-page: 3021
  year: 2018
  end-page: 3031
  article-title: Comprehensive analysis of a cis‐regulatory region reveals pleiotropy in enhancer function
  publication-title: Cell Rep
– volume: 11
  start-page: 909
  year: 2015
  end-page: 916
  article-title: Discovery and characterization of smORF‐encoded bioactive polypeptides
  publication-title: Nat Chem Biol
– ident: e_1_2_8_69_1
  doi: 10.1016/j.gene.2016.11.034
– ident: e_1_2_8_31_1
  doi: 10.1242/jcs.180448
– ident: e_1_2_8_35_1
  doi: 10.1371/journal.pgen.1005634
– ident: e_1_2_8_63_1
  doi: 10.7554/eLife.39748
– ident: e_1_2_8_72_1
  doi: 10.1016/j.devcel.2014.03.006
– ident: e_1_2_8_9_1
  doi: 10.1242/dev.056671
– ident: e_1_2_8_52_1
  doi: 10.1038/nature04333
– ident: e_1_2_8_79_1
  doi: 10.1038/onc.2016.304
– ident: e_1_2_8_7_1
  doi: 10.1016/j.ydbio.2009.10.045
– ident: e_1_2_8_13_1
  doi: 10.1101/gad.1827009
– ident: e_1_2_8_19_1
  doi: 10.1016/j.cell.2014.11.041
– ident: e_1_2_8_42_1
  doi: 10.1016/S0166-2236(00)01791-4
– ident: e_1_2_8_5_1
  doi: 10.1523/JNEUROSCI.18-11-04335.1998
– ident: e_1_2_8_44_1
  doi: 10.1038/nature07329
– ident: e_1_2_8_55_1
  doi: 10.1387/ijdb.15272387
– ident: e_1_2_8_62_1
  doi: 10.1016/j.ydbio.2011.03.033
– ident: e_1_2_8_64_1
  doi: 10.1371/journal.pone.0076773
– ident: e_1_2_8_38_1
  doi: 10.1016/j.celrep.2016.04.020
– ident: e_1_2_8_46_1
  doi: 10.1038/nature05988
– ident: e_1_2_8_80_1
  doi: 10.7554/eLife.55795
– ident: e_1_2_8_78_1
  doi: 10.1242/dev.113357
– ident: e_1_2_8_70_1
  doi: 10.1371/journal.pgen.1004568
– ident: e_1_2_8_47_1
  doi: 10.1186/gb-2013-14-8-r86
– ident: e_1_2_8_74_1
  doi: 10.7554/eLife.33934
– ident: e_1_2_8_76_1
  doi: 10.1126/science.aac5677
– ident: e_1_2_8_68_1
  doi: 10.1186/s40851-015-0031-2
– ident: e_1_2_8_71_1
  doi: 10.1038/s41598-019-43021-z
– ident: e_1_2_8_24_1
  doi: 10.1038/nature10200
– ident: e_1_2_8_41_1
  doi: 10.1016/j.celrep.2012.06.018
– ident: e_1_2_8_14_1
  doi: 10.1016/j.celrep.2013.04.001
– ident: e_1_2_8_23_1
  doi: 10.1038/nature09158
– ident: e_1_2_8_30_1
  doi: 10.1038/srep40056
– ident: e_1_2_8_32_1
  doi: 10.1242/dev.026955
– ident: e_1_2_8_4_1
  doi: 10.15252/embj.201591517
– ident: e_1_2_8_45_1
  doi: 10.15252/embj.201489050
– ident: e_1_2_8_58_1
  doi: 10.3390/genes9030138
– ident: e_1_2_8_75_1
  doi: 10.1053/j.gastro.2015.11.041
– ident: e_1_2_8_56_1
  doi: 10.1038/22330
– ident: e_1_2_8_51_1
  doi: 10.1016/j.gene.2005.10.018
– ident: e_1_2_8_26_1
  doi: 10.1016/S0960-9822(00)00044-0
– ident: e_1_2_8_61_1
  doi: 10.1016/j.celrep.2018.02.073
– ident: e_1_2_8_6_1
  doi: 10.1242/dev.039404
– ident: e_1_2_8_48_1
  doi: 10.1016/0925-4773(94)00305-7
– ident: e_1_2_8_49_1
  doi: 10.1038/nature04371
– ident: e_1_2_8_29_1
  doi: 10.15252/embr.201846273
– ident: e_1_2_8_20_1
  doi: 10.1016/j.ajhg.2015.11.018
– ident: e_1_2_8_10_1
  doi: 10.1016/j.celrep.2014.05.024
– ident: e_1_2_8_8_1
  doi: 10.1016/j.stem.2008.07.024
– ident: e_1_2_8_11_1
  doi: 10.1371/journal.pgen.1001159
– ident: e_1_2_8_12_1
  doi: 10.1038/s41467-018-07569-0
– ident: e_1_2_8_60_1
  doi: 10.1016/j.devcel.2016.10.010
– ident: e_1_2_8_28_1
  doi: 10.1126/science.aab0988
– ident: e_1_2_8_37_1
  doi: 10.1016/j.stemcr.2018.12.008
– ident: e_1_2_8_43_1
  doi: 10.1242/dmm.024232
– ident: e_1_2_8_53_1
  doi: 10.1126/science.1136606
– ident: e_1_2_8_65_1
  doi: 10.1038/nchembio.1964
– ident: e_1_2_8_15_1
  doi: 10.1371/journal.pbio.0040290
– ident: e_1_2_8_34_1
  doi: 10.1016/j.cell.2009.05.014
– ident: e_1_2_8_2_1
  doi: 10.1038/s41586-020-2462-y
– ident: e_1_2_8_66_1
  doi: 10.1038/nature01768
– ident: e_1_2_8_67_1
  doi: 10.1016/j.stemcr.2018.03.014
– ident: e_1_2_8_21_1
  doi: 10.1016/S0925-4773(03)00081-9
– ident: e_1_2_8_36_1
  doi: 10.18632/oncotarget.4629
– ident: e_1_2_8_40_1
  doi: 10.15252/embj.201489072
– ident: e_1_2_8_3_1
  doi: 10.1242/dev.127.4.881
– ident: e_1_2_8_77_1
  doi: 10.1002/dvg.20661
– ident: e_1_2_8_22_1
  doi: 10.1016/j.devcel.2009.11.009
– ident: e_1_2_8_18_1
  doi: 10.1016/S0960-9822(00)00826-5
– ident: e_1_2_8_17_1
  doi: 10.1371/journal.pbio.3000041
– ident: e_1_2_8_25_1
  doi: 10.2147/OTT.S110409
– ident: e_1_2_8_39_1
  doi: 10.1126/science.1188158
– ident: e_1_2_8_54_1
  doi: 10.1242/dev.119.3.897
– ident: e_1_2_8_57_1
  doi: 10.1242/dev.065292
– ident: e_1_2_8_59_1
  doi: 10.1146/annurev-cellbio-100616-060516
– ident: e_1_2_8_16_1
  doi: 10.1038/ncb3052
– ident: e_1_2_8_33_1
  doi: 10.1016/j.stem.2010.11.026
– ident: e_1_2_8_27_1
  doi: 10.1371/journal.pbio.0050106
– ident: e_1_2_8_73_1
  doi: 10.1016/j.celrep.2018.12.079
– ident: e_1_2_8_50_1
  doi: 10.1016/j.cell.2016.06.028
SSID ssj0005871
Score 2.4449382
Snippet Adult stem cells must continuously fine‐tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to...
Adult stem cells must continuously fine-tune their behavior to regenerate damaged organs and avoid tumors. While several signaling pathways are well known to...
SourceID pubmedcentral
hal
proquest
pubmed
crossref
wiley
springer
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage e104347
SubjectTerms Animals
Cell Differentiation
Cell interactions
Cell proliferation
Cell Self Renewal
Cell survival
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
Drosophila
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
EMBO03
EMBO34
EMBO37
enterocyte differentiation
Enterocytes
Epidermal growth factor receptors
Female
Fruit flies
Gene Expression Regulation, Developmental
Hormones
Insects
intestinal stem cells
Intestine
Intestines - physiology
Life Sciences
Male
Organs
Ovaries
OvoL transcription factors
Proteasomes
Signal transduction
Signaling
Stem cells
Stem Cells - cytology
Stem Cells - metabolism
Steroid hormones
Steroids
Steroids - pharmacology
Survival
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
Tumors
Wnt and EFGR pathways
Wnt protein
SummonAdditionalLinks – databaseName: Springer Nature OA Free Journals
  dbid: C6C
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1LT9wwEB4VqqpcKkofpDzkol5aKVoSP_cIK9AKQXsAJG5RnMTarWhSNbsgbv0J_EZ-CTN5LRGlVY-JHdvxN4lnPONvAD5pm_J0iAiYMDU-EdD5Bi0PP05dGFrNbeDooPDJVzU-F0cX8qLZ76CzMA_99zKU4SD7Yb9TBBYua4ILvQTPJf52KXhvpEaLYA5TmVbVbooIzLBxSP6phd4CtDSh8MfHuuXjEMnOT9rXYqtl6HAVXjX6I9urAX8Nz7J8DV7UGSVv1uDlqE3g9gbmpzhnxTS9-33bprqdsfJ6ijixwrFvV8Xx4HRC6eRtbG9YE7ResjK7dPgMcV1eY1cUtzEvWZtJZVZjSS0Q1QT-IWg8RAfNyAlQvoXzw4Oz0dhvsiz4iZRc-1YFRqeBsFLFygUVARiu4yZVCKGjQpeimmSU00MbJ3HCpU0qJrndjCtr-DtYzos8WwfmcCASG1FGoN2Y8djGQ4caFEczzAqTeDBopz5KGgpyyoRxGZEpQmBFBFa0AMuDz90TP2v6jb_U3UE0u2rEmz3eO47oHhlGqGjKq9CDzRbsqPlayygU5KylgCAPPnbFiBbNW5xnxZzqaK4lnfT14H0tG11XnHNUA3eNB7onNb2x9Evy6aTi8tbGoDQLD7608rUY1tMvKisJ_OeMRAcn-0eLyw__08kGrIQUvkO5b-QmLM9-zbMt1L9mdrv69O4BbvYntg
  priority: 102
  providerName: Springer Nature
Title Steroid‐dependent switch of OvoL/Shavenbaby controls self‐renewal versus differentiation of intestinal stem cells
URI https://link.springer.com/article/10.15252/embj.2019104347
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.2019104347
https://www.ncbi.nlm.nih.gov/pubmed/33372708
https://www.proquest.com/docview/2489135209
https://www.proquest.com/docview/2473752825
https://hal.science/hal-03065225
https://pubmed.ncbi.nlm.nih.gov/PMC7883054
Volume 40
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVFSB
  databaseName: Free Full-Text Journals in Chemistry
  customDbUrl:
  eissn: 1460-2075
  dateEnd: 20241001
  omitProxy: true
  ssIdentifier: ssj0005871
  issn: 0261-4189
  databaseCode: HH5
  dateStart: 19820101
  isFulltext: true
  titleUrlDefault: http://abc-chemistry.org/
  providerName: ABC ChemistRy
– providerCode: PRVAFT
  databaseName: Open Access Digital Library
  customDbUrl:
  eissn: 1460-2075
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0005871
  issn: 0261-4189
  databaseCode: KQ8
  dateStart: 19970101
  isFulltext: true
  titleUrlDefault: http://grweb.coalliance.org/oadl/oadl.html
  providerName: Colorado Alliance of Research Libraries
– providerCode: PRVBFR
  databaseName: Free Medical Journals
  customDbUrl:
  eissn: 1460-2075
  dateEnd: 20241001
  omitProxy: true
  ssIdentifier: ssj0005871
  issn: 0261-4189
  databaseCode: DIK
  dateStart: 19820101
  isFulltext: true
  titleUrlDefault: http://www.freemedicaljournals.com
  providerName: Flying Publisher
– providerCode: PRVFQY
  databaseName: GFMER Free Medical Journals
  customDbUrl:
  eissn: 1460-2075
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0005871
  issn: 0261-4189
  databaseCode: GX1
  dateStart: 19820101
  isFulltext: true
  titleUrlDefault: http://www.gfmer.ch/Medical_journals/Free_medical.php
  providerName: Geneva Foundation for Medical Education and Research
– providerCode: PRVAQN
  databaseName: PubMed Central
  customDbUrl:
  eissn: 1460-2075
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0005871
  issn: 0261-4189
  databaseCode: RPM
  dateStart: 19820101
  isFulltext: true
  titleUrlDefault: https://www.ncbi.nlm.nih.gov/pmc/
  providerName: National Library of Medicine
– providerCode: PRVAQT
  databaseName: Springer Nature Journals
  customDbUrl:
  eissn: 1460-2075
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0005871
  issn: 0261-4189
  databaseCode: NAO
  dateStart: 20031001
  isFulltext: true
  titleUrlDefault: https://www.nature.com/siteindex/index.html
  providerName: Nature Publishing
– providerCode: PRVAVX
  databaseName: Springer Nature HAS Fully OA
  customDbUrl:
  eissn: 1460-2075
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0005871
  issn: 0261-4189
  databaseCode: AAJSJ
  dateStart: 19970101
  isFulltext: true
  titleUrlDefault: https://www.springernature.com
  providerName: Springer Nature
– providerCode: PRVAVX
  databaseName: Springer Nature OA Free Journals
  customDbUrl:
  eissn: 1460-2075
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0005871
  issn: 0261-4189
  databaseCode: C6C
  dateStart: 20031001
  isFulltext: true
  titleUrlDefault: http://www.springeropen.com/
  providerName: Springer Nature
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB7RIgQXVMor0CKDuIAUbRPbsfdYVq1WVQtIpVJvkZ3E2q1Kgshuq974CfxGfgkzzmObVoDEZaVdP-L1N_bMxONvAN4qm_N8jAjoONchEdCFGj2P0OQujq3iNnJ0UfjoYzI9EQen8vTaXZiGH6J_4UYrw-_XtMCNrbuMPcQaWny1ZxSbhQpPcKHW4G5Eyp_YncXnVZiH9k6Xf88iIj1ujyqpj9GNHgaqaW1GgZG3rc7bwZP9CerQvvUKan8DHraWJdttROER3CnKTbjX5Jq82oT7ky6122NYHuNsVvP814-fXRLcBasv54ggqxz7dFEdjo5nlGjeGnvF2nD2mtXFucM2xIJ5iY-iiI5lzbocK4sGZeqBSChw76DxEFE0o-OB-gmc7O99mUzDNv9CmEnJVWiTSKs8ElYmJnGRpwZDDa_zBMF1VOhyNKB04tTYmsxkXNrMc8ztFDyxmj-F9bIqi-fAHA5EYieJFuhRFtxYM3ZoW3F00KzQWQCjburTrCUnpxwZ5yk5KQRWSmClK7ACeNe3-NYQc_yl7htEs69GjNrT3cOUfiOXCU1QeREHsNWBnbbruE5jQce4FCoUwOu-GNGieTNlUS2pjuJK0h3gAJ41stE_inOOBuKODkANpGYwlmFJOZ95lm-lNe7FIoD3nXythvXnPyq9BP5zRtK9ow8Hq68v_rPdS3gQU4wPJciRW7C--L4sttFIW9hXfhXi5ySZ_Ab9ejRJ
linkProvider Wiley-Blackwell
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3NbtQwEB61RahcEBQogQIGcQEp2k1sx95jWbVaym5Baiv1ZsVJrF1UEkR2W_XGI_CMPAkz-VuFCpA4Jv6J429sz9jjbwBeK5vydIQI6DDVPhHQ-RotDz9OXRhaxW3g6KLw7DianImjc3m-AeP2LkzND9FtuNHIqOZrGuC0Id2G7CHa0OyL_UzOWbjiCS7UJtwSUTgk0Q7Fp7Wfh66srmqjRQR61JxVUh2D32rorU2bc_KMvKl23vSe7I5Q-wputUId3oO7jWrJ9mtZuA8bWb4Dt-tgk9c7sD1uY7s9gNUJdmexSH9-_9FGwV2y8mqBELLCsY-XxXRwMqdI8za216zxZy9ZmV04LEM0mFf4KXLpWJWsDbKyrGGmGoiFAicPag8xRTM6Hygfwtnhwel44jcBGPxESq58GwVapYGwMoojF1TcYLjE6zRCdB0luhQ1KB05NbJxEidc2qQimRtmPLKaP4KtvMizx8AcNkRiJZEWaFJmPLbxyKFyxdFCs0InHgzarjdJw05OQTIuDFkpBJYhsMwaLA_edCW-1swcf8n7CtHsshGl9mR_augd2Uyog8rL0IO9FmzTDOTShILOcclXyIOXXTKiRf0W51mxojyKK0mXgD3YrWWj-xTnHDXEofZA9aSm15Z-Sr6YVzTfSmucjIUHb1v5Wjfrzz8qKwn8Z4-Yg9m7o_Xjk_8s9wK2J6ezqZm-P_7wFO6E5PBD0XLkHmwtv62yZ6ixLe3zakT-Al5PNts
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB7RIh4XBIXSQAGDuIAUbRPbsfdYSldL2ZZKpVJvURzH2kUlqZrdVr3xE_iN_BJm8lpCBUgcEz_i-BvbM_b4G4DXylhuh4iADq32iYDO12h5-Il1YWgUN4Gji8L7B9H4WOydyJNf7sLU_BDdhhuNjGq-pgF-Zl0bsYdYQ7Ov5gv5ZuGCJ7hQK3BTEHMLsTuLw6Wbh66MrmqfRQR62BxVUh2D32roLU0rU3KMvK51Xnee7E5Q-_pttUCN7sO9RrNk27UoPIAbWb4Gt-pYk1drcGenDe32EBZH2JvFzP749r0Ngjtn5eUMEWSFY58uisngaEqB5k1irljjzl6yMjt1WIZYMC_xU-TRsShZG2NlXqNMNRAJBc4d1B4iimZ0PFA-guPR7uedsd_EX_BTKbnyTRRoZQNhZJRELqiowXCF1zZCcB0lOosKlI6cGpokTVIuTVpxzG1lPDKar8NqXuTZBjCHDZFYSaQFWpQZT0wydKhbcTTQjNCpB4O26-O0ISenGBmnMRkpBFZMYMVLsDx405U4q4k5_pL3FaLZZSNG7fH2JKZ3ZDKhCiovQg82W7DjZhyXcSjoGJdchTx42SUjWtRvSZ4VC8qjuJJ0B9iDx7VsdJ_inKOCuKU9UD2p6bWln5LPphXLt9Ia52LhwdtWvpbN-vOPykoC_9kj8e7-u73l45P_LPcCbh--H8WTDwcfn8LdkNx9KFaO3ITV-fkie4b62tw8rwbkT1vDNg0
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Steroid-dependent+switch+of+OvoL%2FShavenbaby+controls+self-renewal+versus+differentiation+of+intestinal+stem+cells&rft.jtitle=The+EMBO+journal&rft.au=Al+Hayek%2C+Sandy&rft.au=Alsawadi%2C+Ahmad&rft.au=Kambris%2C+Zakaria&rft.au=Boquete%2C+Jean-Philippe&rft.date=2021-02-15&rft.pub=EMBO+Press&rft.issn=0261-4189&rft.eissn=1460-2075&rft.volume=40&rft.issue=4&rft_id=info:doi/10.15252%2Fembj.2019104347&rft_id=info%3Apmid%2F33372708&rft.externalDBID=HAS_PDF_LINK&rft.externalDocID=oai_HAL_hal_03065225v2
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0261-4189&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0261-4189&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0261-4189&client=summon