Insertional Mutagenesis Identifies a STAT3/Arid1b/β-catenin Pathway Driving Neurofibroma Initiation
To identify genes and signaling pathways that initiate Neurofibromatosis type 1 (NF1) neurofibromas, we used unbiased insertional mutagenesis screening, mouse models, and molecular analyses. We mapped an Nf1-Stat3-Arid1b/β-catenin pathway that becomes active in the context of Nf1 loss. Genetic delet...
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| Published in | Cell reports (Cambridge) Vol. 14; no. 8; pp. 1979 - 1990 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.03.2016
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2211-1247 2211-1247 |
| DOI | 10.1016/j.celrep.2016.01.074 |
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| Abstract | To identify genes and signaling pathways that initiate Neurofibromatosis type 1 (NF1) neurofibromas, we used unbiased insertional mutagenesis screening, mouse models, and molecular analyses. We mapped an Nf1-Stat3-Arid1b/β-catenin pathway that becomes active in the context of Nf1 loss. Genetic deletion of Stat3 in Schwann cell progenitors (SCPs) and Schwann cells (SCs) prevents neurofibroma formation, decreasing SCP self-renewal and β-catenin activity. β-catenin expression rescues effects of Stat3 loss in SCPs. Importantly, P-STAT3 and β-catenin expression correlate in human neurofibromas. Mechanistically, P-Stat3 represses Gsk3β and the SWI/SNF gene Arid1b to increase β-catenin. Knockdown of Arid1b or Gsk3β in Stat3fl/fl;Nf1fl/fl;DhhCre SCPs rescues neurofibroma formation after in vivo transplantation. Stat3 represses Arid1b through histone modification in a Brg1-dependent manner, indicating that epigenetic modification plays a role in early tumorigenesis. Our data map a neural tumorigenesis pathway and support testing JAK/STAT and Wnt/β-catenin pathway inhibitors in neurofibroma therapeutic trials.
[Display omitted]
•Insertional mutagenesis identifies STAT3 as a driver of benign neurofibromas•Stat3 activates β-catenin to initiate neurofibroma formation•Stat3 represses Gsk3β and Arid1b to increase β-catenin•Neurofibroma-initiating cells require Stat3 and β-catenin for tumorigenesis
Wu et al. map an Nf1-Stat3-Arid1b/β-catenin pathway that initiates Neurofibromatosis type 1 (Nf1) neurofibromas, using unbiased insertional mutagenesis screening. Stat3 transcriptionally represses Gsk3β and Arid1b, thereby activating β-catenin in Schwann cell precursors and resulting in neurofibroma initiation and maintenance. Stat3-mediated modification plays a role in early tumorigenesis. |
|---|---|
| AbstractList | To identify genes and signaling pathways that initiate Neurofibromatosis type 1 (
Nf1
) neurofibroma, we used unbiased insertional mutagenesis screening, mouse models, and molecular analyses. We mapped an
Nf1-Stat3-Arid1b/β-catenin
pathway which becomes active in the context of
Nf1
loss. Genetic deletion of
Stat3
in Schwann cells progenitors (SCPs) and Schwann cells (SCs) prevents neurofibroma formation, decreasing SCP self-renewal and β-catenin activity. β-catenin expression rescues effects of Stat3 loss in SCPs. Importantly, P-STAT3 and β-catenin expression correlate in human neurofibromas. Mechanistically, P-Stat3 represses
Gsk3
β and the SWI/SNF gene
Arid1b
, to increase β-catenin. Knock-down of
Arid1b
or
Gsk3
β in
Stat3
fl/f
;Nf1
fl/fl
;DhhCre
SCPs rescues neurofibroma formation after in vivo transplantation. Stat3 represses
Arid1b
through histone modification in a
Brg1
dependent manner, indicating that epigenetic modification plays a role in early tumorigenesis. Our data map a neural tumorigenesis pathway, and support testing JAK/STAT and Wnt/β-catenin pathway inhibitors in neurofibroma therapeutic trials.
Wu et al map an
Nf1-Stat3-Arid1b/β-catenin
pathway that initiates Neurofibromatosis type 1 (
Nf1
) neurofibroma, using unbiased insertional mutagenesis screening.
Stat3
transcriptionally represses
Gsk3β
and
Arid1b
, thereby activating β-catenin in Schwann cell precursors - resulting in neurofibroma initiation and maintenance. Stat3 mediated epigenetic modification plays a role in early tumorigenesis. To identify genes and signaling pathways that initiate Neurofibromatosis type 1 (NF1) neurofibromas, we used unbiased insertional mutagenesis screening, mouse models, and molecular analyses. We mapped an Nf1-Stat3-Arid1b/β-catenin pathway that becomes active in the context of Nf1 loss. Genetic deletion of Stat3 in Schwann cell progenitors (SCPs) and Schwann cells (SCs) prevents neurofibroma formation, decreasing SCP self-renewal and β-catenin activity. β-catenin expression rescues effects of Stat3 loss in SCPs. Importantly, P-STAT3 and β-catenin expression correlate in human neurofibromas. Mechanistically, P-Stat3 represses Gsk3β and the SWI/SNF gene Arid1b to increase β-catenin. Knockdown of Arid1b or Gsk3β in Stat3fl/fl;Nf1fl/fl;DhhCre SCPs rescues neurofibroma formation after in vivo transplantation. Stat3 represses Arid1b through histone modification in a Brg1-dependent manner, indicating that epigenetic modification plays a role in early tumorigenesis. Our data map a neural tumorigenesis pathway and support testing JAK/STAT and Wnt/β-catenin pathway inhibitors in neurofibroma therapeutic trials. [Display omitted] •Insertional mutagenesis identifies STAT3 as a driver of benign neurofibromas•Stat3 activates β-catenin to initiate neurofibroma formation•Stat3 represses Gsk3β and Arid1b to increase β-catenin•Neurofibroma-initiating cells require Stat3 and β-catenin for tumorigenesis Wu et al. map an Nf1-Stat3-Arid1b/β-catenin pathway that initiates Neurofibromatosis type 1 (Nf1) neurofibromas, using unbiased insertional mutagenesis screening. Stat3 transcriptionally represses Gsk3β and Arid1b, thereby activating β-catenin in Schwann cell precursors and resulting in neurofibroma initiation and maintenance. Stat3-mediated modification plays a role in early tumorigenesis. To identify genes and signaling pathways that initiate Neurofibromatosis type 1 (NF1) neurofibromas, we used unbiased insertional mutagenesis screening, mouse models, and molecular analyses. We mapped an Nf1-Stat3-Arid1b/β-catenin pathway that becomes active in the context of Nf1 loss. Genetic deletion of Stat3 in Schwann cell progenitors (SCPs) and Schwann cells (SCs) prevents neurofibroma formation, decreasing SCP self-renewal and β-catenin activity. β-catenin expression rescues effects of Stat3 loss in SCPs. Importantly, P-STAT3 and β-catenin expression correlate in human neurofibromas. Mechanistically, P-Stat3 represses Gsk3β and the SWI/SNF gene Arid1b to increase β-catenin. Knockdown of Arid1b or Gsk3β in Stat3fl/fl;Nf1fl/fl;DhhCre SCPs rescues neurofibroma formation after in vivo transplantation. Stat3 represses Arid1b through histone modification in a Brg1-dependent manner, indicating that epigenetic modification plays a role in early tumorigenesis. Our data map a neural tumorigenesis pathway and support testing JAK/STAT and Wnt/β-catenin pathway inhibitors in neurofibroma therapeutic trials. To identify genes and signaling pathways that initiate Neurofibromatosis type 1 (NF1) neurofibromas, we used unbiased insertional mutagenesis screening, mouse models, and molecular analyses. We mapped an Nf1-Stat3-Arid1b/β-catenin pathway that becomes active in the context of Nf1 loss. Genetic deletion of Stat3 in Schwann cell progenitors (SCPs) and Schwann cells (SCs) prevents neurofibroma formation, decreasing SCP self-renewal and β-catenin activity. β-catenin expression rescues effects of Stat3 loss in SCPs. Importantly, P-STAT3 and β-catenin expression correlate in human neurofibromas. Mechanistically, P-Stat3 represses Gsk3β and the SWI/SNF gene Arid1b to increase β-catenin. Knockdown of Arid1b or Gsk3β in Stat3(fl/fl);Nf1(fl/fl);DhhCre SCPs rescues neurofibroma formation after in vivo transplantation. Stat3 represses Arid1b through histone modification in a Brg1-dependent manner, indicating that epigenetic modification plays a role in early tumorigenesis. Our data map a neural tumorigenesis pathway and support testing JAK/STAT and Wnt/β-catenin pathway inhibitors in neurofibroma therapeutic trials. |
| Author | Cancelas, Jose A. Spinner, Robert J. Ratner, Nancy Jessen, Walter J. Patel, Ami V. Dombi, Eva Stemmer-Rachamimov, Anat O. Silverstein, Kevin A.T. Largaespada, David A. Keng, Vincent W. Zou, Yuanshu Schwartz, Eric B. Levy, David E. Patmore, Deanna M. Wu, Jianqiang Fan, Danhua Jousma, Edwin Kim, Mi-Ok Huang, Gang Tschida, Barbara R. Kendall, Jed J. Choi, Kwangmin Fuchs, James R. |
| AuthorAffiliation | 5 Center for Genome Engineering, University of Minnesota, Minneapolis, MN 55455, USA 6 Biostatistics and Informatics, University of Minnesota, Minneapolis, MN 55455, USA 3 Masonic Cancer Center, University of Minnesota, Minneapolis, MN 55455, USA 9 Department of Pathology and New York University Cancer Institute, New York, University School of Medicine, 550 First Avenue, New York, NY 10016, USA 7 Ohio State University, College of Pharmacy, Columbus, OH 43210, USA 8 Pediatric Oncology Branch, National Cancer Institute, Bethesda, MD 20892, USA 11 Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, 02114, USA 12 Department of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USA 1 Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital Research Foundation, Cincinnati Children’s Hospital, University of Cincinnati, Cincinnati, OH 45229, USA 2 Division of Biostatistics and Epidemiology, |
| AuthorAffiliation_xml | – name: 1 Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital Research Foundation, Cincinnati Children’s Hospital, University of Cincinnati, Cincinnati, OH 45229, USA – name: 9 Department of Pathology and New York University Cancer Institute, New York, University School of Medicine, 550 First Avenue, New York, NY 10016, USA – name: 2 Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Research Foundation, Cincinnati Children’s Hospital, University of Cincinnati, Cincinnati, OH 45229, USA – name: 12 Department of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USA – name: 6 Biostatistics and Informatics, University of Minnesota, Minneapolis, MN 55455, USA – name: 3 Masonic Cancer Center, University of Minnesota, Minneapolis, MN 55455, USA – name: 7 Ohio State University, College of Pharmacy, Columbus, OH 43210, USA – name: 11 Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, 02114, USA – name: 4 Department of Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, MN 55455, USA – name: 5 Center for Genome Engineering, University of Minnesota, Minneapolis, MN 55455, USA – name: 8 Pediatric Oncology Branch, National Cancer Institute, Bethesda, MD 20892, USA – name: 10 Hoxworth Blood Center, College of Medicine, University of Cincinnati, Cincinnati, OH 45229, USA |
| Author_xml | – sequence: 1 givenname: Jianqiang surname: Wu fullname: Wu, Jianqiang organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 2 givenname: Vincent W. surname: Keng fullname: Keng, Vincent W. organization: Masonic Cancer Center, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 3 givenname: Deanna M. surname: Patmore fullname: Patmore, Deanna M. organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 4 givenname: Jed J. surname: Kendall fullname: Kendall, Jed J. organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 5 givenname: Ami V. surname: Patel fullname: Patel, Ami V. organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 6 givenname: Edwin surname: Jousma fullname: Jousma, Edwin organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 7 givenname: Walter J. surname: Jessen fullname: Jessen, Walter J. organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 8 givenname: Kwangmin surname: Choi fullname: Choi, Kwangmin organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 9 givenname: Barbara R. surname: Tschida fullname: Tschida, Barbara R. organization: Masonic Cancer Center, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 10 givenname: Kevin A.T. surname: Silverstein fullname: Silverstein, Kevin A.T. organization: Biostatistics and Informatics, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 11 givenname: Danhua surname: Fan fullname: Fan, Danhua organization: Biostatistics and Informatics, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 12 givenname: Eric B. surname: Schwartz fullname: Schwartz, Eric B. organization: Ohio State University, College of Pharmacy, Columbus, OH 43210, USA – sequence: 13 givenname: James R. surname: Fuchs fullname: Fuchs, James R. organization: Ohio State University, College of Pharmacy, Columbus, OH 43210, USA – sequence: 14 givenname: Yuanshu surname: Zou fullname: Zou, Yuanshu organization: Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Research Foundation, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 15 givenname: Mi-Ok surname: Kim fullname: Kim, Mi-Ok organization: Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Research Foundation, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 16 givenname: Eva surname: Dombi fullname: Dombi, Eva organization: Pediatric Oncology Branch, National Cancer Institute, Bethesda, MD 20892, USA – sequence: 17 givenname: David E. surname: Levy fullname: Levy, David E. organization: Department of Pathology and New York University Cancer Institute, New York University School of Medicine, 550 First Avenue, New York, NY 10016, USA – sequence: 18 givenname: Gang surname: Huang fullname: Huang, Gang organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 19 givenname: Jose A. surname: Cancelas fullname: Cancelas, Jose A. organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA – sequence: 20 givenname: Anat O. surname: Stemmer-Rachamimov fullname: Stemmer-Rachamimov, Anat O. organization: Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, 02114, USA – sequence: 21 givenname: Robert J. surname: Spinner fullname: Spinner, Robert J. organization: Department of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USA – sequence: 22 givenname: David A. surname: Largaespada fullname: Largaespada, David A. organization: Masonic Cancer Center, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 23 givenname: Nancy surname: Ratner fullname: Ratner, Nancy email: nancy.ratner@cchmc.org organization: Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital University of Cincinnati, Cincinnati, OH 45229, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26904939$$D View this record in MEDLINE/PubMed |
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| Copyright | 2016 The Authors Copyright © 2016 The Authors. Published by Elsevier Inc. All rights reserved. |
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| Notes | Present address: Department of Applied Biology and Chemical Technology, the Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong. |
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| Snippet | To identify genes and signaling pathways that initiate Neurofibromatosis type 1 (NF1) neurofibromas, we used unbiased insertional mutagenesis screening, mouse... To identify genes and signaling pathways that initiate Neurofibromatosis type 1 ( Nf1 ) neurofibroma, we used unbiased insertional mutagenesis screening, mouse... |
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| SourceType | Open Website Open Access Repository Index Database Enrichment Source Publisher |
| StartPage | 1979 |
| SubjectTerms | Animals beta Catenin - genetics beta Catenin - metabolism Carcinogenesis - genetics Carcinogenesis - metabolism Carcinogenesis - pathology Disease Models, Animal DNA Helicases - genetics DNA Helicases - metabolism DNA-Binding Proteins - antagonists & inhibitors DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Female Gene Expression Regulation, Neoplastic Glycogen Synthase Kinase 3 beta - antagonists & inhibitors Glycogen Synthase Kinase 3 beta - genetics Glycogen Synthase Kinase 3 beta - metabolism Histones - genetics Histones - metabolism Humans Mice Mice, Nude Mutagenesis, Insertional N-Terminal Acetyltransferase A - antagonists & inhibitors N-Terminal Acetyltransferase A - genetics N-Terminal Acetyltransferase A - metabolism Neoplasm Transplantation Neural Stem Cells - metabolism Neural Stem Cells - pathology Neurofibromatosis 1 - genetics Neurofibromatosis 1 - metabolism Neurofibromatosis 1 - pathology Neurofibromin 1 - genetics Neurofibromin 1 - metabolism Nuclear Proteins - genetics Nuclear Proteins - metabolism Peripheral Nervous System Neoplasms - genetics Peripheral Nervous System Neoplasms - metabolism Peripheral Nervous System Neoplasms - pathology Phosphorylation RNA, Small Interfering - genetics RNA, Small Interfering - metabolism Schwann Cells - metabolism Schwann Cells - pathology Signal Transduction STAT3 Transcription Factor - antagonists & inhibitors STAT3 Transcription Factor - genetics STAT3 Transcription Factor - metabolism Transcription Factors - genetics Transcription Factors - metabolism |
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| Title | Insertional Mutagenesis Identifies a STAT3/Arid1b/β-catenin Pathway Driving Neurofibroma Initiation |
| URI | https://dx.doi.org/10.1016/j.celrep.2016.01.074 https://www.ncbi.nlm.nih.gov/pubmed/26904939 https://pubmed.ncbi.nlm.nih.gov/PMC4782770 https://doaj.org/article/b85859bc4dea43bd98344313076ad5bb |
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