Cell-type-specific interacting proteins collaborate to regulate the timing of Cyclin B protein expression in male meiotic prophase

During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period termed meiotic prophase. In Drosophila males, meiotic prophase lasts 3.5 days, during which spermatocytes upregulate over 1800 genes and gro...

Full description

Saved in:
Bibliographic Details
Published inDevelopment (Cambridge) Vol. 150; no. 22
Main Authors Baker, Catherine C., Gallicchio, Lorenzo, Matias, Neuza R., Porter, Douglas F., Parsanian, Lucineh, Taing, Emily, Tam, Cheuk, Fuller, Margaret T.
Format Journal Article
LanguageEnglish
Published England The Company of Biologists Ltd 15.11.2023
Subjects
Online AccessGet full text
ISSN0950-1991
1477-9129
1477-9129
DOI10.1242/dev.201709

Cover

Abstract During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period termed meiotic prophase. In Drosophila males, meiotic prophase lasts 3.5 days, during which spermatocytes upregulate over 1800 genes and grow 25-fold. Previous work has shown that the cell cycle regulator Cyclin B (CycB) is subject to translational repression in immature spermatocytes, mediated by the RNA-binding protein Rbp4 and its partner Fest. Here, we show that the spermatocyte-specific protein Lut is required for translational repression of cycB in an 8-h window just before spermatocytes are fully mature. In males mutant for rbp4 or lut, spermatocytes enter and exit meiotic division 6-8 h earlier than in wild type. In addition, spermatocyte-specific isoforms of Syncrip (Syp) are required for expression of CycB protein in mature spermatocytes and normal entry into the meiotic divisions. Lut and Syp interact with Fest independent of RNA. Thus, a set of spermatocyte-specific regulators choreograph the timing of expression of CycB protein during male meiotic prophase.
AbstractList During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period termed meiotic prophase. In Drosophila males, meiotic prophase lasts 3.5 days, during which spermatocytes upregulate over 1800 genes and grow 25-fold. Previous work has shown that the cell cycle regulator Cyclin B (CycB) is subject to translational repression in immature spermatocytes, mediated by the RNA-binding protein Rbp4 and its partner Fest. Here, we show that the spermatocyte-specific protein Lut is required for translational repression of cycB in an 8-h window just before spermatocytes are fully mature. In males mutant for rbp4 or lut, spermatocytes enter and exit meiotic division 6-8 h earlier than in wild type. In addition, spermatocyte-specific isoforms of Syncrip (Syp) are required for expression of CycB protein in mature spermatocytes and normal entry into the meiotic divisions. Lut and Syp interact with Fest independent of RNA. Thus, a set of spermatocyte-specific regulators choreograph the timing of expression of CycB protein during male meiotic prophase.
During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period termed meiotic prophase. In Drosophila males, meiotic prophase lasts 3.5 days, during which spermatocytes upregulate over 1800 genes and grow 25-fold. Previous work has shown that the cell cycle regulator Cyclin B (CycB) is subject to translational repression in immature spermatocytes, mediated by the RNA-binding protein Rbp4 and its partner Fest. Here, we show that the spermatocyte-specific protein Lut is required for translational repression of cycB in an 8-h window just before spermatocytes are fully mature. In males mutant for rbp4 or lut , spermatocytes enter and exit meiotic division 6-8 h earlier than in wild type. In addition, spermatocyte-specific isoforms of Syncrip (Syp) are required for expression of CycB protein in mature spermatocytes and normal entry into the meiotic divisions. Lut and Syp interact with Fest independent of RNA. Thus, a set of spermatocyte-specific regulators choreograph the timing of expression of CycB protein during male meiotic prophase. Summary: Timing of expression of conserved cell cycle regulator Cyclin B is controlled by multiple cell-type-specific proteins in Drosophila meiotic prophase male germ cells.
During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period termed meiotic prophase. In Drosophila males, meiotic prophase lasts 3.5 days, during which spermatocytes upregulate over 1800 genes and grow 25-fold. Previous work has shown that the cell cycle regulator Cyclin B (CycB) is subject to translational repression in immature spermatocytes, mediated by the RNA-binding protein Rbp4 and its partner Fest. Here, we show that the spermatocyte-specific protein Lut is required for translational repression of cycB in an 8-h window just before spermatocytes are fully mature. In males mutant for rbp4 or lut, spermatocytes enter and exit meiotic division 6-8 h earlier than in wild type. In addition, spermatocyte-specific isoforms of Syncrip (Syp) are required for expression of CycB protein in mature spermatocytes and normal entry into the meiotic divisions. Lut and Syp interact with Fest independent of RNA. Thus, a set of spermatocyte-specific regulators choreograph the timing of expression of CycB protein during male meiotic prophase.During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period termed meiotic prophase. In Drosophila males, meiotic prophase lasts 3.5 days, during which spermatocytes upregulate over 1800 genes and grow 25-fold. Previous work has shown that the cell cycle regulator Cyclin B (CycB) is subject to translational repression in immature spermatocytes, mediated by the RNA-binding protein Rbp4 and its partner Fest. Here, we show that the spermatocyte-specific protein Lut is required for translational repression of cycB in an 8-h window just before spermatocytes are fully mature. In males mutant for rbp4 or lut, spermatocytes enter and exit meiotic division 6-8 h earlier than in wild type. In addition, spermatocyte-specific isoforms of Syncrip (Syp) are required for expression of CycB protein in mature spermatocytes and normal entry into the meiotic divisions. Lut and Syp interact with Fest independent of RNA. Thus, a set of spermatocyte-specific regulators choreograph the timing of expression of CycB protein during male meiotic prophase.
Author Baker, Catherine C.
Matias, Neuza R.
Gallicchio, Lorenzo
Parsanian, Lucineh
Tam, Cheuk
Taing, Emily
Porter, Douglas F.
Fuller, Margaret T.
AuthorAffiliation 2 Program in Epithelial Biology , Stanford University School of Medicine , Stanford, CA 94305 , USA
1 Department of Developmental Biology , Stanford University School of Medicine , Stanford, CA 94305 , USA
AuthorAffiliation_xml – name: 2 Program in Epithelial Biology , Stanford University School of Medicine , Stanford, CA 94305 , USA
– name: 1 Department of Developmental Biology , Stanford University School of Medicine , Stanford, CA 94305 , USA
Author_xml – sequence: 1
  givenname: Catherine C.
  orcidid: 0000-0002-6225-7632
  surname: Baker
  fullname: Baker, Catherine C.
– sequence: 2
  givenname: Lorenzo
  orcidid: 0000-0002-5040-0139
  surname: Gallicchio
  fullname: Gallicchio, Lorenzo
– sequence: 3
  givenname: Neuza R.
  orcidid: 0000-0003-1548-037X
  surname: Matias
  fullname: Matias, Neuza R.
– sequence: 4
  givenname: Douglas F.
  orcidid: 0000-0001-9491-8258
  surname: Porter
  fullname: Porter, Douglas F.
– sequence: 5
  givenname: Lucineh
  orcidid: 0000-0002-1401-4337
  surname: Parsanian
  fullname: Parsanian, Lucineh
– sequence: 6
  givenname: Emily
  orcidid: 0000-0003-4689-134X
  surname: Taing
  fullname: Taing, Emily
– sequence: 7
  givenname: Cheuk
  orcidid: 0000-0001-9932-8396
  surname: Tam
  fullname: Tam, Cheuk
– sequence: 8
  givenname: Margaret T.
  orcidid: 0000-0002-3804-4987
  surname: Fuller
  fullname: Fuller, Margaret T.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37882771$$D View this record in MEDLINE/PubMed
BookMark eNpVkc1qGzEUhUVJaZy0mz5A0bIUJtXPzGi0Co1pkkKgm3YtruU7topGmkpyiLd58ipxEtKFuEL67jlwzgk5CjEgIR85O-OiFV_XeHsmGFdMvyEL3irVaC70EVkw3bGGa82PyUnOfxhjslfqHTmWahiEUnxB7pfofVP2MzZ5RutGZ6kLBRPY4sKGzikWdCFTG72HVUxQkJZIE252_vG-rcdND2wc6XJvvQv04nmP4t2cMGcXQ5WlE3ikE7pYqk1F5i1kfE_ejuAzfniap-T35fdfy-vm5ufVj-W3m8ZKOZQGRitahjACaNa3XddzYJ3WrB1wzeXKWissQNcKANFJHLseQfYo1hYHy1GekvOD7rxbTVhfQ0ngzZzcBGlvIjjz_09wW7OJt4YzJRnjfVX4_KSQ4t8d5mIml20NEALGXTaipipFqwWv6KfXZi8uz8lX4MsBsCnmnHB8QTgzD7WaWqs51Cr_AcRumWg
Cites_doi 10.1093/nar/gkz1187
10.7554/eLife.58880
10.1126/science.aal3096
10.1101/gad.349689.122
10.1242/dev.003764
10.1038/11091
10.1242/dev.149500
10.1016/j.cub.2005.01.048
10.1128/MCB.17.5.2708
10.1038/381783a0
10.1093/g3journal/jkaa010
10.1002/1873-3468.13310
10.1242/dev.122341
10.1016/0092-8674(92)90616-K
10.1038/s41467-021-21623-4
10.1242/dev.125.1.125
10.1242/bio.2012885
10.1242/dev.122.4.1331
10.1083/jcb.201903135
10.1126/science.aad1886
10.1242/dev.056572
10.1093/nar/gkw784
10.7554/eLife.82201
10.1242/bio.049684
10.1101/gad.335331.119
10.1038/nprot.2017.030
10.1016/j.celrep.2013.06.020
10.1261/rna.045849.114
10.1074/jbc.275.13.9823
10.1126/science.1090289
ContentType Journal Article
Copyright 2023. Published by The Company of Biologists Ltd.
2023. Published by The Company of Biologists Ltd 2023
Copyright_xml – notice: 2023. Published by The Company of Biologists Ltd.
– notice: 2023. Published by The Company of Biologists Ltd 2023
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7X8
5PM
DOI 10.1242/dev.201709
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE

CrossRef
MEDLINE - Academic
Database_xml – sequence: 1
  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: 2
  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 Medicine
Zoology
Biology
EISSN 1477-9129
ExternalDocumentID PMC10730016
37882771
10_1242_dev_201709
Genre Journal Article
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NIGMS NIH HHS
  grantid: R01 GM081802
– fundername: NIGMS NIH HHS
  grantid: R01 GM124054
– fundername: NIH HHS
  grantid: R35GM136433
– fundername: NIGMS NIH HHS
  grantid: R35 GM136433
– fundername: NCI NIH HHS
  grantid: P30 CA124435
– fundername: NIAMS NIH HHS
  grantid: K01 AR082351
– fundername: ;
– fundername: ;
  grantid: R35GM136433; P30 CA124435; K01AR082351; R01GM124054
GroupedDBID ---
-DZ
-ET
-~X
.55
0R~
18M
2WC
34G
39C
4.4
53G
5GY
5RE
5VS
85S
AAFWJ
AAYXX
ABJNI
ABZEH
ACGFS
ACMFV
ACPRK
ACREN
ADBBV
ADFRT
ADVGF
AENEX
AFFNX
AGGIJ
ALMA_UNASSIGNED_HOLDINGS
AMTXH
BAWUL
BTFSW
CITATION
CS3
DIK
DU5
E3Z
EBS
F5P
F9R
GX1
H13
HZ~
INIJC
KQ8
O9-
OK1
P2P
R.V
RCB
RHI
SJN
TR2
TWZ
UPT
W8F
WH7
WOQ
X7M
XSW
CGR
CUY
CVF
ECM
EIF
NPM
7X8
5PM
ID FETCH-LOGICAL-c338t-afc240eafaa90645561a0599048ed13bccc2caa542aa253ef56ea36e2dce8c1e3
ISSN 0950-1991
1477-9129
IngestDate Thu Aug 21 18:37:45 EDT 2025
Fri Sep 05 04:55:08 EDT 2025
Fri Sep 12 03:41:09 EDT 2025
Tue Jul 01 04:14:50 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 22
Keywords Translation
Meiosis
RNA
Cyclin B
Spermatogenesis
Drosophila
Language English
License http://creativecommons.org/licenses/by/4.0
2023. Published by The Company of Biologists Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c338t-afc240eafaa90645561a0599048ed13bccc2caa542aa253ef56ea36e2dce8c1e3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Handling Editor: Swathi Arur
The authors declare no competing or financial interests.
Competing interests
ORCID 0000-0001-9932-8396
0000-0003-1548-037X
0000-0001-9491-8258
0000-0003-4689-134X
0000-0002-6225-7632
0000-0002-5040-0139
0000-0002-1401-4337
0000-0002-3804-4987
OpenAccessLink https://pubmed.ncbi.nlm.nih.gov/PMC10730016
PMID 37882771
PQID 2882324921
PQPubID 23479
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_10730016
proquest_miscellaneous_2882324921
pubmed_primary_37882771
crossref_primary_10_1242_dev_201709
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2023-11-15
PublicationDateYYYYMMDD 2023-11-15
PublicationDate_xml – month: 11
  year: 2023
  text: 2023-11-15
  day: 15
PublicationDecade 2020
PublicationPlace England
PublicationPlace_xml – name: England
PublicationTitle Development (Cambridge)
PublicationTitleAlternate Development
PublicationYear 2023
Publisher The Company of Biologists Ltd
Publisher_xml – name: The Company of Biologists Ltd
References Semotok (2023112713341006500_DEV201709C20) 2005; 15
Yang (2023112713341006500_DEV201709C25) 2017; 144
Arvola (2023112713341006500_DEV201709C2) 2020; 48
Chen (2023112713341006500_DEV201709C5) 2011; 138
White-Cooper (2023112713341006500_DEV201709C24) 1998; 125
Rossi (2023112713341006500_DEV201709C28) 2020; 9
Kim (2023112713341006500_DEV201709C11) 2017; 356
Lin (2023112713341006500_DEV201709C30) 1996; 122
Alphey (2023112713341006500_DEV201709C1) 1992; 69
Maines (2023112713341006500_DEV201709C14) 1999; 1
Mizutani (2023112713341006500_DEV201709C17) 2000; 275
Giot (2023112713341006500_DEV201709C9) 2003; 302
McDermott (2023112713341006500_DEV201709C15) 2012; 1
Berry (2023112713341006500_DEV201709C4) 2022; 36
Haynes (2023112713341006500_DEV201709C10) 1997; 17
Fukushima (2023112713341006500_DEV201709C7) 2019; 593
Porter (2023112713341006500_DEV201709C18) 2021; 12
Liu (2023112713341006500_DEV201709C12) 2015; 350
Baker (2023112713341006500_DEV201709C3) 2015; 142
Bassett (2023112713341006500_DEV201709C27) 2013; 4
Samuels (2023112713341006500_DEV201709C29) 2020; 9
Titlow (2023112713341006500_DEV201709C21) 2020; 219
Tsanov (2023112713341006500_DEV201709C23) 2016; 44
Baker (2023112713341006500_DEV201709C26) 2007; 134
Eberhart (2023112713341006500_DEV201709C6) 1996; 381
Lu (2023112713341006500_DEV201709C13) 2020; 34
McDermott (2023112713341006500_DEV201709C16) 2014; 20
Gallicchio (2023112713341006500_DEV201709C8) 2021; 11
Trcek (2023112713341006500_DEV201709C22) 2017; 12
Raz (2023112713341006500_DEV201709C19) 2023; 12
36824933 - bioRxiv. 2023 Feb 17:2023.02.16.528869. doi: 10.1101/2023.02.16.528869.
References_xml – volume: 48
  start-page: 1843
  year: 2020
  ident: 2023112713341006500_DEV201709C2
  article-title: Unique repression domains of Pumilio utilize deadenylation and decapping factors to accelerate destruction of target mRNAs
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkz1187
– volume: 9
  start-page: e58880
  year: 2020
  ident: 2023112713341006500_DEV201709C28
  article-title: Extrinsic activin signaling cooperates with an intrinsic temporal program to increase mushroom body neuronal diversity
  publication-title: eLife
  doi: 10.7554/eLife.58880
– volume: 356
  start-page: 717
  year: 2017
  ident: 2023112713341006500_DEV201709C11
  article-title: Blocking promiscuous activation at cryptic promoters directs cell type-specific gene expression
  publication-title: Science
  doi: 10.1126/science.aal3096
– volume: 36
  start-page: 916
  year: 2022
  ident: 2023112713341006500_DEV201709C4
  article-title: Developmentally regulated alternative 3′ end cleavage of nascent transcripts controls dynamic changes in protein expression in an adult stem cell lineage
  publication-title: Genes Dev.
  doi: 10.1101/gad.349689.122
– volume: 134
  start-page: 2863
  year: 2007
  ident: 2023112713341006500_DEV201709C26
  article-title: Translational control of meiotic cell cycle progression and spermatid differentiation in male germ cells by a novel eIF4G homolog
  publication-title: Development
  doi: 10.1242/dev.003764
– volume: 1
  start-page: 171
  year: 1999
  ident: 2023112713341006500_DEV201709C14
  article-title: Post-transcriptional regulation of the meiotic Cdc25 protein Twine by the Dazl orthologue Boule
  publication-title: Nat. Cell Biol.
  doi: 10.1038/11091
– volume: 144
  start-page: 3454
  year: 2017
  ident: 2023112713341006500_DEV201709C25
  article-title: Imp and Syp RNA-binding proteins govern decommissioning of Drosophila neural stem cells
  publication-title: Development
  doi: 10.1242/dev.149500
– volume: 15
  start-page: 284
  year: 2005
  ident: 2023112713341006500_DEV201709C20
  article-title: Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2005.01.048
– volume: 17
  start-page: 2708
  year: 1997
  ident: 2023112713341006500_DEV201709C10
  article-title: Involvement of a tissue-specific RNA recognition motif protein in Drosophila spermatogenesis
  publication-title: Mol. Cell. Biol.
  doi: 10.1128/MCB.17.5.2708
– volume: 381
  start-page: 783
  year: 1996
  ident: 2023112713341006500_DEV201709C6
  article-title: Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia
  publication-title: Nature
  doi: 10.1038/381783a0
– volume: 11
  start-page: jkaa010
  year: 2021
  ident: 2023112713341006500_DEV201709C8
  article-title: Single-cell visualization of mir-9a and Senseless co-expression during Drosophila melanogaster embryonic and larval peripheral nervous system development
  publication-title: G3
  doi: 10.1093/g3journal/jkaa010
– volume: 593
  start-page: 277
  year: 2019
  ident: 2023112713341006500_DEV201709C7
  article-title: TDP-43 accelerates deadenylation of target mRNAs by recruiting Caf1 deadenylase
  publication-title: FEBS Lett.
  doi: 10.1002/1873-3468.13310
– volume: 142
  start-page: 3394
  year: 2015
  ident: 2023112713341006500_DEV201709C3
  article-title: Cell type-specific translational repression of Cyclin B during meiosis in males
  publication-title: Development
  doi: 10.1242/dev.122341
– volume: 69
  start-page: 977
  year: 1992
  ident: 2023112713341006500_DEV201709C1
  article-title: twine, a cdc25 homolog that functions in the male and female germline of Drosophila
  publication-title: Cell
  doi: 10.1016/0092-8674(92)90616-K
– volume: 12
  start-page: 1569
  year: 2021
  ident: 2023112713341006500_DEV201709C18
  article-title: easyCLIP analysis of RNA-protein interactions incorporating absolute quantification
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-021-21623-4
– volume: 125
  start-page: 125
  year: 1998
  ident: 2023112713341006500_DEV201709C24
  article-title: Transcriptional and post-transcriptional control mechanisms coordinate the onset of spermatid differentiation with meiosis I in Drosophila
  publication-title: Development
  doi: 10.1242/dev.125.1.125
– volume: 1
  start-page: 488
  year: 2012
  ident: 2023112713341006500_DEV201709C15
  article-title: Drosophila Syncrip binds the gurken mRNA localisation signal and regulates localised transcripts during axis specification
  publication-title: Biol. Open
  doi: 10.1242/bio.2012885
– volume: 122
  start-page: 1331
  year: 1996
  ident: 2023112713341006500_DEV201709C30
  article-title: Coordinate developmental control of the meiotic cell cycle and spermatid differentiation in Drosophila males
  publication-title: Development
  doi: 10.1242/dev.122.4.1331
– volume: 219
  start-page: e201903135
  year: 2020
  ident: 2023112713341006500_DEV201709C21
  article-title: Syncrip/hnRNP Q is required for activity-induced Msp300/Nesprin-1 expression and new synapse formation
  publication-title: J. Cell Biol.
  doi: 10.1083/jcb.201903135
– volume: 350
  start-page: 317
  year: 2015
  ident: 2023112713341006500_DEV201709C12
  article-title: Opposing intrinsic temporal gradients guide neural stem cell production of varied neuronal fates
  publication-title: Science
  doi: 10.1126/science.aad1886
– volume: 138
  start-page: 2441
  year: 2011
  ident: 2023112713341006500_DEV201709C5
  article-title: Sequential changes at differentiation gene promoters as they become active in a stem cell lineage
  publication-title: Development
  doi: 10.1242/dev.056572
– volume: 44
  start-page: e165
  year: 2016
  ident: 2023112713341006500_DEV201709C23
  article-title: smiFISH and FISH-quant – a flexible single RNA detection approach with super-resolution capability
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkw784
– volume: 12
  start-page: e82201
  year: 2023
  ident: 2023112713341006500_DEV201709C19
  article-title: Emergent dynamics of adult stem cell lineages from single nucleus and single cell RNA-Seq of Drosophila testes
  publication-title: eLife
  doi: 10.7554/eLife.82201
– volume: 9
  start-page: bio049684
  year: 2020
  ident: 2023112713341006500_DEV201709C29
  article-title: Neuronal regulation of Prospero protein is driven by alternative mRNA polyadenylation and Syncrip-mediated mRNA stabilization
  publication-title: Biol. Open
  doi: 10.1242/bio.049684
– volume: 34
  start-page: 663
  year: 2020
  ident: 2023112713341006500_DEV201709C13
  article-title: Developmental regulation of cell type-specific transcription by novel promoter-proximal sequence elements
  publication-title: Genes Dev.
  doi: 10.1101/gad.335331.119
– volume: 12
  start-page: 1326
  year: 2017
  ident: 2023112713341006500_DEV201709C22
  article-title: mRNA quantification using single-molecule FISH in Drosophila embryos
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2017.030
– volume: 4
  start-page: 220
  year: 2013
  ident: 2023112713341006500_DEV201709C27
  article-title: Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2013.06.020
– volume: 20
  start-page: 1593
  year: 2014
  ident: 2023112713341006500_DEV201709C16
  article-title: Drosophila Syncrip modulates the expression of mRNAs encoding key synaptic proteins required for morphology at the neuromuscular junction
  publication-title: RNA
  doi: 10.1261/rna.045849.114
– volume: 275
  start-page: 9823
  year: 2000
  ident: 2023112713341006500_DEV201709C17
  article-title: SYNCRIP, a cytoplasmic counterpart of heterogeneous nuclear ribonucleoprotein R, interacts with ubiquitous synaptotagmin isoforms
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.275.13.9823
– volume: 302
  start-page: 1727
  year: 2003
  ident: 2023112713341006500_DEV201709C9
  article-title: A protein interaction map of Drosophila
  publication-title: Science
  doi: 10.1126/science.1090289
– reference: 36824933 - bioRxiv. 2023 Feb 17:2023.02.16.528869. doi: 10.1101/2023.02.16.528869.
SSID ssj0003677
Score 2.4571424
Snippet During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period...
SourceID pubmedcentral
proquest
pubmed
crossref
SourceType Open Access Repository
Aggregation Database
Index Database
SubjectTerms Animals
Cyclin B - genetics
Cyclin B - metabolism
Drosophila - genetics
Drosophila Proteins - metabolism
Male
Meiosis - genetics
Mitosis
Prophase
Spermatocytes - metabolism
Spermatogenesis - physiology
Title Cell-type-specific interacting proteins collaborate to regulate the timing of Cyclin B protein expression in male meiotic prophase
URI https://www.ncbi.nlm.nih.gov/pubmed/37882771
https://www.proquest.com/docview/2882324921
https://pubmed.ncbi.nlm.nih.gov/PMC10730016
Volume 150
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3db9MwELfKEIiXCQaMjg8ZwVuUkthJ2j7Siml87QFt0sRL5DiOWtElU5cirY_8Jfyp3Nmxk7Y8DF6iyum5Ue5X3_n8uztC3maZBCsWFxheUn6E250sSCRcmBjzTDGZ62qfp8nJefTpIr7o9X53WEurOhvI9V_zSv5HqzAGesUs2X_QrJsUBuAz6BeuoGG43krHU7VY-BhE9TFhEkk_uvyDTnzSSeYV9rK89lpl60YZS9N_Xmmns8a2Xpr4PL3BNElvYuWw-r9hyWo25CWYEu9SzSss8QpfuZrZg53Gt-3wj_TZsM0G6wQbJuLHVuKhNx04CpBYLOZSzuY6evulWqpyXbURc1iKNOZO1WotvG9ODLmwZtJmM-AdD7qxDMYxqc9kc7qgZIDUF4M2ZZbkCA-Zw-ZR7ZptqtU24DSZzTvGALwP0GCufiKDbxiMW5Nnj_m3LKHjJ-LOCKRTkE2N7B1ylw3BO0O3--NnZ-t5ont7uuduCuCC7Lv2dzddnp19zDYdt-PfnD0k-83GhL43KHtEeqo8IPdMq9KbA3L_a0PCgMHvlR58TH7tApB2AEgtAGkHgLSuqAUgBRBQA0BaFdQAkE6sHG0BCNNSBCBtAEgtAJ-Q8-MPZ9MTv2nq4UvOR7UvCglOpBKFEGOslQj-u8AaQWBJVB7yTErJpBBxxIRgMVdFnCjBE8Xg9YxkqPhTsldWpXpGaJgDLIKo4AyMShjLUYLOfZHwLMrHLMj65I197-mVqd2S7mq2T15blaSwtOJ5mShVtbpOGew-OVbUDPvk0KjIzYNtGNhwCHdGG8pzX8Cy7Zt3yvlMl28PdY-IMDm61eM9Jw_af8oLslcvV-ol-MF19kpD8Q8yt7o2
linkProvider Flying Publisher
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=Cell-type-specific+interacting+proteins+collaborate+to+regulate+the+timing+of+Cyclin+B+protein+expression+in+male+meiotic+prophase&rft.jtitle=Development+%28Cambridge%29&rft.au=Baker%2C+Catherine+C.&rft.au=Gallicchio%2C+Lorenzo&rft.au=Matias%2C+Neuza+R.&rft.au=Porter%2C+Douglas+F.&rft.date=2023-11-15&rft.issn=0950-1991&rft.eissn=1477-9129&rft.volume=150&rft.issue=22&rft_id=info:doi/10.1242%2Fdev.201709&rft.externalDBID=n%2Fa&rft.externalDocID=10_1242_dev_201709
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0950-1991&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0950-1991&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0950-1991&client=summon