Distinct roles of two eIF4E isoforms in the germline of Caenorhabditis elegans
Germ cells use both positive and negative mRNA translational control to regulate gene expression that drives their differentiation into gametes. mRNA translational control is mediated by RNA-binding proteins, miRNAs, and translation initiation factors. We have uncovered the discrete roles of two tra...
Saved in:
Published in: | Journal of cell science |
---|---|
Main Authors: | , , , , , , , , , |
Format: | Journal Article |
Language: | English |
Published: |
England
01-01-2020
|
Subjects: | |
Online Access: | Get full text |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
Abstract | Germ cells use both positive and negative mRNA translational control to regulate gene expression that drives their differentiation into gametes. mRNA translational control is mediated by RNA-binding proteins, miRNAs, and translation initiation factors. We have uncovered the discrete roles of two translation initiation factor eIF4E isoforms (IFE-1 and -3) that bind m7GTP mRNA caps during C. elegans germline development. IFE-3 plays important roles in germline sex determination (GSD), where it promotes oocyte cell fate and is dispensable for spermatogenesis. IFE-3 is expressed throughout the germline, localizes to germ granules but distinct from IFE-1 and PGL-1, and facilitates oocyte growth and viability. This contrasts with the robust expression of IFE-1 in spermatocytes, the isoform that resides within P granules in spermatocytes and oocytes, and promotes late spermatogenesis. Each eIF4E is localized by its cognate eIF4E binding protein (IFE-1:PGL-1 and IFE-3:IFET-1). IFE-3 and IFET-1 regulate translation of several GSD mRNAs, but not those under control of IFE-1. Distinct mutant phenotypes, in vivo localization, and differential mRNA translation suggest independent dormant and active periods for each eIF4E isoform in the germline. |
---|---|
AbstractList | Germ cells use both positive and negative mRNA translational control to regulate gene expression that drives their differentiation into gametes. mRNA translational control is mediated by RNA-binding proteins, miRNAs, and translation initiation factors. We have uncovered the discrete roles of two translation initiation factor eIF4E isoforms (IFE-1 and -3) that bind m7GTP mRNA caps during C. elegans germline development. IFE-3 plays important roles in germline sex determination (GSD), where it promotes oocyte cell fate and is dispensable for spermatogenesis. IFE-3 is expressed throughout the germline, localizes to germ granules but distinct from IFE-1 and PGL-1, and facilitates oocyte growth and viability. This contrasts with the robust expression of IFE-1 in spermatocytes, the isoform that resides within P granules in spermatocytes and oocytes, and promotes late spermatogenesis. Each eIF4E is localized by its cognate eIF4E binding protein (IFE-1:PGL-1 and IFE-3:IFET-1). IFE-3 and IFET-1 regulate translation of several GSD mRNAs, but not those under control of IFE-1. Distinct mutant phenotypes, in vivo localization, and differential mRNA translation suggest independent dormant and active periods for each eIF4E isoform in the germline. |
Author | Subash, Jacob S Buckner, David S Henderson, Melissa A Lee, Myon-Hee Keiper, Brett D Stoffel, Hamilton Sengupta, Madhu S Hoffman, Jenna L Boag, Peter R Huggins, Hayden P |
Author_xml | – sequence: 1 givenname: Hayden P surname: Huggins fullname: Huggins, Hayden P organization: Department of Biochemistry and Molecular Biology, Brody School of Medicine at East Carolina University, Greenville, NC 27834, USA – sequence: 2 givenname: Jacob S surname: Subash fullname: Subash, Jacob S organization: Department of Biochemistry and Molecular Biology, Brody School of Medicine at East Carolina University, Greenville, NC 27834, USA – sequence: 3 givenname: Hamilton surname: Stoffel fullname: Stoffel, Hamilton organization: Department of Biochemistry and Molecular Biology, Brody School of Medicine at East Carolina University, Greenville, NC 27834, USA – sequence: 4 givenname: Melissa A surname: Henderson fullname: Henderson, Melissa A organization: Department of Molecular Sciences, DeBusk College of Osteopathic Medicine, Lincoln Memorial University, Harrogate, TN 37752, USA – sequence: 5 givenname: Jenna L surname: Hoffman fullname: Hoffman, Jenna L organization: Department of Biochemistry and Molecular Biology, Brody School of Medicine at East Carolina University, Greenville, NC 27834, USA – sequence: 6 givenname: David S surname: Buckner fullname: Buckner, David S organization: Department of Biochemistry and Molecular Biology, Brody School of Medicine at East Carolina University, Greenville, NC 27834, USA – sequence: 7 givenname: Madhu S surname: Sengupta fullname: Sengupta, Madhu S organization: Monash Biomedicine Discovery Institute and Department of Biochemistry & Molecular Biology, Monash University, Melbourne, Australia – sequence: 8 givenname: Peter R orcidid: 0000-0002-0889-0859 surname: Boag fullname: Boag, Peter R organization: Monash Biomedicine Discovery Institute and Department of Biochemistry & Molecular Biology, Monash University, Melbourne, Australia – sequence: 9 givenname: Myon-Hee orcidid: 0000-0001-9020-2391 surname: Lee fullname: Lee, Myon-Hee organization: Department of Internal Medicine, Brody School of Medicine at East Carolina University, Greenville, NC 27834, USA – sequence: 10 givenname: Brett D orcidid: 0000-0002-8621-9825 surname: Keiper fullname: Keiper, Brett D organization: Department of Biochemistry and Molecular Biology, Brody School of Medicine at East Carolina University, Greenville, NC 27834, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34005102$$D View this record in MEDLINE/PubMed |
BookMark | eNqFzr0KwjAUQOEgim3VV5D7AoX0R0Ln2qKLk3tJ7W0bSZOSGxHfXgSdnc7yDSdiS2MNLliY5ELERZKJgEVEd865SAuxZkGWc35IeBqyy1GRV-bmwVmNBLYH_7SA5zqvQJHtrZsIlAE_IgzoJq0MflQp0Vg3yrZTXhGgxkEa2rJVLzXh7tsN29fVtTzF86OdsGtmpybpXs1vIPsL3kcnPK0 |
ContentType | Journal Article |
Copyright | 2020. Published by The Company of Biologists Ltd. |
Copyright_xml | – notice: 2020. Published by The Company of Biologists Ltd. |
DBID | NPM |
DatabaseName | PubMed |
DatabaseTitle | PubMed |
DatabaseTitleList | PubMed |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Biology |
EISSN | 1477-9137 |
ExternalDocumentID | 34005102 |
Genre | Journal Article |
GroupedDBID | --- -DZ -~X 0R~ 18M 2WC 34G 39C 4.4 53G 5GY 5RE 5VS 85S ABDNZ ABJNI ABPPZ ACGFO ACGFS ACIWK ACNCT ACPRK ADBBV ADCOW AEILP AENEX AFFNX AFRAH AGGIJ ALMA_UNASSIGNED_HOLDINGS BAWUL BTFSW CS3 DIK DU5 E3Z EBS F5P F9R GX1 H13 HZ~ IH2 INIJC KQ8 NPM O9- OK1 P2P R.V RCB RHF RHI RNS SJN TN5 TR2 UPT W2D W8F WH7 WOQ YQT ~02 ~KM |
ID | FETCH-pubmed_primary_340051023 |
IngestDate | Wed Oct 16 00:42:53 EDT 2024 |
IsPeerReviewed | true |
IsScholarly | true |
Keywords | eIF4E Germline sex determination Polyribosomes/polysomes Gametogenesis 4EBP mRNA translational control |
Language | English |
License | 2020. Published by The Company of Biologists Ltd. |
LinkModel | OpenURL |
MergedId | FETCHMERGED-pubmed_primary_340051023 |
ORCID | 0000-0002-8621-9825 0000-0001-9020-2391 0000-0002-0889-0859 |
PMID | 34005102 |
ParticipantIDs | pubmed_primary_34005102 |
PublicationCentury | 2000 |
PublicationDate | 2020-Jan-01 |
PublicationDateYYYYMMDD | 2020-01-01 |
PublicationDate_xml | – month: 01 year: 2020 text: 2020-Jan-01 day: 01 |
PublicationDecade | 2020 |
PublicationPlace | England |
PublicationPlace_xml | – name: England |
PublicationTitle | Journal of cell science |
PublicationTitleAlternate | J Cell Sci |
PublicationYear | 2020 |
SSID | ssj0007297 |
Score | 4.289073 |
Snippet | Germ cells use both positive and negative mRNA translational control to regulate gene expression that drives their differentiation into gametes. mRNA... |
SourceID | pubmed |
SourceType | Index Database |
Title | Distinct roles of two eIF4E isoforms in the germline of Caenorhabditis elegans |
URI | https://www.ncbi.nlm.nih.gov/pubmed/34005102 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtZ3PS8MwFMeDGwhexN-_Rw7eSqFbgtuO4jqq4C7bwdtI09QNtBlrh-y_9-VXM5WBHryUNikl9NO8vHz7kofQrehwGNYiEbI2vwsp4WmYCiXA8ywihHCluynpYtwdvfQGMY191jVf9q-koQxYq5Wzf6BdPxQK4ByYwxGow_FX3Aeq0xa80nGDOk6j-pCBeBzSOJiXUvmopQtufAWzrN1MvUhLFHI5Y2mmdjkKVDoKZpW8n76rkvsDO3j6D6MWrxO2BnPml46BdWLlzATlcpl6uXVcyTw3cQKJUloqHxSQ6Bx3dj3Ys3iDD4RZ4dWKFJ1oQ6QQxrBS9au4bTZ42cCweNccCNXWoeNHpTpW0FU1UIO0VdDm-GlUj7UwNVBpFN093-YG2keYHKB9-4LwvaFyiHZEcYR2TbrP9TEaOTZYs8Eyx8AGazbYscHzAgMb7Niou76ywZbNCWoN48lDEprGTBdm45CpayY5Rc1CFuIc4R7tQ68AlyHvUQpTz76IWDcjBC5FTnJ-gc62PORya80V2vMMrlGzWq7EDWqU2aql394nF0MjCg |
link.rule.ids | 315,782,786 |
linkProvider | Multiple Vendors |
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=Distinct+roles+of+two+eIF4E+isoforms+in+the+germline+of+Caenorhabditis+elegans&rft.jtitle=Journal+of+cell+science&rft.au=Huggins%2C+Hayden+P&rft.au=Subash%2C+Jacob+S&rft.au=Stoffel%2C+Hamilton&rft.au=Henderson%2C+Melissa+A&rft.date=2020-01-01&rft.eissn=1477-9137&rft_id=info%3Apmid%2F34005102&rft.externalDocID=34005102 |