Literature DB >> 11641215

An isoform of eIF4E is a component of germ granules and is required for spermatogenesis in C. elegans.

A Amiri1, B D Keiper, I Kawasaki, Y Fan, Y Kohara, R E Rhoads, S Strome.   

Abstract

Control of gene expression at the translational level is crucial for many developmental processes. The mRNA cap-binding protein, eIF4E, is a key player in regulation of translation initiation; appropriate levels of eIF4E are essential for normal cell-cycle regulation and tissue differentiation. The observation that eIF4E levels are elevated during gametogenesis in several organisms suggests that eIF4E might have a specific role in gamete formation as well. We show that one of the five isoforms of C. elegans eIF4E, IFE-1, is enriched in the germline and is a component of germ granules (P granules). The association of IFE-1 with P granules requires the P-granule protein PGL-1. In vitro PGL-1 interacts directly with IFE-1, but not with the other four isoforms of eIF4E. Analysis of animals depleted of IFE-1 by RNAi shows that IFE-1 is required for spermatogenesis, specifically for efficient progression through the meiotic divisions and for the production of functional sperm, in both hermaphrodites and males. The requirement for IFE-1 is highly sensitive to temperature. IFE-1 is not required for oogenesis, as ife-1(RNAi) hermaphrodites produce viable progeny when normal sperm are supplied. Consistent with a primary role in spermatogenesis, ife-1 mRNA levels are highest in regions of the gonad undergoing spermatogenesis. Our results suggest that C. elegans spermatogenesis requires either this specific isoform of eIF4E or an elevated level of eIF4E.

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Year:  2001        PMID: 11641215      PMCID: PMC2430591          DOI: 10.1242/dev.128.20.3899

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.868


  70 in total

Review 1.  Protein synthesis, cell growth and oncogenesis.

Authors:  R E Rhoads
Journal:  Curr Opin Cell Biol       Date:  1991-12       Impact factor: 8.382

Review 2.  An analysis of vertebrate mRNA sequences: intimations of translational control.

Authors:  M Kozak
Journal:  J Cell Biol       Date:  1991-11       Impact factor: 10.539

3.  Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5' cap.

Authors:  A Lazaris-Karatzas; K S Montine; N Sonenberg
Journal:  Nature       Date:  1990-06-07       Impact factor: 49.962

Review 4.  Regulation of eukaryotic protein synthesis by initiation factors.

Authors:  R E Rhoads
Journal:  J Biol Chem       Date:  1993-02-15       Impact factor: 5.157

5.  Overexpression of eukaryotic protein synthesis initiation factor 4E in HeLa cells results in aberrant growth and morphology.

Authors:  A De Benedetti; R E Rhoads
Journal:  Proc Natl Acad Sci U S A       Date:  1990-11       Impact factor: 11.205

6.  Expression of antisense RNA against initiation factor eIF-4E mRNA in HeLa cells results in lengthened cell division times, diminished translation rates, and reduced levels of both eIF-4E and the p220 component of eIF-4F.

Authors:  A De Benedetti; S Joshi-Barve; C Rinker-Schaeffer; R E Rhoads
Journal:  Mol Cell Biol       Date:  1991-11       Impact factor: 4.272

7.  The mRNA 5' cap-binding protein, eIF-4E, cooperates with v-myc or E1A in the transformation of primary rodent fibroblasts.

Authors:  A Lazaris-Karatzas; N Sonenberg
Journal:  Mol Cell Biol       Date:  1992-03       Impact factor: 4.272

8.  Translation in Saccharomyces cerevisiae: initiation factor 4E-dependent cell-free system.

Authors:  M Altmann; N Sonenberg; H Trachsel
Journal:  Mol Cell Biol       Date:  1989-10       Impact factor: 4.272

9.  Characterization of a germ-line proliferation mutation in C. elegans.

Authors:  M J Beanan; S Strome
Journal:  Development       Date:  1992-11       Impact factor: 6.868

10.  mRNAs containing extensive secondary structure in their 5' non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E.

Authors:  A E Koromilas; A Lazaris-Karatzas; N Sonenberg
Journal:  EMBO J       Date:  1992-11       Impact factor: 11.598

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  58 in total

1.  A C. elegans eIF4E-family member upregulates translation at elevated temperatures of mRNAs encoding MSH-5 and other meiotic crossover proteins.

Authors:  Anren Song; Sara Labella; Nadejda L Korneeva; Brett D Keiper; Eric J Aamodt; Monique Zetka; Robert E Rhoads
Journal:  J Cell Sci       Date:  2010-06-08       Impact factor: 5.285

2.  S6K links cell fate, cell cycle and nutrient response in C. elegans germline stem/progenitor cells.

Authors:  Dorota Z Korta; Simon Tuck; E Jane Albert Hubbard
Journal:  Development       Date:  2012-01-25       Impact factor: 6.868

Review 3.  New insights into the regulation of RNP granule assembly in oocytes.

Authors:  Jennifer A Schisa
Journal:  Int Rev Cell Mol Biol       Date:  2012       Impact factor: 6.813

4.  Caenorhabditis elegans decapping proteins: localization and functional analysis of Dcp1, Dcp2, and DcpS during embryogenesis.

Authors:  Sabbi Lall; Fabio Piano; Richard E Davis
Journal:  Mol Biol Cell       Date:  2005-10-05       Impact factor: 4.138

5.  Translational control of meiotic cell cycle progression and spermatid differentiation in male germ cells by a novel eIF4G homolog.

Authors:  Catherine C Baker; Margaret T Fuller
Journal:  Development       Date:  2007-07-04       Impact factor: 6.868

6.  Translational activation of developmental messenger RNAs during neonatal mouse testis development.

Authors:  Vesna A Chappell; Jonathan T Busada; Brett D Keiper; Christopher B Geyer
Journal:  Biol Reprod       Date:  2013-09-19       Impact factor: 4.285

7.  Large P body-like RNPs form in C. elegans oocytes in response to arrested ovulation, heat shock, osmotic stress, and anoxia and are regulated by the major sperm protein pathway.

Authors:  Molly C Jud; Michael J Czerwinski; Megan P Wood; Rachel A Young; Christopher M Gallo; Jeremy S Bickel; Emily L Petty; Jennifer M Mason; Brent A Little; Pamela A Padilla; Jennifer A Schisa
Journal:  Dev Biol       Date:  2008-03-14       Impact factor: 3.582

Review 8.  P granule assembly and function in Caenorhabditis elegans germ cells.

Authors:  Dustin Updike; Susan Strome
Journal:  J Androl       Date:  2009-10-29

9.  Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells.

Authors:  Ujwal Sheth; Jason Pitt; Shannon Dennis; James R Priess
Journal:  Development       Date:  2010-03-10       Impact factor: 6.868

Review 10.  eIF4E: new family members, new binding partners, new roles.

Authors:  Robert E Rhoads
Journal:  J Biol Chem       Date:  2009-02-23       Impact factor: 5.157

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