Functional analysis of seven genes encoding eight translation initiation factor 4E (eIF4E) isoforms in Drosophila

Hernández, Greco; Altmann, Michael; Sierra, J M; Urlaub, Henning; Corral, Ruth Díez del; Schwartz, Peter J.; Rivera‐Pomar, Rolando

doi:10.1016/j.mod.2004.11.011

Cited by 104 publications

(166 citation statements)

References 80 publications

Supporting

Mentioning

156

Contrasting

Unclassified

Order By: Relevance

“…The coding sequence of eIF4E1 was likewise amplified from testes cDNA, ligated into pCRII-TOPO and inserted into the SalI/SacI sites of pMT-Myc (Bunch et al, 1988). The eIF4E1 protein is one of the two polypeptides that are generated from the eIF-4E (FlyBase) locus; eIF-4E-RA and eIF-4E-RC encode eIF4E1 and eIF4E2, respectively (Hernandez et al, 2005).…”

Section: Cloningmentioning

confidence: 99%

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

Baker

Fuller

2007

Development

View full text Add to dashboard Cite

Translational control is crucial for proper timing of developmental events that take place in the absence of transcription, as in meiotic activation in oocytes, early embryogenesis in many organisms, and spermatogenesis. Here we show that a novel form of the translation initiation complex component eIF4G in Drosophila, eIF4G2, is required specifically for male germ cells to undergo meiotic division and proper spermatid differentiation. Flies mutant for eIF4G2 are viable and female fertile but male sterile. Spermatocytes form, but the germ cells in mutant males skip the major events of the meiotic divisions and form aberrant spermatids with large nuclei. Consistent with the failure to undergo the meiotic divisions, function of eIF4G2 is required posttranscriptionally for normal accumulation of the core cell cycle regulatory proteins Twine and CycB in mature spermatocytes. Loss of eIF4G2 function also causes widespread defects in spermatid differentiation. Although differentiation markers Dj and Fzo are expressed in late-stage eIF4G2 mutant germ cells, several key steps of spermatid differentiation fail, including formation of a compact mitochondrial derivative and full elongation. Our results suggest that an alternate form of the translation initiation machinery may be required for regulation and execution of key steps in male germ cell differentiation.

show abstract

Section: Cloningmentioning

confidence: 99%

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

Baker

Fuller

2007

Development

View full text Add to dashboard Cite

show abstract

“…Variants of eIF4E may show developmental regulation. Drosophila melanogaster has eight isoforms that show distinct patterns of expression during embryogenesis (Hernández et al 2005). Distinct variant eIF4E-eIF4G interactions are thus expected and observed (Ptushkina et al 2001).…”

Section: Introductionmentioning

confidence: 97%

eIF4F-like complexes formed by cap-binding homolog TbEIF4E5 with TbEIF4G1 or TbEIF4G2 are implicated in post-transcriptional regulation in Trypanosoma brucei

Freire

Vashisht

Malvezzi

et al. 2014

RNA

View full text Add to dashboard Cite

Members of the eIF4E mRNA cap-binding family are involved in translation and the modulation of transcript availability in other systems as part of a three-component complex including eIF4G and eIF4A. The kinetoplastids possess four described eIF4E and five eIF4G homologs. We have identified two new eIF4E family proteins in Trypanosoma brucei, and define distinct complexes associated with the fifth member, TbEIF4E5. The cytosolic TbEIF4E5 protein binds cap 0 in vitro. TbEIF4E5 was found in association with two of the five TbEIF4Gs. TbIF4EG1 bound TbEIF4E5, a 47.5-kDa protein with two RNA-binding domains, and either the regulatory protein 14-3-3 II or a 117.5-kDa protein with guanylyltransferase and methyltransferase domains in a potentially dynamic interaction. The TbEIF4G2/TbEIF4E5 complex was associated with a 17.9-kDa hypothetical protein and both 14-3-3 variants I and II. Knockdown of TbEIF4E5 resulted in the loss of productive cell movement, as evidenced by the inability of the cells to remain in suspension in liquid culture and the loss of social motility on semisolid plating medium, as well as a minor reduction of translation. Cells appeared lethargic, as opposed to compromised in flagellar function per se. The minimal use of transcriptional control in kinetoplastids requires these organisms to implement downstream mechanisms to regulate gene expression, and the TbEIF4E5/TbEIF4G1/117.5-kDa complex in particular may be a key player in that process. We suggest that a pathway involved in cell motility is affected, directly or indirectly, by one of the TbEIF4E5 complexes.

show abstract

“…Drosophila species have undergone extensive expansion of EIF4E-encoding loci to as many as seven different Class I eIF4E isoforms (Tettweiler et al, 2012). The seven EIF4E isoforms of Drosophila melanogaster are differentially expressed, with only five able to bind to eIF4G and complement deletion of yeast eIF4E (Hernández et al, 2005). The eIF4E-3 isoform of D. melanogaster was recently described as having a specific role in spermatogenesis .…”

mentioning

confidence: 99%

Two Arabidopsis Loci Encode Novel Eukaryotic Initiation Factor 4E Isoforms That Are Functionally Distinct from the Conserved Plant Eukaryotic Initiation Factor 4E

et al. 2014

View full text Add to dashboard Cite

Canonical translation initiation in eukaryotes begins with the Eukaryotic Initiation Factor 4F (eIF4F) complex, made up of eIF4E, which recognizes the 7-methylguanosine cap of messenger RNA, and eIF4G, which serves as a scaffold to recruit other translation initiation factors that ultimately assemble the 80S ribosome. Many eukaryotes have secondary EIF4E genes with divergent properties. The model plant Arabidopsis (Arabidopsis thaliana) encodes two such genes in tandem loci on chromosome 1, EIF4E1B (At1g29550) and EIF4E1C (At1g29590). This work identifies EIF4E1B/EIF4E1C-type genes as a Brassicaceae-specific diverged form of EIF4E. There is little evidence for EIF4E1C gene expression; however, the EIF4E1B gene appears to be expressed at low levels in most tissues, though microarray and RNA Sequencing data support enrichment in reproductive tissue. Purified recombinant eIF4E1b and eIF4E1c proteins retain cap-binding ability and form functional complexes in vitro with eIF4G. The eIF4E1b/eIF4E1c-type proteins support translation in yeast (Saccharomyces cerevisiae) but promote translation initiation in vitro at a lower rate compared with eIF4E. Findings from surface plasmon resonance studies indicate that eIF4E1b and eIF4E1c are unlikely to bind eIF4G in vivo when in competition with eIF4E. This study concludes that eIF4E1b/eIF4E1c-type proteins, although bona fide cap-binding proteins, have divergent properties and, based on apparent limited tissue distribution in Arabidopsis, should be considered functionally distinct from the canonical plant eIF4E involved in translation initiation.

show abstract

Functional analysis of seven genes encoding eight translation initiation factor 4E (eIF4E) isoforms in Drosophila

Cited by 104 publications

References 80 publications

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

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

eIF4F-like complexes formed by cap-binding homolog TbEIF4E5 with TbEIF4G1 or TbEIF4G2 are implicated in post-transcriptional regulation in Trypanosoma brucei

Two Arabidopsis Loci Encode Novel Eukaryotic Initiation Factor 4E Isoforms That Are Functionally Distinct from the Conserved Plant Eukaryotic Initiation Factor 4E

Contact Info

Product

Resources

About