Regulation of Sperm-Specific Proteins by IFE-1, a Germline-Specific Homolog of eIF4E, in C. elegans

Kawasaki, Ichiro; Jeong, Myung-Hwan; Shim, Yhong–Hee

doi:10.1007/s10059-011-0021-y

Cited by 20 publications

(22 citation statements)

References 20 publications

(28 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…mRNAs from these latter two genes increase 2.2-and 2.4-fold after P-granule RNAi. Interestingly, genes regulated by P granules do not include those encoding SPE-44 and ELT-1, which have been shown to promote sperm-specific transcription (Kulkarni et al, 2012;Shim, 1999), or IFE-1, which promotes sperm-specific translation (Kawasaki et al, 2011).…”

Section: Expression In P-granule-depleted Germlinesmentioning

confidence: 99%

“…This small time window, when PGL-1/3 begins to be cleared from P granules in primary spermatocytes until spermatid budding, coincides with the onset of transcription and subsequent translation of sperm-specific mRNAs. IFE-1, which facilitates this sperm-specific translation (Henderson et al, 2009;Kawasaki et al, 2011), physically interacts with PGL-1 (Amiri et al, 2001). This interaction is predicted to repress IFE-1 activity until PGL-1 is cleared from P granules at the onset of spermatogenesis (Amiri et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

Campbell

Updike

2015

Development

View full text Add to dashboard Cite

Germ granules (P granules) in C. elegans are required for fertility and function to maintain germ cell identity and pluripotency. Sterility in the absence of P granules is often accompanied by the misexpression of soma-specific proteins and the initiation of somatic differentiation in germ cells. To investigate whether this is caused by the accumulation of somatic transcripts, we performed mRNA-seq on dissected germlines with and without P granules. Strikingly, we found that somatic transcripts do not increase in the young adult germline when P granules are impaired. Instead, we found that impairing P granules causes sperm-specific mRNAs to become highly overexpressed. This includes the accumulation of major sperm protein (MSP) transcripts in germ cells, a phenotype that is suppressed by feminization of the germline. A core component of P granules, the endo-siRNA-binding Argonaute protein CSR-1, has recently been ascribed with the ability to license transcripts for germline expression. However, impairing CSR-1 has very little effect on the accumulation of its mRNA targets. Instead, we found that CSR-1 functions with P granules to prevent MSP and sperm-specific mRNAs from being transcribed in the hermaphrodite germline. These findings suggest that P granules protect germline integrity through two different mechanisms, by (1) preventing the inappropriate expression of somatic proteins at the level of translational regulation, and by (2) functioning with CSR-1 to limit the domain of sperm-specific expression at the level of transcription.

show abstract

Section: Expression In P-granule-depleted Germlinesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

Campbell

Updike

2015

Development

View full text Add to dashboard Cite

show abstract

“…This suggests that a ubiquitous eIF4E isoform might carry out global translation initiation, whereas the other isoforms might be involved in more specific processes of translation (Hernández and VazquezPianzola, 2005). Work in C. elegans supports this, as IFE-1, a germline-specific eIF4E, is required for sperm (Amiri et al, 2001;Kawasaki et al, 2011) and oocyte (Henderson et al, 2009) maturation, loss of IFE-2 affects chromosome segregation at meiosis (Song et al, 2010), and IFE-4 is involved in translating only a small set of neural and muscle mRNAs involved in egg laying (Dinkova et al, 2005).…”

Section: Introductionmentioning

confidence: 96%

Eukaryotic initiation factor 4E-3 is essential for meiotic chromosome segregation, cytokinesis and male fertility in Drosophila

et al. 2012

View full text Add to dashboard Cite

SUMMARYGene expression is translationally regulated during many cellular and developmental processes. Translation can be modulated by affecting the recruitment of mRNAs to the ribosome, which involves recognition of the 5Ј cap structure by the cap-binding protein eIF4E. Drosophila has several genes encoding eIF4E-related proteins, but the biological role of most of them remains unknown. Here, we report that Drosophila eIF4E-3 is required specifically during spermatogenesis. Males lacking eIF4E-3 are sterile, showing defects in meiotic chromosome segregation, cytokinesis, nuclear shaping and individualization. We show that eIF4E-3 physically interacts with both eIF4G and eIF4G-2, the latter being a factor crucial for spermatocyte meiosis. In eIF4E-3 mutant testes, many proteins are present at different levels than in wild type, suggesting widespread effects on translation. Our results imply that eIF4E-3 forms specific eIF4F complexes that are essential for spermatogenesis.

show abstract

“…Five isoforms of eIF4E (IFE-1-IFE-5) are expressed in the nematode C. elegans (Jankowska- Anyszka et al, 1998;Keiper et al, 2000). We have previously shown that individual isoforms regulate a unique subset of mRNAs in a tissue-specific manner (Amiri et al, 2001;Dinkova et al, 2005;Henderson et al, 2009;Kawasaki et al, 2011;Song et al, 2010). Given that all IFEs bind to mRNA caps, these findings suggest a selective cap-dependent regulation that goes beyond mTOR regulation.…”

Section: Introductionmentioning

confidence: 99%

Spatial and temporal translational control of germ cell mRNAs mediated by the eIF4E isoform IFE-1

Friday

Henderson

Morrison

et al. 2015

Journal of Cell Science

View full text Add to dashboard Cite

Regulated mRNA translation is vital for germ cells to produce new proteins in the spatial and temporal patterns that drive gamete development. Translational control involves the de-repression of stored mRNAs and their recruitment by eukaryotic initiation factors (eIFs) to ribosomes. C. elegans expresses five eIF4Es (IFE-1-IFE-5); several have been shown to selectively recruit unique pools of mRNA. Individual IFE knockouts yield unique phenotypes due to inefficient translation of certain mRNAs. Here, we identified mRNAs preferentially translated through the germline-specific eIF4E isoform IFE-1. Differential polysome microarray analysis identified 77 mRNAs recruited by IFE-1. Among the IFE-1-dependent mRNAs are several required for late germ cell differentiation and maturation. Polysome association of gld-1, vab-1, vpr-1, rab-7 and rnp-3 mRNAs relies on IFE-1. Live animal imaging showed IFE-1-dependent selectivity in spatial and temporal translation of germline mRNAs. Altered MAPK activation in oocytes suggests dual roles for IFE-1, both promoting and suppressing oocyte maturation at different stages. This single eIF4E isoform exerts positive, selective translational control during germ cell differentiation.

show abstract

Regulation of Sperm-Specific Proteins by IFE-1, a Germline-Specific Homolog of eIF4E, in C. elegans

Cited by 20 publications

References 20 publications

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

Eukaryotic initiation factor 4E-3 is essential for meiotic chromosome segregation, cytokinesis and male fertility in Drosophila

Spatial and temporal translational control of germ cell mRNAs mediated by the eIF4E isoform IFE-1

Contact Info

Product

Resources

About