Diverse cap-binding properties of Drosophila eIF4E isoforms

Zuberek, Joanna; Kuchta, Krzysztof; Hernández, Greco; Sonenberg, Nahum; Ginalski, Krzysztof

doi:10.1016/j.bbapap.2016.06.015

Cited by 5 publications

(7 citation statements)

References 79 publications

(106 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Positive interactions were detected between eIF4E-5 and 4E-BP, eIF4G-2, 4E-T, and Cup, but not eIF4G. The lack of interaction between eIF4E-5 and eIF4G was unexpected, as we previously detected a weak interaction of these proteins in a more sensitive yeast two-hybrid assay (Hernández et al, 2005) and in fluorescent binding assays with a short eIF4G peptide containing the eIF4E-binding motif (Zuberek et al, 2016). In addition, unlike binding of eIF4E-5 to 4E-BP, 4E-T and Cup, binding to eIF4G-2 was sensitive to more stringent selection conditions, indicating that eIF4E-5 may preferentially bind inhibitors of translation rather than translational activators.…”

Section: Resultsmentioning

confidence: 87%

“…C. elegans has five paralogs (IFE-1 to IFE-5): IFE-3, which is most similar to mammalian eIF4E1 ( i.e., canonical), is essential for viability; IFE-1 is required for spermatogenesis and oocyte maturation; IFE-2 is needed for meiotic recombination; and IFE-4 is required to translate mRNAs involved in egg laying (Amiri et al, 2001; Dinkova et al, 2005; Henderson et al, 2009; Kawasaki et al, 2011; Keiper et al, 2000; Song et al, 2010). Drosophila has eight paralogs (eIF4E-1 to eIF4E-8/4E-HP) that bind to mRNA 5’ caps with varying affinities in vitro (Zuberek et al, 2016). Canonical eIF4E-1 and 4E-HP are essential for viability, and eIF4E-3 is needed for meiotic chromosome segregation and cytokinesis during spermatogenesis (Brown et al, 2014; Chintapalli et al, 2007; Ghosh and Lasko, 2015; Hernández et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Eukaryotic translation initiation factor eIF4E-5 is required for spermiogenesis in Drosophila melanogaster

Shao

Fingerhut

Falk

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Drosophila sperm development is characterized by extensive post-transcriptional regulation whereby thousands of transcripts are preserved for translation during later stages. A key step in translation initiation is the binding of eukaryotic initiation factor 4E (eIF4E) to the 5' mRNA cap. Drosophila has multiple paralogs of eIF4E, including four (eIF4E-3, -4, -5, and -7) that are highly expressed in the testis. Other than eIF4E-3, none of these has been characterized genetically. Here, using CRISPR/Cas9 mutagenesis, we determined that eIF4E-5 is essential for male fertility. eIF4E-5 mutants exhibit defects during post-meiotic stages, including a fully penetrant defect in individualization, resulting in failure to produce mature sperm. eIF4E-5 protein localizes to the distal ends of elongated spermatid cysts, where it regulates non-apoptotic caspase activity during individualization by promoting local accumulation of the E3 ubiquitin ligase inhibitor Soti. eIF4E-5 mutants also have mild defects in spermatid cyst polarization, similar to mutants affecting the cytoplasmic polyadenylation-element binding protein Orb2 and atypical protein kinase C (aPKC). Our results further extend the diversity of non-canonical eIF4Es that carry out distinct spatiotemporal roles during spermatogenesis.

show abstract

Section: Resultsmentioning

confidence: 87%

Section: Introductionmentioning

confidence: 99%

Eukaryotic translation initiation factor eIF4E-5 is required for spermiogenesis in Drosophila melanogaster

Shao

Fingerhut

Falk

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…However, stress and aging promote protein aggregation, organelle dysfunction and oxidative processes, which eventually might lead to cell damage and impairments in tissue repair, promoting dysfunction and development of age-dependent diseases [ 52 ]. 4E-BP affects translational processes through its interaction with eIF4E-1, the ubiquitous eIF4E [ 53 ], and this interaction might alter the abundance of other proteins in the heart during aging. Summarising, the triad 4E-BP, eIF4E-4 and SERCA should be explored in more detail in the future to understand the effects of ageing in the cardiomyocyte response to variable levels of 4E-BP.…”

Section: Discussionmentioning

confidence: 99%

Interplay between SERCA, 4E-BP, and eIF4E in the Drosophila heart

et al. 2022

Self Cite

View full text Add to dashboard Cite

Appropriate cardiac performance depends on a tightly controlled handling of Ca2+ in a broad range of species, from invertebrates to mammals. The role of the Ca2+ ATPase, SERCA, in Ca2+ handling is pivotal, and its activity is regulated, inter alia, by interacting with distinct proteins. Herein, we give evidence that 4E binding protein (4E-BP) is a novel regulator of SERCA activity in Drosophila melanogaster during cardiac function. Flies over-expressing 4E-BP showed improved cardiac performance in young individuals associated with incremented SERCA activity. Moreover, we demonstrate that SERCA interacts with translation initiation factors eIF4E-1, eIF4E-2 and eIF4E-4 in a yeast two-hybrid assay. The specific identification of eIF4E-4 in cardiac tissue leads us to propose that the interaction of elF4E-4 with SERCA may be the basis of the cardiac effects observed in 4E-BP over-expressing flies associated with incremented SERCA activity.

show abstract

“…The biochemical properties of all D. melanogaster eIF4E proteins are well characterised. Homology modelling and fluorescence binding assays determined that all proteins possess cap‐binding ability (Zuberek et al ., 2016), albeit with a 14‐fold affinity difference among them. eIF4E‐3 and eIF4E‐4 exhibited the highest and the lowest cap‐binding affinities, respectively, and eIF4E‐3 and eIF4E‐5 bind the second nucleoside of the cap in an unusual manner via stacking interactions with histidine or phenylalanine, respectively.…”

Section: Eif4e In Drosophilamentioning

confidence: 99%

eIF4E as a molecular wildcard in metazoans RNA metabolism

Hernández

Vázquez-Pianzola

2023

Biological Reviews

Self Cite

View full text Add to dashboard Cite

The evolutionary origin of eukaryotes spurred the transition from prokaryotic‐like translation to a more sophisticated, eukaryotic translation. During this process, successive gene duplication of a single, primordial eIF4E gene encoding the mRNA cap‐binding protein eukaryotic translation initiation factor 4E (eIF4E) gave rise to a plethora of paralog genes across eukaryotes that underwent further functional diversification in RNA metabolism. The ability to take different roles is due to eIF4E promiscuity in binding many partner proteins, rendering eIF4E a highly versatile and multifunctional player that functions as a molecular wildcard. Thus, in metazoans, eIF4E paralogs are involved in various processes, including messenger RNA (mRNA) processing, export, translation, storage, and decay. Moreover, some paralogs display differential expression in tissues and developmental stages and show variable biochemical properties. In this review, we discuss recent advances shedding light on the functional diversification of eIF4E in metazoans. We emphasise humans and two phylogenetically distant species which have become paradigms for studies on development, namely the fruit fly Drosophila melanogaster and the roundworm Caenorhabditis elegans.

show abstract

Diverse cap-binding properties of Drosophila eIF4E isoforms

Cited by 5 publications

References 79 publications

Eukaryotic translation initiation factor eIF4E-5 is required for spermiogenesis in Drosophila melanogaster

Eukaryotic translation initiation factor eIF4E-5 is required for spermiogenesis in Drosophila melanogaster

Interplay between SERCA, 4E-BP, and eIF4E in the Drosophila heart

eIF4E as a molecular wildcard in metazoans RNA metabolism

Contact Info

Product

Resources

About