Functional characterization of C. elegans Y-box-binding proteins reveals tissue-specific functions and a critical role in the formation of polysomes

Andreas Arnold, Md Masuder Rahman, Man C Lee, Sandra Meuhlhaeusser, Iskra Katic, Dimos Gaidatzis, Daniel Hess, Claudia Scheckel, Jane E Wright, Attila Stetak, Peter R Boag, Rafal Ciosk

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Abstract

The cold shock domain is one of the most highly conserved motifs between bacteria and higher eukaryotes. Y-box-binding proteins represent a subfamily of cold shock domain proteins with pleiotropic functions, ranging from transcription in the nucleus to translation in the cytoplasm. These proteins have been investigated in all major model organisms except Caenorhabditis elegans. In this study, we set out to fill this gap and present a functional characterization of CEYs, the C. elegans Y-box-binding proteins. We find that, similar to other organisms, CEYs are essential for proper gametogenesis. However, we also report a novel function of these proteins in the formation of large polysomes in the soma. In the absence of the somatic CEYs, polysomes are dramatically reduced with a simultaneous increase in monosomes and disomes, which, unexpectedly, has no obvious impact on animal biology. Because transcripts that are enriched in polysomes in wild-type animals tend to be less abundant in the absence of CEYs, our findings suggest that large polysomes might depend on transcript stabilization mediated by CEY proteins.
Original languageEnglish
Pages (from-to)13353 - 13369
Number of pages17
JournalNucleic Acids Research
Volume42
Issue number21
DOIs
Publication statusPublished - 2014

Cite this

Arnold, Andreas ; Rahman, Md Masuder ; Lee, Man C ; Meuhlhaeusser, Sandra ; Katic, Iskra ; Gaidatzis, Dimos ; Hess, Daniel ; Scheckel, Claudia ; Wright, Jane E ; Stetak, Attila ; Boag, Peter R ; Ciosk, Rafal. / Functional characterization of C. elegans Y-box-binding proteins reveals tissue-specific functions and a critical role in the formation of polysomes. In: Nucleic Acids Research. 2014 ; Vol. 42, No. 21. pp. 13353 - 13369.
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abstract = "The cold shock domain is one of the most highly conserved motifs between bacteria and higher eukaryotes. Y-box-binding proteins represent a subfamily of cold shock domain proteins with pleiotropic functions, ranging from transcription in the nucleus to translation in the cytoplasm. These proteins have been investigated in all major model organisms except Caenorhabditis elegans. In this study, we set out to fill this gap and present a functional characterization of CEYs, the C. elegans Y-box-binding proteins. We find that, similar to other organisms, CEYs are essential for proper gametogenesis. However, we also report a novel function of these proteins in the formation of large polysomes in the soma. In the absence of the somatic CEYs, polysomes are dramatically reduced with a simultaneous increase in monosomes and disomes, which, unexpectedly, has no obvious impact on animal biology. Because transcripts that are enriched in polysomes in wild-type animals tend to be less abundant in the absence of CEYs, our findings suggest that large polysomes might depend on transcript stabilization mediated by CEY proteins.",
author = "Andreas Arnold and Rahman, {Md Masuder} and Lee, {Man C} and Sandra Meuhlhaeusser and Iskra Katic and Dimos Gaidatzis and Daniel Hess and Claudia Scheckel and Wright, {Jane E} and Attila Stetak and Boag, {Peter R} and Rafal Ciosk",
year = "2014",
doi = "10.1093/nar/gku1077",
language = "English",
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Arnold, A, Rahman, MM, Lee, MC, Meuhlhaeusser, S, Katic, I, Gaidatzis, D, Hess, D, Scheckel, C, Wright, JE, Stetak, A, Boag, PR & Ciosk, R 2014, 'Functional characterization of C. elegans Y-box-binding proteins reveals tissue-specific functions and a critical role in the formation of polysomes', Nucleic Acids Research, vol. 42, no. 21, pp. 13353 - 13369. https://doi.org/10.1093/nar/gku1077

Functional characterization of C. elegans Y-box-binding proteins reveals tissue-specific functions and a critical role in the formation of polysomes. / Arnold, Andreas; Rahman, Md Masuder; Lee, Man C; Meuhlhaeusser, Sandra; Katic, Iskra; Gaidatzis, Dimos; Hess, Daniel; Scheckel, Claudia; Wright, Jane E; Stetak, Attila; Boag, Peter R; Ciosk, Rafal.

In: Nucleic Acids Research, Vol. 42, No. 21, 2014, p. 13353 - 13369.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Functional characterization of C. elegans Y-box-binding proteins reveals tissue-specific functions and a critical role in the formation of polysomes

AU - Arnold, Andreas

AU - Rahman, Md Masuder

AU - Lee, Man C

AU - Meuhlhaeusser, Sandra

AU - Katic, Iskra

AU - Gaidatzis, Dimos

AU - Hess, Daniel

AU - Scheckel, Claudia

AU - Wright, Jane E

AU - Stetak, Attila

AU - Boag, Peter R

AU - Ciosk, Rafal

PY - 2014

Y1 - 2014

N2 - The cold shock domain is one of the most highly conserved motifs between bacteria and higher eukaryotes. Y-box-binding proteins represent a subfamily of cold shock domain proteins with pleiotropic functions, ranging from transcription in the nucleus to translation in the cytoplasm. These proteins have been investigated in all major model organisms except Caenorhabditis elegans. In this study, we set out to fill this gap and present a functional characterization of CEYs, the C. elegans Y-box-binding proteins. We find that, similar to other organisms, CEYs are essential for proper gametogenesis. However, we also report a novel function of these proteins in the formation of large polysomes in the soma. In the absence of the somatic CEYs, polysomes are dramatically reduced with a simultaneous increase in monosomes and disomes, which, unexpectedly, has no obvious impact on animal biology. Because transcripts that are enriched in polysomes in wild-type animals tend to be less abundant in the absence of CEYs, our findings suggest that large polysomes might depend on transcript stabilization mediated by CEY proteins.

AB - The cold shock domain is one of the most highly conserved motifs between bacteria and higher eukaryotes. Y-box-binding proteins represent a subfamily of cold shock domain proteins with pleiotropic functions, ranging from transcription in the nucleus to translation in the cytoplasm. These proteins have been investigated in all major model organisms except Caenorhabditis elegans. In this study, we set out to fill this gap and present a functional characterization of CEYs, the C. elegans Y-box-binding proteins. We find that, similar to other organisms, CEYs are essential for proper gametogenesis. However, we also report a novel function of these proteins in the formation of large polysomes in the soma. In the absence of the somatic CEYs, polysomes are dramatically reduced with a simultaneous increase in monosomes and disomes, which, unexpectedly, has no obvious impact on animal biology. Because transcripts that are enriched in polysomes in wild-type animals tend to be less abundant in the absence of CEYs, our findings suggest that large polysomes might depend on transcript stabilization mediated by CEY proteins.

UR - http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4245946/pdf/gku1077.pdf

U2 - 10.1093/nar/gku1077

DO - 10.1093/nar/gku1077

M3 - Article

VL - 42

SP - 13353

EP - 13369

JO - Nucleic Acids Research

JF - Nucleic Acids Research

SN - 0305-1048

IS - 21

ER -