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

被引:36
作者
Arnold, Andreas [1 ,2 ]
Rahman, Md Masuder [3 ]
Lee, Man Chun [3 ]
Muehlhaeusser, Sandra [1 ]
Katic, Iskra [1 ]
Gaidatzis, Dimos [1 ,5 ]
Hess, Daniel [1 ]
Scheckel, Claudia [1 ,2 ]
Wright, Jane E. [1 ]
Stetak, Attila [4 ]
Boag, Peter R. [3 ]
Ciosk, Rafal [1 ]
机构
[1] Friedrich Miescher Inst Biomed Res, CH-4058 Basel, Switzerland
[2] Univ Basel, CH-4003 Basel, Switzerland
[3] Monash Univ, Dept Biochem & Mol Biol, Clayton, Vic 3800, Australia
[4] Pharmazentrum, Biozentrum, Dept Neurosci, CH-4046 Basel, Switzerland
[5] Swiss Inst Bioinformat, CH-4058 Basel, Switzerland
基金
瑞士国家科学基金会; 英国医学研究理事会;
关键词
COLD-SHOCK DOMAIN; PHYSIOLOGICAL GERMLINE APOPTOSIS; MATERNAL MESSENGER-RNAS; CAENORHABDITIS-ELEGANS; GENE-EXPRESSION; STATISTICAL-MODEL; LIFE-SPAN; IN-VIVO; TRANSLATION; HELICASE;
D O I
10.1093/nar/gku1077
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
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.
引用
收藏
页码:13353 / 13369
页数:17
相关论文
共 63 条
[1]   Apoptosis Maintains Oocyte Quality in Aging Caenorhabditis elegans Females [J].
Andux, Sara ;
Ellis, Ronald E. .
PLOS GENETICS, 2008, 4 (12)
[2]   A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans [J].
Audhya, A ;
Hyndman, F ;
McLeod, IX ;
Maddox, AS ;
Yates, JR ;
Desai, A ;
Oegema, K .
JOURNAL OF CELL BIOLOGY, 2005, 171 (02) :267-279
[3]   Ribosomal protein L35 is required for 27SB pre-rRNA processing in Saccharomyces cerevisiae [J].
Babiano, Reyes ;
de la Cruz, Jesus .
NUCLEIC ACIDS RESEARCH, 2010, 38 (15) :5177-5192
[4]   ODORANT-SELECTIVE GENES AND NEURONS MEDIATE OLFACTION IN C-ELEGANS [J].
BARGMANN, CI ;
HARTWIEG, E ;
HORVITZ, HR .
CELL, 1993, 74 (03) :515-527
[5]   Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome [J].
Baugh, LR ;
Hill, AA ;
Slonim, DK ;
Brown, EL ;
Hunter, CP .
DEVELOPMENT, 2003, 130 (05) :889-900
[6]   Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis [J].
Boag, Peter R. ;
Atalay, Arzu ;
Robida, Stacey ;
Reinke, Valerie ;
Blackwell, T. Keith .
JOURNAL OF CELL BIOLOGY, 2008, 182 (03) :543-557
[7]   A conserved RNA-protein complex component involved in physiological germline apoptosis regulation in C-elegans [J].
Boag, PR ;
Nakamura, A ;
Blackwell, TK .
DEVELOPMENT, 2005, 132 (22) :4975-4986
[8]   A ROLE FOR TRANSCRIPTION AND FRGY2 IN MASKING MATERNAL MESSENGER-RNA WITHIN XENOPUS-OOCYTES [J].
BOUVET, P ;
WOLFFE, AP .
CELL, 1994, 77 (06) :931-941
[9]   Nucleolin interacts with several ribosomal proteins through its RGG domain [J].
Bouvet, P ;
Diaz, JJ ;
Kindbeiter, K ;
Madjar, JJ ;
Amalric, F .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1998, 273 (30) :19025-19029
[10]   LAB-1 antagonizes the Aurora B kinase in C. elegans [J].
de Carvalho, Carlos Egydio ;
Zaaijer, Sophie ;
Smolikov, Sarit ;
Gu, Yanjie ;
Schumacher, Jill M. ;
Colaiacovo, Monica P. .
GENES & DEVELOPMENT, 2008, 22 (20) :2869-2885