Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae

被引:196
作者
Buchan, J. Ross [1 ,2 ]
Yoon, Je-Hyun [2 ]
Parker, Roy [1 ,2 ]
机构
[1] Univ Arizona, Howard Hughes Med Inst, Tucson, AZ 85721 USA
[2] Univ Arizona, Dept Mol & Cellular Biol, Tucson, AZ 85721 USA
基金
美国国家卫生研究院;
关键词
Stress granules; P-bodies; Translation; mRNA; CYTOPLASMIC PROCESSING BODIES; MESSENGER-RNA TRANSLATION; P-BODIES; ELECTRON TRANSPORT; YEAST; INITIATION; INHIBITION; PROTEIN; EIF4G; PHOSPHORYLATION;
D O I
10.1242/jcs.078444
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Eukaryotic cells respond to cellular stresses by the inhibition of translation and the accumulation of mRNAs in cytoplasmic RNA-protein (ribonucleoprotein) granules termed stress granules and P-bodies. An unresolved issue is how different stresses affect formation of messenger RNP (mRNP) granules. In the present study, we examine how sodium azide (NaN(3)), which inhibits mitochondrial respiration, affects formation of mRNP granules as compared with glucose deprivation in budding yeast. We observed that NaN(3) treatment inhibits translation and triggers formation of P-bodies and stress granules. The composition of stress granules induced by NaN(3) differs from that of glucose-deprived cells by containing eukaryotic initiation factor (eIF)3, eIF4A/B, eIF5B and eIF1A proteins, and by lacking the heterogeneous nuclear RNP (hnRNP) protein Hrp1. Moreover, in contrast with glucose-deprived stress granules, NaN(3)-triggered stress granules show different assembly rules, form faster and independently from P-bodies and dock or merge with P-bodies over time. Strikingly, addition of NaN(3) and glucose deprivation in combination, regardless of the order, always results in stress granules of a glucose deprivation nature, suggesting that both granules share an mRNP remodeling pathway. These results indicate that stress granule assembly, kinetics and composition in yeast can vary in a stress-specific manner, which we suggest reflects different rate-limiting steps in a common mRNP remodeling pathway.
引用
收藏
页码:228 / 239
页数:12
相关论文
共 38 条
[21]   Uncoupling Stress Granule Assembly and Translation Initiation Inhibition [J].
Mokas, Sophie ;
Mills, John R. ;
Garreau, Cristina ;
Fournier, Marie-Josee ;
Robert, Francis ;
Arya, Prabhat ;
Kaufman, Randal J. ;
Pelletier, Jerry ;
Mazroui, Rachid .
MOLECULAR BIOLOGY OF THE CELL, 2009, 20 (11) :2673-2683
[22]   Translationally Repressed mRNA Transiently Cycles through Stress Granules during Stress [J].
Mollet, Stephanie ;
Cougot, Nicolas ;
Wilczynska, Ania ;
Dautry, Francois ;
Kress, Michel ;
Bertrand, Edouard ;
Weil, Dominique .
MOLECULAR BIOLOGY OF THE CELL, 2008, 19 (10) :4469-4479
[23]   A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly [J].
Ohn, Takbum ;
Kedersha, Nancy ;
Hickman, Tyler ;
Tisdale, Sarah ;
Anderson, Paul .
NATURE CELL BIOLOGY, 2008, 10 (10) :1224-1231
[24]   P bodies and the control of mRNA translation and degradation [J].
Parker, Roy ;
Sheth, Ujwal .
MOLECULAR CELL, 2007, 25 (05) :635-646
[25]   Clotrimazole and bifonazole detach hexokinase from mitochondria of melanoma cells [J].
Penso, J ;
Beitner, R .
EUROPEAN JOURNAL OF PHARMACOLOGY, 1998, 342 (01) :113-117
[26]  
Rikhvanov E G, 2001, Mikrobiologiia, V70, P300
[27]   Sodium azide reduces the thermotolerance of respiratively grown yeasts [J].
Rikhvanov, EG ;
Varakina, NN ;
Rusaleva, TM ;
Rachenko, EI ;
Voinikov, VK .
CURRENT MICROBIOLOGY, 2002, 45 (06) :394-399
[28]   Synthetic genetic array analysis in Saccharomyces cerevisiae provides evidence for an interaction between RAT81DBP5 and genes encoding p-body components [J].
Scarcelli, John J. ;
Viggiano, Susan ;
Hodge, Christine A. ;
Heath, Catherine V. ;
Amberg, David C. ;
Cole, Charles N. .
GENETICS, 2008, 179 (04) :1945-1955
[29]   Identification of PatL1, a human homolog to yeast P body component Pat1 [J].
Scheller, Nicoletta ;
Resa-Infante, Patricia ;
de la Luna, Susana ;
Galao, Rui Pedro ;
Albrecht, Mario ;
Kaestner, Lars ;
Lipp, Peter ;
Lengauer, Thomas ;
Meyerhans, Andreas ;
Diez, Juana .
BIOCHIMICA ET BIOPHYSICA ACTA-MOLECULAR CELL RESEARCH, 2007, 1773 (12) :1786-1792