Translation suppression promotes stress granule formation and cell survival in response to cold shock

Molecular Biology of the Cell

Volumn 23, Issue 19, 2012, Pages 3786-3800

  Hofmann, Sarah ^a   Cherkasova, Valeria ^a   Bankhead, Peter ^a   Bukau, Bernd ^a   Stoecklin, Georg ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INITIATION FACTOR 2ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOTRANSFERASE; PROTEIN KINASE RNA LIKE ENDOPLASMIC RETICULUM KINASE; PROTEIN SERINE THREONINE KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ENERGY; CELL FUNCTION; CELL GROWTH; CELL STRESS; CELL SURVIVAL; COLD SHOCK RESPONSE; ENZYME ACTIVATION; ENZYME INHIBITION; HYPOTHERMIA; INTRACELLULAR SIGNALING; MAMMAL; MAMMAL CELL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; TEMPERATURE; YEAST;

ADENYLATE KINASE; ANIMALS; CELL LINE; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; COLD-SHOCK RESPONSE; CYTOPLASMIC GRANULES; ENERGY METABOLISM; ENZYME ACTIVATION; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-3; HUMANS; KINETICS; MICE; PHOSPHORYLATION; POLY(A)-BINDING PROTEINS; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TOR SERINE-THREONINE KINASES;

EUKARYOTA; MAMMALIA;

EID: 84867186265     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-04-0296     Document Type: Article

References (43)

1. Anderson P, Kedersha N (2008). Stress granules: the Tao of RNA triage. Trends Biochem Sci 33, 141-150.
2. Arimoto K, Fukuda H, Imajoh-Ohmi S, Saito H, Takekawa M (2008). Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat Cell Biol 10, 1324-1332.
3. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P (2007). The selectivity of protein kinase inhibitors: a further update. Biochem J 408, 297-315.
4. Bouma HR, Ketelaar ME, Yard BA, Ploeg RJ, Henning RH (2010). AMP-activated protein kinase as a target for preconditioning in transplantation medicine. Transplantation 90, 353-358.
5. Buchan JR, Muhlrad D, Parker R (2008). P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183, 441-455.
6. Buttgereit F, Brand MD (1995). A hierarchy of ATP-consuming processes in mammalian cells. Biochem J 312, 163-167.
7. Carey HV, Andrews MT, Martin SL (2003). Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83, 1153-1181. (Pubitemid 37222270)
8. Castelli LM et al. (2011). Glucose depletion inhibits translation initiation via eIF4A loss and subsequent 48S preinitiation complex accumulation, while the pentose phosphate pathway is coordinately up-regulated. Mol Biol Cell 22, 3379-3393.
9. Choo AY, Kim SG, Vander Heiden MG, Mahoney SJ, Vu H, Yoon SO, Cantley LC, Blenis J (2010). Glucose addiction of TSC null cells is caused by failed mTORC1-dependent balancing of metabolic demand with supply. Mol Cell 38, 487-499.
10. Dowling RJ et al. (2010). mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328, 1172-1176.
11. Finger A, Knop M, Wolf DH (1993). Analysis of two mutated vacuolar proteins reveals a degradation pathway in the endoplasmic reticulum or a related compartment of yeast. Eur J Biochem 218, 565-574. (Pubitemid 24003774)
12. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P (2004). Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15, 5383-5398. (Pubitemid 39564732)
13. Grousl T et al. (2009). Robust heat shock induces eIF2alpha- phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae. J Cell Sci 122, 2078-2088.
14. Hardie DG (2007). AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8, 774-785.
15. Harding HP, Zhang Y, Ron D (1999). Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274. (Pubitemid 29051178)
16. Harding HP et al. (2003). An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11, 619-633. (Pubitemid 36385118)
17. Heus R, Daanen HA, Havenith G (1995). Physiological criteria for functioning of hands in the cold: a review. Appl Ergon 26, 5-13.
18. Holcik M, Sonenberg N (2005). Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6, 318-327. (Pubitemid 40516898)
19. Holz MK, Ballif BA, Gygi SP, Blenis J (2005). mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123, 569-580. (Pubitemid 41608461)
20. Homma T, Iwahashi H, Komatsu Y (2003). Yeast gene expression during growth at low temperature. Cryobiology 46, 230-237. (Pubitemid 36724564)
21. Horman S, Browne G, Krause U, Patel J, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud C, Rider M (2002). Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12, 1419-1423. (Pubitemid 34915545)
22. Horman S, Hussain N, Dilworth SM, Storey KB, Rider MH (2005). Evaluation of the role of AMP-activated protein kinase and its downstream targets in mammalian hibernation. Comp Biochem Physiol B Biochem Mol Biol 142, 374-382. (Pubitemid 41643001)
23. Hoyle NP, Castelli LM, Campbell SG, Holmes LE, Ashe MP (2007). Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J Cell Biol 179, 65-74. (Pubitemid 47606684)
24. Janke C et al. (2004). A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962. (Pubitemid 39206863)
25. Kedersha N, Chen S, Gilks N, Li W, Miller IJ, Stahl J, Anderson P (2002). Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol Biol Cell 13, 195-210. (Pubitemid 34106069)
26. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, Gilks N, Golan DE, Anderson P (2000). Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol 151, 1257-1268.
27. Kedersha NL, Gupta M, Li W, Miller I, Anderson P (1999). RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 147, 1431-1442.
28. Kim WJ, Back SH, Kim V, Ryu I, Jang SK (2005). Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol Cell Biol 25, 2450-2462. (Pubitemid 40354638)
29. Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, Sonenberg N, Koromilas A, Wouters BG (2002). Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 22, 7405-7416.
30. Laderoute KR, Amin K, Calaoagan JM, Knapp M, Le T, Orduna J, Foretz M, Viollet B (2006). 5′-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol Cell Biol 26, 5336-5347. (Pubitemid 44036203)
31. McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, Han A, Chen JJ, Anderson P, Kaufman RJ (2005). Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J Biol Chem 280, 16925-16933. (Pubitemid 41389152)
32. Murata Y et al. (2006). Genome-wide expression analysis of yeast response during exposure to 4 degrees C. Extremophiles 10, 117-128.
33. Richter JD, Sonenberg N (2005). Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433, 477-480. (Pubitemid 40204297)
34. Roobol A, Carden MJ, Newsam RJ, Smales CM (2009). Biochemical insights into the mechanisms central to the response of mammalian cells to cold stress and subsequent rewarming. FEBS J 276, 286-302.
35. Ruggieri A et al. (2012). Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 12, 71-85.
36. Saraste J, Palade GE, Farquhar MG (1986). Temperature-sensitive steps in the transport of secretory proteins through the Golgi complex in exocrine pancreatic cells. Proc Natl Acad Sci USA 83, 6425-6429. (Pubitemid 17174747)
37. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ (2001). Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7, 1165-1176. (Pubitemid 32607351)
38. Schiestl RH, Gietz RD (1989). High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet 16, 339-346. (Pubitemid 20034019)
39. Schwab MH, Druffel-Augustin S, Gass P, Jung M, Klugmann M, Bartholomae A, Rossner MJ, Nave KA (1998). Neuronal basic helix-loop-helix proteins (NEX, neuroD, NDRF): spatiotemporal expression and targeted disruption of the NEX gene in transgenic mice. J Neurosci 18, 1408-1418. (Pubitemid 28082426)
40. Takahara T, Maeda T (2012). Transient sequestration of TORC1 into stress granules during heat stress. Mol Cell 47, 242-252.
41. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J (2003). The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160, 823-831. (Pubitemid 36350838)
42. Wullschleger S, Loewith R, Hall MN (2006). TOR signaling in growth and metabolism. Cell 124, 471-484. (Pubitemid 43199434)
43. Zhou G et al. (2001). Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108, 1167-1174. (Pubitemid 32995375)