Mammalian RNA Granules

  • Jayabalan, Aravinth Kumar (Department of Cellular and Molecular Medicine, College of Medicine, Chosun University) ;
  • Ohn, Takbum (Department of Cellular and Molecular Medicine, College of Medicine, Chosun University)
  • Received : 2014.02.20
  • Accepted : 2014.03.13
  • Published : 2014.03.31

Abstract

RNA granules such as Stress Granules (SG) and P-Bodies (PB) are aggregates of translationally stalled messenger ribonucleoprotein (mRNP) complexes induced by a wide range of stresses. Over the past decade, extensive studies described key components of RNA granules, their molecular interactions and signaling pathways require for their assembly and disassembly. However, researches defining their exact roles under stress conditions have not been performed so far, although several studies suggested their roles in neurodegenerative diseases recently. In this review, we provide an introduction about their basic properties, key components, and the dynamic nature for their assembly.

Keywords

References

  1. Anderson P, Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem Sci. 2008. 33: 141-150. https://doi.org/10.1016/j.tibs.2007.12.003
  2. Anderson P, Kedersha N. Stress granules. Curr Biol. 2009. 19: R397-398. https://doi.org/10.1016/j.cub.2009.03.013
  3. Arimoto K, Fukuda H, Imajoh-Ohmi S, Saito H,Takekawa M. Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat Cell Biol. 2008. 10: 1324-1332. https://doi.org/10.1038/ncb1791
  4. Buchan JR, Kolaitis RM, Taylor JP, Parker R. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell. 2013. 153: 1461-1474. https://doi.org/10.1016/j.cell.2013.05.037
  5. Buchan JR, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell. 2009. 36: 932-941. https://doi.org/10.1016/j.molcel.2009.11.020
  6. Calkhoven CF, Muller C, Leutz A. Translational control of gene expression and disease. Trends Mol Med. 2002. 8: 577-583. https://doi.org/10.1016/S1471-4914(02)02424-3
  7. de Nadal E, Ammerer G, Posas F. Controlling gene expression in response to stress. Nat Rev Genet. 2011. 12: 833-845.
  8. Dolzhanskaya N, Merz G, Aletta JM, Denman RB. Methylation regulates the intracellular protein-protein and protein-RNA interactions of FMRP. J Cell Sci. 2006. 119: 1933-1946. https://doi.org/10.1242/jcs.02882
  9. Emara MM, Fujimura K, Sciaranghella D, Ivanova V, Ivanov P, Anderson P. Hydrogen peroxide induces stress granule formation independent of eIF2alpha phosphorylation. Biochem Biophys Res Commun. 2012. 423: 763-769. https://doi.org/10.1016/j.bbrc.2012.06.033
  10. Fujimura K, Sasaki AT, Anderson P. Selenite targets eIF4E-binding protein-1 to inhibit translation initiation and induce the assembly of non-canonical stress granules. Nucleic Acids Res. 2012. 40: 8099-8110. https://doi.org/10.1093/nar/gks566
  11. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell. 2004. 15: 5383-5398. https://doi.org/10.1091/mbc.E04-08-0715
  12. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell. 2000a. 6: 1099-1108. https://doi.org/10.1016/S1097-2765(00)00108-8
  13. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell. 2000b. 5: 897-904. https://doi.org/10.1016/S1097-2765(00)80330-5
  14. Hilliker A, Parker R. Stressed out? Make some modifications! Nat Cell Biol. 2008. 10: 1129-1130. https://doi.org/10.1038/ncb1008-1129
  15. Hofmann S, Cherkasova V, Bankhead P, Bukau B, Stoecklin G. Translation suppression promotes stress granule formation and cell survival in response to cold shock. Mol Biol Cell. 2012. 23: 3786-3800. https://doi.org/10.1091/mbc.E12-04-0296
  16. Holcik M, Sonenberg N. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol. 2005. 6: 318-327. https://doi.org/10.1038/nrm1618
  17. Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol. 2010. 11: 113-127. https://doi.org/10.1038/nrm2838
  18. Kedersha N, Anderson P. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem Soc Trans. 2002. 30: 963-969. https://doi.org/10.1042/bst0300963
  19. Kedersha N, Anderson P. Mammalian stress granules and processing bodies. Methods Enzymol. 2007. 431: 61-81. https://doi.org/10.1016/S0076-6879(07)31005-7
  20. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, Gilks N, Golan DE, Anderson P. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol. 2000. 151: 1257-1268. https://doi.org/10.1083/jcb.151.6.1257
  21. Kedersha N, Ivanov P, Anderson P. Stress granules and cell signaling: more than just a passing phase? Trends Biochem Sci. 2013. 38: 494-506. https://doi.org/10.1016/j.tibs.2013.07.004
  22. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, Scheuner D, Kaufman RJ, Golan DE, Anderson P. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol. 2005. 169: 871-884. https://doi.org/10.1083/jcb.200502088
  23. Kedersha NL, Gupta M, Li W, Miller I, Anderson P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol. 1999. 147: 1431-1442. https://doi.org/10.1083/jcb.147.7.1431
  24. Kim WJ, Back SH, Kim V, Ryu I, Jang SK. Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol Cell Biol. 2005. 25: 2450-2462. https://doi.org/10.1128/MCB.25.6.2450-2462.2005
  25. Kwon S, Zhang Y, Matthias P. The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev. 2007. 21: 3381-3394. https://doi.org/10.1101/gad.461107
  26. Li CH, Ohn T, Ivanov P, Tisdale S, Anderson P. eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PloS One. 2010. 5: e9942. https://doi.org/10.1371/journal.pone.0009942
  27. McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, Han A, Chen JJ, Anderson P, Kaufman RJ. 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. 2005. 280: 16925-16933. https://doi.org/10.1074/jbc.M412882200
  28. Mollet S, Cougot N, Wilczynska A, Dautry F, Kress M, Bertrand E, Weil D. Translationally repressed mRNA transiently cycles through stress granules during stress. Mol Biol Cell. 2008. 19: 4469-4479. https://doi.org/10.1091/mbc.E08-05-0499
  29. Ohn T, Anderson P. The role of posttranslational modifications in the assembly of stress granules. Wiley Interdiscip Rev RNA. 2010. 1: 486-493. https://doi.org/10.1002/wrna.23
  30. Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat Cell Biol. 2008. 10: 1224-1231. https://doi.org/10.1038/ncb1783
  31. Parker F, Maurier F, Delumeau I, Duchesne M, Faucher D, Debussche L, Dugue A, Schweighoffer F, Tocque B. A Ras- GTPase-activating protein SH3-domain-binding protein. Mol Cell Biol. 1996. 16: 2561-2569. https://doi.org/10.1128/MCB.16.6.2561
  32. Ramaswami M, Taylor JP,Parker R. Altered ribostasis: RNAprotein granules in degenerative disorders. Cell. 2013. 154: 727-736. https://doi.org/10.1016/j.cell.2013.07.038
  33. Reineke LC, Dougherty JD, Pierre P, Lloyd RE. Large G3BPinduced granules trigger eIF2alpha phosphorylation. Mol Biol Cell. 2012. 23: 3499-3510. https://doi.org/10.1091/mbc.E12-05-0385
  34. Richter JD, Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature. 2005. 433: 477-480. https://doi.org/10.1038/nature03205
  35. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol. 2004. 5: 897-907. https://doi.org/10.1038/nrm1496
  36. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell. 2009. 136: 731-745. https://doi.org/10.1016/j.cell.2009.01.042
  37. Spriggs KA, Bushell M, Willis AE. Translational regulation of gene expression during conditions of cell stress. Mol Cell. 2010. 40: 228-237. https://doi.org/10.1016/j.molcel.2010.09.028
  38. Srivastava SP, Kumar KU, Kaufman RJ. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNAdependent protein kinase. J Biol Chem. 1998. 273: 2416-2423. https://doi.org/10.1074/jbc.273.4.2416
  39. Stoecklin G, Kedersha N. Relationship of GW/P-bodies with stress granules. Adv Exp Med Biol. 2013. 768: 197-211. https://doi.org/10.1007/978-1-4614-5107-5_12
  40. Stoecklin G, Stubbs T, Kedersha N, Wax S, Rigby WF, Blackwell TK, Anderson P. MK2-induced tristetraprolin: 14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J. 2004. 23: 1313-1324. https://doi.org/10.1038/sj.emboj.7600163
  41. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol. 2003. 160: 823-831. https://doi.org/10.1083/jcb.200212128
  42. Wek RC, Jiang HY,Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans. 2006. 34: 7-11. https://doi.org/10.1042/BST0340007
  43. Wippich F, Bodenmiller B, Trajkovska MG, Wanka S, Aebersold R, Pelkmans L. Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell. 2013. 152: 791-805. https://doi.org/10.1016/j.cell.2013.01.033