Mechanistic insights into mammalian stress granule dynamics

Journal of Cell Biology

Volumn 215, Issue 3, 2016, Pages 313-323

  Panas, Marc D ^a   Ivanov, Pavel ^a   Anderson, Paul ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4A; INITIATION FACTOR 4E; INITIATION FACTOR 4F; INITIATION FACTOR 4G; INTRINSICALLY DISORDERED PROTEIN; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; RIBONUCLEOPROTEIN; RIBOSOME PROTEIN; RNA BINDING PROTEIN;

CELL STRESS; CELL SURVIVAL; CELLULAR STRESS RESPONSE; DEGENERATIVE DISEASE; ENVIRONMENTAL STRESS; HUMAN; LIQUID; MAMMAL; METABOLIC STRESS; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PHASE SEPARATION; PRION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; REVIEW; RIBOSOME; STRESS GRANULE; TRANSLATION INITIATION; ANIMAL; BIOLOGICAL MODEL; CELL GRANULE; METABOLISM; PHYSIOLOGICAL STRESS;

ANIMALS; CYTOPLASMIC GRANULES; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MAMMALS; MODELS, BIOLOGICAL; RIBOSOMAL PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84995977436     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201609081     Document Type: Review

References (115)

1. Anderson, P., and N. Kedersha. 2002. Stressful initiations. J. Cell Sci. 115:3227-3234.
2. Anderson, P., and N. Kedersha. 2006. RNA granules. J. Cell Biol. 172:803-808. http://dx.doi.org/10.1083/jcb.200512082
3. Anderson, P., and N. Kedersha. 2009. Stress granules. Curr. Biol. 19:R397-R398. http://dx.doi.org/10.1016/j.cub.2009.03.013
4. Anderson, P., N. Kedersha, and P. Ivanov. 2014. Stress granules, P-bodies and cancer. Biochim. Biophys. Acta. 1849:861-870. http://dx.doi.org/10.1016/j.bbagrm.2014.11.009
5. Banani, S.F., A.M. Rice, W.B. Peeples, Y. Lin, S. Jain, R. Parker, and M.K. Rosen. 2016. Compositional control of phase-separated cellular bodies. Cell. 166:651-663. http://dx.doi.org/10.1016/j.cell.2016.06.010
6. Bley, N., M. Lederer, B. Pfalz, C. Reinke, T. Fuchs, M. Glaβ, B. Möller, and S. Hüttelmaier. 2015. Stress granules are dispensable for mRNA stabilization during cellular stress. Nucleic Acids Res. 43:e26. http://dx.doi.org/10.1093/nar/gku1275
7. Bordeleau, M.E., R. Cencic, L. Lindqvist, M. Oberer, P. Northcote, G. Wagner, and J. Pelletier. 2006a. RNA-mediated sequestration of the RNA helicase eIF4A by Pateamine A inhibits translation initiation. Chem. Biol. 13:1287-1295. http://dx.doi.org/10.1016/j.chembiol.2006.10.005
8. Bordeleau, M.E., A. Mori, M. Oberer, L. Lindqvist, L.S. Chard, T. Higa, G.J. Belsham, G. Wagner, J. Tanaka, and J. Pelletier. 2006b. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat. Chem. Biol. 2:213-220. http://dx.doi.org/10.1038/nchembio776
9. Bordeleau, M.E., F. Robert, B. Gerard, L. Lindqvist, S.M. Chen, H.G. Wendel, B. Brem, H. Greger, S.W. Lowe, J.A. Porco Jr., and J. Pelletier. 2008. Therapeutic suppression of translation initiation modulates chemosensitivity in a mouse lymphoma model. J. Clin. Invest. 118:2651-2660. http://dx.doi.org/10.1172/JCI34753
10. Bounedjah, O., L. Hamon, P. Savarin, B. Desforges, P.A. Curmi, and D. Pastré. 2012. Macromolecular crowding regulates assembly of mRNA stress granules after osmotic stress: new role for compatible osmolytes. J. Biol. Chem. 287:2446-2458. http://dx.doi.org/10.1074/jbc.M111.292748
11. Brangwynne, C.P. 2013. Phase transitions and size scaling of membrane-less organelles. J. Cell Biol. 203:875-881. http://dx.doi.org/10.1083/jcb.201308087
12. Brangwynne, C.P., C.R. Eckmann, D.S. Courson, A. Rybarska, C. Hoege, J. Gharakhani, F. Jülicher, and A.A. Hyman. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science. 324:1729-1732. http://dx.doi.org/10.1126/science.1172046
13. Brangwynne, C.P., T.J. Mitchison, and A.A. Hyman. 2011. Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA. 108:4334-4339. http://dx.doi.org/10.1073/pnas.1017150108
14. Buchan, J.R. 2014. mRNP granules. Assembly, function, and connections with disease. RNA Biol. 11:1019-1030. http://dx.doi.org/10.4161/15476286.2014.972208
15. Buchan, J.R., and R. Parker. 2009. Eukaryotic stress granules: The ins and outs of translation. Mol. Cell. 36:932-941. http://dx.doi.org/10.1016/j.molcel.2009.11.020
16. Burke, K.A., A.M. Janke, C.L. Rhine, and N.L. Fawzi. 2015. Residue-by-residue view of in vitro FUS granules that bind the C-terminal domain of RNA polymerase II. Mol. Cell. 60:231-241. http://dx.doi.org/10.1016/j.molcel.2015.09.006
17. Cencic, R., M. Carrier, G. Galicia-Vázquez, M.E. Bordeleau, R. Sukarieh, A. Bourdeau, B. Brem, J.G. Teodoro, H. Greger, M.L. Tremblay, et al. 2009. Antitumor activity and mechanism of action of the cyclopenta[b] benzofuran, silvestrol. PLoS One. 4:e5223. http://dx.doi.org/10.1371/ journal.pone.0005223
18. Cencic, R., F. Robert, G. Galicia-Vázquez, A. Malina, K. Ravindar, R. Somaiah, P. Pierre, J. Tanaka, P. Deslongchamps, and J. Pelletier. 2013. Modifying chemotherapy response by targeted inhibition of eukaryotic initiation factor 4A. Blood Cancer J. 3:e128. http://dx.doi.org/10.1038/bcj.2013.25
19. Chernov, K.G., A. Barbet, L. Hamon, L.P. Ovchinnikov, P.A. Curmi, and D. Pastré. 2009. Role of microtubules in stress granule assembly: microtubule dynamical instability favors the formation of micrometric stress granules in cells. J. Biol. Chem. 284:36569-36580. http://dx.doi.org/10.1074/jbc.M109.042879
20. Cioce, M., and A.I. Lamond. 2005. Cajal bodies: A long history of discovery. Annu. Rev. Cell Dev. Biol. 21:105-131. http://dx.doi.org/10.1146/annurev.cellbio.20.010403.103738
21. Costa, M., A. Ochem, A. Staub, and A. Falaschi. 1999. Human DNA helicase VIII: a DNA and RNA helicase corresponding to the G3BP protein, an element of the ras transduction pathway. Nucleic Acids Res. 27:817-821. http://dx.doi.org/10.1093/nar/27.3.817
22. Damgaard, C.K., and J. Lykke-Andersen. 2011. Translational coregulation of 5'TOP mRNAs by TIA-1 and TIAR. Genes Dev. 25:2057-2068. http://dx.doi.org/10.1101/gad.17355911
23. Dang, Y., N. Kedersha, W.K. Low, D. Romo, M. Gorospe, R. Kaufman, P. Anderson, and J.O. Liu. 2006. Eukaryotic initiation factor 2alphaindependent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem. 281:32870-32878. http://dx.doi.org/10.1074/jbc.M606149200
24. Decker, M., S. Jaensch, A. Pozniakovsky, A. Zinke, K.F. O'Connell, W. Zachariae, E. Myers, and A.A. Hyman. 2011. Limiting amounts of centrosome material set centrosome size in C. elegans embryos. Curr. Biol. 21:1259-1267. http://dx.doi.org/10.1016/j.cub.2011.06.002
25. Doyle, S.M., O. Genest, and S. Wickner. 2013. Protein rescue from aggregates by powerful molecular chaperone machines. Nat. Rev. Mol. Cell Biol. 14:617-629. http://dx.doi.org/10.1038/nrm3660
26. Emara, M.M., P. Ivanov, T. Hickman, N. Dawra, S. Tisdale, N. Kedersha, G.F. Hu, and P. Anderson. 2010. Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. J. Biol. Chem. 285:10959-10968. http://dx.doi.org/10.1074/jbc.M109.077560
27. Emara, M.M., K. Fujimura, D. Sciaranghella, V. Ivanova, P. Ivanov, and P. Anderson. 2012. Hydrogen peroxide induces stress granule formation independent of eIF2a phosphorylation. Biochem. Biophys. Res. Commun. 423:763-769. http://dx.doi.org/10.1016/j.bbrc.2012.06.033
28. Fujimura, K., A.T. Sasaki, and P. Anderson. 2012. Selenite targets eIF4E-binding protein-1 to inhibit translation initiation and induce the assembly of nonDownloaded canonical stress granules. Nucleic Acids Res. 40:8099-8110. http://dx.doi.org/10.1093/nar/gks566
29. Ganassi, M., D. Mateju, I. Bigi, L. Mediani, I. Poser, H.O. Lee, S.J. Seguin, F.F. Morelli, J. Vinet, G. Leo, et al. 2016. A surveillance function of the HSPB8-BAG3-HSP70 chaperone complex ensures stress granule integrity and dynamism. Mol. Cell. 63:796-810. http://dx.doi.org/10.1016/j.molcel.2016.07.021
30. Gareau, C., D. Martel, L. Coudert, S. Mellaoui, and R. Mazroui. 2013. Characterization of fragile X mental retardation protein granules formation and dynamics in Drosophila. Biol. Open. 2:68-81. http://dx.doi.org/10.1242/bio.20123012
31. Gilks, N., N. Kedersha, M. Ayodele, L. Shen, G. Stoecklin, L.M. Dember, and P. Anderson. 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell. 15:5383-5398. http://dx.doi.org/10.1091/mbc.E04-08-0715
32. Goehring, N.W., and A.A. Hyman. 2012. Organelle growth control through limiting pools of cytoplasmic components. Curr. Biol. 22:R330-R339. http://dx.doi.org/10.1016/j.cub.2012.03.046
33. Hamill, D., J. Davis, J. Drawbridge, and K.A. Suprenant. 1994. Polyribosome targeting to microtubules: Enrichment of specific mRNAs in a reconstituted microtubule preparation from sea urchin embryos. J. Cell Biol. 127:973-984. http://dx.doi.org/10.1083/jcb.127.4.973
34. Han, T.W., M. Kato, S. Xie, L.C. Wu, H. Mirzaei, J. Pei, M. Chen, Y. Xie, J. Allen, G. Xiao, and S.L. McKnight. 2012. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell. 149:768-779. http://dx.doi.org/10.1016/j.cell.2012.04.016
35. Harding, H.P., Y. Zhang, A. Bertolotti, H. Zeng, and D. Ron. 2000. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell. 5:897-904. http://dx.doi.org/10.1016/S1097-2765(00)80330-5
36. Hernandez-Verdun, D. 2011. Assembly and disassembly of the nucleolus during the cell cycle. Nucleus. 2:189-194. http://dx.doi.org/10.4161/nucl.2.3.16246
37. Higgins, R., J.M. Gendron, L. Rising, R. Mak, K. Webb, S.E. Kaiser, N. Zuzow, P. Riviere, B. Yang, E. Fenech, et al. 2015. The unfolded protein response triggers site-specific regulatory ubiquitylation of 40S ribosomal proteins. Mol. Cell. 59:35-49. http://dx.doi.org/10.1016/j.molcel.2015.04.026
38. Hofmann, S., V. Cherkasova, P. Bankhead, B. Bukau, and G. Stoecklin. 2012. Translation suppression promotes stress granule formation and cell survival in response to cold shock. Mol. Biol. Cell. 23:3786-3800. http:// dx.doi.org/10.1091/mbc.E12-04-0296
39. Iakoucheva, L.M., P. Radivojac, C.J. Brown, T.R. O'Connor, J.G. Sikes, Z. Obradovic, and A.K. Dunker. 2004. The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 32:1037-1049. http://dx.doi.org/10.1093/nar/gkh253
40. Ivanov, P.A., E.M. Chudinova, and E.S. Nadezhdina. 2003. Disruption of microtubules inhibits cytoplasmic ribonucleoprotein stress granule formation. Exp. Cell Res. 290:227-233. http://dx.doi.org/10.1016/S0014-4827(03)00290-8
41. Ivanov, P., M.M. Emara, J. Villen, S.P. Gygi, and P. Anderson. 2011a. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell. 43:613-623. http://dx.doi.org/10.1016/j.molcel.2011.06.022
42. Ivanov, P., N. Kedersha, and P. Anderson. 2011b. Stress puts TIA on TOP. Genes Dev. 25:2119-2124. http://dx.doi.org/10.1101/gad.17838411
43. Jackson, R.J., C.U. Hellen, and T.V. Pestova. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11:113-127. http://dx.doi.org/10.1038/nrm2838
44. Jain, S., J.R. Wheeler, R.W. Walters, A. Agrawal, A. Barsic, and R. Parker. 2016. ATPase-modulated stress granules contain a diverse proteome and substructure. Cell. 164:487-498. http://dx.doi.org/10.1016/j.cell.2015.12.038
45. Kahvejian, A., Y.V. Svitkin, R. Sukarieh, M.N. M'Boutchou, and N. Sonenberg. 2005. Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev. 19:104-113. http://dx.doi.org/10.1101/gad.1262905
46. Kato, M., T.W. Han, S. Xie, K. Shi, X. Du, L.C. Wu, H. Mirzaei, E.J. Goldsmith, J. Longgood, J. Pei, et al. 2012. Cell-free formation of RNA granules: Low complexity sequence domains form dynamic fibers within hydrogels. Cell. 149:753-767. http://dx.doi.org/10.1016/j.cell.2012.04.017
47. Keating, C.D. 2012. Aqueous phase separation as a possible route to compartmentalization of biological molecules. Acc. Chem. Res. 45:2114-2124. http://dx.doi.org/10.1021/ar200294y
48. Kedersha, N., and P. Anderson. 2009. Regulation of translation by stress granules and processing bodies. Prog. Mol. Biol. Transl. Sci. 90:155-185. http://dx.doi.org/10.1016/S1877-1173(09)90004-7
49. Kedersha, N.L., M. Gupta, W. Li, I. Miller, and P. Anderson. 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. http://dx.doi.org/10.1083/jcb.147.7.1431
50. Kedersha, N., M.R. Cho, W. Li, P.W. Yacono, S. Chen, N. Gilks, D.E. Golan, and P. Anderson. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151:1257-1268. http://dx.doi.org/10.1083/jcb.151.6.1257
51. Kedersha, N., S. Chen, N. Gilks, W. Li, I.J. Miller, J. Stahl, and P. Anderson. 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. http://dx.doi.org/10.1091/ mbc.01-05-0221
52. Kedersha, N., G. Stoecklin, M. Ayodele, P. Yacono, J. Lykke-Andersen, M.J. Fritzler, D. Scheuner, R.J. Kaufman, D.E. Golan, and P. Anderson. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871-884. http://dx.doi.org/10.1083/jcb.200502088
53. Kedersha, N., P. Ivanov, and P. Anderson. 2013. Stress granules and cell signaling: More than just a passing phase? Trends Biochem. Sci. 38:494-506. http://dx.doi.org/10.1016/j.tibs.2013.07.004
54. Kedersha, N., M.D. Panas, C.A. Achorn, S. Lyons, S. Tisdale, T. Hickman, M. Thomas, J. Lieberman, G.M. McInerney, P. Ivanov, and P. Anderson. 2016. G3BP-Caprin1-USP10 complexes mediate stress granule condensation and associate with 40S subunits. J. Cell Biol. 212:845-860. http://dx.doi.org/10.1083/jcb.201508028
55. Khatter, H., A.G. Myasnikov, S.K. Natchiar, and B.P. Klaholz. 2015. Structure of the human 80S ribosome. Nature. 520:640-645. http://dx.doi.org/10.1038/nature14427
56. Kim, H.J., N.C. Kim, Y.D. Wang, E.A. Scarborough, J. Moore, Z. Diaz, K.S. MacLea, B. Freibaum, S. Li, A. Molliex, et al. 2013. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature. 495:467-473. http://dx.doi.org/10.1038/nature11922
57. Kim, W.J., J.H. Kim, and S.K. Jang. 2007. Anti-inflammatory lipid mediator 15d-PGJ2 inhibits translation through inactivation of eIF4A. EMBO J. 26:5020-5032. http://dx.doi.org/10.1038/sj.emboj.7601920
58. Kogure, T., A.D. Kinghorn, I. Yan, B. Bolon, D.M. Lucas, M.R. Grever, and T. Patel. 2013. Therapeutic potential of the translation inhibitor silvestrol in hepatocellular cancer. PLoS One. 8:e76136. http://dx.doi.org/10.1371/journal.pone.0076136
59. Kriwacki, R.W., L. Hengst, L. Tennant, S.I. Reed, and P.E. Wright. 1996. Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: Conformational disorder mediates binding diversity. Proc. Natl. Acad. Sci. USA. 93:11504-11509. http://dx.doi.org/10.1073/pnas.93.21.11504
60. Kroschwald, S., S. Maharana, D. Mateju, L. Malinovska, E. Nüske, I. Poser, D. Richter, and S. Alberti. 2015. Promiscuous interactions and protein disaggregases determine the material state of stress-inducible RNP granules. eLife. 4:e06807. http://dx.doi.org/10.7554/eLife.06807
61. Lee, C.F., C.P. Brangwynne, J. Gharakhani, A.A. Hyman, and F. Jülicher. 2013. Spatial organization of the cell cytoplasm by position-dependent phase separation. Phys. Rev. Lett. 111:088101. http://dx.doi.org/10.1103/ PhysRevLett.111.088101
62. Li, S., L.M. Iakoucheva, S.D. Mooney, and P. Radivojac. 2010. Loss of post-translational modification sites in disease. Pac. Symp. Biocomput. 2010:337-347.
63. Lin, Y., D.S. Protter, M.K. Rosen, and R. Parker. 2015. Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol. Cell. 60:208-219. http://dx.doi.org/10.1016/j.molcel.2015.08.018
64. Lloyd, R.E. 2013. Regulation of stress granules and P-bodies during RNA virus infection. Wiley Interdiscip. Rev. RNA. 4:317-331. http://dx.doi.org/10.1002/wrna.1162
65. Loschi, M., C.C. Leishman, N. Berardone, and G.L. Boccaccio. 2009. Dynein and kinesin regulate stress-granule and P-body dynamics. J. Cell Sci. 122:3973-3982. http://dx.doi.org/10.1242/jcs.051383
66. Lyons, S.M., C. Achorn, N.L. Kedersha, P.J. Anderson, and P. Ivanov. 2016. YB-1 regulates tiRNA-induced stress granule formation but not translational repression. Nucleic Acids Res. 44:6949-6960. http://dx.doi.org/10.1093/nar/gkw418
67. McEwen, E., N. Kedersha, B. Song, D. Scheuner, N. Gilks, A. Han, J.J. Chen, P. Anderson, and R.J. Kaufman. 2005. Heme-regulated inhibitor kinasemediated 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. http:// dx.doi.org/10.1074/jbc.M412882200
68. McInerney, G.M., N.L. Kedersha, R.J. Kaufman, P. Anderson, and P. Liljeström. 2005. Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell. 16:3753-3763. http://dx.doi.org/10.1091/mbc.E05-02-0124
69. Mendoza, R., I. Savin, K. Thornton, and P.W. Voorhees. 2004. Topological complexity and the dynamics of coarsening. Nat. Mater. 3:385-388. http://dx.doi.org/10.1038/nmat1138
70. Mitchell, S.F., S. Jain, M. She, and R. Parker. 2013. Global analysis of yeast mRNPs. Nat. Struct. Mol. Biol. 20:127-133. http://dx.doi.org/10.1038/ nsmb.2468
71. Mollet, S., N. Cougot, A. Wilczynska, F. Dautry, M. Kress, E. Bertrand, and D. Weil. 2008. Translationally repressed mRNA transiently cycles through stress granules during stress. Mol. Biol. Cell. 19:4469-4479. http://dx.doi.org/10.1091/mbc.E08-05-0499
72. Molliex, A., J. Temirov, J. Lee, M. Coughlin, A.P. Kanagaraj, H.J. Kim, T. Mittag, and J.P. Taylor. 2015. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell. 163:123-133. http://dx.doi.org/10.1016/j.cell.2015.09.015
73. Murakami, T., S. Qamar, J.Q. Lin, G.S. Schierle, E. Rees, A. Miyashita, A.R. Costa, R.B. Dodd, F.T. Chan, C.H. Michel, et al. 2015. ALS/FTD mutation-induced phase transition of FUS liquid droplets and reversible hydrogels into irreversible hydrogels impairs RNP granule function. Neuron. 88:678-690. http://dx.doi.org/10.1016/j.neuron.2015.10.030
74. Myasnikov, A.G., Z.A. Afonina, J.F. Ménétret, V.A. Shirokov, A.S. Spirin, and B.P. Klaholz. 2014. The molecular structure of the left-handed supramolecular helix of eukaryotic polyribosomes. Nat. Commun. 5:5294. http://dx.doi.org/10.1038/ncomms6294
75. Nott, T.J., E. Petsalaki, P. Farber, D. Jervis, E. Fussner, A. Plochowietz, T.D. Craggs, D.P. Bazett-Jones, T. Pawson, J.D. Forman-Kay, and A.J. Baldwin. 2015. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol. Cell. 57:936-947. http://dx.doi.org/10.1016/j.molcel.2015.01.013
76. Ohn, T., N. Kedersha, T. Hickman, S. Tisdale, and P. Anderson. 2008. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 10:1224-1231. http://dx.doi.org/10.1038/ncb1783
77. Panas, M.D., M. Varjak, A. Lulla, K.E. Eng, A. Merits, G.B. Karlsson Hedestam, and G.M. McInerney. 2012. Sequestration of G3BP coupled with efficient translation inhibits stress granules in Semliki Forest virus infection. Mol. Biol. Cell. 23:4701-4712. http://dx.doi.org/10.1091/mbc.E12-08-0619
78. Panas, M.D., T. Schulte, B. Thaa, T. Sandalova, N. Kedersha, A. Achour, and G.M. McInerney. 2015. Viral and cellular proteins containing FGDF motifs bind G3BP to block stress granule formation. PLoS Pathog. 11:e1004659. http://dx.doi.org/10.1371/journal.ppat.1004659
79. Patel, A., H.O. Lee, L. Jawerth, S. Maharana, M. Jahnel, M.Y. Hein, S. Stoynov, J. Mahamid, S. Saha, T.M. Franzmann, et al. 2015. A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell. 162:1066-1077. http://dx.doi.org/10.1016/j.cell.2015.07.047
80. Pejaver, V., W.L. Hsu, F. Xin, A.K. Dunker, V.N. Uversky, and P. Radivojac. 2014. The structural and functional signatures of proteins that undergo multiple events of post-translational modification. Protein Sci. 23:1077-1093. http://dx.doi.org/10.1002/pro.2494
81. Peng, Z., C.J. Oldfield, B. Xue, M.J. Mizianty, A.K. Dunker, L. Kurgan, and V.N. Uversky. 2014. A creature with a hundred waggly tails: Intrinsically disordered proteins in the ribosome. Cell. Mol. Life Sci. 71:1477-1504. http://dx.doi.org/10.1007/s00018-013-1446-6
82. Protter, D.S., and R. Parker. 2016. Principles and properties of stress granules. Trends Cell Biol. 26:668-679. http://dx.doi.org/10.1016/j.tcb.2016.05.004
83. Schulte, T., L. Liu, M.D. Panas, B. Thaa, N. Dickson, B. Götte, A. Achour, and G.M. McInerney. 2016. Combined structural, biochemical and cellular evidence demonstrates that both FGDF motifs in alphavirus nsP3 are required for efficient replication. Open Biol. 6:6. http://dx.doi.org/10.1098/rsob.160078
84. Shenton, D., J.B. Smirnova, J.N. Selley, K. Carroll, S.J. Hubbard, G.D. Pavitt, M.P. Ashe, and C.M. Grant. 2006. Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. J. Biol. Chem. 281:29011-29021. http://dx.doi.org/10.1074/jbc.M601545200
85. Singh, G.P., M. Ganapathi, and D. Dash. 2007. Role of intrinsic disorder in transient interactions of hub proteins. Proteins. 66:761-765. http://dx.doi.org/10.1002/prot.21281
86. Sonenberg, N., and A.G. Hinnebusch. 2009. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell. 136:731-745. http://dx.doi.org/10.1016/j.cell.2009.01.042
87. Souquere, S., S. Mollet, M. Kress, F. Dautry, G. Pierron, and D. Weil. 2009. Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J. Cell Sci. 122:3619-3626. http://dx.doi.org/10.1242/jcs.054437
88. Srivastava, S.P., K.U. Kumar, and R.J. Kaufman. 1998. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 273:2416-2423. http://dx.doi.org/10.1074/jbc.273.4.2416
89. Stoecklin, G., T. Stubbs, N. Kedersha, S. Wax, W.F. Rigby, T.K. Blackwell, and P. Anderson. 2004. MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J. 23:1313-1324. http://dx.doi.org/10.1038/sj.emboj.7600163
90. Suprenant, K.A., L.B. Tempero, and L.E. Hammer. 1989. Association of ribosomes with in vitro assembled microtubules. Cell Motil. Cytoskeleton. 14:401-415. http://dx.doi.org/10.1002/cm.970140310
91. Szaflarski, W., M.M. Fay, N. Kedersha, M. Zabel, P. Anderson, and P. Ivanov. 2016. Vinca alkaloid drugs promote stress-induced translational repression and stress granule formation. Oncotarget. 7:30307-30322. http://dx.doi.org/10.18632/oncotarget.8728
92. Tarun, S.Z. Jr., and A.B. Sachs. 1995. A common function for mRNA 5' and 3' ends in translation initiation in yeast. Genes Dev. 9:2997-3007. http://dx.doi.org/10.1101/gad.9.23.2997
93. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27:527-533. http://dx.doi.org/10.1016/S0968-0004(02)02169-2
94. Tompa, P. 2005. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 579:3346-3354. http://dx.doi.org/10.1016/j.febslet.2005.03.072
95. Tourriàre, H., K. Chebli, L. Zekri, B. Courselaud, J.M. Blanchard, E. Bertrand, and J. Tazi. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160:823-831. http://dx.doi.org/10.1083/jcb.200212128
96. Tsai, W.C., S. Gayatri, L.C. Reineke, G. Sbardella, M.T. Bedford, and R.E. Lloyd. 2016. Arginine demethylation of G3BP1 promotes stress granule assembly. J. Biol. Chem. http://dx.doi.org/10.1074/jbc.M116.739573
97. Tsumuraya, T., C. Ishikawa, Y. Machijima, S. Nakachi, M. Senba, J. Tanaka, and N. Mori. 2011. Effects of hippuristanol, an inhibitor of eIF4A, on adult T-cell leukemia. Biochem. Pharmacol. 81:713-722. http://dx.doi.org/10.1016/j.bcp.2010.12.025
98. Tyedmers, J., A. Mogk, and B. Bukau. 2010. Cellular strategies for controlling protein aggregation. Nat. Rev. Mol. Cell Biol. 11:777-788. http://dx.doi.org/10.1038/nrm2993
99. Uversky, V.N. 2003. A protein-chameleon: Conformational plasticity of alphasynuclein, a disordered protein involved in neurodegenerative disorders. J. Biomol. Struct. Dyn. 21:211-234. http://dx.doi.org/10.1080/07391102.2003.10506918
100. Uversky, V.N. 2013. Unusual biophysics of intrinsically disordered proteins. Biochim. Biophys. Acta. 1834:932-951. http://dx.doi.org/10.1016/j.bbapap.2012.12.008
101. Uversky, V.N. 2014. Introduction to intrinsically disordered proteins (IDPs). Chem. Rev. 114:6557-6560. http://dx.doi.org/10.1021/cr500288y
102. Uversky, V.N., and A.K. Dunker. 2010. Understanding protein non-folding. Biochim. Biophys. Acta. 1804:1231-1264. http://dx.doi.org/10.1016/j.bbapap.2010.01.017
103. Vanderweyde, T., K. Youmans, L. Liu-Yesucevitz, and B. Wolozin. 2013. Role of stress granules and RNA-binding proteins in neurodegeneration: A minireview. Gerontology. 59:524-533. http://dx.doi.org/10.1159/000354170
104. Vognsen, T., and O. Kristensen. 2012. Crystal structure of the Rasputin NTF2-like domain from Drosophila melanogaster. Biochem. Biophys. Res. Commun. 420:188-192. http://dx.doi.org/10.1016/j.bbrc.2012.02.140
105. Ward, J.J., J.S. Sodhi, L.J. McGuffin, B.F. Buxton, and D.T. Jones. 2004. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337:635-645. http://dx.doi.org/10.1016/j.jmb.2004.02.002
106. Weber, S.C., and C.P. Brangwynne. 2012. Getting RNA and protein in phase. Cell. 149:1188-1191. http://dx.doi.org/10.1016/j.cell.2012.05.022
107. Wek, S.A., S. Zhu, and R.C. Wek. 1995. The histidyl-tRNA synthetase-related sequence in the eIF-2 alpha protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15:4497-4506. http://dx.doi.org/10.1128/MCB.15.8.4497
108. White, J.P., and R.E. Lloyd. 2012. Regulation of stress granules in virus systems. Trends Microbiol. 20:175-183. http://dx.doi.org/10.1016/j.tim.2012.02.001
109. White, J.P., A.M. Cardenas, W.E. Marissen, and R.E. Lloyd. 2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe. 2:295-305. http://dx.doi.org/10.1016/j.chom.2007.08.006
110. Wippich, F., B. Bodenmiller, M.G. Trajkovska, S. Wanka, R. Aebersold, and L. Pelkmans. 2013. Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell. 152:791-805. http://dx.doi.org/10.1016/j.cell.2013.01.033
111. Wolozin, B. 2012. Regulated protein aggregation: Stress granules and neurodegeneration. Mol. Neurodegener. 7:56. http://dx.doi.org/10.1186/1750-1326-7-56
112. Wolozin, B. 2014. Physiological protein aggregation run amuck: Stress granules and the genesis of neurodegenerative disease. Discov. Med. 17:47-52.
113. Wright, P.E., and H.J. Dyson. 1999. Intrinsically unstructured proteins: Reassessing the protein structure-function paradigm. J. Mol. Biol. 293:321-331. http://dx.doi.org/10.1006/jmbi.1999.3110
114. Yang, Z.R., R. Thomson, P. McNeil, and R.M. Esnouf. 2005. RONN: The bio-basis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics. 21:3369-3376. http://dx.doi.org/10.1093/bioinformatics/bti534
115. Zhang, J., K. Okabe, T. Tani, and T. Funatsu. 2011. Dynamic associationdissociation and harboring of endogenous mRNAs in stress granules. J. Cell Sci. 124:4087-4095. http://dx.doi.org/10.1242/jcs.090951