Principles and Properties of Stress Granules

Trends in Cell Biology

Volumn 26, Issue 9, 2016, Pages 668-679

  Protter, David S W ^a   Parker, Roy ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

intrinsically disordered protein; phase separation; RNP granule; stress granule

Indexed keywords

INTRINSICALLY DISORDERED PROTEIN; MESSENGER RNA; RIBONUCLEOPROTEIN;

CELL COMPARTMENTALIZATION; CELL GRANULE; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; HUMAN; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STRESS; ANIMAL; BIOLOGICAL MODEL; DISEASES; METABOLISM; PHYSIOLOGICAL STRESS;

ANIMALS; CYTOPLASMIC GRANULES; DISEASE; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MODELS, BIOLOGICAL; RIBONUCLEOPROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84991238633     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2016.05.004     Document Type: Review

References (86)

1. 1 Spector, D.L., SnapShot: cellular bodies. Cell 127 (2006), 1071.e1–1071.e2.
2. 2 Barbarese, E., et al. Conditional knockout of tumor overexpressed gene in mouse neurons affects RNA granule assembly, granule translation, LTP and short term habituation. PLoS ONE, 8, 2013, e69989.
3. 3 Brangwynne, C.P., et al. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324 (2009), 1729–1732.
4. 4 Anderson, P., Kedersha, N., RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 10 (2009), 430–436.
5. 5 Buchan, J.R., Parker, R., Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36 (2009), 932–941.
6. 6 Parker, R., Sheth, U., P bodies and the control of mRNA translation and degradation. Mol. Cell 25 (2007), 635–646.
7. 7 Jain, S., et al. ATPase-modulated stress granules contain a diverse proteome and substructure. Cell 164 (2016), 487–498.
8. 8 Aizer, A., et al. Quantifying mRNA targeting to P-bodies in living human cells reveals their dual role in mRNA decay and storage. J. Cell Sci. 127 (2014), 4443–4456.
9. 9 Buchan, J.R., et al. P bodies promote stress granule assembly in Saccharomyces cerevisiae. J. Cell Biol. 183 (2008), 441–455.
10. 10 Kedersha, N., et al. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169 (2005), 871–884.
11. 11 Bhattacharyya, S.N., et al. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125 (2006), 1111–1124.
12. 12 Brengues, M., et al. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310 (2005), 486–489.
13. 13 Buchan, J.R., et al. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 153 (2013), 1461–1474.
14. 14 Barbee, S.A., et al. Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52 (2006), 997–1009.
15. 15 Li, Y.R., et al. Stress granules as crucibles of ALS pathogenesis. J. Cell Biol. 201 (2013), 361–372.
16. 16 Ramaswami, M., et al. Altered ribostasis: RNA–protein granules in degenerative disorders. Cell 154 (2013), 727–736.
17. 17 Martin, K.C., Ephrussi, A., mRNA localization: gene expression in the spatial dimension. Cell 136 (2009), 719–730.
18. 18 Damgaard, C.K., Lykke-Andersen, J., Translational coregulation of 5’TOP mRNAs by TIA-1 and TIAR. Genes Dev. 25 (2011), 2057–2068.
19. 19 Buchan, J.R., mRNP granules: assembly, function, and connections with disease. RNA Biol. 11 (2014), 1019–1030.
20. 20 Cherkasov, V., et al. Systemic control of protein synthesis through sequestration of translation and ribosome biogenesis factors during severe heat stress. FEBS Lett. 589 (2015), 3654–3664.
21. 21 Wallace, E.W.J., et al. Reversible, specific, active aggregates of endogenous proteins assemble upon heat stress. Cell 162 (2015), 1286–1298.
22. 22 Souquere, S., et al. Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J. Cell Sci. 122 (2009), 3619–3626.
23. 23 Brangwynne, C.P., et al. Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. Proc. Natl. Acad. Sci.U.S.A. 108 (2011), 4334–4339.
24. 24 Sheth, U., et al. Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells. Development. 137 (2010), 1305–1314.
25. 25 Wang, J.T., et al. Regulation of RNA granule dynamics by phosphorylation of serine-rich, intrinsically disordered proteins in C. elegans. Elife., 3, 2015, e04591.
26. 26 Little, S.C., et al. Independent and coordinate trafficking of single Drosophila germ plasm mRNAs. Nat. Cell Biol. 17 (2015), 558–568.
27. 27 Gilks, N., et al. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 15 (2004), 5383–5398.
28. 28 Tourriere, H., The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160 (2003), 823–831.
29. 29 Solomon, S., et al. Distinct structural features of caprin-1 mediate its interaction with G3BP-1 and its induction of phosphorylation of eukaryotic translation initiation factor 2, entry to cytoplasmic stress granules, and selective interaction with a subset of mRNAs. Mol. Cell Biol. 27 (2007), 2324–2342.
30. 30 Kedersha, N., et al. G3BP–Caprin1–USP10 complexes mediate stress granule condensation and associate with 40S subunits. J. Cell Biol. 212 (2016), 845–860.
31. 31 Yang, X., et al. Stress granule-defective mutants deregulate stress responsive transcripts. PLoS Genet., 10, 2014, e1004763.
32. 32 Tsai, N.P., et al. Regulation of stress granule dynamics by Grb7 and FAK signalling pathway. EMBO J. 27 (2008), 715–726.
33. 33 Wippich, F., et al. Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell 152 (2013), 791–805.
34. 34 Nott, T.J., et al. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol. Cell 57 (2015), 936–947.
35. 35 Goulet, I., et al. TDRD3, a novel Tudor domain-containing protein, localizes to cytoplasmic stress granules. Hum. Mol. Genet. 17 (2008), 3055–3074.
36. 36 Ohn, T., et al. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell. Biol., 2008 [Internet]. 2008 Jan 1; Available from: http://www.nature.com/ncb/journal/v10/n10/abs/ncb1783.htmlhttp://www.nature.com/ncb/journal/v10/n10/abs/ncb1783.html.
37. 37 Kwon, S., et al. The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev. 21 (2007), 3381–3394.
38. 38 Leung, A.K.L., et al. Poly(ADP-Ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell. 42 (2011), 489–499.
39. 39 Lin, Y., et al. Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol. Cell 60 (2015), 208–219.
40. 40 Molliex, A., et al. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163 (2015), 123–133.
41. 41 Kroschwald, S., et al. Promiscuous interactions and protein disaggregases determine the material state of stress-inducible RNP granules. Elife, 4, 2015, e06807.
42. 42 Elbaum-Garfinkle, S., et al. The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), 7189–7194.
43. 43 Updike, D.L., et al. P granules extend the nuclear pore complex environment in the C. elegans germ line. J. Cell Biol. 192 (2011), 939–948.
44. 44 Decker, C.J., et al. Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J. Cell Biol. 179 (2007), 437–449.
45. 45 Kato, M., et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149 (2012), 753–767.
46. 46 Reijns, M.A.M., et al. A role for Q/N-rich aggregation-prone regions in P-body localization. J. Cell Sci. 121:Pt 15 (2008), 2463–2472.
47. 47 Hanazawa, M., et al. PGL proteins self associate and bind RNPs to mediate germ granule assembly in C. elegans. J. Cell Biol. 192 (2011), 929–937.
48. 48 Hennig, S., et al. Prion-like domains in RNA binding proteins are essential for building subnuclear paraspeckles. J. Cell Biol. 1210 (2015), 529–539.
49. 49 Jonas, S., Izaurralde, E., The role of disordered protein regions in the assembly of decapping complexes and RNP granules. Genes Dev. 27 (2013), 2628–2641.
50. 50 Guo, W., et al. An ALS-associated mutation affecting TDP-43 enhances protein aggregation, fibril formation and neurotoxicity. Nat. Struct. Mol. Biol. 18 (2011), 822–830.
51. 51 Patel, A., et al. A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell 162 (2015), 1066–1077.
52. 52 Zhang, H., et al. RNA controls PolyQ protein phase transitions. Mol. Cell 60 (2015), 220–230.
53. 53 Xiang, S., et al. The LC domain of hnRNPA2 Adopts similar conformations in hydrogel polymers, liquid-like droplets, and nuclei. Cell 163 (2015), 829–839.
54. 54 Cherkasov, V., et al. Coordination of translational control and protein homeostasis during severe heat stress. Curr. Biol. 23 (2013), 2452–2462.
55. 55 Chernov, K.G., et al. Role of microtubules in stress granule assembly: microtubule dynamical instability favors the formation of micrometric stress granules in cells. J. Biol. Chem. 284 (2009), 36569–36580.
56. 56 Loschi, M., et al. Dynein and kinesin regulate stress-granule and P-body dynamics. J. Cell Sci. 122 (2009), 3973–3982.
57. 57 Nadezhdina, E.S., et al. Microtubules govern stress granule mobility and dynamics. Biochim. Biophys. Acta BBA – Mol. Cell Res. 1803 (2010), 361–371.
58. 58 Hubstenberger, A., et al. Translation repressors, an RNA helicase, and developmental cues control RNP phase transitions during early development. Dev. Cell 27 (2013), 161–173.
59. 59 Hilliker, A., et al. The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F–mRNA complex. Mol. Cell 43 (2011), 962–972.
60. 60 Chalupnikova, K., et al. Recruitment of the RNA helicase RHAU to stress granules via a unique RNA-binding domain. J. Biol. Chem. 283 (2008), 35186–35198.
61. 61 Bell, S.D., Botchan, M.R., The minichromosome maintenance replicative helicase. Cold Spring Harb. Perspect. Biol., 5, 2013, a012807.
62. 62 Mu, X., et al. HIV-1 exploits the host factor RuvB-like 2 to balance viral protein expression. Cell Host Microbe 18 (2015), 233–242.
63. 63 Meyer, H., Weihl, C.C., The VCP/p97 system at a glance: connecting cellular function to disease pathogenesis. J. Cell Sci. 127 (2014), 3877–3883.
64. 64 Mazroui, R., et al. Inhibition of the ubiquitin–proteasome system induces stress granule formation. Mol. Biol. Cell 18 (2007), 2603–2618.
65. 65 Walters, R.W., et al. Differential effects of Ydj1 and Sis1 on Hsp70-mediated clearance of stress granules in Saccharomyces cerevisiae. RNA 21 (2015), 1660–1671.
66. 66 Vanderweyde, T., et al. Contrasting pathology of the stress granule proteins TIA-1 and G3BP in tauopathies. J. Neurosci. 32 (2012), 8270–8283.
67. 67 Onomoto, K., et al. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS ONE, 7, 2012, e43031.
68. 68 Reineke, L.C., Lloyd, R.E., The stress granule protein G3BP1 recruits protein kinase r to promote multiple innate immune antiviral responses. J. Virol. 89 (2015), 2575–2589.
69. 69 Reineke, L.C., et al. Stress granules regulate double-stranded RNA-dependent protein kinase activation through a complex containing G3BP1 and caprin1. MBio, 6, 2015, e02486.
70. 70 Reineke, L.C., Lloyd, R.E., Diversion of stress granules and P-bodies during viral infection. Virology 436 (2013), 255–267.
71. 71 Arimoto, K., et al. Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat. Cell Biol. 10 (2008), 1324–1332.
72. 72 Kim, W.J., et al. Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol. Cell Biol. 25 (2005), 2450–2462.
73. 73 Takahara, T., Maeda, T., Transient sequestration of TORC1 into stress granules during heat stress. Mol. Cell 47 (2012), 242–252.
74. 74 Thedieck, K., et al. Inhibition of mTORC1 by astrin and stress granules prevents apoptosis in cancer cells. Cell 154 (2013), 859–874.
75. 75 Klar, J., et al. Welander distal myopathy caused by an ancient founder mutation in TIA1 associated with perturbed splicing. Hum. Mutat. 34 (2013), 572–577.
76. 76 Johnson, J.O., et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68 (2010), 857–864.
77. 77 Kimonis, V.E., et al. Clinical studies in familial VCP myopathy associated with Paget disease of bone and frontotemporal dementia. Am. J. Med. Genet. A 146A (2008), 745–757.
78. 78 Cipolat Mis, M.S., et al. Autophagy in motor neuron disease: key pathogenetic mechanisms and therapeutic targets. Mol. Cell Neurosci. 72 (2016), 84–90.
79. 79 Li, S., et al. Genetic interaction of hnRNPA2B1 and DNAJB6 in a Drosophila model of multisystem proteinopathy. Hum. Mol. Genet. 25 (2016), 936–950.
80. 80 Freibaum, B.D., et al. GGGGCC repeat expansion in C9orf72 compromises nucleocytoplasmic transport. Nature 525 (2015), 129–133.
81. 81 Ling, S.-C., et al. Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron 79 (2013), 416–438.
82. 82 Zhang, K., et al. The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature 525 (2015), 56–61.
83. 83 Anderson, P., et al. Stress granules, P-bodies and cancer. Biochim. Biophys. Acta BBA – Gene Regul Mech. 1849 (2015), 861–870.
84. 84 Adjibade, P., et al. Sorafenib, a multikinase inhibitor, induces formation of stress granules in hepatocarcinoma cells. Oncotarget 6 (2015), 43927–43943.
85. 85 Kaehler, C., et al. 5-Fluorouracil affects assembly of stress granules based on RNA incorporation. Nucleic Acids Res. 42 (2014), 6436–6447.
86. 86 Somasekharan, S.P., et al. YB-1 regulates stress granule formation and tumor progression by translationally activating G3BP1. J. Cell Biol. 208 (2015), 913–929.