Picornavirus 2A protease regulates stress granule formation to facilitate viral translation

PLoS Pathogens

Volumn 14, Issue 2, 2018, Pages

  Yang, Xiaodan ^a   Hu, Zhulong ^a   Fan, Shanshan ^a   Zhang, Qiang ^a   Zhong, Yi ^a   Guo, Dong ^a   Qin, Yali ^a   Chen, Mingzhou ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENITE SODIUM; HEAT SHOCK PROTEIN; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4G; MESSENGER RNA; PICORNAVIRUS 2A PROTEASE; PROTEINASE; RENILLA LUCIFERIN 2 MONOOXYGENASE; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; CYSTEINE PROTEINASE; EIF4G1 PROTEIN, HUMAN; VIRAL PROTEIN;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA SEQUENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; GENOTYPE; HEAT SHOCK; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; NONHUMAN; PICORNAVIRUS INFECTION; PLASMID; POLIOMYELITIS VIRUS; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA; STRESS; STRESS GRANULE FORMATION; TRANSCRIPTION INITIATION; VIRUS RECOMBINANT; VIRUS TRANSCRIPTION; WESTERN BLOTTING; CELL GRANULE; ENZYMOLOGY; HEK293 CELL LINE; HELA CELL LINE; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PICORNAVIRIDAE; PROTEIN DEGRADATION; PROTEIN SYNTHESIS;

CYSTEINE ENDOPEPTIDASES; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-4G; HEK293 CELLS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; PICORNAVIRIDAE; PROTEIN BIOSYNTHESIS; PROTEOLYSIS; STRESS, PHYSIOLOGICAL; VIRAL PROTEINS;

EID: 85042712176     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006901     Document Type: Article

References (61)

1. White JP, Lloyd RE, (2012) Regulation of stress granules in virus systems. Trends Microbiol20: 175–183. doi: 10.1016/j.tim.2012.02.001 22405519
2. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, et al. (2003) The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol160: 823–831. doi: 10.1083/jcb.200212128 12642610
3. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, et al. (2004) Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell15: 5383–5398. doi: 10.1091/mbc.E04-08-0715 15371533
4. Neumann D, Lichtenberger O, Gunther D, Tschiersch K, Nover L, (1994) Heat-Shock Proteins Induce Heavy-Metal Tolerance in Higher-Plants. Planta194: 360–367.
5. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, et al. (2000) Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol151: 1257–1268. 11121440
6. McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, et al. (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 Chem280: 16925–16933. doi: 10.1074/jbc.M412882200 15684421
7. Murtha-Riel P, Davies MV, Scherer BJ, Choi SY, Hershey JW, et al. (1993) Expression of a phosphorylation-resistant eukaryotic initiation factor 2 alpha-subunit mitigates heat shock inhibition of protein synthesis. J Biol Chem268: 12946–12951. 8509427
8. Panas MD, Ivanov P, Anderson P, (2016) Mechanistic insights into mammalian stress granule dynamics. Journal of Cell Biology215: 313–323. doi: 10.1083/jcb.201609081 27821493
9. Dang Y, Kedersha N, Low WK, Romo D, Gorospe M, et al. (2006) Eukaryotic initiation factor 2alpha-independent pathway of stress granule induction by the natural product pateamine A. J Biol Chem281: 32870–32878. doi: 10.1074/jbc.M606149200 16951406
10. Mazroui R, Sukarieh R, Bordeleau ME, Kaufman RJ, Northcote P, et al. (2006) Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol Biol Cell17: 4212–4219. doi: 10.1091/mbc.E06-04-0318 16870703
11. Mokas S, Mills JR, Garreau C, Fournier MJ, Robert F, et al. (2009) Uncoupling stress granule assembly and translation initiation inhibition. Mol Biol Cell20: 2673–2683. doi: 10.1091/mbc.E08-10-1061 19369421
12. Emara MM, Fujimura K, Sciaranghella D, Ivanova V, Ivanov P, et al. (2012) Hydrogen peroxide induces stress granule formation independent of eIF2alpha phosphorylation. Biochem Biophys Res Commun423: 763–769. doi: 10.1016/j.bbrc.2012.06.033 22705549
13. Arrigo AP, Suhan JP, Welch WJ, (1988) Dynamic changes in the structure and intracellular locale of the mammalian low-molecular-weight heat shock protein. Mol Cell Biol8: 5059–5071. 3072471
14. Piotrowska J, Hansen SJ, Park N, Jamka K, Sarnow P, et al. (2010) Stable formation of compositionally unique stress granules in virus-infected cells. J Virol84: 3654–3665. doi: 10.1128/JVI.01320-09 20106928
15. Wong SS, Yip CC, Lau SK, Yuen KY, (2010) Human enterovirus 71 and hand, foot and mouth disease. Epidemiol Infect138: 1071–1089. doi: 10.1017/S0950268809991555 20056019
16. Racaniello V, David M., Knipe PMH, (2007) Picornaviridae: the viruses and their replication; Lippincott Williams and Wilkins.
17. Pelletier J, Sonenberg N, (1988) Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature334: 320–325. doi: 10.1038/334320a0 2839775
18. Rose JK, Trachsel H, Leong K, Baltimore D, (1978) Inhibition of translation by poliovirus: inactivation of a specific initiation factor. Proc Natl Acad Sci U S A75: 2732–2736. 208073
19. Tsai WC, Lloyd RE, (2014) Cytoplasmic RNA Granules and Viral Infection. Annu Rev Virol1: 147–170. doi: 10.1146/annurev-virology-031413-085505 26958719
20. Reineke LC, Lloyd RE, (2013) Diversion of stress granules and P-bodies during viral infection. Virology436: 255–267. doi: 10.1016/j.virol.2012.11.017 23290869
21. White JP, Cardenas AM, Marissen WE, Lloyd RE, (2007) Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe2: 295–305. doi: 10.1016/j.chom.2007.08.006 18005751
22. Wu S, Wang Y, Lin L, Si X, Wang T, et al. (2014) Protease 2A induces stress granule formation during coxsackievirus B3 and enterovirus 71 infections. Virol J11: 192. doi: 10.1186/s12985-014-0192-1 25410318
23. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, et al. (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. Journal of Cell Biology169: 871–884. doi: 10.1083/jcb.200502088 15967811
24. Mollet S, Cougot N, Wilczynska A, Dautry F, Kress M, et al. (2008) Translationally repressed mRNA transiently cycles through stress granules during stress. Mol Biol Cell19: 4469–4479. doi: 10.1091/mbc.E08-05-0499 18632980
25. Anderson P, Kedersha N, (2008) Stress granules: the Tao of RNA triage. Trends Biochem Sci33: 141–150. doi: 10.1016/j.tibs.2007.12.003 18291657
26. Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P, (2008) A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat Cell Biol10: 1224–1231. doi: 10.1038/ncb1783 18794846
27. Scheuner D, Song BB, McEwen E, Liu C, Laybutt R, et al. (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Molecular Cell7: 1165–1176. 11430820
28. Kedersha N, Chen S, Gilks N, Li W, Miller IJ, et al. (2002) Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol Biol Cell13: 195–210. doi: 10.1091/mbc.01-05-0221 11809833
29. 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 Biol147: 1431–1442. 10613902
30. Ansardi DC, Pal-Ghosh R, Porter D, Morrow CD, (1995) Encapsidation and serial passage of a poliovirus replicon which expresses an inactive 2A proteinase. J Virol69: 1359–1366. 7815522
31. Cai Q, Yameen M, Liu W, Gao Z, Li Y, et al. (2013) Conformational plasticity of the 2A proteinase from enterovirus 71. J Virol87: 7348–7356. doi: 10.1128/JVI.03541-12 23616646
32. Hsu YY, Liu YN, Lu WW, Kung SH, (2009) Visualizing and quantifying the differential cleavages of the eukaryotic translation initiation factors eIF4GI and eIF4GII in the enterovirus-infected cell. Biotechnol Bioeng104: 1142–1152. doi: 10.1002/bit.22495 19655339
33. Svitkin YV, Gradi A, Imataka H, Morino S, Sonenberg N, (1999) Eukaryotic initiation factor 4GII (eIF4GII), but not eIF4GI, cleavage correlates with inhibition of host cell protein synthesis after human rhinovirus infection. J Virol73: 3467–3472. 10074204
34. Coldwell MJ, Sack U, Cowan JL, Barrett RM, Vlasak M, et al. (2012) Multiple isoforms of the translation initiation factor eIF4GII are generated via use of alternative promoters, splice sites and a non-canonical initiation codon. Biochem J448: 1–11. doi: 10.1042/BJ20111765 22909319
35. Lamphear BJ, Rhoads RE, (1996) A single amino acid change in protein synthesis initiation factor 4G renders cap-dependent translation resistant to picornaviral 2A proteases. Biochemistry35: 15726–15733. doi: 10.1021/bi961864t 8961935
36. Kobayashi M, Arias C, Garabedian A, Palmenberg AC, Mohr I, (2012) Site-specific cleavage of the host poly(A) binding protein by the encephalomyocarditis virus 3C proteinase stimulates viral replication. J Virol86: 10686–10694. doi: 10.1128/JVI.00896-12 22837200
37. Kerekatte V, Keiper BD, Badorff C, Cai A, Knowlton KU, et al. (1999) Cleavage of Poly(A)-binding protein by coxsackievirus 2A protease in vitro and in vivo: another mechanism for host protein synthesis shutoff?J Virol73: 709–717. 9847377
38. Ng CS, Jogi M, Yoo JS, Onomoto K, Koike S, et al. (2013) Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J Virol87: 9511–9522. doi: 10.1128/JVI.03248-12 23785203
39. Tolskaya EA, Romanova LI, Kolesnikova MS, Gmyl AP, Gorbalenya AE, et al. (1994) Genetic studies on the poliovirus 2C protein, an NTPase. A plausible mechanism of guanidine effect on the 2C function and evidence for the importance of 2C oligomerization. J Mol Biol236: 1310–1323. 8126722
40. Baltera RF, Jr.Tershak DR, (1989) Guanidine-resistant mutants of poliovirus have distinct mutations in peptide 2C. J Virol63: 4441–4444. 2550675
41. White JP, Lloyd RE, (2011) Poliovirus unlinks TIA1 aggregation and mRNA stress granule formation. J Virol85: 12442–12454. doi: 10.1128/JVI.05888-11 21957303
42. Dabo S, Meurs EF, (2012) dsRNA-dependent protein kinase PKR and its role in stress, signaling and HCV infection. Viruses4: 2598–2635. doi: 10.3390/v4112598 23202496
43. Lopez de Silanes I, Galban S, Martindale JL, Yang X, Mazan-Mamczarz K, et al. (2005) Identification and functional outcome of mRNAs associated with RNA-binding protein TIA-1. Mol Cell Biol25: 9520–9531. doi: 10.1128/MCB.25.21.9520-9531.2005 16227602
44. Rivera CI, Lloyd RE, (2008) Modulation of enteroviral proteinase cleavage of poly(A)-binding protein (PABP) by conformation and PABP-associated factors. Virology375: 59–72. doi: 10.1016/j.virol.2008.02.002 18321554
45. Hyman AA, Weber CA, Julicher F, (2014) Liquid-liquid phase separation in biology. Annu Rev Cell Dev Biol30: 39–58. doi: 10.1146/annurev-cellbio-100913-013325 25288112
46. Molliex A, Temirov J, Lee J, Coughlin M, Kanagaraj AP, et al. (2015) Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell163: 123–133. doi: 10.1016/j.cell.2015.09.015 26406374
47. Wippich F, Bodenmiller B, Trajkovska MG, Wanka S, Aebersold R, et al. (2013) Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell152: 791–805. doi: 10.1016/j.cell.2013.01.033 23415227
48. Alvarez E, Castello A, Carrasco L, Izquierdo JM, (2013) Poliovirus 2A protease triggers a selective nucleo-cytoplasmic redistribution of splicing factors to regulate alternative pre-mRNA splicing. PLoS One8: e73723. doi: 10.1371/journal.pone.0073723 24066065
49. Fung G, Shi J, Deng H, Hou J, Wang C, et al. (2015) Cytoplasmic translocation, aggregation, and cleavage of TDP-43 by enteroviral proteases modulate viral pathogenesis. Cell Death Differ22: 2087–2097. doi: 10.1038/cdd.2015.58 25976304
50. Gustin KE, Sarnow P, (2001) Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J20: 240–249. doi: 10.1093/emboj/20.1.240 11226174
51. Zhang H, Cong H, Song L, Tien P, (2014) The nuclear protein Sam68 is redistributed to the cytoplasm and is involved in PI3K/Akt activation during EV71 infection. Virus Res180: 1–11. doi: 10.1016/j.virusres.2013.11.020 24316008
52. Zhao X, Lamphear BJ, Xiong D, Knowlton K, Rhoads RE, (2003) Protection of cap-dependent protein synthesis in vivo and in vitro with an eIF4G-1 variant highly resistant to cleavage by Coxsackievirus 2A protease. J Biol Chem278: 4449–4457. doi: 10.1074/jbc.M212393200 12475969
53. Reineke LC, Lloyd RE, (2015) The Stress Granule Protein G3BP1 Recruits Protein Kinase R To Promote Multiple Innate Immune Antiviral Responses. Journal of Virology89: 2575–2589. doi: 10.1128/JVI.02791-14 25520508
54. Leppek K, Das R, Barna M, (2017) Functional 5' UTR mRNA structures in eukaryotic translation regulation and how to find them. Nat Rev Mol Cell Biol.
55. Protter DS, Parker R, (2016) Principles and Properties of Stress Granules. Trends Cell Biol26: 668–679. doi: 10.1016/j.tcb.2016.05.004 27289443
56. Li YR, King OD, Shorter J, Gitler AD, (2013) Stress granules as crucibles of ALS pathogenesis. Journal of Cell Biology201: 361–372. doi: 10.1083/jcb.201302044 23629963
57. Ramaswami M, Taylor JP, Parker R, (2013) Altered Ribostasis: RNA-Protein Granules in Degenerative Disorders. Cell154: 727–736. doi: 10.1016/j.cell.2013.07.038 23953108
58. Stewart SA, Dykxhoorn DM, Palliser D, Mizuno H, Yu EY, et al. (2003) Lentivirus-delivered stable gene silencing by RNAi in primary cells. Rna-a Publication of the Rna Society9: 493–501.
59. Li XL, Mao CM, Ma SJ, Wang XQ, Sun Z, et al. (2009) Generation of neutralizing monoclonal antibodies against Enterovirus 71 using synthetic peptides. Biochemical and Biophysical Research Communications390: 1126–1128. doi: 10.1016/j.bbrc.2009.09.103 19799860
60. Lahaye X, Vidy A, Pomier C, Obiang L, Harper F, et al. (2009) Functional characterization of Negri bodies (NBs) in rabies virus-infected cells: Evidence that NBs are sites of viral transcription and replication. J Virol83: 7948–7958. doi: 10.1128/JVI.00554-09 19494013
61. Zamora M, Marissen WE, Lloyd RE, (2002) Multiple eIF4GI-specific protease activities present in uninfected and poliovirus-infected cells. Journal of Virology76: 165–177. doi: 10.1128/JVI.76.1.165-177.2002 11739682