Inhibition of stress granule formation by middle east respiratory syndrome coronavirus 4a accessory protein facilitates viral translation, leading to efficient virus replication

Journal of Virology

Volumn 92, Issue 20, 2018, Pages

  Nakagawa, Keisuke ^a   Narayanan, Krishna ^a   Wada, Masami ^a   Makino, Shinji ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Accessory protein; MERS coronavirus; Stress granules

Indexed keywords

DOUBLE STRANDED RNA; INITIATION FACTOR 2ALPHA; PROTEIN KINASE R; SMALL INTERFERING RNA; VIRAL PROTEIN; VIRUS MESSENGER RNA; VIRUS RNA;

4A GENE; ARTICLE; CELL GRANULE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME INHIBITION; GENE DELETION; HELA CELL LINE; HUMAN; HUMAN CELL; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STRESS GRANULE; STRESS GRANULE FORMATION; VERO CELL LINE; VIRUS GENE; VIRUS REPLICATION; VIRUS TRANSCRIPTION; ANIMAL; CHLOROCEBUS AETHIOPS; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS;

ANIMALS; CERCOPITHECUS AETHIOPS; GENE DELETION; HELA CELLS; HUMANS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; PROTEIN BIOSYNTHESIS; VERO CELLS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS REPLICATION;

EID: 85054767678     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00902-18     Document Type: Article

References (65)

1. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367:1814-1820. https://doi.org/10.1056/ NEJMoa1211721.
2. Alagaili AN, Briese T, Mishra N, Kapoor V, Sameroff SC, Burbelo PD, de Wit E, Munster VJ, Hensley LE, Zalmout IS, Kapoor A, Epstein JH, Karesh WB, Daszak P, Mohammed OB, Lipkin WI. 2014. Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. mBio 5:e00884-14. https://doi.org/10.1128/mBio.00884-14.
3. Wernery U, Lau SK, Woo PC. 2017. Middle East respiratory syndrome (MERS) coronavirus and dromedaries. Vet J 220:75-79. https://doi.org/ 10.1016/j.tvjl.2016.12.020.
4. Chu DK, Poon LL, Gomaa MM, Shehata MM, Perera RA, Abu Zeid D, El Rifay AS, Siu LY, Guan Y, Webby RJ, Ali MA, Peiris M, Kayali G. 2014. MERS coronaviruses in dromedary camels, Egypt. Emerg Infect Dis 20: 1049-1053. https://doi.org/10.3201/eid2006.140299.
5. Drosten C, Kellam P, Memish ZA. 2014. Evidence for camel-to-human transmission of MERS coronavirus. N Engl J Med 371:1359-1360. https:// doi.org/10.1056/NEJMc1409847.
6. Drosten C, Gunther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA, Berger A, Burguiere AM, Cinatl J, Eickmann M, Escriou N, Grywna K, Kramme S, Manuguerra JC, Muller S, Rickerts V, Sturmer M, Vieth S, Klenk HD, Osterhaus AD, Schmitz H, Doerr HW. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348:1967-1976. https://doi.org/10.1056/NEJMoa030747.
7. Lee HJ, Shieh CK, Gorbalenya AE, Koonin EV, La Monica N, Tuler J, Bagdzhadzhyan A, Lai MM. 1991. The complete sequence (22 kilobases) of murine coronavirus gene 1 encoding the putative proteases and RNA polymerase. Virology 180:567-582. https://doi.org/10.1016/0042-6822(91)90071-I.
8. Lomniczi B. 1977. Biological properties of avian coronavirus RNA. J Gen Virol 36:531-533. https://doi.org/10.1099/0022-1317-36-3-531.
9. Lomniczi B, Kennedy I. 1977. Genome of infectious bronchitis virus. J Virol 24:99-107.
10. Raj VS, Mou H, Smits SL, Dekkers DH, Muller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, Thiel V, Drosten C, Rottier PJ, Osterhaus AD, Bosch BJ, Haagmans BL. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251-254. https://doi.org/10.1038/nature12005.
11. Hurst-Hess KR, Kuo L, Masters PS. 2015. Dissection of amino-terminal functional domains of murine coronavirus nonstructural protein 3. J Virol 89:6033-6047. https://doi.org/10.1128/JVI.00197-15.
12. Graham RL, Sims AC, Brockway SM, Baric RS, Denison MR. 2005. The nsp2 replicase proteins of murine hepatitis virus and severe acute respiratory syndrome coronavirus are dispensable for viral replication. J Virol 79: 13399-13411. https://doi.org/10.1128/JVI.79.21.13399-13411.2005.
13. Neuman BW, Chamberlain P, Bowden F, Joseph J. 2014. Atlas of coronavirus replicase structure. Virus Res 194:49-66. https://doi.org/10 .1016/j.virusres.2013.12.004.
14. Lai MM, Baric RS, Brayton PR, Stohlman SA. 1984. Characterization of leader RNA sequences on the virion and mRNAs of mouse hepatitis virus, a cytoplasmic RNA virus. Proc Natl Acad Sci U S A 81:3626-3630.
15. Lai MM, Patton CD, Baric RS, Stohlman SA. 1983. Presence of leader sequences in the mRNA of mouse hepatitis virus. J Virol 46:1027-1033.
16. Leibowitz JL, Wilhelmsen KC, Bond CW. 1981. The virus-specific intracellular RNA species of two murine coronaviruses: MHV-a59 and MHV-JHM. Virology 114:39-51. https://doi.org/10.1016/0042-6822(81)90250-6.
17. Spaan WJ, Rottier PJ, Horzinek MC, van der Zeijst BA. 1982. Sequence relationships between the genome and the intracellular RNA species 1, 3, 6, and 7 of mouse hepatitis virus strain A59. J Virol 42:432-439.
18. Menachery VD, Mitchell HD, Cockrell AS, Gralinski LE, Yount BL, Jr, Graham RL, McAnarney ET, Douglas MG, Scobey T, Beall A, Dinnon K, III, Kocher JF, Hale AE, Stratton KG, Waters KM, Baric RS. 2017. MERS-CoV accessory ORFs play key role for infection and pathogenesis. mBio 8:e00665-17. https://doi.org/10.1128/mBio.00665-17.
19. Thornbrough JM, Jha BK, Yount B, Goldstein SA, Li Y, Elliott R, Sims AC, Baric RS, Silverman RH, Weiss SR. 2016. Middle East respiratory syndrome coronavirus NS4b protein inhibits host RNase L activation. mBio 7:e00258-16. https://doi.org/10.1128/mBio.00258-16.
20. Matthews KL, Coleman CM, van der Meer Y, Snijder EJ, Frieman MB. 2014. The ORF4b-encoded accessory proteins of Middle East respiratory syndrome coronavirus and two related bat coronaviruses localize to the nucleus and inhibit innate immune signalling. J Gen Virol 95:874-882. https://doi.org/10.1099/vir.0.062059-0.
21. Niemeyer D, Zillinger T, Muth D, Zielecki F, Horvath G, Suliman T, Barchet W, Weber F, Drosten C, Muller MA. 2013. Middle East respiratory syndrome coronavirus accessory protein 4a is a type I interferon antagonist. J Virol 87:12489-12495. https://doi.org/10.1128/JVI.01845-13.
22. Canton J, Fehr AR, Fernandez-Delgado R, Gutierrez-Alvarez FJ, Sanchez-Aparicio MT, Garcia-Sastre A, Perlman S, Enjuanes L, Sola I. 2018. MERSCoV 4b protein interferes with the NF-kappaB-dependent innate immune response during infection. PLoS Pathog 14:e1006838. https://doi .org/10.1371/journal.ppat.1006838.
23. Holcik M, Sonenberg N. 2005. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318-327. https://doi.org/10.1038/nrm1618.
24. Garcia MA, Meurs EF, Esteban M. 2007. The dsRNA protein kinase PKR: virus and cell control. Biochimie 89:799-811. https://doi.org/10.1016/j .biochi.2007.03.001.
25. Farrell PJ, Balkow K, Hunt T, Jackson RJ, Trachsel H. 1977. Phosphorylation of initiation factor eIF-2 and the control of reticulocyte protein synthesis. Cell 11:187-200. https://doi.org/10.1016/0092-8674(77)90330-0.
26. Wek RC, Jiang HY, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34:7-11. https://doi.org/10 .1042/BST0340007.
27. Anderson P, Kedersha N. 2008. Stress granules: the Tao of RNA triage. Trends Biochem Sci 33:141-150. https://doi.org/10.1016/j.tibs.2007.12 .003.
28. Anderson P, Kedersha N. 2009. Stress granules. Curr Biol 19:R397-R398. https://doi.org/10.1016/j.cub.2009.03.013.
29. Kedersha N, Anderson P. 2009. Regulation of translation by stress granules and processing bodies. Prog Mol Biol Transl Sci 90:155-185. https:// doi.org/10.1016/S1877-1173(09)90004-7.
30. 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. https://doi.org/10.1083/jcb.147.7.1431.
31. Onomoto K, Jogi M, Yoo JS, Narita R, Morimoto S, Takemura A, Sambhara S, Kawaguchi A, Osari S, Nagata K, Matsumiya T, Namiki H, Yoneyama M, Fujita T. 2012. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS One 7:e43031. https://doi.org/10.1371/journal.pone.0043031.
32. Reineke LC, Lloyd RE. 2015. The stress granule protein G3BP1 recruits protein kinase R to promote multiple innate immune antiviral responses. J Virol 89:2575-2589. https://doi.org/10.1128/JVI.02791-14.
33. Langereis MA, Feng Q, van Kuppeveld FJ. 2013. MDA5 localizes to stress granules, but this localization is not required for the induction of type I interferon. J Virol 87:6314-6325. https://doi.org/10.1128/JVI.03213-12.
34. Onomoto K, Yoneyama M, Fung G, Kato H, Fujita T. 2014. Antiviral innate immunity and stress granule responses. Trends Immunol 35:420-428. https://doi.org/10.1016/j.it.2014.07.006.
35. Okonski KM, Samuel CE. 2013. Stress granule formation induced by measles virus is protein kinase PKR dependent and impaired by RNA adenosine deaminase ADAR1. J Virol 87:756-766. https://doi.org/10 .1128/JVI.02270-12.
36. Ng CS, Jogi M, Yoo JS, Onomoto K, Koike S, Iwasaki T, Yoneyama M, Kato H, Fujita T. 2013. Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J Virol 87:9511-9522. https://doi.org/10.1128/JVI.03248-12.
37. White JP, Lloyd RE. 2012. Regulation of stress granules in virus systems. Trends Microbiol 20:175-183. https://doi.org/10.1016/j.tim.2012.02.001.
38. Poblete-Duran N, Prades-Perez Y, Vera-Otarola J, Soto-Rifo R, Valiente-Echeverria F. 2016. Who regulates whom? An overview of RNA granules and viral infections. Viruses 8:E180. https://doi.org/10.3390/v8070180.
39. Khaperskyy DA, Hatchette TF, McCormick C. 2012. Influenza A virus inhibits cytoplasmic stress granule formation. FASEB J 26:1629-1639. https://doi.org/10.1096/fj.11-196915.
40. Sciortino MT, Parisi T, Siracusano G, Mastino A, Taddeo B, Roizman B. 2013. The virion host shutoff RNase plays a key role in blocking the activation of protein kinase R in cells infected with herpes simplex virus 1. J Virol 87:3271-3276. https://doi.org/10.1128/JVI.03049-12.
41. Cassady KA, Gross M. 2002. The herpes simplex virus type 1 U(S)11 protein interacts with protein kinase R in infected cells and requires a 30-amino-acid sequence adjacent to a kinase substrate domain. J Virol 76:2029-2035. https://doi.org/10.1128/jvi.76.5.2029-2035.2002.
42. He B, Gross M, Roizman B. 1997. The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc Natl Acad Sci U S A 94:843-848.
43. Mulvey M, Arias C, Mohr I. 2007. Maintenance of endoplasmic reticulum (ER) homeostasis in herpes simplex virus type 1-infected cells through the association of a viral glycoprotein with PERK, a cellular ER stress sensor. J Virol 81:3377-3390. https://doi.org/10.1128/JVI.02191-06.
44. Simpson-Holley M, Kedersha N, Dower K, Rubins KH, Anderson P, Hensley LE, Connor JH. 2011. Formation of antiviral cytoplasmic granules during orthopoxvirus infection. J Virol 85:1581-1593. https://doi.org/10 .1128/JVI.02247-10.
45. White JP, Cardenas AM, Marissen WE, Lloyd RE. 2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2:295-305. https://doi.org/10.1016/j.chom.2007.08.006.
46. Sun Y, Dong L, Yu S, Wang X, Zheng H, Zhang P, Meng C, Zhan Y, Tan L, Song C, Qiu X, Wang G, Liao Y, Ding C. 2017. Newcastle disease virus induces stable formation of bona fide stress granules to facilitate viral replication through manipulating host protein translation. FASEB J 31: 1337-1353. https://doi.org/10.1096/fj.201600980R.
47. Heinrich BS, Cureton DK, Rahmeh AA, Whelan SP. 2010. Protein expression redirects vesicular stomatitis virus RNA synthesis to cytoplasmic inclusions. PLoS Pathog 6:e1000958. https://doi.org/10.1371/ journal.ppat.1000958.
48. Dinh PX, Beura LK, Das PB, Panda D, Das A, Pattnaik AK. 2013. Induction of stress granule-like structures in vesicular stomatitis virus-infected cells. J Virol 87:372-383. https://doi.org/10.1128/JVI.02305-12.
49. Garaigorta U, Heim MH, Boyd B, Wieland S, Chisari FV. 2012. Hepatitis C virus (HCV) induces formation of stress granules whose proteins regulate HCV RNA replication and virus assembly and egress. J Virol 86: 11043-11056. https://doi.org/10.1128/JVI.07101-11.
50. Ruggieri A, Dazert E, Metz P, Hofmann S, Bergeest JP, Mazur J, Bankhead P, Hiet MS, Kallis S, Alvisi G, Samuel CE, Lohmann V, Kaderali L, Rohr K, Frese M, Stoecklin G, Bartenschlager R. 2012. Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 12:71-85. https://doi.org/10.1016/j .chom.2012.05.013.
51. Sola I, Galan C, Mateos-Gomez PA, Palacio L, Zuniga S, Cruz JL, Almazan F, Enjuanes L. 2011. The polypyrimidine tract-binding protein affects coronavirus RNA accumulation levels and relocalizes viral RNAs to novel cytoplasmic domains different from replication-transcription sites. J Virol 85:5136-5149. https://doi.org/10.1128/JVI.00195-11.
52. Raaben M, Groot Koerkamp MJ, Rottier PJ, de Haan CA. 2007. Mouse hepatitis coronavirus replication induces host translational shutoff and mRNA decay, with concomitant formation of stress granules and processing bodies. Cell Microbiol 9:2218-2229. https://doi.org/10.1111/j .1462-5822.2007.00951.x.
53. Rabouw HH, Langereis MA, Knaap RC, Dalebout TJ, Canton J, Sola I, Enjuanes L, Bredenbeek PJ, Kikkert M, de Groot RJ, van Kuppeveld FJ. 2016. Middle East respiratory coronavirus accessory protein 4a inhibits PKR-mediated antiviral stress responses. PLoS Pathog 12:e1005982. https://doi.org/10.1371/journal.ppat.1005982.
54. Park SH, Choi J, Kang JI, Choi SY, Hwang SB, Kim JP, Ahn BY. 2006. Attenuated expression of interferon-induced protein kinase PKR in a simian cell devoid of type I interferons. Mol Cells 21:21-28.
55. Scobey T, Yount BL, Sims AC, Donaldson EF, Agnihothram SS, Menachery VD, Graham RL, Swanstrom J, Bove PF, Kim JD, Grego S, Randell SH, Baric RS. 2013. Reverse genetics with a full-length infectious cDNA of the Middle East respiratory syndrome coronavirus. Proc Natl Acad Sci U S A 110:16157-16162. https://doi.org/10.1073/pnas.1311542110.
56. Lokugamage KG, Narayanan K, Nakagawa K, Terasaki K, Ramirez SI, Tseng CT, Makino S. 2015. Middle East respiratory syndrome coronavirus nsp1 inhibits host gene expression by selectively targeting mRNAs transcribed in the nucleus while sparing mRNAs of cytoplasmic origin. J Virol 89:10970-10981. https://doi.org/10.1128/JVI.01352-15.
57. Dauber B, Poon D, Dos Santos T, Duguay BA, Mehta N, Saffran HA, Smiley JR. 2016. The herpes simplex virus virion host shutoff protein enhances translation of viral true late mRNAs independently of suppressing protein kinase R and stress granule formation. J Virol 90:6049-6057. https:// doi.org/10.1128/JVI.03180-15.
58. Emeny JM, Morgan MJ. 1979. Regulation of the interferon system: evidence that Vero cells have a genetic defect in interferon production. J Gen Virol 43:247-252. https://doi.org/10.1099/0022-1317-43-1-247.
59. Wathelet MG, Berr PM, Huez GA. 1992. Regulation of gene expression by cytokines and virus in human cells lacking the type-I interferon locus. Eur JBiochem206:901-910. https://doi.org/10.1111/j.1432-1033. 1992.tb16999.x.
60. Baric RS, Nelson GW, Fleming JO, Deans RJ, Keck JG, Casteel N, Stohlman SA. 1988. Interactions between coronavirus nucleocapsid protein and viral RNAs: implications for viral transcription. J Virol 62:4280-4287.
61. Compton SR, Rogers DB, Holmes KV, Fertsch D, Remenick J, McGowan JJ. 1987. In vitro replication of mouse hepatitis virus strain A59. J Virol 61:1814-1820.
62. Panas MD, Varjak M, Lulla A, Eng KE, Merits A, Karlsson Hedestam GB, McInerney GM. 2012. Sequestration of G3BP coupled with efficient translation inhibits stress granules in Semliki Forest virus infection. Mol Biol Cell 23:4701-4712. https://doi.org/10.1091/mbc.e12-08-0619.
63. Emara MM, Liu H, Davis WG, Brinton MA. 2008. Mutation of mapped TIA-1/TIAR binding sites in the 3= terminal stem-loop of West Nile virus minus-strand RNA in an infectious clone negatively affects genomic RNA amplification. J Virol 82:10657-10670. https://doi.org/ 10.1128/JVI.00991-08.
64. Li W, Li Y, Kedersha N, Anderson P, Emara M, Swiderek KM, Moreno GT, Brinton MA. 2002. Cell proteins TIA-1 and TIAR interact with the 3= stem-loop of the West Nile virus complementary minus-strand RNA and facilitate virus replication. J Virol 76:11989-12000. https://doi.org/10 .1128/JVI.76.23.11989-12000.2002.
65. Scholte FE, Tas A, Albulescu IC, Zusinaite E, Merits A, Snijder EJ, van Hemert MJ. 2015. Stress granule components G3BP1 and G3BP2 play a proviral role early in Chikungunya virus replication. J Virol 89:4457-4469. https://doi.org/10.1128/JVI.03612-14.