Foot-and-mouth disease virus leader protease cleaves G3BP1 and G3BP2 and inhibits stress granule formation

Journal of Virology

Volumn 93, Issue 2, 2019, Pages

  Visser, Linda J ^a   Medina, Gisselle N ^b   Rabouw, Huib H ^a   de Groot, Raoul J ^a   Langereis, Martijn A ^a   de los Santos, Teresa ^b   van Kuppeveld, Frank J M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b PLUM ISLAND ANIMAL DISEASE CENTER   (United States)

Author keywords

Aphthovirus; FMDV; G3BP1; G3BP2; SGs; Stress granules

Indexed keywords

G3BP1 PROTEIN; G3BP2 PROTEIN; INITIATION FACTOR 2ALPHA; LEADER PROTEASE; NUCLEOLYSIN TIA 1 ISOFORM P40; PROTEIN KINASE; PROTEINASE; RNA DEPENDENT PROTEIN KINASE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; PEPTIDE HYDROLASE; RNA RECOGNITION MOTIF PROTEIN; VIRAL PROTEIN;

APHTHOVIRUS; ARTICLE; CELL GRANULE; CHIMERA; CONTROLLED STUDY; ENCEPHALOMYOCARDITIS VIRUS; EQUINE RHINITIS A VIRUS; FLOW CYTOMETRY; FOOT AND MOUTH DISEASE VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRESS; VIRUS RECOMBINANT; WESTERN BLOTTING; ANIMAL; CELL LINE; ENZYMOLOGY; FOOT AND MOUTH DISEASE; HAMSTER; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHYSIOLOGICAL STRESS; VIROLOGY;

ANIMALS; APHTHOVIRUS; CELL LINE; CRICETINAE; CYTOPLASMIC GRANULES; ENCEPHALOMYOCARDITIS VIRUS; FOOT-AND-MOUTH DISEASE; FOOT-AND-MOUTH DISEASE VIRUS; HEK293 CELLS; HELA CELLS; HUMANS; PEPTIDE HYDROLASES; RNA RECOGNITION MOTIF PROTEINS; STRESS, PHYSIOLOGICAL; VIRAL PROTEINS;

EID: 85059500994     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00922-18     Document Type: Article

References (62)

1. Wu J, Chen ZJ. 2014. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 32:461–488. https://doi.org/10.1146/annurev-immunol-032713-120156.
2. McCormick C, Khaperskyy DA. 2017. Translation inhibition and stress granules in the antiviral immune response. Nat Rev Immunol 17: 647–660. https://doi.org/10.1038/nri.2017.63.
3. PakosZebrucka K, Koryga I, Mnich K, Ljujic M, Samali A, Gorman AM. 2016. The integrated stress response. EMBO Rep 17:1374–1395. https://doi.org/10.15252/embr.201642195.
4. Kedersha N, Ivanov P, Anderson P. 2013. Stress granules and cell signaling: more than just a passing phase? Trends Biochem Sci 38: 494–506. https://doi.org/10.1016/j.tibs.2013.07.004.
5. 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.
6. Reineke LC, Kedersha N, Langereis MA, van Kuppeveld FJMM, Lloyd RE. 2015. Stress granules regulate double-stranded RNA-dependent protein kinase activation through a complex containing G3BP1 and Caprin1. mBio 6:e02486-14. https://doi.org/10.1128/mBio.02486-14.
7. Reineke LC, Dougherty JD, Pierre P, Lloyd RE. 2012. Large G3BP-induced granules trigger eIF2 phosphorylation. Mol Biol Cell 23:3499–3510. https://doi.org/10.1091/mbc.E12-05-0385.
8. 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.
9. 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.
10. Kim WJ, Back SH, Kim V, Ryu I, Jang SK. 2005. Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol Cell Biol 25:2450 –2462. https://doi.org/10.1128/MCB.25.6.2450-2462.2005.
11. Humoud MN, Doyle N, Royall E, Willcocks MM, Sorgeloos F, van Kuppeveld F, Roberts LO, Goodfellow IG, Langereis MA, Locker N. 2016. Feline calicivirus infection disrupts assembly of cytoplasmic stress granules and induces G3BP1 cleavage. J Virol 90:6489 – 6501. https://doi.org/10.1128/JVI.00647-16.
12. 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.
13. Xia J, Chen X, Xu F, Wang Y, Shi Y, Li Y, He J, Zhang P. 2015. Dengue virus infection induces formation of G3BP1 granules in human lung epithelial cells. Arch Virol 160:2991–2999. https://doi.org/10.1007/s00705-015-2578-9.
14. Bidet K, Dadlani D, Garcia-Blanco MA. 2014. G3BP1, G3BP2 and Caprin1 are required for translation of interferon stimulated mRNAs and are targeted by a dengue virus non-coding RNA. PLoS Pathog 10:e1004242. https://doi.org/10.1371/journal.ppat.1004242.
15. 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.
16. Scholte FEM, Tas A, Albulescu IC, Žusinaite 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.
17. Fros JJ, Domeradzka NE, Baggen J, Geertsema C, Flipse J, Vlak JM, Pijlman GP. 2012. Chikungunya virus nsP3 blocks stress granule assembly by recruitment of G3BP into cytoplasmic foci. J Virol 86:10873–10879. https://doi.org/10.1128/JVI.01506-12.
18. Feng Q, Langereis MA, Lork M, Nguyen M, Hato SV, Lanke K, Emdad L, Bhoopathi P, Fisher PB, Lloyd RE, van Kuppeveld FJM. 2014. Enterovirus 2Apro targets MDA5 and MAVS in infected cells. J Virol 88:3369–3378. https://doi.org/10.1128/JVI.02712-13.
19. Rui Y, Su J, Wang H, Chang J, Wang S, Zheng W, Cai Y, Wei W, Gordy JT, Markham R, Kong W, Zhang W, Yu X-F. 2017. Disruption of MDA5 mediated innate immune responses by the 3C proteins of Coxsackievirus A16, Coxsackievirus A6, and Enterovirus D68. J Virol 91:e00546-17.
20. Barral PM, Sarkar D, Fisher PB, Racaniello VR. 2009. RIG-I is cleaved during picornavirus infection. Virology 391:171–176. https://doi.org/10.1016/j.virol.2009.06.045.
21. Wang B, Xi X, Lei X, Zhang X, Cui S, Wang J, Jin Q, Zhao Z. 2013. Enterovirus 71 protease 2Apro targets MAVS to inhibit anti-viral type I interferon responses. PLoS Pathog 9:e1003231. https://doi.org/10.1371/journal.ppat.1003231.
22. Mukherjee A, Morosky SA, Delorme-Axford E, Dybdahl-Sissoko N, Ober-ste MS, Wang T, Coyne CB. 2011. The coxsackievirus B 3Cpro protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLoS Pathog 7:e1001311. https://doi.org/10.1371/journal.ppat.1001311.
23. Wang C, Sun M, Yuan X, Ji L, Jin Y, Cardona CJ, Xing Z. 2017. Enterovirus 71 suppresses interferon responses by blocking Janus kinase (JAK)/ signal transducer and activator of transcription (STAT) signaling through inducing karyopherin-1 degradation. J Biol Chem 292:10262–10274. https://doi.org/10.1074/jbc.M116.745729.
24. 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.
25. Dougherty JD, Tsai WC, Lloyd RE. 2015. Multiple poliovirus proteins repress cytoplasmic RNA granules. Viruses 7:6127–6140. https://doi.org/10.3390/v7122922.
26. Borghese F, Michiels T. 2011. The leader protein of cardioviruses inhibits stress granule assembly. J Virol 85:9614–9622. https://doi.org/10.1128/JVI.00480-11.
27. Feng Q, Langereis MA, van Kuppeveld FJM. 2014. Induction and suppression of innate antiviral responses by picornaviruses. Cytokine Growth Factor Rev 25:577–585. https://doi.org/10.1016/j.cytogfr.2014.07.003.
28. Ng CS, Jogi M, Yoo J-S, 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.
29. Guarné A, Tormo J, Kirchweger R, Pfistermueller D, Fita I, Skern T. 1998. Structure of the foot-and-mouth disease virus leader protease: a papain-like fold adapted for self-processing and eIF4G recognition. EMBO J 17:7469–7479. https://doi.org/10.1093/emboj/17.24.7469.
30. Brown CC, Piccone ME, Mason PW, McKenna TS, Grubman MJ. 1996. Pathogenesis of wild-type and leaderless foot-and-mouth disease virus in cattle. J Virol 70:5638–5641.
31. de Los Santos T, de Avila Botton S, Weiblen R, Grubman MJ. 2006. The leader proteinase of foot-and-mouth disease virus inhibits the induction of beta interferon mRNA and blocks the host innate immune response. J Virol 80:1906–1914. https://doi.org/10.1128/JVI.80.4.1906-1914.2006.
32. de Los Santos T, Diaz-San Segundo F, Grubman MJ. 2007. Degradation of nuclear factor kappa B during foot-and-mouth disease virus infection. J Virol 81:12803–12815. https://doi.org/10.1128/JVI.01467-07.
33. Wang D, Fang L, Luo R, Ye R, Fang Y, Xie L, Chen H, Xiao S. 2010. Foot-and-mouth disease virus leader proteinase inhibits dsRNA-induced type I interferon transcription by decreasing interferon regulatory factor 3/7 in protein levels. Biochem Biophys Res Commun 399:72–78. https://doi.org/10.1016/j.bbrc.2010.07.044.
34. Wang D, Fang L, Li P, Sun L, Fan J, Zhang Q, Luo R, Liu X, Li K, Chen H, Chen Z, Xiao S. 2011. The leader proteinase of foot-and-mouth disease virus negatively regulates the type I Interferon pathway by acting as a viral deubiquitinase. J Virol 85:3758–3766. https://doi.org/10.1128/JVI.02589-10.
35. Swatek KN, Aumayr M, Pruneda JN, Visser LJ, Berryman S, Kueck AF, Geurink PP, Ovaa H, van Kuppeveld FJM, Tuthill TJ, Skern T, Komander D. 2018. Irreversible inactivation of ISG15 by a viral leader protease enables alternative infection detection strategies. Proc Natl Acad Sci U S A 115:2371–2376. https://doi.org/10.1073/pnas.1710617115.
36. Bailey-Elkin BA, Knaap RCM, Kikkert M, Mark BL. 2017. Structure and function of viral deubiquitinating enzymes. J Mol Biol 429:3441–3470. https://doi.org/10.1016/j.jmb.2017.06.010.
37. Wang D, Fang L, Li K, Zhong H, Fan J, Ouyang C, Zhang H, Duan E, Luo R, Zhang Z, Liu X, Chen H, Xiao S. 2012. Foot-and-mouth disease virus 3C protease cleaves NEMO to impair innate immune signaling. J Virol 86:9311–9322. https://doi.org/10.1128/JVI.00722-12.
38. Du Y, Bi J, Liu J, Liu X, Wu X, Jiang P, Yoo D, Zhang Y, Wu J, Wan R, Zhao X, Guo L, Sun W, Cong X, Chen L, Wang J. 2014. 3Cpro of foot-and-mouth disease virus antagonizes the interferon signaling pathway by blocking STAT1/STAT2 nuclear translocation. J Virol 88:4908 – 4920. https://doi.org/10.1128/JVI.03668-13.
39. Monaghan P, Gold S, Simpson J, Zhang Z, Weinreb PH, Violette SM, Alexandersen S, Jackson T. 2005. The v6 integrin receptor for foot- and-mouth disease virus is expressed constitutively on the epithelial cells targeted in cattle. J Gen Virol 86:2769–2780. https://doi.org/10.1099/vir.0.81172-0.
40. LaRocco M, Krug PW, Kramer E, Ahmed Z, Pacheco JM, Duque H, Baxt B, Rodriguez LL. 2013. A continuous bovine kidney cell line constitutively expressing bovine v6 integrin has increased susceptibility to foot- and-mouth disease virus. J Clin Microbiol 51:1714–1720. https://doi.org/10.1128/JCM.03370-12.
41. Hato SV, Ricour C, Schulte BM, Lanke KHW, de Bruijn M, Zoll J, Melchers WJG, Michiels T, van Kuppeveld FJM. 2007. The mengovirus leader protein blocks interferon-alpha/beta gene transcription and inhibits activation of interferon regulatory factor 3. Cell Microbiol 9:2921–2930. https://doi.org/10.1111/j.1462-5822.2007.01006.x.
42. Feng Q, Hato SVV, Langereis MA, Zoll J, Virgen-Slane R, Peisley A, Hur S, Semler BLL, van Rij RP, van Kuppeveld FJM. 2012. MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. Cell Rep 2:1187–1196. https://doi.org/10.1016/j.celrep.2012.10.005.
43. Rabouw HH, Langereis MA, Knaap RCM, Dalebout TJ, Canton J, Sola I, Enjuanes L, Bredenbeek PJ, Kikkert M, de Groot RJ, van Kuppeveld FJM. 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.
44. Kaminski A, Belsham GJ, Jackson RJ. 1994. Translation of encephalomyocarditis virus RNA: parameters influencing the selection of the internal initiation site. EMBO J 13:1673–1681. https://doi.org/10.1002/j.1460-2075.1994.tb06431.x.
45. Hato SV, Sorgeloos F, Ricour C, Zoll J, Melchers WJG, Michiels T, van Kuppeveld FJM. 2010. Differential IFN-/ production suppressing capacities of the leader proteins of mengovirus and foot-and-mouth disease virus. Cell Microbiol 12:310–317. https://doi.org/10.1111/j.1462-5822.2009.01395.x.
46. Piccone ME, Rieder E, Mason PW, Grubman MJ. 1995. The foot-and-mouth disease virus leader proteinase gene is not required for viral replication. J Virol 69:5376–5382.
47. Fung G, Ng CS, Zhang J, Shi J, Wong J, Piesik P, Han L, Chu F, Jagdeo J, Jan E, Fujita T, Luo H. 2013. Production of a dominant-negative fragment due to G3BP1 cleavage contributes to the disruption of mitochondria-associated protective stress granules during CVB3 infection. PLoS One 8:e79546. https://doi.org/10.1371/journal.pone.0079546.
48. Yang X, Hu Z, Fan S, Zhang Q, Zhong Y, Guo D, Qin Y, Chen M. 2018. Picornavirus 2A protease regulates stress granule formation to facilitate viral translation. PLoS Pathog 14:e1006901. https://doi.org/10.1371/journal.ppat.1006901.
49. Kedersha N, Panas MD, Achorn CA, Lyons S, Tisdale S, Hickman T, Thomas M, Lieberman J, McInerney GM, Ivanov P, Anderson P. 2016. G3BP-Caprin1-USP10 complexes mediate stress granule condensation and associate with 40S subunits. J Cell Physiol 212:845–860. https://doi.org/10.1083/jcb.201508028.
50. Agol VI, Gmyl AP. 2010. Viral security proteins: counteracting host defences. Nat Rev Microbiol 8:867–878. https://doi.org/10.1038/nrmicro2452.
51. Rai DK, Lawrence P, Kloc A, Schafer E, Rieder E. 2015. Analysis of the interaction between host factor Sam68 and viral elements during foot- and-mouth disease virus infections. Virol J 12:224. https://doi.org/10.1186/s12985-015-0452-8.
52. Lawrence P, Schafer EA, Rieder E. 2012. The nuclear protein Sam68 is cleaved by the FMDV 3C protease redistributing Sam68 to the cytoplasm during FMDV infection of host cells. Virology 425:40 –52. https://doi.org/10.1016/j.virol.2011.12.019.
53. Zhu Y, Wang B, Huang H, Zhao Z. 2016. Enterovirus 71 induces anti-viral stress granule-like structures in RD cells. Biochem Biophys Res Commun 476:212–217. https://doi.org/10.1016/j.bbrc.2016.05.094.
54. Zhang H, Chen N, Li P, Pan Z, Ding Y, Zou D, Li L, Xiao L, Shen B, Liu S, Cao H, Cui Y. 2016. The nuclear protein Sam68 is recruited to the cytoplasmic stress granules during enterovirus 71 infection. Microb Pathog 96:58–66. https://doi.org/10.1016/j.micpath.2016.04.001.
55. Black TL, Safer B, Hovanessian A, Katze MG. 1989. The cellular 68,000-Mr protein kinase is highly autophosphorylated and activated yet significantly degraded during poliovirus infection: implications for translational regulation. J Virol 63:2244–2251.
56. Chang Y-H, Lau KS, Kuo R-L, Horng J-T. 2017. dsRNA binding domain of PKR is proteolytically released by enterovirus A71 to facilitate viral replication. Front Cell Infect Microbiol 7:284. https://doi.org/10.3389/fcimb.2017.00284.
57. Li C, Zhu Z, Du X, Cao W, Yang F, Zhang X, Feng H, Li D, Zhang K, Liu X, Zheng H. 2017. Foot-and-mouth disease virus induces lysosomal degradation of host protein kinase PKR by 3C proteinase to facilitate virus replication. Virology 509:222–231. https://doi.org/10.1016/j.virol.2017.06.023.
58. Chinsangaram J, Koster M, Grubman MJ. 2001. Inhibition of L-deleted foot-and-mouth disease virus replication by alpha/beta interferon involves double-stranded RNA-dependent protein kinase. J Virol 75: 5498–5503. https://doi.org/10.1128/JVI.75.12.5498-5503.2001.
59. Galan A, Lozano G, Piñeiro D, Martinez-Salas E. 2017. G3BP1 interacts directly with the FMDV IRES and negatively regulates translation. FEBS J 284:3202–3217. https://doi.org/10.1111/febs.14184.
60. Rieder E, Bunch T, Brown F, Mason PW. 1993. Genetically engineered foot-and-mouth disease viruses with poly(C) tracts of two nucleotides are virulent in mice. J Virol 67:5139–5145.
61. van der Schaar HM, Leyssen P, Thibaut HJ, de Palma A, van der Linden L, Lanke KHW, Lacroix C, Verbeken E, Conrath K, MacLeod AM, Mitchell DR, Palmer NJ, van de Poël H, Andrews M, Neyts J, van Kuppeveld FJM. 2013. A novel, broad-spectrum inhibitor of enterovirus replication that targets host cell factor phosphatidylinositol 4-kinase III-beta. Antimicrob Agents Che-mother 57:4971–4981. https://doi.org/10.1128/AAC.01175-13.
62. Van Der Linden L, Ulferts R, Nabuurs SB, Kusov Y, Liu H, George S, Lacroix C, Goris N, Lefebvre D, Lanke KHW, De Clercq K, Hilgenfeld R, Neyts J, Van Kuppeveld FJM. 2014. Application of a cell-based protease assay for testing inhibitors of picornavirus 3C proteases. Antiviral Res 103:17–24. https://doi.org/10.1016/j.antiviral.2013.12.012.