Induction and suppression of innate antiviral responses by picornaviruses

Cytokine and Growth Factor Reviews

Volumn 25, Issue 5, 2014, Pages 577-585

  Feng, Qian ^a   Langereis, Martijn A ^a   van Kuppeveld, Frank J M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Interferon; MDA5; Picornaviruses; Stress granules; Viral evasion

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; DIHYDROLIPOAMIDE DEHYDROGENASE; MESSENGER RIBONUCLEOPROTEIN PARTICLE; PROTEIN MDA5; RETINOIC ACID INDUCIBLE PROTEIN I; RIBONUCLEOPROTEIN; RIG I LIKE RECEPTOR; UNCLASSIFIED DRUG; VIRUS RNA; DEAD BOX PROTEIN;

ANTIVIRAL ACTIVITY; CARDIOVIRUS; CELLULAR STRESS RESPONSE; CYTOKINE PRODUCTION; ENTEROVIRUS; HUMAN; INNATE IMMUNITY; LIFE CYCLE; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PICORNAVIRUS INFECTION; SHORT SURVEY; VIRAL GENETICS; VIRUS CELL INTERACTION; VIRUS CLASSIFICATION; VIRUS REPLICATION; VIRUS VIRULENCE; ANIMAL; CLASSIFICATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; PHYSIOLOGICAL STRESS; PICORNAVIRIDAE; SIGNAL TRANSDUCTION;

ANIMALS; DEAD-BOX RNA HELICASES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; PICORNAVIRIDAE; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; VIRUS REPLICATION;

EID: 84908344793     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2014.07.003     Document Type: Short Survey

References (83)

1. Kato H., Takahasi K., Fujita T. RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunol Rev 2011, 243:91-98.
2. Goubau D., Deddouche S., Reis E., Sousa C. Cytosolic sensing of viruses. Immunity 2013, 38:855-869.
3. Reineke L.C., Lloyd R.E. Diversion of stress granules and P-bodies during viral infection. Virology 2013, 436:255-267.
4. Harris K.G., Coyne C.B. Enter at your own risk: how enteroviruses navigate the dangerous world of pattern recognition receptor signaling. Cytokine 2013, 63:230-236.
5. Chase A.J., Semler B.L. Viral subversion of host functions for picornavirus translation and RNA replication. Future Virol 2012, 7:179-191.
6. Tapparel C., Siegrist F., Petty T.J., Kaiser L. Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 2013, 14:282-293.
7. Yeung W.-C.G., Rawlinson W.D., Craig M.E. Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 2011, 342:d35.
8. Ooi M.H., Wong S.C., Lewthwaite P., Cardosa M.J., Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol 2010, 9:1097-1105.
9. Kurai D., Saraya T., Ishii H., Takizawa H. Virus-induced exacerbations in asthma and COPD. Front Microbiol 2013, 4:293.
10. Canelli E., Luppi A., Lavazza A., Lelli D., Sozzi E., Martin A.M.M., et al. Encephalomyocarditis virus infection in an Italian zoo. Virol J 2010, 7:64.
11. Reddacliff L.A., Kirkland P.D., Hartley W.J., Reece R.L. Encephalomyocarditis virus infections in an Australian zoo. J Zoo Wildl Med 1997, 28:153-157.
12. Himeda T., Ohara Y. Saffold virus, a novel human Cardiovirus with unknown pathogenicity. J Virol 2012, 86:1292-1296.
13. Ehrenfeld E., Domingo E., Roos R.P. The picornaviruses 2010, ASM Press, Washington, DC.
14. Virgen-Slane R., Rozovics J.M., Fitzgerald K.D., Ngo T., Chou W., van der Heden van Noort G.J., et al. An RNA virus hijacks an incognito function of a DNA repair enzyme. Proc Natl Acad Sci USA 2012, 109:14634-14639.
15. Agol V.I., Gmyl A.P. Viral security proteins: counteracting host defences. Nat Rev Microbiol 2010, 8:867-878.
16. Hato S.V., Ricour C., Schulte B.M., Lanke K.H., de Bruijni M., Zoll J., et al. The mengovirus leader protein blocks interferon-alpha/beta gene transcription and inhibits activation of interferon regulatory factor 3. Cell Microbiol 2007, 9:2921-2930.
17. Van Pesch V., van Eyll O., Michiels T. The leader protein of Theiler's virus inhibits immediate-early alpha/beta interferon production. J Virol 2001, 75:7811-7817.
18. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441:101-105.
19. Abe Y., Fujii K., Nagata N., Takeuchi O., Akira S., Oshiumi H., et al. The toll-like receptor 3-mediated antiviral response is important for protection against poliovirus infection in poliovirus receptor transgenic mice. J Virol 2012, 86:185-194.
20. Gitlin L., Barchet W., Gilfillan S., Cella M., Beutler B., Flavell R.A., et al. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci USA 2006, 103:8459-8464.
21. Jin Y.-H., Kim S.J., So E.Y., Meng L., Colonna M., Kim B.S. Melanoma differentiation-associated gene 5 is critical for protection against Theiler's virus-induced demyelinating disease. J Virol 2012, 86:1531-1543.
22. Wang J.P., Cerny A., Asher D.R., Kurt-Jones E.A., Bronson R.T., Finberg R.W. MDA5 and MAVS mediate type I interferon responses to coxsackie B virus. J Virol 2010, 84:254-260.
23. Pichlmair A., Schulz O., Tan C.P., Rehwinkel J., Kato H., Takeuchi O., et al. Activation of MDA5 requires higher-order RNA structures generated during virus infection. J Virol 2009, 83:10761-10769.
24. Feng Q., Hato S.V., Langereis M.A., Zoll J., Virgen-Slane R., Peisley A., et al. MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. Cell Rep 2012, 2:1187-1196.
25. Triantafilou K., Vakakis E., Kar S., Richer E., Evans G.L., Triantafilou M. Visualisation of direct interaction of MDA5 and the dsRNA replicative intermediate form of positive strand RNA viruses. J Cell Sci 2012, 125:4761-4769.
26. Richards O.C., Martin S.C., Jense H.G., Ehrenfeld E. Structure of poliovirus replicative intermediate RNA electron microscope analysis of RNA cross-linked in vivo with psoralen derivative. J Mol Biol 1984, 173:325-340.
27. Kato H., Takeuchi O., Mikamo-Satoh E., Hirai R., Kawai T., Matsushita K., et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 2008, 205:1601-1610.
28. Deddouche S., Goubau D., Rehwinkel J., Chakravarty P., Begum S., Maillard P.V., et al. Identification of an LGP2-associated MDA5 agonist in picornavirus-infected cells. Elife 2014, 3:e01535.
29. Luthra P., Sun D., Silverman R.H., He B. Activation of IFN-β expression by a viral mRNA through RNase L and MDA5. Proc Natl Acad Sci USA 2011, 108:2118-2123.
30. Malathi K., Saito T., Crochet N., Barton D.J., Gale M., Silverman R.H. RNase L releases a small RNA from HCV RNA that refolds into a potent PAMP. RNA 2010, 16:2108-2119.
31. Malathi K., Dong B., Gale M., Silverman R.H. Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 2007, 448:816-819.
32. Satoh T., Kato H., Kumagai Y., Yoneyama M., Sato S., Matsushita K., et al. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc Natl Acad Sci USA 2010, 107:1512-1517.
33. Li X., Ranjith-Kumar C.T., Brooks M.T., Dharmaiah S., Herr A.B., Kao C., et al. The RIG-I-like receptor LGP2 recognizes the termini of double-stranded RNA. J Biol Chem 2009, 284:13881-13891.
34. Saito T., Hirai R., Loo Y.-M., Owen D., Johnson C.L., Sinha S.C., et al. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci USA 2007, 104:582-587.
35. Takahasi K., Kumeta H., Tsuduki N., Narita R., Shigemoto T., Hirai R., et al. Solution structures of cytosolic RNA sensor MDA5 and LGP2 C-terminal domains: identification of the RNA recognition loop in RIG-I-like receptors. J Biol Chem 2009, 284:17465-17474.
36. Peisley A., Lin C., Wu B., Orme-Johnson M., Liu M., Walz T., et al. Cooperative assembly and dynamic disassembly of MDA5 filaments for viral dsRNA recognition. Proc Natl Acad Sci USA 2011, 108:21010-21015.
37. Childs K.S., Randall R.E., Goodbourn S. LGP2 plays a critical role in sensitizing mda-5 to activation by double-stranded RNA. PLOS ONE 2013, 8:e64202.
38. Mukherjee A., Morosky S., Delorme-Axford A.E., Dybdahl-Sissoko N., Oberste M.S., Wang T., et al. The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLOS Pathog 2011, 7:e1001311.
39. Kuo R.-L., Kao L.-T., Lin S.-J., Wang R.Y.-L., Shih S.-R. MDA5 plays a crucial role in enterovirus 71 RNA-mediated IRF3 activation. PLOS ONE 2013, 8:e63431.
40. Drahos J., Racaniello V.R. Cleavage of IPS-1 in cells infected with human rhinovirus. J Virol 2009, 83:11581-11587.
41. pro targets MDA5 and MAVS in infected cells. J Virol 2014, 88:3369-3378.
42. Barral P.M., Morrison J.M., Drahos J., Gupta P., Sarkar D., Fisher P.B., et al. MDA-5 is cleaved in poliovirus-infected cells. J Virol 2007, 81:3677-3684.
43. pro targets MAVS to inhibit anti-viral type I interferon responses. PLOS Pathog 2013, 9:e1003231.
44. Barral P.M., Sarkar D., Fisher P.B., Racaniello V.R. RIG-I is cleaved during picornavirus infection. Virology 2009, 391:171-176.
45. Jiang L.-J., Zhang N.-N., Ding F., Li X.-Y., Chen L., Zhang H.-X., et al. RA-inducible gene-I induction augments STAT1 activation to inhibit leukemia cell proliferation. Proc Natl Acad Sci USA 2011, 108:1897-1902.
46. Belov G.A., Lidsky P.V., Mikitas O.V., Egger D., Lukyanov K.A., Bienz K., et al. Bidirectional increase in permeability of nuclear envelope upon poliovirus infection and accompanying alterations of nuclear pores. J Virol 2004, 78:10166-10177.
47. Park N., Katikaneni P., Skern T., Gustin K.E. Differential targeting of nuclear pore complex proteins in poliovirus-infected cells. J Virol 2008, 82:1647-1655.
48. Watters K., Palmenberg A.C. Differential processing of nuclear pore complex proteins by rhinovirus 2A proteases from different species and serotypes. J Virol 2011, 85:10874-10883.
49. Castelló A., Izquierdo J.M., Welnowska E., Carrasco L. RNA nuclear export is blocked by poliovirus 2A protease and is concomitant with nucleoporin cleavage. J Cell Sci 2009, 122:3799-3809.
50. Reich N.C. Nuclear/cytoplasmic localization of IRFs in response to viral infection or interferon stimulation. J Interferon Cytokine Res 2002, 22:103-109.
51. Porter F.W., Bochkov Y.A., Albee A.J., Wiese C., Palmenberg A.C. A picornavirus protein interacts with Ran-GTPase and disrupts nucleocytoplasmic transport. Proc Natl Acad Sci USA 2006, 103:12417-12422.
52. Basta H.A., Bacot-Davis V.R., Ciomperlik J.J., Palmenberg A.C. Encephalomyocarditis virus leader is phosphorylated by CK2 and Syk as a requirement for subsequent phosphorylation of cellular nucleoporins. J Virol 2014, 88(4):2219-2226.
53. Zoll J., Galama J.M., van Kuppeveld F.J., Melchers W.J. Mengovirus leader is involved in the inhibition of host cell protein synthesis. J Virol 1996, 70:4948-4952.
54. Ricour C., Delhaye S., Hato S.V., Olenyik T.D., Michel B., van Kuppeveld F.J.M., et al. Inhibition of mRNA export and dimerization of interferon regulatory factor 3 by Theiler's virus leader protein. J Gen Virol 2009, 90:177-186.
55. Lidsky P.V., Hato S., Bardina M.V., Aminev A.G., Palmenberg A.C., Sheval E.V., et al. Nucleocytoplasmic traffic disorder induced by cardioviruses. J Virol 2006, 80:2705-2717.
56. Delhaye S., van Pesch V., Michiels T. The leader protein of Theiler's virus interferes with nucleocytoplasmic trafficking of cellular proteins. J Virol 2004, 78:4357-4362.
57. Bacot-Davis V.R., Palmenberg A.C. Encephalomyocarditis virus leader protein hinge domain is responsible for interactions with Ran GTPase. Virology 2013, 443:177-185.
58. Porter F.W., Brown B., Palmenberg A.C. Nucleoporin phosphorylation triggered by the encephalomyocarditis virus leader protein is mediated by mitogen-activated protein kinases. J Virol 2010, 84:12538-12548.
59. Bardina M.V., Lidsky P.V., Sheval E.V., Fominykh K.V., van Kuppeveld F.J.M., Polyakov V.Y., et al. Mengovirus-induced rearrangement of the nuclear pore complex: hijacking cellular phosphorylation machinery. J Virol 2009, 83:3150-3161.
60. Tu L.-C., Fu G., Zilman A., Musser S.M. Large cargo transport by nuclear pores: implications for the spatial organization of FG-nucleoporins. EMBO J 2013, 32:3220-3230.
61. Langereis M.A., Feng Q., van Kuppeveld F.J. MDA5 localizes to stress granules but this localization is not required for the induction of type I interferon. J Virol 2013, 87(11):6314-6325.
62. Zoll J., Melchers W.J.G., Galama J.M.D., van Kuppeveld F.J.M. The mengovirus leader protein suppresses alpha/beta interferon production by inhibition of the iron/ferritin-mediated activation of NF-kappa B. J Virol 2002, 76:9664-9672.
63. Papon L., Oteiza A., Imaizumi T., Kato H., Brocchi E., Lawson T.G., et al. The viral RNA recognition sensor RIG-I is degraded during encephalomyocarditis virus (EMCV) infection. Virology 2009, 393:311-318.
64. Yang Y., Liang Y., Qu L., Chen Z., Yi M., Li K., et al. Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc Natl Acad Sci USA 2007, 104:7253-7258.
65. Wang D., Fang L., Li P., Sun L., Fan J., Zhang Q., et al. The leader proteinase of foot-and-mouth disease virus negatively regulates the type I interferon pathway by acting as a viral deubiquitinase. J Virol 2011, 85:3758-3766.
66. Wang D., Fang L., Li K., Zhong H., Fan J., Ouyang C., et al. Foot-and-mouth disease virus 3C protease cleaves NEMO to impair innate immune signaling. J Virol 2012, 86:9311-9322.
67. White J.P., Lloyd R.E. Regulation of stress granules in virus systems. Trends Microbiol 2012, 20:175-183.
68. Buchan J.R., Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell 2009, 36:932-941.
69. Khaperskyy D.A., Hatchette T.F., McCormick C. Influenza A virus inhibits cytoplasmic stress granule formation. FASEB J 2012, 26:1629-1639.
70. Fung G., Ng C.S., Zhang J., Shi J., Wong J., Piesik P., et al. 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 2013, 8:e79546.
71. White J.P., Cardenas A.M., Marissen W.E., Lloyd R.E. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2007, 2:295-305.
72. Ng C.S., Jogi M., Yoo J.-S., Onomoto K., Koike S., Iwasaki T., et al. Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J Virol 2013, 87:9511-9522.
73. Onomoto K., Jogi M., Yoo J.-S., Narita R., Morimoto S., Takemura A., et al. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLOS ONE 2012, 7:e43031.
74. Borghese F., Michiels T. The leader protein of cardioviruses inhibits stress granule assembly. J Virol 2011, 85:9614-9622.
75. Bonnet M.C., Daurat C., Ottone C., Meurs E.F. The N-terminus of PKR is responsible for the activation of the NF-kappaB signaling pathway by interacting with the IKK complex. Cell Signal 2006, 18:1865-1875.
76. Prigent M., Barlat I., Langen H., Dargemont C. IkappaBalpha and IkappaBalpha/NF-kappa B complexes are retained in the cytoplasm through interaction with a novel partner, RasGAP SH3-binding protein 2. J Biol Chem 2000, 275:36441-36449.
77. Chu W.M., Ostertag D., Li Z.W., Chang L., Chen Y., Hu Y., et al. JNK2 and IKKbeta are required for activating the innate response to viral infection. Immunity 1999, 11:721-731.
78. Yoo J.-S., Takahasi K., Ng C.S., Ouda R., Onomoto K., Yoneyama M., et al. DHX36 enhances RIG-I signaling by facilitating PKR-mediated antiviral stress granule formation. PLOS Pathog 2014, 10:e1004012.
79. Zhang P., Li Y., Xia J., He J., Pu J., Xie J., et al. IPS-1 plays an essential role in stress granule formation induced by dsRNA through interacting with PKR and mediating its activation. J Cell Sci 2014, 127:2471-2482.
80. Ruggieri A., Dazert E., Metz P., Hofmann S., Bergeest J.-P., Mazur J., et al. Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 2012, 12:71-85.
81. John L., Samuel C.E. Induction of stress granules by interferon and down-regulation by the cellular RNA adenosine deaminase ADAR1. Virology 2014, 454-455:299-310.
82. Panas M.D., Varjak M., Lulla A., Eng K.E., Merits A., Karlsson Hedestam G.B., et al. Sequestration of G3BP coupled with efficient translation inhibits stress granules in Semliki Forest virus infection. Mol Biol Cell 2012, 23:4701-4712.
83. Fros J.J., Domeradzka N.E., Baggen J., Geertsema C., Flipse J., Vlak J.M., et al. Chikungunya virus nsP3 blocks stress granule assembly by recruitment of G3BP into cytoplasmic foci. J Virol 2012, 86:10873-10879.