Antagonism of type I interferon responses by new world hantaviruses

Journal of Virology

Volumn 84, Issue 22, 2010, Pages 11790-11801

  Levine, Jessica R ^a,b,c   Prescott, Joseph ^b   Brown, Kyle S ^c,d   Best, Sonja M ^b   Ebihara, Hideki ^b,c   Feldmann, Heinz ^b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^d UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; GLYCOPROTEIN; INTERFERON; JANUS KINASE; NUCLEOCAPSID PROTEIN; STAT PROTEIN; STAT1 PROTEIN; VIRUS PROTEIN;

ANDES VIRUS; ANIMAL CELL; ARTICLE; HANTAVIRUS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; SIN NOMBRE VIRUS; VIRUS VIRULENCE;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; HANTAVIRUS; HANTAVIRUS INFECTIONS; HUMANS; INTERFERON-ALPHA; INTERFERON-BETA; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; VERO CELLS; VIRAL PROTEINS;

ANDES VIRUS; HANTAVIRUS; RNA VIRUSES; SIN NOMBRE VIRUS;

EID: 78049487802     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00916-10     Document Type: Article

References (63)

1. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
2. Alff, P. J., I. N. Gavrilovskaya, E. Gorbunova, K. Endriss, Y. Chong, E. Geimonen, N. Sen, N. C. Reich, and E. R. Mackow. 2006. The pathogenic NY-1 hantavirus G1 cytoplasmic tail inhibits RIG-I- and TBK-1-directed interferon responses. J. Virol. 80:9676-9686.
3. Alff, P. J., N. Sen, E. Gorbunova, I. N. Gavrilovskaya, and E. R. Mackow. 2008. The NY-1 hantavirus Gn cytoplasmic tail coprecipitates TRAF3 and inhibits cellular interferon responses by disrupting TBK1-TRAF3 complex formation. J. Virol. 82:9115-9122.
4. Arikawa, J., K. Yoshimatsu, and H. Kariwa. 2001. Epidemiology and epizootiology of hantavirus infection in Japan. Jpn. J. Infect. Dis. 54:95-102.
5. Basler, C. F., A. Mikulasova, L. Martinez-Sobrido, J. Paragas, E. Muhlberger, M. Bray, H. D. Klenk, P. Palese, and A. Garcia-Sastre. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
6. Basler, C. F., X. Wang, E. Muhlberger, V. Volchkov, J. Paragas, H. D. Klenk, A. Garcia-Sastre, and P. Palese. 2000. The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc. Natl. Acad. Sci. U. S. A. 97:12289-12294.
7. Best, S. M., K. L. Morris, J. G. Shannon, S. J. Robertson, D. N. Mitzel, G. S. Park, E. Boer, J. B. Wolfinbarger, and M. E. Bloom. 2005. Inhibition of interferon-stimulated JAK-STAT signaling by a tick-borne flavivirus and identification of NS5 as an interferon antagonist. J. Virol. 79:12828-12839.
8. Cardenas, W. B., Y. M. Loo, M. Gale, Jr., A. L. Hartman, C. R. Kimberlin, L. Martinez-Sobrido, E. O. Saphire, and C. F. Basler. 2006. Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J. Virol. 80:5168-5178.
9. Casola, A., X. Bao, A. Brasier, and R. Garofalo. 2009. Inhibition of antiviral signaling pathways by paramyxoviruses, p. 247-265. In A. R. Brasier, A. Garcia-Sastre, and S. M. Lemon (ed.), Cellular signaling and innate immune responses to RNA virus infections. ASM Press, Washington, DC.
10. Chang, B., M. Crowley, M. Campen, and F. Koster. 2007. Hantavirus cardiopulmonary syndrome. Semin. Respir. Crit. Care Med. 28:193-200.
11. Chang, T. H., T. Kubota, M. Matsuoka, S. Jones, S. B. Bradfute, M. Bray, and K. Ozato. 2009. Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog. 5:e1000493.
12. Chelbi-Alix, M. K., A. Vidy, J. El Bougrini, and D. Blondel. 2006. Rabies viral mechanisms to escape the IFN system: the viral protein P interferes with IRF-3, Stat1, and PML nuclear bodies. J. Interferon Cytokine Res. 26:271-280.
13. Donelan, N. R., B. Dauber, X. Wang, C. F. Basler, T. Wolff, and A. Garcia-Sastre. 2004. The N- and C-terminal domains of the NS1 protein of influenza B virus can independently inhibit IRF-3 and beta interferon promoter activation. J. Virol. 78:11574-11582.
14. Duchin, J. S., F. T. Koster, C. J. Peters, G. L. Simpson, B. Tempest, S. R. Zaki, T. G. Ksiazek, P. E. Rollin, S. Nichol, E. T. Umland, et al. 1994. Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. The Hantavirus Study Group. N. Engl. J. Med. 330:949-955.
15. Durbin, J. E. 2009. Jak-Stat pathway in response to virus infection, p. 75-90. In A. R. Brasier, A. Garcia-Sastre, and S. M. Lemon (ed.), Cellular signaling and innate immune responses to RNA virus infections. ASM Press, Washington, DC.
16. Enria, D. A., A. M. Briggiler, N. Pini, and S. Levis. 2001. Clinical manifestations of New World hantaviruses. Curr. Top. Microbiol. Immunol. 256:117-134.
17. Fabbri, M., and M. J. Maslow. 2001. Hantavirus pulmonary syndrome in the United States. Curr. Infect. Dis. Rep. 3:258-265.
18. Fauquet, C., M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball (ed.). 2005. Virus taxonomy: eighth report of the International Committee on Taxonomy of Viruses, 8th ed. Elsevier Academic Press, London, United Kingdom.
19. Fredericksen, B., G. R. Akkaraju, E. Foy, C. Wang, J. Pflugheber, Z. J. Chen, and M. Gale, Jr. 2002. Activation of the interferon-beta promoter during hepatitis C virus RNA replication. Viral Immunol. 15:29-40. (Pubitemid 34273436)
20. Fulhorst, C. F., M. N. Cajimat, A. Utrera, M. L. Milazzo, and G. M. Duno. 2004. Maporal virus, a hantavirus associated with the fulvous pygmy rice rat (Oligoryzomys fulvescens) in western Venezuela. Virus Res. 104:139-144.
21. Goodbourn, S., L. Didcock, and R. E. Randall. 2000. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81:2341-2364.
22. Hale, B. G., R. E. Randall, J. Ortin, and D. Jackson. 2008. The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 89:2359-2376.
23. Handke, W., R. Oelschlegel, R. Franke, D. H. Kruger, and A. Rang. 2009. Hantaan virus triggers TLR3-dependent innate immune responses. J. Immunol. 182:2849-2858.
24. Hay, R. T. 2001. Protein modification by SUMO. Trends Biochem. Sci. 26:332-333.
25. Hjelle, B., S. A. Jenison, D. E. Goade, W. B. Green, R. M. Feddersen, and A. A. Scott. 1995. Hantaviruses: clinical, microbiologic, and epidemiologic aspects. Crit. Rev. Clin. Lab. Sci. 32:469-508.
26. Hornung, V., J. Ellegast, S. Kim, K. Brzozka, A. Jung, H. Kato, H. Poeck, S. Akira, K. K. Conzelmann, M. Schlee, S. Endres, and G. Hartmann. 2006. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314:994-997.
27. Jenison, S., B. Hjelle, S. Simpson, G. Hallin, R. Feddersen, and F. Koster. 1995. Hantavirus pulmonary syndrome: clinical, diagnostic, and virologic aspects. Semin. Respir. Infect. 10:259-269.
28. Johnson, A. M., M. D. Bowen, T. G. Ksiazek, R. J. Williams, R. T. Bryan, J. N. Mills, C. J. Peters, and S. T. Nichol. 1997. Laguna Negra virus associated with HPS in western Paraguay and Bolivia. Virology 238:115-127.
29. Kariwa, H., K. Yoshimatsu, and J. Arikawa. 2007. Hantavirus infection in East Asia. Comp. Immunol. Microbiol. Infect. Dis. 30:341-356.
30. Kaukinen, P., A. Vaheri, and A. Plyusnin. 2003. Non-covalent interaction between nucleocapsid protein of Tula hantavirus and small ubiquitin-related modifier-1, SUMO-1. Virus Res. 92:37-45. (Pubitemid 36246654)
31. Khaiboullina, S. F., A. A. Rizvanov, V. M. Deyde, and S. C. St. Jeor. 2005. Andes virus stimulates interferon-inducible MxA protein expression in endothelial cells. J. Med. Virol. 75:267-275.
32. Khan, A. S., and J. C. Young. 2001. Hantavirus pulmonary syndrome: at the crossroads. Curr. Opin. Infect. Dis. 14:205-209.
33. Kochs, G., A. Garcia-Sastre, and L. Martinez-Sobrido. 2007. Multiple anti-interferon actions of the influenza A virus NS1 protein. J. Virol. 81:7011-7021. (Pubitemid 46986637)
34. Lee, B. H., K. Yoshimatsu, A. Maeda, K. Ochiai, M. Morimatsu, K. Araki, M. Ogino, S. Morikawa, and J. Arikawa. 2003. Association of the nucleocapsid protein of the Seoul and Hantaan hantaviruses with small ubiquitin-like modifier-1-related molecules. Virus Res. 98:83-91. (Pubitemid 37377930)
35. Lemon, S. M. 2009. Evasion of host antiviral defences by picornaviruses, p. 335-351. In A. R. Brasier, A. Garcia-Sastre, and S. M. Lemon (ed.), Cellular signaling and innate responses to RNA virus infections. ASM Press, Washington, DC.
36. Loo, Y. M., J. Fornek, N. Crochet, G. Bajwa, O. Perwitasari, L. Martinez-Sobrido, S. Akira, M. A. Gill, A. Garcia-Sastre, M. G. Katze, and M. Gale, Jr. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82:335-345.
37. Maeda, A., B. H. Lee, K. Yoshimatsu, M. Saijo, I. Kurane, J. Arikawa, and S. Morikawa. 2003. The intracellular association of the nucleocapsid protein (NP) of hantaan virus (HTNV) with small ubiquitin-like modifier-1 (SUMO-1) conjugating enzyme 9 (Ubc9). Virology 305:288-297.
38. Meissner, J. D., J. E. Rowe, M. K. Borucki, and S. C. St. Jeor. 2002. Complete nucleotide sequence of a Chilean hantavirus. Virus Res. 89:131-143.
39. Mertz, G. J., B. Hjelle, M. Crowley, G. Iwamoto, V. Tomicic, and P. A. Vial. 2006. Diagnosis and treatment of new world hantavirus infections. Curr. Opin. Infect. Dis. 19:437-442.
40. Mibayashi, M., L. Martinez-Sobrido, Y. M. Loo, W. B. Cardenas, M. Gale, Jr., and A. Garcia-Sastre. 2007. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 81:514-524.
41. Monroe, M. C., S. P. Morzunov, A. M. Johnson, M. D. Bowen, H. Artsob, T. Yates, C. J. Peters, P. E. Rollin, T. G. Ksiazek, and S. T. Nichol. 1999. Genetic diversity and distribution of Peromyscus-borne hantaviruses in North America. Emerg. Infect. Dis. 5:75-86.
42. Narayanan, K., and S. Makino. 2009. Coronaviruses and arteriviruses, p. 373-387. In A. R. Brasier, A. Garcia-Sastre, and S. M. Lemon (ed.), Cellular signaling and innate immune responses to RNA virus infections. ASM Press, Washington, DC.
43. Padula, P. J., A. Edelstein, S. D. Miguel, N. M. Lopez, C. M. Rossi, and R. D. Rabinovich. 1998. Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 241:323-330.
44. Plyusnin, A., and S. P. Morzunov. 2001. Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr. Top. Microbiol. Immunol. 256:47-75.
45. Prescott, J., C. Ye, G. Sen, and B. Hjelle. 2005. Induction of innate immune response genes by Sin Nombre hantavirus does not require viral replication. J. Virol. 79:15007-15015.
46. Prescott, J. B., P. R. Hall, V. S. Bondu-Hawkins, C. Ye, and B. Hjelle. 2007. Early innate immune responses to Sin Nombre hantavirus occur independently of IFN regulatory factor 3, characterized pattern recognition receptors, and viral entry. J. Immunol. 179:1796-1802.
47. Prins, K. C., W. B. Cardenas, and C. F. Basler. 2009. Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKε and TBK-1. J. Virol. 83:3069-3077.
48. Rehwinkel, J., C. P. Tan, D. Goubau, O. Schulz, A. Pichlmair, K. Bier, N. Robb, F. Vreede, W. Barclay, E. Fodor, and E. S. C. Reis. 2010. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 140:397-408.
49. Reid, S. P., L. W. Leung, A. L. Hartman, O. Martinez, M. L. Shaw, C. Carbonnelle, V. E. Volchkov, S. T. Nichol, and C. F. Basler. 2006. Ebola virus VP24 binds karyopherin α1 and blocks STAT1 nuclear accumulation. J. Virol. 80:5156-5167.
50. Reid, S. P., C. Valmas, O. Martinez, F. M. Sanchez, and C. F. Basler. 2007. Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin alpha proteins with activated STAT1. J. Virol. 81:13469-13477.
51. Safronetz, D., N. R. Hegde, H. Ebihara, M. Denton, G. P. Kobinger, S. St. Jeor, H. Feldmann, and D. C. Johnson. 2009. Adenovirus vectors expressing hantavirus proteins protect hamsters against lethal challenge with Andes virus. J. Virol. 83:7285-7295.
52. Saito, T., and M. Gale, Jr. 2007. Principles of intracellular viral recognition. Curr. Opin. Immunol. 19:17-23.
53. Schmaljohn, C. S., and S. T. Nichol. 2007. Bunyaviridae, p. 1742-1789. In D. M. Knipe and P. A. Howley (ed.), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
54. Spiropoulou, C. F., C. G. Albarino, T. G. Ksiazek, and P. E. Rollin. 2007. Andes and Prospect Hill hantaviruses differ in early induction of interferon although both can downregulate interferon signaling. J. Virol. 81:2769-2776.
55. Taylor, S. L., N. Frias-Staheli, A. Garcia-Sastre, and C. S. Schmaljohn. 2009. Hantaan virus nucleocapsid protein binds to importin alpha proteins and inhibits tumor necrosis factor alpha-induced activation of nuclear factor κB. J. Virol. 83:1271-1279.
56. Thompson, A. J., and S. A. Locarnini. 2007. Toll-like receptors, RIG-I-like RNA helicases and the antiviral innate immune response. Immunol. Cell Biol. 85:435-445.
57. Unterholzner, L., and A. G. Bowie. 2008. The interplay between viruses and innate immune signaling: recent insights and therapeutic opportunities. Biochem. Pharmacol. 75:589-602.
58. Vapalahti, O., J. Mustonen, A. Lundkvist, H. Henttonen, A. Plyusnin, and A. Vaheri. 2003. Hantavirus infections in Europe. Lancet Infect. Dis. 3:653-661.
59. Wang, N., Y. Liang, S. Devaraj, J. Wang, S. M. Lemon, and K. Li. 2009. Toll-like receptor 3 mediates establishment of an antiviral state against hepatitis C virus in hepatoma cells. J. Virol. 83:9824-9834.
60. Watanabe, S., T. Watanabe, T. Noda, A. Takada, H. Feldmann, L. D. Jasenosky, and Y. Kawaoka. 2004. Production of novel Ebola virus-like particles from cDNAs: an alternative to Ebola virus generation by reverse genetics. J. Virol. 78:999-1005. (Pubitemid 38067621)
61. Wells, R. M., S. Sosa Estani, Z. E. Yadon, D. Enria, P. Padula, N. Pini, J. N. Mills, C. J. Peters, and E. L. Segura. 1997. An unusual hantavirus outbreak in southern Argentina: person-to-person transmission? Hantavirus Pulmonary Syndrome Study Group for Patagonia. Emerg. Infect. Dis. 3:171-174.
62. Yee, J., I. A. Wortman, R. A. Nofchissey, D. Goade, S. G. Bennett, J. P. Webb, W. Irwin, and B. Hjelle. 2003. Rapid and simple method for screening wild rodents for antibodies to Sin Nombre hantavirus. J. Wildl. Dis. 39:271-277.
63. Young, J. C., G. R. Hansen, T. K. Graves, M. P. Deasy, J. G. Humphreys, C. L. Fritz, K. L. Gorham, A. S. Khan, T. G. Ksiazek, K. B. Metzger, and C. J. Peters. 2000. The incubation period of hantavirus pulmonary syndrome. Am. J. Trop. Med. Hyg. 62:714-717.