Identification of human parainfluenza virus type 2 (HPIV-2) V protein amino acid residues that reduce binding of V to MDA5 and attenuate HPIV-2 replication in nonhuman primates

Journal of Virology

Volumn 85, Issue 8, 2011, Pages 4007-4019

  Schaap Nutt, Anne ^a   Higgins, Caraline ^a   Amaro Carambot, Emerito ^a   Nolan, Sheila M ^a   D'Angelo, Christopher ^a   Murphy, Brian R ^a   Collins, Peter L ^a   Schmidt, Alexander C ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BETA INTERFERON; CYSTEINE; HISTIDINE; INTERFERON; INTERFERON REGULATORY FACTOR 3; PHENYLALANINE; PROTEIN MDA5; RNA HELICASE; SERINE; UNCLASSIFIED DRUG; VIRUS PROTEIN V;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHLOROCEBUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIMERIZATION; GENE SEQUENCE; HUMAN; HUMAN CELL; MUTAGENESIS; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAINFLUENZA VIRUS 2; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; VIRUS REPLICATION; VIRUS VIABILITY; VIRUS VIRULENCE; WILD TYPE;

AMINO ACID SUBSTITUTION; AMINO ACIDS; ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; DEAD-BOX RNA HELICASES; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA MULATTA; MICROBIAL VIABILITY; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PARAINFLUENZA VIRUS 2, HUMAN; PROTEIN BINDING; VIRAL PROTEINS; VIRULENCE FACTORS; VIRUS REPLICATION;

CERCOPITHECUS AETHIOPS; HUMAN PARAINFLUENZA VIRUS 2; PRIMATES;

EID: 79952844570     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02542-10     Document Type: Article

References (68)

1. Abramoff, M. D., P. Magelhaes, and S. J. Ram. 2004. Image processing with ImageJ. Biophoton. Int. 11:36-42.
2. Andrejeva, J., et al. 2004. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFNbeta promoter. Proc. Natl. Acad. Sci. U. S. A. 101:17264-17269.
3. Andrejeva, J., D. F. Young, S. Goodbourn, and R. E. Randall. 2002. Degradation of STAT1 and STAT2 by the V proteins of simian virus 5 and human parainfluenza virus type 2, respectively: consequences for virus replication in the presence of alpha/beta and gamma interferons. J. Virol. 76:2159-2167.
4. Berghäll, H., et al. 2006. The interferon-inducible RNA helicase, mda-5, is involved in measles virus-induced expression of antiviral cytokines. Microbes Infect. 8:2138-2144. (Pubitemid 44311582)
5. Buchholz, U. J., S. Finke, and K. K. Conzelmann. 1999. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J. Virol. 73:251-259.
6. Childs, K., et al. 2007. mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 359:190-200. (Pubitemid 46223502)
7. Childs, K. S., J. Andrejeva, R. E. Randall, and S. Goodbourn. 2009. Mechanism of mda-5 inhibition by paramyxovirus V proteins. J. Virol. 83:1465-1473.
8. Curran, J., M. de Melo, S. Moyer, and D. Kolakofsky. 1991. Characterization of the Sendai virus V protein with an anti-peptide antiserum. Virology 184:108-116.
9. Didcock, L., D. F. Young, S. Goodbourn, and R. E. Randall. 1999. The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J. Virol. 73:9928-9933.
10. Emeny, J. M., and M. J. Morgan. 1979. Regulation of the interferon system: evidence that Vero cells have a genetic defect in interferon production. J. Gen. Virol. 43:247-252.
11. Fensterl, V., and G. C. Sen. 2009. Interferons and viral infections. Biofactors 35:14-20.
12. Ferko, B., et al. 2004. Immunogenicity and protection efficacy of replication-deficient influenza A viruses with altered NS1 genes. J. Virol. 78:13037-13045. (Pubitemid 39507811)
13. Foy, E., et al. 2005. Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc. Natl. Acad. Sci. U. S. A. 102:2986-2991.
14. Gitlin, L., et al. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. U. S. A. 103:8459-8464.
15. Gitlin, L., et al. 2010. Melanoma differentiation-associated gene 5 (MDA5) is involved in the innate immune response to Paramyxoviridae infection in vivo. PLoS Pathog. 6:e1000734.
16. 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.
17. Gottlieb, J., et al. 2009. Community-acquired respiratory viral infections in lung transplant recipients: a single season cohort study. Transplantation 87:1530-1537.
18. Guix, S., et al. 2007. Norwalk virus RNA is infectious in mammalian cells. J. Virol. 81:12238-12248. (Pubitemid 350085839)
19. Hai, R., et al. 2008. Influenza B virus NS1-truncated mutants: live-attenuated vaccine approach. J. Virol. 82:10580-10590. (Pubitemid 352691164)
20. Hall, S. L., et al. 1992. Cold-passaged human parainfluenza type 3 viruses contain ts and non-ts mutations leading to attenuation in rhesus monkeys. Virus Res. 22:173-184.
21. He, B., et al. 2002. Recovery of paramyxovirus simian virus 5 with a V protein lacking the conserved cysteine-rich domain: the multifunctional V protein blocks both interferon-beta induction and interferon signaling. Virology 303:15-32. (Pubitemid 36027162)
22. Horvath, C. M. 2004. Weapons of STAT destruction. Interferon evasion by paramyxovirus V protein. Eur. J. Biochem. 271:4621-4628.
23. Ikegame, S., et al. 2010. Both RIG-I and MDA5 RNA helicases contribute to the induction of alpha/beta interferon in measles virus-infected human cells. J. Virol. 84:372-379.
24. Kapikian, A., et al. 1963. An outbreak of parainfluenza 2 (croup-associated) virus infection. JAMA 183:324-330.
25. Karron, R. A., and P. L. Collins. 2007. Parainfluenza viruses, p. 1497-1526. In D. M. Knipe, P. M. Howley, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed., vol. 1. Lippincott Williams & Wilkins, Philadelphia, PA.
26. Kato, H., et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
27. Kawano, M., et al. 2001. Recovery of infectious human parainfluenza type 2 virus from cDNA clones and properties of the defective virus without V-specific cysteine-rich domain. Virology 284:99-112. (Pubitemid 32476699)
28. Komatsu, T., K. Takeuchi, and B. Gotoh. 2007. Bovine parainfluenza virus type 3 accessory proteins that suppress beta interferon production. Microbes Infect. 9:954-962. (Pubitemid 46924839)
29. Komatsu, T., K. Takeuchi, J. Yokoo, and B. Gotoh. 2004. C and V proteins of Sendai virus target signaling pathways leading to IRF-3 activation for the negative regulation of interferon-beta production. Virology 325:137-148.
30. Li, T., X. Chen, K. C. Garbutt, P. Zhou, and N. Zheng. 2006. Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124:105-117. (Pubitemid 43069313)
31. Lin, G. Y., and R. A. Lamb. 2000. The paramyxovirus simian virus 5 V protein slows progression of the cell cycle. J. Virol. 74:9152-9166.
32. Lu, L. L., M. Puri, C. M. Horvath, and G. C. Sen. 2008. Select paramyxoviral V proteins inhibit IRF3 activation by acting as alternative substrates for inhibitor of kappaB kinase epsilon (IKKe)/TBK1. J. Biol. Chem. 283:14269-14276.
33. McAuliffe, J. M., et al. 2004. Codon substitution mutations at two positions in the L polymerase protein of human parainfluenza virus type 1 yield viruses with a spectrum of attenuation in vivo and increased phenotypic stability in vitro. J. Virol. 78:2029-2036. (Pubitemid 38176734)
34. McCartney, S. A., et al. 2008. MDA-5 recognition of a murine norovirus. PLoS Pathog. 4:e1000108.
35. Mosca, J. D., and P. M. Pitha. 1986. Transcriptional and posttranscriptional regulation of exogenous human beta interferon gene in simian cells defective in interferon synthesis. Mol. Cell. Biol. 6:2279-2283.
36. Murphy, B. R. 1988. Current approaches to the development of vaccines effective against parainfluenza viruses. Bull. World Health Organ. 66:391-397.
37. Newman, J. T., et al. 2004. Generation of recombinant human parainfluenza virus type 1 vaccine candidates by importation of temperature-sensitive and attenuating mutations from heterologous paramyxoviruses. J. Virol. 78:2017-2028. (Pubitemid 38176733)
38. Newman, J. T., et al. 2002. Sequence analysis of the Washington/1964 strain of human parainfluenza virus type 1 (HPIV1) and recovery and characterization of wild-type recombinant HPIV1 produced by reverse genetics. Virus Genes 24:77-92. (Pubitemid 34229615)
39. Nishio, M., D. Garcin, V. Simonet, and D. Kolakofsky. 2002. The carboxyl segment of the mumps virus V protein associates with Stat proteins in vitro via a tryptophan-rich motif. Virology 300:92-99.
40. Nishio, M., J. Ohtsuka, M. Tsurudome, T. Nosaka, and D. Kolakofsky. 2008. Human parainfluenza virus type 2 V protein inhibits genome replication by binding to the L protein: possible role in promoting viral fitness. J. Virol. 82:6130-6138. (Pubitemid 351875095)
41. Nishio, M., M. Tsurudome, H. Ishihara, M. Ito, and Y. Ito. 2007. The conserved carboxyl terminus of human parainfluenza virus type 2 V protein plays an important role in virus growth. Virology 362:85-98. (Pubitemid 46617691)
42. Nishio, M., et al. 2005. Identification of paramyxovirus V protein residues essential for STAT protein degradation and promotion of virus replication. J. Virol. 79:8591-8601. (Pubitemid 40853558)
43. Nolan, S. M., et al. 2007. Recombinant human parainfluenza virus type 2 vaccine candidates containing a 3′ genomic promoter mutation and L polymerase mutations are attenuated and protective in non-human primates. Vaccine 25:6409-6422. (Pubitemid 47096752)
44. Nolan, S. M., S. S. E. Amaro-Carambot, P. L. Collins, B. R. Murphy, and M. H. Skiadopoulos. 2005. Live-attenuated intranasal parainfluenza virus type 2 vaccine candidates developed by reverse genetics containing L polymerase protein mutations imported from heterologous paramyxoviruses. Vaccine 39:4765-4774.
45. Parisien, J. P., et al. 2009. A shared interface mediates paramyxovirus interference with antiviral RNA helicases MDA5 and LGP2. J. Virol. 83:7252-7260.
46. Parrott, R., A. K. H. W. Vargosko, J. Bell, and R. Chanock. 1962. Myxoviruses. III. Parainfluenza. Am. J. Public Health 52:907-917.
47. Paterson, R., G. Leser, M. Shaughnessy, and R. Lamb. 1995. The paramyxovirus SV5 V protein binds two atoms of zinc and is a structural component of virions. Virology 208:121-131.
48. Pfaller, C. K., and K. K. Conzelmann. 2008. Measles virus V protein is a decoy substrate for IkappaB kinase alpha and prevents Toll-like receptor 7/9-mediated interferon induction. J. Virol. 82:12365-12373.
49. Poole, E., B. He, R. A. Lamb, R. E. Randall, and S. Goodbourn. 2002. The V proteins of Simian virus 5 and other paramyxoviruses inhibit induction of interferon-beta. Virology 303:33-46. (Pubitemid 36027163)
50. Ramachandran, A., and C. M. Horvath. 2010. Dissociation of paramyxovirus interferon evasion activities: universal and virus-specific requirements for conserved V protein amino acids in MDA5 interference. J. Virol. 84:11152-11163.
51. Saito, T., and M. Gale, Jr. 2008. Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity. J. Exp. Med. 205:1523-1527.
52. Saito, T., D. M. Owen, F. Jiang, J. Marcotrigiano, and M. Gale, Jr. 2008. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454:523-527.
53. Schaap-Nutt, A., et al. 2010. Recombinant human parainfluenza virus type 2 with mutations in V that permit cellular interferon signaling are not attenuated in non-human primates. Virology 406:65-79.
54. Schaap-Nutt, A., et al. 2010. Human parainfluenza virus type 2 V protein inhibits interferon production and signaling and is required for replication in non-human primates. Virology 397:285-298.
55. Reference deleted.
56. Skiadopoulos, M. H., et al. 2003. The genome length of human parainfluenza virus type 2 follows the rule of six, and recombinant viruses recovered from non-polyhexameric-length antigenomic cDNAs contain a biased distribution of correcting mutations. J. Virol. 77:270-279. (Pubitemid 36004967)
57. Stojdl, D. F., B. D. Lichty, B. R. tenOever, et al. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
58. Talon, J., et al. 2000. Influenza A and B viruses expressing altered NS1 proteins: a vaccine approach. Proc. Natl. Acad. Sci. U. S. A. 97:4309-4314.
59. Teng, M. N., et al. 2000. Recombinant respiratory syncytial virus that does not express the NS1 or M2-2 protein is highly attenuated and immunogenic in chimpanzees. J. Virol. 74:9317-9321.
60. Tsurudome, M., M. Nishio, H. Komada, H. Bando, and Y. Ito. 1989. Extensive antigenic diversity among human parainfluenza type 2 virus isolates and immunological relationships among paramyxoviruses revealed by monoclonal antibodies. Virology 171:38-48. (Pubitemid 19180770)
61. Van Cleve, W., et al. 2006. Attenuating mutations in the P/C gene of human parainfluenza virus type 1 (HPIV1) vaccine candidates abrogate the inhibition of both induction and signaling of type I interferon (IFN) by wild-type HPIV1. Virology 352:61-73. (Pubitemid 44164412)
62. van Wyke Coelingh, K. L., et al. 1990. Antibody responses of humans and nonhuman primates to individual antigenic sites of the hemagglutinin- neuraminidase and fusion glycoproteins after primary infection or reinfection with parainfluenza type 3 virus. J. Virol. 64:3833-3843.
63. Wansley, E. K., and G. D. Parks. 2002. Naturally occurring substitutions in the p/v gene convert the noncytopathic paramyxovirus simian virus 5 into a virus that induces alpha/beta interferon synthesis and cell death. J. Virol. 76:10109-10121.
64. Wathelet, M. G., P. M. Berr, and G. A. Huez. 1992. Regulation of gene expression by cytokines and virus in human cells lacking the type-I interferon locus. Eur. J. Biochem. 206:901-910.
65. Whitehead, S. S., et al. 1999. Recombinant respiratory syncytial virus bearing a deletion of either the NS2 or SH gene is attenuated in chimpanzees. J. Virol. 73:3438-3442. (Pubitemid 29135738)
66. Wright, P. F., et al. 2006. The interferon antagonist NS2 protein of respiratory syncytial virus is an important virulence determinant for humans. J. Infect. Dis. 193:573-581.
67. Yoneyama, M., et al. 2005. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175:2851-2858. (Pubitemid 41170502)
68. Young, D. F., L. Didcock, S. Goodbourn, and R. E. Randall. 2000. Paramyxoviridae use distinct virus-specific mechanisms to circumvent the interferon response. Virology 269:383-390.