Measles Virus C protein interferes with beta interferon transcription in the nucleus

Journal of Virology

Volumn 86, Issue 2, 2012, Pages 796-805

  Sparrer, Konstantin M J ^a   Pfaller, Christian K ^a,b   Conzelmann, Karl Klaus ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BETA INTERFERON; INTERFERON REGULATORY FACTOR 3; PHOSPHOTRANSFERASE; PROTEIN C;

ARTICLE; BIOACCUMULATION; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; MEASLES VIRUS; NONHUMAN; NUCLEAR IMPORT; NUCLEOLAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; TARGET CELL; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS CELL INTERACTION; VIRUS ISOLATION; VIRUS MUTATION; VIRUS STRAIN; WILD TYPE;

AMINO ACID SEQUENCE; CELL LINE; CELL NUCLEUS; CYTOPLASM; DOWN-REGULATION; HUMANS; INTERFERON-BETA; MEASLES; MEASLES VIRUS; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

MEASLES VIRUS; MORBILLIVIRUS;

EID: 84856918188     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05899-11     Document Type: Article

References (75)

1. Bankamp B, Takeda M, Zhang Y, Xu W, Rota PA. 2011. Genetic characterization of measles vaccine strains. J. Infect. Dis. 204(Suppl. 1): S533-S548.
2. Bankamp B, Wilson J, Bellini WJ, Rota PA. 2005. Identification of naturally occurring amino acid variations that affect the ability of the measles virus C protein to regulate genome replication and transcription. Virology 336:120-129.
3. Bellini WJ, Englund G, Rozenblatt S, Arnheiter H, Richardson CD. 1985. Measles virus P gene codes for two proteins. J. Virol. 53:908-919.
4. Boonyaratanakornkit J, et al. 2011. The C proteins of human parainfluenza virus type 1 limit double-stranded RNA accumulation that would otherwise trigger activation of MDA5 and protein kinase R. J. Virol. 85: 1495-1506.
5. Boxer EL, Nanda SK, Baron MD. 2009. The rinderpest virus nonstructural C protein blocks the induction of type 1 interferon. Virology 385:134-142.
6. Brzózka K, Finke S, Conzelmann KK. 2005. Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J. Virol. 79:7673-7681.
7. Caignard G, Bourai M, Jacob Y, Tangy F, Vidalain PO. 2009. Inhibition of IFN-alpha/beta signaling by two discrete peptides within measles virus Vprotein that specifically bind STAT1 and STAT2. Virology 383:112-120.
8. Caignard G, et al. 2007. Measles virus V protein blocks Jak1-mediated phosphorylation of STAT1 to escape IFN-alpha/beta signaling. Virology 368:351-362.
9. Cattaneo R, Kaelin K, Baczko K, Billeter MA. 1989. Measles virus editing provides an additional cysteine-rich protein. Cell 56:759-764.
10. Childs KS, Andrejeva J, Randall RE, Goodbourn S. 2009. Mechanism of mda-5 inhibition by paramyxovirus V proteins. J. Virol. 83:1465-1473.
11. Chuderland D, Konson A, Seger R. 2008. Identification and characterization of a general nuclear translocation signal in signaling proteins. Mol. Cell 31:850-861.
12. Cruz CD, et al. 2006. Measles virus V protein inhibits p53 family member p73. J. Virol. 80:5644-5650.
13. Devaux P, Cattaneo R. 2004. Measles virus phosphoprotein gene products: conformational flexibility of the P/V protein amino-terminal domain and C protein infectivity factor function. J. Virol. 78: 11632-11640.
14. Devaux P, von Messling V, Songsungthong W, Springfeld C, Cattaneo R. 2007. Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360:72-83.
15. Escoffier C, et al. 1999. Nonstructural C protein is required for efficient measles virus replication in human peripheral blood cells. J. Virol. 73: 1695-1698.
16. Fontana JM, Bankamp B, Bellini WJ, Rota PA. 2008. Regulation of interferon signaling by the C and V proteins from attenuated and wildtype strains of measles virus. Virology 374:71-81.
17. Ford E, Thanos D. 2010. The transcriptional code of human IFN-beta gene expression. Biochim. Biophys. Acta 1799:328-336.
18. Furuse Y, Suzuki A, Oshitani H. 2010. Origin of measles virus: divergence from rinderpest virus between the 11th and 12th centuries. Virol. J. 7:52.
19. Gale M, Jr, Sen GC. 2009. Viral evasion of the interferon system. J. Interferon Cytokine Res. 29:475-476.
20. Gerlier D, Valentin H. 2009. Measles virus interaction with host cells and impact on innate immunity. Curr. Top. Microbiol. Immunol. 329: 163-191.
21. Goh FG, et al. 2010. Beyond the enhanceosome: cluster of novel kappaB sites downstream of the human IFN-beta gene is essential for lipopolysaccharide-induced gene activation. Blood 116:5580-5588.
22. Goodbourn S, Randall RE. 2009. The regulation of type I interferon production by paramyxoviruses. J. Interferon Cytokine Res. 29:539-547.
23. Griffin DE. 2010. Measles virus-induced suppression of immune responses. Immunol. Rev. 236:176-189.
24. Horikami SM, Moyer SA. 1995. Structure, transcription, and replication of measles virus. Curr. Top. Microbiol. Immunol. 191:35-50.
25. Hornung V, et al. 2006. 5'-Triphosphate RNA is the ligand for RIG-I. Science 314:994-997.
26. 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.
27. Kato H, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
28. Kessler JR, Kremer JR, Muller CP. 2011. Interplay of measles virus with early induced cytokines reveals different wild type phenotypes. Virus Res. 155:195-202.
29. Kosugi S, Hasebe M, Tomita M, Yanagawa H. 2009. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. U. S. A. 106:10171-10176.
30. Kumar H, Kawai T, Akira S. 2011. Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30:16-34.
31. Lin R, Heylbroeck C, Pitha PM, Hiscott J. 1998. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18:2986-2996.
32. Lu LL, Puri M, Horvath CM, Sen GC. 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. McAllister CS, Samuel CE. 2009. The RNA-activated protein kinase enhances the induction of interferon-beta and apoptosis mediated by cytoplasmic RNA sensors. J. Biol. Chem. 284:1644-1651.
34. McAllister CS, et al. 2010. Mechanisms of protein kinase PKR-mediated amplification of beta interferon induction by C protein-deficient measles virus. J. Virol. 84:380-386.
35. Mrkic B, et al. 2000. Lymphatic dissemination and comparative pathology of recombinant measles viruses in genetically modified mice. J. Virol. 74:1364-1372.
36. Nakatsu Y, Takeda M, Ohno S, Koga R, Yanagi Y. 2006. Translational inhibition and increased interferon induction in cells infected with C protein-deficient measles virus. J. Virol. 80:11861-11867.
37. Nakatsu Y, et al. 2008. Measles virus circumvents the host interferon response by different actions of the C and V proteins. J. Virol. 82: 8296-8306.
38. Naniche D. 2009. Human immunology of measles virus infection. Curr. Top. Microbiol. Immunol. 330:151-171.
39. Naniche D, et al. 2000. Evasion of host defenses by measles virus: wildtype measles virus infection interferes with induction of alpha/beta interferon production. J. Virol. 74:7478-7484.
40. Nishie T, Nagata K, Takeuchi K. 2007. The C protein of wild-type measles virus has the ability to shuttle between the nucleus and the cytoplasm. Microbes Infect. 9:344-354.
41. Ohno S, Ono N, Takeda M, Takeuchi K, Yanagi Y. 2004. Dissection of measles virus V protein in relation to its ability to block alpha/beta interferon signal transduction. J. Gen. Virol. 85:2991-2999.
42. Ono N, et al. 2001. Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J. Virol. 75:4399-4401.
43. Onomoto K, Onoguchi K, Takahasi K, Fujita T. 2010. Type I interferon production induced by RIG-I-like receptors. J. Interferon Cytokine Res. 30:875-881.
44. Palosaari H, Parisien JP, Rodriguez JJ, Ulane CM, Horvath CM. 2003. STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J. Virol. 77:7635-7644.
45. Parisien JP, et al. 2009. A shared interface mediates paramyxovirus interference with antiviral RNA helicases MDA5 and LGP2. J. Virol. 83: 7252-7260.
46. Parks CL, et al. 2001. Comparison of predicted amino acid sequences of measles virus strains in the Edmonston vaccine lineage. J. Virol. 75: 910-920.
47. Patterson JB, Thomas D, Lewicki H, Billeter MA, Oldstone MB. 2000. V and C proteins of measles virus function as virulence factors in vivo. Virology 267:80-89.
48. Pfaller CK, Conzelmann KK. 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. Pichlmair A, et al. 2006. RIG-I-mediated antiviral responses to singlestranded RNA bearing 5'-phosphates. Science 314:997-1001.
50. Platanias LC. 2005. Mechanisms of type-I- and type-II-interferonmediated signalling. Nat. Rev. Immunol. 5:375-386.
51. Plumet S, et al. 2007. Cytosolic 5'-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS One 2:e279.
52. Radecke F, Billeter MA. 1996. The nonstructural C protein is not essential for multiplication of Edmonston B strain measles virus in cultured cells. Virology 217:418-421.
53. Ramachandran A, Horvath CM. 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.
54. Ramachandran A, Parisien JP, Horvath CM. 2008. STAT2 is a primary target for measles virus V protein-mediated alpha/beta interferon signaling inhibition. J. Virol. 82:8330-8338.
55. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47.
56. Ray J, Fujinami RS. 1987. Characterization of in vitro transcription and transcriptional products of measles virus. J. Virol. 61:3381-3387.
57. Reutter GL, Cortese-Grogan C, Wilson J, Moyer SA. 2001. Mutations in the measles virus C protein that up regulate viral RNA synthesis. Virology 285:100-109.
58. Rieder M, et al. 2011. Genetic dissection of interferon-antagonistic functions of rabies virus phosphoprotein: inhibition of interferon regulatory factor 3 activation is important for pathogenicity. J. Virol. 85:842-852.
59. Schuhmann KM, Pfaller CK, Conzelmann KK. 2011. The Measles virus V protein binds to p65 (RelA) to suppress NF-{kappa}B activity. J. Virol. 85:3162-3171.
60. Shaffer JA, Bellini WJ, Rota PA. 2003. The C protein of measles virus inhibits the type I interferon response. Virology 315:389-397.
61. Slifka MK, Homann D, Tishon A, Pagarigan R, Oldstone MB. 2003. Measles virus infection results in suppression of both innate and adaptive immune responses to secondary bacterial infection. J. Clin. Invest. 111:805-810.
62. Strahle L, et al. 2007. Activation of the beta interferon promoter by unnatural Sendai virus infection requires RIG-I and is inhibited by viral C proteins. J. Virol. 81:12227-12237.
63. Takaki H, et al. 2011. Strain-to-strain difference of V protein of measles virus affects MDA5-mediated IFN-beta-inducing potential. Mol. Immunol. 48:497-504.
64. Takeuchi K, Komatsu T, Kitagawa Y, Sada K, Gotoh B. 2008. Sendai virus C protein plays a role in restricting PKR activation by limiting the generation of intracellular double-stranded RNA. J. Virol. 82: 10102-10110.
65. Toth AM, Devaux P, Cattaneo R, Samuel CE. 2009. Protein kinase PKR mediates the apoptosis induction and growth restriction phenotypes of C protein-deficient measles virus. J. Virol. 83:961-968.
66. Valsamakis A, et al. 1998. Recombinant measles viruses with mutations in the C, V, or F gene have altered growth phenotypes in vivo. J. Virol. 72:7754-7761.
67. Versteeg GA, Garcia-Sastre A. 2010. Viral tricks to grid-lock the type I interferon system. Curr. Opin. Microbiol. 13:508-516.
68. WHO. 2009. WHO fact sheet, no. 286. WHO, Geneva, Switzerland.
69. Yanagi Y, Takeda M, Ohno S, Hashiguchi T. 2009. Measles virus receptors. Curr. Top. Microbiol. Immunol. 329:13-30.
70. Ye J, Maniatis T. 2011. Negative regulation of interferon-beta gene expression during acute and persistent virus infections. PLoS One 6:e20681.
71. Yokota S, Okabayashi T, Fujii N. 2011. Measles virus C protein suppresses gamma-activated factor formation and virus-induced cell growth arrest. Virology 414:74-82.
72. Yokota S, Okabayashi T, Yokosawa N, Fujii N. 2008. Measles virus P protein suppresses Toll-like receptor signal through up-regulation of ubiquitin-modifying enzyme A20. FASEB J. 22:74-83.
73. Yokota S, et al. 2003. Measles virus suppresses interferon-alpha signaling pathway: suppression of Jak1 phosphorylation and association of viral accessory proteins, C and V, with interferon-alpha receptor complex. Virology 306:135-146.
74. Yoneyama M, et al. 1998. Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J. 17:1087-1095.
75. Yount JS, Gitlin L, Moran TM, Lopez CB. 2008. MDA5 participates in the detection of paramyxovirus infection and is essential for the early activation of dendritic cells in response to Sendai Virus defective interfering particles. J. Immunol. 180:4910-4918.