STAT2 is a primary target for measles virus V protein-mediated alpha/beta interferon signaling inhibition

Journal of Virology

Volumn 82, Issue 17, 2008, Pages 8330-8338

  Ramachandran, Aparna ^a   Parisien, Jean Patrick ^a,b   Horvath, Curt M ^a,b,c  

^a NORTHWESTERN UNIVERSITY   (United States)

^b Evanston Northwestern Healthcare ^*  (United States)

^c Pancoe ENH Pavilion   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; AMINO ACID; ASPARTIC ACID; BETA INTERFERON; GAMMA INTERFERON; STAT1 PROTEIN; STAT2 PROTEIN; VIRUS PROTEIN V;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; INTERVENTION STUDY; MEASLES VIRUS; MOLECULAR MODEL; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ZINC FINGER MOTIF;

AMINO ACID SEQUENCE; CELL LINE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENES, REPORTER; HUMANS; INTERFERON-ALPHA; INTERFERON-BETA; KIDNEY; LUCIFERASES, RENILLA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; PLASMIDS; POINT MUTATION; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; STAT2 TRANSCRIPTION FACTOR; TRANSFECTION; VIRAL PROTEINS;

MEASLES VIRUS; MORBILLIVIRUS;

EID: 50149100345     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00831-08     Document Type: Article

References (48)

1. Andrejeva, J., K. S. Childs, D. F. Young, T. S. Carlos, N. Stock, S. Goodbourn, and R. E. Randall. 2004. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. USA 101:17264-17269.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1994. Current protocols in molecular biology. John Wiley and Sons, Inc., New York, NY.
3. Caignard, G., M. Guerbois, J. L. Labernardiere, Y. Jacob, L. M. Jones, F. Wild, F. Tangy, and P. O. Vidalain. 2007. Measles virus V protein blocks Jakl-mediated phosphorylation of STAT1 to escape IFN-alpha/beta signaling. Virology 368:351-362.
4. Cattaneo, R., K. Kaelin, K. Baczko, and M. A. Billeter. 1989. Measles virus editing provides an additional cysteine-rich protein. Cell 56:759-764.
5. Centers for Disease Control and Prevention. 2008. Multistate measles outbreak associated with an international youth sporting event - Pennsylvania, Michigan, and Texas, August-September 2007. MMWR Morb. Mortal. Wkly. Rep. 57:169-173.
6. Centers for Disease Control and Prevention. 2008. Outbreak of measles - San Diego, California, January-February 2008. MMWR Morb. Mortal. Wkly. Rep. 57:203-206.
7. Combredet, C, V. Labrousse, L. Mollet, C. Lorin, F. Delebecque, B. Hurtrel, H. McClure, M. B. Feinberg, M. Brahic, and F. Tangy. 2003. A molecularly cloned Schwarz strain of measles virus vaccine induces strong immune responses in macaques and transgenic mice. J. Virol. 77:11546-11554.
8. Devaux, P., V. von Messung, W. Songsungthong, C. Springfeld, and R. Cattaneo. 2007. Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360:72-83.
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. Fontana, J. M., B. Bankamp, W. J. Bellini, and P. A. Rota. 2008. Regulation of interferon signaling by the C and V proteins from attenuated and wildtype strains of measles virus. Virology 374:71-81.
11. Friedman, R. M. 1981. Interferons: a primer. Academic Press, New York, NY.
12. Fu, X. Y., D. S. Kessler, S. A. Veals, D. E. Levy, and J. E. Darnell, Jr. 1990. ISGF3, the transcriptional activator induced by interferon alpha, consists of multiple interacting polypeptide chains. Proc. Natl. Acad. Sci. USA 87:8555-8559.
13. García-Sastre, A., and C. A. Biron. 2006. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312:879-882.
14. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723.
15. Hahm, B., M. J. Trifilo, E. I. Zuniga, and M. B. Oldstone. 2005. Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity 22:247-257.
16. He, B., R. G. Paterson, N. Stock, J. E. Durbin, R. K. Durbin, S. Goodbourn, R. E. Randall, and R. A. Lamb. 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.
17. Horvath, C. M., and J. E. Darnell, Jr. 1996. The antiviral state induced by alpha interferon and gamma interferon requires transcriptionally active Stat1 protein. J. Virol. 70:647-650.
18. Isaacs, A., and J. Lindemann. 1957. Virus interference. I. The interferon. Proc. R. Soc. Lond. B. 147:258-267.
19. Karlin, D., S. Longhi, V. Receveur, and B. Canard. 2002. The N-terminal domain of the phosphoprotein of Morbilliviruses belongs to the natively unfolded class of proteins. Virology 296:251-262.
20. Kessler, D. S., S. A. Veals, X. Y. Fu, and D. E. Levy. 1990. Interferon-alpha regulates nuclear translocation and DNA-binding affinity of ISGF3, a multimeric transcriptional activator. Genes Dev. 4:1753-1765.
21. Lamb, R. A., and D. Kolakofsky. 2001. Paramyxoviridae: the viruses and their replication, p. 1305-1340. In B. N. Fields, D. M. Knipe, P. M. Howley, and D. E. Griffin (ed.), Fields virology, 4th ed. Lippincott-Raven Publishers, Philadelphia, PA.
22. Leung, S., S. A. Qureshi, I. M. Kerr, J. E. Darnell, Jr., and G. R. Stark. 1995. Role of STAT2 in the alpha interferon signaling pathway. Mol. Cell. Biol. 15:1312-1317.
23. 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.
24. 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.
25. Liston, P., and D. J. Briedis. 1994. Measles virus V protein binds zinc. Virology 198:399-404.
26. Ludlow, L. E., M. K. Lo, J. J. Rodriguez, P. A. Rota, and C. M. Horvath. 2008. Henipavirus V protein association with polo-like kinase reveals functional overlap with STAT1 binding and interferon evasion. J. Virol. 82:6259-6271.
27. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
28. Moss, W. J., and D. E. Griffin. 2006. Global measles elimination. Nat. Rev. Microbiol. 4:900-908.
29. Mulholland, E. K. 2006. Measles in the United States, 2006. N. Engl. J. Med. 355:440-443.
30. Müller, M., C. Laxton, J. Briscoe, C. Schindler, T. Improta, J. E. Darnell, Jr., G. R. Stark, and I. M. Kerr. 1993. Complementation of a mutant cell line: central role of the 91 kDa polypeptide of ISGF3 in the interferon-alpha and -gamma signal transduction pathways. EMBO J. 12:4221-4228.
31. Ohno, S., N. Ono, M. Takeda, K. Takeuchi, and Y. Yanagi. 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.
32. Oldstone, M. B. 2006. Viral persistence: parameters, mechanisms and future predictions. Virology 344:111-118.
33. Palosaari, H., J. P. Parisien, J. J. Rodriguez, C. M. Ulane, and C. M. Horvath. 2003. STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J. Virol. 77:7635-7644.
34. Parisien, J. P., J. F. Lau, J. J. Rodriguez, C. M. Ulane, and C. M. Horvath. 2002. Selective STAT protein degradation induced by paramyxoviruses requires both STAT1 and STAT2 but is independent of alpha/beta interferon signal transduction. J. Virol. 76:4190-4198.
35. Paterson, R. G., G. P. Leser, M. A. Shaughnessy, and R. A. Lamb. 1995. The paramyxovirus SV5 V protein binds two atoms of zinc and is a structural component of virions. Virology 208:121-131.
36. 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.
37. Radecke, F., P. Spielhofer, H. Schneider, K. Kaelin, M. Huber, C. Dotsch, G. Christiansen, and M. A. Billeter. 1995. Rescue of measles viruses from cloned DNA. EMBO J. 14:5773-5784.
38. Rodriguez, J. J., C. D. Cruz, and C. M. Horvath. 2004. Identification of the nuclear export signal and STAT-binding domains of the Nipah virus V protein reveals mechanisms underlying interferon evasion. J. Virol. 78:5358-5367.
39. Rodriguez, J. J., and C. M. Horvath. 2004. Host evasion by emerging paramyxoviruses: Hendra virus and Nipah virus v proteins inhibit interferon signaling. Viral Immunol. 17:210-219.
40. Rodriguez, J. J., J. P. Parisien, and C. M. Horvath. 2002. Nipah virus V protein evades alpha and gamma interferons by preventing STAT1 and STAT2 activation and nuclear accumulation. J. Virol. 76:11476-11483.
41. Schindler, C., K. Shuai, V. R. Prezioso, and J. E. Darnell, Jr. 1992. Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257:809-813.
42. Shaw, M. L., A. García-Sastre, P. Palese, and C. F. Basler. 2004. Nipah virus V and W proteins have a common STAT1-binding domain yet inhibit STAT1 activation from the cytoplasmic and nuclear compartments, respectively. J. Virol. 78:5633-5641.
43. Springfeld, C., V. von Messung, M. Frenzke, G. Ungerechts, C. J. Buchholz, and R. Cattaneo. 2006. Oncolytic efficacy and enhanced safety of measles virus activated by tumor-secreted matrix metalloproteinases. Cancer Res. 66:7694-7700.
44. Takeuchi, K., S. I. Kadota, M. Takeda, N. Miyajima, and K. Nagata. 2003. Measles virus V protein blocks interferon (IFN)-alpha/beta but not IFN-gamma signaling by inhibiting STAT1 and STAT2 phosphorylation. FEBS Lett. 545:177-182.
45. Thomas, S. M., R. A. Lamb, and R. G. Paterson. 1988. Two mRNAs that differ by two nontemplated nucleotides encode the amino coterminal proteins P and V of the paramyxovirus SV5. Cell 54:891-902.
46. Ulane, C. M., and C. M. Horvath. 2002. Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 304:160-166.
47. Ulane, C. M., J. J. Rodriguez, J. P. Parisien, and C. M. Horvath. 2003. STAT3 ubiquitylation and degradation by mumps virus suppress cytokine and oncogene signaling. J. Virol. 77:6385-6393.
48. 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.