The conserved carboxyl terminus of human parainfluenza virus type 2 V protein plays an important role in virus growth

Virology

Volumn 362, Issue 1, 2007, Pages 85-98

  Nishio, Machiko ^a   Tsurudome, Masato ^a   Ishihara, Hisamitsu ^b   Ito, Morihiro ^c   Ito, Yasuhiko ^c  

^a MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c CHUBU UNIVERSITY   (Japan)

Author keywords

Human parainfluenza virus type 2; V protein; Virus growth

Indexed keywords

INTERFERON; NUCLEOCAPSID PROTEIN; PROTEIN AIP1; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN V;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GROWTH INHIBITION; HELA CELL; HUMAN; HUMAN CELL; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PARAINFLUENZA VIRUS 2; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIROGENESIS; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; GENETIC COMPLEMENTATION TEST; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOPROTEINS; PARAINFLUENZA VIRUS 2, HUMAN; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; VERO CELLS; VIRAL PROTEINS;

HUMAN PARAINFLUENZA VIRUS 2;

EID: 34247253019     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.12.017     Document Type: Article

References (72)

1. Andrejeva J., Poole E., Young D.F., Goodbourn S., and Randall R.E. The p127 subunit (DDB1) of the UV-DNA damage repair binding protein is essential for the targeted degradation of STAT1 by the V protein of the paramyxovirus simian virus 5. J. Virol. 76 (2002) 11379-11386
2. Andrejeva J., Childs K.S., Young D.F., Carlos T.S., Stock N., Goodbourn S., and Randall R.E. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-β promoter. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 17264-17269
3. Delenda C., Hausmann S., Garcin D., and Kolalofsky D. Normal cellular replication of Sendai virus without the trans-frame, nonstructural V protein. Virology 228 (1997) 55-62
4. Didcock L., Young D.F., Goodbourn S., and Randall R.E. Sendai virus and simian virus 5 block activation of interferon-responsive genes: importance for virus pathogenesis. J. Virol. 73 (1999) 3125-3133
5. Didcock L., Young D.F., Goodbourn S., and Randall R.E. The V protein of simian virus 5 inhibits interferon signaling by targeting STAT1 for protease-mediated degradation. J. Virol. 73 (1999) 9928-9933
6. Garcin D., Latorre P., and Kolakofsky D. Sendai virus C proteins counteract the interferon-mediated induction of an antiviral state. J. Virol. 73 (1999) 6559-6565
7. Garcin D., Curran J., and Kolakofsky D. Sendai virus C proteins must interact directly with cellular components to interfere with interferon action. J. Virol. 74 (2000) 8823-8830
8. Garcin D., Marq J.B., Strahle L., Le Mercier P., and Kolakofsky D. All four Sendai virus C proteins bind Stat1, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295 (2002) 256-265
9. Gotoh B., Takeuchi K., Komatsu T., Yokoo J., Kimura Y., Kurotani A., Kato A., and Nagai Y. Knockout of the Sendai virus C gene eliminates the viral ability to prevent the interferon-alpha/beta-mediated responses. FEBS Lett. 459 (1999) 205-210
10. Gotoh B., Takeuchi K., Komatsu T., and Yokoo J. The STAT2 activation process is a crucial target of Sendai virus C protein for the blockade of alpha interferon signaling. J. Virol. 77 (2003) 3360-3370
11. He B., Paterson R.G., Stock N., Durbin J.E., Durbin R.K., Goodbourn S., Randall R.E., and Lamb R.A. 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 (2002) 15-32
12. Horikami A.M., Smallwood S., and Moyer S.A. The Sendai virus V protein interacts with the NP protein to regulate viral genome RNA replication. Virology 222 (1996) 383-390
13. Huang Z., Krishnamurthy S., Panda A., and Samal S.K. Newcastle disease virus V protein is associated with viral pathogenesis and functions as an alpha interferon antagonist. J. Virol. 77 (2003) 8676-8685
14. Kato A., Kiyotani K., Sakai Y., Yoshida T., and Nagai Y. The paramyxovirus Sendai virus V protein encodes a luxury function required for virus pathogenesis. EMBO J. 16 (1997) 578-587
15. Kato A., Ohnishi Y., Kohase M., Saito S., Tashiro M., and Nagai Y. Y2 the smallest of the Sendai virus C proteins, is fully capable of both counteracting the antiviral action of interferons and inhibiting virus RNA synthesis. J. Virol. 75 (2001) 3802-3810
16. Kawano M., Tsurudome M., Oki N., Nishio M., Komada H., Matsumura H., Kusagawa S., Ohta H., and Ito Y. Sequence determination of the P gene of simian virus 41: presence of irregular deletions near the RNA-editing sites of paramyxoviruses. J. Gen. Virol. 74 (1993) 911-916
17. Kawano M., Kaito M., Kozuka Y., Komada H., Noda N., Nanba K., Tsurudome M., Ito M., Nishio M., and Ito Y. 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 (2001) 99-112
18. Komatsu T., Takeuchi K., Yokoo Y., and Gotoh B. Sendai virus blocks alpha interferon signaling to signal transducers and activators of transcription. J. Virol. 74 (2000) 2477-2480
19. Kondo K., Bando H., Tsurudome M., Kawano M., Nishio M., and Ito Y. Sequence analysis of the phosphoprotein (P) genes of human parainfluenza type 4A and 4B viruses and RNA editing at transcript of the P genes: the number of G residues added is imprecise. Virology 178 (1990) 321-326
20. Koyama A.H., Irie H., Kato A., Nagai Y., and Adachi A. Virus multiplication and induction of apoptosis by Sendai virus: role of the C proteins. Microbes Infect. 5 5 (2003) 373-378
21. Kubota T., Yokosawa N., Yokota S., and Fujii N. C terminal CYS-RICH region of mumps virus structural V protein correlates with block of interferon alpha and gamma signal transduction pathway through decrease of STAT 1-alpha. Biochem. Biophys. Res. Commun. 283 (2001) 255-259
22. Kurotani A., Kiyotani K., Kato A., Shioda T., Sakai Y., Mizumoto K., Yoshida T., and Nagai Y. Sendai virus C proteins are categorically nonessential gene products but silencing their expression severely impairs viral replication and pathogenesis. Genes Cells 3 (1998) 111-124
23. Lamb R.A., and Kolakofsky D. Paramyxoviridae: the viruses and their replication. In: Fields B., Knipe D., and Howley P. (Eds). Virology. 4th ed. (2001), Lippincott-Raven Publishers
24. Leung S., Qureshi S.A., Kerr I.M., Darnell Jr. J.E., and Stark G.R. Role of STAT2 in the alpha interferon signaling pathway. Mol. Cell. Biol. 15 (1995) 1312-1317
25. Li T., Chen X., Garbutt K.C., Zhou P., and Zheng N. Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124 (2006) 105-117
26. Lin G.Y., Paterson R.G., Richardson C.D., and Lamb R.A. The V protein of the paramyxovirus SV5 interacts with damage-specific DNA binding protein. Virology 249 (1998) 189-200
27. Lin Y., Horvath F., Aligo J.A., Wilson R., and He B. The role of simian virus 5 V protein on viral RNA synthesis. Virology 338 (2005) 270-280
28. Malur A.G., Chattopadhyay S., Maitra R.K., and Banerjee A.K. Inhibition of STAT1 phosphorylation by human parainfluenza virus type 3 C protein. J. Virol. 79 (2005) 7877-7882
29. McKendry R., John J., Flavell D., Muller M., Kerr I.M., and Stark G.R. High-frequency mutagenesis of human cells and characterization of a mutant unresponsive to both alpha and gamma interferons. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 11455-11459
30. Mebatsion T., Verstegen S., De Veen L.T.C., Romer-Oberdorfer A., and Schrier C.C. A recombinant Newcastle disease virus with low-level V protein expression is immunogenic and lacks pathogenicity for chicken embryos. J. Virol. 75 (2001) 420-428
31. Missotten M., Nichols A., Rieger K., and Sadoul R. Alix, a novel mouse protein undergoing calcium-dependent interaction with the apoptosis-linked-gene-2 (ALG-2) protein. Cell Death Differ. 6 (1999) 124-129
32. Muller M., Laxton C., Briscoe J., Schindler C., Improta T., Darnell Jr. J.E., Stark G.R., and Kerr I.M. Complementation of a mutant cell line: central role of the 91-kDa polypeptide of ISGF3 in the interferon-α and γ signal transduction pathway. EMBO J. 12 (1993) 4221-4228
33. Nishio M., Tsurudome M., Kawano M., Watanabe N., Ohgimoto S., Ito M., Komada H., and Ito Y. Interaction between nucleocapsid protein (NP) and phosphoprotein (P) of human parainfluenza virus type 2: one of the two NP binding sites on P is essential for granule formation. J. Gen. Virol. 77 (1996) 2457-2463
34. Nishio M., Tsurudome M., Ito M., Watanabe N., Kawano M., Komada H., and Ito Y. Human parainfluenza virus type 2 phosphoprotein: mapping of monoclonal antibody epitopes and location of the multimerization domain. J. Gen. Virol. 77 (1997) 2457-2463
35. Nishio M., Tsurudome M., Ito M., Kawano M., Kusagawa S., Komada H., and Ito Y. Isolation of monoclonal antibodies directed against the V protein of human parainfluenza virus type 2 and localization of the V protein in virus-infected cells. Med. Microbiol. Immunol. 188 (1999) 79-82
36. Nishio M., Tsurudome M., Ito M., Kawano M., Kusagawa S., Komada H., and Ito Y. Mapping of domains on the human parainfluenza virus type 2 nucleocapsid protein (NP) required for NP-phosphoprotein or NP-NP interaction. J. Gen. Virol. 80 (1999) 2017-2022
37. Nishio M., Tsurudome M., Ito M., Kawano M., Komada H., and Ito Y. High resistance of human parainfluenza type 2 virus protein-expressing cells to the antiviral and anti-cell proliferative activities of alpha/beta interferons: cysteine-rich V-specific domain is required for high resistance to the interferons. J. Virol. 75 (2001) 9165-9176
38. Nishio M., Garcin D., Simonet V., and Kolakofsky D. The carboxyl segment of the mumps virus V protein associates with Stat proteins in vitro via a tryptophan-rich motif. Virology 300 (2002) 92-99
39. Nishio M., Tsurudome M., Ito M., and Ito Y. Human parainfluenza virus type 4 is incapable of evading the interferon-induced antiviral effect. J. Virol. 79 (2005) 14756-14768
40. Nishio M., Tsurudome M., Ito M., Garcin D., Kolakofsky D., and Ito Y. Identification of paramyxovirus V protein residues essential for STAT protein degradation and promotion of virus replication. J. Virol. 79 (2005) 8591-8601
41. Nishio M., Tsurudome M., Ito M., and Ito Y. Identification of RNA-binding regions on the P and V proteins of human parainfluenza virus type 2. Med. Microbiol. Immunol. 195 (2006) 29-36
42. Ohgimoto S., Bando H., Kawano M., Okamoto K., Kondo K., Tsurudome M., Nishio M., and Ito Y. Sequence analysis of P gene of human parainfluenza type 2 virus: P and cysteine-rich proteins are translated by two mRNAs that differ by two nontemplated G residues. Virology 177 (1990) 116-123
43. Palosaari H., Parisien J.-P., Rodriguez J.J., Ulane C.M., and Horvath C.M. STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J. Virol. 77 (2003) 7635-7644
44. Parisien J.-P., Lau J.F., Rodriguez J.J., Sullivan B.M., Moscona A., Parks G.D., Lamb R.A., and Horvath C.M. The V protein of human parainfluenza virus 2 antagonizes type I interferon responses by destabilizing signal transducer and activator of transcription 2. Virology 283 (2001) 230-239
45. Park M.S., Garcia-Sastre A., Cros J.F., Basler C.F., and Palese P. Newcastle disease virus V protein is a determinant of host range restriction. J. Virol. 77 (2003) 9522-9532
46. Paterson R.G., Leser G.P., Shqughnessy M.A., and Lamb R.A. The paramyxovirus SV5 V protein binds two atoms of zinc and is a structural component of virions. Virology 208 (1995) 121-131
47. Pellegrini S., Joh J., Shearer M., Kerr I.M., and Stark G.R. Use of a selectable marker regulated by alpha interferon to obtain mutations in the signaling pathway. Mol. Cell. Biol. 9 (1989) 4605-4612
48. Precious B., Young D.F., Bermingham A., Fearns R., Ryan M., and Randall R.E. Inducible expression of the, P, V and NP genes of the paramyxovirus SV5 in cell-lines and an examination of NP:P and NP:V interactions. J. Virol. 69 (1995) 8001-8010
49. Randall R.E., and Bermingham A. NP:P and NP:V interactions of the paramyxovirus simian virus 5 examined using a novel protein:protein capture assay. Virology 224 (1996) 121-129
50. Rodriguez J.J., Parisien J.-P., and Horvath C.M. Nipah virus V protein evades alpha and gamma interferons by preventing STAT1 and STAT2 activation and nuclear accumulation. J. Virol. 76 (2002) 11476-11483
51. Rodriguez J.J., Wang L.F., and Horvath C.M. Hendra virus V protein inhibits interferon signaling by preventing STAT1 and STAT2 nuclear accumulation. J. Virol. 77 (2003) 11842-11845
52. Sakaguchi T., Kato A., Sugahara F., Shimazu Y., Inoue M., Kiyotani K., Nagai Y., and Yoshida T. AIP1/Alix is a binding partner of Sendai virus C protein and facilitates virus budding. J. Virol. 79 (2005) 8933-8941
53. Schmitt A., Leser G.P., Waning D.L., and Lamb R.A. Requirements for budding of paramyxovirus simian virus 5 virus-like particles. J. Virol. 76 (2002) 3952-3964
54. Schmitt A., Leser G.P., Morita E., Sundquist W.I., and Lamb R.A. Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus. J. Virol. 79 (2005) 2988-2997
55. Schneider H., Kaelin K., and Billeter M.A. Recombinant measles viruses defective for RNA editing and V protein synthesis are viable in cultured cells. Virology 227 (1997) 314-322
56. Segura-Morales C., Pescia C., Chatellard-Casse C., Sadoul R., Bertrand E., and Basyuk E. Tsg101 and Alix interact with murine leukemia virus gag and cooperate with Nedd4 ubiquitin ligases during budding. J. Biol. Chem. 280 (2005) 27004-27012
57. Strack B., Calistri A., Craig S., Popova E., and Gottlinger H.G. AIP1/Alix is a binding partner for HIV-1 p6 and EIV p9 functioning in virus budding. Cell 114 (2003) 689-699
58. Sun M., Rothermel T.A., Shuman L., Aligo J.A., Xu S., Lin Y., Lamb R.A., and He B. Conserved cysteine-rich domain of paramyxovirus simian virus 5 V protein plays an important role in blocking apoptosis. J. Virol. 78 (2004) 5068-5078
59. Takebe Y., Seiki M., Fujisawa J., Hoy P., Yokota K., Arai K., Yoshida M., and Arai N. SR promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of the human T-cell leukemia virus type 1 long terminal repeat. Mol. Cell. Biol. 8 (1988) 466-472
60. 2+ concentration in the endoplasmic reticulum. FEBS Lett. 580 (2006) 5635-5640
61. Takeuchi K., Tanabayashi K., Hishiyama M., Yamada Y., Yamada A., and Sugiura A. Determination and characterization of mumps virus V protein. Virology 178 (1990) 247-253
62. Takeuchi K., Komatsu T., Yokoo J., Kato A., Shioda T., Nagai Y., and Gotoh B. Sendai virus C protein physically associates with Stat1. Genes cells 6 (2001) 545-557
63. Takeuchi K., Kadota S.I., Takeda M., Miyajima N., and Nagata K. Measles virus V protein blocks interferon (IFN)-alpha/beta but not IFN-gamma signaling by inhibiting STAT1 and STAT2 phosphorylation. FEBS Lett. 545 (2003) 177-182
64. Ulane C.M., and Horvath C.M. Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 304 (2002) 160-166
65. Ulane C.M., Rodriguez J.J., Parisien J.-P., and Horvath C.M. STAT3 ubiquitylation and degradation by mumps virus suppress cytokine and oncogene signaling. J. Virol. 77 (2003) 6385-6393
66. Ulane C.M., Kentsis A., Cruz C.D., Parisien J.-P., Schneider K., and Horvath C.M. Composition and assembly of STAT-targeting ubiquitin ligase complex: paramyxovirus V protein carboxyl terminus is an oligomerization domain. J. Virol. 79 (2005) 10180-10189
67. Valsamakis A., Schneider H., Auwaerter P.G., Kaneshima H., Billeter M.A., and Griffin D.G. Recombinant measles viruses with mutations in the C, V, or F gene have altered growth phenotypes in vivo. J. Virol. 72 (1998) 7754-7761
68. 2+-dependent reaction. J. Biol. Chem. 274 (1999) 1533-1540
69. Watanabe N., Kawano M., Tsurudome M., Kusagawa S., Nishio M., Komada H., Shima T., and Ito Y. Identification of the sequences responsible for nuclear targeting of the V protein of human parainfluenza type 2 virus. J. Gen.Virol. 77 (1996) 327-338
70. Watanabe N., Kawano M., Tsurudome M., Nishio M., Ito M., Ohgimoto S., Suga S., Komada H., and Ito Y. Binding of the V proteins to the nucleocapsid proteins of human parainfluenza type 2 virus. Med. Microbiol. Immunol. 185 (1996) 89-94
71. Yokosawa N., Yokota S., Kubota T., and Fujii N. C-terminal region of STAT-1α is not necessary for its ubiquitination and degradation caused by mumps virus V protein. J. Virol. 76 (2002) 12683-12690
72. Young D.F., Didcock L., Goodbourn S., and Randall R.E. Paramyxoviridae use distinct virus-specific mechanisms to circumvent the interferon response. Virology 269 (2000) 383-390