Mumps virus matrix, fusion, and nucleocapsid proteins cooperate for efficient production of virus-like particles

Journal of Virology

Volumn 83, Issue 14, 2009, Pages 7261-7272

  Li, Ming ^a   Schmitt, Phuong Tieu ^a   Li, Zhuo ^a   McCrory, Thomas S ^a   He, Biao ^a   Schmitt, Anthony P ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HN PROTEIN; HYBRID PROTEIN; MATRIX PROTEIN; NUCLEOCAPSID PROTEIN; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE DISRUPTION; GENE SEQUENCE; HUMAN; HUMAN CELL; MUMPS VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAINFLUENZA VIRUS; PARAINFLUENZA VIRUS 5; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; VIRION; VIRUS LIKE AGENT; VIRUS MORPHOLOGY;

CELL LINE; HUMANS; MUMPS; MUMPS VIRUS; NUCLEOCAPSID PROTEINS; VIRAL FUSION PROTEINS; VIRAL MATRIX PROTEINS; VIRION; VIRUS ASSEMBLY;

MAMMALIA; MUMPS VIRUS; PARAINFLUENZA VIRUS; PARAMYXOVIRIDAE;

EID: 67650407490     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00421-09     Document Type: Article

References (67)

1. Bieniasz, P. D. 2006. Late budding domains and host proteins in enveloped virus release. Virology 344:55-63.
2. Buchholz, C. J., D. Spehner, R. Drillien, W. J. Neubert, and H. E. Homann. 1993. The conserved N-terminal region of Sendai virus nucleocapsid protein NP is required for nucleocapsid assembly. J. Virol. 67:5803-5812.
3. Calistri, A., C. Salata, C. Parolin, and G. Palù. 2009. Role of multivesicular bodies and their components in the egress of enveloped RNA viruses. Rev. Med. Virol. 19:31-45.
4. Cathomen, T., H. Y. Naim, and R. Cattaneo. 1998. Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J. Virol. 72:1224-1234.
5. Cattaneo, R., A. Schmid, D. Eschle, K. Baczko, V. ter Meulen, and M. A. Billeter. 1988. Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 55:255-265.
6. CDC. 2006. Mumps epidemic - United kingdom, 2004-2005. MMWR Morb. Mortal. Wkly. Rep. 55:173-175.
7. CDC. 2006. Update: multistate outbreak of mumps - United States, January 1-May 2, 2006. MMWR Morb. Mortal. Wkly. Rep. 55:559-563.
8. Chen, B. J., and R. A. Lamb. 2008. Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372:221-232.
9. Chen, B. J., G. P. Leser, E. Morita, and R. A. Lamb. 2007. Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J. Virol. 81:7111-7123.
10. Chen, M., T. Ogino, and A. K. Banerjee. 2007. Interaction of vesicular stomatitis virus P and N proteins: identification of two overlapping domains at the N terminus of P that are involved in N0-P complex formation and encapsidation of viral genome RNA. J. Virol. 81:13478-13485.
11. Ciancanelli, M. J., and C. F. Basler. 2006. Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. J. Virol. 80:12070-12078.
12. Coronel, E. C., K. G. Murti, T. Takimoto, and A. Portner. 1999. Human parainfluenza virus type 1 matrix and nucleoprotein genes transiently expressed in mammalian cells induce the release of virus-like particles containing nucleocapsid-like structures. J. Virol. 73:7035-7038.
13. Curran, J., J. B. Marq, and D. Kolakofsky. 1995. An N-terminal domain of the Sendai paramyxovirus P protein acts as a chaperone for the NP protein during the nascent chain assembly step of genome replication. J. Virol. 69:849-855.
14. Dayan, G. H., M. P. Quinlisk, A. A. Parker, A. E. Barskey, M. L. Harris, J. M. Schwartz, K. Hunt, C. G. Finley, D. P. Leschinsky, A. L. O'Keefe, J. Clayton, L. K. Kightlinger, E. G. Dietle, J. Berg, C. L. Kenyon, S. T. Goldstein, S. K. Stokley, S. B. Redd, P. A. Rota, J. Rota, D. Bi, S. W. Roush, C. B. Bridges, T. A. Santibanez, U. Parashar, W. J. Bellini, and J. F. Seward. 2008. Recent resurgence of mumps in the United States. N. Engl. J. Med. 358: 1580-1589.
15. Duc-Nguyen, H., and E. N. Rosenblum. 1967. Immuno-electron microscopy of the morphogenesis of mumps virus. J. Virol. 1:415-429.
16. Errington, W., and P. T. Emmerson. 1997. Assembly of recombinant Newcastle disease virus nucleocapsid protein into nucleocapsid-like structures is inhibited by the phosphoprotein. J. Gen. Virol. 78:2335-2339.
17. Fouillot-Coriou, N., and L. Roux. 2000. Structure-function analysis of the Sendai virus F and HN cytoplasmic domain: different role for the two proteins in the production of virus particle. Virology 270:464-475.
18. Garrus, J. E., U. K. von Schwedler, O. W. Pornillos, S. G. Morham, K. H. Zavitz, H. E. Wang, D. A. Wettstein, K. M. Stray, M. Côté, R. L. Rich, D. G. Myszka, and W. I. Sundquist. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55-65.
19. Gosselin-Grenet, A. S., J. B. Marq, L. Abrami, D. Garcin, and L. Roux. 2007. Sendai virus budding in the course of an infection does not require Alix and VPS4A host factors. Virology 365:101-112.
20. Harty, R. N., M. E. Brown, G. Wang, J. M. Huibregtse, and F. P. Hayes. 2000. A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proc. Natl. Acad. Sci. USA 97:13871-13876.
21. Horne, R., A. Waterson, P. Wildy, and A. Farnham. 1960. The structure and composition of the myxoviruses. I. Electron microscope studies of the structure of myxovirus particles by negative staining techniques. Virology 11: 79-98.
22. Hviid, A., S. Rubin, and K. Mühlemann. 2008. Mumps. Lancet 371:932-944.
23. Irie, T., J. M. Licata, J. P. McGettigan, M. J. Schnell, and R. N. Harty. 2004. Budding of PPxY-containing rhabdoviruses is not dependent on host proteins TGS101 and VPS4A. J. Virol. 78:2657-2665.
24. Irie, T., N. Nagata, T. Yoshida, and T. Sakaguchi. 2008. Recruitment of Alix/AIP1 to the plasma membrane by Sendai virus C protein facilitates budding of virus-like particles. Virology 371:108-120.
25. Irie, T., Y. Shimazu, T. Yoshida, and T. Sakaguchi. 2007. The YLDL sequence within Sendai virus M protein is critical for budding of virus-like particles and interacts with Alix/AIP1 independently of C protein. J. Virol. 81:2263-2273.
26. Jin, H., G. P. Leser, J. Zhang, and R. A. Lamb. 1997. Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J. 16:1236-1247.
27. Justice, P. A., W. Sun, Y. Li, Z. Ye, P. R. Grigera, and R. R. Wagner. 1995. Membrane vesiculation function and exocytosis of wild-type and mutant matrix proteins of vesicular stomatitis virus. J. Virol. 69:3156-3160.
28. Kaletsky, R. L., J. R. Francica, C. Agrawal-Gamse, and P. Bates. 2009. Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc. Natl. Acad. Sci. USA 106:2886-2891.
29. Kubota, T., N. Yokosawa, S. Yokota, and N. Fujii. 2001. C terminal CYSRICH 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. 283:255-259.
30. Kubota, T., N. Yokosawa, S. Yokota, N. Fujii, M. Tashiro, and A. Kato. 2005. Mumps virus V protein antagonizes interferon without the complete degradation of STAT1. J. Virol. 79:4451-4459.
31. Licata, J. M., R. F. Johnson, Z. Han, and R. N. Harty. 2004. Contribution of Ebola virus glycoprotein, nucleoprotein, and VP24 to budding of VP40 virus-like particles. J. Virol. 78:7344-7351.
32. Licata, J. M., M. Simpson-Holley, N. T. Wright, Z. Han, J. Paragas, and R. N. Harty. 2003. Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4. J. Virol. 77:1812-1819.
33. Masters, P. S., and A. K. Banerjee. 1988. Complex formation with vesicular stomatitis virus phosphoprotein NS prevents binding of nucleocapsid protein N to nonspecific RNA. J. Virol. 62:2658-2664.
34. Mebatsion, T., M. Konig, and K. K. Conzelmann. 1996. Budding of rabies virus particles in the absence of the spike glycoprotein. Cell 84:941-951.
35. Moll, M., H. D. Klenk, and A. Maisner. 2002. Importance of the cytoplasmic tails of the measles virus glycoproteins for fusogenic activity and the generation of recombinant measles viruses. J. Virol. 76:7174-7186.
36. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199.
37. Pantua, H. D., L. W. McGinnes, M. E. Peeples, and T. G. Morrison. 2006. Requirements for the assembly and release of Newcastle disease virus-like particles. J. Virol. 80:11062-11073.
38. Patch, J. R., G. Crameri, L. F. Wang, B. T. Eaton, and C. C. Broder. 2007. Quantitative analysis of Nipah virus proteins released as virus-like particles reveals central role for the matrix protein. Virol. J. 4:1.
39. Patch, J. R., Z. Han, S. E. McCarthy, L. Yan, L. F. Wang, R. N. Harty, and C. C. Broder. 2008. The YPLGVG sequence of the Nipah virus matrix protein is required for budding. Virol. J. 5:137.
40. Peltola, H., P. S. Kulkarni, S. V. Kapre, M. Paunio, S. S. Jadhav, and R. M. Dhere. 2007. Mumps outbreaks in Canada and the United States: time for new thinking on mumps vaccines. Clin. Infect. Dis. 45:459-466.
41. Perez, M., R. C. Craven, and J. C. de la Torre. 2003. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc. Natl. Acad. Sci. USA 100:12978-12983.
42. Pohl, C., W. P. Duprex, G. Krohne, B. K. Rima, and S. Schneider-Schaulies. 2007. Measles virus M and F proteins associate with detergent-resistant membrane fractions and promote formation of virus-like particles. J. Gen. Virol. 88:1243-1250.
43. Portner, A., R. A. Scroggs, P. S. Marx, and D. W. Kingsbury. 1975. A temperature-sensitive mutant of Sendai virus with an altered hemagglutinin-neuraminidase polypeptide: consequences for virus assembly and cytopathology. Virology 67:179-187.
44. Randall, R. E., D. F. Young, K. K. Goswami, and W. C. Russell. 1987. Isolation and characterization of monoclonal antibodies to simian virus 5 and their use in revealing antigenic differences between human, canine and simian isolates. J. Gen. Virol. 68:2769-2780.
45. Roy, P., and R. Noad. 2008. Virus-like particles as a vaccine delivery system: myths and facts. Hum. Vaccin. 4:5-12.
46. Sakaguchi, T., A. Kato, F. Sugahara, Y. Shimazu, M. Inoue, K. Kiyotani, Y. Nagai, and T. Yoshida. 2005. AIP1/Alix is a binding partner of Sendai virus C protein and facilitates virus budding. J. Virol. 79:8933-8941.
47. Schmid, A., P. Spielhofer, R. Cattaneo, K. Baczko, V. ter Meulen, and M. A. Billeter. 1992. Subacute sclerosing panencephalitis is typically characterized by alterations in the fusion protein cytoplasmic domain of the persisting measles virus. Virology 188:910-915.
48. Schmitt, A. P., B. He, and R. A. Lamb. 1999. Involvement of the cytoplasmic domain of the hemagglutinin-neuraminidase protein in assembly of the paramyxovirus simian virus 5. J. Virol. 73:8703-8712.
49. Schmitt, A. P., and R. A. Lamb. 2004. Escaping from the cell: assembly and budding of negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283:145-196.
50. Schmitt, A. P., G. P. Leser, E. Morita, W. I. Sundquist, and R. A. Lamb. 2005. Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus. J. Virol. 79:2988-2997.
51. Schmitt, A. P., G. P. Leser, D. L. Waning, and R. A. Lamb. 2002. Requirements for budding of paramyxovirus simian virus 5 virus-like particles. J. Virol. 76:3952-3964.
52. Schnell, M. J., L. Buonocore, E. Boritz, H. P. Ghosh, R. Chernish, and J. K. Rose. 1998. Requirement for a non-specific glycoprotein cytoplasmic domain sequence to drive efficient budding of vesicular stomatitis virus. EMBO J. 17:1289-1296.
53. Spehner, D., A. Kirn, and R. Drillien. 1991. Assembly of nucleocapsidlike structures in animal cells infected with a vaccinia virus recombinant encoding the measles virus nucleoprotein. J. Virol. 65:6296-6300.
54. Studier, F. W. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41:207-234.
55. Sugahara, F., T. Uchiyama, H. Watanabe, Y. Shimazu, M. Kuwayama, Y. Fujii, K. Kiyotani, A. Adachi, N. Kohno, T. Yoshida, and T. Sakaguchi. 2004. Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein. Virology 325:1-10.
56. Takimoto, T., K. G. Murti, T. Bousse, R. A. Scroggs, and A. Portner. 2001. Role of matrix and fusion proteins in budding of Sendai virus. J. Virol. 75:11384-11391.
57. Takimoto, T., and A. Portner. 2004. Molecular mechanism of paramyxovirus budding. Virus Res. 106:133-145.
58. Tao, T., A. P. Durbin, S. S. Whitehead, F. Davoodi, P. L. Collins, and B. R. Murphy. 1998. Recovery of a fully viable chimeric human parainfluenza virus (PIV) type 3 in which the hemagglutinin-neuraminidase and fusion glycoproteins have been replaced by those of PIV type 1. J. Virol. 72:2955-2961.
59. Tao, T., M. H. Skiadopoulos, F. Davoodi, J. M. Riggs, P. L. Collins, and B. R. Murphy. 2000. Replacement of the ectodomains of the hemagglutinin-neuraminidase and fusion glycoproteins of recombinant parainfluenza virus type 3 (PIV3) with their counterparts from PIV2 yields attenuated PIV2 vaccine candidates. J. Virol. 74:6448-6458.
60. Teng, M. N., and P. L. Collins. 1998. Identification of the respiratory syncytial virus proteins required for formation and passage of helper-dependent infectious particles. J. Virol. 72:5707-5716.
61. Timmins, J., S. Scianimanico, G. Schoehn, and W. Weissenhorn. 2001. Vesicular release of Ebola virus matrix protein VP40. Virology 283:1-6.
62. 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.
63. Urata, S., T. Noda, Y. Kawaoka, H. Yokosawa, and J. Yasuda. 2006. Cellular factors required for Lassa virus budding. J. Virol. 80:4191-4195.
64. Utley, T. J., N. A. Ducharme, V. Varthakavi, B. E. Shepherd, P. J. Santangelo, M. E. Lindquist, J. R. Goldenring, and J. E. Crowe, Jr. 2008. Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2. Proc. Natl. Acad. Sci. USA 105:10209-10214.
65. von Schwedler, U. K., M. D. Stuchell, B. Müller, D. M. Ward, H. Y. Chung, E. Morita, H. E. Wang, T. Davis, G. P. He, D. M. Cimbora, A. Scott, H. G. Krausslich, J. Kaplan, S. G. Morham, and W. I. Sundquist. 2003. The protein network of HIV budding. Cell 114:701-713.
66. Waning, D. L., A. P. Schmitt, G. P. Leser, and R. A. Lamb. 2002. Roles for the cytoplasmic tails of the fusion and hemagglutinin-neuraminidase proteins in budding of the paramyxovirus simian virus 5. J. Virol. 76:9284-9297.
67. Wilson, R. L., S. M. Fuentes, P. Wang, E. C. Taddeo, A. Klatt, A. J. Henderson, and B. He. 2006. Function of small hydrophobic proteins of paramyxovirus. J. Virol. 80:1700-1709.