Association of influenza virus NP and M1 proteins with cellular cytoskeletal elements in influenza virus-infected cells

Journal of Virology

Volumn 71, Issue 4, 1997, Pages 2947-2958

  Avalos, Roy T ^a   Yu, Zhong ^a   Nayak, Debi P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 [(3 CHOLAMIDOPROPYL)DIMETHYLAMMONIO] 1 PROPANESULFONIC ACID; CYCLOHEXIMIDE; HEMAGGLUTININ; OCTYL GLUCOSIDE; RIBONUCLEOPROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL CLONE; CELL FRACTIONATION; CYTOSKELETON; HELA CELL; HOST CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; INFLUENZA VIRUS; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROTEIN ANALYSIS; VIRUS INFECTION;

EID: 0030966390     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.4.2947-2958.1997     Document Type: Article

References (77)

1. Barak, L. S., R. R. Yocum, E. A. Nothnagel, and W. W. Webb. 1980. Fluorescence staining of the actin cytoskeleton in living cells with 7-nitrobenz-2-Oxa-1,3-diazole-phallacidin. Proc. Natl. Acad. Sci. U.S.A. 77:980-984.
2. Baudin, F., C. Bach, S. Cusack, and R. W. H. Ruigrok. 1994. Structure of influenza virus RNP. I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent. EMBO J. 13:3158-3165.
3. Ben-Ze'ev, A., A. Duerr, F. Solomon, and S. Penman. 1979. The outer boundary of the cytoskeleton: a lamina derived from plasma membrane proteins. Cell 17:859-865.
4. Bohn, W., G. Rutter, H. Hohenberg, K. Mannweiler, and P. Nobis. 1986. Involvement of actin filaments in budding of measles virus: studies on cytoskeletons of infected cells. Virology 149:91-106.
5. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544.
6. Bucher, D., S. Popple, M. Baer, A. Mikhail, Y.-F. Gong, C. Whitaker, E. Paoletti, and A. Judd. 1989. M protein (M1) of influenza virus: antigenic analysis and intracellular localization with monoclonal antibodies. J. Virol. 63:3622-3633.
7. Cooper, J. A. 1987. Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105:1473-1478.
8. Cudmore, S., P. Cossart, G. Griffith, and M. Way. 1995. Actin-based motility of vaccinia virus. Nature 378:636-638.
9. Damsky, C. H., J. P. Sheffield, G. P. Tuszynski, and L. Warren. 1977. Is there a role for actin in virus budding? J. Cell Biol. 75:593-605.
10. Enami, M., and K. Enami. 1996. Influenza virus hcmagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein. J. Virol. 70:6653-6657.
11. Gaedigk-Nitschko, K., and M. J. Schlesinger. 1991. Site-directed mutations in Sindbis virus E2 glycoprotein's cytoplasmic domain and the 6K protein lead to similar defects in virus assembly and budding. Virology 183:206-214.
12. Giuffre, R. M., D. R. Tovell, C. M. Kay, and D. L. J. Tyrell. 1982. Evidence for an interaction between the membrane protein of a paramyxovirus and actin. J. Virol. 42:963-968.
13. Granoff, A., and D. W. Kingsbury. 1964. Effect of actinomycin D on the replication of Newcastle disease and influenza virus. Ciba Found. Symp. Cell. Biol. 1964:96-115.
14. Gregoriades, A., and B. Frangoine. 1981. Insertion of influenza virus M1 protein into the viral lipid bilayer and localization of site of insertion. J. Virol. 40:323-328.
15. Greenspan, D., P. Palese, and M. Krystal. 1988. Two nuclear localization signals in the influenza virus NS1 nonstructural protein. J. Virol. 62:3020-3026.
16. Griffin, J. A., and R. W. Compans. 1979. Effect of cytochalasin B on the maturation of enveloped viruses. J. Exp. Med. 150:379-391.
17. Griffiths, G., and P. Rottier. 1992. Cell biology of viruses that assemble along the biosynthetic pathway. Semin. Cell Biol. 3:367-381.
18. Gujuluva, C. N., A. Kundu, K. G. Murti, and D. P. Nayak. 1994. Abortive replication of influenza virus A/WSN/33 in HeLa 229 cells: defective membrane function during entry and budding processes. Virology 204:491-505.
19. Hay, A. J. 1974. Studies on the formation of the influenza virus envelope. Virology 60:398-418.
20. Heskett, J. E., and I. F. Pryme. 1991. Interaction between mRNA, ribosomes and the cytoskeleton. J. Biochem. 277:1-10.
21. Hiller, G., K. Weber, L. Schnieder, C. Parajsz, and C. Junwirth. 1979. Interaction of assembled progeny pox viruses with the cellular cytoskeleton. Virology 98:142-153.
22. Hovland, R., G. Campbell, I. Pryme, and J. Hesketh. 1995. The mRNA for cyclin A, c-myc and ribosomal protein L4 and S6 are associated with cytoskeletal-bound polysomes in HepG2 cells. J. Biochem. 310:193-196.
23. Hunter, E. 1994. Macromolecular interactions in the assembly of HIV and other retroviruses. Virology 5:71-83.
24. Kasaraatsu, H., W. Lin, J. Eden, and J. P. Revel. 1983. Visualization of antigens attached to cytoskeletal framework in animal cells: colocalization of simian virus 40 vp1 polypeptide and actin in TC7 cells. Proc. Natl. Acad. Sci. USA 80:4339-4343.
25. Klenk, H.-D., W. Wollert, R. Rott, and C. Scholtissek. 1974. Association of influenza virus proteins with cytoplasmic fractions. Virology 57:28-41.
26. Klymkowsky, M. W. 1995. Intermediate filaments: new proteins, some answers, more questions. Curr. Biol. 7:46-54.
27. Krug, R. M., M. Ueda, and P. Palese. 1975. Temperature-sensitive mutants of influenza WSN virus defective in virus-specific RNA synthesis. J. Virol. 16:790-796.
28. Kundu, A. K., R. T. Avalos, C. N. Sanderson, and D. P. Nayak. 1995. Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCKcells. J. Virol. 70:6508-6515.
29. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Lafont, F., J. K. Burkhard, and K. Simons. 1995. Involvement of microtubule motors in basolateral and apical transport in kidney cells. Nature 372: 801-803.
31. Lazarowitz, S. G., R. W. Compans, and P. W. Choppin. 1971. Influenza virus structural and nonstructural proteins in infected cells and their plasma membranes. Virology 46:830-843.
32. Li, R., P. Palese, and M. Krystal. 1989. Complementation and analysis of an NP mutant of influenza virus. Virus Res. 12:97-112.
33. Li, S., M. Xu, and K. Coelingh. 1995. Electroporation of influenza virus ribonucleoprotein complexes for rescue of the nucleoprotein and matrix genes. Virus Res. 37:153-161.
34. Liu, C., and G. M. Air. 1993. Selection and characterization of neuraminidase-minus mutant of influenza virus and its rescue by cloned neuraminidase genes. Virology 194:403-407.
35. Liu, C., M. C. Eichelberger, R. W. Compans, and G. M. Air. 1995. Influenza type A virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. J. Virol. 69:1099-1106.
36. Lohmeyer, J., L. T. Talens, and H.-D. Klenk. 1979. Biosynthesis of the influenza virus envelope in abortive infection. J. Gen. Virol. 42:73-88.
37. Low, S. H., B. L. Tang, S. H. Wong, and W. Hong. 1992. Selective inhibition of protein targeting to the apical domain of MDCK cells by brefeldin A. J. Cell Biol. 118:51-62.
38. Loza-Tulimowska, M., T. Michalak, and R. Semkow. 1981. Attempts at detection of actomyosin associated with influenza virus. Acta Virol. 25:251-253.
39. Luna, E. J., and A. L. Hitt. 1992. Cytoskeleton-plasma membrane interactions. Science 258:955-964.
40. Lydy, S. L., S. Basak, and R. W. Compans. 1990. Host cell-dependent lateral mobility of viral glycoproteins. Microb. Pathog. 9:375-386.
41. Melki, R., Y. Gaudin, and D. Blondel. 1994. Interaction between tubulin and the viral matrix protein of vesicular stomatitis virus: possible implications in the viral cytopathic effect. J. Virol. 202:339-347.
42. Mitnaul, L. J., M. R. Castrucci, K. G. Murti, and Y. Kowaoka. 1996. The cytoplasmic tail of influenza a virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication. J. Virol. 70:873-879.
43. Morrison, T. G., and L. J. McGinnes. 1985. Cytochalasin D accelerates the release of Newcastle disease virus from infected cells. Virus Res. 4:93-106.
44. Mortara, R. A., and G. I. E. Koch. 1989. An association between actin and nucleocapsid polypeptides in isolated murine retroviral particles. J. Submicrosc. Cytol. Patho. 21:295-306.
45. Murti, K. G., M. Chen, and R. Goorha. 1985. Interaction of frog virus 3 with the cytomatrix III. Role of microfilaments in virus release. Virology 142:317-325.
46. Naim, H. Y., and M. G. Roth. 1993. Basis of selective incorporation of glycoproteins into the influenza virus envelope. J. Virol. 67:4831-4841.
47. Nayak, D. P. 1996. A look at assembly and morphogenesis of orthomyxo-and paramyxoviruses. ASM News 62:411-414.
48. Nayak, D. P., and M. A. Jabbar. 1989. Structural domains and organizational conformation involved in sorting and transport of the influenza virus transmembrane proteins. Annu. Rev. Microbiol. 43:465-501.
49. Ojakian, G. K., and R. Schwimmor. 1988. The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells. J. Cell Biol. 107:2377-2387.
50. Patterson, S., J. Gross, and J. S. Oxford. 1988. The intracellular distribution of influenza virus matrix protein and nucleoprotein in infected cells and their relationship to hemagglutinin in the plasma membrane. J. Gen. Virol. 69: 1859-1872.
51. Pattnaik, A. K., D. J. Brown, and D. P. Nayak. 1986. Formation of influenza virus particles lacking hemagglutinin on the viral envelope. J. Virol. 60:994-1001.
52. Pearce-Pratt, R., D. Malamud, and D. M. Phillips. 1994. Role of the cytoskeleton in cell-to-cell transmission of human immunodeficiency virus. J. Virol. 68:2898-2905.
53. Perotti, M.-E., X. Tan, and D. M. Phillips. 1996. Directional budding of human immunodeficiency virus from monocytes. J. Virol. 70:5916-5921.
54. Pons, M. W. 1973. The inhibition of influenza virus RNA synthesis by actinomycin D and cycloheximide. Virology 51:120-128.
55. Rey, O., and D. P. Nayak. 1992. Nuclear retention of M1 protein via temperature-sensitive mutant of influenza virus (A/WSN/33) does not affect nuclear export of viral ribonucleoproteins. J. Virol. 66:5815-5824.
56. Rindler, M. J., I. E. Ivanov, and D. D. Sabatini. 1987. Microtubule-acting drugs lead to the nonpolarized delivery of the influenza hemagglutinin to the cell surface of polarized Madin-Darby canine kidney cells. J. Cell Biol. 104:231-241.
57. Rutter, G., and K. Mannweiler. 1977. Alterations of actin-containing structures in BHK21 cells infected with Newcastle disease virus and vesicular stomatitis virus. J. Gen. Virol. 37:233-242.
58. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
59. Sanders, M. C., and Y.-I. Wang. 1990. Exogenous nucleation sites fail to induce detectable polymerization of actin in living cells. J. Cell Biol. 110: 359-365.
60. Sanderson, C. M., R. Avalos, A. Kundu, and D. P. Nayak. 1995. Interaction of Sendai viral F, HN, and M protein cytoskeletal and lipid components in Sendai virus-infected BHK ceils. Virology 209:701-707.
61. Sanderson, C. M., H.-H. Wu, and D. P. Nayak. 1994. Sendai virus M protein binds independently to either the F or the HN glyeoprotein in vivo. J. Virol. 68:69-76.
62. Scholtissek, C., and R. Rott. 1970, Synthesis in vivo of influenza virus plus and minus strand RNA and its preferential inhibition by antibiotics. Virology 40:989-996.
63. Scholtissek, C., R. Kruczina, R. Rott, and H.-D. Klenk. 1974. Characteristics of an influenza mutant temperature-sensitive for viral RNA synthesis. Virology 58:317-322.
64. Sheshberadaran, H., and R. A. Lamb. 1991. Simian virus 5 membrane protein maturation: expression in virus-infected cells and from an eukaryotic vector. Virology 183:803-809.
65. Skehel, J. J. 1973. Early polypeptide synthesis in influenza virus-infected cells. Virology 56:394-399.
66. Skibbens, J. E., M. G. Roth, and K. S. Matlin. 1989. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts. J. Cell Biol. 108:821-832.
67. Stephen, J. N., and C. M. Isacke. 1993. The cytoplasmic tail of CD44 is required for basolateral localization in epithelial MDCK cells but does not mediate association with the detergent-insoluble cytoskeleton of fibroblasts. J. Cell Biol. 121:1299-1310.
68. Sun, H-Q., K. Kwiatkowska, and H. L. Yin. 1995. Actin monomer binding proteins. Curr. Biol. 7:102-110.
69. Sundell, C. L., and R. H. Singer. 1991. Requirement of microfilaments in sorting of actin messenger RNA. 253:1275-1277.
70. Sveda, M. M., L. J. Markoff, and C.-J. Lai. 1984. Influenza virus hemagglutinin containing an altered hydrophobic carboxy terminus accumulates intracellularty. J. Virol. 49:223-228.
71. Tashiro, M., J. T. Seto, H.-D. Klenk, and R. Roll. 1993. Possible involvement of microtubule disruption in bipolar budding of a Sendai virus mutant, F1-R, in epithelial MDCK cells. J. Virol._67:5902-5910.
72. Whittaker, G., M. Bui, and A. Helenius. 1996. Nuclear trafficking of influenza virus ribonucleoprotein in heterokaryons. J. Virol. 70:2743-2756.
73. Whittaker, G., I. Kemler, and A. Helenius. 1995. Hyperphosphorylation of mutant influenza virus matrix protein, M1, causes its retention in the nucleus. J. Virol. 69:439-445.
74. Yasuda, J., D. J. Bucher, and A. Ishihama.1994. Growth control of influenza A virus by M1 protein: analysis of transfectant viruses carrying the chimeric M gene. J. Virol. 68:8141-8146.
75. 1) of influenza virus. J. Virol. 69:1964-1970.
76. Zhang, J., and R. A. Lamb. 1996. Characterization of membrane association of the influenza virus matrix protein in living cell. Virology 225:255-266.
77. Zhirnov, O. P. 1992. Isolation of matrix protein M1 from influenza viruses by acid-dependent extraction with nonionic detergent. Virology 186:324-330.