Influenza A virus can undergo multiple cycles of replication without M2 Ion channel activity

Journal of Virology

Volumn 75, Issue 12, 2001, Pages 5656-5662

  Watanabe, Tokiko ^a,b   Watanabe, Shinji ^a   Ito, Hiroshi ^a   Kida, Hiroshi ^b   Kawaoka, Yoshihiro ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; ION CHANNEL; MUTANT PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSAY; CELL CULTURE; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; FEMALE; INFLUENZA VIRUS A; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; VIROGENESIS; VIRUS REPLICATION;

ANIMALS; CELL LINE; HUMANS; INFLUENZA A VIRUS; ION CHANNELS; MALE; MICE; MICE, INBRED BALB C; MUTATION; ORTHOMYXOVIRIDAE INFECTIONS; PLASMIDS; TRANSFECTION; VIRAL MATRIX PROTEINS; VIRION; VIRUS REPLICATION;

EID: 0035017262     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.75.12.5656-5662.2001     Document Type: Article

References (54)

1. Alberts, B., D. Bray, J. Lewis, M. Raff, K. Roberts, and J. D. Watson (ed.). 1994. Molecular biology of the cell. Garland Publishing, Inc., New York, N.Y.
2. Appleyard, G. 1977. Amantadine-resistance as a genetic marker for influenza viruses. J. Gen. Virol. 36:249-255.
3. Bilsel, P., M. R. Castrucci, and Y. Kawaoka. 1993. Mutations in the cytoplasmic tail of influenza A virus neuraminidase affect incorporation into virions. J. Virol. 67:6762-6767.
4. Castrucci, M. R., and Y. Kawaoka. 1995. Reverse genetics system for generation of an influenza A virus mutant containing a deletion of the carboxyl-terminal residue of M2 protein. J. Virol. 69:2725-2728.
5. Cohen, E. A., E. F. Terwilliger, J. G. Sodroski, and W. A. Haseltine. 1988 Identification of a protein encoded by the vpu gene of HIV-1. Nature 334:532-534.
6. Cox, N. J., F. Kitame, A. P. Kendal, H. F. Maassab, and C. Naeve. 1988. Identification of sequence changes in the cold-adapted, live attenuated influenza vaccine strain, A/Ann Arbor/6/60 (H2N2). Virology 167:554-567.
7. Daniels, R. S., J. C. Downie, A. J. Hay, M. Knossow, J. J. Skehel, M. L. Wang, and D. C. Wiley. 1985. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 40:431-439.
8. Dedera, D., W. Hu, H. Vander Heyden, and L. Ratner. 1989. Viral protein R of human immunodeficiency virus types 1 and 2 is dispensable for replication and cytopathogenicity in lymphoid cells. J. Virol. 63:3205-3208.
9. DuBridge, R. B., P. Tang, H. C. Hsia, P. M. Leong, J. H. Miller, and M. P. Calos. 1987. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7:379-387.
10. Duff, K. C., and R. H. Ashley. 1992. The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers. Virology 190:485-489.
11. Duff, K. C., S. M. Kelly, N. C. Price, and J. P. Bradshaw. 1992. The secondary structure of influenza A M2 transmembrane domain. FEBS Lett. 311: 256-258.
12. Ewart, G. D., T. Sutherland, P. W. Gage, and G. B. Cox. 1996. The Vpu protein of human immunodeficiency virus type 1 forms cation-selective ion channels. J. Virol. 70:7108-7115.
13. Fodor, E., L. Devenish, O. G. Engelhardt, P. Palese, G. G. Brownlee, and A. Garcia-Sastre. 1999. Rescue of influenza A virus from recombinant DNA. J. Virol. 73:9679-9682.
14. Grambas, S., M. S. Bennett, and A. J. Hay. 1992. Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A viruses. Virology 190:541-549.
15. Hay, A. J., A. J. Wolstenholme, J. J. Skehel, and M. H. Smith. 1985. The molecular basis of the specific anti-influenza action of amantadine. EMBO J. 4:3021-3024.
16. Helenius, A. 1992. Unpacking the incoming influenza virus. Cell 69:577-578.
17. Herlocher, M. L., H. F. Maassab, and R. G. Webster. 1993. Molecular and biological changes in the cold-adapted "master strain" A/AA/6/60 (H2N2) influenza virus. Proc. Natl. Acad. Sci. USA 90:6032-6036.
18. Holsinger, L. J., D. Nichani, L. H. Pinto, and R. A. Lamb. 1994. Influenza A virus M2 ion channel protein: a structure-function analysis. J. Virol. 68:1551-1563.
19. Horimoto, T., and Y. Kawaoka. 1995. Molecular changes in virulent mutants arising from avirulent avian influenza viruses during replication in 14-day-old embryonated eggs. Virology 206:755-759.
20. Horimoto, T., E. Rivera, J. Pearson, D. Sanne, S. Krauss, Y. Kawaoka, and R. G. Webster. 1995. Origin and molecular changes associated with emergence of a highly pathogenic H5N2 influenza virus in Mexico. Virology 213:223-230.
21. Katz, J. M., M. Wang, and R. G. Webster. 1990. Direct sequencing of the hemagglutinin gene of influenza (H3N2) virus in original clinical samples reveals sequence identity with mammalian-cell-grown virus. J. Virol. 64: 1808-1811.
22. Kawaoka, Y., C. W. Naeve, and R. G. Webster. 1984. Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology 139:303-316.
23. Klimkait, T., K. Strebel, M. D. Hoggan, M. A. Martin, and J. M. Orenstein. 1990. The human immunodeficiency virus type 1-specific protein Vpu is required for efficient virus maturation and release. J. Virol. 64:621-629.
24. Lamb, R. A., and R. A. Krug. 1996. Orthomyxoviridae: the viruses and their replication, p. 1353-1395. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
25. Maassab, H. F., and M. L. Bryant. 1999. The development of live attenuated cold-adapted influenza virus vaccine for humans. Rev. Med. Virol. 9:237-244.
26. Martin, K., and A. Helenius. 1991. Nuclear transport of influenza virus ribonucleoproteins: The viral matrix protein (M1) promotes export and inhibits import. Cell 67:117-130.
27. Neumann, G., T. Watanabe, H. Ito, S. Watanabe, H. Goto, P. Gao, M. Hughes, D. R. Perez, R. Donis, E. Hoffmann, G. Hobom, and Y. Kawaoka. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. USA 96:9345-9350.
28. Ochman, H., A. S. Gerber, and D. L. Hartl. 1988. Genetics applications of an inverse polymerase chain reaction. Genetics 120:621-623.
29. Ohuchi, M., A. Cramer, M. Vey, R. Ohuchi, W. Garten, and H.-D. Klenk. 1994. Rescue of vector-expressed fowl plague virus hemagglutinin in biologically active form by acid-tropic agents and coexpressed M2 protein. J. Virol. 68:920-926.
30. Park, E. K., M. R. Castrucci, A. Portner, and Y. Kawaoka. 1998. The M2 ectodomain is important for its incorporation into influenza A virions. J. Virol. 72:2449-2455.
31. Piller, S. C., G. D. Ewart, A. Premkumar, G. B. Cox, and P. W. Gage. 1996. Vpr protein of human immunodeficiency virus type 1 forms cation-selective channels in planar lipid bilayers. Proc. Natl. Acad. Sci. USA 93:111-115.
32. Pinto, L. H., L. J. Holsinger, and R. A. Lamb. 1992. Influenza A virus M2 protein has ion channel activity. Cell 69:517-528.
33. Plugge, B., S. Gazzarrini, M. Nelson, R. Cerana, J. L. Van Etten, C. Derst, D. DiFrancesco, A. Moroni, and G. Thiel. 2000. A potassium channel protein encoded by chlorella virus PBCV-1. Science 287:1641-1644.
34. Roizman, B., and P. Palese. 1996. Multiplication of viruses: an overview, p. 101-111. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
35. Sansom, M. S. P., and I. D. Kerr. 1993. Influenza virus M2 protein: A molecular modeling study of the ion channel. Protein Eng. 6:65-74.
36. Schubert, U., K. A. Clouse, and K. Strebel. 1995. Augmentation of virus secretion by the human immunodeficiency virus type 1 Vpu protein is cell type independent and occurs in cultured human primary macrophages and lymphocytes. J. Virol. 69:7699-7711.
37. Schubert, U., A. V. Ferrer-Montiel, M. Oblatt-Montal, P. Henklein, K. Strebel, and M. Montal. 1996. Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HIV-1 infected cells. FEBS Lett. 398:12-18.
38. Sears, S. D., M. L. Clements, R. F. Betts, H. F. Maassab, B. R. Murphy, and M. H. Snyder. 1988. Comparison of live, attenuated H1N1 and H3N2 cold-adapted and avian-human influenza A reassortant viruses and inactivated virus vaccine in adults. J. Infect. Dis. 158:1209-1219.
39. Steinhoff, M. C., N. A. Halsey, M. H. Wilson, B. A. Burns, R. K. Samorodin, L. F. Fries, B. R. Murphy, and M. L. Clements. 1990. Comparison of live attenuated cold-adapted and avian-human influenza A/Bethesda/85 (H3N2) reassortant virus vaccines in infants and children. J. Infect. Dis. 162:394-401.
40. Steinhoff, M. C., N. A. Halsey, L. F. Fries, M. H. Wilson, J. King, B. A. Burns, R. K. Samorodin, V. Perkis, B. R. Murphy, and M. L. Clements. 1991. The A/Mallard/6750/78 avian-human, but not the A/Ann Arbor/6/60 cold-adapted, influenza A/Kawasaki/86 (H1N1) reassortant virus vaccine retains partial virulence for infants and children. J. Infect. Dis. 163:1023-1028.
41. Strebel, K., T. Klimkait, and M. A. Martin. 1988. A novel gene of HIV-1, VPU, and its 16-kilodalton product. Science 241:1221-1223.
42. Strebel, K., T. Klimkait, F. Maldarelli, and M. A. Martin. 1989. Molecular and biochemical analyses of human immunodeficiency virus type 1 Vpu protein. J. Virol. 63:3784-3791.
43. Sugrue, R. J., G. Bahadur, M. C. Zambom, M. Hall-Smith, A. R. Douglas, and A. J. Hay. 1990. Specific structure alteration of the influenza haemagglutinin by amantadine. EMBO J. 9:3469-3476.
44. Sugrue, R. J., and A. J. Hay. 1991. Structural characteristics of the M2 protein of the influenza A viruses: evidence that it forms a tetrameric channel. Virology 180:617-624.
45. Sunstrom, N. A., L. S. Premkumar, A. Premkumar, G. Ewart, G. B. Cox, and P. W. Gage. 1996. Ion channels formed by NB, an influenza B virus protein. J. Membr. Biol. 150:127-132.
46. Takeuchi, K., and R. A. Lamb. 1994. Influenza virus M2 protein ion channel activity stabilizes the native form of fowl plague virus hemagglutinin during intracellular transport. J. Virol. 68:911-919.
47. Terwilliger, E. F., E. A. Cohen, Y. C. Lu, J. G. Sodroski, and W. A. Haseltine. 1989. Functional role of human immunodeficiency virus type 1 vpu. Proc. Natl. Acad. Sci. USA 86:5163-5167.
48. Tobler, K., M. L. Kelly, L. H. Pinto, and R. A. Lamb. 1999. Effect of cytoplasmic tail truncations on the activity of the M2 ion channel of influenza A virus. J. Virol. 73:9695-9701.
49. Wang, C., K. Takeuchi, L. H. Pinto, and R. A. Lamb. 1993. The ion channel activity of influenza A virus protein: characterization of the amantadine block. J. Virol. 67:5585-5594.
50. Wharton, S. A., L. J. Calder, R. W. H. Ruigrok, J. J. Skehel, D. A. Steinhauer, and D. C. Wiley. 1995. Electron microscopy of antibody complexes of influenza virus heamagglutinin in the fusion pH conformation. EMBO J. 14:240-246.
51. Zebedee, S. L., and R. A. Lamb. 1988. Influenza virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J. Virol. 62:2762-2772.
52. Zebedee, S. L., and R. A. Lamb. 1989. Growth restriction of influenza A virus by M2 protein antibody is genetically linked to the M1 protein. Proc. Natl. Acad. Sci. USA 86:1061-1065.
53. Zhirnov, O., and A. G. Bukrinskaya. 1984. Nucleoproteins of animal influenza viruses, in contrast to those of human strains, are not cleaved in infected cells. J. Gen. Virol. 65:1127-1134.
54. Zhirnov, O. P. 1990. Solubilization of matrix protein M1/M from virions occurs at different pH for orthomyxo- and paramyxoviruses. Virology 176: 274-279.