Mutation of neuraminidase cysteine residues yields temperature-sensitive influenza viruses

Journal of Virology

Volumn 73, Issue 10, 1999, Pages 8095-8103

  Basler, Christopher F ^a   García Sastre, Adolfo ^a   Palese, Peter ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CYSTEINE; GLYCINE; MUTANT PROTEIN; SIALIDASE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE MUTATION; GENETIC TRANSFECTION; HELPER VIRUS; INFLUENZA; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TEMPERATURE SENSITIVITY; VIRUS REPLICATION;

EID: 0345426371     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.10.8095-8103.1999     Document Type: Article

References (55)

1. Blick, T. J., A. Sahasrabudhe, M. McDonald, I. J. Ownes, P. J. Morley, R. J. Fenton, and J. L. McKimm-Breschkin. 1998. The interaction of neuraminidase and hemagglutinin mutations in influenza virus in resistance to 4-guanidino-Neu5Ac2en. Virology 246:95-103.
2. Bos, T. J., and D. Nayak, 1986. Identification of defects in the neuraminidase gene of four temperature-sensitive mutants of A/WSN/33 influenza virus. Virology 154:85-96.
3. Braakman, I., H. Hoover-Litty, K. R. Wagner, and A. Helenius. 1991. Folding of influenza virus hemagglutinin in the endoplasmic reticulum. J. Cell. Biol. 114:401-411.
4. Castrucci, M. R., P. Bilsel, and Y. Kawaoka. 1992. Attenuation of influenza A virus by insertion of a foreign epitope into the neuraminidase. J. Virol. 66:4647-4653.
5. Castrucci, M. R., M. Hughes, I. Donatelli, K. Wells, A. Takada, and Y. Kawaoka. 1997. The cysteine residues of the M2 protein are not required for influenza A virus replication. Virology 238:128-134.
6. Colman, P. M. 1989. Neuraminidase: enzyme and antigen, p. 175-218. In R. M. Krug (ed.), The influenza viruses. Plenum Press, New York, N.Y.
7. Colman, P. M., J. N. Varghese, and W. G. Laver. 1983. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 303:41-44.
8. Creighton, T. E. 1997. Protein folding coupled to disulfide bond formation. Biol. Chem. 378:731-744.
9. Enami, M., W. Luytjes, M. Krystal, and P. Palese. 1990. Introduction of site-specific mutations into the genome of influenza virus. Proc. Natl. Acad. Sci. USA 87:3802-3805.
10. Enami, M., and P. Palese. 1991. High-efficiency formation of influenza virus transfectants. J. Virol. 65:2711-2713.
11. Fuerst, T. R., P. L. Earl, and B. Moss. 1987. Use of a hybrid vaccinia virus-T7 RNA polymerase system for expression of target genes. Mol. Cell. Biol. 7:2538-2544.
12. García-Sastre, A., and P. Palese. 1995. The cytoplasmic tail of the neuraminidase protein of influenza A virus does not play an important role in the packaging of this protein into viral envelopes. Virus Res. 37:37-47.
13. García-Sastre, A., T. Muster, W. S. Barclay, N. Percy, and P. Palese. 1994. Use of a mammalian internal ribosomal entry site element for expression of a foreign protein by a transfectant influenza virus. J. Virol. 68:6254-6261.
14. Ghate, A. A., and G. M. Air. 1998. Site-directed mutagenesis of catalytic residues of influenza virus neuraminidase as an aid to drug design. Eur. J. Biochem. 258:320-331.
15. Gonzalo, R. M., D. Rodriguez, A. García-Sastre, J. R. Rodriguez, P. Palese, and M. Esteban. 1999. Enhanced CD8+ T cell response to HIV-1 env by combined immunization with influenza and vaccinia virus recombinants. Vaccine 17:887-892.
16. Goto, H., and Y. Kawaoka. 1998. A novel mechanism for the acquisition of virulence by a human influenza A virus. Proc. Natl. Acad. Sci. USA 95: 10224-10228.
17. Gottschalk, A. 1957. The specific enzyme of influenza virus and Vibrio cholerae. Biochim. Biophys. Acta 23:645-646.
18. Gubareva, L. V., R. Bethell, G. J. Hart, K. G. Murti, C. R. Penn, and R. G. Webster. 1996. Characterization of mutants of influenza A virus selected with the neuraminidase inhibitor 4-guanidino-Neu5Ac2en. J. Virol. 70:1818-1827.
19. Hausmann, J., E. Kretzchmar, W. Garten, and H.-D. Klenk. 1997. Biosynthesis, intracellular transport and enzymatic activity of an avian influenza A virus neuraminidase: role of unpaired cysteines and individual oligosaccharides. J. Gen, Virol. 78:3233-3245.
20. Hayden, F. G., J. J. Treanor, B. F. Betts, M. Lobo, J. D. Esinhart, and E. K. Hussey. 1996. Saftey and efficacy of the neuraminidase inhibitor GG167 in experimental human influenza. JAMA 275:295-299.
21. Hayden, F. G., A. D. Osterhaus, J. J. Treanor, D. M. Fleming, F. Y. Aoki, K. G. Nicholson, A. M. Bohnen, H. M. Hirst, O. Keene, and K. Wightman. 1997. Efficacy and safety of the neuraminidase inhibitor zanamivir in the treatment of influenza virus infections. GG167 Influenza Study Group. N. Engl. J. Med. 337:874-880.
22. Hiti, A. L., and D. P. Nayak. 1982. Complete nucleotide sequence of the neuraminidase gene of human influenza virus A/WSN/33. J. Virol. 41:730-734.
23. Holsinger, L. J., and R. A. Lamb. 1991. Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology 183:32-43.
24. 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.
25. Kobasa, D., M. E. Rodgers, K. Wells, and Y. Kawaoka. 1997. Neuraminidase hemadosorption activity, conserved in avian influenza viruses, does not influence viral replication in ducks. J. Virol. 71:6706-6713.
26. Laver, W. G., P. M. Colman, R. G. Webster, V. S. Hinshaw, and G. M. Air. 1984. Influenza virus neuraminidase with hemagglutinin activity. Virology 137:314-323.
27. Lentz, M. R., and G. M. Air. 1986. Loss of enzyme activity in a site-directed mutant of influenza neuraminidase compared to expressed wild-type protein. Virology 148:74-83.
28. Lentz, M. R., R. G. Webster, and G. M. Air. 1987. Site-directed mutation of the active site of influenza neuraminidase and implications for the catalytic mechanism. Biochemistry 26:5351-5358.
29. Li, S., J. Schulman, S. Itamura, and P. Palese. 1993. Glycosylation of neuraminidase determines the neurovirulence of influenza A/WSN/33 virus. J. Virol. 67:6667-6673.
30. Liu, C., and G. M. Air. 1993. Selection and characterization of a neuraminidase-minus mutant of influenza virus and its rescue by cloned neuraminidase genes. Virology 194:403-407.
31. Long, D., G. H. Cohen, M. I. Muggeridge, and R. J. Eisenberg. 1990. Cysteine mutants of herpes simplex virus type 1 glycoprotein D exhibit temperature-sensitive properties in structure and function. J. Virol. 64:5542-5552.
32. Long, D., W. C. Wilcox, W. R. Abrams, G. H. Cohen, and R. J. Eisenberg. 1992. Disulfide bond structure of glycoprotein D of herpes simplex virus types 1 and 2. J. Virol. 66:6668-6685.
33. Luo, G., J. Chung, and P. Palese. 1993. Alterations of the stalk of influenza virus neuraminidase: deletions and insertions. Virus Res. 29:141-153.
34. Mastrovich, M., N. Zhou, Y. Kawaoka, and R. G. Webster. 1999. The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J. Virol. 73:1146-1155.
35. McKimm-Breschkin, J. L., T. J. Blick, A. Sahastabudhe, T. Tiong, D. Marshall, G. J. Hart, R. C. Bethell, and C. R. Penn. 1996. Generation and characterization of variants of NWS/G70C influenza virus after in vitro passage in 4-amino-Neu5Ac2en and 4-guanido-Neu5Ac2en. Antimicrob. Agents Chemother. 40:40-46.
36. Meindl, P., G. Bodo, P. Palese, J. Schulman, and H. Tuppy. 1974. Inhibition of neuraminidase activity by derivatives of 2-deoxy-2,3-dehydro-N-acetylneuraminic acid. Virology 58:457-463.
37. Miyahara, Y., A. García-Sastre, D. Rodriguez, J. R. Rodriguez, K. Murata, M. Tsuji, P. Palese, M. Esteban, F. Zavala, and R. S. Nussenzweig. 1998. Recombinant viruses expressing a human malaria antigen can elicit potentially protective immune CD8+ responses in mice. Proc. Natl. Acad. Sci. USA 95:3954-3959.
38. Morris, S. J., G. E. Price, J. M. Barnett, S. A. Hiscox, H. Smith, and C. Sweet. 1999. Role of neuraminidase in influenza virus-induced apoptosis. J. Gen. Virol. 80:137-146.
39. Ogawa, S., M. Yoshikawa, and T. Taki. 1992. Synthesis of a carbocyclic analogue of N-acetylneuraminic acid (pseudo-N-acetylneuraminic acid). J. Chem. Soc. Chem. Commun. 406-408.
40. Palese, P., K. Tobita, M. Ueda, and R. W. Compans. 1974. Characterization of temperature-sensitive influenza virus mutants defective in neuraminidase. Virology 61:397-410.
41. Palese, P., and R. W. Compans. 1976. Inhibition of influenza virus replication in tissue culture by 2-deoxy-2,3-dehydro-N-fluoroacetylneuraminic acid (FANA): mechanism of action. J. Gen. Virol. 33:2142-2146.
42. Parkin, N. T., P. Chiu, and K. L. Coelingh. 1996. Temperature sensitive mutants of influenza A virus generated by reverse genetics and clustered charged to alanine mutagenesis. Virus Res. 46:31-44.
43. Percy, N., W. S. Barclay, A. García-Sastre, and P. Palese. 1994. Expression of a foreign protein by influenza A virus. J. Virol. 68:4485-4492.
44. Poon, A. P. W., and B. Roizman. 1995. The phenotype in vitro and in infected cells of herpes simplex virus 1 α trans-inducing factor (VP16) carrying temperature-sensitive mutations introduced by substitution of cysteines. J. Virol. 69:7658-7667.
45. Restifo, N. P., D. R. Surman, H. Zheng, P. Palese, S. A. Rosenberg, and A. García-Sastre. 1998. Transfectant influenza A viruses are effective recombinant immunogens in the treatment of experimental cancer. Virology 249: 89-97.
46. Rudneva, I. E., E. I. Sklyanskava, O. S. Barulina, S. S. Yamnikova, V. P. Kovaleva, I. V. Tsvetkova, and N. V. Kaverin. 1996. Phenotypic expression of HA-NA combinations in human-avian influenza A virus reassortants. Arch. Virol. 141:1091-1099.
47. Schultz-Cherry, S., and V. S. Hinshaw. 1996. Influenza virus neuraminidase activates latent transforming growth factor β J. Virol. 70:8624-8629.
48. Segal, M. S., J. M. Bye, J. F. Sambrook, M.-J. H. Gething. 1992. Disulfide bond formation during the folding of influenza virus hemagglutinin. J. Cell Biol. 118:227-244.
49. Subbarao, E. K., E. J. Park, C. M. Lawson, A. Y. Chen, and B. R. Murphy. 1995. Sequential addition of temperature-sensitive missense mutations into the PB2 gene of influenza A transfectant viruses can effect an increase in temperature sensitivity and attenuation and permits the rational design of a genetically engineered live influenza A virus vaccine. J. Virol. 69:5969-5977.
50. Subbarao, K., A. Klimov, J. Katz, H. Regenery, W. Lim, H. Hall, M. Perdue, D. Swayne, C. Bender, J. Huang, M. Hemphill, T. Rowe, M. Shaw, X. Xu, K. Fukada, and N. Cox. 1998. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279:393-396.
51. Varghese, J. N., W. G. Laver, and P. M. Colman. 1983. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature 303:35-40.
52. Varghese, J. N., P. M. Colman, A. van Donkelaar, T. J. Blick, A. Sahasrabudhe, and J. L. McKimm-Breschkin. 1997. Structural evidence for a second sialic acid binding site in avian influenza virus neuraminidase. Proc. Natl. Acad. Sci. USA 94:11808-11812.
53. von Itzstein, M., W. Y. Wu, G. B. Kok, M. S. Pegg, J. C. Dyason, B. Jin, T. Van Phan, M. L. Smythe, H. F. White, S. W. Oliver, et al. 1993. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363:418-423.
54. Wilcox, W. C., D. Long, D. L. Sodora, R. J. Eisenberg, and G. H. Cohen. 1988. The contribution of cysteine residues to antigenicity and extent of processing of herpes simplex virus type 1 glycoprotein D. J. Virol. 62:1941-1947.
55. Yamamoto-Goshima, F., K. Maeno, T. Morishits, M. Ueda, Y. Fujita, K. Nakajima, and S. Yoshii. 1994. Role of neuraminidase in the morphogenesis of influenza B virus. J. Virol. 68:1250-1254.