Comparison of substrate specificities against the fusion glycoprotein of virulent newcastle disease virus between a chick embryo fibroblast processing protease and mammalian subtilisin-like proteases

Microbiology and Immunology

Volumn 43, Issue 2, 1999, Pages 133-140

  Fujii, Yutaka ^a   Sakaguchi, Takemasa ^a   Kiyotani, Katsuhiro ^a   Yoshida, Tetsuya ^a  

^a HIROSHIMA UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

Activating protease; Fusion glycoprotein; NDV; Substrate specificity

Indexed keywords

FURIN; HYBRID PROTEIN; PROTEINASE; SUBTILISIN; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CHICK EMBRYO; COMPARATIVE STUDY; EMBRYO; ENZYME SPECIFICITY; FIBROBLAST; NEWCASTLE DISEASE PARAMYXOVIRUS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN STRUCTURE;

ANIMALIA; MAMMALIA; NEWCASTLE DISEASE VIRUS; PARAMYXOVIRIDAE; RNA VIRUSES; VACCINIA; VACCINIA VIRUS;

EID: 0033029779     PISSN: 03855600     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1348-0421.1999.tb02384.x     Document Type: Article

References (46)

1. Abenes, G., Kida, H., and Yanagawa, R. 1986. Antigenic mapping and functional analysis of the F protein of Newcastle disease virus using monoclonal antibodies. Arch. Virol. 90: 97-110.
2. Barr, P.J. 1991. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell 66: 1-3.
3. Bosch, F.X., Garten, W., Klenk, H.-D., and Rott, R. 1981. Proteolytic cleavage of influenza virus hemagglutinins: primary structure of the connecting peptide between HA1 and HA2 determines proteolytic cleavability and pathogenicity of avian influenza viruses. Virology 113: 725-735.
4. Bratt, M.A., and Hightower, L.E. 1977. Genetics and paragenetic phenomena of paramyxoviruses, p. 457-533. In Fraenkel-Conrat, H., and Wagner, R.R. (eds), Comprehensive virology. Vol. 9, Plenum Press, New York.
5. Bresnahan, P.A., Leduc, R., Thomas, L., Thorner, J., Gibson, H.L., Brake, A.J., Barr, P.J., and Thomas, G. 1990. Human fur gene encodes a yeast KEX2-like endoprotease that cleaves pro-beta-NGF in vivo. J. Cell Biol. 111: 2851-2859.
6. Chambers, P., Millar, N.S., and Emmerson, P.T. 1986. Nucleotide sequence of the gene encoding the fusion glycoprotein of Newcastle disease virus. J. Gen. Virol. 67: 2685-2694.
7. Creemers, J.W., Kormelink, P.J., Roebroek, A.J., Nakayama, K., and Van de Ven, W.J. 1993. Proprotein processing activity and cleavage site selectivity of the Kex2-like endoprotease PACE4. FEBS Lett. 336: 65-69.
8. Glickman, R.L., Syddall, R.J., Iorio, R.M., Sheehan, J.P., and Bratt, M.A. 1988. Quantitative basic residue requirements in the cleavage-activation site of the fusion glycoprotein as a determinant of virulence for Newcastle disease virus. J. Virol. 62: 354-356.
9. Gotoh, B., Ogasawara, T., Toyoda, T., Inocencio, N.M., Hainaguchi, M., and Nagai, Y. 1990. An endoprotease homologous to the blood clotting factor X as a determinant of viral tropism in chick embryo. EMBO J. 9: 4189-4195.
10. Gotoh, B., Ohnishi, Y. Inocencio, N.M., Esaki, E., Nakayama, K., Barr, P.J., Thomas, G., and Nagai, Y. 1992. Mammalian subtilisin-related proteinases in cleavage activation of the paramyxovirus fusion glycoprotein: superiority of furin/PACE to PC2 or PC1/PC3. J. Virol. 66: 6391-6397.
11. Gotoh, H., Shioda, T., Sakai, Y. Mizumoto, K., and Shibuta, H. 1989. Rescue of Sendai virus from viral ribonucleoprotein-transfected cells by infection with recombinant vaccinia viruses carrying Sendai virus L and P/C genes. Virology 171: 434-443.
12. Granoff, A. 1959. Studies on mixed infection with Newcastle disease virus. I. Isolation of Newcastle disease virus mutant and tests for genetic recombination between them. Virology 9: 636-648.
13. Horimoto, T., and Kawaoka, Y. 1995. The hemagglutinin cleavability of a virulent avian influenza virus by subtilisin-like endoproteases is influenced by the amino acid immediately downstream of the cleavage site. Virology 210: 466-470.
14. Horimoto, T., Nakayama, K., Smeekens, S.P., and Kawaoka, Y. 1994. Proprotein-processing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses. J. Virol. 68: 6074-6078.
15. Hosaka, M., Nagahama, M., Kim, W.S., Watanabe, T., Hatsuzawa, K., Ikemizu, J., Murakami, K., and Nakayama, K. 1991. Arg-X-Lys/Arg-Arg motif as a signal for precursor cleavage catalyzed by furin within the constitutive secretory pathway. J. Biol. Chem. 266: 12127-12130.
16. Kawaoka, Y., and Webster, R.G. 1988. Sequence requirements for cleavage activation of influenza virus hemagglutinin expressed in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 85: 324-328.
17. Kido, H., Yokogoshi, Y., Sakai, K., Tashiro, M., Kishino, Y., Fukutomi, A., and Katunuma, N. 1992. Isolation and characterization of a novel trypsin-like protease found in rat bronchiolar epithelial Clara cells. A possible activator of the viral fusion glycoprotein. J. Biol. Chem. 267: 13573-13579.
18. Kiefer, M.C., Tucker, J.E., Joh, R., Landsberg, K.E., Saltman, D., and Barr, P.J. 1991. Identification of a second human subtilisin-like protease gene in the fes/fps region of chromosome 15. DNA Cell Biol. 10: 757-769.
19. Kunkel, T.A. 1985. Rapid and efficient site-specific muta-genesis without phenotypic selection. Proc. Natl. Acad. Sci. U.S.A. 82: 488-492.
20. Li, Z., Sergel, T., Razvi, E., and Morrison, T. 1998. Effect of cleavage mutants on syncytium formation directed by the wild-type fusion protein of Newcastle disease virus. J. Virol. 72: 3789-3795.
21. Lusson, J., Vieau, D., Hamelin, J., Day, R., Chretien, M., and Seidah, N.G. 1993. cDNA structure of the mouse and rat subtilisin/kexin-like PC5: a candidate proprotein convertase expressed in endocrine and nonendocrine cells. Proc. Natl. Acad. Sci. U.S.A. 90: 6691-6695.
22. Molloy, S.S., Bresnahan, P.A., Leppla, S.H., Kumpel, K.R., and Thomas, G. 1992. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence ArgX-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem. 267: 16396-16402.
23. 1 of the Newcastle disease virus fusion protein in cleavage and fusion. Virology 193: 997-1000.
24. Morrison, T.G., Ward, L.J., and Semerjian, A. 1985. Intracellular processing of the Newcastle disease virus fusion glycoprotein. J. Virol. 53: 851-857.
25. Nagai, Y. 1993. Protease-dependent virus tropism and pathogenicity. Trends Microbiol. 1: 81-87.
26. Nagai, Y., Klenk, H.D., and Rott, R. 1976. Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology 72: 494-508.
27. Nakagawa, T., Hosaka, M., Torii, S., Watanabe, T., Murakami, K., and Nakayama, K. 1993. Identification and functional expression of a new member of the mammalian Kex2-like processing endoprotease family: its striking structural similarity to PACE4. J. Biochem. 113: 132-135.
28. Naruse, H., Nagai, Y., Yoshida, T., Hamaguchi, M., Matsumoto, T., Isomura, S., and Suzuki, S. 1981. The polypeptides of mumps virus and their synthesis in infected chick embryo cells. Virology 112: 119-130.
29. Ohnishi, Y., Shioda, T., Nakayama, K., Iwata, S., Gotoh, B., Hamaguchi, M., and Nagai, Y. 1994. A furin-defective cell line is able to process correctly the gp160 of human immuno-deficiency virus type 1. J. Virol. 68: 4075-4079.
30. Ohuchi, M., Orlich, M., Ohuchi, R., Simpson, B.E.J., Garten, W., Klenk, H.-D., and Rott, R. 1989. Mutations at the cleavage site of the hemagglutinin alter the pathogenicity of influenza virus A/chick/Penn/83(H5N2). Virology 168: 274-280.
31. Pritzer, E., Kuroda, K., Garten, W., Nagai, Y., and Klenk, H.D. 1990. A host range mutant of Newcastle disease virus with an altered cleavage site for proteolytic activation of the F protein. Virus Res. 15: 237-242.
32. Rehemtulla, A., Barr, P.J., Rhodes, C.J., and Kaufman, R.J. 1993. PACE4 is a member of the mammalian propeptidase family that has overlapping hut not identical substrate specificity to PACE. Biochemistry 32: 11586-11590.
33. Sakaguchi, T., Fujii, Y., Kiyotani, K., and Yoshida, T. 1994. Correlation of proteolytic cleavage of F protein precursors in paramyxoviruses with expression of the fur. PACE4 and PC6 genes in mammalian cells. J. Gen. Virol. 75: 2821-2827.
34. Sakaguchi, T., Matsuda, Y., Kiyokage, R., Kawahara, N., Kiyotani, K., Kutunuma, N., Nagai, Y., and Yoshida, T. 1991. Identification of endoprotease activity in the trans Golgi membranes of rat liver cells that specifically processes in vitro the fusion glycoprotein precursor of virulent Newcastle disease virus. Virology 184: 504-512.
35. Sakaguchi, T., Takao, S., Kiyotani, K., Fujii, Y., Nakayama, T., and Yoshida, T. 1993. Expression of the HN, F, NP and M proteins of Sendai virus by recombinant vaccinia viruses and their contribution to protective immunity against Sendai virus infections in mice. J. Gen. Virol. 74: 479-484.
36. Sakaguchi, T., Toyoda, T., Gotoh, B., Inocencio, N.M., Kuma, K., Miyata, T., and Nagai, Y. 1989. Newcastle disease virus evolution. I. Multiple lineages defined by sequence variability ot the hemagglutinin-neuraminidase gene. Virology 169: 260-272.
37. Sanger, F., Nicklen, S., and Coulson, A.R. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74: 5463-5467.
38. Sato, H., Oh-hira, M., Ishida, N., Imamura, Y., Hattori, S., and Kawakita, M. 1987. Molecular cloning and nucleotide sequence of P, M and F genes of Newcastle disease virus avirulent strain D26. Virus Res. 7: 241-255.
39. Steiner, D.F., Smeekens, S.P., Ohagi, S., and Chan, S.J. 1992. The new enzymology of precursor processing endoproteases. J. Biol. Chem. 267: 23435-23438.
40. Toyoda, T., Sakaguchi, T., Hirota, H., Gotoh, B., Kuma, K., Miyata, T., and Nagai, Y. 1989. Newcastle disease virus evolution. II. Lack of gene recombination in generating virulent and avirulent strains. Virology 169: 273-282.
41. Toyoda, T., Sakaguchi, T., Imai, K., Inocencio, N.M., Gotoh, B., Humaguchi, M., and Nagai, Y. 1987. Structural comparison of the cleavage-activation site of the fusion glycoprotein between virulent and avirulent strains of Newcastle disease virus. Virology 158: 242-247.
42. Tsuji, A., Mine, C., Mori, K., Tamai, Y., Higashine, K., Nagamune, H., and Matsuda, Y. 1994. A novel member. PC7, of the mammalian kexin-like protease family: homology to PACE4A, its brain-specific expression and identification of isoforms. Biochem. Biophys. Res. Commun. 202: 1452-1459.
43. Vey, M., Orlich, M., Adler, S., Klenk, H.-D., Rott, R., and Garten, W. 1992. Hemagglutinin activation of pathogenic avian influenza viruses of serotype H7 requires the protease recognition motif R-X-K/R-R. Virology 188: 408-413.
44. Walker, J.A., and Kawaoka, Y. 1993. Importance of conserved amino acids at the cleavage site of the haemagglutinin of a virulent avian influenza A virus. J. Gen. Virol. 74: 311-314.
45. Walker, J.A., Molloy, S.S., Thomas, G., Sakaguchi, T., Yoshida, T., Chambers, T.M., and Kawaoka, Y. 1994. Sequence specificity of furin, a proprotein-processing endoprotease, for the hemagglutinin of a virulent avian influenza virus. J. Virol. 68: 1213-1218.
46. Yoshida, T., Nakayama, Y., Nagura, H., Toyoda, T., Nishikawa, K. Hamaguchi, M., and Nagai, Y. 1986. Inhibition of the assembly of Newcastle disease virus by monensin. Virus Res. 4: 179-195.