Mutagenesis of the NS2B-NS3-mediated cleavage site in the flavivirus capsid protein demonstrates a requirement for coordinated processing

Journal of Virology

Volumn 73, Issue 10, 1999, Pages 8083-8094

  Amberg, Sean M ^a   Rice, Charles M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CAPSID PROTEIN; MUTANT PROTEIN; PROTEINASE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME SPECIFICITY; FLAVIVIRUS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; VIRUS INFECTIVITY; VIRUS PARTICLE; YELLOW FEVER FLAVIVIRUS;

EID: 0032845108     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.10.8083-8094.1999     Document Type: Article

References (48)

1. Allison, S. L., K. Stadler, C. W. Mandl, C. Kunz, and F. X. Heinz. 1995. Synthesis and secretion of recombinant tick-borne encephalitis virus protein E in soluble and particulate form. J. Virol. 69:5816-5820.
2. Amberg, S. M., A. Nestorowicz, D. W. McCourt, and C. M. Rice. 1994. NS2B-3 proteinase-mediated processing in the yellow fever virus structural region: in vitro and in vivo studies. J. Virol. 68:3794-3802.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1998. Current protocols in molecular biology. John Wiley & Sons, New York, N.Y.
4. Barrett, A. J. 1994. Classification of peptidases. Methods Enzymol. 244:1-15.
5. Bredenbeek, P. J., E. Kool, B. D. Lindenbach, M. Lucassen, N. Huijkman, W. J. M. Spaan, and C. M. Rice. Unpublished data.
6. Castle, E., T. Nowak, U. Leidner, G. Wengler, and G. Wengler. 1985. Sequence analysis of the viral core protein and the membrane-associated proteins V1 and NV2 of the flavivirus West Nile virus and of the genome sequence for these proteins. Virology 145:227-236.
7. Chambers, T. J., C. S. Hahn, R. Galler, and C. M. Rice. 1990. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 44:649-688.
8. Chambers, T. J., D. W. McCourt, and C. M. Rice. 1990. Production of yellow fever virus proteins in infected cells: identification of discrete polyprotein species and analysis of cleavage kinetics using region-specific polyclonal antisera. Virology 177:159-174.
9. Chambers, T. J., D. W. McCourt, and C. M. Rice. 1989. Yellow fever virus proteins NS2A, NS2B, and NS4B: identification and partial N-terminal amino acid sequence analysis. Virology 169:100-109.
10. Chambers, T. J., A. Nestorowicz, S. M. Amberg, and C. M. Rice. 1993. Mutagenesis of the yellow fever virus NS2B protein: effects on proteolytic processing, NS2B-NS3 complex formation, and viral replication. J. Virol. 67:6797-6807.
11. Chambers, T. J., A. Nestorowicz, and C. M. Rice. 1995. Mutagenesis of the yellow fever virus NS2B/3 cleavage site: determinants of cleavage site specificity and effects on polyprotein processing and viral replication. J. Virol. 69:1600-1605.
12. Chambers, T. J., R. C. Weir, A. Grakoui, D. W. McCourt, J. F. Bazan, R. J. Fletterick, and C. M. Rice. 1990. Evidence that the N-terminal domain of nonstructural protein NS3 from yellow fever virus is a serine protease responsible for site-specific cleavages in the viral polyprotein. Proc. Natl. Acad. Sci. USA 87:8898-8902.
13. Dubuisson, J., H. H. Hsu, R. C. Cheung, H. B. Greenberg, D. G. Russell, and C. M. Rice. 1994. Formation and intracellular localization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia and Sindbis viruses. J. Virol. 68:6147-6160.
14. Fuerst, T. R., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83:8122-8126.
15. Grakoui, A., and C. M. Rice. Unpublished data.
16. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82:488-492.
17. Lee, E., C. E. Stocks, S. M. Amberg, C. M. Rice, and M. Lobigs. Submitted for publication.
18. Lin, C., S. M. Amberg, T. J. Chambers, and C. M. Rice. 1993. Cleavage at a novel site in the NS4A region by the yellow fever virus NS2B-3 proteinase is a prerequisite for processing at the downstream 4A/4B signalase site. J. Virol. 67:2327-2335.
19. Lin, C., T. J. Chambers, and C. M. Rice. 1993. Mutagenesis of conserved residues at the yellow fever virus 3/4A and 4B/5 dibasic cleavage sites: effects on cleavage efficiency and polyprotein processing. Virology 192:596-604.
20. Lin, C., B. D. Lindenbach, B. Prágai, D. W. McCourt, and C. M. Rice. 1994. Processing in the hepatitis C virus E2-NS2 region: identification of p7 and two distinct E2-specific products with different C termini. J. Virol. 68:5063-5073.
21. Lindenbach, B. D., and C. M. Rice. 1997. trans-complementation of yellow fever virus NS1 reveals a role in early RNA replication. J. Virol. 71:9608-9617.
22. Liu, Q., C. Tackney, R. A. Bhat, A. M. Prince, and P. Zhang. 1997. Regulated processing of hepatitis C virus core protein is linked to subcellular localization. J. Virol. 71:657-662.
23. Lobigs, M. 1993. Flavivirus premembrane protein cleavage and spike heterodimer secretion requires the function of the viral proteinase NS3. Proc. Natl. Acad. Sci. USA 90:6218-6222.
24. Markoff, L. 1989. In vitro processing of dengue virus structural proteins: cleavage of the pre-membrane protein. J. Virol. 63:3345-3352.
25. Martoglio, B., and B. Dobberstein. 1998. Signal sequences: more than just greasy peptides. Trends Cell Biol. 8:410-415.
26. Martoglio, B., R. Graf; and B. Dobberstein. 1997. Signal peptide fragments of preprolactin and HIV-1 p-gp160 interact with calmodulin. EMBO J. 16:6636-6645.
27. Mason, P. W., S. Pincus, M. J. Fournier, T. L. Mason, R. E. Shop and E. Paoletti. 1991. Japanese encephalitis virus-vaccinia recombinants produce paniculate forms of the structural membrane proteins and induce high levels of protection against lethal JEV infection. Virology 180:294-305.
28. Mizushima, H., H. Hijikata, S.-I. Asabe, M. Hirota, K. Kimura, and K. Shimotohno. 1994. Two hepatitis C virus glycoprotein E2 products with different C termini. J. Virol. 68:6215-6222.
29. Moss, B., O. Elroy-Stein, T. Mizukami, W. A. Alexander, and T. R. Fuerst. 1990. New mammalian expression vectors. Nature (London) 348:91-92.
30. Murphy, F. A. 1980. Togavirus morphology and morphogenesis, p. 241-316. In R. W. Schlesinger (ed.), The togaviruses: biology, structure, replication. Academic Press, New York, N.Y.
31. Nestorowicz, A., T. J. Chambers, and C. M. Rice. 1994. Mutagenesis of the yellow fever virus NS2A/2B cleavage site: effects on proteolytic processing, viral replication and evidence for alternative processing of the NS2A protein. Virology 199:114-123.
32. Nowak, T., P. M. Färber, G. Wengler, and G. Wengler. 1989. Analyses of the terminal sequences of West Nile virus structural proteins and of the in vitro translation of these proteins allow the proposal of a complete scheme of the proteolytic cleavages involved in their synthesis. Virology 169:365-376.
33. Rice, C. M. 1996. Flaviviridae: the viruses and their replication, p. 931-960. In B. N. Fields, D. M. Knipe, P. M. Howley, et al. (ed.), Fields virology, 3rd ed., vol. 1. Lippincott-Raven Publishers, Philadelphia, Pa.
34. Rice, C. M., A. Grakoui, R. Galler, and T. J. Chambers. 1989. Transcription of infectious yellow fever virus RNA from full-length cDNA templates produced by in vitro ligation. New Biol. 1:285-296.
35. Rümenapf, T., G. Unger, J. H. Strauss, and H.-J. Thiel. 1993. Processing of the envelope glycoproteins of pestiviruses. J. Virol. 67:3288-3294.
36. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
37. Santolini, E., G. Migliaccio, and N. La Monica. 1994. Biosynthesis and biochemical properties of the hepatitis C virus core protein. J. Virol. 68: 3631-3641.
38. Sato, T., C. Takamura, A. Yasuda, M. Miyamoto, K. Kamogawa, and K. Yasul. 1993. High-level expression of the Japanese encephalitis virus E protein by recombinant vaccinia virus and enhancement of its extracellular release by the NS3 gene product. Virology 192:483-490.
39. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrytamide gel electrophoresis for the separation of proteins in the range of 1 to 100 kDa. Anal. Biochem. 166:368-379.
40. Schalich, J., S. L. Allison, K. Stiasny, C. W. Mandl, C. Kunz, and F. X. Heinz. 1996. Recombinant subviral particles from tick-borne encephalitis virus are fusogenic and provide a model system for studying flavivirus envelope glycoprotein functions. J. Virol. 70:4549-4557.
41. Speight, G., and E. G. Westaway. 1989. Carboxy-terminal analysis of nine proteins specified by the flavivirus Kunjin: evidence that only the intracellular core protein is truncated. J. Gen. Virol. 70:2209-2214.
42. Stocks, C. E., and M. Lobigs. 1995. Posttranslational signal peptidase cleavage at the flavivirus C-prM junction in vitro. J. Virol. 69:8123-8126.
43. Stocks, C. E., and M. Lobigs. 1998. Signal peptidase cleavage at the flavivirus C-prM junction: dependence on the viral NS2B-3 protease for efficient processing requires determinants in C, the signal peptide, and prM. J. Virol. 72:2141-2149.
44. Yamshckikov, V. F., and R. W. Compans. 1995. Formation of the flavivirus envelope: role of the viral NS2B-NS3 protease. J. Virol. 69:1995-2003.
45. Yamshchikov, V. F., and R. W., Compans. 1994. Processing of the intracellular form of the West Nile virus capsid protein by the viral NS2B-NS3 protease: an in vitro study. J. Virol. 68:5765-5771.
46. Yamshchikov, V. F., and R. W. Compans. 1993. Regulation of the late events in flavivirus protein processing and maturation. Virology 192:38-51.
47. Yamshchikov, V. F., D. W. Trent, and R. W. Compans. 1997. Upregulation of signalase processing and induction of prM-E secretion by the flavivirus NS2B-NS3 protease: roles of protease components. J. Virol. 71:4364-4371.
48. Yasui, K., T. Wakita, K. Tsukiyama-Kohara, S.-I. Funahashi, M. Ichikawa, T. Kajita, D. Moradpour, J. R. Wands, and M. Kohara. 1998. The native form and maturation process of hepatitis C virus core protein. J. Virol. 72:6048-6055.