Separate functional domains of the herpes simplex virus type 1 protease: Evidence for cleavage inside capsids

Journal of Virology

Volumn 70, Issue 7, 1996, Pages 4317-4328

  Robertson, Barbara J ^a   McCann III, Patrick J ^a   Matusick Kumar, Linda ^a,d   Newcomb, William W ^b   Brown, Jay C ^b   Colonno, Richard J ^c   Gao, Min ^a,d  

^a BRISTOL MYERS SQUIBB   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^c BRISTOL MYERS SQUIBB PHARMACEUTICAL RESEARCH INSTITUTE   (United States)

^d PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SERINE PROTEINASE; VIRUS ENZYME;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; HERPES SIMPLEX VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; VERO CELL; VIROGENESIS; VIRUS ASSEMBLY; VIRUS CAPSID;

EID: 0029938474     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.7.4317-4328.1996     Document Type: Article

References (58)

1. Baker, T. S., W. W. Newcomb, F. O. Booy, J. C. Brown, and A. C. Steven. 1990. Three-dimensional structures of maturable and abortive capsids of equine herpesvirus 1 from cryoelectron microscopy. J. Virol. 64:563-573.
2. Baum, E. Z., G. A. Bebernitz, J. D. Hulmes, V. P. Muzithras, T. R. Jones, and Y. Gluzman. 1992. Expression and analysis of the human cytomegalovirus UL80-encoded protease: identification of autoproteolytic sites. J. Virol. 67: 497-506.
3. Braun, D. K., B. Roizman, and L. Pereira. 1984. Characterization of post-translational products of herpes simplex virus gene 35 proteins binding to the surfaces of full capsids but not empty capsids. J. Virol. 49:142-153.
4. Casjens, S., and J. King. 1975. Virus assembly. Annu. Rev. Biochem. 44: 555-611.
5. Darke, P. L., J. L. Cole, L. Waxman, D. L. Hall, M. K. Sardana, and L. C. Kuo. 1996. Active human cytomegalovirus protease is a dimer. J. Biol. Chem. 271:7445-7449.
6. Deckman, I. C., M. Hagen, and P. J. McCann III. 1992. Herpes simplex virus type 1 protease expressed in Escherichia coli exhibits autoprocessing and specific cleavage of the ICP35 assembly protein. J. Virol. 66:7362-7367.
7. Desai, P., N. A. DeLuca, J. C. Glorioso, and S. Person. 1993. Mutations in herpes simplex virus type 1 genes encoding VP5 and VP23 abrogate capsid formation and cleavage of replicated DNA. J. Virol. 67:1357-1364.
8. Desai, P., S. C. Watkins, and S. Person. 1994. The size and symmetry of B capsids of herpes simplex virus type 1 are determined by the gene products of the UL26 open reading frame. J. Virol. 68:5365-5374.
9. DiIanni, C. L., D. A. Drier, I. C. Deckman, P. J. McCann III, F. Liu, B. Roizman, R. J. Colonno, and M. G. Cordingley. 1993. Identification of the herpes simplex virus-1 protease cleavage sites by direct sequence analysis of autoproteolytic cleavage products. J. Biol. Chem. 268:2048-2051.
10. DiIanni, C. L., C. Mapelli, D. A. Drier, J. Tsao, S. Natarajan, D. Riexinger, S. M. Festin, M. Bolgar, G. Yamanaka, S. Weinheimer, C. A. Meyers, R. J. Colonno, and M. G. Cordingley. 1993. In vitro activity of the herpes simplex virus-1 protease with peplide substrates. J. Biol. Chem. 268:25449-25454.
11. DiIanni, C. L., J. T. Stevens, M. Bolgar, D. R. O'Boyle II, S. W. Weinheimer, and R. J. Colonno. 1994. Identification of the serine residue at the active site of the herpes simplex virus type 1 protease. J. Biol. Chem. 269:12672-12676.
12. Gao, M., et al. Unpublished data.
13. Gao, M., L. Matusick-Kumar, W. Hurlburt, S. F. DiTusa, W. W. Newcomb, J. C. Brown, P. J. McCann III, I. C. Deckman, and R. J. Colonno. 1994. The protease of herpes simplex virus type 1 is essential for functional capsid formation and viral growth. J. Virol. 68:3702-3712.
14. Gibson, W., A. I. Marcy, J. C. Comoli, and J. Lee. 1990. Identification of precursor to cytomegalovirus capsid assembly protein and evidence that processing results in loss of its carboxy-terminal end. J. Virol. 64:1241-1249.
15. Gibson, W., and B. Roizman. 1972. Proteins specified by herpes simplex virus. VIII. Characterization and composition of multiple capsid forms of subtypes 1 and 2. J. Virol. 10:1044-1052.
16. Gibson, W., and B. Roizman. 1974. Proteins specified by herpes simplex virus. X. Staining and radiolabeling properties of B capsids and virion pro- teins in polyacrylamide gels. J. Virol. 13:155-165.
17. Goldstein, J., and S. P. Champe. 1974. T4-induced activity required for specific cleavage of bacteriophage protein in vitro. J. Virol. 13:419-427.
18. Hall, L. D., and P. L. Darke. 1995. Activation of the herpes simplex virus type 1 protease. J. Biol. Chem. 270:22697-22700.
19. Heilman, C. J., M. Zweig, J. R. Stephenson, and B. Hampar. 1979. Isolation of nucleocapsid proteins of herpes simplex virus types 1 and 2 possessing immunologically type-specific and cross-reactive determinants. J. Virol. 29: 34-42.
20. Holland, L. E., R. M. Sandri-Goldin, A. L. Goldin, J. C. Glorioso, and M. Levin. 1984. Transcriptional and genetic analyses of the herpes simplex virus type 1 genome: coordinates 0.29 to 0.45. J. Virol. 49:947-959.
21. Holwerda, B. B., A. J. Wittwer, K. L. Duffin, C. Smith, M. V. Toth, L. S. Carr, R. C. Wiegand, and M. L. Bryant. 1994. Activity of two-chain recombinant human cytomegalovirus protease. J. Biol. Chem. 269:25911-25915.
22. Hong, Z., M. Beaudet-Miller, J. Durkin, R. Zhang, and A. D. Kwong. 1996. Identification of a minimal hydrophohic domain in the herpes simplex virus type 1 scaffolding protein which is required for interaction with the major capsid protein. J. Virol. 70:533-540.
23. Knipe, D. M., M. P. Quinlan, and A. E. Spang. 1982. Characterization of two conformational forms of the major DNA-binding protein encoded by herpes simplex virus 1. J. Virol. 44:736-741.
24. Knipe, D. M., and A. E. Spang. 1982. Definition of a series of stages in the association of two herpesvirus proteins with the cell nucleus. J. Virol. 43: 314-324.
25. Liu, F., and B. Roizman. 1991. The promoter, transcriptional unit, and coding sequences of the herpes simplex virus 1 family 35 proteins are contained within and in frame with the UL26 open reading frame. J. Virol. 65:206-212.
26. Liu, F., and B. Roizman. 1991. The herpes simplex virus 1 gene encoding a protease also contains within its coding domain the gene encoding the more abundant substrate. J. Virol. 65:5149-5156.
27. Liu, F., and B. Roizman. 1992. Differentiation of multiple domains in the herpes simplex virus 1 protease encoded by the UL26 gene. Proc. Natl. Acad. Sci. USA 89:2076-2080.
28. L 26 protein. J. Virol. 67:1300-1309.
29. Matusick-Kumar, L., W. Hurlburt, S. W. Weinheimer, W. W. Newcomb, J. C. Brown, and M. Gao. 1994. Phenotype of the herpes simplex virus type 1 protease substrate ICP35 mutant virus. J. Virol. 68:5384-5394.
30. 0 from the herpes simplex virus type 1 protease is required for viral growth. J. Virol. 69:7113-7121.
31. Matusick-Kumar, L., W. W. Newcomb, J. C. Brown, P. J. McCann III, W. Hurlburt, S. P. Weinheimer, and M. Gao. 1995. The C-terminal 25 amino acids of the protease and its substrate ICP35 of herpes simplex virus type 1 are involved in the formation of sealed capsids. J. Virol. 69:4347-4356.
32. McCann, P. J., III, D. R. O'Boyle II, and I. C. Deckman. 1994. Investigation of the specificity of the herpes simplex virus type 1 protease by point mutagenesis of the autoproteolysis sites. J. Virol. 68:526-529.
33. McGeoch, D. J., M. A. Dalrymple, A. J. Davison, A. Dolan, M. C. Frame, D. McNab, L. J. Perry, J. E. Scott, and P. Taylor. 1988. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J. Gen. Virol. 69:1531-1574.
34. Morgenatern, J. P., and H. Lane. 1990. A series of mammalian expression vectors and characterization of their expression of a reporter gene in stably and transient transformed cells. Nucleic Acids Res. 18:1068.
35. + plasma etching to localize structural proteins in the capsid of herpes simplex virus type 1. J. Virol. 63:4697-4702.
36. Newcomb, W. W., and J. C. Brown. 1991. Structure of the herpes simplex virus capsid: effects of extraction with guanidine hydrochloride and partial reconstitution of extracted capsids. J. Virol. 65:613-620.
37. Newcomb, W. W., B. L. Trus, F. P. Booy, A. C. Steven, J. S. Wall, and J. C. Brown. 1993. Structure of the herpes simplex virus capsid: molecular composition of the pentons and the triplexes. J. Mol. Biol. 232:499-511.
38. Nicholson, P., C. Addison, A. M. Cross, J. Kennard, V. G. Preston, and F. J. Rixon. 1994. Localization of the herpes simplex virus type 1 major capsid protein VP5 to the cell nucleus requires the abundant scaffolding protein VP22a. J. Gen. Virol. 75:1091-1099.
39. O'Boyle, D. R., II, K. Wager-Smith, J. T. Stevens III, and S. P. Weinheimer. 1995. The effect of internal autocleavage on kinetic properties of the human cytomegalovirus protease catalytic domain. J. Biol. Chem. 270:4753-4758.
40. Patel, A. H., and J. B. Maclean. 1995. The product of the UL6 gene of herpes simplex virus type 1 is associated with virus capsids. Virology 206:465-478.
41. Perdue, M. L., J. C. Cohen, C. C. Randall, and D. J. O'Callaghan. 1976. Biochemical studies on the maturation of herpesvirus nucleocapsid species. Virology 74:194-208.
42. Person, S., S. Laquerre, D. Prashant, and J. Hempel. 1993. Herpes simplex virus type 1 capsid protein, VP21, originates within the UL26 open reading frames. J. Gen. Virol. 74:2269-2273.
43. Pertuiset, B., M. Boccara, J. Cebrian, N. Berthelot, S. Chousterman, F. Puvion-Dutilleul, J. Sisman, and P. Sheldrick. 1989. Physical mapping and nucleotide sequence of a herpes simplex virus type 1 gene required for capsid assembly. J. Virol. 63:2169-2179.
44. Preston, V. G., J. A. V. Coates, and F. J. Rixon. 1983 Identification and characterization of a herpes simplex virus gene product required for encapsidation of virus DNA. J. Virol. 45:1056-1064.
45. Preston, V. G., F. J. Rixon, I. M. McDougall, M. McGregor, and M. F. AI Kobaisi. 1992. Processing of the herpes simplex viral assembly protein ICP35 near its C-terminal end requires the product of the whole of the UL26 reading frame. Virology 186:87-98.
46. Rixon, F. J., A. M. Cross, C. Addison, and V. G. Preston. 1988. The products of herpes simplex virus type 1 gene UL26 which are involved in DNA packaging are strongly associated with empty but not with full capsids. J. Gen. Virol. 69:2879-2891.
47. Shepard, A. A., and N. A. Deluca. 1989. Intragenic complementation of herpes simplex virus regulatory protein ICP4. J. Virol. 63:1203-1211.
48. Showe, M. K., E. Isobe, and L. Onorato. 1976. Bacteriophage T4 prohead proteinase. II. Its cleavage from the product of gene 21 and regulation in phage-infected cells. J. Mol. Biol. 107:55-69.
49. Tatman, J. D., V. G. Preston, P. Nicholson, R. M. Elliott, and F. J. Rixon. 1994. Assembly of herpes simplex virus type 1 capsids using a panel of recombinant baculovirus. J. Gen. Virol. 75:1101-1113.
50. Thomsen, D. R., W. W. Newcomb, J. C. Brown, and F. L. Homa. 1995. Assembly of the herpes simplex virus capsids: requirement for the carboxyl-terminal twenty-five amino acids of the proteins encoded by the UL26 and UL26.5 genes. J. Virol. 69:3690-3703.
51. Thomsen, D. R., L. L. Roof, and F. L. Homa. 1994. Assembly of herpes simplex virus (HSV) intermediate capsids in insect cells infected with re- combinant baculoviruses expressing HSV capsid proteins. J. Virol. 68:2442-2457.
52. Vernon, S. K., M. Ponce de Leon, G. H. Cohen, R. J. Eisenberg, and B. A. Rubin. 1981. Morphological components of herpesvirus. III. Localization of herpes simplex virus type 1 nucleocapsid polypeptides by electron microscopy. J. Gen. Virol. 54:39-46.
53. Weinheimer, S. P., P. J. McCann III, D. R O'Boyle II, J. T. Stevens, B. A. Boyd, D. A. Drier, G. A. Yamanaka, C. L. Dilanni, I. C. Deckman, and M. G. Cordingley. 1993. Autoproteolysis of herpes simplex virus type 1 protease releases an active catalytic domain found in intermediate capsid particles. J. Virol. 67:5813-5822.
54. Welch, A. R., L. M. McNally, M. R. T. Hall, and W. Gibson. 1993. Herpesvirus proteinase: site-directed mutagenesis used to study maturational, release, and inactivation cleavage sites of precursor and to identify a possible catalytic site serine and histidine. J. Virol. 67:7350-7372.
55. Welch, A. R., E. C. Villarreal, and W. Gibson. 1995. Cytomegalovirus protein substrates are not cleaved by the herpes simplex virus type 1 proteinase. J. Virol. 69:341-347.
56. Welch, A. R., A. S. Wood, L. M. McNally, R. J. Cotter, and W. Gibson. 1991. A herpes maturational proteinase, assemblin: identification of its gene, putative active site domain, and cleavage site. Proc. Natl. Acad. Sci. USA 88:10792-10796.
57. Yamanaka, G., C. L. Dilanni, D. R. O'Boyle II, J. Stevens, S. P. Weinheimer, I. C. Deckman, L. Matusick-Kumar, and R. Colonno. 1995. Stimulation of the herpes simplex virus type 1 protease by anticheaotrophic salts. J. Biol. Chem. 270:30168-30172.
58. Zabin, I., and A. V. Fowler. 1978. β-Galactosidase, the lactose permease protein and thiogalactoside transacetylase, p. 89-121. In J. H. Miller and W. S. Reznikoff (ed.), The operon. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.