The protease and the assembly protein of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8)

Journal of Virology

Volumn 71, Issue 9, 1997, Pages 7030-7038

  Ünal, Ayçe ^a   Pray, Todd R ^a   Lagunoff, Michael ^b   Pennington, Michael W ^c   Ganem, Don ^b   Craik, Charles S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Bachem Holding AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PROTEINASE; SYNTHETIC PEPTIDE; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; HERPES VIRUS SAIMIRI; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; KAPOSI SARCOMA; MOLECULAR CLONING; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ISOLATION; SEQUENCE HOMOLOGY; VIRUS ASSEMBLY; VIRUS GENE;

EID: 1842292816     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.9.7030-7038.1997     Document Type: Article

References (70)

1. Albrecht, J.-C., J. Nicholas, D. Biller, K. R. Cameron, B. Biesinger, C. Newman, S. Wittmann, M. A. Craxton, H. Coleman, B. Fleckenstein, and R. W. Honess. 1992. Primary structure of the herpesvirus saimiri genome. J. Virol. 66:5047-5058.
2. Ambroziak, J. A., D. J. Blackbourn, B. G. Herndier, R. G. Glogau, J. H. Gullett, A. R. McDonald, E. T. Lennette, and J. A. Levy. 1995. Herpes-like sequences in HIV-infected and uninfected Kaposi's sarcoma patients. Science 268:582-583.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1990. Current protocols in molecular biology. Wiley & Sons, New York, N.Y.
4. Babé, L. M., J. Rosé, and C. S. Craik. 1992. Synthetic "interface" peptides alter dimeric assembly of the HIV 1 and 2 proteases. Protein Sci. 1:1244-1253.
5. Beral, V. 1991. Epidemiology of Kaposi's sarcoma. Cancer Surv. 10:5-22. (Erratum, 12:225, 1992.)
6. Beral, V., T. A. Peterman, R. L. Berkelman, and H. W. Jaffe. 1990. Kaposi's sarcoma among persons with AIDS: a sexually transmitted infection? Lancet 335:123-128.
7. Boshoff, C., T. F. Schulz, M. M. Kennedy, A. K. Graham, C. Fisher, A. Thomas, J. O. McGee, R. A. Weiss, and J. J. O'Leary. 1995. Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells. Nat. Med. 1:1274-1278.
8. Burck, P. J., D. H. Berg, T. P. Luk, L. M. Sussmannshausen, M. Wakulchik, D. P. Smith, H. M. Hsiung, G. W. Becker, W. Gibson, and E. C. Villarreal. 1994. Human cytomegalovirus maturational proteinase: expression in Escherichia coli, purification, and enzymatic characterization by using peptide substrate mimics of natural cleavage sites. J. Virol. 68:2937-2946.
9. Chang, Y., E. Cesarman, M. S. Pessin, F. Lee, J. Culpepper, D. M. Knowtes, and P. S. Moore. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
10. Chen, P., H. Tsuge, R. J. Almassy, C. L. Gribskov, S. Katoh, D. L. Venderpool, S. A. Margosiak, C. Pinko, D. A. Matthews, and C. C. Kan. 1996. Structure of the human cytomegalovirus protease catalytic domain reveals a novel serine protease fold and catalytic triad. Cell 86:835-843.
11. Chuck, S., R. M. Grant, E. Katongole-Mbidde, M. Conant, and D. Ganem. 1996. Frequent presence of a novel herpesvirus genome in lesions of human immunodeficiency virus-negative Kaposi's sarcoma. J. Infect. Dis. 173:248-251.
12. Cole, J. L. 1996. Characterization of human cytomegalovirus protease dimerization by analytical centrifugation, Biochemistry 35:15601-15610
13. Condra, J. H., W. A. Schleif, O. M. Blahy, L. J. Gabryelski, D. J. Grahm, J. C. Quintero, A. Rhodes, H. L. Robbins, E. Roth, M. Shivoprakash, et al. 1995. In vivo emergence of HIV-1 variants resistant to multiple protease inhibitors. Nature 374:569-571.
14. Cox. G. A., M. Wakulchik, L. M. Sassmannshausen, W. Gibson, and E. C. Villarreal. 1995. Human cytomegalovirus proteinase: candidate glutamic acid identified as third member of putative active-site triad. J. Virol. 69: 4524-4528.
15. Craik, C. S., S. Roczniak, C. Largmun, and W. J. Rutter. 1987. The catalytic role of the active site aspartic acid in serine proteases. Science 237:909-913.
16. Darke, P. L., J. L, Cole, L. Waxman, D. L. Hall, M. K. Surdana, and L. C. Kuo. 1996. Active human cytomegalovirus protease is a dimer. J. Biol. Chem. 271:7445-7449.
17. 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.
18. Dilanni, C. L., J. T. Stevens, M. Bolgar, D. R. O'Boyle, S. P. 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.
19. Dilannl, C. L., C. Mapelli, D. A. Drier, J. Tsao, S. Natarajan, D. Riexinger, S. M. Festin, M. Bolgar, G. Yamanaka, S. P. Weinheimer, C. A. Meyers, R. J Colonno, and M. G. Cordingley. 1993. In vitro activity of the herpes simplex virus type 1 protease with peptide substrates. J. Biol. Chem. 268:25449-25454.
20. Ensoli, B., G. Barillari, and R. C Gallo. 1991. Pathogenesis of AIDSassociated Kaposi's sarcoma. Hematol. Oneol. Clin. N. Am. 5:281-295.
21. Evnin, L. B., J. R. Vasquez, and C. S. Craik. 1990. Substrate specificity of trypsin investigated by using a genetic selection. Proc. Natl. Acad. Sci. USA 87:6659-6663.
22. Ganem, D. 1994. Viruses, cytokines and Kaposi's sarcoma. Curr. Biol. 5:4693.
23. Gao, M., L. Matusick-Kumar, W. Hurlburt, S. F. DiTusa, W. W. Newcomb, J. C. Brown, P. J. McCann III, I. 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.
24. Gao, S. J., L. Kingsley, M. Li, W. Zheng, C. Parravicini, J. Ziegler, R. Newton, C. R. Rinaldo, A. Saah, J. Phair, R. Detels, Y. Chang, and P. S. Moore. 1996. KSHV antibodies among Americans, Italians and Ugandans with and without Kaposi's sarcoma. Nat. Med. 2:925-928.
25. Gibson, W. 1981. Structural and nonstructural proteins of strain Colburn cytomegalovirus. Virology 111:516-537.
26. Gibson, W., A. I. Marcy, J. C. Comolli. 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.
27. 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.
28. Gibson, W., A. R. Welch, and M. R. T. Hall. 1994. Assemblin, a herpes virus serine maturational proteinase and new molecular target for antivirals. Perspect. Drug Discov. Desn. 2:413-426.
29. Hall, D. L., and P. L. Darke. 1995. Activation of the herpes simplex virus type 1 protease. J. Biol. Chem. 270:22697-22700.
30. Holskin, B. P., M. Bukhtiyarova, B. M. Dunn, P. Baur, J. de Chastonay, and M. W. Pennington. 1995. A continuous fluorescence-based assay of human cytomegalovirus proteasc using a peptide substrate. Anal. Biochem. 227: 148-155.
31. Holwerda, B. C., 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.
32. Hong, Z., M. Beaudet-Miller, J. Durkin, R. Zhang, and A. D. Kwong. 1996. Identification of a minimal hydrophobic 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.
33. Huang, Y. Q., J. J. Li, M. H. Kaplan, B. Poiesz, E. Katabira, W. C. Zhang, D. Feiner, and A. E. Friedman-Kien. 1995. Human herpesvirus-like nucleic acid in various forms of Kaposi's sarcoma. Lancet 345:759-761.
34. Irmiere, A., and W. Gibson. 1985. Isolation of human cytomegalovirus intranuclear capsids, characterization of their protein constituents, and demonstration that the B-capsid assembly protein is also abundant in noninfectious enveloped particles. J. Virol. 56:277-283.
35. Junker, U., S. Escaich, I. Plavec, J. Baker, F. McPhee, J. R. Rosé, C. S. Craik, and E. Böhnlein. 1996. Intracellular expression of human immunodeficiency virus type 1 (HIV-1) protease varíants ínhíbíts replícatíon of wíld-type and protease inhibitor-resistant HIV-1 strains in human T-cell lines. J. Virol. 70:7765-7772.
36. Kaiser, E., R. L. Colescott, C. D. Bossinger, and P. I. Cook. 1970. Color test for detection of free terminal amino groups in the solid-phase synthesis of peptides. Anal. Biochem. 34:595-598.
37. Kedes, D. H., E. Operskalski, M. Busch, R. Kohn, J. Flood, and D. Ganem. 1996. The seroepidemiology of human herpesvirus 8 (Kaposi's sarcomaassociated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission. Nat. Med. 2:918-924. (Comments.)
38. King, D. S., C. G. Fields, and G. B. Fields. 1990. A cleavage method which minimizes side reactions following Fmoc solid phase peptide synthesis. Int. J. Pept. Protein Res. 36:255-266.
39. 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.
40. Liu, F. Y., 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.
41. Loutsch, J. M., N. J, Galvin, M. L. Bryant, and B. C. Holwerda. 1994. Cloning and sequence analysis of murine cytomegalovirus protease and capsid assembly protein genes. Biochem. Biophys. Res. Commun. 203:472-478.
42. McPhee, F., A. C. Good, I. D. Kuntz, and C. S. Craik, 1996. Engineering HIV-1 protease heterodimers as macromolecular inhibitors of viral maturation. Proc. Natl. Acad. Sci. USA 93:11477-11481.
43. Moore, P., L. Kingsley, S. Holmberg, T. Spira, P. Gupta, D. Hoover, J. Parry, L. Conley, H. Jaffe, and Y. Chang. 1995. Kaposi's sarcoma-associated herpesvirus infection prior to onset of Kaposi's sarcoma. AIDS 10:175-180.
44. Moore, P. S., and Y, Chang. 1995. Detection of herpesvirus-like DNA sequences in Kaposi's sarcoma in patients with and without HIV infection. N. Engl. J. Mod. 332:1181-1185.
45. Moore, P. S., S. J. Gao, G. Dominguez, E. Cesarman, O. Lungu, D. M. Knowles, R. Garber, P. E. Pellett, D. J. MeGeoch, and Y. Chang. 1996. Primary characterization of a herpesvirus agent associated with Kaposi's sarcoma. J. Virol. 70:549-558.
46. Nagase, H., C. G, Fields, and G. B, Fields. 1994. Design and characterization of a fluorogenic substrate selectively hydrolyzed by stromelysin 1 (matrix metalloproteinase-3). J. Biol. Chem.269:20952-20957.
47. Nicholson, P., C. Addison, A. M. Cross, and J. Kennard. 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.
48. O'Callaghan, D. J., and C. C. Randall, 1976, Molecular anatomy of herpesviruses: recent studies. Prog. Med. Virol. 22:152-210.
49. Perona, J. J., and C. S. Craik. 1995. Structural basis of substrate specificity in the serine proteases. Protein Sci. 4:337-360.
50. Preston, V. G., M. F. al-Kobaísí, I. M. McDougall, and F. J. Rixon. 1994. The herpes simplex virus gene UL26 proteinase in the presence of the UL26.5 gene product promotes the formation of scaffold-like structures. J. Gen. Virol. 75:2355-2366.
51. Preston, V. G., J. A. 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.
52. Preston, V. G., F. J. Rixon, I. M. McDougall, M. McGregor, and M. F. al-Kobaisi. 1992. Processing of the herpes simplex virus assembly protein ICP35 near its carboxy terminal end requires the product of the whole of the UL26 reading frame. Virology 186:87-98.
53. Qiu, X., J. S. Culp, A. G. DiLella, B. Hellmig, S. S. Hoog, C. A. Janson, W. W. Smith, and S. S. Abdel-Meguid. 1996. Unique fold and active site in cytomegalovirus protease. Nature 383:275-279.
54. Renne, R., W. Zhong, B. Henudier, M. McGrath, N. Abbey, D. Kedes, and D. Ganem. 1996. Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat. Med. 2:342-346.
55. 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.
56. Russo, J. J., R. A. Bohenzky, M.-C. Chien, J. Chen, M. Yan, U. Maddalena, J. P. P. Parry, D. Peruzzi, I. S. Edelman, Y. Chang, and P. S. Moore. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. USA 93:14862-14867.
57. Schalling, M., M. Ekman, E. E. Kaaya, A. Linde, and P. Biberfeld. 1995. A role for a new herpes virus (KSHV) in different forms of Kaposi's sarcoma. Nat. Med. 1:705-706.
58. Schechter, I., and A. Berger. 1968. On the active site of proteases. 3. Mapping the active site of papain: specific peptide inhibitors of papain. Biochem. Biophys. Res. Commun. 32:898-902.
59. Sherman, G., and S. L. Bachenheimer. 1988. Characterization of intranuclear capsids made by ts morphogenic mutants of HSV-1. Virology 163:471-480.
60. Shieh, H. S., R. G. Kurumbail, A. M. Stevens, R. A. Stegeman, E. J. Sturman, J. Y. Pak, A. J. Wittwer, M. O. Palmier, R. C. Wiegand, B. C. Holwerda, and W. C. Stallings. 1996. Three-dimensional structure of human cytomegalovirus protease. Nature 383:279-282.
61. Soulier, J., L. Grollet, E. Oksenhendler, P. Cacoub, D. Cazals-Hatem, P. Babinet, M. F. d'Agay, J. P. Clauvel, M. Raphael, L. Degos, et al. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86:1276-1280.
62. Stevens, J. T., C. Mapelli, J. Tsao, M. Hall, D. N. O'Boyle, S. P. Weinheimer, and C. L. Diianni. 1994. In vitro proteolytic activity and active-site identification of the human cytomegalovirus protease. Eur. J. Biochem. 226:361-367.
63. Thomsen, D. R., L. L. Roof, and F. L. Homa. 1994. Assembly of herpes simplex virus (HSV) intermediate capsids in insect cells infected with recombinant baculoviruses expressing HSV capsid proteins. J. Virol. 68:2442-2457.
64. Tigue, N. J., P. J. Matharu, N. A. Roberts, J. S. Mills, J. Kay, and R. Jupp. 1996. Cloning, expression and characterization of the proteinase from human herpesvirus 6. J. Virol. 70:4136-4141.
65. Tong, L., C. Qian, M. J. Massariol, P. R. Bonneau, M. G. Cordingley, and L. Lagace. 1996. A new scrine-protease fold revealed by the crystal structure of human cytomegalovirus protease. Nature 383:272-275.
66. 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 ossible catalytic silc serine and histidine. J. Virol. 67:7360-7372.
67. Welch, A. R., A. S. Woods, L. M. McNally, R. J. Cotter, and W. Gibson. 1991. A herpesvirus maturational proteinase, assemblin: identification of its gene, putative active site domain, and cleavage site. Proc. Natl. Acad. Sci. USA 88:10792-10796.
68. Whitby, D., M. R. Howard, M. Tenant-Flowers, N. S. Brink, A. Copas, C. Boshoff, T. Hatzioannou, F. E. Suggett, D. M. Aldam, A. S. Denton, et al. 1995. Detection of Kaposi sarcoma associated herpesvirus in peripheral blood of HIV-infected individuals and progression to Kaposi's sarcoma. Lancet 346:799-802.
69. Wood, L. J., M. K. Baxter, S. M. Plafker, and W. Gibson. 1997. Human cytomegalovirus capsid assembly protein precursor (pUL80.5) interacts with itself and with the major capsid protein (pUL86) through two different domains. J. Virol. 71:179-190.
70. Zhong, W., H. Wang, B. Herndier, and D. Ganem. 1996. Restricted expression of Kaposi sarcoma-associated herpesvirus (human herpesvirus B) genes in Kaposi sarcoma. Proc. Natl. Acad. Sci. USA 93:6641-6646.