Initial cleavage of the human immunodeficiency virus type 1 GagPol precursor by its activated protease occurs by an intramolecular mechanism

Journal of Virology

Volumn 78, Issue 16, 2004, Pages 8477-8485

  Pettit, Steven C ^a   Everitt, Lorraine E ^a   Choudhury, Sumana ^a   Dunn, Ben M ^b   Kaplan, Andrew H ^a,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GAGPOL FUSION PROTEIN; HYBRID PROTEIN; POL PROTEIN; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CONCENTRATION (PARAMETERS); ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME INHIBITION; ENZYME MECHANISM; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROCESSING; VIRUS ASSEMBLY; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ANIMALS; ENZYME ACTIVATION; FUSION PROTEINS, GAG-POL; HIV PROTEASE; HIV-1; HUMANS; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RABBITS; RETICULOCYTES; VIRUS ASSEMBLY;

EID: 3543142335     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.16.8477-8485.2004     Document Type: Article

References (57)

1. Bebenek, K., and T. A. Kunkel. 1989. The use of native T7 DNA polymerase for site-directed mutagenesis. Nucleic Acids Res. 17:5408.
2. Bruice, T. C., and S. Benkovic. 1966. Bioorganic mechanisms, p. 119-125. W. A. Benjamin, New York, N.Y.
3. Burstein, H., D. Bizub, M. Kotler, G. Schatz, V. M. Vogt, and A. M. Skalka. 1992. Processing of avian retroviral gag polyprotein precursors is blocked by a mutation at the NC-PR cleavage site. J. Virol. 66:1781-1785.
4. Campbell, S., R. J. Fisher, E. M. Towler, S. Fox, H. J. Issaq, T. Wolfe, L. R. Phillips, and A. Rein. 2001. Modulation of HIV-like particle assembly in vitro by inositol phosphates. Proc. Natl. Acad. Sci. USA 98:10875-10879.
5. Campbell, S., and A. Rein. 1999. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 73:2270-2279.
6. Carter, C., and G. Zybarth. 1994. Processing of retroviral Gag polyproteins: an in vitro approach. Methods Enzymol. 241:227-253.
7. Co, E., G. Koelsch, Y. Lin, E. Ido, J. A. Hartsuck, and J. Tang. 1994. Proteolytic processing mechanisms of a miniprecursor of the aspartic protease of human immunodeficiency virus type 1. Biochemistry 33:1248-1254.
8. Dautin, N., G. Karimova, and D. Ladant. 2003. Human immunodeficiency virus (HIV) type 1 transframe protein can restore activity to a dimerization-deficient HIV protease variant. J. Virol. 77:8216-8226.
9. Gatlin, J., S. J. Arrigo, and M. G. Schmidt. 1998. HIV-1 protease regulation: the role of the major homology region and adjacent C-terminal capsid sequences. J. Biomed. Sci. 5:305-308.
10. Gorelick, R. J., and L. E. Henderson. 1994. Part III: analyses, p. 2-5. In G. Myers, B. Korber, S. Wain-Hobson, K. T. Jeang, L. Henderson, and G. Pavlakis (ed.), Human retroviruses and AIDS. Los Alamos National Laboratory, Los Alamos, N.Mex.
11. Gulnik, S. V., L. I. Suvorov, B. Liu, B. Yu, B. Anderson, H. Mitsuya, and J. W. Erickson. 1995. Kinetic characterization and cross-resistance patterns of HIV-1 protease mutants selected under drug pressure. Biochemistry 34:9282-9287.
12. Henderson, L. E., R. C. Sowder, T. D. Copeland, S. Oroszlan, and R. E. Benveniste. 1990. Gag precursors of HIV and SIV are cleaved into six proteins found in the mature virions. J. Med. Primatol. 19:411-419.
13. gag and p17MA. J. Virol. 73:1902-1908.
14. Jacks, T., M. D. Power, F. R. Maslarz, P. A. Luciw, P. J. Barr, and H. E. Varmus. 1988. Characterization of ribosomal frame-shifting in HIV-1 gag/ pol expression. Nature (London) 331:280-283.
15. Jencks, W. P. 1975. Binding energy, specificity, and enzymic catalysis: the circe effect. Adv. Enzymol. Relat. Areas Mol. Biol. 43:219-410.
16. Jencks, W. P. 1969. Catalysis in chemistry and enzymology, p. 7-41. McGraw-Hill, New York, N.Y.
17. Kaplan, A. H., J. A. Zack, M. Knigge, D. A. Paul, D. J. Kempf, D. W. Norbeck, and R. Swanstrom. 1993. Partial inhibition of the human immunodeficiency virus type 1 protease results in aberrant virus assembly and the formation of noninfectious particles. J. Virol. 67:4050-4055.
18. Karacostas, V., E. J. Wolffe, K. Nagashima, M. A. Gonda, and B. Moss. 1993. Overexpression of the HIV-1 gag-pol polyprotein results in intracellular activation of HIV-1 protease and inhibition of assembly and budding of virus-like particles. Virology 193:661-671.
19. Kaye, J., and A. Lever. 1996. trans-acting proteins involved in RNA encapsidation and viral assembly in human immunodeficiency virus type 1. J. Virol. 70:880-886.
20. Klabe, R. M., L. T. Bacheler, P. J. Ala, S. Erickson-Viitanen, and J. L. Meek. 1998. Resistance to HIV protease inhibitors: a comparison of enzyme inhibition and antiviral potency. Biochemistry 37:8735-8742.
21. Krausslich, H. G., M. Facke, A. M. Heuser, J. Konvalinka, and H. Zentgraf. 1995. The spacer peptide between human immunodeficiency virus capsid and nucleocapsid proteins is essential for ordered assembly and viral infectivity. J. Virol. 69:3407-3419.
22. Kunkel, T. A., K. Bebenek, and J. McClary. 1991. Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204:125-139.
23. Lee, Y. M., B. Liu, and X. F. Yu. 1999. Formation of virus assembly intermediate complexes in the cytoplasm by wild-type and assembly-defective mutant human immunodeficiency virus type 1 and their association with membranes. J. Virol. 73:5654-5662.
24. Leis, J., D. Baltimore, J. M. Bishop, J. Coffin, E. Fleissner, S. P. Goff, S. Oroszlan, H. Robinson, A. M. Skalka, H. M. Temin, and V. Vogt. 1988. Standardized and simplified nomenclature for proteins common to all retroviruses. J. Virol. 62:1808-1809.
25. Lindhofer, H. K., von der Helm, and H. Nitschko. 1995. In vivo processing of Pr160gag-pol from human immunodeficiency virus type 1 (HIV) in acutely infected, cultured human T-lymphocytes. Virology 214:624-627.
26. Louis, J. M., G. M. Clore, and A. M. Gronenborn. 1999. Autoprocessing of HIV-1 protease is tightly coupled to protein folding. Nat. Struct. Biol. 6:868-875.
27. Louis, J. M., E. M. Wondrak, A. R. Kimmel, P. T. Wingfield, and N. T. Nashed. 1999. Proteolytic processing of HIV-1 protease precursor, kinetics and mechanism. J. Biol. Chem. 274:23437-23442.
28. Mervis, R. J., N. Ahmad, E. P. Lillehoj, M. G. Raum, F. H. Salazar, H. W. Chan, and S. Venkatesan. 1988. The gag gene products of human immunodeficiency virus type 1: alignment within the gag open reading frame, identification of posttranslational modifications, and evidence for alternative gag precursors. J. Virol. 62:3993-4002.
29. Molla, A., M. Korneyeva, Q. Gao, S. Vasavanonda, P. J. Schipper, H. M. Mo, M. Markowitz, T. Chernyavskiy, P. Niu, N. Lyons, A. Hsu, G. R. Granneman, D. D. Ho, C. A. Boucher, J. M. Leonard, D. W. Norbeck, and D. J. Kempf, 1996. Ordered accumulation of mutations in HIV protease confers resistance to ritonavir. Nat. Med. 2:760-766.
30. Moody, M. D., S. C. Pettit, W. Shao, L. Everitt, D. D. Loeb, C. A. Hutchison III, and R. Swanstrom. 1995. A side chain at position 48 of the human immunodeficiency virus type-1 protease flap provides an additional specificity determinant. Virology 207:475-485.
31. Navia, M. A., and B. M. McKeever. 1990. A role for the aspartyl protease from the human immunodeficiency virus type 1 (HIV-1) in the orchestration of virus assembly. Ann. N. Y. Acad. Sci. 616:73-85.
32. Oroszlan, S., and T. B. Luftig. 1990. Retroviral proteinases. Curr. Top. Microbiol. Immunol. 157:153-185.
33. Partin, K., G. Zybarth, L. Ehrlich, M. DeCrombrugghe, E. Wimmer, and C. Carter. 1991. Deletion of sequences upstream of the proteinase improves the proteolytic processing of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 88:4776-4780.
34. Pettit, S. C., S. Guinik, L. Everitt, and A. H. Kaplan. 2003. The dimer interfaces of protease and extra-protease domains influence the activation of protease and the specificity of GagPol cleavage. J. Virol. 77:366-374.
35. Pettit, S. C., G. J. Henderson, C. A. Schiffer, and R. Swanstrom. 2002. Replacement of the P1 amino acid of human immunodeficiency virus type 1 Gag processing sites can inhibit or enhance the rate of cleavage by the viral protease. J. Virol. 76:10226-10233.
36. Pettit, S. C., M. D. Moody, R. S. Wehbie, A. H. Kaplan, P. V. Nantermet, C. A. Klein, and R. Swanstrom. 1994. The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions. J. Virol. 68:8017-8027.
37. Pettit, S. C., J. Simsic, D. D. Loeb, L. Everitt, C. A. Hutchison IH, and R. Swanstrom. 1991. Analysis of retroviral protease cleavage sites reveals two types of cleavage sites and the structural requirements of the P1 amino acid. J. Biol. Chem. 266:14539-14547.
38. Platt, E. J., and O. K. Haffar. 1994. Characterization of human immunodeficiency virus type 1 Pr55gag membrane association in a cell-free system: requirement for a C-terminal domain. Proc. Natl. Acad. Sci. USA 91:4594-4598.
39. Quillent, C., A. M. Borman, S. Paulous, C. Dauguet, and F. Clavel. 1996. Extensive regions of pol are required for efficient human immunodeficiency virus polyprotein processing and particle maturation. Virology 219:29-36.
40. Ratner, L., A. Fisher, L. L. Jagodzinski, H. Mitsuya, R.-S. Liou, R. C. Gallo, and F. Wong-Staal. 1987. Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Res. Hum. Retrovir. 3:57-69.
41. Reil, H., H. Kollmus, U. H. Weidle, and H. Hauser. 1993. A heptanucleotide sequence mediates ribosomal frameshifting in mammalian cells. J. Virol. 67:5579-5584.
42. Richards, A. D., L. H. Phylip, W. G. Farmerie, P. E. Scarborough, A. Alvarez, B. M. Dunn, P. H. Hirel, J. Konvalinka, P. Strop, L. Pavlickova, V. Kostka, and J. Kay. 1990. Sensitive, soluble chromogenic substrates for HIV-1 proteinase. J. Biol. Chem. 265:7733-7736.
43. Schatz, G., I. Pichova, and V. M. Vogt. 1997. Analysis of cleavage site mutations between the NC and PR Gag domains of Rous sarcoma virus. J. Virol. 71:444-450.
44. Schatz, G. W., J. Reinking, J. Zippin, L. K. Nicholson, and V. M. Vogt. 2001. Importance of the N terminus of Rous sarcoma virus protease for structure and enzymatic function. J. Virol. 75:4761-4770.
45. Schechter, I., and A. Berger. 1967. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27:157-162.
46. Sellos-Moura, M., and V. M. Vogt. 1996. Proteolytic activity of purified avian sarcoma and leukemia virus NC-PR protein expressed in Escherichia coli. Virology 221:335-345.
47. Sheng, N., S. C. Pettit, R. J. Tritch, D. H. Ozturk, M. M. Rayner, R. Swanstrom, and S. Erickson-Viitanen. 1997. Determinants of the human immunodeficiency virus type 1 p15NC-RNA interaction that affect enhanced cleavage by the viral protease. J. Virol. 71:5723-5732.
48. Spearman, P., and L. Ratner. 1996. Human immunodeficiency virus type 1 capsid formation in reticulocyte lysates. J. Virol. 70:8187-8194.
49. Stewart, L., and V. M. Vogt. 1994. Proteolytic cleavage at the Gag-Pol junction in avian leukosis virus: differences in vitro and in vivo. Virology 204:45-59.
50. Tomasselli, A. G., M. K. Olsen, J. O. Hui, D. J. Staples, T. K. Sawyer, P. L. Heinrikson, and C. C. Tomich. 1990. Substrate analogue inhibition and active site titration of purified recombinant HIV-1 protease. Biochemistry 29:264-269.
51. Tozser, J., I. Blaha, T. D. Copeland, E. M. Wondrak, and S. Oroszlan. 1991. Comparison of the HIV-1 and HIV-2 proteinases using oligopeptide substrates representing cleavage sites in Gag and Gag-Pol polyproteins. FEBS Lett. 281:77-80.
52. Tozser, J., I. T. Weber, A. Gustchina, I. Blaha, T. D. Copeland, J. M. Louis, and S. Oroszlan. 1992. Kinetic and modeling studies of S3-S3′ subsites of HIV proteinases. Biochemistry 31:4793-4800.
53. Wan, M., M. Takagi, B. N. Loh, X. Z. Xu, and T. Imanaka. 1996. Autoprocessing: an essential step for the activation of HIV-1 protease. Biochem. J. 316:569-573.
54. Wiegers, K., G. Rutter, H. Kottler, U. Tessmer, H. Hohenberg, and H. G. Krausslich. 1998. Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J. Virol. 72:2846-2854.
55. Wondrak, E. M., and J. M. Louis. 1996. Influence of flanking sequences on the dimer stability of human immunodeficiency virus type 1 protease. Biochemistry 35:12957-12962.
56. Xiang, Y., T. W. Ridky, N. K. Krishna, and J. Leis. 1997. Altered Rous sarcoma virus Gag polyprotein processing and its effects on particle formation. J. Virol. 71:2083-2091.
57. Zybarth, G., and C. Carter. 1995. Domains upstream of the protease (PR) in human immunodeficiency virus type 1 Gag-Pol influence PR autoprocessing. J. Virol. 69:3878-3884.