Structural and biochemical studies of retroviral proteases

Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology

Volumn 1477, Issue 1-2, 2000, Pages 16-34

  Wlodawer, Alexander ^a   Gustchina, Alla ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

AIDS; Aspartic protease; Enzyme kinetics; Protein structure; Retrovirus

Indexed keywords

PROTEINASE;

ENZYME KINETICS; ENZYME STRUCTURE, FUNCTION AND VARIABILITY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; RETROVIRUS; REVIEW; SIMIAN IMMUNODEFICIENCY VIRUS;

AMINO ACID SEQUENCE; AVIAN SARCOMA VIRUSES; BINDING SITES; ENDOPEPTIDASES; ENZYME INHIBITORS; HIV-1; HIV-2; IMMUNODEFICIENCY VIRUS, FELINE; INFECTIOUS ANEMIA VIRUS, EQUINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; RETROVIRIDAE; SEQUENCE ALIGNMENT; SIMIAN IMMUNODEFICIENCY VIRUS; SUBSTRATE SPECIFICITY;

EQUIDAE; EQUINE INFECTIOUS ANEMIA VIRUS; FELIDAE; FELINE IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS; ROUS SARCOMA VIRUS; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS; UNIDENTIFIED RETROVIRUS;

EID: 0034615571     PISSN: 01674838     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4838(99)00267-8     Document Type: Review

References (107)

1. Vondrasek J., van Buskirk C.P., Wlodawer A. Database of three-dimensional structures of HIV proteinases. Nat. Struct. Biol. 4:1997;8.
2. Martin J.A. Recent advances in the design of HIV proteinase inhibitors. Antiviral Res. 17:1992;265-278.
3. Tomasselli A.G., Howe W.J., Sawyer T.K., Wlodawer A., Heinrikson R.L. The complexities of AIDS: an assessment of the HIV protease as a therapeutic target. Chim. Oggi. 9:1991;6-27.
4. Winslow D.L., Otto M.J. HIV protease inhibitors. AIDS. 9:1995;S183-S192.
5. Moyle G., Gazzard B. Current knowledge and future prospects for the use of HIV protease inhibitors. Drugs. 51:1996;701-712.
6. Vacca J.P., Condra J.H. Clinically effective HIV-1 protease inhibitors. Drug Discov. Today. 2:1997;261-272.
7. Bischofberger N., Öberg B. Antivirals (HIV) editorial overview. Curr. Opin. Anti-Infect. Invest. Drugs. 1:1999;125-126.
8. Wlodawer A., Erickson J.W. Structure-based inhibitors of HIV-1 protease. Annu. Rev. Biochem. 62:1993;543-585.
9. Fitzgerald P.M., Springer J.P. Structure and function of retroviral proteases. Annu. Rev. Biophys. Biophys. Chem. 20:1991;299-320.
10. Fitzgerald P.M.D. HIV protease-ligand complexes. Curr. Opin. Struct. Biol. 3:1993;868-874.
11. Wlodawer A., Vondrasek J. Inhibitors of HIV-1 protease: a major success of structure-assisted drug design. Annu. Rev. Biophys. Biomol. Struct. 27:1998;249-284.
12. Ratner L., Haseltine W., Patarca R., Livak K.J., Starcich B., Josephs S.F., Doran E.R., Rafalski J.A., Whitehorn E.A., Baumeister K. Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature. 313:1985;277-284.
13. Toh H., Ono M., Saigo K., Miyata T. Retroviral protease-like sequence in the yeast transposon Ty1. Nature. 315:1985;691-691.
14. Kohl N.E., Emini E.A., Schleif W.A., Davis L.J., Heimbach J.C., Dixon R.A., Scolnick E.M., Sigal I.S. Active human immunodeficiency virus protease is required for viral infectivity. Proc. Natl. Acad. Sci. USA. 85:1988;4686-4690.
15. Katoh I., Yoshinaka Y., Rein A., Shibuya M., Odaka T., Oroszlan S. Murine leukemia virus maturation: protease region required for conversion from immature to mature form and for virus infectivity. Virology. 145:1985;280-292.
16. Richards A.D., Roberts R., Dunn B.M., Graves M.C., Kay J. Effective blocking of HIV-1 proteinase activity by characteristic inhibitors of aspartic proteinases. FEBS Lett. 247:1989;113-117.
17. Seelmeier S., Schmidt H., Turk V., von der Helm K. Human immunodeficiency virus has an aspartic-type protease that can be inhibited by pepstatin A. Proc. Natl. Acad. Sci. USA. 85:1988;6612-6616.
18. Loeb D.D., Hutchison C.A., Edgell M.H., Farmerie W.G., Swanstrom R. Mutational analysis of human immunodeficiency virus type 1 protease suggests functional homology with aspartic proteinases. J. Virol. 63:1989;111-121.
19. Shibagaki Y., Chow S.A. Central core domain of retroviral integrase is responsible for target site selection. J. Biol. Chem. 272:1997;8361-8369.
20. Davies D.R. The structure and function of the aspartic proteinases. Annu. Rev. Biophys. Biophys. Chem. 19:1990;189-215.
21. Pearl L.H., Taylor W.R. A structural model for the retroviral proteases. Nature. 329:1987;351-354.
22. Pechik I.V., Gustchina A.E., Andreeva N.S., Fedorov A.A. Possible role of some groups in the structure and function of HIV-1 protease as revealed by molecular modeling studies. FEBS Lett. 247:1989;118-122.
23. N. Andreeva, A consensus template of the aspartic proteinase fold, in: B. Dunn (Ed.), Structure and Function of the Aspartic Proteinases, Plenum Press, New York, 1991, pp. 559-572.
24. Andreeva N.S., Gustchina A.E. On the supersecondary structure of acid proteases. Biochem. Biophys. Res. Commun. 87:1979;32-42.
25. Navia M.A., Fitzgerald P.M., McKeever B.M., Leu C.T., Heimbach J.C., Herber W.K., Sigal I.S., Darke P.L., Springer J.P. Three-dimensional structure of aspartyl protease from human immunodeficiency virus HIV-1. Nature. 337:1989;615-620.
26. Fitzgerald P.M.D., McKeever B.M., VanMiddlesworth J.F., Springer J.P., Heimbach J.C., Leu C.-T., Herber W.K., Dixon R.A.F., Darke P.L. Crystallographic analysis of a complex between human immunodeficiency virus type 1 protease and acetyl-pepstatin at 2.0 Å resolution. J. Biol. Chem. 265:1990;14209-14219.
27. Rao J.K.M., Wlodawer A. Is the pseudo-dyad in retroviral proteinase monomers structural or evolutionary? FEBS Lett. 260:1990;201-205.
28. Weber I.T. Structural alignment of retroviral protease sequences. Gene. 85:1989;565-566.
29. Mildner A.M., Rothrock D.J., Leone J.W., Bannow C.A., Lull J.M., Reardon I.M., Sarcich J.L., Howe W.J., Tomich C.S., Smith C.W. The HIV-1 protease as enzyme and substrate: mutagenesis of autolysis sites and generation of a stable mutant with retained kinetic properties. Biochemistry. 33:1994;9405-9413.
30. Miller M., Jaskólski M., Rao J.K.M., Leis J., Wlodawer A. Crystal structure of a retroviral protease proves relationship to aspartic protease family. Nature. 337:1989;576-579.
31. Jaskólski M., Miller M., Rao J.K.M., Leis J., Wlodawer A. Structure of the aspartic protease from Rous sarcoma retrovirus refined at 2-Å resolution. Biochemistry. 29:1990;5889-5898.
32. Ohlendorf D.H., Foundling S.I., Wendoloski J.J., Sedlacek J., Strop P., Salemme F.R. Structural studies of the retroviral proteinase from avian myeloblastosis associated virus. Proteins. 14:1992;382-391.
33. Wlodawer A., Miller M., Jaskólski M., Sathyanarayana B.K., Baldwin E., Weber I.T., Selk L.M., Clawson L., Schneider J., Kent S.B.H. Conserved folding in retroviral proteases: Crystal structure of a synthetic HIV-1 protease. Science. 245:1989;616-621.
34. Lapatto R., Blundell T., Hemmings A., Overington J., Wilderspin A.F., Wood S., Merson J.R., Whittle P.J., Danley D.E., Geoghegan K.F., Hawrylik S.J., Lee S.E., Scheld K.G., Hobart P.M. X-ray analysis of HIV-1 proteinase at 2.7 Å resolution confirms structural homology among retroviral enzymes. Nature. 342:1989;299-302.
35. Spinelli S., Liu Q.Z., Alzari P.M., Hirel P.H., Poljak R.J. The three-dimensional structure of the aspartyl protease from the HIV-1 isolate BRU. Biochimie. 73:1991;1391-1396.
36. Chen Z., Li Y., Chen E., Hall D.L., Darke P.L., Culberson C., Shafer J.A., Kuo L.C. Crystal structure at 1.9-Å resolution of human immunodeficiency virus (HIV) II protease complexed with L-735,524, an orally bioavailable inhibitor of the HIV proteases. J. Biol. Chem. 269:1994;26344-26348.
37. Wilderspin A.F., Sugrue R.J. Alternative native flap conformation revealed by 2.3 Å resolution structure of SIV proteinase. J. Mol. Biol. 239:1994;97-103.
38. Rose R.B., Craik C.S., Stroud R.M. Domain flexibility in retroviral proteases: structural implications for drug resistant mutations. Biochemistry. 37:1998;2607-2621.
39. Gustchina A., Weber I.T. Comparison of inhibitor binding in HIV-1 protease and in non-viral aspartic proteases: the role of the flap. FEBS Lett. 269:1990;269-272.
40. Ishima R., Freedberg D.I., Wang Y.-X., Louis J.M., Torchia D.A. Flap opening and dimer-interface flexibility in the free and inhibitor bound HIV protease, and their implications for function. Structure. 7:1999;1047-1055.
41. Wlodawer A., Gustchina A., Reshetnikova L., Lubkowski J., Zdanov A., Hui K.Y., Angleton E.L., Farmerie W.G., Goodenow M.M., Bhatt D., Zhang L., Dunn B.M. Structure of an inhibitor complex of the proteinase from feline immunodeficiency virus. Nat. Struct. Biol. 2:1995;480-488.
42. Laco G.S., Schalk-Hihi C., Lubkowski J., Morris G., Zdanov A., Olson A., Elder J.H., Wlodawer A., Gustchina A. Crystal structures of the inactive D30N mutant of feline immunodeficiency virus protease complexed with a substrate and an inhibitor. Biochemistry. 36:1997;10696-10708.
43. Zhao B., Winborne E., Minnich M.D., Culp J.S., Debouck C., Abdel-Meguid S.S. Three-dimensional structure of a simian immunodeficiency virus protease/inhibitor complex. Implications for the design of human immunodeficiency virus type 1 and 2 protease inhibitors. Biochemistry. 32:1993;13054-13060.
44. Rose R.B., Rose J.R., Salto R., Craik C.S., Stroud R.M. Structure of the protease from simian immunodeficiency virus: complex with an irreversible nonpeptide inhibitor. Biochemistry. 32:1993;12498-12507.
45. Gustchina A., Kervinen J., Powell D.J., Zdanov A., Kay J., Wlodawer A. Structure of equine infectious anemia virus proteinase complexed with an inhibitor. Protein Sci. 5:1996;1453-1465.
46. Wu J., Adomat J.M., Ridky T.W., Louis J.M., Leis J., Harrison R.W., Weber I.T. Structural basis for specificity of retroviral proteases. Biochemistry. 37:1998;4518-4526.
47. Darke P.L., Huff J.R. HIV protease as an inhibitor target for the treatment of AIDS. Adv. Pharmacol. 25:1994;399-454.
48. Silva A.M., Cachau R.E., Sham H.L., Erickson J.W. Inhibition and catalytic mechanism of HIV-1 aspartic protease. J. Mol. Biol. 255:1996;321-346.
49. Murthy K.H., Winborne E.L., Minnich M.D., Culp J.S., Debouck C. The crystal structures at 2.2 Å resolution of hydroxyethylene-based inhibitors bound to human immunodeficiency virus type 1 protease show that the inhibitors are present in two distinct orientations. J. Biol. Chem. 267:1992;22770-22778.
50. Dreyer G.B., Lambert D.M., Meek T.D., Carr T.J., Tomaszek T.A. Jr., Fernandez A.V., Bartus H., Cacciavillani E., Hassell A.M., Minnich M. Hydroxyethylene isostere inhibitors of human immunodeficiency virus-1 protease structure-activity analysis using enzyme kinetics, X-ray crystallography, and infected T-cell assays. Biochemistry. 31:1992;6646-6659.
51. Swain A.L., Miller M.M., Green J., Rich D.H., Schneider J., Kent S.B., Wlodawer A. X-ray crystallographic structure of a complex between a synthetic protease of human immunodeficiency virus 1 and a substrate-based hydroxyethylamine inhibitor. Proc. Natl. Acad. Sci. USA. 87:1990;8805-8809.
52. Jaskólski M., Tomasselli A.G., Sawyer T.K., Staples D.G., Heinrikson R.L., Schneider J., Kent S.B., Wlodawer A. Structure at 2.5 Å resolution of chemically synthesized human immunodeficiency virus type 1 protease complexed with a hydroxyethylene-based inhibitor. Biochemistry. 30:1991;1600-1609.
53. Miller M., Geller M., Gribskov M., Kent S.B. Analysis of the structure of chemically synthesized HIV-1 protease complexed with a hexapeptide inhibitor. Part I: Crystallographic refinement of 2 Å data. Proteins. 27:1997;184-194.
54. Rutenber E., Fauman E.B., Keenan R.J., Fong S., Furth P.S., Ortiz de Montellano P.R., Meng E., Kuntz I.D., DeCamp D.L., Salto R. Structure of a non-peptide inhibitor complexed with HIV-1 protease. Developing a cycle of structure-based drug design. J. Biol. Chem. 268:1993;15343-15346.
55. Wlodawer A., Nachman J., Gilliland G.L., Gallagher W., Woodward C. Structure of form III crystals of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 198:1987;469-480.
56. Gustchina A., Sansom C., Prevost M., Richelle J., Wodak S.Y., Wlodawer A., Weber I.T. Energy calculations and analysis of HIV-1 protease-inhibitor crystal structure. Protein Eng. 7:1994;309-317.
57. Miller M., Schneider J., Sathyanarayana B.K., Toth M.V., Marshall G.R., Clawson L., Selk L., Kent S.B.H., Wlodawer A. Structure of complex of synthetic HIV-1 protease with a substrate-based inhibitor at 2.3 Å resolution. Science. 246:1989;1149-1152.
58. Powell D.J., Bur D., Wlodawer A., Gustchina A., Payne S.L., Dunn B.M., Kay J. Expression, characterisation and mutagenesis of the aspartic proteinase from equine infectious anaemia virus. Eur. J. Biochem. 241:1996;664-674.
59. Vacca J.P., Dorsey B.D., Schleif W.A., Levin R.B., McDaniel S.L., Darke P.L., Zugay J., Quintero J.C., Blahy O.M., Roth E. L-735,524: an orally bioavailable human immunodeficiency virus type 1 protease inhibitor. Proc. Natl. Acad. Sci. USA. 91:1994;4096-4100.
60. Priestle J.P., Fassler A., Rosel J., Tintelnot-Blomley M., Strop P., Grutter M.G. Comparative analysis of the X-ray structures of HIV-1 and HIV-2 proteases in complex with CGP 53820, a novel pseudosymmetric inhibitor. Structure. 3:1995;381-389.
61. Weber T.T., Wu J., Adomat J., Harrison R.W., Kimmel A.R., Wondrak E.M., Louis M. Crystallographic analysis of human immunodeficiency virus 1 protease with an analog of the conserved CA-p2 substrate. Interactions with frequently occurring glutamic acid residue at P2′ position of substrates. Eur. J. Biochem. 249:1997;523-530.
62. Kervinen J., Lubkowski J., Zdanov A., Bhatt D., Dunn B.M., Hui K.Y., Powell D.J., Kay J., Wlodawer A., Gustchina A. Toward a universal inhibitor of retroviral proteases: comparative analysis of the interactions of LP-130 complexed with proteases from HIV-1, FIV, and EIAV. Protein Sci. 7:1998;2314-2323.
63. Lange-Savage G., Berchtold H., Liesum A., Budt K.H., Peyman A., Knolle J., Sedlacek J., Fabry M., Hilgenfeld R. Structure of HOE/BAY 793 complexed to human immunodeficiency virus (HIV-1) protease in two different crystal forms-structure/function relationship and influence of crystal packing. Eur. J. Biochem. 248:1997;313-322.
64. Schechter I., Berger A. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27:1967;157-162.
65. Cameron C.E., Grinde B., Jacques P., Jentoft J., Leis J., Wlodawer A., Weber I.T. Comparison of the substrate-binding pockets of the Rous sarcoma virus and human immunodeficiency virus type 1 proteases. J. Biol. Chem. 268:1993;11711-11720.
66. Grinde B., Cameron C.E., Leis J., Weber I.T., Wlodawer A., Burstein H., Skalka A.M. Analysis of substrate interactions of the Rous sarcoma virus wild type and mutant proteases and human immunodeficiency virus-1 protease using a set of systematically altered peptide substrates. J. Biol. Chem. 267:1992;9491-9498.
67. Tözsér J., Weber I.T., Gustchina A., Blaha I., Copeland T.D., Louis J.M., Oroszlan S. Kinetic and modeling studies of S3-S3′ subsites of HIV proteinases. Biochemistry. 31:1992;4793-4800.
68. Dunn B.M., Gustchina A., Wlodawer A., Kay J. Subsite preferences of retroviral proteinases. Methods Enzymol. 241:1994;254-278.
69. Rosin C.D., Belew R.K., Walker W.L., Morris G.M., Olson A.J., Goodsell D.S. Coevolution and subsite decomposition for the design of resistance-evading HIV-1 protease inhibitors. J. Mol. Biol. 287:1999;77-92.
70. Cameron C.E., Ridky T.W., Shulenin S., Leis J., Weber I.T., Copeland T., Wlodawer A., Burstein H., Bizub-Bender D., Skalka A.M. Mutational analysis of the substrate binding pockets of the Rous sarcoma virus and human immunodeficiency virus-1 proteases. J. Biol. Chem. 269:1994;11170-11177.
71. Tözsér J., Friedman D., Weber I.T., Blaha I., Oroszlan S. Studies on the substrate specificity of the proteinase of equine infectious anemia virus using oligopeptide substrates. Biochemistry. 32:1993;3347-3353.
72. Griffiths J.T., Phylip L.H., Konvalinka J., Strop P., Gustchina A., Wlodawer A., Davenport R.J., Briggs R., Dunn B.M., Kay J. Different requirements for productive interaction between the active site of HIV-1 proteinase and substrates containing -hydrophobic*obic- or -aromatic*eavage sites. Biochemistry. 31:1992;5193-5200.
73. Griffiths J.T., Tomchak L.A., Mills J.S., Graves M.C., Cook N.D., Dunn B.M., Kay J. Interactions of substrates and inhibitors with a family of tethered HIV-1 and HIV-2 homo- and heterodimeric proteinases. J. Biol. Chem. 269:1994;4787-4793.
74. Daenke S., Schramm H.J., Bangham C.R. Analysis of substrate cleavage by recombinant protease of human T cell leukaemia virus type 1 reveals preferences and specificity of binding. J. Gen. Virol. 75:1994;2233-2239.
75. Lee T., Laco G.S., Torbett B.E., Fox H.S., Lerner D., Elder J.H., Wong C.-H. Analysis of the S3 and S3′ subsite specificities of feline immunodeficiency virus (FIV) protease: Development of a broad-based protease inhibitor efficacious against FIV, SIV, and HIV in vitro and ex vivo. Proc. Natl. Acad. Sci. USA. 95:1998;939-944.
76. C.E. Cameron, H. Burstein, D. Bizub-Bender, T. Ridky, I.T. Weber, A. Wlodawer, A.M. Skalka, J. Leis, Identification of amino acid residues of the retroviral aspartic proteinases important for substrate specificity and catalytic efficiency, in: K. Takahashi (Ed.), Aspartic Proteinases: Structure, Function, Biology, and Biomedical Implications, Plenum Press, New York, 1995, pp. 399-406.
77. Tözsér J., Gustchina A., Weber I.T., Blaha I., Wondrak E.M., Oroszlan S. Studies on the role of the S4 substrate binding site of HIV proteinases. FEBS Lett. 279:1991;356-360.
78. Smith R., Brereton I.M., Chai R.Y., Kent S.B. Ionization states of the catalytic residues in HIV-1 protease. Nat. Struct. Biol. 3:1996;946-950.
79. Bizub D., Weber I.T., Cameron C.E., Leis J.P., Skalka A.M. A range of catalytic efficiencies with avian retroviral protease subunits genetically linked to form single polypeptide chains. J. Biol. Chem. 266:1991;4951-4958.
80. Cheng Y.S., Yin F.H., Foundling S., Blomstrom D., Kettner C.A. Stability and activity of human immunodeficiency virus protease: comparison of the natural dimer with a homologous, single-chain tethered dimer. Proc. Natl. Acad. Sci. USA. 24:1999;9660-9664.
81. DiIanni C.L., Davis L.J., Holloway M.K., Herber W.K., Darke P.L., Kohl N.E., Dixon R.A. Characterization of an active single polypeptide form of the human immunodeficiency virus type 1 protease. J. Biol. Chem. 265:1990;17348-17354.
82. Bhat T.N., Baldwin E.T., Liu B., Cheng Y.S., Erickson J.W. Crystal structure of a tethered dimer of HIV-1 proteinase complexed with an inhibitor. Nat. Struct. Biol. 1:1994;552-556.
83. Tözsér J., Yin F.H., Cheng Y.S., Bagossi P., Weber I.T., Harrison R.W., Oroszlan S. Activity of tethered human immunodeficiency virus 1 protease containing mutations in the flap region of one subunit. Eur. J. Biochem. 244:1997;235-241.
84. Xiang Y., Ridky T.W., Krishna N.K., Leis J. Altered Rous sarcoma virus Gag polyprotein processing and its effects on particle formation. J. Virol. 71:1997;2083-2091.
85. S.C. Pettit, N. Sheng, R. Tritch, S. Erickson-Viitanen, R. Swanstrom, The regulation of sequential processing of HIV-1 Gag by the viral protease, in: M.N.G. James (Ed.), Aspartic Proteinases, Retroviral and Cellular Enzymes, Plenum Press, New York, 1998, pp. 15-25.
86. Shoeman R.L., Honer B., Stoller T.J., Kesselmeier C., Miedel M.C., Traub P., Graves M.C. Human immunodeficiency virus type 1 protease cleaves the intermediate filament proteins vimentin, desmin, and glial fibrillary acidic protein. Proc. Natl. Acad. Sci. USA. 87:1990;6336-6340.
87. Hui J.O., Tomasselli A.G., Zurcher-Neely H.A., Heinrikson R.L. Ribonuclease A as a substrate of the protease from human immunodeficiency virus-1. J. Biol. Chem. 265:1990;21386-21389.
88. Tomaszek T.A. Jr., Moore M.L., Strickler J.E., Sanchez R.L., Dixon J.S., Metcalf B.W., Hassell A., Dreyer G.B., Brooks I., Debouck C. Proteolysis of an active site peptide of lactate dehydrogenase by human immunodeficiency virus type 1 protease. Biochemistry. 31:1992;10153-10168.
89. Tomasselli A.G., Howe W.J., Hui J.O., Sawyer T.K., Reardon I.M., DeCamp D.L., Craik C.S., Heinrikson R.L. Calcium-free calmodulin is a substrate of proteases from human immunodeficiency viruses 1 and 2. Proteins. 10:1991;1-9.
90. Tomasselli A.G., Hui J.O., Adams L., Chosay J., Lowery D., Greenberg B., Yem A., Deibel M.R., Zurcher-Neely H., Heinrikson R.L. Actin, troponin C, Alzheimer amyloid precursor protein and pro-interleukin 1 beta as substrates of the protease from human immunodeficiency virus. J. Biol. Chem. 266:1991;14548-14553.
91. Poorman R.A., Tomasselli A.G., Heinrikson R.L., Kezdy F.J. A cumulative specificity model for proteases from human immunodeficiency virus types 1 and 2, inferred from statistical analysis of an extended substrate data base. J. Biol. Chem. 266:1991;14554-14561.
92. Ridky T.W., Cameron C.E., Cameron J., Leis J., Copeland T., Wlodawer A., Weber I.T., Harrison R.W. Human immunodeficiency virus, type 1 protease substrate specificity is limited by interactions between substrate amino acids bound in adjacent enzyme subsites. J. Biol. Chem. 271:1996;4709-4717.
93. Chou K.C. A vectorized sequence-coupling model for predicting HIV protease cleavage sites in proteins. J. Biol. Chem. 268:1993;16938-16948.
94. Billich S., Knoop M.T., Hansen J., Strop P., Sedlacek J., Mertz R., Moelling K. Synthetic peptides as substrates and inhibitors of human immune deficiency virus-1 protease. J. Biol. Chem. 263:1988;17905-17908.
95. Cameron C.E., Grinde B., Jentoft J., Leis J., Weber I.T., Copeland T.D., Wlodawer A. Mechanism of inhibition of the retroviral protease by a Rous sarcoma virus peptide substrate representing the cleavage site between the gag p2 and p10 proteins. J. Biol. Chem. 267:1992;23735-23741.
96. Richards A.D., Phylip L.H., Farmerie W.G., Scarborough P.E., Alvarez A., Dunn B.M., Hirel P.H., Konvalinka J., Strop P., Pavlickova L. Sensitive, soluble chromogenic substrates for HIV-1 proteinase. J. Biol. Chem. 265:1990;7733-7736.
97. Matayoshi E.D., Wang G.T., Krafft G.A., Erickson J. Novel fluorogenic substrates for assaying retroviral proteases by resonance energy transfer. Science. 247:1990;954-958.
98. Ridky T.W., Bizub-Bender D., Cameron C.E., Weber I.T., Wlodawer A., Copeland T., Skalka A.M., Leis J. Programming the Rous sarcoma virus protease to cleave new substrate sequences. J. Biol. Chem. 271:1996;10538-10544.
99. Slee D.H., Laslo K.L., Elder J.H., Ollmann I.R., Gustchina A., Kervinen J., Zdanov A., Wlodawer A., Wong C.-H. Selectivity in the inhibition of HIV and FIV protease: inhibitory and mechanistic studies of pyrrolidine-containing a-keto amide and hydroxyethylamine core structures. J. Am. Chem. Soc. 117:1995;11867-11878.
100. Ho D.D., Neumann A.U., Perelson A.S., Chen W., Leonard J.M., Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 373:1995;123-126.
101. Gulnik S.V., Suvorov L.I., Liu B., Yu B., Anderson B., Mitsuya H., Erickson J.W. Kinetic characterization and cross-resistance patterns of HIV-1 protease mutants selected under drug pressure. Biochemistry. 34:1995;9282-9287.
102. Condra J.H., Schleif W.A., Blahy O.M., Gabryelski L.J., Graham D.J., Quintero J.C., Rhodes A., Robbins H.L., Roth E., Shivaprakash M., Titus D., Yang T., Teppler H., Squires K.E., Deutsch P.J., Emini E.A. In vivo emergence of HIV-1 variants resistant to multiple protease inhibitors. Nature. 374:1995;569-571.
103. Schinazi R.F., Larder B.A., Mellors J.W. Mutations in retroviral genes associated with drug resistance. Int. Antiviral News. 5:1997;129-142.
104. Schnolzer M., Rackwitz H.R., Gustchina A., Laco G.S., Wlodawer A., Elder J.H., Kent S.B. Comparative properties of feline immunodeficiency virus (FIV) and human immunodeficiency virus type 1 (HIV-1) proteinases prepared by total chemical synthesis. Virology. 224:1996;268-275.
105. Elder J.H., Schnolzer M., Hasselkus-Light C., Henson M., Lerner D.A., Philips T.R., Wagaman P.C., Kent S.B.H. Identification of proteolytic processing sites within the Gag and Pol polyproteins of feline immunodeficiency virus. J. Virol. 67:1993;1869-1876.
106. V.M. Vogt, Proteolytic processing and particle maturation, in: H.-G. Kräusslich (Ed.), Current Topics in Microbiology and Immunology, Morphogenesis and Maturation of Retroviruses, Springer-Verlag, Berlin, 1996, pp. 95-131.
107. Li M., Morris G.M., Lee T., Laco G.S., Wong C.-H., Olson A.J., Elder J.H., Wlodawer A., Gustchina A. Structural studies of FIV and HIV-1 proteases complexed with an efficient inhibitor of FIV protease. Proteins. 38:2000;29-40.