Novel method for probing the specificity binding profile of ligands: Applications to HIV protease

Chemical Biology and Drug Design

Volumn 71, Issue 5, 2008, Pages 387-407

  Sherman, Woody ^a,b,c   Tidor, Bruce ^c,d,e  

^a SCHRÖDINGER INC   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Massachusetts Institute of Technology Cambridge   (United States)

^e USA   (United States)

Author keywords

Binding affinity; Charge optimization; Continuum electrostatics

Indexed keywords

AMPRENAVIR; CATHEPSIN D; INDINAVIR; NELFINAVIR; PEPSTATIN; PROTEINASE; PROTEINASE INHIBITOR; RITONAVIR; SAQUINAVIR; TIPRANAVIR;

ARTICLE; BINDING AFFINITY; CHEMICAL MODIFICATION; DRUG PROTEIN BINDING; DRUG SELECTIVITY; ELECTRICITY; ENZYME CONFORMATION; ENZYME SPECIFICITY; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MUTATION; NONHUMAN; PRIORITY JOURNAL;

ELECTROSTATICS; HIV PROTEASE; HIV PROTEASE INHIBITORS; LIGANDS; METHODS; MOLECULAR CONFORMATION; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 42049099944     PISSN: 17470277     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1747-0285.2008.00659.x     Document Type: Article

References (78)

1. Hartwell L.H., Hopfield J.J., Leibler S., Murray A.W. (1999) From molecular to modular cell biology. Nature 402 (Suppl. C47 C52.
2. Yeh P., Tschumi A., Kishony R. (2006) Functional classification of drugs by properties of their pairwise interactions. Nat Genet 38: 489 494.
3. Kholodenko B. (2006) Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 7: 165 176.
4. Sebolt-Leopold J., English J. (2006) Mechanisms of drug inhibition of signalling molecules. Nature 441: 457 462.
5. Hanks S.K., Quinn A.M., Hunter T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42 52.
6. Freire E. (2002) Designing drugs against heterogeneous targets. Nat Biotech 20: 15 16.
7. Ma C., Chang G. (2004) Structure of the multidrug resistance efflux transporter EmrE from Escherichia coli. Proc Natl Acad Sci USA 10: 2852 2857.
8. Arens M. (2001) Clinically relevant sequence-based genotyping of HBV, HCV, CMV, and HIV. J Clin Virol 22: 11 29.
9. Rossmann M.G., Arnold E., Griffith J.P., Kamer G., Luo M., Smith T.J., Vriend G., Rueckert R.R., Sherry B., McKinlay M.A., Diana G., Otto M. (1987) Common cold viruses. Trends Biochem Sci 12: 313 318.
10. Tomasselli A.G., Heinrikson R.L. (2000) Targeting the HIV-protease in AIDS therapy: a current clinical perspective. Biochim Biophys Acta 1477: 189 214.
11. Wang S., Folkes A., Chuckowree I., Cockcroft X., Sohal S., Miller W., Milton J. et al. (2004) Studies on pyrrolopyrimidines as selective inhibitors of multidrug-resistance-associated protein in multidrug resistance. J Med Chem 47: 1329 1338.
12. Wang S., Wan N.C., Harrison J., Miller W., Chuckowree I., Sohal S., Hancox T.C. et al. (2004) Design and synthesis of new templates derived from pyrrolopyrimidine as selective multidrug-resistance-associated protein inhibitors in multidrug resistance. J Med Chem 47: 1339 1350.
13. Hartman J.L., Garvik B., Hartwell L. (2001) Principles for the buffering of genetic variation. Science 291: 1001 1004.
14. Tong A.H.Y., Evangelista M., Parsons A.B., Xu H., Bader G.D., Page N., Robinson M., Raghibizadeh S., Hogue C.W.V., Bussey H., Andrews B., Tyers M., Boone C. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364 2368.
15. Bursavich M.G., Rich D.H. (2002) Designing non-peptide peptidomimetics in the 21st century: inhibitors targeting conformational ensembles. J Med Chem 45: 541 558.
16. Carlson H.A. (2002) Protein flexibility and drug design: how to hit a moving target. Curr Opin Chem Biol 6: 447 452.
17. Sarkar C.A., Lowenhaupt K., Horan T., Boone T.C., Tidor B., Lauffenburger D.A. (2002) Rational cytokine design for increased lifetime and enhanced potency using pH-activated "histidine switching". Nat Biotechnol 20: 908 913.
18. Friedman A.R., Roberts V.A., Tainer J.A. (1994) Predicting molecular interactions and inducible complementarity: fragment docking of Fab-peptide complexes. Proteins Struct Funct Genet 20: 15 24.
19. Chen Y.Z., Zhi D.G. (2001) Ligand-protein inverse docking and its potential use in the computer search of protein targets of a small molecule. Proteins Struct Funct Genet 43: 217 226.
20. Bolon D., Grant R., Baker T., Sauer R. (2005) Specificity versus stability in computational protein design. Proc Natl Acad Sci USA 102: 12724 12729.
21. Havranek J.J., Harbury P.B. (2003) Automated design of specificity in molecular recognition. Nat Struct Biol 10: 45 52.
22. Kangas E., Tidor B. (2000) Electrostatic specificity in molecular ligand design. J Chem Phys 112: 9120 9131.
23. Lee L.-P., Tidor B. (1997) Optimization of electrostatic binding free energy. J Chem Phys 106: 8681 8690.
24. Kangas E., Tidor B. (1998) Optimizing electrostatic affinity in ligand-receptor binding: theory, computation, and ligand properties. J Chem Phys 109: 7522 7545.
25. Kangas E., Tidor B. (1999) Charge optimization leads to favorable electrostatic binding free energy. Phys Rev E 59: 5958 5961.
26. Kangas E., Tidor B. (2001) Electrostatic complementarity at ligand binding sites: application to chorismate mutase. J Phys Chem B 105: 880 888.
27. Armstrong K., Tidor B., Cheng A. (2006) Optimal charges in lead progression: a structure-based neuraminidase case study. J Med Chem 49: 2470 2477.
28. Lee L.-P., Tidor B. (2001) Barstar is electrostatically optimized for tight-binding to barnase. Nat Struct Biol 8: 73 76.
29. Clark L., Boriack-Sjodin P., Eldredge J., Fitch C., Friedman B., Hanf K., Jarpe M. et al. (2006) Affinity enhancement of an in vivo matured therapeutic antibody using structure-based computational design. Protein Sci 15: 949 960.
30. Debouck C., Metcalf B.W. (1990) Human immunodeficiency virus protease: a target for AIDS therapy. Drug Dev Res 21: 1 17.
31. Wlodawer A., Vondrasek J. (1998) Inhibitors of HIV-1 protease: a major success of structure-assisted drug design. Annu Rev Biophys Biomol Struct 27: 249 284.
32. Andreeva N.S., Rumsh L.D. (2001) Analysis of crystal structures of aspartic proteinases: on the role of amino acid residues adjacent to the catalytic site of pepsin-like enzymes. Protein Sci 10: 2439 2450.
33. Giam C.-Z., Boros I. (1988) In vivo and in vitro autoprocessing in human immunodeficiency virus protease expressed in Escherichia coli. J Biol Chem 263: 14617 14620.
34. Darke P.L., Leu C.-T., Davis L.J., Heimbach J.C., Diehl R.E., Hill W.S., Dixon R.A.F., Sigal I.S. (1989) Human immunodeficiency virus protease: bacterial expression and characterization of the purified aspartic protease. J Biol Chem 264: 2307 2312.
35. Fruton J.S. (2002) A history of pepsin and related enzymes. Q Rev Biol 77: 127 147.
36. Shafer R.W., Stevenson D., Chan B. (1999) Human immunodeficiency virus reverse transcriptase and protease sequence database. Nucleic Acids Res 27: 348 352.
37. Maguire M., Shortino D., Klein A., Harris W., Manohitharajah V., Tisdale M., Elston R., Yeo J., Randall S., Xu F., Parker H., May J., Snowden W. (2002) Emergence of resistance to protease inhibitor amprenavir in human immunodeficiency virus type 1-infected patients: selection of four alternative viral protease genotypes and influence of viral susceptibility to coadministered reverse transcriptase nucleoside inhibitors. Antimicrob Agents Chemother 46: 731 738.
38. Kantor R., Fessel W.J., Zolopa A.R., Israelski D., Shulman N., Montoya J.G., Harbour M., Schapiro J.M., Shafer R.W. (2002) Evolution of primary protease inhibitor resistance mutations during protease inhibitor salvage therapy. Antimicrob Agents Chemother 46: 1086 1092.
39. Perryman A.L., Lin J.-H, McCammon J.A. (2004) HIV-1 protease molecular dynamics of a wild-type and of the V82F/I84V mutant: possible contributions to drug resistance and a potential new target site for drugs. Protein Sci 13: 1108 1123.
40. Scott W.R.P., Schiffer C.A. (2000) Curling of flap tips in HIV-1 protease as a mechanism for substrate entry and tolerance of drug resistance. Structure 8: 1259 1265.
41. Piana S., Carloni P., Rothlisberger U. (2002) Drug resistance in HIV-1 protease: flexibility-assisted mechanism of compensatory mutations. Protein Sci 11: 2393 2402.
42. Perryman A., Lin J., McCammon J.A. (2006) Optimization and computational evaluation of a series of potential active site inhibitors of the V82F/I84V drug-resistant mutant of HIV-1 protease: an application of the relaxed complex method of structure-based drug design. Chem Biol Drug Des 67: 336 345.
43. Wang W., Kollman P.A. (2001) Computational study of protein specificity: the molecular basis of HIV-1 protease drug resistance. Proc Natl Acad Sci USA 98: 14937 14942.
44. Fujinaga M., Chernaia M.M., Tarasova N.I., Mosimann S.C., James M.N.G. (1995) Crystal-structure of human pepsin and its complex with pepstatin. Protein Sci 4: 960 972.
45. Rich D.H., Sun E.T.O. (1980) Mechanism of inhibition of pepsin by pepstatin: effect of inhibitor structure on dissociation constant and time-dependent inhibition. Biochem Pharmacol 29: 2205 2212.
46. Baldwin E.T., Bhat T.N., Gulnik S., Hosur M.V., Sowder R.C., Cachau R.E., Collins J., Silva A.M., Erickson J.W. (1993) Crystal-structures of native and inhibited forms or human cathepsin D - implications for lysosomal targeting and drug design. Proc Natl Acad Sci USA 90: 6796 6800.
47. Pesenti C., Arnone A., Bellosta S., Bravo P., Canavesi M., Corradi E., Frigerio M., Meille S.V., Monetti M., Panzeri W., Viani F., Venturini R., Zanda M. (2001) Total synthesis of a pepstatin analog incorporating two trifluoromethyl hydroxymethylene isosteres (Tfm-GABOB) and evaluation of Tfm-GABOB containing peptides as inhibitors of HIV-1 protease and MMP-9. Tetrahedron 57: 6511 6522.
48. Fitzgerald P.M.D., McKeever B.M., VanMiddlesworth J.F., Springer J.P. (1990) Crystallographic analysis of a complex between human immunodeficiency virus type 1 protease and acetyl-pepstatin at 2.0 Angstroms resolution. J Mol Biol 265: 14209 14229.
49. Prabu-Jeyabalan M., Nalivaika E., Schiffer C.A. (2000) How does a symmetric dimer recognize an asymmetric substrate? A substrate complex of HIV-1 protease. J Mol Biol 301: 1207 1220.
50. Hirsch M.S., Brun-Vezinet F., D'Aquila R.T., Manner S.M., Johnson V.A., Kuritzkes D.R., Loveday C., Mellors J.W., Clotet B., Conway B., Demnter L.M., Vella S., Jacobson D.M., Richman D.D. (2000) Antiretroviral drug resistance testing in adult HIV-1 infection: recommendations of an international AIDS Society-USA Panel. J Am Med Assoc 283: 2417 2426.
51. Kervinen J., Thanki N., Zdanov A., Tino J., Barrish J., Lin P.F., Colonno R., Riccardi K., Samanta H., Wlodawer A. (1996) Structural analysis of the native and drug-resistant HIV-1 proteinases complexed with an aminodiol inhibitor. Protein Pept Lett 3: 399 406.
52. King N.M., Melnick L., Prabu-Jeyabalan M., Nalivaika E.A., Yang S.-S., Gao Y., Nie X., Zepp C., Heefner D.L., Schiffer C.A. (2002) Lack of synergy for inhibitors targeting a multi-drug resistant HIV-1 protease. Protein Sci 11: 418 429.
53. Thaisrivongs S., Skulnick H.I., Turner S.R., Strohbach J.W., Tommasi R.A., Johnson P.D., Aristoff P.A. et al. (1996) Structure-based design of HIV protease inhibitors: sulfonamide-containing 5,6-dihydro-4-hydroxy-2-pyrones as non-peptidic inhibitors. J Med Chem 39: 4349 4353.
54. Gulnik S.V., Surorov L.I., Liu B., Yu B., Anderson B., Mitsuya H., Erickson J.W. (1995) Kinetic characterization and cross-resistance patterns of HIV-1 protease mutants selected under drug pressure. Biochemistry 34: 9282 9287.
55. Schock H.B., Garsky V.M., Kuo L.C. (1996) Mutational anatomy of an HIV-1 protease variant conferring cross-resistance to protease inhibitors in clinical trials: compensatory modulations of binding and activity. J Biol Chem 271: 31957 31967.
56. Sherman W., Day T., Jacobson M., Friesner R., Farid R. (2006) Novel procedure for modeling ligand/receptor induced fit effects. J Med Chem 49: 534 553.
57. Martinez-Picado J., Savara L.V., Sutton L., D'Aquila R.T. (1999) Replicative fitness of protease inhibitor-resistant mutants of human immunodeficiency virus type 1. J Virol 73: 3744 3752.
58. Ermolieff J., Lin X.L., Tang J. (1997) Kinetic properties of saquinavir-resistant mutants of human immunodeficiency virus type 1 protease and their implications in drug resistance in vivo. Biochemistry 36: 12364 12370.
59. Zoete V., Michielin O., Karplus M. (2002) Relationship between sequence and structure of HIV-1 protease inhibitor complexes: a model for the analysis of protein flexibility. J Mol Biol 315: 21 52.
60. Massova I., Kollman P.A. (2000) Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding. Perspect Drug Discov Des 18: 113 135.
61. Obiol-Pardo C., Rubio-Martinez J. (2007) Comparative evaluation of MMPBSA and XSCORE to compute binding free energy in XIAP-peptide complexes. J Chem Inf Model 47: 134 142.
62. Lyne P.D., Lamb M.L., Saeh J.C. (2006) Accurate prediction of the relative potencies of members of a series of kinase inhibitors using molecular docking and MM-GBSA scoring. J Med Chem 49: 4805 4808.
63. GAMS (1993) GAMS - The Solver Manuals. Washington DC: GAMS Development Corporation.
64. Drud A. (1985) CONOPT - a GRG code for large sparse dynamic nonlinear optimization problems. Math Program 31: 153 191.
65. Bernstein F.C., Koetzle T.F., Williams G.J.B., Meyer E.F. Jr., Brice M.D., Rodgers J.R., Kennard O., Shimanouchi T., Tasumi M. (1977) The protein data bank: a computer-based archival file for macromolecular structures. J Mol Biol 112: 535 542.
66. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., Karplus M. (1983) CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 4: 187 217.
67. Momany F.A., Rone R. (1992) Validation of the general-purpose Quanta©3.2/CHARMM(R) force-field. J Comput Chem 13: 888 900.
68. Li Z., Lazaridis T. (2003) Thermodynamics of the ordered water molecule in HIV-1 protease. J Am Chem Soc 125: 6636 6637.
69. Brünger A.T., Karplus M. (1988) Polar hydrogen positions in proteins: empirical energy placement and neutron diffraction comparison. Proteins Struct Funct Genet 4: 148 156.
70. Connolly M.L. (1983) Solvent-accessible surfaces of proteins and nucleic acids. Science 221: 709 713.
71. Bockris J.O'.M., Reddy A.K.N. (1973) Modern Electrochemistry. New York: Plenum.
72. Gilson M.K., Sharp K.A., Honig B.H. (1988) Calculating the electrostatic potential of molecules in solution: method and error assessment. J Comput Chem 9: 327 335.
73. Sharp K.A., Honig B. (1990) Electrostatic interactions in macromolecules: theory and applications. Annu Rev Biophys Biophys Chem 19: 301 332.
74. Sitkoff D., Sharp K.A., Honig B. (1994) Accurate calculation of hydration free energies using macroscopic solvent models. J Phys Chem 98: 1978 1988.
75. Frisch M.J., Trucks G.W., Schlegel H.B., Scuseria G.E., Robb M.A., Cheeseman J.R., Zakrzewski V.G. et al. (1998) Gaussian 98 (Revision A.1). Pittsburgh: Gaussian, Inc.
76. Bayly C.I., Cieplak P., Cornell W.D., Kollman P.A. (1993) A well-behaved electrostatic potential based method using charge restraints for determining atom-centered charges: the RESP model. J Phys Chem 97: 10269 10280.
77. Tawarmalani M., Sahinidis N. (2002) Convexification and Global Optimization in Continuous and Mixed-integer Nonlinear Programming: Theory, Algorithms, Software and Applications. Vol. 65. Nonconvex Optimization and its Applications. Springer.
78. Wallace A.C., Laskowski R.A., Thornton J.M. (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8: 127 134.