Identification of Structural Mechanisms of HIV-1 Protease Specificity Using Computational Peptide Docking: Implications for Drug Resistance

Structure

Volumn 17, Issue 12, 2009, Pages 1636-1648

  Chaudhury, Sidhartha ^a   Gray, Jeffrey J ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b Johns Hopkins University   (United States)

Author keywords

HUMDISEASE; MICROBIO; PROTEINS

Indexed keywords

AMPRENAVIR; ATAZANAVIR; INDINAVIR; LOPINAVIR; NELFINAVIR; PROTEINASE; RITONAVIR; SAQUINAVIR;

AMINO ACID SEQUENCE; ANTIVIRAL RESISTANCE; ARTICLE; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HUMAN IMMUNODEFICIENCY VIRUS 1; MATHEMATICAL ANALYSIS; MOLECULAR DOCKING; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN INTERACTION;

ALGORITHMS; DRUG RESISTANCE, VIRAL; HIV PROTEASE; MODELS, MOLECULAR; PEPTIDES; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 71049127018     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2009.10.008     Document Type: Article

References (61)

1. Altman M.D., Ali A., Reddy G.S., Nalam M.N., Anjum S.G., Cao H., Chellappan S., Kairys V., Fernandes M.X., Gilson M.K., et al. HIV-1 protease inhibitors from inverse design in the substrate envelope exhibit subnanomolar binding to drug-resistant variants. J. Am. Chem. Soc. 130 (2008) 6099-6113
2. Altman M.D., Nalivaika E.A., Prabu-Jeyabalan M., Schiffer C.A., and Tidor B. Computational design and experimental study of tighter binding peptides to an inactivated mutant of HIV-1 protease. Proteins 70 (2008) 678-694
3. Bagossi P., Sperka T., Feher A., Kadas J., Zahuczky G., Miklossy G., Boross P., and Tozser J. Amino acid preferences for a critical substrate binding subsite of retroviral proteases in type 1 cleavage sites. J. Virol. 79 (2005) 4213-4218
4. Beck Z.Q., Lin Y.C., and Elder J.H. Molecular basis for the relative substrate specificity of human immunodeficiency virus type 1 and feline immunodeficiency virus proteases. J. Virol. 75 (2001) 9458-9469
5. Beck Z.Q., Morris G.M., and Elder J.H. Defining HIV-1 protease substrate selectivity. Curr. Drug Targets 2 (2002) 37-50
6. Chattopadhyay D., Evans D.B., Deibel Jr. M.R., Vosters A.F., Eckenrode F.M., Einspahr H.M., Hui J.O., Tomasselli A.G., Zurcher-Neely H.A., Heinrikson R.L., et al. Purification and characterization of heterodimeric human immunodeficiency virus type 1 (HIV-1) reverse transcriptase produced by in vitro processing of p66 with recombinant HIV-1 protease. J. Biol. Chem. 267 (1992) 14227-14232
7. Chaudhury S., and Gray J.J. Conformer selection and induced fit in flexible backbone protein-protein docking using computational and NMR ensembles. J. Mol. Biol. 381 (2008) 1068-1087
8. Chellappan S., Kairys V., Fernandes M.X., Schiffer C., and Gilson M.K. Evaluation of the substrate envelope hypothesis for inhibitors of HIV-1 protease. Proteins 68 (2007) 561-567
9. Chellappan S., Kiran Kumar Reddy G.S., Ali A., Nalam M.N., Anjum S.G., Cao H., Kairys V., Fernandes M.X., Altman M.D., Tidor B., et al. Design of mutation-resistant HIV protease inhibitors with the substrate envelope hypothesis. Chem. Biol. Drug Des. 69 (2007) 298-313
10. Chou K.C. Prediction of human immunodeficiency virus protease cleavage sites in proteins. Anal. Biochem. 233 (1996) 1-14
11. Dauber D.S., Ziermann R., Parkin N., Maly D.J., Mahrus S., Harris J.L., Ellman J.A., Petropoulos C., and Craik C.S. Altered substrate specificity of drug-resistant human immunodeficiency virus type 1 protease. J. Virol. 76 (2002) 1359-1368
12. Debouck C., Gorniak J.G., Strickler J.E., Meek T.D., Metcalf B.W., and Rosenberg M. Human immunodeficiency virus protease expressed in Escherichia coli exhibits autoprocessing and specific maturation of the gag precursor. Proc. Natl. Acad. Sci. USA 84 (1987) 8903-8906
13. Doyon L., Croteau G., Thibeault D., Poulin F., Pilote L., and Lamarre D. Second locus involved in human immunodeficiency virus type 1 resistance to protease inhibitors. J. Virol. 70 (1996) 3763-3769
14. Dunbrack Jr. R.L., and Cohen F.E. Bayesian statistical analysis of protein side-chain rotamer preferences. Protein Sci. 6 (1997) 1661-1681
15. Eizert H., Bander P., Bagossi P., Sperka T., Miklossy G., Boross P., Weber I.T., and Tozser J. Amino acid preferences of retroviral proteases for amino-terminal positions in a type 1 cleavage site. J. Virol. 82 (2008) 10111-10117
16. Engh R.A., and Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallogr. A 47 (1991) 392-400
17. Gray J.J., Moughon S., Wang C., Schueler-Furman O., Kuhlman B., Rohl C.A., and Baker D. Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. J. Mol. Biol. 331 (2003) 281-299
18. Hao J., Serohijos A.W., Newton G., Tassone G., Wang Z., Sgroi D.C., Dokholyan N.V., and Basilion J.P. Identification and rational redesign of peptide ligands to CRIP1, a novel biomarker for cancers. PLoS Comput. Biol. 4 (2008) e1000138
19. Hellen C.U., Krausslich H.G., and Wimmer E. Proteolytic processing of polyproteins in the replication of RNA viruses. Biochemistry 28 (1989) 9881-9890
20. Ho S.K., Coman R.M., Bunger J.C., Rose S.L., O'Brien P., Munoz I., Dunn B.M., Sleasman J.W., and Goodenow M.M. Drug-associated changes in amino acid residues in Gag p2, p7(NC), and p6(Gag)/p6(Pol) in human immunodeficiency virus type 1 (HIV-1) display a dominant effect on replicative fitness and drug response. Virology 378 (2008) 272-281
21. Humphris E.L., and Kortemme T. Design of multi-specificity in protein interfaces. PLoS Comput. Biol. 3 (2007) e164
22. Kim H., Zhang Y., Heo Y.S., Oh H.B., and Chen S.S. Specificity rule discovery in HIV-1 protease cleavage site analysis. Comput. Biol. Chem. 32 (2008) 71-78
23. King N.M., Prabu-Jeyabalan M., Nalivaika E.A., and Schiffer C.A. Combating susceptibility to drug resistance: lessons from HIV-1 protease. Chem. Biol. 11 (2004) 1333-1338
24. Kontijevskis A., Prusis P., Petrovska R., Yahorava S., Mutulis F., Mutule I., Komorowski J., and Wikberg J.E. A look inside HIV resistance through retroviral protease interaction maps. PLoS Comput. Biol. 3 (2007) e48
25. Kontijevskis A., Wikberg J.E., and Komorowski J. Computational proteomics analysis of HIV-1 protease interactome. Proteins 68 (2007) 305-312
26. Kortemme T., and Baker D. A simple physical model for binding energy hot spots in protein-protein complexes. Proc. Natl. Acad. Sci. USA 99 (2002) 14116-14121
27. Krohn A., Redshaw S., Ritchie J.C., Graves B.J., and Hatada M.H. Novel binding mode of highly potent HIV-proteinase inhibitors incorporating the (R)-hydroxyethylamine isostere. J. Med. Chem. 34 (1991) 3340-3342
28. Kuhlman B., and Baker D. Native protein sequences are close to optimal for their structures. Proc. Natl. Acad. Sci. USA 97 (2000) 10383-10388
29. Kurt N., Haliloglu T., and Schiffer C.A. Structure-based prediction of potential binding and nonbinding peptides to HIV-1 protease. Biophys. J. 85 (2003) 853-863
30. Lazaridis T., and Karplus M. Effective energy function for proteins in solution. Proteins 35 (1999) 133-152
31. Lin Y., Lin X., Hong L., Foundling S., Heinrikson R.L., Thaisrivongs S., Leelamanit W., Raterman D., Shah M., Dunn B.M., et al. Effect of point mutations on the kinetics and the inhibition of human immunodeficiency virus type 1 protease: relationship to drug resistance. Biochemistry 34 (1995) 1143-1152
32. Lin Y.C., Beck Z., Lee T., Le V.D., Morris G.M., Olson A.J., Wong C.H., and Elder J.H. Alteration of substrate and inhibitor specificity of feline immunodeficiency virus protease. J. Virol. 74 (2000) 4710-4720
33. Lin Y.C., Beck Z., Morris G.M., Olson A.J., and Elder J.H. Structural basis for distinctions between substrate and inhibitor specificities for feline immunodeficiency virus and human immunodeficiency virus proteases. J. Virol. 77 (2003) 6589-6600
34. Mammano F., Trouplin V., Zennou V., and Clavel F. Retracing the evolutionary pathways of human immunodeficiency virus type 1 resistance to protease inhibitors: virus fitness in the absence and in the presence of drug. J. Virol. 74 (2000) 8524-8531
35. Martinez-Picado J., Savara A.V., Shi L., Sutton L., and D'Aquila R.T. Fitness of human immunodeficiency virus type 1 protease inhibitor-selected single mutants. Virology 275 (2000) 318-322
36. Mendez R., Leplae R., Lensink M.F., and Wodak S.J. Assessment of CAPRI predictions in rounds 3-5 shows progress in docking procedures. Proteins 60 (2005) 150-169
37. Oswald M., and von der Helm K. Fibronectin is a non-viral substrate for the HIV proteinase. FEBS Lett. 292 (1991) 298-300
38. Ozer N., Haliloglu T., and Schiffer C.A. Substrate specificity in HIV-1 protease by a biased sequence search method. Proteins 64 (2006) 444-456
39. Prabu-Jeyabalan M., Nalivaika E., and Schiffer C.A. How does a symmetric dimer recognize an asymmetric substrate? A substrate complex of HIV-1 protease. J. Mol. Biol. 301 (2000) 1207-1220
40. Prabu-Jeyabalan M., Nalivaika E., and Schiffer C.A. Substrate shape determines specificity of recognition for HIV-1 protease: analysis of crystal structures of six substrate complexes. Structure 10 (2002) 369-381
41. Prabu-Jeyabalan M., Nalivaika E.A., King N.M., and Schiffer C.A. Structural basis for coevolution of a human immunodeficiency virus type 1 nucleocapsid-p1 cleavage site with a V82A drug-resistant mutation in viral protease. J. Virol. 78 (2004) 12446-12454
42. Prasad P.A., Kanagasabai V., Arunachalam J., and Gautham N. Exploring conformational space using a mean field technique with MOLS sampling. J. Biosci. 32 (2007) 909-920
43. R Development Core Team. R: A Language and Environment for Statistical Computing (2004), R Foundation for Statistical Computing, Vienna, Austria
44. Rhee S.Y., Gonzales M.J., Kantor R., Betts B.J., Ravela J., and Shafer R.W. Human immunodeficiency virus reverse transcriptase and protease sequence database. Nucleic Acids Res. 31 (2003) 298-303
45. Ridky T.W., Cameron C.E., Cameron J., Leis J., Copeland T., Wlodawer A., Weber I.T., and 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
46. Riviere Y., Blank V., Kourilsky P., and Israel A. Processing of the precursor of NF-kappa B by the HIV-1 protease during acute infection. Nature 350 (1991) 625-626
47. Rohl C.A., Strauss C.E., Misura K.M., and Baker D. Protein structure prediction using Rosetta. Methods Enzymol. 383 (2004) 66-93
48. Sammond D.W., Eletr Z.M., Purbeck C., Kimple R.J., Siderovski D.P., and Kuhlman B. Structure-based protocol for identifying mutations that enhance protein-protein binding affinities. J. Mol. Biol. 371 (2007) 1392-1404
49. Silva A.M., Cachau R.E., Sham H.L., and Erickson J.W. Inhibition and catalytic mechanism of HIV-1 aspartic protease. J. Mol. Biol. 255 (1996) 321-346
50. Sood V.D., and Baker D. Recapitulation and design of protein binding peptide structures and sequences. J. Mol. Biol. 357 (2006) 917-927
51. Surleraux D.L., de Kock H.A., Verschueren W.G., Pille G.M., Maes L.J., Peeters A., Vendeville S., De Meyer S., Azijn H., Pauwels R., et al. Design of HIV-1 protease inhibitors active on multidrug-resistant virus. J. Med. Chem. 48 (2005) 1965-1973
52. Tie Y., Boross P.I., Wang Y.F., Gaddis L., Liu F., Chen X., Tozser J., Harrison R.W., and Weber I.T. Molecular basis for substrate recognition and drug resistance from 1.1 to 1.6 angstroms resolution crystal structures of HIV-1 protease mutants with substrate analogs. FEBS J. 272 (2005) 5265-5277
53. Tomasselli A.G., Sarcich J.L., Barrett L.J., Reardon I.M., Howe W.J., Evans D.B., Sharma S.K., and Heinrikson R.L. Human immunodeficiency virus type-1 reverse transcriptase and ribonuclease H as substrates of the viral protease. Protein Sci. 2 (1993) 2167-2176
54. Tomaszek Jr. T.A., Moore M.L., Strickler J.E., Sanchez R.L., Dixon J.S., Metcalf B.W., Hassell A., Dreyer G.B., Brooks I., Debouck C., et al. Proteolysis of an active site peptide of lactate dehydrogenase by human immunodeficiency virus type 1 protease. Biochemistry 31 (1992) 10153-10168
55. Tozser J., Blaha I., Copeland T.D., Wondrak E.M., and Oroszlan S. Comparison of the HIV-1 and HIV-2 proteinases using oligopeptide substrates representing cleavage sites in Gag and Gag-Pol polyproteins. FEBS Lett. 281 (1991) 77-80
56. Wang W., and Kollman P.A. Computational study of protein specificity: the molecular basis of HIV-1 protease drug resistance. Proc. Natl. Acad. Sci. USA 98 (2001) 14937-14942
57. Wang C., Bradley P., and Baker D. Protein-protein docking with backbone flexibility. J. Mol. Biol. 373 (2007) 503-519
58. Wang C., Schueler-Furman O., and Baker D. Improved side-chain modeling for protein-protein docking. Protein Sci. 14 (2005) 1328-1339
59. You L., Garwicz D., and Rognvaldsson T. Comprehensive bioinformatic analysis of the specificity of human immunodeficiency virus type 1 protease. J. Virol. 79 (2005) 12477-12486
60. Zennou V., Mammano F., Paulous S., Mathez D., and Clavel F. Loss of viral fitness associated with multiple Gag and Gag-Pol processing defects in human immunodeficiency virus type 1 variants selected for resistance to protease inhibitors in vivo. J. Virol. 72 (1998) 3300-3306
61. Zhang Y.M., Imamichi H., Imamichi T., Lane H.C., Falloon J., Vasudevachari M.B., and Salzman N.P. Drug resistance during indinavir therapy is caused by mutations in the protease gene and in its Gag substrate cleavage sites. J. Virol. 71 (1997) 6662-6670