Why is substrate peptide binding unsusceptible to multidrug-resistant mutations in HIV-1 protease? A structural and energetic analysis

International Journal of Peptide Research and Therapeutics

Volumn 20, Issue 1, 2014, Pages 43-51

  Ni, Zhong ^a   Chen, Huayou ^a   Qi, Xianghui ^a   Jin, Rongzhong ^b  

^a JIANGSU UNIVERSITY   (China)

^b GUILIN MEDICAL UNIVERSITY   (China)

Author keywords

HIV 1 protease; Inhibitor; Multidrug resistance; Substrate peptide

Indexed keywords

EID: 84893719797     PISSN: 15733149     EISSN: 15733904     Source Type: Journal    
DOI: 10.1007/s10989-013-9365-9     Document Type: Article

References (48)

1. Ali A, Reddy GS, Nalam MN, Anjum SG, Cao H, Schiffer CA, Rana TM (2010) Structure-based design, synthesis, and structure-activity relationship studies of HIV-1 protease inhibitors incorporating phenyloxazolidinones. J Med Chem 53:7699-7708
2. Bashford D, Case DA (2000) Generalized Born models of macromolecular solvation effects. Annu Rev Phys Chem 51:129-152
3. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235-242
4. Beerenwinkel N, Sing T, Lengauer T, Rahnenfuhrer J, Roomp K, Savenkov I, Fischer R, Hoffmann D, Selbig J, Korn K, Walter H, Berg T, Braun P, Fatkenheuer G, Oette M, Rockstroh J, Kupfer B, Kaiser R, Daumer M (2005) Computational methods for the design of effective therapies against drug resistant HIV strains. Bioinformatics 21:3943-3950
5. Cornell WD, Cieplak P, Bayly CI, Kollman PA (1993) Application of RESP charges to calculate conformational energies, hydrogen bond energies, and free energies of solvation. J Am Chem Soc 115:9620-9631
6. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM Jr, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J Am Chem Soc 117:5179-5197
7. Clavel F, Hance AJ (2004) HIV drug resistance. N Engl J Med 350:1023-1035
8. de Oliveira T, Engelbrecht S, Janse van Rensburg E, Gordon M, Bishop K, zur Megede J, Barnett SW, Cassol S (2003) Variability at human immunodeficiency virus type 1 subtype C protease cleavage sites: an indication of viral fitness? J Virol 77:9422-9430
9. Dewar MJS, Zoebisch EG, Healy EF, Stewart JJP (1985) Development and use of quantum mechanical molecular models. 76. AM1: a new general purpose quantum mechanical molecular model. J Am Chem Soc 107:3902-3909
10. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong GM, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang JM, Kollman P (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 24:1999-2012
11. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Zakrzewski VG, Montgomery JA Jr, Stratmann RE, Burant JC, Dapprich S, Millam JM, Daniels AD, Kudin KN, Strain MC, Farkas O, Tomasi J, Barone V, Cossi M, Cammi R, Mennucci B, Pomelli C, Adamo C, Clifford S, Ochterski J, Petersson GA, Ayala PY, Cui Q, Morokuma K, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Cioslowski J, Ortiz JV, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Gomperts R, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Gonzalez C, Challacombe M, Gill PMW, Johnson BG, Chen W, Wong MW, Andres JL, Head-Gordon M, Replogle ES, Pople JA (2003) Gaussian 03. Gaussian Inc., Wallingford
12. Ghosh AK, Sridhar PR, Leshchenko S, Hussain AK, Li J, Kovalevsky AY, Walters DE, Wedekind JE, Grum-Tokars V, Das D, Koh Y, Maeda K, Gatanaga H, Weber IT, Mitsuya H (2006) Structure-based design of novel HIV-1 protease inhibitors to combat drug resistance. J Med Chem 49:5252-5261
13. Ghosh AK, Chapsal BD, Weber IT, Mitsuya H (2008) Design of HIV protease inhibitors targeting protein backbone: an effective strategy for combating drug resistance. Acc Chem Res 41:78-86
14. Gulnik SV, Suvorov LI, Liu B, Yu B, Anderson B, Mitsuya H, Erickson JW (1995) Kinetic characterization and cross-resistance patterns of HIV-1 protease mutants selected under drug pressure. Biochemistry 34:9282-9287
15. Guo X, He D, Liu L, Kuang R, Liu L (2012a) Use of QM/MM scheme to reproduce macromolecule-small molecule noncovalent binding energy. Comput Theor Chem 991:134-140
16. Guo X, He D, Huang L, Liu L, Liu L, Yang H (2012b) Strain energy in enzyme-substrate binding: an energetic insight into the flexibility versus rigidity of enzyme active site. Comput Theor Chem 995:17-23
17. Hou TJ, Yu R (2007) Molecular dynamics and free energy studies on the wild-type and double mutant HIV-1 protease complexed with amprenavir and two amprenavir-related inhibitors: mechanism for binding and drug resistance. J Med Chem 50:1177-1188
18. Hou T, McLaughlin WA, Wang W (2008) Evaluating the potency of HIV-1 protease drugs to combat resistance. Proteins 71:1163-1174
19. Hou T, Zhang W, Wang J, Wang W (2009) Predicting drug resistance of the HIV-1 protease using molecular interaction energy components. Proteins 74:837-846
20. Johnson VA, Calvez V, Gunthard HF, Paredes R, Pillay D, Shafer RW, Wensing AM, Richman DD (2013) Update of the drug resistance mutations in HIV-1: March 2013. Top Antivir Med 21:6-14
21. Kar P, Knecht V (2012) Energetic basis for drug resistance of HIV-1 protease mutants against amprenavir. J Comput Aided Mol Des 26:215-232
22. King NM, Prabu-Jeyabalan M, Nalivaika EA, Schiffer CA (2004) Combating susceptibility to drug resistance: lessons from HIV-1 protease. Chem Biol 11:1333-1338
23. Kovalevsky AY, Tie Y, Liu F, Boross PI, Wang YF, Leshchenko S, Ghosh AK, Harrison RW, Weber IT (2006) Effectiveness of nonpeptide clinical inhibitor TMC-114 on HIV-1 protease with highly drug resistant mutations D30N, I50V, and L90M. J Med Chem 49:1379-1387
24. Krivov GG, Shapovalov MV, Dunbrack RL Jr (2009) Improved prediction of protein side-chain conformations with SCWRL4. Proteins 77:778-795
25. Maschera B, Darby G, Palú G, Wright LL, Tisdale M, Myers R, Blair ED, Furfine ES (1996) Human immunodeficiency virus. Mutations in the viral protease that confer resistance to saquinavir increase the dissociation rate constant of the protease-saquinavir complex. J Biol Chem 271:33231-33235
26. Massova I, Kollman PA (1999) Computational alanine scanning to probe protein-protein interactions: a novel approach to evaluate binding free energies. J Am Chem Soc 121:8133-8143
27. Meher BR, Wang Y (2012) Interaction of I50V mutant and I50L/A71V double mutant HIV-protease with inhibitor TMC114 (darunavir): molecular dynamics simulation and binding free energy studies. J Phys Chem B 116:1884-1900
28. Ni Z, Jin X, Zhou P, Wu Q, Lin XF (2011a) A combination of computational and experimental approaches to investigate the binding behavior of B. sub Lipase A mutants with substrate pNPP. Mol Inf 30:359-367
29. Ni Z, Zhou P, Jin X, Lin XF (2011b) Integrating in silico and in vitro approaches to dissect the stereoselectivity of Bacillus subtilis lipase A toward ketoprofen vinyl ester. Chem Biol Drug Des 78:301-308
30. Ohtaka H, Schön A, Freire E (2003) Multidrug resistance to HIV-1 protease inhibition requires cooperative coupling between distal mutations. Biochemistry 42:13659-13666
31. a predictions. J Chem Theory Comput 7:525-537
32. Partaledis JA, Yamaguchi K, Tisdale M, Blair EE, Falcione C, Maschera B, Myers RE, Pazhanisamy S, Futer O, Cullinan AB (1995) In vitro selection and characterization of human immunodeficiency virus type 1 (HIV-1) isolates with reduced sensitivity to hydroxyethylamino sulfonamide inhibitors of HIV-1 aspartyl protease. J Virol 69:5228-5235
33. Rocchia W, Alexov E, Honig B (2001) Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions. J Phys Chem B 105:6507-6514
34. Sasková KG, Kozísek M, Lepsík M, Brynda J, Rezácová P, Václavíková J, Kagan RM, Machala L, Konvalinka J (2008) Enzymatic and structural analysis of the I47A mutation contributing to the reduced susceptibility to HIV protease inhibitor lopinavir. Protein Sci 17:1555-1564
35. Senn HM, Thiel W (2009) QM/MM methods for biomolecular systems. Angew Chem Int Ed 48:1198-1229
36. Soares EAJM, Santos AFA, Sousa TM, Sprinz E, Martinez AMB, Silveira J, Tanuri A, Soares MA (2007) Differential drug resistance acquisition in HIV-1 of subtypes B and C. PLoS One 2:e730
37. Tian F, Yang L, Lv F, Luo X, Pan Y (2011a) Why OppA protein can bind sequence-independent peptides? A combination of QM/MM, PB/SA, and structure-based QSAR analyses. Amino Acids 40:493-503
38. Tian F, Lv Y, Zhou P, Yang L (2011b) Characterization of PDZ domain-peptide interactions using an integrated protocol of QM/MM, PB/SA, and CFEA analyses. J Comput Aided Mol Des 25:947-958
39. Velazquez-Campoy A, Muzammil S, Ohtaka H, Schön A, Vega S, Freire E (2003) Structural and thermodynamic basis of resistance to HIV-1 protease inhibition: implications for inhibitor design. Curr Drug Targets Infect Disord 3:311-328
40. Vreven T, Byun KS, Komáromi I, Dapprich S, Montgomery JA, Morokuma K, Frisch MJ (2006) Combining quantum mechanics methods with molecular mechanics methods in ONIOM. J Chem Theory Comput 2:815-826
41. Wang J, Morin P, Wang W, Kollman PA (2001) Use of MM-PBSA in reproducing the binding free energies to HIV-1 RT of TIBO derivatives and predicting the binding mode to HIV-1 RT of efavirenz by docking and MM-PBSA. J Am Chem Soc 123:5221-5230
42. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. J Comput Chem 25:1157-1174
43. Wainberg MA, Friedland G (1998) Public health implications of antiretroviral therapy and HIV drug resistance. JAMA 279:1977-1983
44. Weikl TR, Hemmateenejad B (2013) How conformational changes can affect catalysis, inhibition and drug resistance of enzymes with induced-fit binding mechanism such as the HIV-1 protease. Biochim Biophys Acta 1834:867-873
45. Word JM, Lovell SC, Richardson JS, Richardson DC (1999) Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation. J Mol Biol 285:1735-1747
46. Zhou P, Zou J, Tian F, Shang Z (2009a) Fluorine bonding - how does it work in protein-ligand interactions? J Chem Inf Model 49:2344-2355
47. Zhou P, Tian F, Shang Z (2009b) 2D depiction of nonbonding interactions for protein complexes. J Comput Chem 30:940-951
48. Zhou P, Wang C, Ren Y, Yang C, Tian F (2013) Computational peptidology: a new and promising approach to therapeutic peptide design. Curr Med Chem 20:1985-1996