Compensatory Role of Double Mutation N348I/M184V on Nevirapine Binding Landscape: Insight from Molecular Dynamics Simulation

Protein Journal

Volumn 33, Issue 5, 2014, Pages 432-446

  Karubiu, Wilson ^a   Bhakat, Soumendranath ^a   Soliman, Mahmoud E S ^a,b  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

^b Zagazig University   (Egypt)

Author keywords

Molecular dynamics; Nevirapine; Principal component analysis; Residue interaction network; Reverse transcriptase

Indexed keywords

NEVIRAPINE; REVERSE TRANSCRIPTASE, HUMAN IMMUNODEFICIENCY VIRUS 1; RNA DIRECTED DNA POLYMERASE; RNA DIRECTED DNA POLYMERASE INHIBITOR;

BINDING SITE; CHEMISTRY; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; MOLECULAR DYNAMICS; MUTATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; THERMODYNAMICS;

BINDING SITES; HIV REVERSE TRANSCRIPTASE; HIV-1; MOLECULAR DYNAMICS SIMULATION; MUTATION; NEVIRAPINE; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; REVERSE TRANSCRIPTASE INHIBITORS; THERMODYNAMICS;

EID: 84924993292     PISSN: 15723887     EISSN: 15734943     Source Type: Journal    
DOI: 10.1007/s10930-014-9576-8     Document Type: Article

References (45)

1. Das KSSG, Sarafianos SG, Arnold E, Hughes SH, William JL, Lane MD (2004) Encyclopedia of biological chemistry. Elsevier, New York
2. Sarafianos SG, Das K, Hughes SH, Arnold E (2004) Taking aim at a moving target: designing drugs to inhibit drug-resistant HIV-1 reverse transcriptases. Curr Opin Struct Biol 14:716–730
3. Cihlar T, Ray AS (2010) Nucleoside and nucleotide HIV reverse transcriptase inhibitors: 25 years after zidovudine. Antiviral Res 85:39–58
4. Maiga AI, Descamps D, Morand-Joubert L, Malet I, Derache A, Cisse M, Koita V, Akonde A, Diarra B, Wirden M, Tounkara A, Verlinden Y, Katlama C, Costagliola D, Masquelier B, Calvez V, Marcelin A-G (2010) Resistance-associated mutations to etravirine (TMC-125) in antiretroviral-naive patients infected with Non-B HIV-1 Subtypes. Antimicrob Agents Chemother 54:728–733
5. Marcelin A-G, Flandre P, Descamps D, Morand-Joubert L, Charpentier C, Izopet J, Trabaud M-A, Saoudin H, Delaugerre C, Tamalet C, Cottalorda J, Bouvier-Alias M, Bettinger D, Dos Santos G, Ruffault A, Alloui C, Henquell C, Rogez S, Barin F, Signori-Schmuck A, Vallet S, Masquelier B, Calvez V, Grp AARS (2010) Factors associated with virological response to etravirine in nonnucleoside reverse transcriptase inhibitor-experienced HIV-1-infected patients. Antimicrob Agents Chemother 54:72–77
6. Ehteshami M, Goette M (2008) Effects of mutations in the connection and RNase H domains of HIV-1 reverse transcriptase on drug susceptibility. Aids Rev 10:224–235
7. Hachiya A, Kodama EN, Sarafianos SG, Schuckmann MM, Sakagami Y, Matsuoka M, Takiguchi M, Gatanaga H, Oka S (2008) Amino acid mutation N348I in the connection subdomain of human immunodeficiency virus type 1 reverse transcriptase confers multiclass resistance to nucleoside and nonnucleoside reverse transcriptase inhibitors. J Virol 82:3261–3270
8. McCormick AL, Parry CM, Crombe A, Goodall RL, Gupta RK, Kaleebu P, Kityo C, Chirara M, Towers GJ, Pillay D (2011) Impact of the N348I mutation in HIV-1 reverse transcriptase on nonnucleoside reverse transcriptase inhibitor resistance in non-subtype B HIV-1. Antimicrob Agents Chemother 55:1806–1809
9. Brehm JH, Koontz DL, Wallis CL, Shutt KA, Sanne I, Wood R, McIntyre JA, Stevens WS, Sluis-Cremer N, Mellors JW, Team C-SPS (2012) Frequent emergence of N348I in HIV-1 subtype c reverse transcriptase with failure of initial therapy reduces susceptibility to reverse-transcriptase inhibitors. Clin Infect Dis 55:737–745
10. Xu H-T, Colby-Germinario SP, Oliveira M, Han Y, Quan Y, Zanichelli V, Wainberg MA (2014) The connection domain mutation N348I in HIV-1 reverse transcriptase enhances resistance to etravirine and rilpivirine but restricts the emergence of the E138 K resistance mutation by diminishing viral replication capacity. J Virol 88:1536–1547
11. Menendez-Arias L, Betancor G, Matamoros T (2011) HIV-1 reverse transcriptase connection subdomain mutations involved in resistance to approved non-nucleoside inhibitors. Antiviral Res 92:139–149
12. Yap SH, Herman BD, Radzio J, Sluis-Cremer N, Tachedjian G (2012) N348I in HIV-1 reverse transcriptase counteracts the synergy between zidovudine and nevirapine. Jaids J Acquir Immune Defic Syndr 61:153–157
13. Maiga AI, Penugonda S, Katile D, Diallo F, Fofana DB, Berzins B, Maiga MY, Sylla A, Traore HA, Marcelin AG, Calvez V, Tounkara A, Bellosillo N, Murphy R, Taiwo B (2012) Connection domain mutations during antiretroviral treatment failure in mali: frequencies and impact on reverse transcriptase inhibitor activity. Jaids J Acquir Immune Defic Syndr 61:293–296
14. Schuckmann MM, Marchand B, Hachiya A, Kodama EN, Kirby KA, Singh K, Sarafianos SG (2010) The N348I mutation at the connection subdomain of HIV-1 reverse transcriptase decreases binding to nevirapine. J Biol Chem 285:38700–38709
15. Yap S-H, Sheen C-W, Fahey J, Zanin M, Tyssen D, Lima VD, Wynhoven B, Kuiper M, Sluis-Cremer N, Harrigan PR, Tachedjian G (2007) N348I in the connection domain of HIV-1 reverse transcriptase confers zidovudine and nevirapine resistance. Plos Med 4:1887–1900
16. von Wyl V, Ehteshami M, Symons J, Buergisser P, Nijhuis M, Demeter LM, Yerly S, Boeni J, Klimkait T, Schuurman R, Ledergerber B, Goette M, Guenthard HF, Swiss HIVCS (2010) Epidemiological and biological evidence for a compensatory effect of connection domain mutation N348I on M184V in HIV-1 reverse transcriptase. J Infect Dis 201:1054–1062
17. Das K, Martinez SE, Bauman JD, Arnold E (2012) HIV-1 reverse transcriptase complex with DNA and nevirapine reveals non-nucleoside inhibition mechanism. Nat Struct Mol Biol 19:253–259
18. Zhou ZG, Madrid M, Evanseck JD, Madura JD (2005) Effect of a bound non-nucleoside RT inhibitor on the dynamics of wild-type and mutant HIV-1 reverse transcriptase. J Am Chem Soc 127:17253–17260
19. Honarparvar B, Govender T, Maguire GEM, Soliman MES, Kruger HG (2014) Integrated approach to structure-based enzymatic drug design: molecular modeling, spectroscopy, and experimental bioactivity. Chem Rev 114:493–537
20. Bhakat S, Martin AJM, Soliman MES (2014) An integrated molecular dynamics, principal component analysis and residue interaction network approach reveals the impact of M184V mutation on HIV reverse transcriptase resistance to lamivudine. Mol BioSyst 10:2215–2228
21. Martin AJM, Vidotto M, Boscariol F, Di Domenico T, Walsh I, Tosatto SCE (2011) RING: networking interacting residues, evolutionary information and energetics in protein structures. Bioinformatics 27:2003–2005
22. Das K, Martinez SE, Bauman JD, Arnold E (2012) HIV--1 reverse transcriptase complex with DNA and nevirapine reveals non-nucleoside inhibition mechanism. Nat Struct Mol Biol 19:253–259
23. Chamberlain PP, Ren J, Nichols CE, Douglas L, Lennerstrand J, Larder BA, Stuart DI, Stammers DK (2002) Crystal structures of Zidovudine- or Lamivudine-resistant human immunodeficiency virus type 1 reverse transcriptases containing mutations at codons 41, 184, and 215. J Virol 76:10015–10019
24. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612
25. Goetz AW, Williamson MJ, Xu D, Poole D, Le Grand S, Walker RC (2012) Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized born. J Chem Theory Comput 8:1542–1555
26. Case DA, Darden TA, Cheatham III TE, Simmerling CL, Wang J, Duke RE, Luo R, Walker RC, Zhang W, Merz KM, Roberts B, Hayik S, Roitberg A, Seabra G, Swails J, Goetz AW, Kolossváry I, Wong KF, Paesani F, Vanicek J, Wolf RM, Liu J, Wu X, Brozell SR, Steinbrecher T, Gohlke H, Cai Q, Ye X, Wang J, Hsieh M-J, Cui G, Roe DR, Mathews DH, Seetin MG, Salomon-Ferrer R, Sagui C, Babin V, Luchko T, Gusarov S, Kovalenko A, Kollman PA (2012) AMBER 12, University of California, San Francisco
27. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dror RO, Shaw DE (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins Struct Funct Bioinform 78:1950–1958
28. Cieplak P, Cornell WD, Bayly C, Kollman PA (1995) Application of the multimolecule and multiconformational RESP methodology to biopolymers—charge derivation for DNA, RNA, and proteins. J Comput Chem 16:1357–1377
29. Frisch MJ, Trucks G, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR MJ, Vreven T, Kudin KN, Burant JC, MJ, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, EM, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima THY, Kitao O, Nakai H, Klene M, Li X, Knox, JE, Hratchian H, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts RSR, Yazyev O, Austin AJ, Cammi R, Pomelli COJ, Ayala PY, Morokuma K, Voth GA, Salvador PDJ, Zakrzewski VG, Dapprich S, Daniels, AD, SM, Farkas O, Malick DK, Rabuck AD, Raghavachari KFJ, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski JSB, Liu G, Liashenko A, Piskorz P, Komaromi IMR, Fox DJ, Keith T, Al-Laham MA, Peng CY, NA, Challacombe M, Gill PMW, Johnson B, Chen WWM, Gonzalez C, Pople JA (2004) Gaussian Inc., Wallingford
30. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926–935
31. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103:8577–8593
32. Roe DR, Cheatham TE (2013) PTRAJ and CPPTRAJ: software for processing and analysis of molecular dynamics trajectory data. J Chem Theory Comput 9:3084–3095
33. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14:33–38
34. Hou T, Wang J, Li Y, Wang W (2011) Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. Molecular dynamics simulations. J Chem Inf Model 51:69–82
35. Godschalk F, Genheden S, Soderhjelm P, Ryde U (2013) Comparison of MM/GBSA calculations based on explicit and implicit solvent simulations. Phys Chem Chem Phys 15:7731–7739
36. Kollman PA, Massova I, Reyes C, Kuhn B, Huo SH, Chong L, Lee M, Lee T, Duan Y, Wang W, Donini O, Cieplak P, Srinivasan J, Case DA, Cheatham TE (2000) Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 33:889–897
37. Massova I, Kollman PA (2000) Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding. Perspect Drug Discov Des 18:113–135
38. Tsui V, Case DA (2000) Theory and applications of the generalized born solvation model in macromolecular simulations. Biopolymers 56:275–291
39. Onufriev A, Bashford D, Case DA (2000) Modification of the generalized Born model suitable for macromolecules. J Phys Chem B 104:3712–3720
40. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph Model 14:33–38
41. Bakan A, Meireles LM, Bahar I (2011) ProDy: protein dynamics inferred from theory and experiments. Bioinformatics 27:1575–1577
42. Word JM, Lovell SC, LaBean TH, Taylor HC, Zalis ME, Presley BK, Richardson JS, Richardson DC (1999) Visualizing and quantifying molecular goodness-of-fit: small-probe contact dots with explicit hydrogen atoms. J Mol Biol 285:1711–1733
43. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
44. Doncheva NT, Klein K, Domingues FS, Albrecht M (2011) Analyzing and visualizing residue networks of protein structures. Trends Biochem Sci 36:179–182
45. Hachiya AS, Sarafianos K, Stefan G et al (2009) Clinical relevance of substitutions in the connection subdomain and RNase H domain of HIV-1 reverse transcriptase from a cohort of antiretroviral treatment-naive patients. Antiviral Res 82:115–121