Mechanisms of anti-retroviral drug resistance: Implications for novel drug discovery and development

Infectious Disorders - Drug Targets

Volumn 13, Issue 5, 2013, Pages 330-336

  Emamzadeh Fard, Sahra ^a,b   Esmaeeli, Shooka ^a,b   Arefi, Khalilullah ^a,b   Moradbeigi, Majedeh ^c   Heidari, Behnam ^a,b   Fard, Sahar E ^d   Paydary, Koosha ^a,b   SeyedAlinaghi, SeyedAhmad ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d Stevens Institute of Technology   (United States)

Author keywords

Anti retroviral; Drug discovery; Drug resistance; HIV infection; NNRTIS

Indexed keywords

4 [(4 BROMOPHENYL)(ETHOXYIMINO)METHYL] 1' [(2,4 DIMETHYL 3 PYRIDINYL)CARBONYL] 4' METHYL 1,4' BIPIPERIDINE; 4 [1 [(2, 4 DIMETHYL 3 PYRIDINYL) CARBONYL] 4 METHYL 4 PIPERIDINYL] 2 METHYL 1 [1[4 (TRIFLUOROMETHYL) PHENYL] ETHYL] PIPERAZINE; 4 [1 [(2,4 DIMETHYL 3 PYRIDINYL)CARBONYL] 4 METHYL 4 PIPERIDINYL] 2 METHYL 1 [1 [4 (TRIFLUOROMETHYL)PHENYL]ETHYL]PIPERAZINE; ANTIRETROVIRUS AGENT; APLAVIROC; BINDING PROTEIN; BMS 626529; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; EFAVIRENZ; GLYCOPROTEIN GP 120; IBALIZUMAB; MARAVIROC; N [3 [4 (3 BENZYL 1 ETHYL 5 PYRAZOLYL) 1 PIPERIDINYLMETHYL] 4 (3 FLUOROPHENYL) CYCLOPENTYL] N METHYLVALINE; N [3 [4 (3 BENZYL 1 ETHYL 5 PYRAZOLYL) 1 PIPERIDINYLMETHYL] 4 (3 FLUOROPHENYL)CYCLOPENTYL] N METHYLVALINE; N [4 [[[6, 7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL] CARBONYL] AMINO] BENZYL] N, N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; N [4 [[[6,7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL]CARBONYL]AMINO]BENZYL] N,N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; PROTEINASE; RIBONUCLEASE H; RILPIVIRINE; RNA DIRECTED DNA POLYMERASE; UNCLASSIFIED DRUG; VICRIVIROC; VIRUS DNA; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; RNA DIRECTED DNA POLYMERASE INHIBITOR;

ANTIVIRAL RESISTANCE; ARTICLE; BINDING AFFINITY; CLINICAL TRIAL (TOPIC); DRUG EFFICACY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYDROGEN BOND; NONHUMAN; VIRUS MUTATION; AMINO ACID SUBSTITUTION; ANTAGONISTS AND INHIBITORS; DRUG DESIGN; DRUG DEVELOPMENT; GENETICS; HIV INFECTIONS; MUTATION; VIROLOGY;

AMINO ACID SUBSTITUTION; ANTI-HIV AGENTS; DRUG DESIGN; DRUG DISCOVERY; DRUG RESISTANCE, VIRAL; HIV INFECTIONS; HIV REVERSE TRANSCRIPTASE; HUMANS; MUTATION; REVERSE TRANSCRIPTASE INHIBITORS;

EID: 84900805412     PISSN: 18715265     EISSN: 18755852     Source Type: Journal    
DOI: 10.2174/1871526514666140321104049     Document Type: Article

References (76)

1. Who, U.; Unicef, Global HIV/AIDS response: Epidemic update and health sector progress towards universal access. Progress report. November, 2011.
2. WHO, WHO HIV Drug Resistance Report 2012.
3. Wittkop, L.; Gunthard, H.F.; De Wolf, F.; Dunn, D.; Cozzi-Lepri, A.; De Luca, A.; Kucherer, C.; Obel, N.; von Wyl, V.; Masquelier, B.; Stephan, C.; Torti, C.; Antinori, A.; Garcia, F.; Judd, A.; Porter, K.; Thiebaut, R.; Castro, H.; Van Sighem, A. I.; Colin, C.; Kjaer, J.; Lundgren, J. D.; Paredes, R.; Pozniak, A.; Clotet, B.; Phillips, A.; Pillay, D.; Chene, G. Effect of transmitted drug resistance on virological and immunological response to initial combination antiretroviral therapy for HIV (EuroCoord-CHAIN joint project): A European multicohort study. Lancet Infect. Dis., 2011, 11(5), 363-371.
4. Razavi, P.; Hajifathalian, K.; Saeidi, B.; Esmaeeli Djavid, G.; Ra-soulinejad, M.; Hajiabdolbaghi, M.; Paydary, K.; Kheirandish, P.; Foroughi, M.; SeyedAlinaghi, S. Quality of life among persons with HIV/AIDS in Iran: Internal reliability and validity of an international instrument and associated factors. AIDS Res. Treat., 2012: 849406.
5. Paydary, K.; Khaghani, P.; Emamzadeh-Fard, S.; Alinaghi, S. A. S.; Baesi, K. The emergence of drug resistant HIV variants and novel anti-retroviral therapy. Asian Pac. J. Trop. Biomed., 2013, 3(7), 515- 522.
6. Jordan, M.; Bennett, D.; Wainberg, M.; Havlir, D.; Hammer, S.; Yang, C.; Morris, L.; Peeters, M.; Wensing, A.; Parkin, N. Update on World Health Organization HIV drug resistance prevention and assessment strategy: 2004-2011. Clin. Infect. Dis., 2012, 54(4), S245-S249.
7. Wheeler, W.H.; Ziebell, R.A.; Zabina, H.; Pieniazek, D.; Prejean, J.; Bodnar, U.R.; Mahle, K.C.; Heneine, W.; Johnson, J.A.; Hall, H.I. Prevalence of transmitted drug resistance associated mutations and HIV-1 subtypes in new HIV-1 diagnoses, U.S. 2006. AIDS (London, England)., 2010, 24(8), 1203-1212.
8. Booth, C.L.; Geretti, A.M. Prevalence and determinants of transmitted antiretroviral drug resistance in HIV-1 infection. J Antimicrob. Chemother., 2007, 59(6), 1047-56.
9. Pillay, D.; Bhaskaran, K.; Jurriaans, S.; Prins, M.; Masquelier, B.; Dabis, F.; Gifford, R.; Nielsen, C.; Pedersen, C.; Balotta, C.; Rezza, G.; Ortiz, M.; de Mendoza, C.; Kucherer, C.; Poggensee, G.; Gill, J.; Porter, K. The impact of transmitted drug resistance on the natural history of HIV infection and response to first-line therapy. AIDS (London, England)., 2006, 20(1), 21-28.
10. Vercauteren, J.; Wensing, A.M.; Van de Vijver, D.A.; Albert, J.; Balotta, C.; Hamouda, O.; Kucherer, C.; Struck, D.; Schmit, J.C.; Asjo, B.; Bruckova, M.; Camacho, R.J.; Clotet, B.; Coughlan, S.; Grossman, Z.; Horban, A.; Korn, K.; Kostrikis, L.; Nielsen, C.; Paraskevis, D.; Poljak, M.; Puchhammer-Stockl, E.; Riva, C.; Ruiz, L.; Salminen, M.; Schuurman, R.; Sonnerborg, A.; Stanekova, D.; Stanojevic, M.; Vandamme, A.M.; Boucher, C.A. Transmission of drug-resistant HIV-1 is stabilizing in Europe. J. Infect. Dis., 2009, 200(10), 1503-1508.
11. Paydary, K.; Esmaeeli, S.; Seyed Alinaghi, S.; Rouzrokh, P.; Emamzadeh-Fard, S. Emerging HIV drug resistance in the resource-poor world: Challenges and strategies. J. AIDS Clin. Res., 2013, S5, 006, 2.
12. Maldarelli, F.; Kearney, M.; Palmer, S.; Stephens, R.; Mican, J.; Polis, M. A.; Davey, R. T.; Kovacs, J.; Shao, W.; Rock-Kress, D. HIV populations are large and accumulate high genetic diversity in nonlinear fashion. J. Virol., 2013, 18(87), 10313-10323
13. Thompson, M.A.; Aberg, J.A.; Cahn, P.; Montaner, J.S.; Rizzardini, G.; Telenti, A.; Gatell, J. M.; Gunthard, H. F.; Hammer, S.M.; Hirsch, M.S.; Jacobsen, D.M.; Reiss, P.; Richman, D.D.; Volberding, P.A.; Yeni, P.; Schooley, R.T. Antiretroviral treatment of adult HIV infection: 2010 recommendations of the International AIDS Society-USA panel. JAMA: J. Am. Med. Assoc., 2010, 304(3), 321-33.
14. Johnson, V. A.; Calvez, V.; Gunthard, H.; Paredes, R.; Pillay, D.; Shafer, R. W.; Wensing, A. M.; Richman, D. D. Update of the drug resistance mutations in HIV-1: March 2013. Top Antivir. Med., 2013, 21, 4-12.
15. Abar, A. E.; Jlizi, A.; Darar, H. Y.; Kacem, M.; Slim, A. HIV-1 drug resistance genotyping from antiretroviral therapy (ART) naïve and first-line treatment failures in djiboutian patients. Dign. Pathol., 2012, 7 (1), 138.
16. Boucher, C.; Cammack, N.; Schipper, P.; Schuurman, R.; Rouse, P.; Wainberg, M.; Cameron, J. High-level resistance to (-) enantiomeric 2'-deoxy-3'-thiacytidine in vitro is due to one amino acid substitution in the catalytic site of human immunodeficiency virus type 1 reverse transcriptase. Antimicrob. Agents Chem., 1993, 37(10), 2231-2234.
17. Phillips, A.; Dunn, D.; Sabin, C.; Pozniak, A.; Matthias, R.; Geretti, A.; Clarke, J.; Churchill, D.; Williams, I.; Hill, T. Long term probability of detection of HIV-1 drug resistance after starting antiretroviral therapy in routine clinical practice. AIDS (London, England)., 2005, 19(5), 487.
18. Theys, K.; Deforche, K.; Libin, P.; Camacho, R.J.; Van Laethem, K.; Vandamme, A.-M. Resistance pathways of human immunodeficiency virus type 1 against the combination of zidovudine and lamivudine. J. Gen.Virol., 2010, 91(8), 1898-1908.
19. Crespan, E.; Locatelli, G.A.; Cancio, R.; Hübscher, U.; Spadari, S.; Maga, G. Drug resistance mutations in the nucleotide binding pocket of human immunodeficiency virus type 1 reverse transcriptase differentially affect the phosphorolysis-dependent primer unblocking activity in the presence of stavudine and zidovudine and its inhibition by efavirenz. Antimicrob. Agents Chem., 2005, 49(1), 342-349.
20. Doualla-Bell, F.; Avalos, A.; Brenner, B.; Gaolathe, T.; Mine, M.; Gaseitsiwe, S.; Oliveira, M.; Moisi, D.; Ndwapi, N.; Moffat, H. High prevalence of the K65R mutation in human immunodeficiency virus type 1 subtype C isolates from infected patients in Botswana treated with didanosine-based regimens. Antimicrob. Agents Chem., 2006, 50(12), 4182-4185.
21. Cong, M.E.; Mitchell, J.; Sweeney, E.; Bachman, S.; Hanson, D.L.; Heneine, W.; García-Lerma, J.G. Prophylactic efficacy of oral emtricitabine (ftc) and tenofovir disoproxil fumarate (tdf) combination against a tenofovir-resistant shiv containing the k65r mutation in macaques. J. Infect. Dis., 2013.
22. Sunpath, H.; Wu, B.; Gordon, M.; Hampton, J.; Johnson, B.; Moosa, M.-Y.S.; Ordonez, C.; Kuritzkes, D.R.; Marconi, V.C., High rate of K65R for antiretroviral therapy-naive patients with subtype C HIV infection failing a tenofovir-containing first-line regimen. AIDS (London, England) 2012, 26(13), 1679-1684.
23. Little, S. J.; Holte, S.; Routy, J.-P.; Daar, E.S.; Markowitz, M.; Collier, A.C.; Koup, R.A.; Mellors, J.W.; Connick, E.; Conway, B. Antiretroviral-drug resistance among patients recently infected with HIV. New Eng. J. Med., 2002, 347(6), 385-394.
24. Parikh, U.M.; Bacheler, L.; Koontz, D.; Mellors, J.W. The K65R mutation in human immunodeficiency virus type 1 reverse transcriptase exhibits bidirectional phenotypic antagonism with thymidine analog mutations. J. Virol., 2006, 80(10), 4971-4977.
25. Jlizi, A.; El Gaaied, A.B.A.; Slim, A.; Tebourski, F.; Mamou, M.B.; Chaabane, T.B.; Letaief-Omezzine, A.; Chakroun, M.; Garbouj, M.; Rejeb, S.B. Profile of drug resistance mutations among HIV-1-infected Tunisian subjects failing antiretroviral therapy. Arch. Virol., 2008, 153(6), 1103-1108.
26. Oliveira, M.; Moisi, D.; Spira, B.; Cox, S.; Brenner, B.G.; Wainberg, M.A. Apricitabine does not select additional drug resistance mutations in tissue culture in human immunodeficiency virus type 1 variants containing K65R, M184V, or M184V plus thymidine analogue mutations. Antimicrob. Agents Chem., 2009, 53(4), 1683-1685.
27. Barnas, D.; Koontz, D.; Bazmi, H.; Bixby, C.; Jemsek, J.; Mellors, J.W. Clonal resistance analyses of HIV-1 after failure of therapy with didanosine, lamivudine, and tenofovir. Antiviral Therap., 2010, 15(3), 437.
28. Bennett, D.E.; Camacho, R.J.; Otelea, D.; Kuritzkes, D.R.; Fleury, H.; Kiuchi, M.; Heneine, W.; Kantor, R.; Jordan, M.R.; Schapiro, J.M. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PloS One, 2009, 4(3), e4724.
29. R.W. Genotypic testing for human immunodeficiency virus type 1 drug resistance. Clinic. Microbiol. Rev., 2002, 15(2), 247-277.
30. Hughes, C.A.; Robinson, L.; Tseng, A.; MacArthur, R.D. New antiretroviral drugs: A review of the efficacy, safety, pharmacokinetics, and resistance profile of tipranavir, darunavir, etravirine, rilpivirine, maraviroc, and raltegravir. Exp. Opin Pharmacother., 2009, 10(15), 2445-2466.
31. Li, J.Z.; Paredes, R.; Ribaudo, H.J.; Kozal, M.J.; Svarovskaia, E.S.; Johnson, J.A.; Geretti, A.M.; Metzner, K.J.; Jakobsen, M.R.; Hullsiek, K.H.; Ostergaard, L.; Miller, M.D.; Kuritzkes, D.R. Impact of minority nonnucleoside reverse transcriptase inhibitor resistance mutations on resistance genotype after virologic failure. J. Infect. Dis., 2013, 207(6), 893-897.
32. Ren, J.; Stammers, D.K. Structural basis for drug resistance mechanisms for non-nucleoside inhibitors of HIV reverse transcriptase. Virus Res., 2008, 134(1-2), 157-170.
33. Di Vincenzo, P.; Rusconi, S.; Adorni, F.; Vitiello, P.; Maggiolo, F.; Francisci, D.; Di Biagio, A.; Monno, L.; Antinori, A.; Boeri, E.; Punzi, G.; Perno, C.F.; Callegaro, A.; Bruzzone, B.; Zazzi, M. Prevalence of mutations and determinants of genotypic resistance to etravirine (TMC125) in a large Italian resistance database (ARCA). HIV Med., 2010, 11(8), 530-534.
34. Xu, H.T.; Oliveira, M.; Quan, Y.; Bar-Magen, T.; Wainberg, M.A. Differential impact of the HIV-1 non-nucleoside reverse transcriptase inhibitor mutations K103N and M230L on viral replication and enzyme function. Antimicrob. Agents Chem., 2010, 65(11), 2291-2299.
35. Lazzarin, A.; Campbell, T.; Clotet, B.; Johnson, M.; Katlama, C.; Moll, A.; Towner, W.; Trottier, B.; Peeters, M.; Vingerhoets, J.; De Smedt, G.; Baeten, B.; Beets, G.; Sinha, R.; Woodfall, B. Efficacy and safety of TMC125 (etravirine) in treatment-experienced HIV-1-infected patients in DUET-2: 24-week results from a randomised, double-blind, placebo-controlled trial. Lancet., 2007, 370 (9581), 39-48.
36. Madruga, J.V.; Cahn, P.; Grinsztejn, B.; Haubrich, R.; Lalezari, J.; Mills, A.; Pialoux, G.; Wilkin, T.; Peeters, M.; Vingerhoets, J.; De Smedt, G.; Leopold, L.; Trefiglio, R.; Woodfall, B. Efficacy and safety of TMC125 (etravirine) in treatment-experienced HIV-1-infected patients in DUET-1: 24-week results from a randomised, double-blind, placebo-controlled trial. Lancet., 2007, 370(9581), 29-38.
37. Poveda, E.; Anta, L.; Blanco, J.L.; Perez-Elias, M. J.; Garcia, F.; Leal, M.; Ribera, E.; Gutierrez, F.; Soriano, V.; De Mendoza, C., Etravirine resistance associated mutations in HIV-infected patients failing efavirenz or nevirapine in the Spanish antiretroviral resistance database. AIDS (London, England)., 2010, 24 (3), 469-471.
38. Imaz, A.; Podzamczer, D., The role of rilpivirine in clinical practice: strengths and weaknesses of the new nonnucleoside reverse transcriptase inhibitor for HIV therapy. AIDS Rev., 2012, 14(4), 268-278.
39. Rimsky, L.; Vingerhoets, J.; Van Eygen, V.; Eron, J.; Clotet, B.; Hoogstoel, A.; Boven, K.; Picchio, G., Genotypic and phenotypic characterization of HIV-1 isolates obtained from patients on rilpivirine therapy experiencing virologic failure in the phase 3 ECHO and THRIVE studies: 48-week analysis. JAIDS-J. Acq. Immun. Def. Synd., 2012, 59(1), 39-46.
40. Wensing, A.M.; Van Maarseveen, N.M.; Nijhuis, M. Fifteen years of HIV Protease Inhibitors: raising the barrier to resistance. Antiv. Res., 2010, 85(1), 59-74.
41. Kirby, B.J.; Collier, A.C.; Kharasch, E.D.; Whittington, D.; Thummel, K.E.; Unadkat, J.D. Complex drug interactions of HIV protease inhibitors 1: Inactivation, induction, and inhibition of cytochrome P450 3A by ritonavir or nelfinavir. Drug Metab. Dispos., 2011, 39(6), 1070-1078.
42. Gantt, S.; Carlsson, J.; Ikoma, M.; Gachelet, E.; Gray, M.; Geballe, A. P.; Corey, L.; Casper, C.; Lagunoff, M.; Vieira, J., The HIV protease inhibitor nelfinavir inhibits Kaposi's sarcoma-associated herpesvirus replication in vitro. Antimicrob. Agents Chem., 2011, 55(6), 2696-2703.
43. See, A.P.; Zeng, J.; Tran, P.T.; Lim, M. Acute toxicity of second generation HIV protease-inhibitors in combination with radiotherapy: A retrospective case series. Radiat. Oncol., 2011, 6(25), 2-8.
44. Flint, O.P.; Noor, M.A.; Hruz, P.W.; Hylemon, P.B.; Yarasheski, K.; Kotler, D.P.; Parker, R.A.; Bellamine, A. The role of protease inhibitors in the pathogenesis of HIV-associated lipodystrophy: cellular mechanisms and clinical implications. Toxicol. Pathol., 2009, 37(1), 65-77.
45. Dam, E.; Quercia, R.; Glass, B.; Descamps, D.; Launay, O.; Duval, X.; Kräusslich, H.-G.; Hance, A.J.; Clavel, F. Gag mutations strongly contribute to HIV-1 resistance to protease inhibitors in highly drug-experienced patients besides compensating for fitness loss. PLoS Pathog., 2009, 5(3), e1000345.
46. Rhee, S.-Y.; Taylor, J.; Fessel, W.J.; Kaufman, D.; Towner, W.; Troia, P.; Ruane, P.; Hellinger, J.; Shirvani, V.; Zolopa, A. HIV-1 protease mutations and protease inhibitor cross-resistance. Antimicrob. Agents Chem., 2010, 54(10), 4253-4261.
47. Clavel, F.; Mammano, F. Role of gag in HIV resistance to protease inhibitors. Viruses., 2010, 2(7), 1411-1426.
48. Ali, A.; Bandaranayake, R.M.; Cai, Y.; King, N.M.; Kolli, M.; Mittal, S.; Murzycki, J.F.; Nalam, M.N.; Nalivaika, E.A.; Özen, A., Molecular basis for drug resistance in HIV-1 protease. Viruses., 2010, 2(11), 2509-2535.
49. Nalam, M.N.; Ali, A.; Altman, M.D.; Reddy, G.K.K.; Chellappan, S.; Kairys, V.; Özen, A.; Cao, H.; Gilson, M. K.; Tidor, B. Evaluating the substrate-envelope hypothesis: structural analysis of novel HIV-1 protease inhibitors designed to be robust against drug resistance. J. Virol., 2010, 84(10), 5368-5378.
50. Martinez-Cajas, J.L.; Wainberg, M.A.; Oliveira, M.; Asahchop, E.L.; Doualla-Bell, F.; Lisovsky, I.; Moisi, D.; Mendelson, E.; Grossman, Z.; Brenner, B.G. The role of polymorphisms at position 89 in the HIV-1 protease gene in the development of drug resistance to HIV-1 protease inhibitors. J. Antimicrob. Chem., 2012, 67(4), 988-994.
51. Soares, R.O.; Batista, P.R.; Costa, M.G.; Dardenne, L.E.; Pascutti, P.G.; Soares, M.A. Understanding the HIV-1 protease nelfinavir resistance mutation D30N in subtypes B and C through molecular dynamics simulations. J. Mol. Grap. Model., 2010, 29(2), 137-147.
52. Baxter, J.D.; Schapiro, J.M.; Boucher, C.A.; Kohlbrenner, V.M.; Hall, D.B.; Scherer, J.R.; Mayers, D.L. Genotypic changes in human immunodeficiency virus type 1 protease associated with reduced susceptibility and virologic response to the protease inhibitor tipranavir. J. Virol., 2006, 80(21), 10794-10801.
53. De Meyer, S.; Vangeneugden, T.; Van Baelen, B.; De Paepe, E.; Van Marck, H.; Picchio, G.; Lefebvre, E.; De Bethune, M. P. Resistance profile of darunavir: Combined 24-week results from the POWER trials. AIDS Res. Hum. Retrov., 2008, 24(3), 379-388.
54. Lobritz, M. A.; Ratcliff, A. N.; Arts, E. J., HIV-1 entry, inhibitors, and resistance. Viruses., 2010, 2(5), 1069-1105.
55. De Feo, C.J.; Weiss, C.D. Escape from human immunodeficiency virus type 1 (HIV-1) entry inhibitors. Viruses., 2012, 4(12), 3859-3911.
56. Tilton, J.C.; Doms, R.W. Entry inhibitors in the treatment of HIV-1 infection. Antiviral Res., 2010, 85 (1), 91-100.
57. Eggink, D.; Berkhout, B.; Sanders, W.R. Inhibition of HIV-1 by fusion inhibitors. Cur. Pharmaceut. Des., 2010, 16(33), 3716-3728.
58. Kuritzkes, D.R. HIV-1 entry inhbitors: An overview. Cur. Opin. HIV AIDS, 2009, 4(2), 82.
59. Melikyan, G.B., Membrane fusion mediated by human immunodeficiency virus envelope glycoprotein. Curr. Top Membr., 2011, 68, 81-106.
60. Eckert, D.M.; Kim, P.S., Mechanisms of viral membrane fusion and its inhibition. Ann. Rev. Biochem., 2001, 70(1), 777-810.
61. Yoshimura, K.; Harada, S.; Shibata, J.; Hatada, M.; Yamada, Y.; Ochiai, C.; Tamamura, H.; Matsushita, S. Enhanced exposure of human immunodeficiency virus type 1 primary isolate neutralization epitopes through binding of CD4 mimetic compounds. J. Virol., 2010, 84(15), 7558-7568.
62. Singh, I.P.; Chauthe, S.K. Small molecule HIV entry inhibitors: Part II. Attachment and fusion inhibitors: 2004-2010. Exp. Opin. Therapeut. Pat., 2011, 21(3), 399-416.
63. Zhou, N.; Nowicka-Sans, B.; Zhang, S.; Fan, L.; Fang, J.; Fang, H.; Gong, Y.-F.; Eggers, B.; Langley, D.R.; Wang, T. In vivo patterns of resistance to the HIV attachment inhibitor BMS-488043. Antimicrob. Agents Chem., 2011, 55(2), 729-737.
64. Anastassopoulou, C.G.; Ketas, T.J.; Klasse, P.J.; Moore, J.P. Resistance to CCR5 inhibitors caused by sequence changes in the fusion peptide of HIV-1 gp41. Proceed. Nat. Acad. Sci., 2009, 106(13), 5318-5323.
65. Charpentier, C.; Larrouy, L.; Visseaux, B.; Landman, R.; Levittas, M.; Storto, A.; Damond, F.; Yazdanpanah, Y.; Yeni, P.; Brun-Vézinet, F. Prevalence of subtype-related polymorphisms associated with in vitro resistance to attachment inhibitor BMS-626529 in HIV-1 'non-B'-infected patients. Antimicrob. Agents Chem., 2012, 67(6), 1459-1461.
66. Pace, C.S.; Fordyce, M.W.; Franco, D.; Kao, C.-Y.; Seaman, M.S.; Ho, D.D. Anti-CD4 monoclonal antibody ibalizumab exhibits breadth and potency against HIV-1, with natural resistance mediated by the loss of a V5 glycan in envelope. JAIDS- J. Acq. Imm. Def., 2013, 62(1), 1-9.
67. Cai, L.; Jiang, S. Development of peptide and small molecule HIV 1 fusion inhibitors that target gp41. Chem. Med. Chem., 2010, 5(11), 1813-1824.
68. Hanna, S.L.; Yang, C.; Owen, S.M.; Lal, R.B. Resistance mutation in HIV entry inhibitors. AIDS (London, England), 2002, 16(12), 1603-1608.
69. Coetzer, M.; Cilliers, T.; Ping, L.-H.; Swanstrom, R.; Morris, L. Genetic characteristics of the V3 region associated with CXCR4 usage in HIV-1 subtype C isolates. Virology., 2006, 356 (1), 95-105.
70. Sterjovski, J.; Churchill, M.J.; Wesselingh, S.L.; Gorry, P.R. HIV-1 entry inhibitors: Classes, applications and factors affecting potency. Curr. HIV Res., 2006, 4(4), 387-400.
71. Berro, R.; Klasse, P.J.; Moore, J.P.; Sanders, R.W. V3 determinants of HIV-1 escape from the CCR5 inhibitors Maraviroc and Vicriviroc. Virology., 2012, 427(2), 158-165.
72. Ratcliff, A.N.; Shi, W.; Arts, E.J., HIV-1 resistance to maraviroc conferred by a Cd4 binding site mutation in the envelope glycoprotein Gp120. J. Virol., 2013, 87(2), 923-934.
73. Lobritz, M.A.; Ratcliff, A.N.; Marozsan, A.J.; Dudley, D.M.; Tilton, J.C.; Arts, E.J. Multifaceted mechanisms of HIV inhibition and resistance to CCR5 inhibitors PSC-RANTES and Maraviroc. Antimicrob. Agent. Chemotherap., 2013, 57(6), 2640-2650.
74. Menéndez-Arias, L. HIV reverse transcriptase fidelity, clade diversity, and acquisition of drug resistance. Hum. Immunodef. Virus Rev. Trans., 2013, 225-252.
75. Herschhorn, A.; Hizi, A. Retroviral reverse transcriptases. Cell. Mol. Life Sci., 2010, 67(16), 2717-2747.
76. Emamzadeh-Fard, S.; Efard, S.; SeyedAlinaghi, S.; Paydary, K. Adherence to anti-retroviral therapy and its determinants in HIV/AIDS patients: A review. Infect. Disord. Drug Targets Disord., 2012, 12(5), 346-356.