Diminished efficiency of HIV-1 reverse transcriptase containing the K65R and M184V drug resistance mutations

AIDS

Volumn 21, Issue 6, 2007, Pages 665-675

  Frankel, Fernando A ^a,b   Invernizzi, Cédric F ^a   Oliveira, Maureen ^a   Wainberg, Mark A ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

( )ssDNA; Drug resistance; K65R; M184V; Replication capacity

Indexed keywords

RNA DIRECTED DNA POLYMERASE; TENOFOVIR; ZIDOVUDINE;

ARTICLE; CELL CULTURE; DATA ANALYSIS; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; UMBILICAL CORD BLOOD; VIRUS MUTATION; VIRUS REPLICATION;

CELL LINE; DNA PRIMERS; DNA, SINGLE-STRANDED; DNA, VIRAL; DRUG RESISTANCE, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; MUTATION; PHOSPHORYLATION; REVERSE TRANSCRIPTASE INHIBITORS; RNA, VIRAL; VIRUS REPLICATION; ZIDOVUDINE;

EID: 34147132711     PISSN: 02699370     EISSN: None     Source Type: Journal    
DOI: 10.1097/QAD.0b013e3280187505     Document Type: Article

References (60)

1. Morens DM, Folkers GK, Fauci AS. The challenge of emerging and re-emerging infectious diseases. Nature 2004; 430:242-249.
2. Hubner A, Kruhoffer M, Grosse F, Krauss G. Fidelity of human immunodeficiency virus type I reverse transcriptase in copying natural RNA. J Mol Biol 1992; 223:595-600.
3. Preston BD, Poiesz BJ, Loeb LA. Fidelity of HIV-1 reverse transcriptase. Science 1988; 242:1168-1171.
4. Saksena NK, Potter SJ. Reservoirs of HIV-1 in vivo: implications for antiretroviral therapy. AIDS Rev 2003; 5:3-18.
5. Siliciano JD, Siliciano RF. A long-term latent reservoir for HIV-1: discovery and clinical implications. J Antimicrob Chemother 2004; 54:6-9.
6. Cheung PK, Wynhoven B, Harrigan PR. 2004: which HIV-1 drug resistance mutations are common in clinical practice? AIDS Rev 2004; 6:107-116.
7. Locatelli GA, Cancio R, Spadari S, Maga G. HIV-1 reverse transcriptase inhibitors: current issues and future perspectives. Curr Drug Metab 2004; 5:283-290.
8. Johnson VA, Brun-Vezinet F, Clotet B, Conway B, D'Aquila RT, Demeter LM, et al. Update of the drug resistance mutations in HIV-1: 2004. Top HIV Med 2004; 12:119-124.
9. Krebs R, Immendorfer U, Thrall SH, Wohrl BM, Goody RS. Single-step kinetics of HIV-1 reverse transcriptase mutants responsible for virus resistance to nucleoside inhibitors zidovudine and 3-TC. Biochemistry 1997; 36:10292-10300.
10. Arion D, Parniak MA. HIV resistance to zidovudine: the role of pyrophosphorolysis. Drug Resist Updat 1999; 2:91-95.
11. Meyer PR, Matsuura SE, Mian AM, So AG, Scott WA. A mechanism of AZT resistance: an increase in nucleotide-dependent primer unblocking by mutant HIV-1 reverse transcriptase. Mol Cell 1999; 4:35-43.
12. Wainberg MA, Miller MD, Quan Y, Salomon H, Mulato AS, Lamy PD, et al. In vitro selection and characterization of HIV-1 with reduced susceptibility to PMPA. Antivir Ther 1999; 4:87-94.
13. Miller MD, Margot NA, Hertogs K, Larder B, Miller V. Antiviral activity of tenofovir (PMPA) against nucleoside-resistant clinical HIV samples. Nucleosides Nucleotides Nucl Acids 2001; 20:1025-1028.
14. Gu Z, Gao Q, Fang H, Salomon H, Parniak MA, Goldberg E, et al. Identification of a mutation at codon 65 in the IKKK motif of reverse transcriptase that encodes human immunodeficiency virus resistance to 2′,3′-dideoxycytidine and 2′,3′-dideoxy-3′- thiacytidine. Antimicrob Agents Chemother 1994; 38:275-281.
15. Zhang D, Caliendo AM, Eron JJ, DeVore KM, Kaplan JC, Hirsch MS, D'Aquila RT. Resistance to 2′,3′-dideoxycytidine conferred by a mutation in codon 65 of the human immunodeficiency virus type 1 reverse transcriptase. Antimicrob Agents Chemother 1994; 38:282-287.
16. Harrigan PR, Stone C, Griffin P, Najera I, Bloor S, Kemp S, et al. Resistance profile of the human immunodeficiency virus type 1 reverse transcriptase inhibitor abacavir (1592U89) after monotherapy and combination therapy. CNA2001 Investigative Group. J Infect Dis 2000; 181:912-920.
17. Martin JL, Wilson JE, Haynes RL, Furman PA. Mechanism of resistance of human immunodeficiency virus type 1 to 2′,3′-dideoxyinosine. Proc Natl Acad Sci U S A 1993; 90:6135-6139.
18. Miller V, Ait-Khaled M, Stone C, Griffin P, Mesogiti D, Cutrell A, et al. HIV-1 reverse transcriptase (RT) genotype and susceptibility to RT inhibitors during abacavir monotherapy and combination therapy. AIDS 2000; 14:163-171.
19. Goldschmidt V, Marquet R. Primer unblocking by HIV-1 reverse transcriptase and resistance to nucleoside RT inhibitors (NRTIs). Int J Biochem Cell Biol 2004; 36:1687-1705.
20. Sharma PL, Crumpacker CS. Attenuated replication of human immunodeficiency virus type 1 with a didanosine-selected reverse transcriptase mutation. J Virol 1997; 71:8846-8851.
21. Weber J, Chakraborty B, Weberova J, Miller MD, Quinones-Mateu ME. Diminished replicative fitness of primary human immunodeficiency virus type 1 isolates harboring the K65R mutation. J Clin Microbiol 2005; 43:1395-1400.
22. White KL, Margot NA, Wrin T, Petropoulos CJ, Miller MD, Naeger LK. Molecular mechanisms of resistance to human immunodeficiency virus type 1 with reverse transcriptase mutations K65R and K65RRM184V and their effects on enzyme function and viral replication capacity. Antimicrob Agents Chemother 2002; 46:3437-3446.
23. St Clair MH, Martin JL, Tudor-Williams G, Bach MC, Vavro CL, King DM, et al. Resistance to ddI and sensitivity to AZT induced by a mutation in HIV-1 reverse transcriptase. Science 1991; 253:1557-1559.
24. Winters MA, Shafer RW, Jellinger RA, Mamtora G, Gingeras T, Merigan TC. Human immunodeficiency virus type 1 reverse transcriptase genotype and drug susceptibility changes in infected individuals receiving dideoxyinosine monotherapy for 1 to 2 years. Antimicrob Agents Chemother 1997; 41:757-762.
25. Deval J, White KL, Miller MD, Parkin NT, Courcambeck J, Halfon P, et al. Mechanistic basis for reduced viral and enzymatic fitness of HIV-1 reverse transcriptase containing both K65R and M184V mutations. J Biol Chem 2004; 279:509-516.
26. Le Grice SF, Gruninger-Leitch F. Rapid purification of homodimer and heterodimer HIV-1 reverse transcriptase by metal chelate affinity chromatography. Eur J Biochem 1990; 187:307-314.
27. Roldan A, Russell RS, Marchand B, Gotte M, Liang C, Wainberg MA. In vitro identification and characterization of an early complex linking HIV-1 genomic RNA recognition and Pr55Gag multimerization. J Biol Chem 2004; 279:39886-39894.
28. Gotte M, Kameoka M, McLellan N, Cellai L, Wainberg MA. Analysis of efficiency and fidelity of HIV-1 (+)-strand DNA synthesis reveals a novel rate-limiting step during retroviral reverse transcription. J Biol Chem 2001; 276:6711-6719.
29. Liang C, Rong L, Gotte M, Li X, Quan Y, Kleiman L, Wainberg MA. Mechanistic studies of early pausing events during initiation of HIV-1 reverse transcription. J Biol Chem 1998; 273:21309-21315.
30. Quan Y, Brenner BG, Marlink RG, Essex M, Kurimura T, Wainberg MA. Drug resistance profiles of recombinant reverse transcriptases from human immunodeficiency virus type 1 subtypes A/E, B, and C. AIDS Res Hum Retroviruses 2003; 19:743-753.
31. Frankel FA, Marchand B, Turner D, Gotte M, Wainberg MA. Impaired rescue of chain-terminated DNA synthesis associated with the L74V mutation in human immunodeficiency virus type 1 reverse transcriptase. Antimicrob Agents Chemother 2005; 49:2657-2664.
32. Wei X, Liang C, Gotte M, Wainberg MA. Negative effect of the M184V mutation in HIV-1 reverse transcriptase on initiation of viral DNA synthesis. Virology 2003; 311:202-212.
33. Gao Q, Parniak MA, Gu Z, Wainberg MA. Generation of nucleoside-resistant variants of HIV-1 by in vitro selection in the presence of AZT or DDI but no by combinations. Leukemia 1992; 6 (suppl 3):192S-195S.
34. Salomon H, Belmonte A, Nguyen K, Gu Z, Gelfand M, Wainberg MA. Comparison of cord blood and peripheral blood mononuclear cells as targets for viral isolation and drug sensitivity studies involving human immunodeficiency virus type 1. J Clin Microbiol 1994; 32:2000-2002.
35. Diallo K, Marchand B, Wei X, Cellai L, Gotte M, Wainberg MA. Diminished RNA primer usage associated with the L74V and M184V mutations in the reverse transcriptase of human immunodeficiency virus type 1 provides a possible mechanism for diminished viral replication capacity. J Virol 2003; 77:8621-8632.
36. Gao Q, Gu Z, Parniak MA, Cameron J, Cammack N, Boucher C, Wainberg MA. The same mutation that encodes low-level human immunodeficiency virus type 1 resistance to 2′,3′-dideoxyinosine and 2′,3′- dideoxycytidine confers high-level resistance to the (-) enantiomer of 2′,3′-dideoxy-3′-thiacytidine. Antimicrob Agents Chemother 1993; 37:1390-1392.
37. Victoria JG, Lee DJ, McDougall BR, Robinson WE Jr. Replication kinetics for divergent type 1 human immunodeficiency viruses using quantitative SYBR green I real-time polymerase chain reaction. AIDS Res Hum Retroviruses 2003; 19:865-874.
38. Gu Z, Salomon H, Cherrington JM, Mulato AS, Chen MS, Yarchoan R, et al. K65R mutation of human immunodeficiency virus type 1 reverse transcriptase encodes cross-resistance to 9-(2-phosphonylmethoxyethyl)adenine. Antimicrob Agents Chemother 1995; 39:1888-1891.
39. Quan Y, Gu Z, Li X, Li Z, Morrow CD, Wainberg MA. Endogenous reverse transcription assays reveal high-level resistance to the triphosphate of (-)2′-dideoxy-3′-thiacytidine by mutated M184V human immunodeficiency virus type 1. J Virol 1996; 70:5642-5645.
40. Gu Z, Arts EJ, Parniak MA, Wainberg MA. Mutated K65R recombinant reverse transcriptase of human immunodeficiency virus type 1 shows diminished chain termination in the presence of 2′,3′-dideoxycytidine 5′-triphosphate and other drugs. Proc Natl Acad Sci U S A 1995; 92:2760-2764.
41. Boyer PL, Sarafianos SG, Arnold E, Hughes SH. Selective excision of AZTMP by drug-resistant human immunodeficiency virus reverse transcriptase. J Virol 2001; 75:4832-4842.
42. Miranda LR, Gotte M, Kuritzkes DR. The L74V mutation in human immunodeficiency virus type 1 reverse transcriptase counteracts enhanced excision of zidovudine monophosphate associated with thymidine analog resistance mutations. Antimicrob Agents Chemother 2005; 49:2648-2656.
43. Miller MD. K65R, TAMs and tenofovir. AIDS Rev 2004; 6:22-33.
44. Wei X, Liang C, Gotte M, Wainberg MA. The M184V mutation in HIV-1 reverse transcriptase reduces the restoration of wild-type replication by attenuated viruses. AIDS 2002; 16:2391-2398.
45. Feng YX, Campbell S, Harvin D, Ehresmann B, Ehresmann C, Rein A. The human immunodeficiency virus type 1 Gag polyprotein has nucleic acid chaperone activity: possible role in dimerization of genomic RNA and placement of tRNA on the primer binding site. J Virol 1999; 73:4251-4256.
46. Darlix JL, Cristofari G, Rau M, Pechoux C, Berthoux L, Roques B. Nucleocapsid protein of human immunodeficiency virus as a model protein with chaperoning functions and as a target for antiviral drugs. Adv Pharmacol 2000; 48:345-372.
47. Rong L, Liang C, Hsu M, Guo X, Roques BP, Wainberg MA. HIV-1 nucleocapsid protein and the secondary structure of the binary complex formed between tRNA(Lys.3) and viral RNA template play different roles during initiation of (-) strand DNA reverse transcription. J Biol Chem 2001; 276:47725-47732.
48. Bampi C, Jacquenet S, Lener D, Decimo D, Darlix JL. The chaperoning and assistance roles of the HIV-1 nucleocapsid protein in proviral DNA synthesis and maintenance. Curr HIV Res 2004; 2:79-92.
49. Levin JG, Guo J, Rouzina I, Musier-Forsyth K. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog Nucleic Acid Res Mol Biol 2005; 80:217-286.
50. Deval J, Navarro JM, Selmi B, Courcambeck J, Boretto J, Halfon P, et al. A loss of viral replicative capacity correlates with altered DNA polymerization kinetics by the human immunodeficiency virus reverse transcriptase bearing the K65R and L74V dideoxynucleoside resistance substitutions. J Biol Chem 2004; 279:25489-25496.
51. Kim SY, Byrn R, Groopman J, Baltimore D. Temporal aspects of DNA and RNA synthesis during human immunodeficiency virus infection: evidence for differential gene expression. J Virol 1989; 63:3708-3713.
52. Terai C, Carson DA. Pyrimidine nucleotide and nucleic acid synthesis in human monocytes and macrophages. Exp Cell Res 1991; 193:375-381.
53. Gotte M, Arion D, Parniak MA, Wainberg MA. The M184V mutation in the reverse transcriptase of human immunodeficiency virus type 1 impairs rescue of chain-terminated DNA synthesis. J Virol 2000; 74:3579-3585.
54. White KL, Margot NA, Ly JK, Chen JM, Ray AS, Pavelko M, et al. A combination of decreased NRTI incorporation and decreased excision determines the resistance profile of HIV-1 K65R RT. AIDS 2005; 19:1751-1760.
55. Boucher S, Recordon-Pinson P, Ragnaud JM, Dupon M, Fleury H, Masquelier B. HIV-1 reverse transcriptase (RT) genotypic patterns and treatment characteristics associated with the K65R RT mutation. HIV Med 2006; 7:294-298.
56. Parikh UM, Bacheler L, Koontz D, Mellors JW. The K65R mutation in human immunodeficiency virus type 1 reverse transcriptase exhibits bidirectional phenotypic antagonism with thymidine analog mutations. J Virol 2006; 80:4971-4977.
57. Parikh UM, Barnas DC, Faruki H, Mellors JW. Antagonism between the HIV-1 reverse-transcriptase mutation K65R and thymidine-analogue mutations at the genomic level. J Infect Dis 2006; 194:651-660.
58. Nikolenko GN, Svarovskaia ES, Delviks KA, Pathak VK. Antiretroviral drug resistance mutations in human immunodeficiency virus type 1 reverse transcriptase increase templateswitching frequency. J Virol 2004; 78:8761-8770.
59. Delaunay C, Brun-Vezinet F, Landman R, Collin G, Peytavin G, Trylesinski A, et al. Comparative selection of the K65R and M184V/I mutations in human immunodeficiency virus type 1-infected patients enrolled in a trial of first-line triple-nucleoside analog therapy (Tonus IMEA 021). J Virol 2005; 79:9572-9578.
60. Margot NA, Lu B, Cheng A, Miller MD. Resistance development over 144 weeks in treatment-naive patients receiving tenofovir disoproxil fumarate or stavudine with lamivudine and efavirenz in Study 903. HIV Med 2006; 7:442-450.