Genome-wide association study of virologic response with efavirenz-containing or abacavir-containing regimens in AIDS clinical trials group protocols

Pharmacogenetics and Genomics

Volumn 25, Issue 2, 2015, Pages 51-59

  Lehmann, David S ^a   Ribaudo, Heather J ^b   Daar, Eric S ^d   Gulick, Roy M ^f   Haubrich, Richard H ^e   Robbins, Gregory K ^c   De Bakker, Paul I W ^h   Haas, David W ^g   McLaren, Paul J ^i,j  

^a BRANDEIS UNIVERSITY   (United States)

^b CENTER FOR BIOSTATISTICS IN AIDS RESEARCH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARBOR UCLA MEDICAL CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

^g VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

ⁱ SWISS FEDERAL INSTITUTE OF TECHNOLOGY   (Switzerland)

^j LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

more..

Author keywords

abacaviR; efavirenz; HIV 1; pharmacogenomics; virologic failure

Indexed keywords

ABACAVIR; ABACAVIR PLUS LAMIVUDINE; ABACAVIR PLUS LAMIVUDINE PLUS ZIDOVUDINE; ATAZANAVIR PLUS RITONAVIR; CYTOCHROME P450 2B; EFAVIRENZ; EMTRICITABINE PLUS TENOFOVIR DISOPROXIL; LAMIVUDINE; LAMIVUDINE PLUS STAVUDINE; LAMIVUDINE PLUS TENOFOVIR DISOPROXIL; LAMIVUDINE PLUS ZIDOVUDINE; LOPINAVIR PLUS RITONAVIR; VIRUS RNA; 2',3' DIDEOXYNUCLEOSIDE DERIVATIVE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; BENZOXAZINE DERIVATIVE;

ANTIVIRAL THERAPY; ARTICLE; CLINICAL TRIAL (TOPIC); GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; RACE; RANDOMIZED CONTROLLED TRIAL (TOPIC); ACQUIRED IMMUNODEFICIENCY SYNDROME; DRUG COMBINATION; DRUG EFFECTS; GENETICS; HIV INFECTIONS; META ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICS AND NUMERICAL DATA; TREATMENT OUTCOME;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANTI-HIV AGENTS; BENZOXAZINES; DIDEOXYNUCLEOSIDES; DRUG THERAPY, COMBINATION; GENOME-WIDE ASSOCIATION STUDY; HIV INFECTIONS; HIV-1; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TREATMENT OUTCOME;

EID: 84920870870     PISSN: 17446872     EISSN: 17446880     Source Type: Journal    
DOI: 10.1097/FPC.0000000000000106     Document Type: Article

References (50)

1. The Panel on Clinical Practices for Treatment of HIV Infection. Guidelines for the use of antiretroviral agents in HIV-1-infected adults and adolescents. National Institute of Health: Rockville, MD. Available at: http://www.aidsinfo. nih.gov/contentfiles/lvguidelines/adultandadolescentgl.pdf. [Accessed 8 October 2014].
2. Gulick RM, Ribaudo HJ, Shikuma CM, Lalama C, Schackman BR, Meyer WA 3rd, et al. AIDS Clinical Trials Group (ACTG) A5095 Study Team. Three-vs four-drug antiretroviral regimens for the initial treatment of HIV-1 infection: a randomized controlled trial. JAMA 2006; 296:769-781.
3. Gallant JE, DeJesus E, Arribas JR, Pozniak AL, Gazzard B, Campo RE, et al. Study 934 Group. Tenofovir DF, emtricitabine, and efavirenz vs. zidovudine, lamivudine, and efavirenz for HIV. N Engl J Med 2006; 354:251-260.
4. Riddler SA, Haubrich R, DiRienzo AG, Peeples L, Powderly WG, Klingman KL, et al. AIDS Clinical Trials Group Study A5142 Team. Classsparing regimens for initial treatment of HIV-1 infection. N Engl J Med 2008; 358:2095-2106.
5. Lennox JL, DeJesus E, Lazzarin A, Pollard RB, Madruga JV, Berger DS, et al. STARTMRK investigators. Safety and efficacy of raltegravir-based versus efavirenz-based combination therapy in treatment-naive patients with HIV-1 infection: a multicentre, double-blind randomised controlled trial. Lancet 2009; 374:796-806.
6. Cooper DA, Heera J, Goodrich J, Tawadrous M, Saag M, Dejesus E, et al. Maraviroc versus efavirenz, both in combination with zidovudine-lamivudine, for the treatment of antiretroviral-naive subjects with CCR5-tropic HIV-1 infection. J Infect Dis 2010; 201:803-813.
7. Daar ES, Tierney C, Fischl MA, Sax PE, Mollan K, Budhathoki C, et al. AIDS Clinical Trials Group Study A5202 Team. Atazanavir plus ritonavir or efavirenz as part of a 3-drug regimen for initial treatment of HIV-1. Ann Intern Med 2011; 154:445-456.
8. Sax PE, DeJesus E, Mills A, Zolopa A, Cohen C, Wohl D, et al. GS-US-236-0102 study team. Co-formulated elvitegravir, cobicistat, emtricitabine, and tenofovir versus co-formulated efavirenz, emtricitabine, and tenofovir for initial treatment of HIV-1 infection: a randomised, double-blind, phase 3 trial, analysis of results after 48 weeks. Lancet 2012; 379:2439-2448.
9. Cohen CJ, Molina JM, Cahn P, Clotet B, Fourie J, Grinsztejn B, et al. ECHO Study Group; THRIVE Study Group. Efficacy and safety of rilpivirine (TMC278) versus efavirenz at 48 weeks in treatment-naive HIV-1-infected patients: pooled results from the phase 3 double-blind randomized ECHO and THRIVE Trials. J Acquir Immune Defic Syndr 2012; 60:33-42.
10. Fellay J, Marzolini C, Meaden ER, Back DJ, Buclin T, Chave JP, et al. Swiss HIV Cohort Study. Response to antiretroviral treatment in HIV-1-infected individuals with allelic variants of the multidrug resistance transporter 1: a pharmacogenetics study. Lancet 2002; 359:30-36.
11. Ribaudo HJ, Liu H, Schwab M, Schaeffeler E, Eichelbaum M, Motsinger-Reif AA, et al. Effect of CYP2B6, ABCB1, and CYP3A5 polymorphisms on efavirenz pharmacokinetics and treatment response: an AIDS Clinical Trials Group study. J Infect Dis 2010; 202:717-722.
12. Ward BA, Gorski JC, Jones DR, Hall SD, Flockhart DA, Desta Z. The cytochrome P450 2B6 (CYP2B6) is the main catalyst of efavirenz primary and secondary metabolism: implication for HIV/AIDS therapy and utility of efavirenz as a substrate marker of CYP2B6 catalytic activity. J Pharmacol Exp Ther 2003; 306:287-300.
13. Haas DW, Severe P, Jean Juste MA, Pape JW, Fitzgerald DW. Functional CYP2B6 variants and virologic response to an efavirenz-containing regimen in Port-Au-Prince, Haiti. J Antimicrob Chemother 2014; 69:2187-2190.
14. Haas DW, Ribaudo HJ, Kim RB, Tierney C, Wilkinson GR, Gulick RM, et al. Pharmacogenetics of efavirenz and central nervous system side effects: an Adult AIDS Clinical Trials Group study. AIDS 2004; 18:2391-2400.
15. Tsuchiya K, Gatanaga H, Tachikawa N, Teruya K, Kikuchi Y, Yoshino M, et al. Homozygous CYP2B6 6 (Q172H and K262R) correlates with high plasma efavirenz concentrations in HIV-1 patients treated with standard efavirenzcontaining regimens. Biochem Biophys Res Commun 2004; 319:1322-1326.
16. Rotger M, Colombo S, Furrer H, Bleiber G, Buclin T, Lee BL, et al. Swiss HIV Cohort Study. Influence of CYP2B6 polymorphism on plasma and intracellular concentrations and toxicity of efavirenz and nevirapine in HIVinfected patients. Pharmacogenet Genomics 2005; 15:1-5.
17. Haas DW, Smeaton LM, Shafer RW, Robbins GK, Morse GD, Labbe L, et al. Pharmacogenetics of long-term responses to antiretroviral regimens containing Efavirenz and/or Nelfinavir: an Adult Aids Clinical Trials Group Study. J Infect Dis 2005; 192:1931-1942.
18. Rodriguez-Novoa S, Barreiro P, Rendón A, Jiménez-Nacher I, González-Lahoz J, Soriano V. Influence of 516Ggt;T polymorphisms at the gene encoding the CYP450-2B6 isoenzyme on efavirenz plasma concentrations in HIV-infected subjects. Clin Infect Dis 2005; 40:1358-1361.
19. Holzinger ER, Grady B, Ritchie MD, Ribaudo HJ, Acosta EP, Morse GD, et al. Genome-wide association study of plasma efavirenz pharmacokinetics in AIDS Clinical Trials Group protocols implicates several CYP2B6 variants. Pharmacogenet Genomics 2012; 22:858-867.
20. Wyen C, Hendra H, Vogel M, Hoffmann C, Knechten H, Brockmeyer NH, et al. German Competence Network for HIV/AIDS. Impact of CYP2B6 983Tgt;C polymorphism on non-nucleoside reverse transcriptase inhibitor plasma concentrations in HIV-infected patients. J Antimicrob Chemother 2008; 61:914-918.
21. Wang J, Sönnerborg A, Rane A, Josephson F, Lundgren S, Stahle L, Ingelman-Sundberg M. Identification of a novel specific CYP2B6 allele in Africans causing impaired metabolism of the HIV drug efavirenz. Pharmacogenet Genomics 2006; 16:191-198.
22. National Center for Biotechnology Information, dbSNP-Short genetic variations. Available at: http://www.ncbi.nlm.nih.gov/projects/SNP/. [Accessed 9 December 2011].
23. Barrett JS, Joshi AS, Chai M, Ludden TM, Fiske WD, Pieniaszek HJ Jr. Population pharmacokinetic meta-Analysis with efavirenz. Int J Clin Pharmacol Ther 2002; 40:507-519.
24. Pfister M, Labbé L, Hammer SM, Mellors J, Bennett KK, Rosenkranz S, Sheiner LB. Adult AIDS Clinical Trial Group Study 398. Population pharmacokinetics and pharmacodynamics of efavirenz, nelfinavir, and indinavir: adult AIDS Clinical Trial Group Study 398. Antimicrob Agents Chemother 2003; 47:130-137.
25. Ziagen (abacavir sulfate) full prescribing information. Available at: http://www.viivhealthcare.com/gskprm/htdocs/documents/ZIAGEN-PI-MG.PDF. [Accessed 9 May] 2012.
26. Mallal S, Nolan D, Witt C, Masel G, Martin AM, Moore C, et al. Association between presence of HLA-B5701, HLA-DR7, and HLA-DQ3 and hypersensitivity to HIV-1 reverse-transcriptase inhibitor abacavir. Lancet 2002; 359:727-732.
27. Hetherington S, Hughes AR, Mosteller M, Shortino D, Baker KL, Spreen W, et al. Genetic variations in HLA-B region and hypersensitivity reactions to abacavir. Lancet 2002; 359:1121-1122.
28. Mallal S, Phillips E, Carosi G, Molina JM, Workman C, Tomazic J, et al. PREDICT-1 Study Team. HLA-B5701 screening for hypersensitivity to abacavir. N Engl J Med 2008; 358:568-579.
29. Sax PE, Tierney C, Collier AC, Fischl MA, Mollan K, Peeples L, et al. AIDS Clinical Trials Group Study A5202 Team. Abacavir-lamivudine versus tenofovir-emtricitabine for initial HIV-1 therapy. N Engl J Med 2009; 361:2230-2240.
30. Smith KY, Patel P, Fine D, Bellos N, Sloan L, Lackey P, et al. HEAT Study Team. Randomized, double-blind, placebo-matched, multicenter trial of abacavir/lamivudine or tenofovir/emtricitabine with lopinavir/ritonavir for initial HIV treatment. AIDS 2009; 23:1547-1556.
31. Walmsley SL, Antela A, Clumeck N, Duiculescu D, Eberhard A, Gutiérrez F, et al. SINGLE Investigators. Dolutegravir plus abacavir-lamivudine for the treatment of HIV-1 infection. N Engl J Med 2013; 369:1807-1818.
32. Robbins GK, De GV, Shafer RW, Smeaton LM, Snyder SW, Pettinelli C, et al. Comparison of sequential three-drug regimens as initial therapy for HIV-1 infection. N Engl J Med 2003; 349:2293-2303.
33. Shafer RW, Smeaton LM, Robbins GK, De Gruttola V, Snyder SW, D'Aquila RT, et al. AIDS Clinical Trials Group 384 Team. Comparison of fourdrug regimens and pairs of sequential three-drug regimens as initial therapy for HIV-1 infection. N Engl J Med 2003; 349:2304-2315.
34. Haas DW, Wilkinson GR, Kuritzkes DR, Richman D, Nicotera J, Mahon LF, et al. A multi-investigator/institutional DNA bank for AIDS-related human genetic studies: AACTG Protocol A5128. HIV Clin Trials 2003; 4:287-300.
35. Pereyra F, Jia X, McLaren PJ, Telenti A, de Bakker PI, Walker BD, et al. International HIV Controllers Study. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 2010; 330:1551-1557.
36. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007; 81:559-575.
37. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 2006; 38:904-909.
38. Browning BL, Browning SR. A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Genet 2009; 84:210-223.
39. Purcell S, Sham PC. Available at: http://pngu.mgh.harvard.edu/~purcell/gpc/. [Accessed 10 May 2012].
40. Segré AV, Groop L, Mootha VK, Daly MJ, Altshuler D. DIAGRAM Consortium; MAGIC investigators. Common inherited variation in mitochondrial genes is not enriched for associations with type 2 diabetes or related glycemic traits. PLoS Genet 2010; 6:e1001058.
41. Squires K, Lazzarin A, Gatell JM, Powderly WG, Pokrovskiy V, Delfraissy JF, et al. Comparison of once-daily atazanavir with efavirenz, each in combination with fixed-dose zidovudine and lamivudine, as initial therapy for patients infected with HIV. J Acquir Immune Defic Syndr 2004; 36:1011-1019.
42. van Leth F, Phanuphak P, Ruxrungtham K, Baraldi E, Miller S, Gazzard B, et al. 2NN Study team. Comparison of first-line antiretroviral therapy with regimens including nevirapine, efavirenz, or both drugs, plus stavudine and lamivudine: a randomised open-label trial, the 2NN Study. Lancet 2004; 363:1253-1263.
43. Nelson MR, Bacanu SA, Mosteller M, Li L, Bowman CE, Roses AD, et al. Genome-wide approaches to identify pharmacogenetic contributions to adverse drug reactions. Pharmacogenomics J 2009; 9:23-33.
44. Tanaka Y, Kurosaki M, Nishida N, Sugiyama M, Matsuura K, Sakamoto N, et al. Genome-wide association study identified ITPA/DDRGK1 variants reflecting thrombocytopenia in pegylated interferon and ribavirin therapy for chronic hepatitis C. Hum Mol Genet 2011; 20:3507-3516.
45. Link E, Parish S, Armitage J, Bowman L, Heath S, Matsuda F, et al. SLCO1B1 variants and statin-induced myopathy-A genomewide study. N Engl J Med 2008; 359:789-799.
46. Chantarangsu S, Mushiroda T, Mahasirimongkol S, Kiertiburanakul S, Sungkanuparph S, Manosuthi W, et al. Genome-wide association study identifies variations in 6p21.3 associated with nevirapine-induced rash. Clin Infect Dis 2011; 53:341-348.
47. Kiyotani K, Mushiroda T, Kubo M, Zembutsu H, Sugiyama Y, Nakamura Y. Association of genetic polymorphisms in SLCO1B3 and ABCC2 with docetaxel-induced leukopenia. Cancer Sci 2008; 99:967-972.
48. Martin AM, Nolan D, James I, Cameron P, Keller J, Moore C, et al. Predisposition to nevirapine hypersensitivity associated with HLADRB1 0101 and abrogated by low CD4 T-cell counts. AIDS 2005; 19:97-99.
49. Kwara A, Lartey M, Sagoe KW, Court MH. Paradoxically elevated efavirenz concentrations in HIV/tuberculosis-coinfected patients with CYP2B6 516TT genotype on rifampin-containing antituberculous therapy. AIDS 2011; 25:388-390.
50. Johnson DH, Venuto C, Ritchie MD, Morse GD, Daar ES, McLaren PJ, Haas DW. Genomewide association study of atazanavir pharmacokinetics and hyperbilirubinemia in AIDS Clinical Trials Group protocol A5202. Pharmacogenet Genomics 2014; 24:195-203.