Polymorphism in gag gene cleavage sites of HIV-1 non-B subtype and virological outcome of a first-line lopinavir/ritonavir single drug regimen

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Ghosn, Jade ^a,b   Delaugerre, Constance ^a,c   Flandre, Philippe ^d   Galimand, Julie ^a   Cohen Codar, Isabelle ^e   Raffi, François ^f   Delfraissy, Jean François ^b   Rouzioux, Christine ^a,c   Chaix, Marie Laure ^a,c  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b BICÊTRE HOSPITAL   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d INSERM   (France)

^e Abbott   (France)

^f HÔTEL DIEU   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LAMIVUDINE PLUS ZIDOVUDINE; LOPINAVIR PLUS RITONAVIR; GAG PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; LOPINAVIR; RITONAVIR;

AMINO ACID SUBSTITUTION; ARTICLE; CLEAVAGE SITE; CONTROLLED STUDY; DRUG TREATMENT FAILURE; GENE MUTATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC POLYMORPHISM; GROUP SPECIFIC ANTIGEN GENE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MAJOR CLINICAL STUDY; MONOTHERAPY; NONHUMAN; RANDOMIZED CONTROLLED TRIAL; TREATMENT OUTCOME; VIRUS GENE; VIRUS STRAIN; DRUG EFFECT; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MUTATION; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV PROTEASE INHIBITORS; HIV-1; HUMANS; LOPINAVIR; MUTATION; POLYMORPHISM, GENETIC; RITONAVIR; TREATMENT OUTCOME;

EID: 80052959305     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024798     Document Type: Article

References (47)

1. Daar ES, Tierney C, Fischl MA, Sax PE, Mollan K, et al. (2011) Atazanavir plus ritonavir or efavirenz as part of a 3-drug regimen for initial treatment of HIV-1. Ann Intern Med 154 (7): 445-56.
2. Eron J Jr, Yeni P, Gathe J Jr, Estrada V, DeJesus E, et al. (2006) The KLEAN study of fosamprenavir-ritonavir versus lopinavir-ritonavir, each in combination with abacavir-lamivudine, for initial treatment of HIV infection over 48 weeks: a randomised non-inferiority trial. Lancet 368: 476-482.
3. Ortiz R, Dejesus E, Khanlou H, Voronin E, van Lunzen J, et al. (2008) Efficacy and safety of once-daily darunavir/ritonavir versus lopinavir/ritonavir in treatment-naive HIV-1-infected patients at week 48. AIDS 22: 1389-1397.
4. Riddler SA, Haubrich R, DiRienzo AG, Peeples L, Powderly WG, et al. (2008) Class-sparing regimens for initial treatment of HIV-1 infection. N Engl J Med 358: 2095-2106.
5. Soulie C, Assoumou L, Ghosn J, Duvivier C, Peytavin G, et al. (2009) Nucleoside reverse transcriptase inhibitor-sparing regimen (nonnucleoside reverse transcriptase inhibitor+protease inhibitor) was more likely associated with resistance comparing to nonnucleoside reverse transcriptase inhibitor or protease inhibitor+nucleoside reverse transcriptase inhibitor in the randomized ANRS 121 trial. AIDS 23: 1605-1608.
6. Condra JH, Schleif WA, Blahy OM, Gabryelski LJ, Graham DJ, et al. (1995) In vivo emergence of HIV-1 variants resistant to multiple protease inhibitors. Nature 374: 569-571.
7. Croteau G, Doyon L, Thibeault D, McKercher G, Pilote L, et al. (1997) Impaired fitness of human immunodeficiency virus type 1 variants with high-level resistance to protease inhibitors. J Virol 71: 1089-1096.
8. Molla A, Korneyeva M, Gao Q, Vasavanonda S, Schipper PJ, et al. (1996) Ordered accumulation of mutations in HIV protease confers resistance to ritonavir. Nat Med 2: 760-766.
9. Mammano F, Petit C, Clavel F, (1998) Resistance-associated loss of viral fitness in human immunodeficiency virus type 1: phenotypic analysis of protease and gag coevolution in protease inhibitor-treated patients. J Virol 72: 7632-7637.
10. Mammano F, Trouplin V, Zennou V, Clavel F, (2000) Retracing the evolutionary pathways of human immunodeficiency virus type 1 resistance to protease inhibitors: virus fitness in the absence and in the presence of drug. J Virol 74: 8524-8531.
11. Nijhuis M, Schuurman R, de Jong D, Erickson J, Gustchina E, et al. (1999) Increased fitness of drug resistant HIV-1 protease as a result of acquisition of compensatory mutations during suboptimal therapy. AIDS 13: 2349-2359.
12. Zhang YM, Imamichi H, Imamichi T, Lane HC, Falloon J, et al. (1997) Drug resistance during indinavir therapy is caused by mutations in the protease gene and in its Gag substrate cleavage sites. J Virol 71: 6662-6670.
13. Dinman JD, Richter S, Plant EP, Taylor RC, Hammell AB, et al. (2002) The frameshift signal of HIV-1 involves a potential intramolecular triplex RNA structure. Proc Natl Acad Sci U S A 99: 5331-5336.
14. Girnary R, King L, Robinson L, Elston R, Brierley I, (2007) Structure-function analysis of the ribosomal frameshifting signal of two human immunodeficiency virus type 1 isolates with increased resistance to viral protease inhibitors. J Gen Virol 88: 226-235.
15. Park J, Morrow CD, (1991) Overexpression of the gag-pol precursor from human immunodeficiency virus type 1 proviral genomes results in efficient proteolytic processing in the absence of virion production. J Virol 65: 5111-5117.
16. Parkin NT, Chamorro M, Varmus HE, (1992) Human immunodeficiency virus type 1 gag-pol frameshifting is dependent on downstream mRNA secondary structure: demonstration by expression in vivo. J Virol 66: 5147-5151.
17. Doyon L, Croteau G, Thibeault D, Poulin F, Pilote L, et al. (1996) Second locus involved in human immunodeficiency virus type 1 resistance to protease inhibitors. J Virol 70: 3763-3769.
18. Maguire MF, Guinea R, Griffin P, Macmanus S, Elston RC, et al. (2002) Changes in human immunodeficiency virus type 1 Gag at positions L449 and P453 are linked to I50V protease mutants in vivo and cause reduction of sensitivity to amprenavir and improved viral fitness in vitro. J Virol 76: 7398-7406.
19. Nijhuis M, van Maarseveen NM, Lastere S, Schipper P, Coakley E, et al. (2007) A novel substrate-based HIV-1 protease inhibitor drug resistance mechanism. PLoS Med 4: e36.
20. Dam E, Quercia R, Glass B, Descamps D, Launay O, et al. (2009) Gag mutations strongly contribute to HIV-1 resistance to protease inhibitors in highly drug-experienced patients besides compensating for fitness loss. PLoS Pathog 5: e1000345.
21. Parry CM, Kohli A, Boinett CJ, Towers GJ, McCormick AL, et al. (2009) Gag determinants of fitness and drug susceptibility in protease inhibitor-resistant human immunodeficiency virus type 1. J Virol 83: 9094-9101.
22. Malet I, Roquebert B, Dalban C, Wirden M, Amellal B, et al. (2007) Association of Gag cleavage sites to protease mutations and to virological response in HIV-1 treated patients. J Infect 54: 367-374.
23. Verheyen J, Litau E, Sing T, Daumer M, Balduin M, et al. (2006) Compensatory mutations at the HIV cleavage sites p7/p1 and p1/p6-gag in therapy-naive and therapy-experienced patients. Antivir Ther 11: 879-887.
24. Delfraissy JF, Flandre P, Delaugerre C, Ghosn J, Horban A, et al. (2008) Lopinavir/ritonavir monotherapy or plus zidovudine and lamivudine in antiretroviral-naive HIV-infected patients. AIDS 22: 385-393.
25. Ghosn J, Flandre P, Cohen-Codar I, Girard PM, Chaix ML, et al. (2010) Long-term (96-week) follow-up of antiretroviral-naive HIV-infected patients treated with first-line lopinavir/ritonavir monotherapy in the MONARK trial. HIV Med 11: 137-142.
26. Delaugerre C, Flandre P, Chaix ML, Ghosn J, Raffi F, et al. (2009) Protease inhibitor resistance analysis in the MONARK trial comparing first-line lopinavir-ritonavir monotherapy to lopinavir-ritonavir plus zidovudine and lamivudine triple therapy. Antimicrob Agents Chemother 53: 2934-2939.
27. Flandre P, Delaugerre C, Ghosn J, Chaix ML, Horban A, et al. (2009) Prognostic factors for virological response in antiretroviral therapy-naive patients in the MONARK Trial randomized to ritonavir-boosted lopinavir alone. Antivir Ther 14: 93-97.
28. Cote HC, Brumme ZL, Harrigan PR, (2001) Human immunodeficiency virus type 1 protease cleavage site mutations associated with protease inhibitor cross-resistance selected by indinavir, ritonavir, and/or saquinavir. J Virol 75: 589-594.
29. Kolli M, Lastere S, Schiffer CA, (2006) Co-evolution of nelfinavir-resistant HIV-1 protease and the p1-p6 substrate. Virology 347: 405-409.
30. Gupta RK, Kohli A, McCormick AL, Towers GJ, Pillay D, et al. (2010) Full-length HIV-1 Gag determines protease inhibitor susceptibility within in vitro assays. AIDS 24: 1651-1655.
31. Jinnopat P, Isarangkura-na-ayuthaya P, Utachee P, Kitagawa Y, de Silva UC, et al. (2009) Impact of amino acid variations in Gag and protease of HIV type 1 CRF01_AE strains on drug susceptibility of virus to protease inhibitors. J Acquir Immune Defic Syndr 52: 320-328.
32. Chang SY, Sutthent R, Auewarakul P, Apichartpiyakul C, Essex M, et al. (1999) Differential stability of the mRNA secondary structures in the frameshift site of various HIV type 1 viruses. AIDS Res Hum Retroviruses 15: 1591-1596.
33. Larrouy L, Chazallon C, Landman R, Capitant C, Peytavin G, et al. (2010) Gag mutations can impact virological response to dual-boosted protease inhibitor combinations in antiretroviral-naive HIV-infected patients. Antimicrob Agents Chemother 54: 2910-2919.
34. Telenti A, Martinez R, Munoz M, Bleiber G, Greub G, et al. (2002) Analysis of natural variants of the human immunodeficiency virus type 1 gag-pol frameshift stem-loop structure. J Virol 76: 7868-7873.
35. Holguin A, Paxinos E, Hertogs K, Womac C, Soriano V, (2004) Impact of frequent natural polymorphisms at the protease gene on the in vitro susceptibility to protease inhibitors in HIV-1 non-B subtypes. J Clin Virol 31: 215-220.
36. Pieniazek D, Rayfield M, Hu DJ, Nkengasong J, Wiktor SZ, et al. (2000) Protease sequences from HIV-1 group M subtypes A-H reveal distinct amino acid mutation patterns associated with protease resistance in protease inhibitor-naive individuals worldwide. HIV Variant Working Group. AIDS 14: 1489-1495.
37. Holguin A, Sune C, Hamy F, Soriano V, Klimkait T, (2006) Natural polymorphisms in the protease gene modulate the replicative capacity of non-B HIV-1 variants in the absence of drug pressure. J Clin Virol 36: 264-271.
38. Kantor R, Katzenstein DA, Efron B, Carvalho AP, Wynhoven B, et al. (2005) Impact of HIV-1 subtype and antiretroviral therapy on protease and reverse transcriptase genotype: results of a global collaboration. PLoS Med 2: e112.
39. Lisovsky I, Schader SM, Martinez-Cajas JL, Oliveira M, Moisi D, et al. (2010) HIV-1 protease codon 36 polymorphisms and differential development of resistance to nelfinavir, lopinavir, and atazanavir in different HIV-1 subtypes. Antimicrob Agents Chemother 54: 2878-2885.
40. Verheyen J, Knops E, Kupfer B, Hamouda O, Somogyi S, et al. (2009) Prevalence of C-terminal gag cleavage site mutations in HIV from therapy-naive patients. J Infect 58: 61-67.
41. de Mendoza C, Garrido C, Corral A, Zahonero N, Soriano V, (2008) Prevalence and impact of HIV-1 protease mutation L76V on lopinavir resistance. AIDS 22: 311-313.
42. Knops E, Kemper I, Schulter E, Pfister H, Kaiser R, et al. (2010) The evolution of protease mutation 76V is associated with protease mutation 46I and gag mutation 431V. AIDS 24: 779-781.
43. Nijhuis M, Wensing AM, Bierman WF, de Jong D, Kagan R, et al. (2009) Failure of treatment with first-line lopinavir boosted with ritonavir can be explained by novel resistance pathways with protease mutation 76V. J Infect Dis 200: 698-709.
44. Barth RE, van der Loeff MF, Schuurman R, Hoepelman AI, Wensing AM, (2010) Virological follow-up of adult patients in antiretroviral treatment programmes in sub-Saharan Africa: a systematic review. Lancet Infect Dis 10: 155-166.
45. Touloumi G, Pantazis N, Chaix ML, Meyer L, Thiebaut R, et al. (2011) Virologic and immunologic response to cART by HIV-1 subtype in the CASCADE collaboration. 18th Conference on Retroviruses and Opportunistic Infections. Boston, USA.
46. Bartlett J, Aga E, Ribaudo H, Wallis C, Katzenstein D, et al. (2011) A pilot study of LPV/r monotherapy following virologic failure of first-line NNRTI-containing regimens in resource-limited settings: the week-24 primary analysis of ACTG 5230. 18th Conference on Retroviruses and Opportunistic Infections. Boston USA.
47. Bunupuradah T, Chetchotisakd P, Munsakul W, Jirajariyavet S, Kantipong P, et al. (2011) Second-line LPV/r monotherapy was inferior to TDF/3TC/LPV/r in patients who failed NNRTI regimen: HIV STAR study. 18th Conference on Retroviruses and Opportunistic Infections. Boston, USA.