SHIV-162P3 infection of rhesus macaques given maraviroc gel vaginally does not involve resistant viruses

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Tsibris, Athe M N ^a,b   Pal, Urboshi ^c   Schure, Allison L ^a   Veazey, Ronald S ^d   Kunstman, Kevin J ^e   Henrich, Timothy J ^b,f   Klasse, P J ^g   Wolinsky, Steven M ^e   Kuritzkes, Daniel R ^b,f   Moore, John P ^g  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

^g WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 160; MARAVIROC; AGENTS USED INTRAVAGINALLY; CYCLOHEXANE DERIVATIVE; GP120 PROTEIN, SIMIAN IMMUNODEFICIENCY VIRUS; MEMBRANE PROTEIN; TRIAZOLE DERIVATIVE; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; DRUG EFFICACY; ENTROPY; GEL; GENE MUTATION; GENETIC DISTANCE; GENOTYPE; HUMAN; HUMAN CELL; IC 50; INOCULATION; LENTIVIRINAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POISSON DISTRIBUTION; RHESUS MONKEY; SIMIAN HUMAN IMMUNODEFICIENCY VIRUS; UNINDEXED SEQUENCE; VIREMIA; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS INHIBITION; VIRUS ISOLATION; VIRUS RESISTANCE; VIRUS STRAIN; VIRUS TRANSMISSION; ANIMAL; ANTIVIRAL RESISTANCE; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; FEMALE; GENETICS; INTRAVAGINAL DRUG ADMINISTRATION; MACACA MULATTA; METABOLISM; MOLECULAR GENETICS; MUTATION; REPRODUCIBILITY; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS GENOME; VIRUS LOAD;

ADMINISTRATION, INTRAVAGINAL; ANIMALS; CELL LINE; CYCLOHEXANES; DRUG RESISTANCE, VIRAL; ENTROPY; FEMALE; GENOME, VIRAL; HUMANS; MACACA MULATTA; MEMBRANE GLYCOPROTEINS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; REPRODUCIBILITY OF RESULTS; SIMIAN IMMUNODEFICIENCY VIRUS; TRIAZOLES; VAGINAL CREAMS, FOAMS, AND JELLIES; VIRAL ENVELOPE PROTEINS; VIRAL LOAD; VIRAL PROTEINS;

EID: 82555175887     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028047     Document Type: Article

References (51)

1. Hladik F, Hope TJ, (2009) HIV infection of the genital mucosa in women. Curr HIV/AIDS Rep 6: 20-28.
2. UNAIDS website. UNAIDS Report on the Global AIDS Epidemic (2008) Available: http://www.unaids.org/en/dataanalysis/epidemiology/2008reportontheglobalaidsepidemic/. Accessed 2011 Nov 10.
3. Grant RM, Hamer D, Hope T, Johnston R, Lange J, et al. (2008) Whither or wither microbicides? Science 321: 532-534.
4. Klasse PJ, Shattock R, Moore JP, (2008) Antiretroviral drug-based microbicides to prevent HIV-1 sexual transmission. Annu Rev Med 59: 455-471.
5. Lederman MM, Veazey RS, Offord R, Mosier DE, Dufour J, et al. (2004) Prevention of vaginal SHIV transmission in rhesus macaques through inhibition of CCR5. Science 306: 485-487.
6. Veazey RS, Klasse PJ, Schader SM, Hu Q, Ketas TJ, et al. (2005) Protection of macaques from vaginal SHIV challenge by vaginally delivered inhibitors of virus-cell fusion. Nature 438: 99-102.
7. Cranage M, Sharpe S, Herrera C, Cope A, Dennis M, et al. (2008) Prevention of SIV rectal transmission and priming of T cell responses in macaques after local pre-exposure application of tenofovir gel. PLoS Med 5: e157; discussion e157.
8. Parikh UM, Dobard C, Sharma S, Cong ME, Jia H, et al. (2009) Complete protection from repeated vaginal simian-human immunodeficiency virus exposures in macaques by a topical gel containing tenofovir alone or with emtricitabine. J Virol 83: 10358-10365.
9. Abdool Karim Q, Abdool Karim SS, Frohlich JA, Grobler AC, Baxter C, et al. (2010) Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 329: 1168-1174.
10. Veazey RS, Ketas TJ, Dufour J, Moroney-Rasmussen T, Green LC, et al. (2010) Protection of rhesus macaques from vaginal infection by vaginally delivered maraviroc, an inhibitor of HIV-1 entry via the CCR5 co-receptor. J Infect Dis 202: 739-744.
11. Pirrone V, Thakkar N, Jacobson JM, Wigdahl B, Krebs FC, (2011) Combinatorial approaches to the prevention and treatment of HIV-1 infection. Antimicrob Agents Chemother 55: 1831-1842.
12. Supervie V, Garcia-Lerma JG, Heneine W, Blower S, (2010) HIV, transmitted drug resistance, and the paradox of preexposure prophylaxis. Proc Natl Acad Sci U S A 107: 12381-12386.
13. Tsibris AM, Korber B, Arnaout R, Russ C, Lo CC, et al. (2009) Quantitative deep sequencing reveals dynamic HIV-1 escape and large population shifts during CCR5 antagonist therapy in vivo. PLoS One 4: e5683.
14. Tilton JC, Amrine-Madsen H, Miamidian JL, Kitrinos KM, Pfaff J, et al. (2010) HIV type 1 from a patient with baseline resistance to CCR5 antagonists uses drug-bound receptor for entry. AIDS Res Hum Retroviruses 26: 13-24.
15. Roche M, Jakobsen MR, Ellett A, Salimiseyedabad H, Jubb B, et al. (2011) HIV-1 predisposed to acquiring resistance to maraviroc (MVC) and other CCR5 antagonists in vitro has an inherent, low-level ability to utilize MVC-bound CCR5 for entry. Retrovirology in press.
16. Connor RI, Sheridan KE, Ceradini D, Choe S, Landau NR, (1997) Change in coreceptor use coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 185: 621-628.
17. Schuitemaker H, Koot M, Kootstra NA, Dercksen MW, de Goede RE, et al. (1992) Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population. J Virol 66: 1354-1360.
18. Fatkenheuer G, Nelson M, Lazzarin A, Konourina I, Hoepelman AI, et al. (2008) Subgroup analyses of maraviroc in previously treated R5 HIV-1 infection. N Engl J Med 359: 1442-1455.
19. Gulick RM, Lalezari J, Goodrich J, Clumeck N, DeJesus E, et al. (2008) Maraviroc for previously treated patients with R5 HIV-1 infection. N Engl J Med 359: 1429-1441.
20. Dudley DM, Wentzel JL, Lalonde MS, Veazey RS, Arts EJ, (2009) Selection of a simian-human immunodeficiency virus strain resistant to a vaginal microbicide in macaques. J Virol 83: 5067-5076.
21. Nedellec R, Coetzer M, Lederman MM, Offord RE, Hartley O, et al. (2010) "Resistance" to PSC-RANTES revisited: two mutations in human immunodeficiency virus type 1 HIV-1 SF162 or simian-human immunodeficiency virus SHIV SF162-p3 do not confer resistance. J Virol 84: 5842-5845.
22. Jordan MR, Kearney M, Palmer S, Shao W, Maldarelli F, et al. (2010) Comparison of standard PCR/cloning to single genome sequencing for analysis of HIV-1 populations. J Virol Methods 168: 114-120.
23. Tsai L, Trunova N, Gettie A, Mohri H, Bohm R, et al. (2007) Efficient repeated low-dose intravaginal infection with X4 and R5 SHIVs in rhesus macaque: implications for HIV-1 transmission in humans. Virology 362: 207-216.
24. Varela M, Landskron L, Lai RP, McKinley TJ, Bogers WM, et al. (2011) Molecular evolution analysis of the Human Immunodeficiency Virus type 1 envelope in SHIV-infected macaques: implications for challenge dose selection. J Virol.
25. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, et al. (2011) Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc Natl Acad Sci U S A 108: 11181-11186.
26. Anastassopoulou CG, Ketas TJ, Klasse PJ, Moore JP, (2009) Resistance to CCR5 inhibitors caused by sequence changes in the fusion peptide of HIV-1 gp41. Proc Natl Acad Sci U S A 106: 5318-5323.
27. Kuhmann SE, Pugach P, Kunstman KJ, Taylor J, Stanfield RL, et al. (2004) Genetic and phenotypic analyses of human immunodeficiency virus type 1 escape from a small-molecule CCR5 inhibitor. J Virol 78: 2790-2807.
28. Tsibris AM, Sagar M, Gulick RM, Su Z, Hughes M, et al. (2008) In vivo emergence of vicriviroc resistance in a human immunodeficiency virus type 1 subtype C-infected subject. J Virol 82: 8210-8214.
29. Moore JP, Kuritzkes DR, (2009) A piece de resistance: how HIV-1 escapes small molecule CCR5 inhibitors. Curr Opin HIV AIDS 4: 118-124.
30. Kirchherr JL, Lu X, Kasongo W, Chalwe V, Mwananyanda L, et al. (2007) High throughput functional analysis of HIV-1 env genes without cloning. J Virol Methods 143: 104-111.
31. Lin NH, Negusse DM, Beroukhim R, Giguel F, Lockman S, et al. (2010) The design and validation of a novel phenotypic assay to determine HIV-1 coreceptor usage of clinical isolates. J Virol Methods 169: 39-46.
32. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, et al. (2011) Geneious v5.4.6, Available: http://www.geneious.com. Accessed 2011 Nov 11.
33. Giorgi EE, Funkhouser B, Athreya G, Perelson AS, Korber BT, et al. (2010) Estimating time since infection in early homogeneous HIV-1 samples using a poisson model. BMC Bioinformatics 11: 532.
34. Greenier JL, Miller CJ, Lu D, Dailey PJ, Lu FX, et al. (2001) Route of simian immunodeficiency virus inoculation determines the complexity but not the identity of viral variant populations that infect rhesus macaques. J Virol 75: 3753-3765.
35. Stone M, Keele BF, Ma ZM, Bailes E, Dutra J, et al. (2010) A limited number of simian immunodeficiency virus (SIV) env variants are transmitted to rhesus macaques vaginally inoculated with SIVmac251. J Virol 84: 7083-7095.
36. Sagar M, Kirkegaard E, Long EM, Celum C, Buchbinder S, et al. (2004) Human immunodeficiency virus type 1 (HIV-1) diversity at time of infection is not restricted to certain risk groups or specific HIV-1 subtypes. J Virol 78: 7279-7283.
37. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, et al. (2008) Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82: 3952-3970.
38. Zhu T, Mo H, Wang N, Nam DS, Cao Y, et al. (1993) Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261: 1179-1181.
39. Zhang LQ, MacKenzie P, Cleland A, Holmes EC, Brown AJ, et al. (1993) Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. J Virol 67: 3345-3356.
40. Valley-Omar Z, Anderson J, Arney L, Sibeko S, Naranbhai V, et al. Multiple Variant HIV Transmission: CAPRISA 004 TNV Microbicide Trial; March 8, 2011; Boston, MA. Abstract #491.
41. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552-7557.
42. Fischer W, Ganusov VV, Giorgi EE, Hraber PT, Keele BF, et al. (2010) Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS One 5: e12303.
43. Shankarappa R, Margolick JB, Gange SJ, Rodrigo AG, Upchurch D, et al. (1999) Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J Virol 73: 10489-10502.
44. Kuiken CL, Lukashov VV, Baan E, Dekker J, Leunissen JA, et al. (1996) Evidence for limited within-person evolution of the V3 domain of the HIV-1 envelope in the amsterdam population. Aids 10: 31-37.
45. Forbes CJ, Lowry D, Geer L, Veazey RS, Shattock RJ, et al. (2011) Non-aqueous silicone elastomer gels as a vaginal microbicide delivery system for the HIV-1 entry inhibitor maraviroc. J Control Release.
46. Haase AT, (2011) Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu Rev Med 62: 127-139.
47. Henrich TJ, Tsibris AM, Lewine NR, Konstantinidis I, Leopold KE, et al. (2010) Evolution of CCR5 antagonist resistance in an HIV-1 subtype C clinical isolate. J Acquir Immune Defic Syndr 55: 420-427.
48. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol.
49. Yang Z, (1994) Estimating the pattern of nucleotide substitution. J Mol Evol 39: 105-111.
50. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
51. Lu J, Sista P, Giguel F, Greenberg M, Kuritzkes DR, (2004) Relative replicative fitness of human immunodeficiency virus type 1 mutants resistant to enfuvirtide (T-20). J Virol 78: 4628-4637.