Viral decay kinetics in the highly active antiretroviral therapy-treated rhesus macaque model of AIDS

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Deere, Jesse D ^a   Higgins, Joanne ^a   Cannavo, Elda ^a   Villalobos, Andradi ^a   Adamson, Lourdes ^a   Fromentin, Emilie ^c   Schinazi, Raymond F ^c   Luciw, Paul A ^a,b   North, Thomas W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EFAVIRENZ; EMTRICITABINE; TENOFOVIR; VIRUS RNA; BENZOXAZINE DERIVATIVE; RNA DIRECTED DNA POLYMERASE; RNA DIRECTED DNA POLYMERASE INHIBITOR;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MACACA; NONHUMAN; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA; VIRUS CONCENTRATION; VIRUS LOAD; ANIMAL; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN IMMUNODEFICIENCY VIRUS 1; METHODOLOGY; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIROLOGY;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

ANIMALS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BENZOXAZINES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HIV REVERSE TRANSCRIPTASE; HIV-1; MACACA; MACACA MULATTA; REVERSE TRANSCRIPTASE INHIBITORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA;

EID: 77955398278     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011640     Document Type: Article

References (53)

1. Collier AC, Coombs RW, Schoenfeld DA, Bassett RL, Timpone J, et al. (1996) Treatment of human immunodeficiency virus infection with saquinavir, zidovudine, and zalcitabine. AIDS Clinical Trials Group. N Engl J Med 334: 1011-1017.
2. Gulick RM, Mellors JW, Havlir D, Eron JJ, Gonzalez C, et al. (1997) Treatment with indinavir, zidovudine, and lamivudine in adults with human immunodeficiency virus infection and prior antiretroviral therapy. N Engl J Med 337: 734-739.
3. Hammer SM, Squires KE, Hughes MD, Grimes JM, Demeter LM, et al. (1997) A controlled trial of two nucleoside analogues plus indinavir in persons with human immunodeficiency virus infection and CD4 cell counts of 200 per cubic millimeter or less. AIDS Clinical Trials Group 320 Study Team. N Engl J Med 337: 725-733.
4. Havlir DV, Strain MC, Clerici M, Ignacio C, Trabattoni D, et al. (2003) Productive infection maintains a dynamic steady state of residual viremia in human immunodeficiency virus type 1-infected persons treated with suppressive antiretroviral therapy for five years. J Virol 77: 11212-11219.
5. Maldarelli F, Palmer S, King MS, Wiegand A, Polis MA, et al. (2007) ART suppresses plasma HIV-1 RNA to a stable set point predicted by pretherapy viremia. PLoS Pathog 3: e46.
6. Palmer S, Maldarelli F, Wiegand A, Bernstein B, Hanna GJ, et al. (2008) Lowlevel viremia persists for at least 7 years in patients on suppressive antiretroviral therapy. Proc Natl Acad Sci U S A 105: 3879-3884.
7. Palmer S, Wiegand AP, Maldarelli F, Bazmi H, Mican JM, et al. (2003) New real-time reverse transcriptase-initiated PCR assay with single-copy sensitivity for human immunodeficiency virus type 1 RNA in plasma. J Clin Microbiol 41: 4531-4536.
8. Deeks SG, Wrin T, Liegler T, Hoh R, Hayden M, et al. (2001) Virologic and immunologic consequences of discontinuing combination antiretroviral-drug therapy in HIV-infected patients with detectable viremia. N Engl J Med 344: 472-480.
9. Harrigan PR, Whaley M, Montaner JS (1999) Rate of HIV-1 RNA rebound upon stopping antiretroviral therapy. AIDS 13: F59-62.
10. Geeraert L, Kraus G, Pomerantz RJ (2008) Hide-and-seek: the challenge of viral persistence in HIV-1 infection. Annu Rev Med 59: 487-501.
11. Lassen K, Han Y, Zhou Y, Siliciano J, Siliciano RF (2004) The multifactorial nature of HIV-1 latency. Trends Mol Med 10: 525-531.
12. Tobin NH, Learn GH, Holte SE, Wang Y, Melvin AJ, et al. (2005) Evidence that low-level viremias during effective highly active antiretroviral therapy result from two processes: expression of archival virus and replication of virus. J Virol 79: 9625-9634.
13. Zhang L, Chung C, Hu BS, He T, Guo Y, et al. (2000) Genetic characterization of rebounding HIV-1 after cessation of highly active antiretroviral therapy. J Clin Invest 106: 839-845.
14. Ho DD, Neumann AU, Perelson AS, Chen W, Leonard JM, et al. (1995) Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373: 123-126.
15. Perelson AS, Essunger P, Ho DD (1997) Dynamics of HIV-1 and CD4+ lymphocytes in vivo. Aids 11 Suppl A: S17-24.
16. Perelson AS, Essunger P, Cao Y, Vesanen M, Hurley A, et al. (1997) Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387: 188-191.
17. Wei X, Ghosh SK, Taylor ME, Johnson VA, Emini EA, et al. (1995) Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373: 117-122.
18. Chun TW, Engel D, Berrey MM, Shea T, Corey L, et al. (1998) Early establishment of a pool of latently infected, resting CD4(+) T cells during primary HIV-1 infection. Proc Natl Acad Sci U S A 95: 8869-8873.
19. Chun TW, Stuyver L, Mizell SB, Ehler LA, Mican JA, et al. (1997) Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci U S A 94: 13193-13197.
20. Finzi D, Blankson J, Siliciano JD, Margolick JB, Chadwick K, et al. (1999) Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med 5: 512-517.
21. Finzi D, Hermankova M, Pierson T, Carruth LM, Buck C, et al. (1997) Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278: 1295-1300.
22. Gavegnano C, Schinazi RF (2009) Antiretroviral therapy in macrophages: implication for HIV eradication. Antivir Chem Chemother 20: 63-78.
23. Wong JK, Hezareh M, Gunthard HF, Havlir DV, Ignacio CC, et al. (1997) Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 278: 1291-1295.
24. Chun TW, Davey RT, Jr., Ostrowski M, Shawn Justement J, Engel D, et al. (2000) Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nat Med 6: 757-761.
25. Lewin SR, Vesanen M, Kostrikis L, Hurley A, Duran M, et al. (1999) Use of real-time PCR and molecular beacons to detect virus replication in human immunodeficiency virus type 1-infected individuals on prolonged effective antiretroviral therapy. J Virol 73: 6099-6103.
26. Chun TW, Fauci AS (1999) Latent reservoirs of HIV: obstacles to the eradication of virus. Proc Natl Acad Sci U S A 96: 10958-10961.
27. Lundgren JD, Babiker A, El-Sadr W, Emery S, Grund B, et al. (2008) Inferior clinical outcome of the CD4+ cell count-guided antiretroviral treatment interruption strategy in the SMART study: role of CD4+ Cell counts and HIV RNA levels during follow-up. J Infect Dis 197: 1145-1155.
28. Giuffre AC, Higgins J, Buckheit RW, Jr., North TW (2003) Susceptibilities of simian immunodeficiency virus to protease inhibitors. Antimicrob Agents Chemother 47: 1756-1759.
29. Shen A, Zink MC, Mankowski JL, Chadwick K, Margolick JB, et al. (2003) Resting CD4+ T lymphocytes but not thymocytes provide a latent viral reservoir in a simian immunodeficiency virus-Macaca nemestrina model of human immunodeficiency virus type 1-infected patients on highly active antiretroviral therapy. J Virol 77: 4938-4949.
30. Van Rompay KK, Matthews TB, Higgins J, Canfield DR, Tarara RP, et al. (2002) Virulence and reduced fitness of simian immunodeficiency virus with the M184V mutation in reverse transcriptase. J Virol 76: 6083-6092.
31. Gardner MB, Luciw PA (1989) Animal models of AIDS. FASEB J 3: 2593-2606.
32. Gardner MB, Carlos MP, Luciw PA (2004) Simian Retroviruses. In: Wormser GP, ed. AIDS and Other Manifestations of HIV Infection, 4th ed: Raven Press (NY). pp 195-262.
33. Dinoso JB, Rabi SA, Blankson JN, Gama L, Mankowski JL, et al. (2009) A simian immunodeficiency virus-infected macaque model to study viral reservoirs that persist during highly active antiretroviral therapy. J Virol 83: 9247-9257.
34. Hammer SM, Eron JJ, Jr., Reiss P, Schooley RT, Thompson MA, et al. (2008) Antiretroviral treatment of adult HIV infection: 2008 recommendations of the International AIDS Society-USA panel. JAMA 300: 555-570.
35. Ambrose Z, Palmer S, Boltz VF, Kearney M, Larsen K, et al. (2007) Suppression of viremia and evolution of human immunodeficiency virus type 1 drug resistance in a macaque model for antiretroviral therapy. J Virol 81: 12145-12155.
36. Hatziioannou T, Ambrose Z, Chung NP, Piatak M, Jr., Yuan F, et al. (2009) A macaque model of HIV-1 infection. Proc Natl Acad Sci U S A 106: 4425-4429.
37. North TW, Van Rompay KK, Higgins J, Matthews TB, Wadford DA, et al. (2005) Suppression of virus load by highly active antiretroviral therapy in rhesus macaques infected with a recombinant simian immunodeficiency virus containing reverse transcriptase from human immunodeficiency virus type 1. J Virol 79: 7349-7354.
38. Uberla K, Stahl-Hennig C, Bottiger D, Matz-Rensing K, Kaup FJ, et al. (1995) Animal model for the therapy of acquired immunodeficiency syndrome with reverse transcriptase inhibitors. Proc Natl Acad Sci U S A 92: 8210-8214.
39. Balzarini J, De Clercq E, Uberla K (1997) SIV/HIV-1 hybrid virus expressing the reverse transcriptase gene of HIV-1 remains sensitive to HIV-1-specific reverse transcriptase inhibitors after passage in rhesus macaques. J Acquir Immune Defic Syndr Hum Retrovirol 15: 1-4.
40. Balzarini J, Weeger M, Camarasa MJ, De Clercq E, Uberla K (1995) Sensitivity/resistance profile of a simian immunodeficiency virus containing the reverse transcriptase gene of human immunodeficiency virus type 1 (HIV-1) toward the HIV-1-specific non-nucleoside reverse transcriptase inhibitors. Biochem Biophys Res Commun 211: 850-856.
41. Hofman MJ, Higgins J, Matthews TB, Pedersen NC, Tan C, et al. (2004) Efavirenz therapy in rhesus macaques infected with a chimera of simian immunodeficiency virus containing reverse transcriptase from human immunodeficiency virus type 1. Antimicrob Agents Chemother 48: 3483-3490.
42. Luciw PA, Pratt-Lowe E, Shaw KE, Levy JA, Cheng-Mayer C (1995) Persistent infection of rhesus macaques with T-cell-line-tropic and macrophage-tropic clones of simian/human immunodeficiency viruses (SHIV). Proc Natl Acad Sci U S A 92: 7490-7494.
43. Soderberg K, Denekamp L, Nikiforow S, Sautter K, Desrosiers RC, et al. (2002) A nucleotide substitution in the tRNA(Lys) primer binding site dramatically increases replication of recombinant simian immunodeficiency virus containing a human immunodeficiency virus type 1 reverse transcriptase. J Virol 76: 5803-5806.
44. Grant CK, DeBoer DJ, Essex M, Worley MB, Higgins J (1977) Antibodies from healthy cats exposed to feline leukemia virus lyse feline lymphoma cells slowly with cat complement. J Immunol 119: 401-406.
45. Van Rompay KK, Brignolo LL, Meyer DJ, Jerome C, Tarara R, et al. (2004) Biological effects of short-term or prolonged administration of 9-[2-(phosphonomethoxy) propyl]adenine (tenofovir) to newborn and infant rhesus macaques. Antimicrob Agents Chemother 48: 1469-1487.
46. Cline AN, Bess JW, Piatak M, Jr., Lifson JD (2005) Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J Med Primatol 34: 303-312.
47. Leutenegger CM, Higgins J, Matthews TB, Tarantal AF, Luciw PA, et al. (2001) Real-time TaqMan PCR as a specific and more sensitive alternative to the branched-chain DNA assay for quantitation of simian immunodeficiency virus RNA. AIDS Res Hum Retroviruses 17: 243-251.
48. Tandon R, Cattori V, Gomes-Keller MA, Meli ML, Golder MC, et al. (2005) Quantitation of feline leukaemia virus viral and proviral loads by TaqMan realtime polymerase chain reaction. J Virol Methods 130: 124-132.
49. North TW, Higgins J, Deere JD, Hayes TL, Villalobos A, et al. (2010) Viral sanctuaries during highly active antiretroviral therapy in a nonhuman primate model for AIDS. J Virol 84: 2913-2922.
50. Chun TW, Nickle DC, Justement JS, Large D, Semerjian A, et al. (2005) HIVinfected individuals receiving effective antiviral therapy for extended periods of time continually replenish their viral reservoir. J Clin Invest 115: 3250-3255.
51. Chun TW, Nickle DC, Justement JS, Meyers JH, Roby G, et al. (2008) Persistence of HIV in gut-associated lymphoid tissue despite long-term antiretroviral therapy. J Infect Dis 197: 714-720.
52. Dinoso JB, Kim SY, Wiegand AM, Palmer SE, Gange SJ, et al. (2009) Treatment intensification does not reduce residual HIV-1 viremia in patients on highly active antiretroviral therapy. Proc Natl Acad Sci U S A 106: 9403-9408.
53. Joos B, Fischer M, Kuster H, Pillai SK, Wong JK, et al. (2008) HIV rebounds from latently infected cells, rather than from continuing low-level replication. Proc Natl Acad Sci U S A 105: 16725-16730.