Simian immunodeficiency virus SIVsab infection of rhesus macaques as a model of complete immunological suppression with persistent reservoirs of replication-competent virus: Implications for cure research

Journal of Virology

Volumn 89, Issue 11, 2015, Pages 6155-6160

  Ma, Dongzhu ^a   Xu, Cuiling ^a   Cillo, Anthony R ^b   Policicchio, Benjamin ^a,c   Kristoff, Jan ^a,c   Haret Richter, George ^a   Mellors, John W ^b   Pandrea, Ivona ^a,b   Apetrei, Cristian ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MALE; NONHUMAN; PRIORITY JOURNAL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; T CELL DEPLETION; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; PHYSIOLOGY; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY;

MACACA MULATTA; REPLICATION COMPETENT VIRUSES; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; IMMUNE TOLERANCE; MACACA MULATTA; MALE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

EID: 84929643176     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00256-15     Document Type: Article

References (43)

1. Allers K, Hutter G, Hofmann J, Loddenkemper C, Rieger K, Thiel E, Schneider T. 2011. Evidence for the cure of HIV infection by CCR5Delta32/Delta32 stem cell transplantation. Blood 117:2791-2799. http://dx.doi.org/10.1182/blood-2010-09-309591.
2. Lewin SR, Evans VA, Elliott JH, Spire B, Chomont N. 2011. Finding a cure for HIV: will it ever be achievable? J Int AIDS Soc 14:4. http://dx.doi.org/10.1186/1758-2652-14-4.
3. Luzuriaga K, Gay H, Ziemniak C, Sanborn KB, Somasundaran M, Rainwater-Lovett K, Mellors JW, Rosenbloom D, Persaud D. 2015. Viremic relapse after HIV-1 remission in a perinatally infected child. N Engl J Med 372:786-788. http://dx.doi.org/10.1056/NEJMc1413931.
4. Henrich TJ, Hanhauser E, Hu Z, Stellbrink HJ, Noah C, Martin JN, Deeks SG, Kuritzkes DR, Pereyra F. 2015. Viremic control and viral coreceptor usage in two HIV-1-infected persons homozygous for CCR5 Δ32. AIDS http://dx.doi.org/10.1097/QAD.0000000000000629.
5. Deeks SG, Barre-Sinoussi F. 2012. Public health: towards a cure for HIV. Nature 487:293-294. http://dx.doi.org/10.1038/487293a.
6. International AIDS Society Scientific Working Group on HIV Cure, Deeks SG, Autran B, Berkhout B, Benkirane M, Cairns S, Chomont N, Chun TW, Churchill M, Di Mascio M, Katlama C, Lafeuillade A, Landay A, Lederman M, Lewin SR, Maldarelli F, Margolis D, Markowitz M, Martinez-Picado J, Mullins JI, Mellors J, Moreno S, O'Doherty U, Palmer S, Penicaud MC, Peterlin M, Poli G, Routy JP, Rouzioux C, Silvestri G, Stevenson M, Telenti A, Van Lint C, Verdin E, Woolfrey A, Zaia J, Barre-Sinoussi F. 2012. Towards an HIV cure: a global scientific strategy. Nat Rev Immunol 12:607-614. http://dx.doi.org/10.1038/nri3262.
7. Saez-Cirion A, Bacchus C, Hocqueloux L, Avettand-Fenoel V, Girault I, Lecuroux C, Potard V, Versmisse P, Melard A, Prazuck T, Descours B, Guergnon J, Viard JP, Boufassa F, Lambotte O, Goujard C, Meyer L, Costagliola D, Venet A, Pancino G, Autran B, Rouzioux C, ANRS VISCONTI Study Group. 2013. Post-treatment HIV-1 controllers with a long-term virological remission after the interruption of early initiated antiretroviral therapy ANRS VISCONTI study. PLoS Pathog 9:e1003211. http://dx.doi.org/10.1371/journal.ppat.1003211.
8. Apetrei C, Pandrea I, Mellors JW. 2012. Nonhuman primate models for HIV cure research. PLoS Pathog 8:e1002892. http://dx.doi.org/10.1371/journal.ppat.1002892.
9. Shytaj IL, Norelli S, Chirullo B, Della Corte A, Collins M, Yalley-Ogunro J, Greenhouse J, Iraci N, Acosta EP, Barreca ML, Lewis MG, Savarino A. 2012. A highly intensified ART regimen induces long-term viral suppression and restriction of the viral reservoir in a simian AIDS model. PLoS Pathog 8:e1002774. http://dx.doi.org/10.1371/journal.ppat.1002774.
10. Del Prete GQ, Shoemaker R, Oswald K, Lara A, Trubey CM, Fast R, Schneider DK, Kiser R, Coalter V, Wiles A, Wiles R, Freemire B, Keele BF, Estes JD, Quinones OA, Smedley J, Macallister R, Sanchez RI, Wai JS, Tan CM, Alvord WG, Hazuda DJ, Piatak M, Jr, Lifson JD. 2014. Effect of suberoylanilide hydroxamic acid (SAHA) administration on the residual virus pool in a model of combination antiretroviral therapymediated suppression in SIVmac239-infected Indian rhesus macaques. Antimicrob Agents Chemother 58:6790-6806. http://dx.doi.org/10.1128/AAC.03746-14.
11. Denton PW, Olesen R, Choudhary SK, Archin NM, Wahl A, Swanson MD, Chateau M, Nochi T, Krisko JF, Spagnuolo RA, Margolis DM, Garcia JV. 2012. Generation of HIV latency in humanized BLT mice. J Virol 86:630-634. http://dx.doi.org/10.1128/JVI.06120-11.
12. Choudhary SK, Archin NM, Cheema M, Dahl NP, Garcia JV, Margolis DM. 2012. Latent HIV-1 infection of resting CD4+ T cells in the humanized Rag2-/- γc1/1 mouse. J Virol 86:114-120. http://dx.doi.org/10.1128/JVI.05590-11.
13. Pandrea I, Apetrei C, Dufour J, Dillon N, Barbercheck J, Metzger M, Jacquelin B, Bohm R, Marx PA, Barre-Sinoussi F, Hirsch VM, Muller-Trutwin MC, Lackner AA, Veazey RS. 2006. Simian immunodeficiency virus SIVagm.sab infection of Caribbean African green monkeys: a new model for the study of SIV pathogenesis in natural hosts. J Virol 80:4858-4867. http://dx.doi.org/10.1128/JVI.80.10.4858-4867.2006.
14. Pandrea I, Gaufin T, Gautam R, Kristoff J, Mandell D, Montefiori D, Keele BF, Ribeiro RM, Veazey RS, Apetrei C. 2011. Functional cure of SIVagm infection in rhesus macaques results in complete recovery of CD4+ T cells and is reverted by CD8+ cell depletion. PLoS Pathog 7:e1002170. http://dx.doi.org/10.1371/journal.ppat.1002170.
15. Pandrea I, Parrish NF, Raehtz K, Gaufin T, Barbian HJ, Ma D, Kristoff J, Gautam R, Zhong F, Haret-Richter GS, Trichel A, Shaw GM, Hahn BH, Apetrei C. 2012. Mucosal simian immunodeficiency virus transmission in African green monkeys: susceptibility to infection is proportional to target cell availability at mucosal sites. J Virol 86:4158-4168. http://dx.doi.org/10.1128/JVI.07141-11.
16. Mandell DT, Kristoff J, Gaufin T, Gautam R, Ma D, Sandler N, Haret-Richter G, Xu C, Aamer H, Dufour J, Trichel A, Douek DC, Keele BF, Apetrei C, Pandrea I. 2014. Pathogenic features associated with increased virulence upon simian immunodeficiency virus cross-species transmission from natural hosts. J Virol 88:6778-6792. http://dx.doi.org/10.1128/JVI.03785-13.
17. Kristoff J, Haret-Richter G, Ma D, Ribeiro RM, Xu C, Cornell E, Stock JL, He T, Mobley AD, Ross S, Trichel A, Wilson C, Tracy R, Landay A, Apetrei C, Pandrea I. 2014. Early microbial translocation blockade reduces SIV-mediated inflammation and viral replication. J Clin Invest 124: 2802-2806. http://dx.doi.org/10.1172/JCI75090.
18. Wijewardana V, Kristoff J, Xu C, Ma D, Haret-Richter G, Stock JL, Policicchio BB, Mobley AD, Nusbaum R, Aamer H, Trichel A, Ribeiro RM, Apetrei C, Pandrea I. 2013. Kinetics of myeloid dendritic cell trafficking and activation: impact on progressive, nonprogressive and controlled SIV infections. PLoS Pathog 9:e1003600. http://dx.doi.org/10.1371/journal.ppat.1003600.
19. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, DC.
20. Hilldorfer BB, Cillo AR, Besson GJ, Bedison MA, Mellors JW. 2012. New tools for quantifying HIV-1 reservoirs: plasma RNA single copy assays and beyond. Curr HIV/AIDS Rep 9:91-100. http://dx.doi.org/10.1007/s11904-011-0104-6.
21. Whitney JB, Hill AL, Sanisetty S, Penaloza-MacMaster P, Liu J, Shetty M, Parenteau L, Cabral C, Shields J, Blackmore S, Smith JY, Brinkman AL, Peter LE, Mathew SI, Smith KM, Borducchi EN, Rosenbloom DI, Lewis MG, Hattersley J, Li B, Hesselgesser J, Geleziunas R, Robb ML, Kim JH, Michael NL, Barouch DH. 2014. Rapid seeding of the viral reservoir prior to SIV viraemia in rhesus monkeys. Nature 512:74-77. http://dx.doi.org/10.1038/nature13594.
22. Pandrea I, Gautam R, Ribeiro R, Brenchley JM, Butler IF, Pattison M, Rasmussen T, Marx PA, Silvestri G, Lackner AA, Perelson AS, Douek DC, Veazey RS, Apetrei C. 2007. Acute loss of intestinal CD4+ T cells is not predictive of SIV virulence. J Immunol 179:3035-3046. http://dx.doi.org/10.4049/jimmunol.179.5.3035.
23. Pandrea I, Kornfeld C, Ploquin MJ, Apetrei C, Faye A, Rouquet P, Roques P, Simon F, Barre-Sinoussi F, Muller-Trutwin MC, Diop OM. 2005. Impact of viral factors on very early in vivo replication profiles in simian immunodeficiency virus SIVagm-infected African green monkeys. J Virol 79:6249-6259. http://dx.doi.org/10.1128/JVI.79.10.6249-6259.2005.
24. Okoye A, Park H, Rohankhedkar M, Coyne-Johnson L, Lum R, Walker JM, Planer SL, Legasse AW, Sylwester AW, Piatak M, Jr, Lifson JD, Sodora DL, Villinger F, Axthelm MK, Schmitz JE, Picker LJ. 2009. Profound CD4+/CCR5+ T cell expansion is induced by CD8+ lymphocyte depletion but does not account for accelerated SIV pathogenesis. J Exp Med 206:1575-1588. http://dx.doi.org/10.1084/jem.20090356.
25. Stockhausen MT, Kristoffersen K, Stobbe L, Poulsen HS. 2014. Differentiation of glioblastoma multiforme stem-like cells leads to downregulation of EGFR and EGFRvIII and decreased tumorigenic and stem-like cell potential. Cancer Biol Ther 15:216-224. http://dx.doi.org/10.4161/cbt.26736.
26. Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, Yassine-Diab B, Boucher G, Boulassel MR, Ghattas G, Brenchley JM, Schacker TW, Hill BJ, Douek DC, Routy JP, Haddad EK, Sekaly RP. 2009. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med 15:893-900. http://dx.doi.org/10.1038/nm.1972.
27. Chomont N, DaFonseca S, Vandergeeten C, Ancuta P, Sekaly RP. 2011. Maintenance of CD4+ T-cell memory and HIV persistence: keeping memory, keeping HIV. Curr Opin HIV AIDS 6:30-36. http://dx.doi.org/10.1097/COH.0b013e3283413775.
28. Ho YC, Shan L, Hosmane NN, Wang J, Laskey SB, Rosenbloom DI, Lai J, Blankson JN, Siliciano JD, Siliciano RF. 2013. Replication-competent noninduced proviruses in the latent reservoir increase barrier to HIV-1 cure. Cell 155:540-551. http://dx.doi.org/10.1016/j.cell.2013.09.020.
29. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping LH, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM. 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. http://dx.doi.org/10.1073/pnas.0802203105.
30. Eisele E, Siliciano RF. 2012. Redefining the viral reservoirs that prevent HIV-1 eradication. Immunity 37:377-388. http://dx.doi.org/10.1016/j.immuni.2012.08.010.
31. Katlama C, Deeks SG, Autran B, Martinez-Picado J, van Lunzen J, Rouzioux C, Miller M, Vella S, Schmitz JE, Ahlers J, Richman DD, Sekaly RP. 2013. Barriers to a cure for HIV: new ways to target and eradicate HIV-1 reservoirs. Lancet 381:2109-2117. http://dx.doi.org/10.1016/S0140-6736(13)60104-X.
32. Margolis DM. 2011. Eradication therapies for HIV infection: time to begin again. AIDS Res Hum Retroviruses 27:347-353. http://dx.doi.org/10.1089/aid.2011.0017.
33. Margolis DM. 2011. Histone deacetylase inhibitors and HIV latency. Curr Opin HIV AIDS 6:25-29. http://dx.doi.org/10.1097/COH.0b013e328341242d.
34. Chun TW, Engel D, Berrey MM, Shea T, Corey L, Fauci AS. 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. http://dx.doi.org/10.1073/pnas.95.15.8869.
35. Shen A, Zink MC, Mankowski JL, Chadwick K, Margolick JB, Carruth LM, Li M, Clements JE, Siliciano RF. 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. http://dx.doi.org/10.1128/JVI.77.8.4938-4949.2003.
36. Nishimura Y, Sadjadpour R, Mattapallil JJ, Igarashi T, Lee W, Buckler-White A, Roederer M, Chun TW, Martin MA. 2009. High frequencies of resting CD4+T cells containing integrated viral DNA are found in rhesus macaques during acute lentivirus infections. Proc Natl Acad Sci U S A 106:8015-8020. http://dx.doi.org/10.1073/pnas.0903022106.
37. Crise B, Li Y, Yuan C, Morcock DR, Whitby D, Munroe DJ, Arthur LO, Wu X. 2005. Simian immunodeficiency virus integration preference is similar to that of human immunodeficiency virus type 1. J Virol 79: 12199-12204. http://dx.doi.org/10.1128/JVI.79.19.12199-12204.2005.
38. Barber SA, Gama L, Dudaronek JM, Voelker T, Tarwater PM, Clements JE. 2006. Mechanism for the establishment of transcriptional HIV latency in the brain in a simian immunodeficiency virus-macaque model. J Infect Dis 193:963-970. http://dx.doi.org/10.1086/500983.
39. Shen A, Yang HC, Zhou Y, Chase AJ, Boyer JD, Zhang H, Margolick JB, Zink MC, Clements JE, Siliciano RF. 2007. Novel pathway for induction of latent virus from resting CD4+ T cells in the simian immunodeficiency virus/macaque model of human immunodeficiency virus type 1 latency. J Virol 81:1660-1670. http://dx.doi.org/10.1128/JVI.01396-06.
40. Bourry O, Mannioui A, Sellier P, Roucairol C, Durand-Gasselin L, Dereuddre-Bosquet N, Benech H, Roques P, Le Grand R. 2010. Effect of a short-termHAARTon SIV load in macaque tissues is dependent on time of initiation and antiviral diffusion. Retrovirology 7:78. http://dx.doi.org/10.1186/1742-4690-7-78.
41. Mannioui A, Bourry O, Sellier P, Delache B, Brochard P, Andrieu T, Vaslin B, Karlsson I, Roques P, Le Grand R. 2009. Dynamics of viral replication in blood and lymphoid tissues during SIVmac251 infection of macaques. Retrovirology 6:106. http://dx.doi.org/10.1186/1742-4690-6-106.
42. Sellier P, Mannioui A, Bourry O, Dereuddre-Bosquet N, Delache B, Brochard P, Calvo J, Prevot S, Roques P. 2010. Antiretroviral treatment start-time during primary SIV(mac) infection in macaques exerts a different impact on early viral replication and dissemination. PLoS One 5:e10570. http://dx.doi.org/10.1371/journal.pone.0010570.
43. Kearney M, Spindler J, Shao W, Maldarelli F, Palmer S, Hu SL, Lifson JD, KewalRamani VN, Mellors JW, Coffin JM, Ambrose Z. 2011. Genetic diversity of simian immunodeficiency virus encoding HIV-1 reverse transcriptase persists in macaques despite antiretroviral therapy. J Virol 85:1067-1076. http://dx.doi.org/10.1128/JVI.01701-10.