Experimental depletion of CD8+ cells in acutely SIVagm-Infected African Green Monkeys results in increased viral replication

Retrovirology

Volumn 7, Issue , 2010, Pages

  Gaufin, Thaidra ^a   Ribeiro, Ruy M ^b   Gautam, Rajeev ^a   Dufour, Jason ^a   Mandell, Daniel ^a   Apetrei, Cristian ^a,c   Pandrea, Ivona ^c  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CERCOPITHECIDAE; CONTROLLED STUDY; IMMUNE RESPONSE; INTESTINE; LENTIVIRUS INFECTION; LYMPH NODE; LYMPHOCYTE PROLIFERATION; NONHUMAN; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; VIRUS LOAD; VIRUS REPLICATION; ANIMAL; CERCOPITHECUS; FOLLOW UP; IMMUNOLOGY; LYMPHOCYTE DEPLETION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIROLOGY;

ANIMALIA; CERCOPITHECUS AETHIOPS; MACACA; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CERCOPITHECUS AETHIOPS; FOLLOW-UP STUDIES; LYMPHOCYTE DEPLETION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIRUS REPLICATION;

EID: 77951950465     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-7-42     Document Type: Article

References (60)

1. Pandrea I, Apetrei C, Gordon S, Barbercheck J, Dufour J, Bohm R, Sumpter B, Roques P, Marx PA, Hirsch VM, Kaur A, Lackner AA, Veazey RS, Silvestri G. Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood 2007, 109:1069-1076. 10.1182/blood-2006-05-024364, 1785133, 17003371.
2. Pandrea I, Sodora DL, Silvestri G, Apetrei C. Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends Immunol 2008, 29:419-428. 10.1016/j.it.2008.05.004, 2840226, 18676179.
3. Pandrea I, Silvestri G, Onanga R, Veazey RS, Marx PA, Hirsch VM, Apetrei C. Simian immunodeficiency viruses replication dynamics in African non-human primate hosts: common patterns and species-specific differences. J Med Primatol 2006, 35:194-201. 10.1111/j.1600-0684.2006.00168.x, 16872282.
4. Apetrei C, Gautam R, Sumpter B, Carter AC, Gaufin T, Staprans SI, Else J, Barnes M, Cao R, Garg S, Milush JM, Sodora DL, Pandrea I, Silvestri G. Virus-subtype specific features of natural SIVsmm infection in sooty mangabeys. J Virol 2007, 81:7913-7923. 10.1128/JVI.00281-07, 1951324, 17507488.
5. 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. Acute loss of intestinal CD4+ T cells is not predictive of SIV virulence. J Immunol 2007, 179:3035-3046. 2367134, 17709518.
6. Onanga R, Kornfeld C, Pandrea I, Estaquier J, Souquiere S, Rouquet P, Mavoungou VP, Bourry O, M'Boup S, Barre-Sinoussi F, Simon F, Apetrei C, Roques P, Müller-Trutwin MC. High levels of viral replication contrast with only transient changes in CD4+ and CD8+ cell numbers during the early phase of experimental infection with simian immunodeficiency virus SIVmnd-1 in Mandrillus sphinx. J Virol 2002, 76:10256-10263. 10.1128/JVI.76.20.10256-10263.2002, 136548, 12239301.
7. Onanga R, Souquiere S, Makuwa M, Mouinga-Ondeme A, Simon F, Apetrei C, Roques P. Primary simian immunodeficiency virus SIVmnd-2 infection in mandrills (Mandrillus sphinx). J Virol 2006, 80:3303-3309.
8. Pandrea I, Apetrei C, Dufour J, Dillon N, Barbercheck J, Metzger M, Jacquelin B, Bohm R, Marx PA, Barre-Sinoussi F, Hirsch VM, Müller-Trutwin MC, Lackner AA, Veazey RS. Simian immunodeficiency virus (SIV) SIVagm.sab infection of Caribbean African green monkeys: New model of the study of SIV pathogenesis in natural hosts. J Virol 2006, 80:4858-4867. 10.1128/JVI.80.10.4858-4867.2006, 1472068, 16641277.
9. Pandrea I, Kornfeld C, Ploquin MJ-I, Apetrei C, Faye A, Rouquet P, Roques P, Simon F, Barré-Sinoussi F, Müller-Trutwin MC, Diop OM. Impact of viral factors on very early in vivo replication profiles in SIVagm-infected African green monkeys. J Virol 2005, 79:6249-6259. 10.1128/JVI.79.10.6249-6259.2005, 1091729, 15858009.
10. Pandrea I, Onanga R, Kornfeld C, Rouquet P, Bourry O, Clifford S, Telfer PT, Abernethy K, White LT, Ngari P, Müller-Trutwin M, Roques P, Marx PA, Simon F, Apetrei C. High levels of SIVmnd-1 replication in chronically infected Mandrillus sphinx. Virology 2003, 317:119-127. 10.1016/j.virol.2003.08.015, 14675630.
11. Pandrea I, Onanga R, Souquiere S, Mouinga-Ondéme A, Bourry O, Makuwa M, Rouquet P, Silvestri G, Simon F, Roques P, Apetrei C. Paucity of CD4+CCR5+ T-cells may prevent breastfeeding transmission of SIV in natural non-human primate hosts. J Virol 2008, 82:5501-5509. 10.1128/JVI.02555-07, 2395173, 18385229.
12. Meythaler M, Martinot A, Wang Z, Pryputniewicz S, Kasheta M, Ling B, Marx PA, O'Neil S, Kaur A. Differential CD4+ T-lymphocyte apoptosis and bystander T-cell activation in rhesus macaques and sooty mangabeys during acute simian immunodeficiency virus infection. J Virol 2009, 83:572-583. 10.1128/JVI.01715-08, 2612394, 18987149.
13. Chakrabarti LA, Lewin SR, Zhang L, Gettie A, Luckay A, Martin LN, Skulsky E, Ho DD, Cheng-Mayer C, Marx PA. Normal T-cell turnover in sooty mangabeys harboring active simian immunodeficiency virus infection. J Virol 2000, 74:1209-1223. 10.1128/JVI.74.3.1209-1223.2000, 111455, 10627531.
14. Pandrea I, Gaufin T, Brenchley JM, Gautam R, Monjure C, Gautam A, Coleman C, Lackner AA, Ribeiro R, Douek DC, Apetrei C. Experimentally-induced immune activation in natural hosts of SIV induces significant increases in viral replication and CD4+ T cell depletion. J Immunol 2008, 181:6687-6691. 2695139, 18981083.
15. VandeWoude S, Apetrei C. Going wild: Lessons from T-lymphotropic naturally occurring lentiviruses. Clin Microbiol Rev 2006, 19:728-762. 10.1128/CMR.00009-06, 1592692, 17041142.
16. Gaufin T, Pattison M, Gautam R, Stoulig C, Dufour J, MacFarland J, Mandell D, Tatum C, Marx M, Ribeiro RM, Montefiori D, Apetrei C, Pandrea I. Effect of B cell depletion on viral replication and clinical outcome of SIV infection in a natural host. J Virol 2009, 83:10347-10357. 10.1128/JVI.00880-09, 2753117, 19656874.
17. Klein MR, van Baalen CA, Holwerda AM, Kerkhof SR, Bende RJ, Keet IP, Eeftinck-Schattenkerk JK, Osterhaus AD, Schuitemaker H, Miedema F. Kinetics of Gag-specific cytotoxic T lymphocyte responses during the clinical course of HIV-1 infection: a longitudinal analysis of rapid progressors and long-term asymptomatics. J Exp Med 1995, 181:1365-1372. 10.1084/jem.181.4.1365, 2191947, 7699324.
18. Rinaldo C, Huang XL, Fan ZF, Ding M, Beltz L, Logar A, Panicali D, Mazzara G, Liebmann J, Cottrill M, et al. High levels of anti-human immunodeficiency virus type 1 (HIV-1) memory cytotoxic T-lymphocyte activity and low viral load are associated with lack of disease in HIV-1-infected long-term nonprogressors. J Virol 1995, 69:5838-5842. 189455, 7637030.
19. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, Abraham J, Lederman MM, Benito JM, Goepfert PA, Connors M, Roederer M, Koup RA. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006, 107:4781-4789. 10.1182/blood-2005-12-4818, 1895811, 16467198.
20. Friedrich TC, Valentine LE, Yant LJ, Rakasz EG, Piaskowski SM, Furlott JR, Weisgrau KL, Burwitz B, May GE, Leon EJ, Soma T, Napoe G, Capuano SV, Wilson NA, Watkins DI. Subdominant CD8+ T-cell responses are involved in durable control of AIDS virus replication. J Virol 2007, 81:3465-3476. 10.1128/JVI.02392-06, 1866056, 17251286.
21. Loffredo JT, Maxwell J, Qi Y, Glidden CE, Borchardt GJ, Soma T, Bean AT, Beal DR, Wilson NA, Rehrauer WM, Lifson JD, Carrington M, Watkins DI. Mamu-B*08-positive Macaques Control Simian Immunodeficiency Virus Replication. J Virol 2007, 81:8827-8832. 10.1128/JVI.00895-07, 1951344, 17537848.
22. Yant LJ, Friedrich TC, Johnson RC, May GE, Maness NJ, Enz AM, Lifson JD, O'Connor DH, Carrington M, Watkins DI. The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 2006, 80:5074-5077. 10.1128/JVI.80.10.5074-5077.2006, 1472056, 16641299.
23. Veazey RS, Acierno PM, McEvers KJ, Baumeister SH, Foster GJ, Rett MD, Newberg MH, Kuroda MJ, Williams K, Kim EY, Wolinsky SM, Rieber EP, Piatak M, Lifson JD, Montefiori DC, Brown CR, Hirsch VM, Schmitz JE. Increased loss of CCR5+ CD45RA- CD4+ T cells in CD8+ lymphocyte-depleted Simian immunodeficiency virus-infected rhesus monkeys. J Virol 2008, 82:5618-5630. 10.1128/JVI.02748-07, 2395171, 18367534.
24. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, Racz P, Tenner-Racz K, Dalesandro M, Scallon BJ, Ghrayeb J, Forman MA, Montefiori DC, Rieber EP, Letvin NL, Reimann KA. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 1999, 283:857-860. 10.1126/science.283.5403.857, 9933172.
25. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, Blanchard J, Irwin CE, Safrit JT, Mittler J, Weinberger L, Kostrikis LG, Zhang L, Perelson AS, Ho DD. Dramatic rise in plasma viremia after CD8+ T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 1999, 189:991-998. 10.1084/jem.189.6.991, 2193038, 10075982.
26. Metzner KJ, Jin X, Lee FV, Gettie A, Bauer DE, Di Mascio M, Perelson AS, Marx PA, Ho DD, Kostrikis LG, Connor RI. Effects of in vivo CD8+ T cell depletion on virus replication in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J Exp Med 2000, 191:1921-1931. 10.1084/jem.191.11.1921, 2213531, 10839807.
27. Metzner KJ, Moretto WJ, Donahoe SM, Jin X, Gettie A, Montefiori DC, Marx PA, Binley JM, Nixon DF, Connor RI. Evaluation of CD8+ T-cell and antibody responses following transient increased viraemia in rhesus macaques infected with live, attenuated simian immunodeficiency virus. J Gen Virol 2005, 86:3375-3384. 10.1099/vir.0.81206-0, 16298985.
28. Willey RL, Byrum R, Piatak M, Kim YB, Cho MW, Rossio JL, Bess J, Igarashi T, Endo Y, Arthur LO, Lifson JD, Martin MA. Control of viremia and prevention of simian-human immunodeficiency virus-induced disease in rhesus macaques immunized with recombinant vaccinia viruses plus inactivated simian immunodeficiency virus and human immunodeficiency virus type 1 particles. J Virol 2003, 77:1163-1174. 10.1128/JVI.77.2.1163-1174.2003, 140830, 12502833.
29. Amara RR, Ibegbu C, Villinger F, Montefiori DC, Sharma S, Nigam P, Xu Y, McClure HM, Robinson HL. Studies using a viral challenge and CD8 T cell depletions on the roles of cellular and humoral immunity in the control of an SHIV-89.6P challenge in DNA/MVA-vaccinated macaques. Virology 2005, 343:246-255. 10.1016/j.virol.2005.08.027, 16185742.
30. Rasmussen RA, Hofmann-Lehmann R, Li PL, Vlasak J, Schmitz JE, Reimann KA, Kuroda MJ, Letvin NL, Montefiori DC, McClure HM, Ruprecht RM. Neutralizing antibodies as a potential secondary protective mechanism during chronic SHIV infection in CD8+ T-cell-depleted macaques. Aids 2002, 16:829-838. 10.1097/00002030-200204120-00002, 11919484.
31. Vaccari M, Mattapallil J, Song K, Tsai WP, Hryniewicz A, Venzon D, Zanetti M, Reimann KA, Roederer M, Franchini G. Reduced protection from simian immunodeficiency virus SIVmac251 infection afforded by memory CD8+ T cells induced by vaccination during CD4+ T-cell deficiency. J Virol 2008, 82:9629-9638. 10.1128/JVI.00893-08, 2546957, 18667509.
32. Genesca M, Skinner PJ, Hong JJ, Li J, Lu D, McChesney MB, Miller CJ. With minimal systemic T-cell expansion, CD8+ T Cells mediate protection of rhesus macaques immunized with attenuated simian-human immunodeficiency virus SHIV89.6 from vaginal challenge with simian immunodeficiency virus. J Virol 2008, 82:11181-11196. 10.1128/JVI.01433-08, 2573271, 18787003.
33. Malkevitch NV, Patterson LJ, Aldrich MK, Wu Y, Venzon D, Florese RH, Kalyanaraman VS, Pal R, Lee EM, Zhao J, Cristillo A, Robert-Guroff M. Durable protection of rhesus macaques immunized with a replicating adenovirus-SIV multigene prime/protein boost vaccine regimen against a second SIVmac251 rectal challenge: role of SIV-specific CD8+ T cell responses. Virology 2006, 353:83-98. 10.1016/j.virol.2006.05.012, 16814356.
34. Van Rompay KK, Singh RP, Pahar B, Sodora DL, Wingfield C, Lawson JR, Marthas ML, Bischofberger N. CD8+-cell-mediated suppression of virulent simian immunodeficiency virus during tenofovir treatment. J Virol 2004, 78:5324-5337. 10.1128/JVI.78.10.5324-5337.2004, 400346, 15113912.
35. Lifson JD, Rossio JL, Piatak M, Parks T, Li L, Kiser R, Coalter V, Fisher B, Flynn BM, Czajak S, Hirsch VM, Reimann KA, Schmitz JE, Ghrayeb J, Bischofberger N, Nowak MA, Desrosiers RC, Wodarz D. Role of CD8(+) lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J Virol 2001, 75:10187-10199. 10.1128/JVI.75.21.10187-10199.2001, 114593, 11581387.
36. Zahn RC, Rett MD, Korioth-Schmitz B, Sun Y, Buzby AP, Goldstein S, Brown CR, Byrum RA, Freeman GJ, Letvin NL, Hirsch VM, Schmitz JE. Simian Immunodeficiency Virus (SIV)-specific CD8+ T cell responses in chronically SIVagm-infected vervet African green monkeys. J Virol 2008, 82:11577-11588. 10.1128/JVI.01779-08, 2583661, 18829748.
37. Lozano Reina JM, Favre D, Kasakow Z, Mayau V, Nugeyre MT, Ka T, Faye A, Miller CJ, Scott-Algara D, McCune JM, Barré-Sinoussi F, Diop OM, Müller-Trutwin MC. Gag p27-specific B- and T-cell responses in Simian immunodeficiency virus SIVagm-infected African green monkeys. J Virol 2009, 83:2770-2777. 10.1128/JVI.01841-08, 2648264, 19109377.
38. Silvestri G, Fedanov A, Germon S, Kozyr N, Kaiser WJ, Garber DA, McClure H, Feinberg MB, Staprans SI. Divergent host responses during primary simian immunodeficiency virus SIVsm infection of natural sooty mangabey and nonnatural rhesus macaque hosts. J Virol 2005, 79:4043-4054. 10.1128/JVI.79.7.4043-4054.2005, 1061583, 15767406.
39. Dunham R, Pagliardini P, Gordon S, Sumpter B, Engram J, Moanna A, Lawson B, McClure HM, Xian-Xu H, Ibegbu C, Easley K, Katz N, Pandrea I, Apetrei C, Sodora DL, Staprans SI, Feinberg MB, Silvestri G. The AIDS-resistance of naturally SIV-infected sooty mangabeys is independent of cellular immunity to the virus. Blood 2006, 108:209-217. 10.1182/blood-2005-12-4897, 1895834, 16522814.
40. Wang Z, Metcalf B, Ribeiro RM, McClure H, Kaur A. Th-1-type cytotoxic CD8+ T-lymphocyte responses to simian immunodeficiency virus (SIV) are a consistent feature of natural SIV infection in sooty mangabeys. J Virol 2006, 80:2771-2783. 10.1128/JVI.80.6.2771-2783.2006, 1395440, 16501086.
41. Kaur A, Alexander L, Staprans SI, Denekamp L, Hale CL, McClure HM, Feinberg MB, Desrosiers RC, Johnson RP. Emergence of cytotoxic T lymphocyte escape mutations in nonpathogenic simian immunodeficiency virus infection. Eur J Immunol 2001, 31:3207-3217. 10.1002/1521-4141(200111)31:11<3207::AID-IMMU3207>3.0.CO;2-H, 11745337.
42. Kaur A, Yang J, Hempel D, Gritz L, Mazzara GP, McClure H, Johnson RP. Identification of multiple simian immunodeficiency virus (SIV)-specific CTL epitopes in sooty mangabeys with natural and experimentally acquired SIV infection. J Immunol 2000, 164:934-943.
43. Barry AP, Silvestri G, Safrit JT, Sumpter B, Kozyr N, McClure HM, Staprans SI, Feinberg MB. Depletion of CD8+ cells in sooty mangabey monkeys naturally infected with simian immunodeficiency virus reveals limited role for immune control of virus replication in a natural host species. J Immunol 2007, 178:8002-8012.
44. Schmitz JE, Zahn RC, Brown CR, Rett MD, Li M, Tang H, Pryputniewicz S, Byrum RA, Kaur A, Montefiori DC, Allan JS, Goldstein S, Hirsch VM. Inhibition of adaptive immune responses leads to a fatal clinical outcome in SIV-infected pigtailed macaques but not vervet African green monkeys. PLoS Pathog 2009, 5:e1000691. 10.1371/journal.ppat.1000691, 2785481, 20011508.
45. Zahn RC, Rett MD, Li M, Tang H, Korioth-Schmitz B, Balachandran H, White R, Pryputniewicz S, Letvin NL, Kaur A, Montefiori DC, Carville A, Hirsch VM, Allan JS, Schmitz JE. Suppression of adaptive immune responses during primary SIV infection of sabaeus African green monkeys delays partial containment of viremia but does not induce disease. Blood 2010, 115:3070-8. 10.1182/blood-2009-10-245225, 20147699.
46. Schmitz JE, Simon MA, Kuroda MJ, Lifton MA, Ollert MW, Vogel CW, Racz P, Tenner-Racz K, Scallon BJ, Dalesandro M, Ghrayeb J, Rieber EP, Sasseville VG, Reimann KA. A nonhuman primate model for the selective elimination of CD8+ lymphocytes using a mouse-human chimeric monoclonal antibody. Am J Pathol 1999, 154:1923-1932. 1866630, 10362819.
47. Matano T, Shibata R, Siemon C, Connors M, Lane HC, Martin MA. Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J Virol 1998, 72:164-169. 109361, 9420212.
48. Pandrea I, Onanga R, Rouquet P, Bourry O, Ngari P, Wickings EJ, Roques P, Apetrei C. Chronic SIV infection ultimately causes immunodeficiency in African non-human primates. AIDS 2001, 15:2461-2462. 10.1097/00002030-200112070-00019, 11826852.
49. Kuroda MJ, Schmitz JE, Charini WA, Nickerson CE, Lifton MA, Lord CI, Forman MA, Letvin NL. Emergence of CTL coincides with clearance of virus during primary simian immunodeficiency virus infection in rhesus monkeys. J Immunol 1999, 162:5127-5133.
50. Okoye A, Park H, Rohankhedkar M, Coyne-Johnson L, Lum R, Walker JM, Planer SL, Legasse AW, Sylwester AW, Piatak M, Lifson JD, Sodora DL, Villinger F, Axthelm MK, Schmitz JE, Picker LJ. Profound CD4+/CCR5+ T cell expansion is induced by CD8+ lymphocyte depletion but does not account for accelerated SIV pathogenesis. J Exp Med 2009, 206:1575-1588. 10.1084/jem.20090356, 2715089, 19546246.
51. Kaur A, Kassis N, Hale CL, Simon M, Elliott M, Gomez-Yafal A, Lifson JD, Desrosiers RC, Wang F, Barry P, Mach M, Johnson RP. Direct relationship between suppression of virus-specific immunity and emergence of cytomegalovirus disease in simian AIDS. J Virol 2003, 77:5749-5758. 10.1128/JVI.77.10.5749-5758.2003, 154043, 12719568.
52. Giavedoni LD, Velasquillo MC, Parodi LM, Hubbard GB, Hodara VL. Cytokine expression, natural killer cell activation, and phenotypic changes in lymphoid cells from rhesus macaques during acute infection with pathogenic simian immunodeficiency virus. J Virol 2000, 74:1648-1657. 10.1128/JVI.74.4.1648-1657.2000, 111639, 10644334.
53. Choi EI, Reimann KA, Letvin NL. In vivo natural killer cell depletion during primary SIV infection in rhesus monkeys. J Virol 2008, 82:6758-6761. 10.1128/JVI.02277-07, 2447079, 18434394.
54. Choi EI, Wang R, Peterson L, Letvin NL, Reimann KA. Use of an anti-CD16 antibody for in vivo depletion of natural killer cells in rhesus macaques. Immunology 2008, 124:215-222. 10.1111/j.1365-2567.2007.02757.x, 2566626, 18201184.
55. Oliva A, Kinter AL, Vaccarezza M, Rubbert A, Catanzaro A, Moir S, Monaco J, Ehler L, Mizell S, Jackson R, Li Y, Romano JW, Fauci AS. Natural killer cells from human immunodeficiency virus (HIV)-infected individuals are an important source of CC-chemokines and suppress HIV-1 entry and replication in vitro. J Clin Invest 1998, 102:223-231. 10.1172/JCI2323, 509084, 9649576.
56. National Research Council Guide for the care and use of laboratory animals. 1996, National Academy Press, Washington, DC, National Research Council.
57. Gaufin T, Gautam R, Kasheta M, Ribeiro RM, Ribka E, Barnes M, Pattison M, Tatum C, MacFarland J, Montefiori D, Kaur A, Pandrea I, Apetrei C. Limited ability of humoral immune responses in control of viremia during infection with SIVsmmD215 strain. Blood 2009, 113:4250-4261. 10.1182/blood-2008-09-177741, 2676085, 19168789.
58. Pandrea I, Ribeiro RM, Gautam R, Gaufin T, Pattison M, Barnes M, Monjure C, Stoulig C, Silvestri G, Miller M, Perelson AS, Apetrei C. Simian immunodeficiency virus SIVagm dynamics in African green monkeys. J Virol 2008, 82:3713-3724. 10.1128/JVI.02402-07, 2268485, 18216122.
59. Simon F, Souquiere S, Damond F, Kfutwah A, Makuwa M, Leroy E, Rouquet P, Berthier JL, Rigoulet J, Lecu A, Telfer PT, Pandrea I, Plantier JC, Barré-Sinoussi F, Roques P, Müller-Trutwin MC, Apetrei C. Synthetic peptide strategy for the detection of and discrimination among highly divergent primate lentiviruses. AIDS Res Hum Retroviruses 2001, 17:937-952. 10.1089/088922201750290050, 11461679.
60. Gautam R, Gaufin T, Butler I, Gautam A, Barnes M, Mandell D, Pattison M, Tatum C, Macfarland J, Monjure C, Marx PA, Pandrea I, Apetrei C. SIVrcm, a unique CCR2-tropic virus, selectively depletes memory CD4+ T cells in pigtailed macaques through rapid coreceptor expansion in vivo. J Virol 2009, 83:7894-7908. 10.1128/JVI.00444-09, 2715763, 19493994.