Vaccination with live attenuated simian immunodeficiency virus causes dynamic changes in intestinal CD4+CCR5+ T cells

Retrovirology

Volumn 8, Issue , 2011, Pages

  Li, Bo ^a   Berry, Neil ^a   Ham, Claire ^a   Ferguson, Deborah ^a   Smith, Deborah ^a   Hall, Joanna ^a   Page, Mark ^a   Quartey Papafio, Ruby ^a   Elsley, William ^a   Robinson, Mark ^a   Almond, Neil ^a   Stebbings, Richard ^a  

^a PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; LIVE VACCINE; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CCR5+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL LOSS; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; LYMPH NODE CELL; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN EXPRESSION; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; UPREGULATION; VACCINATION; VIRUS LOAD; VIRUS REPLICATION;

SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 79551532807     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-8-8     Document Type: Article

References (82)

1. Desrosiers RC, Wyand MS, Kodama T, Ringler DJ, Arthur LO, Sehgal PK, Letvin NL, King NW, Daniel MD. Vaccine protection against simian immunodeficiency virus infection. Proc Natl Acad Sci USA 1989, 86:6353-6357. 10.1073/pnas.86.16.6353, 297837, 2548210.
2. Hu SL, Zarling JM, Chinn J, Travis BM, Moran PA, Sias J, Kuller L, Morton WR, Heidecker G, Benveniste RE. Protection of macaques against simian AIDS by immunization with a recombinant vaccinia virus expressing the envelope glycoproteins of simian type D retrovirus. Proc Natl Acad Sci USA 1989, 86:7213-7217. 10.1073/pnas.86.18.7213, 298027, 2550935.
3. Stott EJ, Almond N, Kent K, Walker B, Hull R, Rose J, Silvera P, Sangster R, Corcoran T, Lines J, Silvera K, Luciw P, Murphy-Corb M, Momin P, Bruck C. Evaluation of a candidate human immunodeficiency virus type 1 (HIV-1) vaccine in macaques: effect of vaccination with HIV-1 gp120 on subsequent challenge with heterologous simian immunodeficiency virus-HIV-1 chimeric virus. J Gen Virol 1998, 79:423-432.
4. Hanke T, Samuel RV, Blanchard TJ, Neumann VC, Allen TM, Boyson JE, Sharpe SA, Cook N, Smith GL, Watkins DI, Cranage MP, McMichael AJ. Effective induction of simian immunodeficiency virus-specific cytotoxic T lymphocytes in macaques by using a multiepitope gene and DNA prime-modified vaccinia virus Ankara boost vaccination regimen. J Virol 1999, 73:7524-7532. 104279, 10438842.
5. Berry N, Stebbings R, Brown S, Christian P, Thorstensson R, Ahmed RK, Davis L, Ferguson D, D'Arcy N, Elsley W, Hull R, Lines J, Wade-Evans A, Stott J, Almond N. Immunological responses and viral modulatory effects of vaccination with recombinant modified vaccinia virus Ankara (rMVA) expressing structural and regulatory transgenes of simian immunodeficiency virus (SIVmac32H/J5M). J Med Primatol 2007, 36:80-94. 10.1111/j.1600-0684.2007.00216.x, 17493138.
6. Barnett SW, Burke B, Sun Y, Kan E, Legg H, Lian Y, Bost K, Zhou F, Goodsell A, Zur Megede J, Polo J, Donnelly J, Ulmer J, Otten GR, Miller CJ, Vajdy M, Srivastava IK. Antibody-mediated protection against mucosal simian-human immunodeficiency virus challenge of macaques immunized with alphavirus replicon particles and boosted with trimeric envelope glycoprotein in MF59 adjuvant. J Virol 2010, 84:5975-5985. 10.1128/JVI.02533-09, 2876657, 20392857.
7. Daniel MD, Kirchhoff F, Czajak SC, Sehgal PK, Desrosiers RC. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science 1992, 258:1938-1941. 10.1126/science.1470917, 1470917.
8. Almond N, Kent K, Cranage M, Rud E, Clarke B, Stott EJ. Protection by attenuated simian immunodeficiency virus in macaques against challenge with virus-infected cells. Lancet 1995, 345:1342-1344. 10.1016/S0140-6736(95)92540-6, 7752758.
9. Bogers WM, Niphuis H, Ten Haaft P, Laman JD, Koornstra W, Heeney JL. Protection from HIV-1 envelope-bearing chimeric simian immunodeficiency virus (SHIV) in rhesus macaques infected with attenuated SIV: consequences of challenge. AIDS 1995, 9:F13-F18.
10. Dunn CS, Hurtrel B, Beyer C, Gloeckler L, Ledger TN, Moog C, Kieny MP, Mehtali M, Schmitt D, Gut JP, Kirn A, Aubertin AM. Pathogenicity of live, attenuated SIV after mucosal infection of neonatal macaques.
11. Shibata R, Siemon C, Czajak SC, Desrosiers RC, Martin MA. Live, attenuated simian immunodeficiency virus vaccines elicit potent resistance against a challenge with a human immunodeficiency virus type 1 chimeric virus. J Virol 1997, 71:8141-8148. 192270, 9343164.
12. Nilsson C, Mäkitalo B, Thorstensson R, Norley S, Binninger-Schinzel D, Cranage M, Rud E, Biberfeld G, Putkonen P. Live attenuated simian immunodeficiency virus (SIV)mac in macaques can induce protection against mucosal infection with SIVsm. AIDS 1998, 12:2261-2270. 10.1097/00002030-199817000-00006, 9863867.
13. Wyand MS, Manson K, Montefiori DC, Lifson JD, Johnson RP, Desrosiers RC. Protection by live, attenuated simian immunodeficiency virus against heterologous challenge. J Virol 1999, 73:8356-8363. 112853, 10482586.
14. Kumar A, Mukherjee S, Shen J, Buch S, Li Z, Adany I, Liu Z, Zhuge W, Piatak M, Lifson J, McClure H, Narayan O. Immunization of macaques with live simian human immunodeficiency virus (SHIV) vaccines conferred protection against AIDS induced by homologous and heterologous SHIVs and simian immunodeficiency virus. Virology 2002, 301:189-205. 10.1006/viro.2002.1544, 12359422.
15. Reynolds MR, Weiler AM, Weisgrau KL, Piaskowski SM, Furlott JR, Weinfurter JT, Kaizu M, Soma T, León EJ, MacNair C, Leaman DP, Zwick MB, Gostick E, Musani SK, Price DA, Friedrich TC, Rakasz EG, Wilson NA, McDermott AB, Boyle R, Allison DB, Burton DR, Koff WC, Watkins DI. Macaques vaccinated with live-attenuated SIV control replication of heterologous virus. J Exp Med 2008, 205:2537-2550. 10.1084/jem.20081524, 2571929, 18838548.
16. Baba TW, Jeong YS, Pennick D, Bronson R, Greene MF, Ruprecht RM. Pathogenicity of live, attenuated SIV after mucosal infection of neonatal macaques. Science 1995, 267:1820-1825. 10.1126/science.7892606, 7892606.
17. Whatmore AM, Cook N, Hall GA, Sharpe S, Rud EW, Cranage MP. Repair and evolution of nef in vivo modulates simian immunodeficiency virus virulence. J Virol 1995, 69:5117-5123. 189330, 7609080.
18. Learmont JC, Geczy AF, Mills J, Ashton LJ, Raynes-Greenow CH, Garsia RJ, Dyer WB, McIntyre L, Oelrichs RB, Rhodes DI, Deacon NJ, Sullivan JS. Immunologic and virologic status after 14 to 18 years of infection with an attenuated strain of HIV-1. A report from the Sydney Blood Bank Cohort. N Engl J Med 1999, 340:1715-1722. 10.1056/NEJM199906033402203, 10352163.
19. Sawai ET, Hamza MS, Ye M, Shaw KE, Luciw PA. Pathogenic conversion of live attenuated simian immunodeficiency virus vaccines is associated with expression of truncated Nef. J Virol 2000, 74:2038-2045. 10.1128/JVI.74.4.2038-2045.2000, 111683, 10644378.
20. Hofmann-Lehmann R, Vlasak J, Williams AL, Chenine AL, McClure HM, Anderson DC, O'Neil S, Ruprecht RM. Live attenuated, nef-deleted SIV is pathogenic in most adult macaques after prolonged observation. AIDS 2003, 17:157-166. 10.1097/00002030-200301240-00004, 12545074.
21. Friedrich TC, Watkins DI. Wanted: correlates of vaccine-induced protection against simian immunodeficiency virus. Curr Opin HIV AIDS 2008, 3:393-398. 10.1097/COH.0b013e3282faa461, 19372996.
22. Stahl-Hennig C, Dittmer U, Nisslein T, Pekrun K, Petry H, Jurkiewicz E, Fuchs D, Wachter H, Rud EW, Hunsmann G. Attenuated SIV imparts immunity to challenge with pathogenic spleen-derived SIV but cannot prevent repair of the nef deletion. Immunol Lett 1996, 51:129-135. 10.1016/0165-2478(96)02567-9, 8811357.
23. Wyand MS, Manson KH, Garcia-Moll M, Montefiori D, Desrosiers RC. Vaccine protection by a triple deletion mutant of simian immunodeficiency virus. J Virol 1996, 70:3724-3733. 190248, 8648707.
24. Almond N, Rose J, Sangster R, Silvera P, Stebbings R, Walker B, Stott EJ. Mechanisms of protection induced by attenuated simian immunodeficiency virus. I. Protection cannot be transferred with immune serum. J Gen Virol 1997, 78:1919-1922.
25. Connor RI, Montefiori DC, Binley JM, Moore JP, Bonhoeffer S, Gettie A, Fenamore EA, Sheridan KE, Ho DD, Dailey PJ, Marx PA. Temporal analyses of virus replication, immune responses, and efficacy in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J Virol 1998, 72:7501-7509. 109989, 9696847.
26. Langlois AJ, Desrosiers RC, Lewis MG, KewalRamani VN, Littman DR, Zhou JY, Manson K, Wyand MS, Bolognesi DP, Montefiori DC. Neutralizing antibodies in sera from macaques immunized with attenuated simian immunodeficiency virus. J Virol 1998, 72:6950-6955. 109912, 9658152.
27. Nixon DF, Donahoe SM, Kakimoto WM, Samuel RV, Metzner KJ, Gettie A, Hanke T, Marx PA, Connor RI. Simian immunodeficiency virus-specific cytotoxic T lymphocytes and protection against challenge in rhesus macaques immunized with a live attenuated simian immunodeficiency virus vaccine. Virology 2000, 266:203-210. 10.1006/viro.1999.0078, 10612675.
28. Johnson RP. Mechanisms of protection against simian immunodeficiency virus infection. Vaccine 2002, 20:1985-1987. 10.1016/S0264-410X(02)00083-X, 11983259.
29. Almond NM, Stott EJ, Berry N, Wade-Evans AM, Hull R, Lines J, Silvera P, Sangster R, Corcoran T, Rose J, Walker KB. Mechanisms of protection induced by attenuated simian immunodeficiency virus. Virology 2002, 296:338-353. 10.1006/viro.2002.1379, 12069532.
30. Abel K, Compton L, Rourke T, Montefiori D, Lu D, Rothaeusler K, Fritts L, Bost K, Miller CJ. Simian-human immunodeficiency virus SHIV89.6-induced protection against intravaginal challenge with pathogenic SIVmac239 is independent of the route of immunization and is associated with a combination of cytotoxic T-lymphocyte and alpha interferon responses. J Virol 2003, 77:3099-3118. 10.1128/JVI.77.5.3099-3118.2003, 149756, 12584336.
31. Sharpe SA, Cope A, Dowall S, Berry N, Ham C, Heeney JL, Hopkins D, Easterbrook L, Dennis M, Almond N, Cranage M. Macaques infected long-term with attenuated simian immunodeficiency virus (SIVmac) remain resistant to wild-type challenge, despite declining cytotoxic T lymphocyte responses to an immunodominant epitope. J Gen Virol 2004, 85:2591-2602. 10.1099/vir.0.80050-0, 15302953.
32. Tenner-Racz K, Stahl Hennig C, Uberla K, Stoiber H, Ignatius R, Heeney J, Steinman RM, Racz P. Early protection against pathogenic virus infection at a mucosal challenge site after vaccination with attenuated simian immunodeficiency virus. Proc Natl Acad Sci USA 2004, 101:3017-3022. 10.1073/pnas.0308677101, 365737, 14970317.
33. Schmitz JE, Johnson RP, McClure HM, Manson KH, Wyand MS, Kuroda MJ, Lifton MA, Khunkhun RS, McEvers KJ, Gillis J, Piatak M, Lifson JD, Grosschupff G, Racz P, Tenner-Racz K, Rieber EP, Kuus-Reichel K, Gelman RS, Letvin NL, Montefiori DC, Ruprecht RM, Desrosiers RC, Reimann KA. Effect of CD8+ lymphocyte depletion on virus containment after simian immunodeficiency virus SIVmac251 challenge of live attenuated SIVmac239delta3-vaccinated rhesus macaques. J Virol 2005, 79:8131-8141. 10.1128/JVI.79.13.8131-8141.2005, 1143721, 15956558.
34. Stebbings R, Berry N, Waldmann H, Bird P, Hale G, Stott J, North D, Hull R, Hall J, Lines J, Brown S, D'Arcy N, Davis L, Elsley W, Edwards C, Ferguson D, Allen J, Almond N. CD8+ lymphocytes do not mediate protection against acute superinfection 20 days after vaccination with a live attenuated simian immunodeficiency virus. J Virol 2005, 79:12264-122672. 10.1128/JVI.79.19.12264-12272.2005, 1211523, 16160152.
35. Gauduin MC, Yu Y, Barabasz A, Carville A, Piatak M, Lifson JD, Desrosiers RC, Johnson RP. Induction of a virus-specific effector-memory CD4+ T cell response by attenuated SIV infection. J Exp Med 2006, 203:2661-2672. 10.1084/jem.20060134, 2118155, 17116733.
36. Goletti D, Macchia I, Leone P, Pace M, Sernicola L, Pavone-Cossut MR, Maggiorella MT, Cafaro A, Ensoli B, Titti F. Innate anti-viral immunity is associated with the protection elicited by the simian immunodeficiency virus (SIV) live attenuated virus vaccine in cynomolgus monkeys. Med Sci Monit 2006, 12:BR330-BR340.
37. Berry N, Stebbings R, Ferguson D, Ham C, Alden J, Brown S, Jenkins A, Lines J, Duffy L, Davis L, Elsley W, Page M, Hull R, Stott J, Almond N. Resistance to superinfection by a vigorously replicating, uncloned stock of simian immunodeficiency virus (SIVmac251) stimulates replication of a live attenuated virus vaccine (SIVmacC8). J Gen Virol 2008, 89:2240-2251. 10.1099/vir.0.2008/001693-0, 18753233.
38. Salha MD, Cheynier R, Halwani R, McGrath H, Langaee TY, Yassine Diab B, Fournier J, Parenteau M, Edgar J, Ko D, Sherring A, Bogdanovic D, Sekaly RP, Rud EW. Persistence of restricted CD4 T cell expansions in SIV-infected macaques resistant to SHIV89.6P superinfection. Virology 2008, 377:239-247. 10.1016/j.virol.2008.04.031, 18570962.
39. Mansfield K, Lang SM, Gauduin MC, Sanford HB, Lifson JD, Johnson RP, Desrosiers RC. Vaccine protection by live, attenuated simian immunodeficiency virus in the absence of high-titer antibody responses and high-frequency cellular immune responses measurable in the periphery. J Virol 2008, 82:4135-4148. 10.1128/JVI.00015-08, 2292994, 18272584.
40. Johnson RP, Lifson JD, Czajak SC, Cole KS, Manson KH, Glickman R, Yang J, Montefiori DC, Montelaro R, Wyand MS, Desrosiers RC. Highly attenuated vaccine strains of simian immunodeficiency virus protect against vaginal challenge: inverse relationship of degree of protection with level of attenuation. J Virol 1999, 73:4952-4961. 112539, 10233957.
41. van der Kuyl AC, Kozaczynska K, Arien KK, Gali Y, Balazs VR, Dekker SJ, Zorgdrager F, Vanham G, Berkhout B, Cornelissen M. Analysis of infectious virus clones from two HIV-1 superinfection cases suggests that the primary strains have lower fitness. Retrovirology 2010, 7:60-74. 10.1186/1742-4690-7-60, 2918528, 20646276.
42. Denesvre C, Le Grand R, Boissin-Cans F, Chakrabarti L, Hurtrel B, Vaslin B, Dormont D, Sonigo P. Highly attenuated SIVmac142 is immunogenic but does not protect against SIVmac251 challenge. AIDS Res Hum Retroviruses 1995, 11:1397-1406. 10.1089/aid.1995.11.1397, 8573398.
43. Berry N, Stott J, Hull R, Walker B, Lines J, Elsley W, Brown S, Wade-Evans A, Davis G, Cowie J, Sethi M, Almond N. Vaccination with live attenuated simian immunodeficiency virus for 21 days protects against superinfection. Virology 2004, 330:249-260. 10.1016/j.virol.2004.09.026, 15527850.
44. Guy-Grand D, Vassalli P. Gut intraepithelial T lymphocytes. Curr Opin Immunol 1993, 5:247-252. 10.1016/0952-7915(93)90012-H, 8507401.
45. Viney JL. The anatomical basis of intestinal immunity. Immunol Rev 1997, 156:145-66. 10.1111/j.1600-065X.1997.tb00966.x, 9176706.
46. Smit-McBride Z, Mattapallil JJ, McChesney M, Ferrick D, Dandekar S. Gastrointestinal T lymphocytes retain high potential for cytokine responses but have severe CD4(+) T-cell depletion at all stages of simian immunodeficiency virus infection compared to peripheral lymphocytes. J Virol 1998, 72:6646-6656. 109855, 9658111.
47. Ganusov VV, De Boer RJ. Do most lymphocytes in humans really reside in the gut?. Trends Immunol 2007, 28:514-518. 10.1016/j.it.2007.08.009, 17964854.
48. Veazey RS, Lackner AA. The gastrointestinal tract and the pathogenesis of AIDS. AIDS 1998, 12(Suppl A)):S35-S42.
49. Agace WW, Roberts AI, Wu L, Greineder C, Ebert EC, Parker CM. Human intestinal lamina propria and intraepithelial lymphocytes express receptors specific for chemokines induced by inflammation. Eur J Immunol 2000, 30:819-826. 10.1002/1521-4141(200003)30:3<819::AID-IMMU819>3.0.CO;2-Y, 10741397.
50. Anton PA, Elliott J, Poles MA, McGowan IM, Matud J, Hultin LE, Grovit-Ferbas K, Mackay CR, Chen ISY, Giorgi JV. Enhanced levels of functional HIV-1 co-receptors on human mucosal T cells demonstrated using intestinal biopsy tissue. AIDS 2000, 14:1761-1765. 10.1097/00002030-200008180-00011, 10985313.
51. Chen Z, Gettie A, Ho DD, Marx PA. Primary SIVsm isolates use the CCR5 coreceptor from sooty mangabeys naturally infected in west Africa: a comparison of coreceptor usage of primary SIVsm, HIV-2, and SIVmac. Virology 1998, 246:113-124. 10.1006/viro.1998.9174, 9656999.
52. Zhang Y, Lou B, Lal RB, Gettie A, Marx PA, Moore JP. Use of inhibitors to evaluate coreceptor usage by simian and simian/human immunodeficiency viruses and human immunodeficiency virus type 2 in primary cells. J Virol 2000, 74:6893-68910. 10.1128/JVI.74.15.6893-6910.2000, 112207, 10888629.
53. Moore JP, Kitchen SG, Pugach P, Zack JA. The CCR5 and CXCR4 coreceptors--central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection. AIDS Res Hum Retroviruses 2004, 20:111-126. 10.1089/088922204322749567, 15000703.
54. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, Nguyen PL, Khoruts A, Larson M, Haase AT, Douek DC. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004, 200:749-759. 10.1084/jem.20040874, 2211962, 15365096.
55. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, Hogan C, Boden D, Racz P, Markowitz M. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 2004, 200:761-770. 10.1084/jem.20041196, 2211967, 15365095.
56. Li Q, Duan L, Estes JD, Ma ZM, Rourke T, Wang Y, Reilly C, Carlis J, Miller CJ, Haase AT. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 2005, 434:1148-1152.
57. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005, 434:1093-1099. 10.1038/nature03501, 15793563.
58. Reeves RK, Gillis J, Wong FE, Johnson RP. Vaccination with SIVmac239Deltanef activates CD4+ T cells in the absence of CD4 T-cell loss. J Med Primatol 2009, 38(Suppl 1):8-16. 10.1111/j.1600-0684.2009.00370.x, 2810497, 19863673.
59. Picker LJ, Reed-Inderbitzin EF, Hagen SI, Edgar JB, Hansen SG, Legasse A, Planer S, Piatak M, Lifson JD, Maino VC, Axthelm MK, Villinger F. IL-15 induces CD4 effector memory T cell production and tissue emigration in nonhuman primates. J Clin Invest 2006, 116:1514-1524. 10.1172/JCI27564, 1459071, 16691294.
60. 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.
61. Rud EW, Cranage M, Yon J, Quirk J, Ogilvie L, Cook N, Webster S, Dennis M, Clarke BE. Molecular and biological characterization of simian immunodeficiency virus macaque strain 32 H proviral clones containing nef size variants. J Gen Virol 1994, 75(Pt 3):529-543. 10.1099/0022-1317-75-3-529, 8126450.
62. Stebbings R, Stott J, Almond N, Hull R, Lines J, Silvera P, Sangster R, Corcoran T, Rose J, Cobbold S, Gotch F, McMichael A, Walker B. Mechanisms of protection induced by attenuated simian immunodeficiency virus. II. Lymphocyte depletion does not abrogate protection. AIDS Res Hum Retroviruses 1998, 14:1187-1198. 10.1089/aid.1998.14.1187, 9737590.
63. Qin S, Rottman JB, Myers P, Kassam N, Weinblatt M, Loetscher M, Koch AE, Moser B, Mackay CR. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J Clin Invest 1998, 101:746-754. 10.1172/JCI1422, 508621, 9466968.
64. Balashov KE, Rottman JB, Weiner HL, Hancock WW. CCR5 (+) and CXCR3 (+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc Natl Acad Sci USA 1999, 96:6873-6878. 10.1073/pnas.96.12.6873, 22009, 10359806.
65. Ebert LM, McColl SR. Up-regulation of CCR5 and CCR6 on distinct subpopulations of antigen-activated CD4+ T lymphocytes. J Immunol 2002, 168:65-72.
66. Loetscher P, Uguccioni M, Bordoli L, Baggiolini M, Moser B, Chizzolini C, Dayer JM. CCR5 is characteristic of Th1 lymphocytes. Nature 1998, 391:344-345. 10.1038/34814, 9450746.
67. Olsson J, Poles M, Spetz AL, Elliott J, Hultin L, Giorgi J, Andersson J, Anton P. Human immunodeficiency virus type 1 infection is associated with significant mucosal inflammation characterized by increased expression of CCR5, CXCR4, and beta-chemokines. J Infect Dis 2000, 182:1625-1635. 10.1086/317625, 11069233.
68. Oki M, Ohtani H, Kinouchi Y, Sato E, Nakamura S, Matsumoto T, Nagura H, Yoshie O, Shimosegawa T. Accumulation of CCR5+ T cells around RANTES+ granulomas in Crohn's disease: a pivotal site of Th1-shifted immune response?. Lab Invest 2005, 85:137-145.
69. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004, 22:745-763. 10.1146/annurev.immunol.22.012703.104702, 15032595.
70. Clarke S, Almond N, Berry N. Simian immunodeficiency virus Nef gene regulates the production of 2-LTR circles in vivo. Virology 2003, 306:100-108. 10.1016/S0042-6822(02)00043-0, 12620802.
71. Ling B, Veazey RS, Hart M, Lackner AA, Kuroda M, Pahar B, Marx PA. Early restoration of mucosal CD4 memory CCR5 T cells in the gut of SIV-infected rhesus predicts long term non-progression. AIDS 2007, 21:2377-2385. 10.1097/QAD.0b013e3282f08b32, 18025874.
72. Monceaux V, Viollet L, Petit F, Cumont MC, Kaufmann GR, Aubertin AM, Hurtrel B, Silvestri G, Estaquier J. CD4+ CCR5+ T-cell dynamics during simian immunodeficiency virus infection of Chinese rhesus macaques. J Virol 2007, 81:13865-13875. 10.1128/JVI.00452-07, 2168866, 17898067.
73. 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.
74. 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.
75. 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.
76. 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.
77. Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999, 401:708-712. 10.1038/44385, 10537110.
78. Amyes E, McMichael AJ, Callan MF. Human CD4+ T cells are predominantly distributed among six phenotypically and functionally distinct subsets. J Immunol 2005, 175:5765-5773.
79. Nethe M, Berkhout B and VDKA. Retroviral superinfection resistance. Retrovirology 2005, 2:52-64. 10.1186/1742-4690-2-52, 1224871, 16107223.
80. 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.
81. Picker LJ, Hagen SI, Lum R, Reed-Inderbitzin EF, Daly LM, Sylwester AW, Walker JM, Siess DC, Piatak M, Wang JC, Allison DB, Maino VC, Lifson JD, Kodama T, Axthelm MK. Insufficient production and tissue delivery of CD4+ memory T cells in rapidly progressive simian immunodeficiency virus infection. J Exp Med 2004, 200:1299-1314. 10.1084/jem.20041049, 2211921, 15545355.
82. Ferguson D, Wade-Evans A, Elsley W, Sangster R, Silvera P, MacManus S, Davis G, Corcoran T, Berry N, Brown S, Jenkins A, Cowie J, Sethi M, Hull R, Stebbings R, Lines J, Norley S, Stott EJ, Almond N. Preparation and characterization of new challenge stocks of SIVmac32 H J5 following rapid serial passage of virus in vivo. J Med Primatol 2007, 36:131-142. 10.1111/j.1600-0684.2007.00224.x, 17517087.