Mechanism of protection of live attenuated simian immunodeficiency virus: Coevolution of viral and immune responses

AIDS

Volumn 24, Issue 5, 2010, Pages 637-648

  Cohen, George B ^a  

^a NONE

Author keywords

Attenuated simian immunodeficiency virus; Evolution; Mechanism; Vaccine

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; LIVE VACCINE; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; SIVMAC239 VACCINE; SIVMAC251 VACCINE; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ATTENUATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL PROTOCOL; CYTOTOXIC T LYMPHOCYTE; DISEASE CONTROL; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; GENE MUTATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNITY; IMMUNIZATION; LOW DRUG DOSE; MONKEY DISEASE; NONHUMAN; NOTE; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS LOAD; VIRUS RECOMBINATION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION; WILD TYPE;

AIDS VACCINES; ANIMALS; ANTIBODIES, VIRAL; IMMUNE EVASION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, CYTOTOXIC; VACCINES, ATTENUATED;

EID: 77949351286     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e328337795a     Document Type: Note

References (145)

1. 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.
2. Koff WC, Johnson PR, Watkins DI, Burton DR, Lifson JD, Hasenkrug KJ, et al. HIV vaccine design: insights from live attenuated SIV vaccines. Nat Immunol 2006; 7:19-23.
3. 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.
4. Baba TW, Liska V, Khimani AH, Ray NB, Dailey PJ, Penninck D, et al. Live attenuated, multiply deleted simian immunodeficiency virus causes AIDS in infant and adult macaques. Nat Med 1999; 5:194-203.
5. Whitney JB, Ruprecht RM. Live attenuated HIV vaccines: pitfalls and prospects. Curr Opin Infect Dis 2004; 17:17-26.
6. 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.
7. Alexander L, Illyinskii PO, Lang SM, Means RE, Lifson J, Mansfield K, Desrosiers RC. Determinants of increased repli-cative capacity of serially passaged simian immunodeficiency virus with nef deleted in rhesus monkeys. J Virol 2003; 77:6823-6835.
8. Munch J, Stolte N, Fuchs D, Stahl-Hennig C, Kirchhoff F. Efficient class I major histocompatibility complex down-regulation by simian immunodeficiency virus Nef is associated with a strong selective advantage in infected rhesus macaques. J Virol 2001; 75:10532-10536.
9. Churchill MJ, Rhodes DI, Learmont JC, Sullivan JS, Wesselingh SL, Cooke IR, et al. Longitudinal analysis of human immunodeficiency virus type 1 nef/long terminal repeat sequences in a cohort of long-term survivors infected from a single source. J Virol 2006; 80:1047-1052.
10. Kirchhoff F, Kestler HW 3rd, Desrosiers RC. Upstream U3 sequences in simian immunodeficiency virus are selectively deleted in vivo in the absence of an intact nef gene. J Virol 1994; 68:2031-2037.
11. 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.
12. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, et al. Control of viremia in simian immunodeficiency virus infection by CD8R lymphocytes. Science 1999; 283:857-860.
13. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, Blanchard J, et al. Dramatic rise in plasma viremia after CD8(R) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 1999; 189:991-998.
14. Goulder PJ, Watkins DI. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat Rev Immunol 2008; 8:619-630.
15. Veazey RS, Acierno PM, McEvers KJ, Baumeister SH, Foster GJ, Rett MD, et al. Increased loss of CCR5R CD45RAS CD4R T cells in CD8R lymphocyte-depleted Simian immunodeficiency virus-infected rhesus monkeys. J Virol 2008; 82:5618-5630.
16. Metzner KJ, Jin X, Lee FV, Gettie A, Bauer DE, Di Mascio M, et al. Effects of in vivo CD8(R) 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.
17. Schmitz JE, Johnson RP, McClure HM, Manson KH, Wyand MS, Kuroda MJ, et al. Effect of CD8R lymphocyte depletion on virus containment after simian immunodeficiency virus SIVmac251 challenge of live attenuated SIVmac239delta3-vaccinated rhesus macaques. J Virol 2005; 79:8131-8141.
18. Forthal DN, Landucci G, Daar ES. Antibody from patients with acute human immunodeficiency virus (HIV) infection inhibits primary strains of HIV type 1 in the presence of natural-killer effector cells. J Virol 2001; 75:6953-6961.
19. Schmitz JE, Kuroda MJ, Santra S, Simon MA, Lifton MA, Lin W, et al. Effect of humoral immune responses on controlling viremia during primary infection of rhesus monkeys with simian immunodeficiency virus. J Virol 2003; 77:2165-2173.
20. Metzner KJ, Moretto WJ, Donahoe SM, Jin X, Gettie A, Montefiori DC, et al. Evaluation of CD8R 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.
21. Miller CJ, Genesca M, Abel K, Montefiori D, Forthal D, Bost K, et al. Antiviral antibodies are necessary for control of simian immunodeficiency virus replication. J Virol 2007; 81:5024-5035.
22. Huber M, Trkola A. Humoral immunity to HIV-1: neutralization and beyond. J Intern Med 2007; 262:5-25.
23. Friedrich TC, Watkins DI. Wanted: correlates of vaccine-induced protection against simian immunodeficiency virus. Curr Opin HIV AIDS 2008; 3:393-398.
24. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL, et al. Gastrointestinal tract as a major site of CD4R T cell depletion and viral replication in SIV infection. Science 1998; 280:427-431.
25. Cromwell MA, Veazey RS, Altman JD, Mansfield KG, Glickman R, Allen TM, et al. Induction of mucosal homing virus-specific CD8(R) T lymphocytes by attenuated simian immunodeficiency virus. J Virol 2000; 74:8762-8766.
26. Veazey RS, Gauduin MC, Mansfield KG, Tham IC, Altman JD, Lifson JD, et al. Emergence and kinetics of simian immunodeficiency virus-specific CD8(R) T cells in the intestines of macaques during primary infection. J Virol 2001; 75:10515-10519.
27. Genesca M, McChesney MB, Miller CJ. Antiviral CD8R T cells in the genital tract control viral replication and delay progression to AIDS after vaginal SIV challenge in rhesus macaques immunized with virulence attenuated SHIV 89.6. J Intern Med 2009; 265:67-77.
28. Gauduin MC, Yu Y, Barabasz A, Carville A, Piatak M, Lifson JD, et al. Induction of a virus-specific effector-memory CD4R T cell response by attenuated SIV infection. J Exp Med 2006; 203:2661-2672.
29. Okoye A, Meier-Schellersheim M, Brenchley JM, Hagen SI, Walker JM, Rohankhedkar M, et al. Progressive CD4R central memory T cell decline results in CD4R effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med 2007; 204:2171-2185.
30. Rollman E, Smith MZ, Brooks AG, Purcell DF, Zuber B, Ramshaw IA, Kent SJ. Killing kinetics of simian immunodeficiency virus-specific CD8R T cells: implications for HIV vaccine strategies. J Immunol 2007; 179:4571-4579.
31. Franchini G. Choosing the right memory T cell for HIV. Nat Med 2009; 15:244-246.
32. Hansen SG, Vieville C, Whizin N, Coyne-Johnson L, Siess DC, Drummond DD, et al. Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat Med 2009; 15:293-299.
33. Genesca M, Skinner PJ, Hong JJ, Li J, Lu D, McChesney MB, Miller CJ. With minimal systemic T-cell expansion, CD8R 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.
34. Connor RI, Montefiori DC, Binley JM, Moore JP, Bonhoeffer S, Gettie A, et al. 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.
35. Abdel-Motal UM, Gillis J, Manson K, Wyand M, Montefiori D, Stefano-Cole K, et al. Kinetics of expansion of SIV Gag-specific CD8R T lymphocytes following challenge of vaccinated macaques. Virology 2005; 333:226-238.
36. Wyand MS, Manson KH, Garcia-Moll M, Montefiori D, Des-rosiers RC. Vaccine protection by a triple deletion mutant of simian immunodeficiency virus. J Virol 1996; 70:3724-3733.
37. Stebbings R, Berry N, Stott J, Hull R, Walker B, Lines J, et al. Vaccination with live attenuated simian immunodeficiency virus for 21 days protects against superinfection. Virology 2004; 330:249-260.
38. Berry N, Stebbings R, Ferguson D, Ham C, Alden J, Brown S, et al. Resistance to superinfection by a vigorously replicating, uncloned stock of simian immunodeficiency virus (SIV-mac251) stimulates replication of a live attenuated virus vaccine (SIVmacC8). J Gen Virol 2008; 89:2240-2251.
39. Desrosiers RC, Lifson JD, Gibbs JS, Czajak SC, Howe AY, Arthur LO, Johnson RP. Identification of highly attenuated mutants of simian immunodeficiency virus. J Virol 1998; 72:1431-1437.
40. Reynolds MR, Weiler AM, Weisgrau KL, Piaskowski SM, Furlott JR, Weinfurter JT, et al. Macaques vaccinated with live-attenuated SIV control replication of heterologous virus. J Exp Med 2008; 205:2537-2550.
41. Jia B, Ng SK, DeGottardi MQ, Piatak M, Yuste E, Carville A, et al. Immunization with single-cycle SIV significantly reduces viral loads after an intravenous challenge with SIV(mac)239. PLoS Pathog 2009; 5:e1000272.
42. Johnson RP, Lifson JD, Czajak SC, Cole KS, Manson KH, Glickman R, et al. 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.
43. Hofmann-Lehmann R, Vlasak J, Williams AL, Chenine AL, McClure HM, Anderson DC, et al. Live attenuated, nef-deleted SIV is pathogenic in most adult macaques after prolonged observation. AIDS 2003; 17:157-166.
44. Gorry PR, Churchill M, Learmont J, Cherry C, Dyer WB, Wesselingh SL, Sullivan JS. Replication-dependent pathogeni-city of attenuated nef-deleted HIV-1 in vivo. J Acquir Immune Defic Syndr 2007; 46:390-394.
45. Swigut T, Alexander L, Morgan J, Lifson J, Mansfield KG, Lang S, et al. Impact of Nef-mediated downregulation of major histocompatibility complex class I on immune response to simian immunodeficiency virus. J Virol 2004; 78:13335-13344.
46. Matano T, Kobayashi M, Igarashi H, Takeda A, Nakamura H, Kano M, et al. Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J Exp Med 2004; 199:1709-1718.
47. Khamsi R. Return to basics might breathe life into HIV vaccine pipeline. Nat Med 2008; 14:469.
48. Overbaugh J, Bangham CR. Selection forces and constraints on retroviral sequence variation. Science 2001; 292:1106-1109.
49. Allen TM, O'Connor DH, Jing P, Dzuris JL, Mothe BR, Vogel TU, et al. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 2000; 407:386-390.
50. O'Connor DH, Allen TM, Watkins DI. Cytotoxic T-lympho-cyte escape monitoring in simian immunodeficiency virus vaccine challenge studies. DNA Cell Biol 2002; 21:659-664.
51. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, Meyers H, et al. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 1997; 3:205-211.
52. Price DA, Goulder PJ, Klenerman P, Sewell AK, Easterbrook PJ, Troop M, et al. Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci USA 1997; 94:1890-1895.
53. Balter M. Modest Briton stirs up storm with views on role of CTLs. Science 1998; 280:1860-1861.
54. O'Connor DH, Allen TM, Vogel TU, JingP,DeSouza IP, Dodds E, et al. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat Med 2002; 8:493-499.
55. O'Connor DH, Mothe BR, Weinfurter JT, Fuenger S, Rehrauer WM, Jing P, et al. Major histocompatibility complex class I alleles associated with slow simian immunodeficiency virus disease progression bind epitopes recognized by dominant acute-phase cytotoxic-T-lymphocyte responses. J Virol 2003; 77:9029-9040.
56. Cao J, McNevin J, Malhotra U, McElrath MJ. Evolution of CD8R T cell immunity and viral escape following acute HIV-1 infection. J Immunol 2003; 171:3837-3846.
57. Bernardin F, Kong D, Peddada L, Baxter-Lowe LA, Delwart E. Human immunodeficiency virus mutations during the first month of infection are preferentially found in known cyto-toxic T-lymphocyte epitopes. J Virol 2005; 79:11523-11528.
58. Jones NA, Wei X, Flower DR, Wong M, Michor F, Saag MS, et al. Determinants of human immunodeficiency virus type 1 escape from the primary CD8R cytotoxic T lymphocyte response. J Exp Med 2004; 200:1243-1256.
59. Bailey JR, Zhang H, Wegweiser BW, Yang HC, Herrera L, AhonkhaiA, et al. Evolutionof HIV-1 in an HLA-BM57-positive patient during virologic escape. J Infect Dis 2007; 196:50-55.
60. Brumme ZL, Brumme CJ, Carlson J, Streeck H, John M, Eich-baum Q, et al. Marked epitope-and allele-specific differences inratesofmutationinhumanimmunodeficiencytype1(HIV-1) Gag, Pol, and Nef cytotoxic T-lymphocyte epitopes in acute/ early HIV-1 infection. J Virol 2008; 82:9216-9227.
61. Loffredo JT, Bean AT, Beal DR, Leon EJ, May GE, Piaskowski SM, et al. Patterns of CD8R immunodominance may influence the ability of Mamu-BM08-positive macaques to naturally control simian immunodeficiency virus SIVmac239 replication. J Virol 2008; 82:1723-1738.
62. Wang YE, Li B, Carlson JM, StreeckH, Gladden AD, Goodman R, et al. Protective HLA class I alleles that restrict acute-phase CD8R T-cell responses are associated with viral escape mutations located in highly conserved regions of human immunodeficiency virus type 1. J Virol 2009; 83:1845-1855.
63. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeodG,Borkowsky W, et al. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 1994; 68:4650-4655.
64. Kestler HW 3rd, Ringler DJ, Mori K, Panicali DL, Sehgal PK, Daniel MD, Desrosiers RC. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 1991; 65:651-662.
65. Regier DA, Desrosiers RC. The complete nucleotide sequence of a pathogenic molecular clone of simian immunodeficiency virus. AIDS Res Hum Retroviruses 1990; 6:1221-1231.
66. Alexander L, Denekamp L, Czajak S, Desrosiers RC. Subopti-mal nucleotides in the infectious, pathogenic simian immunodeficiency virus clone SIVmac239. J Virol 2001; 75:4019-4022.
67. Gundlach BR, Lewis MG, Sopper S, Schnell T, Sodroski J, Stahl-Hennig C, Uberla K. Evidence for recombination of live, attenuated immunodeficiency virus vaccine with challenge virus to a more virulent strain. J Virol 2000; 74:3537-3542.
68. Kim EY, Busch M, Abel K, Fritts L, Bustamante P, Stanton J, et al. Retroviral recombination in vivo: viral replication patterns and genetic structure of simian immunodeficiency virus (SIV) populations in rhesus macaques after simultaneous or sequential intravaginal inoculation with SIVmac239Del tavpx/Deltavpr and SIVmac239Deltanef. J Virol 2005; 79: 4886-4895.
69. Streeck H, Li B, Poon AF, Schneidewind A, Gladden AD, Power KA, et al. Immune-driven recombination and loss of control after HIV superinfection. J Exp Med 2008; 205:1789-1796.
70. Stebbings R, Berry N, Waldmann H, Bird P, Hale G, Stott J, et al. CD8R lymphocytes do not mediate protection against acute superinfection 20 days after vaccination with a live attenuated simian immunodeficiency virus. J Virol 2005; 79:12264-12272.
71. Johnson RP, Desrosiers RC. Protective immunity induced by live attenuated simian immunodeficiency virus. Curr Opin Immunol 1998; 10:436-443.
72. Picker LJ, Hagen SI, Lum R, Reed-Inderbitzin EF, Daly LM, Sylwester AW, et al. Insufficient production and tissue delivery of CD4R memory T cells in rapidly progressive simian immunodeficiency virus infection. J Exp Med 2004; 200: 1299-1314.
73. Li Q, Duan L, Estes JD, Ma ZM, Rourke T, Wang Y, et al. Peak SIV replication in resting memory CD4R T cells depletes gut lamina propria CD4R T cells. Nature 2005; 434:1148-1152.
74. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M. Massive infection and loss of memory CD4R T cells in multiple tissues during acute SIV infection. Nature 2005; 434:1093-1097.
75. Brenchley JM, Price DA, Douek DC. HIV disease: fallout from a mucosal catastrophe? Nat Immunol 2006; 7:235-239.
76. Piantadosi A, Chohan B, Chohan V, McClelland RS, Over-baugh J. Chronic HIV-1 infection frequently fails to protect against superinfection. PLoS Pathog 2007; 3:e177.
77. Jung A, Maier R, Vartanian JP, Bocharov G, Jung V, Fischer U, et al. Multiply infected spleen cells in HIV patients. Nature 2002; 418:144.
78. Levy DN, Aldrovandi GM, Kutsch O, Shaw GM. Dynamics of HIV-1 recombination in its natural target cells. Proc Natl Acad Sci USA 2004; 101:4204-4209.
79. Dixit NM, Perelson AS. HIV dynamics with multiple infections of target cells. Proc Natl Acad Sci USA 2005; 102:8198-8203.
80. Sodora DL, Sheridan KE, Marx PA, Connor RI. Immunization with a live, attenuated simian immunodeficiency virus vaccine leads to restriction of viral diversity in Rhesus macaques not protected from pathogenic challenge. J Virol 1999; 73:4443-4446.
81. Yankee TM, Sheffer D, Liu Z, Dhillon S, Jia F, Chebloune Y, et al. Longitudinal study to assess the safety and efficacy of a live-attenuated SHIV vaccine in long term immunized rhesus macaques. Virology 2009; 383:103-111.
82. Tsukamoto T, Yuasa M, Yamamoto H, Kawada M, Takeda A, Igarashi H, Matano T. Induction of CD8R cells able to suppress CCR5-tropic simian immunodeficiency virus SIV-mac239 replication by controlled infection of CXCR4-tropic simian-human immunodeficiency virus in vaccinated rhesus macaques. J Virol 2007; 81:11640-11649.
83. Gundlach BR, Reiprich S, Sopper S, Means RE, Dittmer U, Matz-Rensing K, et al. Env-independent protection induced by live, attenuated simian immunodeficiency virus vaccines. J Virol 1998; 72:7846-7851.
84. Letvin NL, Li J, Halloran M, Cranage MP, Rud EW, Sodroski J. Prior infection with a nonpathogenic chimeric simian-human immunodeficiency virus does not efficiently protect macaques against challenge with simian immunodeficiency virus. J Virol 1995; 69:4569-4571.
85. 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.
86. Yeh WW, Jaru-Ampornpan P, Nevidomskyte D, Asmal M, Rao SS, Buzby AP, et al. Partial protection of Simian immunodeficiency virus (SIV)-infected rhesus monkeys against super-infection with a heterologous SIV isolate. J Virol 2009; 83:2686-2696.
87. Das AT, Klaver B, Centlivre M, Harwig A, Ooms M, Page M, et al. Optimization of the doxycycline-dependent simian immunodeficiency virus through in vitro evolution. Retro-virology 2008; 5:44.
88. Deacon NJ, Tsykin A, Solomon A, Smith K, Ludford-Menting M, Hooker DJ, et al. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 1995; 270:988-991.
89. Dyer WB, Zaunders JJ, Yuan FF, Wang B, Learmont JC, Geczy AF, et al. Mechanisms of HIV nonprogression; robust and sustained CD4R T-cell proliferative responses to p24 antigen correlate with control of viraemia and lack of disease progression after long-term transfusion-acquired HIV-1 infection. Retrovirology 2008; 5:112.
90. Klenerman P, McMichael A. AIDS/HIV. Finding footprints among the trees. Science 2007; 315:1505-1507.
91. O'Connor DH, McDermott AB, Krebs KC, Dodds EJ, Miller JE, Gonzalez EJ, et al. A dominant role for CD8R-T-lymphocyte selection in simian immunodeficiency virus sequence variation. J Virol 2004; 78:14012-14022.
92. Allen TM, Altfeld M, Geer SC, Kalife ET, Moore C, O'Sullivan KM, et al. Selective escape from CD8R T-cell responses represents a major driving force of human immunodeficiency virus type one (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J Virol 2005; 79:13239-13249.
93. Kelleher AD, Long C, Holmes EC, Allen RL, Wilson J, Conlon C, et al. Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J Exp Med 2001; 193: 375-386.
94. Friedrich TC, Dodds EJ, Yant LJ, Vojnov L, Rudersdorf R, Cullen C, et al. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat Med 2004; 10:275-281.
95. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, Feeney M, et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 2004; 10:282-289.
96. Allen TM, Altfeld M, Yu XG, O'Sullivan KM, Lichterfeld M, Le Gall S, et al. Selection, transmission, and reversion of an antigen-processing cytotoxic T-lymphocyte escape mutation in human immunodeficiency virus type 1 infection. J Virol 2004; 78:7069-7078.
97. Bailey JR, Williams TM, Siliciano RF, Blankson JN. Maintenance of viral suppression in HIV-1-infected HLA-BM57R elite suppressors despite CTL escape mutations. J Exp Med 2006; 203:1357-1369.
98. Maness NJ, Yant LJ, Chung C, Loffredo JT, Friedrich TC, Piaskowski SM, et al. Comprehensive immunological evaluation reveals surprisingly few differences between elite controller and progressor Mamu-BM17-positive Simian immunodeficiency virus-infected rhesus macaques. J Virol 2008; 82:5245-5254.
99. Bailey JR, Brennan TP, O'Connell KA, Siliciano RF, Blankson JN. Evidence of CD8R T-cell-mediated selective pressure on human immunodeficiency virus type 1 nef in HLA-BM57R elite suppressors. J Virol 2009; 83:88-97.
100. Klenerman P, Zinkernagel RM. Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature 1998; 394:482-485.
101. Pamer EG. Immune responses to Listeria monocytogenes. Nat Rev Immunol 2004; 4:812-823.
102. Lewicki H, Tishon A, Borrow P, Evans CF, Gairin JE, Hahn KM, et al. CTL escape viral variants. I: Generation and molecular characterization. Virology 1995; 210:29-40.
103. Yewdell JW, Bennink JR. Immunodominance in major histo-compatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 1999; 17:51-88.
104. Draenert R, Allen TM, Liu Y, Wrin T, Chappey C, Verrill CL, et al. Constraints on HIV-1 evolution and immunodominance revealed in monozygotic adult twins infected with the same virus. J Exp Med 2006; 203:529-539.
105. Yang OO, Church J, Kitchen CM, Kilpatrick R, Ali A, Geng Y, et al. Genetic and stochastic influences on the interaction of human immunodeficiency virus type 1 and cytotoxic T lymphocytes in identical twins. J Virol 2005; 79:15368-15375.
106. Wiseman RW, Wojcechowskyj JA, Greene JM, Blasky AJ, Gopon T, Soma T, et al. Simian immunodeficiency virus SIVmac239 infection of major histocompatibility complex-identical cynomolgus macaques from Mauritius. J Virol 2007; 81:349-361.
107. O'Connor DH, Burton DR. Immune responsesand HIV:alittle order from the chaos. J Exp Med 2006; 203:501-503.
108. Selin LK, Brehm MA, Naumov YN, Cornberg M, Kim SK, Clute SC, Welsh RM. Memory of mice and men: CD8R T-cell cross-reactivity and heterologous immunity. Immunol Rev 2006; 211:164-181.
109. Haas G, Plikat U, Debre P, Lucchiari M, Katlama C, Dudoit Y, et al. Dynamics of viral variants in HIV-1 Nef and specific cytotoxic T lymphocytes in vivo. J Immunol 1996; 157:4212-4221.
110. Douek DC, Betts MR, Brenchley JM, Hill BJ, Ambrozak DR, Ngai KL, et al. A novel approach to the analysis of specificity, clonality, and frequency of HIV-specific T cell responses reveals a potential mechanism for control of viral escape. J Immunol 2002; 168:3099-3104.
111. Price DA, West SM, Betts MR, Ruff LE, Brenchley JM, Am-brozak DR, et al. T cell receptor recognition motifs govern immune escape patterns in acute SIV infection. Immunity 2004; 21:793-803.
112. Allen TM, Yu XG, Kalife ET, Reyor LL, Lichterfeld M, John M, et al. De novo generation of escape variant-specific CD8R T-cell responses following cytotoxic T-lymphocyte escape in chronic human immunodeficiency virus type 1 infection. J Virol 2005; 79:12952-12960.
113. Feeney ME, Tang Y, Pfafferott K, Roosevelt KA, Draenert R, Trocha A, et al. HIV-1 viral escape in infancy followed by emergence of a variant-specific CTL response. J Immunol 2005; 174:7524-7530.
114. Rodriguez F, Harkins S, Slifka MK, Whitton JL. Immunodomi-nance in virus-induced CD8(R) T-cell responses is dramatically modified by DNA immunization and is regulated by gamma interferon. J Virol 2002; 76:4251-4259.
115. Kedl RM, Kappler JW, Marrack P. Epitope dominance, competition and T cell affinity maturation. Curr Opin Immunol 2003; 15:120-127.
116. Liu F, Whitton JL, Slifka MK. The rapidity with which virus-specific CD8R T cells initiate IFN-gamma synthesis increases markedly over the course of infection and correlates with immunodominance. J Immunol 2004; 173:456-462.
117. Assarsson E, Sidney J, Oseroff C, Pasquetto V, Bui HH, Frahm N, et al. A quantitative analysis of the variables affecting the repertoire of T cell specificities recognized after vaccinia virus infection. J Immunol 2007; 178:7890-7901.
118. Gallimore A, Dumrese T, Hengartner H, Zinkernagel RM, Rammensee HG. Protective immunity does not correlate with the hierarchy of virus-specific cytotoxic T cell responses to naturally processed peptides. J Exp Med 1998; 187:1647-1657.
119. Frahm N, Kiepiela P, Adams S, Linde CH, Hewitt HS, Sango K, et al. Control of human immunodeficiency virus replication by cytotoxic T lymphocytes targeting subdominant epitopes. Nat Immunol 2006; 7:173-178.
120. Friedrich TC, Valentine LE, Yant LJ, Rakasz EG, Piaskowski SM, Furlott JR, et al. Subdominant CD8R T-cell responses are involved in durable control of AIDS virus replication. J Virol 2007; 81:3465-3476.
121. Carrington M, Nelson GW, Martin MP, Kissner T, Vlahov D, Goedert JJ, et al. HLA and HIV-1: heterozygote advantage and BM35-CwM04 disadvantage. Science 1999; 283:1748-1752.
122. Barouch DH, Powers J, Truitt DM, Kishko MG, Arthur JC, Peyerl FW, et al. Dynamic immune responses maintain cyto-toxic T lymphocyte epitope mutations in transmitted simian immunodeficiency virus variants. Nat Immunol 2005; 6:247-252.
123. Lifson JD, Rossio JL, Arnaout R, Li L, Parks TL, Schneider DK, et al. Containment of simian immunodeficiency virus infection: cellular immune responses and protection from rechal-lenge following transient postinoculation antiretroviral treatment. J Virol 2000; 74:2584-2593.
124. Lifson JD, Rossio JL, Piatak M Jr, Parks T, Li L, Kiser R, et al. Role of CD8(R) lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J Virol 2001; 75: 10187-10199.
125. Lifson JD, Piatak M Jr, Cline AN, Rossio JL, Purcell J, Pandrea I, et al. Transient early postinoculation antiretroviral treatment facilitates controlled infection with sparing of CD4R T cells in gut-associated lymphoid tissues in SIVmac239-infected rhesus macaques, but not resistance to rechallenge. J Med Primatol 2003; 32:201-210.
126. Van Rompay KK, Singh RP, Pahar B, Sodora DL, Wingfield C, Lawson JR, et al. CD8R-cell-mediated suppression of virulent simian immunodeficiency virus during tenofovir treatment. J Virol 2004; 78:5324-5337.
127. Streeck H, Brumme ZL, Anastario M, Cohen KW, Jolin JS, Meier A, et al. Antigen load and viral sequence diversification determine the functional profile of HIV-1-specific CD8R T cells. PLoS Med 2008; 5:e100.
128. Price DA, Asher TE, Wilson NA, Nason MC, Brenchley JM, Metzler IS, et al. Public clonotype usage identifies protective Gag-specific CD8R T cell responses in SIV infection. J Exp Med 2009; 206:923-936.
129. Miller CJ, Li Q, Abel K, Kim EY, Ma ZM, Wietgrefe S, et al. Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J Virol 2005; 79:9217-9227.
130. Haase AT. Perils at mucosal front lines for HIV and SIV and their hosts. Nat Rev Immunol 2005; 5:783-792.
131. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009; 361:2209-2220.
132. Kuroda MJ, Schmitz JE, Barouch DH, CraiuA,Allen TM, Sette A, etal. AnalysisofGag-specific cytotoxicTlymphocytesinsimian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J Exp Med 1998; 187:1373-1381.
133. 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.
134. Betts MR, Ambrozak DR, Douek DC, Bonhoeffer S, Brenchley JM, Casazza JP, et al. Analysis of total human immunodeficiency virus (HIV)-specific CD4(R) and CD8(R) T-cell responses: relationship to viral load in untreated HIV infection. J Virol 2001; 75:11983-11991.
135. Cao J, McNevin J, Holte S, Fink L, Corey L, McElrath MJ. Comprehensive analysis of human immunodeficiency virus type 1 (HIV-1)-specific gamma interferon-secreting CD8R T cells in primary HIV-1 infection. J Virol 2003; 77:6867-6878.
136. Addo MM, Yu XG, Rathod A, Cohen D, Eldridge RL, Strick D, et al. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J Virol 2003; 77:2081-2092.
137. Koup RA. Reconsidering early HIV treatment and supervised treatment interruptions. PLoS Med 2004; 1:e41.
138. Altfeld M, Rosenberg ES, Shankarappa R, Mukherjee JS, Hecht FM, Eldridge RL, et al. Cellular immune responses and viral diversity in individuals treated during acute and early HIV-1 infection. J Exp Med 2001; 193:169-180.
139. Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, et al. Antibody neutralization and escape by HIV-1. Nature 2003; 422:307-312.
140. Frost SD, Wrin T, Smith DM, Kosakovsky Pond SL, Liu Y, Paxinos E, et al. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc Natl Acad Sci USA 2005; 102:18514-18519.
141. Richman DD, Wrin T, Little SJ, Petropoulos CJ. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci USA 2003; 100:4144-4149.
142. Rolland M, Heckerman D, Deng W, Rousseau CM, Coovadia H, Bishop K, et al. Broad and Gag-biased HIV-1 epitope repertoires are associated with lower viral loads. PLoS One 2008; 3:e1424.
143. Burwitz BJ, Greene JM, O'Connor DH. Pirate primates in uncharted waters: lymphocyte transfers in unrelated, MHC-matched macaques. Curr HIV Res 2009; 7:51-56.
144. Sloan-Lancaster J, Allen PM. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu Rev Immunol 1996; 14:1-27.
145. Overbaugh J, Rudensey LM. Alterations in potential sites for glycosylation predominate during evolution of the simian immunodeficiency virus envelope gene in macaques. J Virol 1992; 66:5937-5948.