The roles of nonhuman primates in the preclinical evaluation of candidate AIDS vaccines

Expert Review of Vaccines

Volumn 3, Issue 4 SUPPL., 2004, Pages

  Staprans, Silvija I ^a,b   Feinberg, Mark B ^b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AIDS vaccine; Challenge models; HIV; Immunogenicity; Nonhuman primate; Preclinical; Simian immunodeficiency virus; Simian human immunodeficiency virus

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; ZIDOVUDINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; CLINICAL RESEARCH; DRUG EFFICACY; DRUG RESEARCH; DRUG SAFETY; DRUG SCREENING; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; IMMUNOGENICITY; IMMUNOPROPHYLAXIS; IMMUNOREGULATION; NONHUMAN; PATHOGENESIS; PRIMATE; PRIORITY JOURNAL; REVIEW; VIROLOGY; VIRUS TRANSMISSION;

ACQUIRED IMMUNODEFICIENCY SYNDROME; AIDS VACCINES; ANIMALS; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; HIV-1; HIV-2; HUMANS; PRIMATES; REASSORTANT VIRUSES; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 3042626395     PISSN: 14760584     EISSN: None     Source Type: Journal    
DOI: 10.1586/14760584.3.4.S5     Document Type: Review

References (222)

1. Hendrickx AG, Makori N, Peterson P. Nonhuman primates: their role in assessing developmental effects of immunomodulatory agents. Hum. Exp. Toxicol. 19(4), 219-225 (2000).
2. Buse E, Habermann G, Osterburg I, Korte R, Weinbauer GF. Reproductive/developmental toxicity and immunotoxicity assessment in the nonhuman primate model. Toxicology 185(3), 221-227 (2003).
3. Vaccines, From Concept to Clinic. Paoletti L, Mcinnes P (Eds.), CRC Press, FL, USA (1999).
4. Hahn BH, Shaw GM, De Cock KM, Sharp PM. AIDS as a zoonosis: scientific and public health implications. Science 287(5453), 607-614 (2000).
5. Salemi M, De Oliveira T, Courgnaud V et al. Mosaic genomes of the six major primate lentivirus lineages revealed by phylogenetic analyses. J. Virol. 77(13), 7202-7213 (2003).
6. Bailes E, Gao F, Bibollet-Ruche F et al. Hybrid origin of SIV in chimpanzees. Science 300, 1713(2003).
7. Gao F, Bailes E, Robertson DL et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes [see comments]. Nature 397(6718), 436-441 (1999).
8. Santiago ML, Lukasik M, Kamenya S et al. Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). J. Virol. 77(13), 7545-7562 (2003).
9. Tong-Starksen SE, Welsh TM, Peterlin BM. Differences in transcriptional enhancers of HIV-1 and HIV-2. Response to T cell activation signals. J. Immunol. 145(12), 4348-4354 (1990).
10. Nath BM, Schumann KE, Boyer JD. The chimpanzee and other non-human-primate models in HIV-1 vaccine research. Trends Microbiol. 8(9), 426-431 (2000).
11. O'Neil SP, Novembre FJ, Hill AB et al. Progressive infection in a subset of HIV-1-positive chimpanzees. J. Infect. Dis. 182(4), 1051-1062 (2000).
12. Novembre FJ, de Rosayro J, Nidtha S et al. Rapid CD4(+) T-cell loss induced by human immunodeficiency virus type 1(NC) in uninfected and previously infected chimpanzees. J. Virol. 75(3), 1533-1539 (2001).
13. + T cells in human immunodeficiency virus type 1-infected chimpanzees is associated with increased lymphocyte apoptosis. J. Virol. 72(6), 4623-4632 (1998).
14. Agy MB, Schmidt A, Horey MJ et al. Serial in vivo passage of HIV-1 infection in Macaca nemestrina. Virology 238(2), 336-343 (1997).
15. Stremlau M, Owens CM, Perron MJ et al. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427(6977), 848-853 (2004).
16. Schrofelbauer B, Chen D, Landau NR. From The Cover: A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif). Proc. Natl Acad. Sci. USA 101(11), 3927-3932 (2004).
17. Kar S, Cummings P, Alexander L. Human immunodeficiency virus type 1 Vif supports efficient primate lentivirus replication in rhesus monkey cells. J. Gen. Virol. 84(Pt 12), 3227-3231 (2003).
18. Locher CP, Barnett SW, Herndier BG et al. Human immunodeficiency virus-2 infection in baboons is an animal model for human immunodeficiency virus pathogenesis in humans. Arch. Pathol. Lab. Med. 122(6), 523-533 (1998).
19. Locher CP, Witt SA, Herndier BG et al. Baboons as an animal model for human immunodeficiency virus pathogenesis and vaccine development. Immunol. Rev. 183, 127-140 (2001).
20. McClure J, Schmidt AM, Rey-Cuille MA et al. Derivation and characterization of a highly pathogenic isolate of human immunodeficiency virus type 2 that causes rapid CD4+ cell depletion in Macaca nemestrina. J. Med. Primatol. 29(3-4), 114-126 (2000).
21. Pullium JK, Adams DR, Jackson E et al. Pig-tailed macaques infected with human immunodeficiency virus (HIV) type 2GB122 or simian/HIV89.6p express virus in semen during primary infection: new model for genital tract shedding and transmission. J. Infect. Dis. 183(7), 1023-1030 (2001).
22. Locher CP, Witt SA, Herndier BG et al. Increased virus replication and virulence after serial passage of human immunodeficiency virus type 2 in baboons. J. Virol. 77(1), 77-83 (2003).
23. Gardner MB. Simian AIDS: an historical perspective. J. Med. Primatol. 32(4-5), 180-186 (2003).
24. Letvin NL, Daniel MD, Sehgal PK et al. Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science 230(4721), 71-73 (1985).
25. Benveniste RE, Arthur LO, Tsai CC et al. Isolation of a lentivirus from a macaque with lymphoma: comparison with HTLV-III/LAV and other lentiviruses. J. Virol. 60(2), 483-490 (1986).
26. Murphey-Corb M, Martin LN, Rangan SR et al. Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature 321(6068), 435-437 (1986).
27. Fultz PN, McClure HM, Anderson DC et al. Isolation of a T-lymphotropic retrovirus from naturally infected sooty mangabey monkeys (Cercocebus atys). Proc. Natl Acad. Sci. USA 83(14), 5286-5290 (1986).
28. Hirsch VM, Lifson JD. Simian immunodeficiency virus infection of monkeys as a model system for the study of AIDS pathogenesis, treatment, and prevention. Adv. Phamacol. 49, 437-477 (2000).
29. Mansfield KG, Lerch NW, Gardner MB, Lackner AA. Origins of simian immunodeficiency virus infection in macaques at the New England Regional Primate Research Center. J. Med. Primatol. 24(3), 116-122 (1995).
30. + T-lymphocyte depletion in simian immunodeficiency virus-infected rapid progresser macaques. J. Virol. 78(1), 275-284 (2004).
31. Shibata R, Kawamura M, Sakai H et al. Generation of a chimeric human and simian immunodeficiency virus infectious to monkey peripheral blood mononuclear cells. J. Virol. 65(7), 3514-3520 (1991).
32. Li J, Lord CI, Haseltine W, Letvin NL, Sodroski J. Infection of cynomolgus monkeys with a chimeric HIV-1/SIVmac virus that expresses the HIV-1 envelope glycoproteins. J. Acquir. Immune Defic. Syndr. 5(7), 639-646 (1992).
33. Bogers WM, Cheng-Mayer C, Montelaro RC. Developments in preclinical AIDS vaccine efficacy models. AIDS 14(Suppl. 3), S141-151 (2000).
34. 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 20(1), 111-126 (2004).
35. Reimann KA, Li JT, Veazey R et al. A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J. Virol. 70(10), 6922-6928 (1996).
36. Zhang Y, Lou B, Lal RB et al. 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. 74(15), 6893-6910 (2000).
37. Igarashi T, Endo Y, Nishimura Y et al. Mechanism(s) responsible for the immunodeficiency induced by highly pathogenic SHIV and SIV appear to be fundamentally different. Paper presented at: 11th Conference on Retroviruses and Opportunistic Infections, CA, USA (2004).
38. Igarashi T, Endo Y, Nishimura Y et al. Early control of highly pathogenic simian immunodeficiency virus/human immunodeficiency virus chimeric virus infections in rhesus monkeys usually results in long-lasting asymptomatic clinical outcomes. J. Virol. 77(20), 10829-10840 (2003).
39. Harouse JM, Gettie A, Eshetu T et al. Mucosal transmission and induction of simian AIDS by CCR5-specific simian/human immunodeficiency virus SHIV(SF162P3). J. Virol. 75(4), 1990-1995 (2001).
40. Tan RC, Harouse JM, Gettie A, Cheng-Mayer C. In vivo adaptation of SHIV(SF162): chimeric virus expressing a NSI, CCR5-specific envelope protein. J. Med. Primatol. 28(4-5), 164-168 (1999).
41. Lard-Whiteford S, Matecka D, O'Rear J, Yuen I, Litterst C, Reichelderfer PS. Recommendations for the nonclinical development of topical microbicides for prevention of HIV transmission: an update. J. Acquir. Immune. Defic. Syndr. 36, 541-552 (2004).
42. Patton DL, Cosgrove-Sweeney YT, Rabe LK, Hillier SL. The pig-tailed macaque rectal model: microflora and chlamydial infection. Sexually Transmitted Dis. 28(7), 363-366 (2001).
43. Van Voorhis WC, Barren LK, Sweeney YT, Kuo CC, Patton DL. Repeated Chlamydia trachomatis infection of Macaca nemestrina fallopian tubes produces a Th1-like cytokine response associated with fibrosis and scarring. Infect. Immun. 65(6), 2175-2182 (1997).
44. Patton DL, Sweeney YC, Bohannon NJ et al. Effects of doxycycline and antiinflammatory agents on experimentally induced chlamydial upper genital tract infection in female macaques. J. Infect. Dis. 175(3), 648-654 (1997).
45. Lichtenwalner AB, Patton DL, Cosgrove Sweeney YT, Gaur LK, Stamm WE. Evidence of genetic susceptibility to Chlamydia trachomatis-induced pelvic inflammatory disease in the pig-tailed macaque. Infect. Immun. 65(6), 2250-2253 (1997).
46. Patton DL, Wolner-Hanssen P, Cosgrove SJ, Holmes KK. The effects of Chlamydia trachomatis on the female reproductive tract of the Macaca nemestrina after a single tubal challenge following repeated cervical inoculations. Obstetrics Gynecology 76(4), 643-650 (1990).
47. Black H. Monkey Trouble. The Scientist (www.the-scientist.com) (2003).
48. Cohen J. AIDS research. Vaccine studies stymied by shortage of animals. Science 287(5455), 959-960 (2000).
49. Council NR. International Perspectives: the Future of Nonhuman Primate Resources, Proceedings of the Workshop Help April 17-19, 2002.
50. Valli PJ, Lukashov W, Heeney JL, Goudsmit J. Shortening of the symptom -free period in rhesus macaques is associated with decreasing nonsynonymous variation in the env variable regions of simian immunodeficiency virus SIVsm during passage. J. Virol. 72(9), 7494-7500 (1998).
51. Holterman L, Niphuis H, ten Haaft PJ et al. Specific passage of simian immunodeficiency virus from end-stage disease results in accelerated progression to AIDS in rhesus macaques. J. Gen. Virol. 80 (Pt 12), 3089-3097 (1999).
52. + T cell depletion and viral replication in SIV infection. Science 280(5362), 427-431 (1998).
53. Veazey R, Marx P, Lackner A. The mucosal immune system: primary target for HIV infection and AIDS. Trends Immunol. 22, 626-633 (2001).
54. Harouse JM, Gettie A, Tan RC, Blanchard J, Cheng-Mayer C. Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. Science 284(5415), 816-819 (1999).
55. Smith PD, Meng G, Salazar-Gonzalez JF, Shaw GM. Macrophage HIV-1 infection and the gastrointestinal tract reservoir. J. Leukoc. Biol. 74(5), 642-649 (2003).
56. Veazey R, Lackner A. The mucosal immune system and HIV-1 infection. AIDS Rev. 5(4), 245-252 (2003).
57. Gray RH, Wawer MJ, Brookmeyer R et al. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 357(9263), 1149-1153 (2001).
58. DeGruttola V, Seage GR 3rd, Mayer KH, Horsburgh CR Jr. Infectiousness of HIV between male homosexual partners. J. Clin. Epidemiol. 42(9), 849-856 (1989).
59. Jewell NP, Shiboski SC. Statistical analysis of HIV infectivity based on partner studies. Biometrics 46(4), 1133-1150 (1990).
60. Safrit JT, Ruprecht R, Ferrantelli F et al. Immunoprophylaxis to prevent mother-to-child transmission of HIV-1. J. Acquir. Immune Defic. Syndr, 35(2), 169-177 (2004).
61. Sodora DL, Gettie A, Miller CJ, Marx PA. Vaginal transmission of SIV: assessing infectivity and hormonal influences in macaques inoculated with cell-free and cell-associated viral stocks. AIDS Res. Hum. Retroviruses 14(Suppl. 1), S119-S123 (1998).
62. Hu J, Gardner MB, Miller Q. Simian immunodeficiency virus rapidly penetrates the cervicovaginal mucosa after intravaginal inoculation and infects intraepithelial dendritic cells. J. Virol. 74(13), 6087-6095 (2000).
63. Couedel-Courteille A, Butor C, Juillard V, Guillet JG, Venet A. Dissemination of SIV after rectal infection preferentially involves paracolic germinal centers. Virology 260(2), 277-294 (1999).
64. Van Rompay KK, Schmidt KA, Lawson JR et al. Topical administration of low-dose tenofovir disoproxil fumarate to protect infant macaques against multiple oral exposures of low doses of simian immunodeficiency virus. J. Infect. Dis. 186(10), 1508-1513 (2002).
65. Hofmann-Lehmann R, Rasmussen RA, Vlasak J et al. Passive immunization against oral AIDS virus transmission: an approach to prevent mother-to-infant HIV-1 transmission? J. Med. Primatol. 30(4), 190-196 (2001).
66. Ruprecht RM, Baba TW, Liska V et al. Oral transmission of primate lentiviruses. J. Infect. Dis. 179(Suppl 3), S408-S412 (1999).
67. Van Rompay KK, Berardi Q, Dillard-Telm S et al. Passive immunization of newborn rhesus macaques prevents oral simian immunodeficiency virus infection. J. Infect. Dis. 177(5), 1247-1259 (1998).
68. Holterman L, Niphuis H, Koornstra W et al. The rate of progression to AIDS is independent of virus dose in simian immunodeficiency virus-infected macaques. J. Gen. Virol. 81(Pt 7), 1719-1726 (2000).
69. Endo Y, Igarashi T, Nishimura Y et al. Short- and long-term clinical outcomes in rhesus monkeys inoculated with a highly pathogenic chimeric simian/human immunodeficiency virus. J. Virol. 74(15), 6935-6945 (2000).
70. Pope M, Haase AT. Transmission, acute HIV-1 infection and the quest for strategies to prevent infection. Nature Med. 9(7), 847-852 (2003).
71. Miller Q, Shattock RJ. Target cells in vaginal HIV transmission. Microbes Infect. 5(1), 59-67 (2003).
72. Spira AI, Marx EA, Patterson BK et al. Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J. Exp Med. 183(1), 215-225 (1996).
73. Zhang Z, Schuler T, Zupancic M et al. Sexual transmission and propagation of SIV and HIV in resting and activated CD4(+) T cells. Science 286, 1353-1357 (1999).
74. Smith SM, Baskin GB, Marx PA. Estrogen protects against vaginal transmission of simian immunodeficiency virus. J. Infect. Dis. 182(3), 708-715 (2000).
75. Aaby P, Ariyoshi K, Buckner M et al. Age of wife as a major determinant of male-to-female transmission of HIV-2 infection: a community study from rural West Africa. AIDS 10(13), 1585-1590 (1996).
76. Martin HL Jr, Nyange PM, Richardson BA et al. Hormonal contraception, sexually transmitted diseases and risk of heterosexual transmission of human immunodeficiency virus Type 1. J. Infect. Dis. 178(4), 1053-1059 (1998).
77. Ungchusak K, Rehle T, Thammapornpilap P et al. Determinants of HIV infection among female commercial sex workers in northeastern Thailand: results from a longitudinal study. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 12(5), 500-507 (1996).
78. Lavreys L, Baeten JM, Kreiss JK et al. Injectable contraceptive use and genital ulcer disease during the early phase of HIV-1 infection increase plasma virus load in women. J. Infect. Dis. 189(2), 303-311 (2004).
79. Parren PW, Marx PA, Hessell AJ et al. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75(17), 8340-8347 (2001).
80. Mellors JW, Kingsley LA, Rinaldo CR Jr. et al. Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann. Intern. Med. 122(8), 573-579 (1995).
81. Staprans SI, Dailey PJ, Rosenthal A et al. Simian immunodeficiency virus disease course is predicted by the extent of virus replication during primary infection. J. Virol. 73(6), 4829-4839 (1999).
82. Watson A, Ranchalis J, Travis B et al. Plasma viremia in macaques infected with simian immunodeficiency virus: plasma viral load early in infection predicts survival. J. Virol. 71(1), 284-290 (1997).
83. Ho DD, Neumann AU, Perelson AS et al. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection [see comments]. Nature 373(6510), 125-126 (1995).
84. Wei X, Ghosh SK, Taylor ME et al. Viral dynamics in human immunodeficiency virus type 1 infection [see comments]. Nature 373(6510), 117-122 (1995).
85. Nowak MA, Lloyd AL, Vasquez GM et al. Viral dynamics of primary viremia and antiretroviral therapy in simian immunodeficiency virus infection. J. Virol. 71(10), 7518-7525 (1997).
86. Finkel TH, Tudor-Williams G, Banda NK et al. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes [see comments]. Nature Med. 1(2), 129-134 (1995).
87. Finkel TH, Banda NK. Indirect mechanisms of HIV pathogenesis: how does HIV kill T cells? Curr. Opin. Immunol. 6(4), 605-615 (1994).
88. + T cells by a cytotoxic T-lymphocyte clone directed against a novel A2-restricted reverse-transcriptase epitope. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 19(2), 111-120 (1998).
89. + lymphocytes by non-HLA-restricted cytotoxic T lymphocytes from HIV-infected individuals. Clin. Exp. Immunol. 93(3), 356-362 (1993).
90. Giorgi JV, Hultin LE, McKeating JA et al. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J. Infect. Dis. 179(4), 859-870 (1999).
91. Sousa AE, Carneiro J, Meier-Schellersheim M, Grossman Z, Victorino RM. CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. J. Immunol. 169(6), 3400-3406 (2002).
92. Douek DC, Picker LJ, Koup RA. T cell dynamics in HIV-1 infection. Annu. Rev. Immunol. 21, 265-304 (2003).
93. Silvestri G, Feinberg MB. Turnover of lymphocytes and conceptual paradigms in HIV infection. J. Clin. Invest. 112(6), 821-824 (2003).
94. Broussard SR, Staprans SI, White R et al. Simian immunodeficiency virus replicates to high levels in naturally infected African green monkeys without inducing immunologic or neurologic disease. J. Virol. 75(5), 2262-2275 (2001).
95. Ondoa P, Kestens L, Davis D et al. Longitudinal comparison of virus load parameters and CDS T-cell suppressive capacity in two SIV cpz-infected chimpanzees. J. Med. Primatol. 30(5), 243-253 (2001).
96. Silvestri G, Sodora DL, Koup RA et al. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18(3), 441-452 (2003).
97. Decks S, Walker B. The immune response to AIDS virus infection: good, bad, or both? (Commentary). J. Clin. Invest. 113, 808-810 (2004).
98. + T-cells in control of SIV replication. J. Clin. Invest. (In Press) (2004).
99. Tsai CC, Emau P, Follis KE et al. Effectiveness of postinoculation (R)-9-(2-phosphonylmethoxypropyl) adenine treatment for prevention of persistent simian immunodeficiency virus SIVmne infection depends critically on timing of initiation and duration of treatment. J. Virol. 75(5), 4265-4273 (1998).
100. Wick D, Self SG. Early HIV infection in vivo: branching-process model for studying timing of immune responses and drug therapy. Mathematical Biosci. 165(2), 115-134 (2000).
101. Veazey RS, Klasse PJ, Ketas TJ et al. Use of a small molecule CCR5 inhibitor in macaques to treat simian immunodeficiency virus infection or prevent simian-human immunodeficiency virus infection. J. Exp. Med. 198(10), 1551-1562 (2003).
102. Lori F, Lewis MG, Xu J et al. Control of SIV rebound through structured treatment interruptions during early infection. Science 290(5496), 1591-1593 (2000).
103. Hel Z, Venzon D, Poudyal M et al. Viremia control following antiretroviral treatment and therapeutic immunization during primary SIV251 infection of macaques. Nature Med. 6(10), 1140-1146 (2000).
104. Lifson JD. Containment of simian immunodeficiency virus infection: cellular immune responses and protection from rechallenge following transient postinoculation antiretroviral treatment. J. Virol. 74(6), 2584-2593 (2000).
105. + T cells in gut-associated lymphoid tissues in SIVmac239-infected rhesus macaques, but not resistance to rechallenge. J. Med. Primatol. 32(4-5), 201-210 (2003).
106. Johnson RP, Desrosiers RC. Protective immunity induced by live attenuated simian immunodeficiency virus. Curr. Opin. Immunol. 10(4), 436-443 (1998).
107. Marthas ML, Sutjipto S, Higgins J et al. Immunization with a live, attenuated simian immunodeficiency virus (SIV) prevents early disease but not infection in rhesus macaques challenged with pathogenic SIV. J. Virol. 64(8), 3694-3700 (1990).
108. 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 [see comments]. Science 258(5090), 1938-1941 (1992).
109. Johnson RP, Lifson JD, Czajak SC 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. 73(6), 4952-4961 (1999).
110. Ruprecht RM. Live attenuated AIDS viruses as vaccines: promise or peril? Immunol. Rev. 170, 135-149 (1999).
111. Connor RI, Montefiori DC, Binley JM 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. 72(9), 7501-7509 (1998).
112. Wyand MS, Manson K, Montefiori DC et al. Protection by live, attenuated simian immunodeficiency virus against heterologous challenge. J. Virol. 73(10), 8356-8363 (1999).
113. Johnson RP. Mechanisms of protection against simian immunodeficiency virus infection. Vaccine 20(15), 1985-1987 (2002).
114. Nathanson N, Mathieson BJ. Biological considerations in the development of a human immunodeficiency virus vaccine. J. Inject. Dis. 182(2), 579-589 (2000).
115. Lifson JD. Role of CD8(+) lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J. Virol. 75(21), 10187-10199 (2001).
116. + T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nature Immunol. 3(11), 1061-1068 (2002).
117. Amara R, Villinger F, Altman J et al. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292, 69-74 (2001).
118. Barouch DH, Santra S, Schmitz JE et al. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination [see comments]. Science 290(5491), 486-492 (2000).
119. Shiver JW, Fu TM, Chen L et al. Replication -incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity [see comments]. Nature 415(6869), 331-335 (2002).
120. Cafaro A, Caputo A, Fracasso C et al. Control of SHIV-89.6P-infection of cynomolgus monkeys by HIV-1 Tat protein vaccine. Nature Med. 5(6), 643-650 (1999).
121. Amara RR, Villinger F, Staprans SI et al. Different patterns of immune responses but similar control of a SHIV 89.6P Mucosal challenge by MVA and DNA/MVA vaccines. J. Virol. 76, 7623-7631 (2002).
122. Chen X, Scala G, Quinto I et al. Protection of rhesus macaques against disease progression from pathogenic SHIV-89.6PD by vaccination with phage-displayed HIV-1 epitopes. Nature Med. 7(11), 1223-1231 (2001).
123. Rose NF, Marx PA, Luckay A et al. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell, 106(5), 539-549 (2001).
124. Garber D, Silvestri G, Feinberg M. Prospects for an AIDS vaccine: three big questions, no easy answers. Lancet 4, 397-413 (2004).
125. Zhang ZQ, Schleif WA, Casimiro DR et al. The impact of early immune destruction on the kinetics of postacute viral replication in rhesus monkey infected with the simian-human immunodeficiency virus 89.6P. Virology 320(1), 75-84 (2004).
126. Horton H, Vogel TU, Carter DK et al. Immunization of rhesus macaques with a DNA prime/modified vaccinia virus Ankara boost regimen induces broad simian immunodeficiency virus (SIV)-specific T -cell responses and reduces initial viral replication but does not prevent disease progression following challenge with pathogenic SIVmac239. J. Virol. 76(14), 7187-7202 (2002).
127. Pal R, Venzon D, Letvin NL et al. ALVAC-SIV-gag-pol-env-based vaccination and macaque major histocompatibility complex class I (A*01) delay simian immunodeficiency virus SIVmac-induced immunodeficiency. J. Virol. 76(1), 292-302 (2002).
128. Emini EA. The use of replication-defective adenovirus vectors in AIDS vaccines. In: AIDS Vaccine 2003. AIDS Vaccine 2003 Conference, September 18-21, NY, USA (2003).
129. Feinberg MB, Moore JP. AIDS vaccine models: challenging challenge viruses, [see comments]. Nature Med. 8(3), 207-210 (2002).
130. Koup RA, Safrit JT, Cao Y et al. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68(7), 4650-4655 (1994).
131. + cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68(9), 6103-6110 (1994).
132. Kuroda MJ, Schmilz JE, Charini WA et al. Emergence of CTL coincides with clearance of virus during primary simian immunodeficiency virus infection in rhesus monkeys. J. Immunol. 162(9), 5127-5133 (1999).
133. Jin X, Bauer DE, Tuttleton SE et al. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189(6), 991-998 (1999).
134. + lymphocytes. Science 283(5403), 857-860 (1999).
135. Matano T, Shibata R, Siemon C et al. 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. 72(1), 164-169 (1998).
136. Metzner KJ, Jin X, Lee FV et al. Meets 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. 191(11), 1921-1931 (2000).
137. Grakoui A, Shoukry NH, Woollard DJ et al. HCV persistence and immune evasion in the absence of memory T cell help. Science 302(5645), 659-662 (2003).
138. Schmitz JE, Kuroda MJ, Santra S et al. Effect of humoral immune responses on controlling viremia during primary infection of rhesus monkeys with simian immunodeficiency virus. J. Virol. 77(3), 2165-2173 (2003).
139. Carrington M, O'Brien SJ. The influence of HLA genotype on AIDS. Ann. Rev. Med. 54, 535-551 (2003).
140. Mothe BR, Weinfurter J, Wang C et al. Expression of the major histocompatibility complex class I molecule Mamu-A*01 is associated with control of simian immunodeficiency virus SIVmac239 replication. J. Virol. 77(4), 2736-2740 (2003).
141. O'Connor DH, Mothe BR, Weinfurter JT et al. Major histocompatibility complex class I slides associated with slow simian immunodeficiency virus disease progression bind epitopes recognized by dominant acute-phase cytotoxic T-lymphocyte responses. J. Virol. 77(16), 9029-9040 (2003).
142. Marthas ML. Titration of an SIVmac251 stock by vaginal inoculation of Indian and Chinese origin rhesus macaques: transmission efficiency, viral loads, and antibody responses. AIDS Res. Hum. Retroviruses 17(15), 1455-1466 (2001).
143. Vogel TU, Reynolds MR, Fuller DH et al. Multispecific vaccine-induced mucosal cytotoxic T lymphocytes reduce acute phase viral replication but fail in long-term control of simian immunodeficiency virus SIVmac239. J. Virol. 77(24), 13348-13360 (2003).
144. Mothe BR, Horton H, Carter DK et al. Dominance of CD8 responses specific for epitopes bound by a single major histocompatibility complex class I molecule during the acute phase of viral infection. J. Virol. 76(2), 875-884 (2002).
145. Viray J, Rolfs B, Smith DG. Comparison of the frequencies of major histocompatibility (MHC) class-II DQA1 and DQB1 alleles in Indian and Chinese rhesus macaques (Macaca mulatta). Comp. Med. 51(6), 555-561 (2001).
146. Trichel AM, Rajakumar PA, Murphey-Corb M. Species-specific variation in SIV disease progression between Chinese and Indian subspecies of rhesus macaque. J. Med. Primatol. 31(4-5), 171-178 (2002).
147. Ling B, Veazey RS, Ludssy A et al. SIV(mac) pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans. AIDS 16(11), 1489-1496 (2002).
148. Leslie AJ, Pfafferott KJ, Chetty P et al. HIV evolution: CTL escape mutation and reversion after transmission. Nature Med. 10(3), 282-289 (2004).
149. O'Connor D, Friedrich T, Hughes A, Allen TM, Watkins D. Understanding cytotoxic T-lymphocyte escape during simian immunodeficiency virus infection. Immunol. Rev. 183, 115-126 (2001).
150. O'Connor DH, Allen TM, Vogel TU et al. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nature Med. 8(5), 493-499 (2002).
151. Barouch DH, Kunstman J, Glowczwskie J et al. Viral escape from dominant simian immunodeficiency virus epitope-specific cytotoxic T lymphocytes in DNA-vaccinated rhesus monkeys. J. Virol. 77(13), 7367-7375 (2003).
152. Barouch DH, Kunstman J, Kuroda MJ et al. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes, [see comments]. Nature 415(6869), 335-339 (2002).
153. Friedrich TC, Dodds EJ, Yant LJ et al. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nature Med. 10(3), 275-281 (2004).
154. Altman JD, Feinberg MB. HIV escape: there and back again. Nature Med. 10(3), 229-230 (2004).
155. Moore CB, John M, James IR et al. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296 (5572), 1439-1443 (2002).
156. Kwong PD, Doyle ML, Casper DJ et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420(6916), 678-682 (2002).
157. Burton DR, Desrosiers RC, Doms RW et al. HIV vaccine design and the neutralizing antibody problem. Nature Immunol. 5(3), 233-236 (2004).
158. Zwick MB, Komori HK, Stanfield RL et al. The long third complementarity-determining region of the heavy chain is important in the activity of the broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2F5. J. Virol. 78(6), 3155-3161 (2004).
159. Shibata R, Igarashi T, Haigwood N et al. Neutralizing antibody directed against the HIV-1 envelope grycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nature Med 5(2), 204-210 (1999).
160. Cho MW, Kim YB, Lee MK et al. Polyvalent envelope grycoprotein vaccine elicits a broader neutralizing antibody response but is unable to provide sterilizing protection against heterologous Simian/human immunodeficiency virus infection in pigtailed macaques. J. Virol. 75(5), 2224-2234 (2001).
161. Mascola JR, Lewis MG, Stiegler G et al. Protection of macaques against pathogenic Simian/Human immunodeficiency virus 89-6PD by passive transfer of neutralizing antibodies. J. Virol. 73(5), 4009-4018 (1999).
162. Nishimura Y, Igarashi T, Haigwood N et al. Determination of a statistically valid neutralization titer in plasma that confers protection against simian-human immunodeficiency virus challenge following passive transfer of high-titered neutralizing antibodies. J. Virol. 76(5), 2123-2130 (2002).
163. Mascola JR. Passive transfer studies to elucidate the role of antibody-mediated protection against HIV-1. Vaccine 20(15), 1922-1925 (2002).
164. Hofmann-Lehmann R, Vlasak J, Rasmussen RA et al. Postnatal passive immunization of neonatal macaques with a triple combination of human monoclonal antibodies against oral simian-human immunodeficiency virus challenge. J. Virol.
165. Mascola JR, Stiegler G, VanCott TC et al. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nature Med. 6(2), 207-210 (2000).
166. Barouch DH, Letvin NL. Cytokine-induced augmentation of DNA vaccine-elicited SIV-specific immunity in rhesus monkeys. Develop. Biologicals 104, 85-92 (2000).
167. Barouch DH, Craiu A, Kuroda MJ et al. Augmentation of immune responses to HIV 1 and simian immunodeficiency virus DNA vaccines by IL-2/Ig plasmid administration in rhesus monkeys. Proc. Natl. Acad. Sci USA 97(8), 4192-4197 (2000).
168. Casimiro DR, Chen L, Fu TM et al. Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replication-defective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. J. Virol. 77(11), 6305-6313 (2003).
169. Casimiro DR, Tang A, Chen L et al. Vaccine-induced immunity in baboons by using DNA and replication-incompetent adenovirus type 5 vectors expressing a human immunodeficiency virus type 1 gag gene. J. Virol. 77(13), 7663-7668 (2003).
170. Staprans S, Barry A, Silvestri G et al. Enhanced simian immunodeficiency virus replication and accelerated progression to AIDS in macaques primed to mount a CD4 but not a CD8 T-cell response to the viral envelope protein. In: 10th Conference on Retroviruses and Opportunistic Infections, MA, USA (2003).
171. Hartmann G, Weeratna RD, Ballas ZK et al. Delineation of a CpG phosphorothioate oligodeoxynucleotide for activating primate immune responses in vitro and in vivo. J. Immunol. 164(3), 1617-1624 (2000).
172. Feinberg M, Wright D, Piliero P et al. The Safety and Immunogenicity of Merck's HIV-1 gag DNA Vaccines (with or without Adjuvants) in Healthy Adults. In: AIDS Vaccine 2003. AIDS Vaccine 2003 Conference, September 18-21, NY, USA (2003).
173. Wang SZ-S, Rushlow K, Issel C et al. Enhancement of EIAV replication and disease by immunization with a baculovirus-expressed recombinant envelope surface glycoprotein. Virology 199, 247-251 (1994).
174. Siebelink KH, Tijhaar E, Huisman RC et al. Enhancement of feline immunodeficiency virus infection after immunization with envelope glycoprotein subunit vaccines. J. Virol. 69(6), 3704-3711 (1995).
175. Russo P, Vitu C, Fontaine J, Vignoni M. Caprine arthritis-encephalitis: trial of an adjuvant vaccine preparation. I. Clinical and virological study. Comp. Immunol. Microbiol. Infect. Dis. 16, 131-136 (1993).
176. Desrosiers RC. Prospects for an AIDS vaccine. Nature Med. 10(3), 221-223 (2004).
177. Michael NL, Nelson JA, KewalRamani VN et al. Exclusive and persistent use of the entry coreceptor CXCR4 by human immunodeficiency virus type 1 from a subject homozygous for CCR5 delta32. J. Virol. 72(7), 6040-6047 (1998).
178. Reyes RA, Canfield DR, Esser U et al. Induction of simian AIDS in infant rhesus macaques infected with CCR5- or CXCR4- utilizing simian-human immunodeficiency viruses is associated with distinct lesions of the thymus. J. Virol. 78(4), 2121-2130 (2004).
179. Hirsch V, Adger-Johnson D, Campbell B et al. A molecularly cloned, pathogenic, neutralization-resistant simian immunodeficiency virus, SIVsmE543-3. J. Virol. 71(2), 1608-1620 (1997).
180. Hirsch VM, Johnson PR. Pathogenic diversity of simian immunodeficiency viruses. Virus Res. 32(2), 183-203 (1994).
181. Johnson WE, Sanford H, Schwall L et al. Assorted mutations in the envelope gene of simian immunodeficiency virus lead to loss of neutralization resistance against antibodies representing a broad spectrum of specificities. J. Virol. 77(18), 9993-10003 (2003).
182. Ruprecht RM, Bronson R. Chemoprevention of retroviral infection: success is determined by virus inoculum strength and cellular immunity. DNA Cell Biol. 13(1), 59-66 (1994).
183. Fazety F, Haseltine WA, Rodger RF, Ruprecht RM. Postexposure chemoprophylaxis with ZDV or ZDV combined with interferon-alpha: failure after inoculating rhesus monkeys with a high dose of SIV. J. Acquir. Immune Defic. Syndr. 4(11), 1093-1097 (1991).
184. Le Grand R, Oayette P, Noack O et al. An animal model for antilentiviral therapy: effect of zidovudine on viral load during acute infection after exposure of macaques to simian immunodeficiency virus. AIDS Res. Hum. Retroviruses 10(10), 1279-1287 (1994).
185. Mofenson LM. Reducing the risk of perinatal HIV-1 transmission with zidovudine: results and implications of AIDS Clinical Trials Group protocol 076. Acta Paediatr. Suppl. 421, 89-96 (1997).
186. Gaschen B, Taylor J, Yusim K et al. Diversity considerations in HIV-1 vaccine selection. Science 296(5577), 2354-2360 (2002).
187. Staprans SI, Hamilton BL, Follansbee SE et al. Activation of virus replication after vaccination of HIV-1-infected individuals. J. Am. Med. 182(6), 1727-1737 (1995).
188. Stanley S, Ostrowski MA, Justement JS et al. Effect of immunization with a common recall antigen on viral expression in patients infected with human immunodeficiency virus type 1. N. Engl. J. Med. 334(19), 1222-1230 (1996).
189. Bentwich Z, Maartens G, Torten D, Lal AA, Lal RB. Concurrent infections and HIV pathogenesis. AIDS 14(14), 2071-2081 (2000).
190. Kovacs JA, Imamichi H, Vogel S et al. Effects of intermittent interleukin-2 therapy on plasma and tissue human immunodeficiency virus levels and quasi-species expression. J. Infect Dis. 182(4), 1063-1069 (2000).
191. Bentwich Z. Concurrent infections that rise the HIV viral load. J. HIV Ther. 8(3), 72-75 (2003).
192. Bentwich Z, Kalinkovich A, Weisman Z. Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunol. Today 16(4), 187-191 (1995).
193. Lawn S, Butera S, Folks T. Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin. Microbiol. Rev. 14, 753-777 (2001).
194. Staprans S, Sumpter B, Paiardini M et al. Housing Conditions of Rhesus Macaques Induce Specific T Cell Activation Profiles and May Influence SIV Replication and the Response to Candidate AIDS Vaccines. In: AIDS Vaccine 2003. AIDS Vaccine 2003 Conference, September 18-21, NY, USA (2003).
195. Ayash-Rashkovsky M, Weisman Z, Diveley J et al. Generation of Th1 immune responses to inactivated, gp120-depleted HIV-1 in mice with a dominant Th2 biased immune profile via immunostimulatory [correction of imunostimulatory] oligonucleotides - relevance to AIDS vaccines in developing countries. Vaccine 20(21-22), 2684-2692 (2002).
196. Zemlin M, Klinger M, Link J et al. Expressed murine and human CDR-H3 intervals of equal length exhibit distinct repertoires that differ in their amino acid composition and predicted range of structures. J. Mol. Biol. 334(4), 733-749 (2003).
197. Penttinen MA, Ekman P, Granfors K. Non-antigen presenting effects of HLA-B27. Curr. Mol. Med. 4(1), 41-49 (2004).
198. Betts MR, Ambrozak DR, Douek DC et al. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 75(24), 11983-11991 (2001).
199. Migueles SA, Connors M. The Role of CD4(+) and CD8(+) T Cells in Controlling HIV Infection. Curr. Infect. Dis. Rep. 4(5), 461-467 (2002).
200. Younes SA, Yassine-Diab B, Dumont AR et al. HIV-1 viremia prevents the establishment of interleukin 2-producing HIV-specific memory CD4+ T cells endowed with proliferative capacity. J. Exp. Med. 198(12), 1909-1922 (2003).
201. Champagne P, Ogg GS, King AS et al. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410(6824), 106-111 (2001).
202. + effector and memory T cell generation. Nature Immunol. 4(9), 835-842 (2003).
203. Corbett EL, Steketee RW, ter Kuile FO et al. HIV-1/AIDS and the control of other infectious diseases in Africa. Lancet 359(9324), 2177-2187 (2002).
204. Kapiga SH, Sam NE, Shao JF et al. HIV-1 epidemic among female bar and hotel workers in northern Tanzania: risk factors and opportunities for prevention. J. Acquir. Immune Defic. Syndr. 29(4), 409-417 (2002).
205. Galvin SR, Cohen MS. The role of sexually transmitted diseases in HIV transmission. Nature Rev. Microbiol. 2(1), 33-42 (2004).
206. O'Farrell N, Windsor I, Becker P. HIV-1 infection among heterosexual attenders at a sexually transmitted diseases clinic in Durban. S. Afr. Med. J. 80(1), 17-20 (1991).
207. Derdeyn C, Decker J, Bibollet-Ruche F et al. Heterosexual transmission of HIV-1 involves envelope-constrained, neutralization-sensitive variants. In: AIDS Vaccine 2003. AIDS Vaccine 2003 Conference, September 18-21, NY, USA (2003).
208. Goldstein S, Brown CR, Dehghani H, Lifson JD, Hirsch VM. Intrinsic susceptibility of rhesus macaque peripheral CD4(+) T cells to simian immunodeficiency virus in vitro is predictive of in vivo viral replication. J. Virol. 74(20), 9388-9395 (2000).
209. Wei X, Decker JM, Wang S et al. Antibody neutralization and escape by HIV-1. Nature 422(6929), 307-312 (2003).
210. 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 100(7), 4144-4149 (2003).
211. McDermott AB, Mitchen J, Piaskowski S et al. Repeated low-dose mucosal simian immunodeficiency virus SIVmac239 challenge results in the same viral and immunological kinetics as high-dose challenge: a model for the evaluation of vaccine efficacy in nonhuman primates. J. Virol. 78(6), 3140-3144 (2004).
212. Otten R, Adams D, Kim C et al. Cellulose Acetate Phthalate Protects Macaques from Multiple, Low-dose Vaginal Exposures with an SHIV Virus: New Strategy to Study HIV Pre-clinical Interventions in Non-human Primates. In: 11th Conference on Retroviruses and Opportunistic Infections, CA, USA (2004).
213. Miller C. Vaginal SIV transmission models: High dose, low dose and hormonally manipulated. In: Mid-Atlantic SIV Interest Group, Fort Derrick, MD, USA (2004).
214. Regoes RR, Longini I, Feinberg M, Staprans S. Assessment of AIDS vaccination success by repeated low-dose challenges. In: 11th Conference on Retroviruses and Opportunistic Infection, CA, USA (2004).
215. Shiver J. A non-replicating adenoviral vector as a potential HIV vaccine. Res. Initiat. Treat. Action 8(2), 14-16 (2003).
216. Cao H, Kanki P, Sankale JL et al. Cytotoxic T-lymphocyte cross-reactivity among different human immunodeficiency virus type 1 clades: implications for vaccine development. J. Virol. 71(11), 8615-8623 (1997).
217. Zhu T, Wang N, Carr A et al. Genetic characterization of human immunodeficiency virus type 1 in blood and genital secretions: evidence for viral compartmentalization and selection during sexual transmission. J. Virol. 70(5), 3098-3107 (1996).
218. Becquart P, Chomont N, Roques P et al. Compartmentalization of HIV-1 between breast milk and blood of HIV-infected mothers. Virology 300(1), 109-117 (2002).
219. Warren J. Preclinical AIDS vaccine research: survey of SIV, SHIV and HIV challenge studies in vaccinated nonhuman primates. J. Med. Primatol. 31(4-5), 237-256 (2002).
220. Cohen J. In: Shots in the Dark: the Wayward Search for an AIDS Vaccine. WW Norton & Company, NY, USA (2001).
221. Klausner RD, Fauci AS, Corey L et al. Medicine. The need for a global HIV vaccine enterprise. Science 300(5628), 2036-2039 (2003).
222. Regoes RR, Antia R, Garber DA, Silvestri G, Feinberg MB, Staprans SI. Roles of target cells and virus-specific cellular immunity in primary simian immunodeficiency virus infection. J. Virol. 78, 4866-4875 (2004).