Using nonhuman primates to model HIV transmission

Current Opinion in HIV and AIDS

Volumn 8, Issue 4, 2013, Pages 280-287

  Fennessey, Christine M ^a   Keele, Brandon F ^a  

^a SAIC FREDERICK INC   (United States)

Author keywords

acute infection; mucosa; nonhuman primate models; simian immunodeficiency virus; transmission

Indexed keywords

CHEMOKINE RECEPTOR CCR5; HUMAN IMMUNODEFICIENCY VIRUS VACCINE;

BLOOD; CD4+ T LYMPHOCYTE; DRUG DESIGN; DRUG EFFICACY; DRUG MEGADOSE; FEMALE GENITAL SYSTEM; GENETIC ANALYSIS; HISTOPATHOLOGY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; INTRAVENOUS DRUG ABUSE; MALE GENITAL SYSTEM; MEDICAL INFORMATION; MOUTH; NONHUMAN; PHENOTYPE; PRIMATE; PRIORITY JOURNAL; RECTUM; REVIEW; SEXUAL TRANSMISSION; SIMIAN VIRUS; SPERM; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; DISEASE MODELS, ANIMAL; EPITHELIUM; HIV INFECTIONS; HUMANS; MACACA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84880332648     PISSN: 1746630X     EISSN: 17466318     Source Type: Journal    
DOI: 10.1097/COH.0b013e328361cfff     Document Type: Review

References (72)

1. Shaw GM, Hunter E. HIV transmission. Cold Spring Harbor Perspect Med 2012; 2.
2. Cohen MS. Preventing sexual transmission of HIV. Clin Infect Dis 2007; 45 (Suppl 4):S287-S292.
3. Cohen MS, Chen YQ, McCauley M, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 2011; 365:493-505.
4. Powers KA, Ghani AC, Miller WC, et al. The role of acute and early HIV infection in the spread of HIV and implications for transmission prevention strategies in Lilongwe, Malawi: a modelling study. Lancet 2011; 378:256-268.
5. Haaland RE, Hawkins PA, Salazar-Gonzalez J, et al. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog 2009; 5:e1000274.
6. Boily MC, Baggaley RF, Wang L, et al. Heterosexual risk of HIV-1 infection per sexual act: systematic review and meta-analysis of observational studies. Lancet Infect Dis 2009; 9:118-129.
7. Powers KA, Poole C, Pettifor AE, Cohen MS. Rethinking the heterosexual infectivity of HIV-1: a systematic review and meta-analysis. Lancet Infect Dis 2008; 8:553-563.
8. Auvert B, Taljaard D, Lagarde E, et al. Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: the ANRS 1265 Trial. PLoS Med 2005; 2:e298.
9. Bailey RC, Moses S, Parker CB, et al. Male circumcision for HIV prevention in young men in Kisumu, Kenya: a randomised controlled trial. Lancet 2007; 369:643-656.
10. Gray RH, Kigozi G, Serwadda D, et al. Male circumcision for HIV prevention in men in Rakai, Uganda: a randomised trial. Lancet 2007; 369:657-666.
11. Abrahams MR, Anderson JA, Giorgi EE, et al. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-Poisson distribution of transmitted variants. J Virol 2009; 83:3556-3567.
12. Kearney M, Maldarelli F, Shao W, et al. Human immunodeficiency virus type 1 population genetics and adaptation in newly infected individuals. J Virol 2009; 83:2715-2727.
13. Keele BF, Giorgi EE, Salazar-Gonzalez JF, et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci USA 2008; 105:7552-7557.
14. Li H, Bar KJ, Wang S, et al. High Multiplicity Infection by HIV-1 in Men Who Have Sex with Men. PLoS Pathog 2010; 6:e1000890.
15. Salazar-Gonzalez JF, Salazar MG, Keele BF, et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 2009; 206:1273-1289.
16. Palmer S, Kearney M, Maldarelli F, et al. Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J Clin Microbiol 2005; 43:406-413.
17. Salazar-Gonzalez JF, Bailes E, Pham KT, et al. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 2008; 82:3952-3970.
18. Ochsenbauer C, Edmonds TG, Ding H, et al. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macro-phages. J Virol 2012; 86:2715-2728.
19. Fischer W, Ganusov VV, Giorgi EE, et al. Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS One 2010; 5:e12303.
20. Lee HY, Giorgi EE, Keele BF, et al. Modeling sequence evolution in acute HIV-1 infection. J Theoret Biol 2009; 261:341-360.
21. Wood N, Bhattacharya T, Keele BF, et al. HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog 2009; 5:e1000414.
22. Song H, Pavlicek JW, Cai F, et al. Impact of immune escape mutations on HIV-1 fitness in the context of the cognate transmitted/founder genome. Retrovirology 2012; 9:89.
23. Bar KJ, Li H, Chamberland A, et al. Wide variation in the multiplicity of HIV-1 infection among injection drug users. J Virol 2010; 84:6241-6247.
24. Masharsky AE, Dukhovlinova EN, Verevochkin SV, et al. A substantial transmission bottleneck among newly and recently HIV-1-infected injection drug users in St Petersburg, Russia. J Infect Dis 2010; 201:1697-1702.
25. Brumme ZL, John M, Carlson JM, et al. HLA-associated immune escape pathways in HIV-1 subtype B Gag, Pol and Nef proteins. PLoS One 2009; 4:e6687.
26. Bar KJ, Tsao CY, Iyer SS, et al. Early low-titer neutralizing antibodies impede HIV-1 replication and select for virus escape. PLoS Pathog 2012; 8:e1002721.
27. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, et al. The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 2009; 206:1253-1272.
28. Tomaras GD, Yates NL, Liu P, et al. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma antigp41 antibodies with ineffective control of initial viremia. J Virol 2008; 82:12449-12463.
29. Asmal M, Hellmann I, Liu W, et al. A signature in HIV-1 envelope leader peptide associated with transition from acute to chronic infection impacts envelope processing and infectivity. PLoS One 2011; 6:e23673.
30. Gnanakaran S, Bhattacharya T, Daniels M, et al. Recurrent signature patterns in HIV-1 B clade envelope glycoproteins associated with either early or chronic infections. PLoS Pathog 2011; 7:e1002209.
31. Liu J, Keele BF, Li H, et al. Low-dose mucosal simian immunodeficiency virus infection restricts early replication kinetics and transmitted virus variants in rhesus monkeys. J Virol 2010; 84:10406-10412.
32. Keele BF, Li H, Learn GH, et al. Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J Exp Med 2009; 206:1117-1134.
33. Stone M, Keele BF, Ma ZM, et al. A limited number of simian immunodeficiency virus (SIV) env variants are transmitted to rhesus macaques vaginally inoculated with SIVmac251. J Virol 2010; 84:7083-7095.
34. Ma ZM, Keele BF, Qureshi H, et al. SIVmac251 is inefficiently transmitted to rhesus macaques by penile inoculation with a single SIVenv variant found in ramp-up phase plasma. AIDS Res Hum Retroviruses 2011; 27:1259-1269.
35. Fenizia C, Keele BF, Nichols D, et al. TRIM5alpha does not affect simian immunodeficiency virus SIV(mac251) replication in vaccinated or unvaccinated Indian rhesus macaques following intrarectal challenge exposure. J Virol 2011; 85:12399-12409.
36. Patel V, Jalah R, Kulkarni V, et al. DNA and virus particle vaccination protects against acquisition and confers control of viremia upon heterologous simian immunodeficiency virus challenge. Proc Natl Acad Sci USA 2013; 110:2975-2980.
37. Pegu P, Vaccari M, Gordon S, et al. Antibodies with high avidity to the gp120 envelope protein in protection from simian immunodeficiency virus SIVmac251 acquisition in an immunization regimen that mimics the RV-144 Thai Trial. J Virol 2013; 87:1708-1719.
38. Vaccari M, Keele BF, Bosinger SE, et al. Protection afforded by an HIV vaccine candidate in macaques dependent on the dose of SIVmac251 challenge exposure. J Virol 2013; 87:3538-3548.
39. Wilson NA, Keele BF, Reed JS, et al. Vaccine-induced cellular responses control simian immunodeficiency virus replication after heterologous chal lenge. J Virol 2009; 83:6508-6521.
40. Xiao P, Patterson LJ, Kuate S, et al. Replicating adenovirus-simian immuno-deficiency virus (SIV) recombinant priming and envelope protein boosting elicits localized, mucosal IgA immunity in rhesus macaques correlated with delayed acquisition following a repeated low-dose rectal SIV(mac251) challenge. J Virol 2012; 86:4644-4657.
41. Hansen SG, Vieville C, Whizin N, 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.
42. Barouch DH, Liu J, Li H, et al. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature 2012; 482:89-93.
43. Keele BF, Estes JD. Barriers to mucosal transmission of immunodeficiency viruses. Blood 2011; 118:839-846.
44. Li Q, Estes JD, Schlievert PM, et al. Glycerol monolaurate prevents mucosal SIV transmission. Nature 2009; 458:1034-1038.
45. Dinh MH, Okocha EA, Koons A, et al. Expression of structural proteins in human female and male genital epithelia and implications for sexually transmitted infections. Biol Reprod 2012; 86:32.
46. Yeh WW, Rao SS, Lim SY, et al. The TRIM5 gene modulates penile mucosal acquisition of simian immunodeficiency virus in rhesus monkeys. J Virol 2011; 85:10389-10398.
47. Qureshi H, Ma ZM, Huang Y, et al. Low-dose penile SIVmac251 exposure of rhesus macaques infected with adenovirus type 5 (Ad5) and then immunized with a replication-defective Ad5-based SIV gag/pol/nef vaccine recapitulates the results of the phase IIb step trial of a similar HIV-1 vaccine. J Virol 2012; 86:2239-2250.
48. Giavedoni LD, Chen HL, Hodara VL, et al. Impact of mucosal inflammation on oral simian immunodeficiency virus transmission. J Virol 2013; 87:1750-1758.
49. Li H, Reeves RK. Functional perturbation of classical natural killer and innate lymphoid cells in the oral mucosa during SIV infection. Front Immunol 2012; 3:417.
50. Bolton DL, Song K, Wilson RL, et al. Comparison of systemic and mucosal vaccination: impact on intravenous and rectal SIV challenge. Mucosal Immunol 2012; 5:41-52.
51. Reynolds MR, Weiler AM, Piaskowski SM, et al. A trivalent recombinant Ad5 gag/pol/nef vaccine fails to protect rhesus macaques from infection or control virus replication after a limiting-dose heterologous SIV challenge. Vaccine 2012; 30:4465-4475.
52. Hansen SG, Ford JC, Lewis MS, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 2011; 473:523-527.
53. Lai L, Kwa SF, Kozlowski PA, et al. SIVmac239 MVA vaccine with and without a DNA prime, similar prevention of infection by a repeated dose SIVsmE660 challenge despite different immune responses. Vaccine 2012; 30:1737-1745.
54. Reece JC, Alcantara S, Gooneratne S, et al. Trivalent live attenuated Influenza-SIV vaccines: efficacy and evolutionofCTL escapein macaques.JVirol 2013; 87:4146-4160.
55. Strbo N, Vaccari M, Pahwa S, et al. Cutting edge: novel vaccination modality provides significant protection against mucosal infection by highly pathogenic simian immunodeficiency virus. J Immunol 2013; 190:2495.
56. Vaccari M, Halwani R, Patterson LJ, et al. Antibodies to gp120 and PD-1 expression on virus-specific CD8\+ T-cells in protection from simian AIDS. J Virol 2013; 87:3526-3537.
57. Yeh WW, Brassard LM, Miller CA, et al. Envelope variable region 4 is the first target of neutralizing antibodies in early simian immunodeficiency virus mac251 infection of rhesus monkeys. J Virol 2012; 86:7052-7059.
58. Kurupati R, Tuyishime S, Kossenkov AV, et al. Correlates of relative resistance against low-dose rectal simian immunodeficiency virus challenges in peripheral blood mononuclear cells of vaccinated rhesus macaques. J Leuk Biol 2013; 93:437-448.
59. Hansen SG, Vieville C, Whizin N, 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.
60. Burton DR, Hessell AJ, Keele BF, et al. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc Natl Acad Sci USA 2011; 108:11181-11186.
61. Dobard C, Sharma S, Martin A, et al. Durable protection from vaginal simian-human immunodeficiency virus infection in macaques by tenofovir gel and its relationship to drug levels in tissue. J Virol 2012; 86:718-725.
62. Zheng Q, Ruone S, Switzer WM, et al. Limited SHIV env diversification in macaques failing oral antiretroviral preexposure prophylaxis. Retrovirology 2012; 9:40.
63. Nishimura Y, Martin MA. The acute HIV infection: implications for intervention, prevention and development of an effective AIDS vaccine. Curr Opin Virol 2011; 1:204-210.
64. Del Prete GQ, Scarlotta M, Newman L, et al. Comparative characterization of transfection-and infection-derived siv challenge stocks for in vivo non-human primate studies. J Virol 2013; 87:4584-4595.
65. Sellier P, Mannioui A, Bourry O, et al. Antiretroviral treatment start-time during primary SIV(mac) infection in macaques exerts a different impact on early viral replication and dissemination. PLoS One 2010; 5: e10570.
66. Clements JE, Gama L, Graham DR, et al. A simian immunodeficiency virus macaque model of highly active antiretroviral treatment: viral latency in the periphery and the central nervous system. Curr Opin HIV AIDS 2011; 6:37-42.
67. Kader M, Hassan WM, Eberly M, et al. Antiretroviral therapy prior to acute viral replication preserves CD4 T cells in the periphery but not in rectal mucosa during acute simian immunodeficiency virus infection. J Virol 2008; 82: 11467-11471.
68. 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 1998; 72:4265-4273.
69. Malzahn J, Shen C, Caruso L, et al. Effect of early antiretroviral therapy on the pathogenic changes in mucosal tissues of SIV infected rhesus macaques. Virol J 2012; 9:269.
70. Heneine W, Kashuba A. HIV prevention by oral preexposure prophylaxis. Cold Spring Harbor Perspect Med 2012; 2:a007419.
71. Garcia-Lerma JG, Heneine W. Animal models of antiretroviral prophylaxis for HIV prevention. Curr Opin HIV AIDS 2012; 7:505-513.
72. Girard MP, Plotkin SA. HIV vaccine development at the turn of the 21st century. Curr Opin HIV AIDS 2012; 7:4-9.