High Profile Diseases - Nonhuman Primates and HIV

“High Profile Diseases” are written by individual NPRC Core Scientists who are experts in the specific subject of each article. Before publication on the website, each article is reviewed by representatives of all seven NPRCs.

Nancy L. Haigwood (ONPRC), Andrew Lackner (TNPRC), and R. Paul Johnson (YNPRC)

Improved therapies to treat HIV patients, as well as an effective vaccine to protect uninfected individuals from future HIV infection, are both urgent public health priorities. Important information has come from studying HIV infection and AIDS in humans over the last 30 years, as well as from studying nonhuman primate (NHP) models for AIDS.

HIV infects and kills millions globally. About 36.9 million people worldwide are infected with HIV, and about 1.2 million die of AIDS-related illnesses each year. There were about 2 million new cases in 2014, with about 200,000 new infections in children. In the United States, AIDS disproportionately affects Hispanics, African Americans, and other ethnic minorities (http://www.cdc.gov/hiv/basics/statistics.html).

One of the major issues with HIV, in contrast to viruses that infect their hosts for a few days or weeks, is that it establishes a persistent infection that has been so far impossible to eradicate in humans (with a single notable exception, see below). Combinations of antiretroviral medications can lengthen lives by keeping viral loads at or near undetectable levels in many HIV patients. However, many HIV-infected patients do not have access to antiretroviral medications or are not able to stay on treatment. In addition, these drugs are not curative and progression to AIDS resumes if drug treatment is interrupted. Thus treatment that is started as soon as infection is detected is now the recommended approach to limit disease progression and damage to immune cells (UCSF news article ). Drug treatment in mothers prior to delivery of newborns has greatly reduced transmission from mother to child, but children born to HIV-infected mothers still have a high risk of contracting the infection during birth or via breastfeeding in areas of the world where drug therapy is not available.

African primates are naturally infected with over 40 different simian immunodeficiency viruses (SIV), two of which have infected humans and generated HIV-1 and HIV-2. Chimpanzees are known to be the source of HIV-1 [1], and they, like humans, are variably susceptible to disease [2]. A few HIV patients have been found with genetic variations or other biological mechanisms that appear to naturally control the virus post-infection. These “elite controllers” are extremely uncommon, however, and scientists can only study them in limited ways.

For the last 30 years, the NPRCs have led the way by hosting research programs using NHP models for AIDS that have resulted in critical breakthroughs, as noted in the Key Publications listed below. All NPRCs have active NHP AIDS research programs serving researchers throughout the United States and impacting research progress worldwide. Genetically well-characterized NHPs used in controlled research and animal care settings at the NPRCs have informed researchers about early viral infection, viral escape from host immune responses, and potential vaccine targets. Asian monkeys, such as rhesus, cynomolgus and pig-tailed macaques have served as the flagship, lifesaving models for understanding the basics of infection routes, timing and doses that SIV requires to set up productive, lifelong infections mimicking HIV in humans and providing fundamental information on how SIV and HIV cause disease.

Some of the key lessons learned include knowledge that the immune systems in these animals are analogous to ours, which opens the door to exploring vaccines and immune-based therapies in NHPs. A lab-modified SIV incorporating parts of HIV– simian human immunodeficiency virus (SHIV) – has proved to be a useful tool in the NHP researchers’ arsenal to develop today’s medicines to treat HIV, as well as in the hunt for a vaccine [3]. NPRC researchers have also contributed to the development of using antiviral drugs for pre-exposure and post-exposure prophylaxis, vaginal microbicides [4] to help prevent sexual transmission of HIV to women [5] and safer medicines to prevent HIV transmission from a pregnant woman to her fetus or newborn [6].

There is still a great need for research into more effective treatments for people who already have HIV. Millions of people around the world cannot afford to take antiretroviral drugs to treat HIV, and many countries do not have the resources to provide their citizens with these medicines. Ultimately, researchers aim to find treatments that will result in long-term suppression of HIV infection or a cure for AIDS. Studies in NHP and other animal models have played an important role in showing promising leads in this effort [7]. The single report of an HIV-infected patient who has remained off antiretroviral medication and apparently free of HIV after undergoing a bone marrow transplant to treat leukemia (the Berlin patient—(#15 Hutter NEJM 2009)) has prompted a renaissance of efforts to develop strategies to eradicate HIV and SIV from infected individuals, and testing in NHP models will undoubtedly play a major role in moving these studies forward to human clinical trials.

The ultimate goal of HIV vaccination is to stimulate immunity that will either prevent the virus from getting established or will help to control it, so that drug therapy is not required [8]. Many candidate HIV vaccines have been tested in preclinical NHP models, and the most promising are moving into human clinical trials. The challenge is to find a vaccine that is safe and effective against all strains of the virus. This is critically important because the virus often mutates as it jumps from person to person. HIV not only incorporates itself into the hosts’ genetic material and hijacks their immune system, but viral mutations from infections of a previous host may allow it to overcome drug therapies and immune responses that have previously controlled it. One new approach to vaccination—and possibly treatment-- includes using powerful human HIV-specific monoclonal antibodies [9] or other protective artificial proteins [10] as “gene therapy.” These proteins can be given “passively” or expressed continuously in nonhuman primates and have been shown to prevent infection when these animals are exposed to SHIV or SIV. Human trials of monoclonal antibodies have been proposed [11] and are underway in the setting of pre-exposure and post-exposure [12], based on the success of some of these antibodies in preventing infection in NHP models [13, 14].

Access to better and safer medicines, a prophylactic vaccine, and continuing preventive strategies are all still urgently needed to achieve the goal of and AIDS-free generation. Strategies known to reduce transmission include educating people about condom use, avoiding contaminated needles, using pre-exposure prophylaxis (PrEP), and treating HIV-infected mothers with drugs during labor to limit virus exposure [11]. With effective deployment of prevention and treatment strategies, many experts in the field believe it will be possible to control and stop the AIDS pandemic.

Article References

1. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, et al.
Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes.
Nature. 1999;397(6718):436-41. doi: 10.1038/17130. PubMed PMID: 9989410.

2. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, et al.
Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz.
Nature. 2009;460(7254):515-9. Epub 2009/07/25. doi: nature08200 [pii]10.1038/nature08200. PubMed PMID: 19626114.

3. Hessell AJ, Haigwood NL.
Animal models in HIV-1 protection and therapy.
Curr Opin HIV AIDS. 2015. doi: 10.1097/COH.0000000000000152. PubMed PMID: 25730345.

4. Veazey RS.
Microbicide safety/efficacy studies in animals: macaques and small animal models.
Curr Opin HIV AIDS. 2008;3(5):567-73. Epub 2009/04/18. doi: 10.1097/COH.0b013e32830891bb01222929-200809000-00008 [pii]. PubMed PMID: 19373023.

5. Abdool Karim Q, Abdool Karim SS, Frohlich JA, Grobler AC, Baxter C, Mansoor LE, et al.
Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women.
Science. 2010;329(5996):1168-74. doi: 10.1126/science.1193748. PubMed PMID: 20643915; PubMed Central PMCID: PMCPMC3001187.

6. Van Rompay KK, Berardi CJ, Aguirre NL, Bischofberger N, Lietman PS, Pedersen NC, et al.
Two doses of PMPA protect newborn macaques against oral simian immunodeficiency virus infection.
AIDS. 1998;12(9):F79-83. PubMed PMID: 9662190.

7. Hansen SG, Piatak M, Jr., Ventura AB, Hughes CM, Gilbride RM, Ford JC, et al.
Immune clearance of highly pathogenic SIV infection.
Nature. 2013;502(7469):100-4. Epub 2013/09/13. doi: 10.1038/nature12519. PubMed PMID: 24025770; PubMed Central PMCID: PMC3849456.

8. Picker LJ, Hansen SG, Lifson JD.
New paradigms for HIV/AIDS vaccine development.
Annu Rev Med. 2012;63:95-111. Epub 2011/09/29. doi: 10.1146/annurev-med-042010-085643. PubMed PMID: 21942424.

9. Johnson PR, Schnepp BC, Zhang J, Connell MJ, Greene SM, Yuste E, et al.
Vector-mediated gene transfer engenders long-lived neutralizing activity and protection against SIV infection in monkeys.
Nat Med. 2009. Epub 2009/05/19. doi: nm.1967 [pii]10.1038/nm.1967. PubMed PMID: 19448633.

10. Gardner MR, Kattenhorn LM, Kondur HR, von Schaewen M, Dorfman T, Chiang JJ, et al.
AAV-expressed eCD4-Ig provides durable protection from multiple SHIV challenges.
Nature. 2015;519(7541):87-91. doi: 10.1038/nature14264. PubMed PMID: 25707797; PubMed Central PMCID: PMCPMC4352131.

11. Voronin Y, Mofenson LM, Cunningham CK, Fowler MG, Kaleebu P, McFarland EJ, et al.
HIV monoclonal antibodies: a new opportunity to further reduce mother-to-child HIV transmission.
PLoS Med. 2014;11(4):e1001616. doi: 10.1371/journal.pmed.1001616. PubMed PMID: 24714363; PubMed Central PMCID: PMCPMC3979646.

12. Ledgerwood JE, Coates EE, Yamshchikov G, Saunders JG, Holman L, Enama ME, et al.
Safety, Pharmacokinetics, and Neutralization of the Broadly Neutralizing HIV-1 Human Monoclonal Antibody VRC01 in Healthy Adults.
Clin Exp Immunol. 2015. doi: 10.1111/cei.12692. PubMed PMID: 26332605.

13. Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, Liu J, et al.
Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys.
Nature. 2013;503(7475):224-8. doi: 10.1038/nature12744. PubMed PMID: 24172905; PubMed Central PMCID: PMCPMC4017780.

14. Shingai M, Nishimura Y, Klein F, Mouquet H, Donau OK, Plishka R, et al.
Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia.
Nature. 2013;503(7475):277-80. doi: 10.1038/nature12746. PubMed PMID: 24172896; PubMed Central PMCID: PMCPMC4133787.

15. Hutter G, Nowak D, Mossner M, Ganepola S, Mussig A, et al. (2009)
Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation.
The New England journal of medicine 360: 692–698. doi: 10.1056/nejmoa0802905. PubMed PMID: 19213682

Recent NPRC Publications

There are currently 657 publications available for HIV, SIV, SHIV, and AIDS.

2017

Anderson DJ, Politch JA, Zeitlin L, Hiatt A, Kadasia K, Mayer KH, Ruprecht RM, Villinger F, Whaley KJ.
Systemic and topical use of monoclonal antibodies to prevent the sexual transmission of HIV.
AIDS 2017 Jul; 31(11): 1505-1517.

Chang WL, Gonzalez DF, Kieu HT, Castillo LD, Messaoudi I, Shen X, Tomaras GD, Shacklett BL, Barry PA, Sparger EE.
Changes in Circulating B Cell Subsets Associated with Aging and Acute SIV Infection in Rhesus Macaques.
PLoS ONE 2017 01; 12(1): e0170154.

Daggett GJ, Zhao C, Connor-Stroud F, Oviedo-Moreno P, Moon H, Cho MW, Moench T, Anderson DJ, Villinger F.
Comparison of the vaginal environment in rhesus and cynomolgus macaques pre- and post-lactobacillus colonization.
J. Med. Primatol. 2017 May; (): .

Feder AF, Kline C, Polacino P, Cottrell M, Kashuba ADM, Keele BF, Hu SL, Petrov DA, Pennings PS, Ambrose Z.
A spatio-temporal assessment of simian/human immunodeficiency virus (SHIV) evolution reveals a highly dynamic process within the host.
PLoS Pathog. 2017 May; 13(5): e1006358.

Kasturi SP, Kozlowski PA, Nakaya HI, Burger MC, Russo P, Pham M, Kovalenkov Y, Silveira EL, Havenar-Daughton C, Burton SL, Kilgore KM, Johnson MJ, Nabi R, Legere T, Sher ZJ, Chen X, Amara RR, Hunter E, Bosinger SE, Spearman P, Crotty S, Villinger F, Derdeyn CA, Wrammert J, Pulendran B.
Adjuvanting a Simian Immunodeficiency Virus Vaccine with Toll-Like Receptor Ligands Encapsulated in Nanoparticles Induces Persistent Antibody Responses and Enhanced Protection in TRIM5α Restrictive Macaques.
J. Virol. 2017 Feb; 91(4): .

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Key HIV/AIDS Publications

Pre-2009

Baba TW, Jeong YS, Penninck D, Bronson R, Greene MF, Ruprecht RM.
Pathogenicity of live, attenuated SIV after mucosal infection of neonatal macaques.
Science. 1995;267:1820-5.

Barouch DH, Santra S, Schmitz JE, Kuroda MJ, Fu TM, Wagner W, et al.
Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination.
Science. 2000;290(5491):486-92. Epub 2000/10/20. doi: 8915 [pii]. PubMed PMID: 11039923.

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;228:1201-4.

Harouse JM, Gettie A, Tan RCH, Blanchard J, Cheng-Mayer C.
Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs.
Science. 1999;284:816-8.

Hu S-L, Abrams K, Barber GN, Moran P, Zarling JM, Langlois AJ, et al.
Protection of macaques against SIV infection by subunit vaccines of SIV envelope glycoprotein gp160.
Science. 1992;255:456-9.

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.
Journal of Virology. 1999;73(6):4952-61.

Letvin NL, Eaton KA, Aldrich WR, Sehgal PK, Blake BJ, Schlossman SF, et al.
Acquired immunodeficiency syndrome in a colony of macaque monkeys.
Proc Natl Acad Sci U S A. 1983;80(9):2718-22. Epub 1983/05/01. PubMed PMID: 6221343; PubMed Central PMCID: PMC393899.

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(14):9217-27. PubMed PMID: 15994816.

Paiardini M, Pandrea I, Apetrei C, Silvestri G.
Lessons learned from the natural hosts of HIV-related viruses.
Annu Rev Med. 2009;60:485-95. Epub 2009/07/28. doi: 10.1146/annurev.med.60.041807.123753. PubMed PMID: 19630581.

Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, et al.
Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes.
Science. 1999;283(5403):857-60. Epub 1999/02/05. PubMed PMID: 9933172.

Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL, et al.
Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection.
Science. 1998;280(5362):427-31. PubMed PMID: 9545219.

Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL, Rosenzweig M, Johnson RP, Desrosiers RC, Lackner AA.
Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection.
Science. 1998;280:427-31.

Wyand MS, Manson KH, Lackner AA, Desrosiers RC.
Resistance of neonatal monkeys to live attenuated vaccine strains of simian immunodeficiency virus.
Nature Medicine. 1997;3:32-6.

Zhang Z, Schuler T, Zupancic M, Wietgrefe S, Staskus KA, Reimann KA, et al.
Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells.
Science. 1999;286(5443):1353-7. PubMed PMID: 10558989.

2009

Beaumier CM, Harris LD, Goldstein S, Klatt NR, Whitted S, McGinty J, et al.
CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection.
Nat Med. 2009;15(8):879-85. doi: 10.1038/nm.1970. PubMed PMID: 19525963; PubMed Central PMCID: PMCPMC2723181.

Hessell AJ, Poignard P, Hunter M, Hangartner L, Tehrani DM, Bleeker WK, et al.
Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques.
Nat Med. 2009;15(8):951-4. Epub 2009/06/16. doi: 10.1038/nm.1974. PubMed PMID: 19525965.

Johnson PR, Schnepp BC, Zhang J, Connell MJ, Greene SM, Yuste E, et al.
Vector-mediated gene transfer engenders long-lived neutralizing activity and protection against SIV infection in monkeys.
Nat Med. 2009. Epub 2009/05/19. doi: nm.1967 [pii]10.1038/nm.1967. PubMed PMID: 19448633.

Li Q, Skinner PJ, Ha SJ, Duan L, Mattila TL, Hage A, et al.
Visualizing antigen-specific and infected cells in situ predicts outcomes in early viral infection.
Science. 2009;323(5922):1726-9. Epub 2009/03/28. doi: 323/5922/1726 [pii] 10.1126/science.1168676. PubMed PMID: 19325114; PubMed Central PMCID: PMC2753492.

Liu J, O'Brien KL, Lynch DM, Simmons NL, La Porte A, Riggs AM, et al.
Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys.
Nature. 2009;457(7225):87-91. Epub 2008/11/11. doi: nature07469 [pii] 10.1038/nature07469. PubMed PMID: 18997770; PubMed Central PMCID: PMC2614452.

Sacha JB, Giraldo-Vela JP, Buechler MB, Martins MA, Maness NJ, Chung C, et al.
Gag- and Nef-specific CD4+ T cells recognize and inhibit SIV replication in infected macrophages early after infection.
Proc Natl Acad Sci U S A. 2009;106(24):9791-6. Epub 2009/05/30. doi: 10.1073/pnas.0813106106. PubMed PMID: 19478057; PubMed Central PMCID: PMC2687996.

Velu V, Titanji K, Zhu B, Husain S, Pladevega A, Lai L, et al.
Enhancing SIV-specific immunity in vivo by PD-1 blockade.
Nature. 2009;458(7235):206-10. Epub 2008/12/17. doi: nature07662 [pii] 10.1038/nature07662. PubMed PMID: 19078956.

2010

Barouch DH, O'Brien KL, Simmons NL, King SL, Abbink P, Maxfield LF, et al.
Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys.
Nat Med. 2010;16(3):319-23. doi: 10.1038/nm.2089. PubMed PMID: 20173752; PubMed Central PMCID: PMCPMC2834868.

Garcia-Lerma JG, Cong ME, Mitchell J, Youngpairoj AS, Zheng Q, Masciotra S, et al.
Intermittent prophylaxis with oral truvada protects macaques from rectal SHIV infection.
Sci Transl Med. 2010;2(14):14ra4. doi: 10.1126/scitranslmed.3000391. PubMed PMID: 20371467.

Kirmaier A, Wu F, Newman RM, Hall LR, Morgan JS, O'Connor S, et al.
TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species.
PLoS Biol. 2010;8(8). doi: 10.1371/journal.pbio.1000462. PubMed PMID: 20808775; PubMed Central PMCID: PMCPMC2927514.

Ng CT, Jaworski JP, Jayaraman P, Sutton WF, Delio P, Kuller L, et al.
Passive neutralizing antibody controls SHIV viremia and enhances B cell responses in infant macaques.
Nat Med. 2010;16(10):1117-9. Epub 2010/10/05. doi: nm.2233 [pii] 10.1038/nm.2233. PubMed PMID: 20890292; PubMed Central PMCID: PMC2952052.

Shingai M, Nishimura Y, Klein F, Mouquet H, Donau OK, Plishka R, et al.
Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia.
Nature. 2013;503(7475):277-80. doi: 10.1038/nature12746. PubMed PMID: 24172896; PubMed Central PMCID: PMCPMC4133787.

Wang X, Xu H, Pahar B, Alvarez X, Green LC, Dufour J, et al.
Simian immunodeficiency virus selectively infects proliferating CD4+ T cells in neonatal rhesus macaques.
Blood. 2010;116(20):4168-74. doi: 10.1182/blood-2010-03-273482. PubMed PMID: 20716768; PubMed Central PMCID: PMCPMC2993622.

Worobey M, Telfer P, Souquiere S, Hunter M, Coleman CA, Metzger MJ, et al.
Island biogeography reveals the deep history of SIV.
Science. 2010;329(5998):1487. doi: 10.1126/science.1193550. PubMed PMID: 20847261.

2011

Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, Moldt B, 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 U S A. 2011;108(27):11181-6. doi: 10.1073/pnas.1103012108. PubMed PMID: 21690411; PubMed Central PMCID: PMCPMC3131343.

Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, Coyne-Johnson L, et al.
Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine.
Nature. 2011;473(7348):523-7. Epub 2011/05/13. doi: 10.1038/nature10003. PubMed PMID: 21562493; PubMed Central PMCID: PMC3102768.

Ortiz AM, Klatt NR, Li B, Yi Y, Tabb B, Hao XP, et al.
Depletion of CD4 T cells abrogates post-peak decline of viremia in SIV-infected rhesus macaques.
J Clin Invest. 2011;121(11):4433-45. Epub 2011/10/19. doi: 10.1172/JCI46023. PubMed PMID: 22005304; PubMed Central PMCID: PMC3204830.

Paiardini M, Cervasi B, Reyes-Aviles E, Micci L, Ortiz AM, Chahroudi A, et al.
Low levels of SIV infection in sooty mangabey central memory CD(4)(+) T cells are associated with limited CCR5 expression.
Nat Med. 2011;17(7):830-6. doi: 10.1038/nm.2395. PubMed PMID: 21706028; PubMed Central PMCID: PMCPMC3253129.

2012

Chahroudi A, Bosinger SE, Vanderford TH, Paiardini M, Silvestri G.
Natural SIV hosts: showing AIDS the door.
Science. 2012;335(6073):1188-93. doi: 10.1126/science.1217550. PubMed PMID: 22403383; PubMed Central PMCID: PMCPMC3822437.

Fukazawa Y, Park H, Cameron MJ, Lefebvre F, Lum R, Coombes N, et al.
Lymph node T cell responses predict the efficacy of live attenuated SIV vaccines.
Nat Med. 2012;18(11):1673-81. Epub 2012/09/11. doi: 10.1038/nm.2934. PubMed PMID: 22961108; PubMed Central PMCID: PMC3493820.

Genesca M, Ma ZM, Wang Y, Assaf B, Qureshi H, Fritts L, et al.
Live-attenuated lentivirus immunization modulates innate immunity and inflammation while protecting rhesus macaques from vaginal simian immunodeficiency virus challenge.
J Virol. 2012;86(17):9188-200. doi: 10.1128/JVI.00532-12. PubMed PMID: 22696662; PubMed Central PMCID: PMCPMC3416105.

Handley SA, Thackray LB, Zhao G, Presti R, Miller AD, Droit L, et al.
Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome.
Cell. 2012;151(2):253-66. doi: 10.1016/j.cell.2012.09.024. PubMed PMID: 23063120; PubMed Central PMCID: PMCPMC3490196.

Mudd PA, Martins MA, Ericsen AJ, Tully DC, Power KA, Bean AT, et al.
Vaccine-induced CD8+ T cells control AIDS virus replication.
Nature. 2012;491(7422):129-33. doi: 10.1038/nature11443. PubMed PMID: 23023123; PubMed Central PMCID: PMCPMC3883109.

2013

Barouch DH, Stephenson KE, Borducchi EN, Smith K, Stanley K, McNally AG, et al.
Protective efficacy of a global HIV-1 mosaic vaccine against heterologous SHIV challenges in rhesus monkeys.
Cell. 2013;155(3):531-9. doi: 10.1016/j.cell.2013.09.061. PubMed PMID: 24243013; PubMed Central PMCID: PMCPMC3846288.

Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, Liu J, et al.
Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys.
Nature. 2013;503(7475):224-8. doi: 10.1038/nature12744. PubMed PMID: 24172905; PubMed Central PMCID: PMCPMC4017780.

Hansen SG, Piatak M, Jr., Ventura AB, Hughes CM, Gilbride RM, Ford JC, et al.
Immune clearance of highly pathogenic SIV infection.
Nature. 2013;502(7469):100-4. Epub 2013/09/13. doi: 10.1038/nature12519. PubMed PMID: 24025770; PubMed Central PMCID: PMC3849456.

Hansen SG, Sacha JB, Hughes CM, Ford JC, Burwitz BJ, Scholz I, et al.
Cytomegalovirus vectors violate CD8+ T cell epitope recognition paradigms.
Science. 2013;340(6135):1237874. Epub 2013/05/25. doi: 10.1126/science.1237874. PubMed PMID: 23704576; PubMed Central PMCID: PMC3816976.

Jaworski JP, Kobie J, Brower Z, Malherbe DC, Landucci G, Sutton WF, et al.
Neutralizing polyclonal IgG present during acute infection prevents rapid disease onset in simian-human immunodeficiency virus SHIVSF162P3-infected infant rhesus macaques.
J Virol. 2013;87(19):10447-59. doi: 10.1128/JVI.00049-13. PubMed PMID: 23885083; PubMed Central PMCID: PMCPMC3807376.

2014

Andrews CD, Spreen WR, Mohri H, Moss L, Ford S, Gettie A, Russell-Lodrigue K, Bohm RP, Cheng-Mayer C, Hong Z, Markowitz M, Ho DD.
Long-acting integrase inhibitor protects macaques from intrarectal simian/human immunodeficiency virus.
Science. 2014;343(6175):1151-4. PMCID: PMC4308974.

Chahroudi A, Cartwright E, Lee ST, Mavigner M, Carnathan DG, Lawson B, et al.
Target cell availability, rather than breast milk factors, dictates mother-to-infant transmission of SIV in sooty mangabeys and rhesus macaques.
PLoS Pathog. 2014;10(3):e1003958. doi: 10.1371/journal.ppat.1003958. PubMed PMID: 24604066; PubMed Central PMCID: PMCPMC3946396.

Mavigner M, Watkins B, Lawson B, Lee ST, Chahroudi A, Kean L, et al.
Persistence of virus reservoirs in ART-treated SHIV-infected rhesus macaques after autologous hematopoietic stem cell transplant.
PLoS Pathog. 2014;10(9):e1004406. doi: 10.1371/journal.ppat.1004406. PubMed PMID: 25254512; PubMed Central PMCID: PMC4177994.

Sandler NG, Bosinger SE, Estes JD, Zhu RT, Tharp GK, Boritz E, et al.
Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression.
Nature. 2014;511(7511):601-5. doi: 10.1038/nature13554. PubMed PMID: 25043006; PubMed Central PMCID: PMCPMC4418221.

2015

Barouch DH, Alter G, Broge T, Linde C, Ackerman ME, Brown EP, et al.
Protective efficacy of adenovirus-protein vaccines against SIV challenges in rhesus monkeys.
Science. 2015. doi: 10.1126/science.aab3886. PubMed PMID: 26138104.

Dinh MH, Anderson MR, McRaven MD, Cianci GC, McCoombe SG, Kelley ZL, et al.
Visualization of HIV-1 interactions with penile and foreskin epithelia: clues for female-to-male HIV transmission.
PLoS Pathog. 2015;11(3):e1004729. doi: 10.1371/journal.ppat.1004729. PubMed PMID: 25748093; PubMed Central PMCID: PMCPMC4352059.

Gardner MR, Kattenhorn LM, Kondur HR, von Schaewen M, Dorfman T, Chiang JJ, et al.
AAV-expressed eCD4-Ig provides durable protection from multiple SHIV challenges.
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