Human immunodeficiency virus type 1 monoclonal antibodies suppress acute simian-human immunodeficiency virus viremia and limit seeding of cell-associated viral reservoirs

Journal of Virology

Volumn 90, Issue 3, 2016, Pages 1321-1332

  Bolton, Diane L ^a,b   Pegu, Amarendra ^c   Wang, Keyun ^c   McGinnis, Kathleen ^c   Nason, Martha ^c   Foulds, Kathryn ^c   Letukas, Valerie ^c   Schmidt, Stephen D ^c   Chen, Xuejun ^c   Todd, John Paul ^c   Lifson, Jeffrey D ^d   Rao, Srinivas ^c,e   Michael, Nelson L ^a   Robb, Merlin L ^a,b   Mascola, John R ^c   Koup, Richard A ^c  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^e NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; ANTIVIRUS AGENT; CD4 ANTIGEN; EMTRICITABINE; GLYCOPROTEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY PGT121; MONOCLONAL ANTIBODY VRC01; MONOCLONAL ANTIBODY VRC07 523; NEUTRALIZING ANTIBODY; RALTEGRAVIR; TENOFOVIR; UNCLASSIFIED DRUG; VIRUS DNA; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENCY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; LENTIVIRINAE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN HUMAN IMMUNODEFICIENCY VIRUS; SINGLE DRUG DOSE; TREATMENT DURATION; VIREMIA; VIRUS LOAD; VIRUS NEUTRALIZATION; VIRUS REPLICATION; ANIMAL; GENETICS; HUMAN; IMMUNOLOGY; PASSIVE IMMUNIZATION; PROVIRUS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; CD4-POSITIVE T-LYMPHOCYTES; DNA, VIRAL; HIV ANTIBODIES; HIV-1; HUMANS; IMMUNIZATION, PASSIVE; MACACA MULATTA; PROVIRUSES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA;

EID: 84958093143     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02454-15     Document Type: Article

References (48)

1. Archin NM, Vaidya NK, Kuruc JD, Liberty AL, Wiegand A, Kearney MF, Cohen MS, Coffin JM, Bosch RJ, Gay CL, Eron JJ, Margolis DM, Perelson AS. 2012. Immediate antiviral therapy appears to restrict resting CD4+cell HIV-1 infection without accelerating the decay of latent infection. Proc Natl Acad Sci U S A 109:9523-9528. http://dx.doi.org/10.1073/pnas.1120248109.
2. Ananworanich J, Schuetz A, Vandergeeten C, Sereti I, de Souza M, Rerknimitr R, Dewar R, Marovich M, van Griensven F, Sekaly R, Pinyakorn S, Phanuphak N, Trichavaroj R, Rutvisuttinunt W, Chomchey N, Paris R, Peel S, Valcour V, Maldarelli F, Chomont N, Michael N, Phanuphak P, Kim JH, RV254/SEARCH 010 Study Group. 2012. Impact of multi-targeted antiretroviral treatment on gut T cell depletion and HIV reservoir seeding during acute HIV infection. PLoS One 7:e33948. http://dx.doi.org/10.1371/journal.pone.0033948.
3. Whitney JB, Hill AL, Sanisetty S, Penaloza-MacMaster P, Liu J, Shetty M, Parenteau L, Cabral C, Shields J, Blackmore S, Smith JY, Brinkman AL, Peter LE, Mathew SI, Smith KM, Borducchi EN, Rosenbloom DI, Lewis MG, Hattersley J, Li B, Hesselgesser J, Geleziunas R, Robb ML, Kim JH, Michael NL, Barouch DH. 2014. Rapid seeding of the viral reservoir prior to SIV viraemia in rhesus monkeys. Nature 512:74-77. http://dx.doi.org/10.1038/nature13594.
4. Sung JA, Lam S, Garrido C, Archin N, Rooney CM, Bollard CM, Margolis DM. 2015. Expanded cytotoxic T-cell lymphocytes target the latent HIV reservoir. J Infect Dis 212:258-263. http://dx.doi.org/10.1093/infdis/jiv022.
5. Archin NM, Margolis DM. 2014. Emerging strategies to deplete the HIV reservoir. Curr Opin Infect Dis 27:29-35. http://dx.doi.org/10.1097/QCO.0000000000000026.
6. Deng K, Pertea M, Rongvaux A, Wang L, Durand CM, Ghiaur G, Lai J, McHugh HL, Hao H, Zhang H, Margolick JB, Gurer C, Murphy AJ, Valenzuela DM, Yancopoulos GD, Deeks SG, Strowig T, Kumar P, Siliciano JD, Salzberg SL, Flavell RA, Shan L, Siliciano RF. 2015. Broad CTL response is required to clear latent HIV-1 due to dominance of escape mutations. Nature 517:381-385. http://dx.doi.org/10.1038/nature14053.
7. Denton PW, Long JM, Wietgrefe SW, Sykes C, Spagnuolo RA, Snyder OD, Perkey K, Archin NM, Choudhary SK, Yang K, Hudgens MG, Pastan I, Haase AT, Kashuba AD, Berger EA, Margolis DM, Garcia JV. 2014. Targeted cytotoxic therapy kills persisting HIV infected cells during ART. PLoS Pathog 10:e1003872. http://dx.doi.org/10.1371/journal.ppat.1003872.
8. Ananworanich J, McSteen B, Robb ML. 2015. Broadly neutralizing antibody and the HIV reservoir in acute HIV infection: a strategy toward HIV remission? Curr Opin HIV AIDS 10:198-206. http://dx.doi.org/10.1097/COH.0000000000000144.
9. Kwong PD, Mascola JR. 2012. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37:412-425. http://dx.doi.org/10.1016/j.immuni.2012.08.012.
10. Burton DR, Poignard P, Stanfield RL, Wilson IA. 2012. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 337:183-186. http://dx.doi.org/10.1126/science.1225416.
11. West AP, Jr, Scharf L, Scheid JF, Klein F, Bjorkman PJ, Nussenzweig MC. 2014. Structural insights on the role of antibodies in HIV-1 vaccine and therapy. Cell 156:633-648. http://dx.doi.org/10.1016/j.cell.2014.01.052.
12. Lewis GK. 2014. Role of Fc-mediated antibody function in protective immunity against HIV-1. Immunology 142:46-57. http://dx.doi.org/10.1111/imm.12232.
13. Milligan C, Richardson BA, John-Stewart G, Nduati R, Overbaugh J. 2015. Passively acquired antibody-dependent cellular cytotoxicity (ADCC) activity in HIV-infected infants is associated with reduced mortality. Cell Host Microbe 17:500-506. http://dx.doi.org/10.1016/j.chom.2015.03.002.
14. Ackerman ME, Alter G. 2013. Opportunities to exploit non-neutralizing HIV-specific antibody activity. Curr HIV Res 11:365-377. http://dx.doi.org/10.2174/1570162X113116660058.
15. Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, Liu J, Stephenson KE, Chang HW, Shekhar K, Gupta S, Nkolola JP, Seaman MS, Smith KM, Borducchi EN, Cabral C, Smith JY, Blackmore S, Sanisetty S, Perry JR, Beck M, Lewis MG, Rinaldi W, Chakraborty AK, Poignard P, Nussenzweig MC, Burton DR. 2013. Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIVinfected rhesus monkeys. Nature 503:224-228. http://dx.doi.org/10.1038/nature12744.
16. Klein F, Halper-Stromberg A, Horwitz JA, Gruell H, Scheid JF, Bournazos S, Mouquet H, Spatz LA, Diskin R, Abadir A, Zang T, Dorner M, Billerbeck E, Labitt RN, Gaebler C, Marcovecchio PM, Incesu RB, Eisenreich TR, Bieniasz PD, Seaman MS, Bjorkman PJ, Ravetch JV, Ploss A, Nussenzweig MC. 2012. HIV therapy by a combination of broadly neutralizing antibodies in humanized mice. Nature 492:118-122. http://dx.doi.org/10.1038/nature11604.
17. Shingai M, Nishimura Y, Klein F, Mouquet H, Donau OK, Plishka R, Buckler-White A, Seaman M, Piatak M, Jr, Lifson JD, Dimitrov DS, Nussenzweig MC, Martin MA. 2013. Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503:277-280. http://dx.doi.org/10.1038/nature12746.
18. Moldt B, Rakasz EG, Schultz N, Chan-Hui PY, Swiderek K, Weisgrau KL, Piaskowski SM, Bergman Z, Watkins DI, Poignard P, Burton DR. 2012. Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proc Natl Acad Sci U S A 109:18921-18925. http://dx.doi.org/10.1073/pnas.1214785109.
19. Mascola JR, Stiegler G, VanCott TC, Katinger H, Carpenter CB, Hanson CE, Beary H, Hayes D, Frankel SS, Birx DL, Lewis MG. 2000. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat Med 6:207-210. http://dx.doi.org/10.1038/72318.
20. Mascola JR, Lewis MG, Stiegler G, Harris D, VanCott TC, Hayes D, Louder MK, Brown CR, Sapan CV, Frankel SS, Lu Y, Robb ML, Katinger H, Birx DL. 1999. Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J Virol 73:4009-4018.
21. Cavacini LA, Samore MH, Gambertoglio J, Jackson B, Duval M, Wisnewski A, Hammer S, Koziel C, Trapnell C, Posner MR. 1998. Phase I study of a human monoclonal antibody directed against the CD4-binding site of HIV type 1 glycoprotein 120. AIDS Res Hum Retroviruses 14:545-550. http://dx.doi.org/10.1089/aid.1998.14.545.
22. Armbruster C, Stiegler GM, Vcelar BA, Jager W, Michael NL, Vetter N, Katinger HW. 2002. A phase I trial with two human monoclonal antibodies (hMAb 2F5, 2G12) against HIV-1. AIDS 16:227-233. http://dx.doi.org/10.1097/00002030-200201250-00012.
23. Armbruster C, Stiegler GM, Vcelar BA, Jager W, Koller U, Jilch R, Ammann CG, Pruenster M, Stoiber H, Katinger HW. 2004. Passive immunization with the anti-HIV-1 human monoclonal antibody (hMAb) 4E10 and the hMAb combination 4E10/2F5/2G12. J Antimicrob Chemother 54:915-920. http://dx.doi.org/10.1093/jac/dkh428.
24. Trkola A, Kuster H, Rusert P, Joos B, Fischer M, Leemann C, Manrique A, Huber M, Rehr M, Oxenius A, Weber R, Stiegler G, Vcelar B, Katinger H, Aceto L, Gunthard HF. 2005. Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat Med 11:615-622. http://dx.doi.org/10.1038/nm1244.
25. Mehandru S, Vcelar B, Wrin T, Stiegler G, Joos B, Mohri H, Boden D, Galovich J, Tenner-Racz K, Racz P, Carrington M, Petropoulos C, Katinger H, Markowitz M. 2007. Adjunctive passive immunotherapy in human immunodeficiency virus type 1-infected individuals treated with antiviral therapy during acute and early infection. J Virol 81:11016-11031. http://dx.doi.org/10.1128/JVI.01340-07.
26. Matsushita S, Yoshimura K, Ramirez KP, Pisupati J, Murakami T, KD-1002 Study Group. 2015. Passive transfer of neutralizing mAb KD-247 reduces plasma viral load in patients chronically infected with HIV-1. AIDS 29:453-462. http://dx.doi.org/10.1097/QAD.0000000000000570.
27. Ledgerwood JE, Coates EE, Yamshchikov G, Saunders JG, Holman L, Enama ME, DeZure A, Lynch R, Gordon I, Plummer S, Hendel CS, Pegu A, Conan-Cibotti M, Sitar S, Bailer RT, Narpala S, McDermott A, Louder M, O'Dell S, Mohan S, Pandey JP, Schwartz RM, Hu Z, Koup RA, Capparelli E, Mascola JR, Graham BS, VRC 602 Study Team. 2015. Safety, pharmacokinetics, and neutralization of the broadly neutralizing HIV-1 human monoclonal antibody VRC01 in healthy adults. Clin Exp Immunol 182:289-301. http://dx.doi.org/10.1111/cei.12692.
28. Caskey M, Klein F, Lorenzi JC, Seaman MS, West AP, Jr, Buckley N, Kremer G, Nogueira L, Braunschweig M, Scheid JF, Horwitz JA, Shimeliovich I, Ben-Avraham S, Witmer-Pack M, Platten M, Lehmann C, Burke LA, Hawthorne T, Gorelick RJ, Walker BD, Keler T, Gulick RM, Fatkenheuer G, Schlesinger SJ, Nussenzweig MC. 2015. Viraemia suppressed in HIV-1-infected humans by broadly neutralizing antibody 3BNC117. Nature 522:487-491. http://dx.doi.org/10.1038/nature14411.
29. Rudicell RS, Kwon YD, Ko SY, Pegu A, Louder MK, Georgiev IS, Wu X, Zhu J, Boyington JC, Chen X, Shi W, Yang ZY, Doria-Rose NA, McKee K, O'Dell S, Schmidt SD, Chuang GY, Druz A, Soto C, Yang Y, Zhang B, Zhou T, Todd JP, Lloyd KE, Eudailey J, Roberts KE, Donald BR, Bailer RT, Ledgerwood J, NISC Comparative Sequencing Program, Mullikin JC, Shapiro L, Koup RA, Graham BS, Nason MC, Connors M, Haynes BF, Rao SS, Roederer M, Kwong PD, Mascola JR, Nabel GJ. 2014. Enhanced potency of a broadly neutralizing HIV-1 antibody in vitro improves protection against lentiviral infection in vivo. J Virol 88:12669-12682. http://dx.doi.org/10.1128/JVI.02213-14.
30. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, Longo NS, McKee K, O'Dell S, Louder MK, WycuffDL, Feng Y, Nason M, Doria-Rose N, Connors M, Kwong PD, Roederer M, Wyatt RT, Nabel GJ, Mascola JR. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861. http://dx.doi.org/10.1126/science.1187659.
31. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien JP, Wang SK, Ramos A, Chan-Hui PY, Moyle M, Mitcham JL, Hammond PW, Olsen OA, Phung P, Fling S, Wong CH, Phogat S, Wrin T, Simek MD, Protocol G Principal Investigators, KoffWC, Wilson IA, Burton DR, Poignard P. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470. http://dx.doi.org/10.1038/nature10373.
32. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academies Press, Washington, DC.
33. Zhou T, Zhu J, Yang Y, Gorman J, Ofek G, Srivatsan S, Druz A, Lees CR, Lu G, Soto C, Stuckey J, Burton DR, KoffWC, Connors M, Kwong PD. 2014. Transplanting supersites of HIV-1 vulnerability. PLoS One 9:e99881. http://dx.doi.org/10.1371/journal.pone.0099881.
34. Wu X, Wang C, O'Dell S, Li Y, Keele BF, Yang Z, Imamichi H, Doria-Rose N, Hoxie JA, Connors M, Shaw GM, Wyatt RT, Mascola JR. 2012. Selection pressure on HIV-1 envelope by broadly neutralizing antibodies to the conserved CD4-binding site. J Virol 86:5844-5856. http://dx.doi.org/10.1128/JVI.07139-11.
35. Catanzaro AT, Roederer M, Koup RA, Bailer RT, Enama ME, Nason MC, Martin JE, Rucker S, Andrews CA, Gomez PL, Mascola JR, Nabel GJ, Graham BS, VRC 007 Study Team. 2007. Phase I clinical evaluation of a six-plasmid multiclade HIV-1 DNA candidate vaccine. Vaccine 25: 4085-4092. http://dx.doi.org/10.1016/j.vaccine.2007.02.050.
36. Foulds KE, Donaldson M, Roederer M. 2012. OMIP-005: quality and phenotype of antigen-responsive rhesus macaque T cells. Cytometry A 81:360-361. http://dx.doi.org/10.1002/cyto.a.22008.
37. Nishimura Y, Sadjadpour R, Mattapallil JJ, Igarashi T, Lee W, Buckler-White A, Roederer M, Chun TW, Martin MA. 2009. High frequencies of resting CD4+T cells containing integrated viral DNA are found in rhesus macaques during acute lentivirus infections. Proc Natl Acad Sci U S A 106:8015-8020. http://dx.doi.org/10.1073/pnas.0903022106.
38. Cline AN, Bess JW, Piatak M, Jr, Lifson JD. 2005. Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J Med Primatol 34:303-312. http://dx.doi.org/10.1111/j.1600-0684.2005.00128.x.
39. Pegu A, Yang ZY, Boyington JC, Wu L, Ko SY, Schmidt SD, McKee K, Kong WP, Shi W, Chen X, Todd JP, Letvin NL, Huang J, Nason MC, Hoxie JA, Kwong PD, Connors M, Rao SS, Mascola JR, Nabel GJ. 2014. Neutralizing antibodies to HIV-1 envelope protect more effectively in vivo than those to the CD4 receptor. Sci Transl Med 6:243ra288. http://dx.doi.org/10.1126/scitranslmed.3008992.
40. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, HoffST, Andersen P, Reed SG, Morris SL, Roederer M, Seder RA. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 13:843-850. http://dx.doi.org/10.1038/nm1592.
41. Seder RA, Darrah PA, Roederer M. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 8:247-258. http://dx.doi.org/10.1038/nri2274.
42. Wu CY, Kirman JR, Rotte MJ, Davey DF, Perfetto SP, Rhee EG, Freidag BL, Hill BJ, Douek DC, Seder RA. 2002. Distinct lineages of T(H)1 cells have differential capacities for memory cell generation in vivo. Nat Immunol 3:852-858. http://dx.doi.org/10.1038/ni832.
43. Saunders KO, Pegu A, Georgiev IS, Zeng M, Joyce MG, Yang ZY, Ko SY, Chen X, Schmidt SD, Haase AT, Todd JP, Bao S, Kwong PD, Rao SS, Mascola JR, Nabel GJ. 2015. Sustained delivery of a broadly neutralizing antibody in nonhuman primates confers long-term protection against simian/human immunodeficiency virus infection. J Virol 89: 5895-5903. http://dx.doi.org/10.1128/JVI.00210-15.
44. Trist HM, Tan PS, Wines BD, Ramsland PA, Orlowski E, Stubbs J, Gardiner EE, Pietersz GA, Kent SJ, Stratov I, Burton DR, Hogarth PM. 2014. Polymorphisms and interspecies differences of the activating and inhibitory FcgammaRII of Macaca nemestrina influence the binding of human IgG subclasses. J Immunol 192:792-803. http://dx.doi.org/10.4049/jimmunol.1301554.
45. Rogers KA, Scinicariello F, Attanasio R. 2006. IgG Fc receptor III homologues in nonhuman primate species: genetic characterization and ligand interactions. J Immunol 177:3848-3856. http://dx.doi.org/10.4049/jimmunol.177.6.3848.
46. Warncke M, Calzascia T, Coulot M, Balke N, Touil R, Kolbinger F, Heusser C. 2012. Different adaptations of IgG effector function inhumanand nonhuman primates and implications for therapeutic antibody treatment. J Immunol 188:4405-4411. http://dx.doi.org/10.4049/jimmunol.1200090.
47. Fletcher CV, Staskus K, Wietgrefe SW, Rothenberger M, Reilly C, Chipman JG, Beilman GJ, Khoruts A, Thorkelson A, Schmidt TE, Anderson J, Perkey K, Stevenson M, Perelson AS, Douek DC, Haase AT, Schacker TW. 2014. Persistent HIV-1 replication is associated with lower antiretroviral drug concentrations in lymphatic tissues. Proc Natl Acad Sci U S A 111:2307-2312. http://dx.doi.org/10.1073/pnas.1318249111.
48. Robb M. 2012. Viral dynamics and immune response in acute infection and their impact on viral set-point, PL02.02. AIDS Vaccine 2012, Boston, MA, 9 to 12 September 2012.