Superiority in rhesus macaques of targeting HIV-1 Env gp140 to CD40 versus LOX-1 in combination with replication-competent NYVAC-KC for induction of Env-specific antibody and T cell responses

Journal of Virology

Volumn 91, Issue 9, 2017, Pages

  Zurawski, Gerard ^a,b   Shen, Xiaoying ^c   Zurawski, Sandra ^a,b   Tomaras, Georgia D ^c   Montefiori, David C ^c   Roederer, Mario ^d   Ferrari, Guido ^c   Lacabaratz, Christine ^a   Klucar, Peter ^a,b   Wang, Zhiqing ^a,b   Foulds, Kathryn E ^d   Kao, Shing Fen ^d   Yu, Xuesong ⁱ   Sato, Alicia ⁱ   Yates, Nicole L ^c   LaBranche, Celia ^c   Stanfield Oakley, Sherry ^c   Kibler, Karen ^e   Jacobs, Bertram ^e   Salazar, Andres ^f   Self, Steve ^g   Fulp, William ^g   Gottardo, Raphael ^g   Galmin, Lindsey ^g   Weiss, Deborah ^g   Cristillo, Anthony ^g,j   Pantaleo, Giuseppe ^h   Levy, Yves ^a   more..

^a FACULTÉ DE MÉDECINE   (France)

^b BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

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

^e ARIZONA STATE UNIVERSITY   (United States)

^f Oncovir   (United States)

^g Fred Hutchinson Cancer Research Center   (United States)

^h ADVANCED BIOSCIENCE LABORATORIES INC   (United States)

ⁱ LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^j SOCIAL AND SCIENTIFIC SYSTEMS INC   (United States)

more..

Author keywords

Dendritic cells; HIV 1; Vaccines

Indexed keywords

CD40 ANTIGEN; EPITOPE; GLYCOPROTEIN GP 140; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; POXVIRUS VECTOR; CARBOXYMETHYLCELLULOSE; CARBOXYMETHYLCELLULOSE POLYCYTIDYLIC POLYINOSINIC ACID POLYLYSINE; GP140 ENVELOPE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEUTRALIZING ANTIBODY; NYVAC-C VACCINE; OLR1 PROTEIN, HUMAN; POLYINOSINIC POLYCYTIDYLIC ACID; POLYLYSINE; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS REACTION; HUMAN IMMUNODEFICIENCY VIRUS 1; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; RHESUS MONKEY; T LYMPHOCYTE; VIRUS ENVELOPE; VIRUS NEUTRALIZATION; VIRUS REPLICATION; ANALOGS AND DERIVATIVES; ANIMAL; CHO CELL LINE; CRICETULUS; DENDRITIC CELL; GENETICS; IMMUNOLOGY; VACCINATION;

AIDS VACCINES; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD40; CARBOXYMETHYLCELLULOSE SODIUM; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHO CELLS; CRICETULUS; DENDRITIC CELLS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV ANTIBODIES; HIV-1; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MACACA MULATTA; MALE; POLY I-C; POLYLYSINE; SCAVENGER RECEPTORS, CLASS E; VACCINATION;

EID: 85017548168     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01596-16     Document Type: Article

References (39)

1. Steinman RM. 2012. Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 30:1-22. https://doi.org/10.1146/annurev-immunol-100311-102839.
2. Zurawski G, Zurawski S, Flamar AL, Richert L, Wagner R, Tomaras GD, Montefiori DC, Roederer M, Ferrari G, Lacabaratz C, Bonnabau H, Klucar P, Wang Z, Foulds KE, Kao SF, Yates NL, LaBranche C, Jacobs BL, Kibler K, Asbach B, Kliche A, Salazar A, Reed S, Self S, Gottardo R, Galmin L, Weiss D, Cristillo A, Thiebaut R, Pantaleo G, Levy Y. 2016. Targeting HIV-1 Env gp140 to LOX-1 elicits immune responses in rhesus macaques. PLoS One 11:e0153484. https://doi.org/10.1371/journal.pone.0153484.
3. Joo H, Li D, Dullaers M, Kim TW, Duluc D, Upchurch K, Xue Y, Zurawski S, Le Grand R, Liu YJ, Kuroda M, Zurawski G, Oh S. 2014. C-type lectin-like receptor LOX-1 promotes dendritic cell-mediated class-switched B cell responses. Immunity 41:592-604. https://doi.org/10.1016/j.immuni.2014.09.009.
4. Kastenmüller W, Kastenmüller K, Kurts C, Seder RA. 2014. Dendritic cell-targeted vaccines-hope or hype? Nat Rev Immunol 14:705-711. https://doi.org/10.1038/nri3727.
5. Cohn L, Delamarre L. 2014. Dendritic cell-targeted vaccines. Front Immunol 5:255.
6. Apostolopoulos V, Pietersz GA, Tsibanis A, Tsikkinis A, Stojanovska L, McKenzie IF, Vassilaros S. 2014. Dendritic cell immunotherapy: clinical outcomes. Clin Transl Immunol 3:e21. https://doi.org/10.1038/cti.2014.14.
7. Schjetne KW, Fredriksen AB, Bogen B. 2007. Delivery of antigen to CD40 induces protective immune responses against tumors. J Immunol 178: 4169-4176. https://doi.org/10.4049/jimmunol.178.7.4169.
8. Chatterjee B, Smed-Sorensen A, Cohn L, Chalouni C, Vandlen R, Lee BC, Widger J, Keler T, Delamarre L, Mellman I. 2012. Internalization and endosomal degradation of receptor-bound antigens regulate the efficiency of cross presentation by human dendritic cells. Blood 120: 2011-2020. https://doi.org/10.1182/blood-2012-01-402370.
9. Flamar AL, Xue Y, Zurawski SM, Montes M, King B, Sloan L, Oh S, Banchereau J, Levy Y, Zurawski G. 2013. Targeting concatenated HIV antigens to human CD40 expands a broad repertoire of multifunctional CD4+ and CD8+ T cells. AIDS 27:2041-2051. https://doi.org/10.1097/QAD.0b013e3283624305.
10. Chen J, Zurawski G, Zurawski S, Wang Z, Akagawa K, Oh S, Hideki U, Fay J, Banchereau J, Song W, Palucka AK. 2015. A novel vaccine for mantle cell lymphoma based on targeting cyclin D1 to dendritic cells via CD40. J Hematol Oncol 8:35. https://doi.org/10.1186/s13045-015-0131-7.
11. Rosalia RA, Cruz LJ, van Duikeren S, Tromp AT, Silva AL, Jiskoot W, de Gruijl T, Lowik C, Oostendorp J, van der Burg SH, Ossendorp F. 2015. CD40-targeted dendritic cell delivery of PLGA-nanoparticle vaccines induce potent anti-tumor responses. Biomaterials 40:88-97. https://doi.org/10.1016/j.biomaterials.2014.10.053.
12. Yin W, Gorvel L, Zurawski S, Li D, Ni L, Duluc D, Upchurch K, Kim JR, Gu C, Ouedraogo R, Wang Z, Xue Y, Joo HM, Gorvel JP, Zurawski G, Oh SK. 2016. Functional specialty of CD40 and dendritic cell surface lectins for exogenous antigen presentation to CD8+ and CD4+ T cells. EBioMedicine 5:46-58.
13. Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y, Noelle RJ. 2009. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev 229:152-172. https://doi.org/10.1111/j.1600-065X.2009.00782.x.
14. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, Evans DT, Montefiori DC, Karnasuta C, Sutthent R, Liao HX, DeVico AL, Lewis GK, Williams C, Pinter A, Fong Y, Janes H, DeCamp A, Huang Y, Rao M, Billings E, Karasavvas N, Robb ML, Ngauy V, de Souza MS, Paris R, Ferrari G, Bailer RT, Soderberg KA, Andrews C, Berman PW, Frahm N, De Rosa SC, Alpert MD, Yates NL, Shen X, Koup RA, Pitisuttithum P, Kaewkungwal J, Nitayaphan S, Rerks-Ngarm S, Michael NL, Kim JH. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 366:1275-1286. https://doi.org/10.1056/NEJMoa1113425.
15. Zolla-Pazner S, deCamp A, Gilbert PB, Williams C, Yates NL, Williams WT, Howington R, Fong Y, Morris DE, Soderberg KA, Irene C, Reichman C, Pinter A, Parks R, Pitisuttithum P, Kaewkungwal J, Rerks-Ngarm S, Nitayaphan S, Andrews C, O'Connell RJ, Yang ZY, Nabel GJ, Kim JH, Michael NL, Montefiori DC, Liao HX, Haynes BF, Tomaras GD. 2014. Vaccineinduced IgG antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infection. PLoS One 9:e87572. https://doi.org/10.1371/journal.pone.0087572.
16. Yates NL, Liao HX, Fong Y, deCamp A, Vandergrift NA, Williams WT, Alam SM, Ferrari G, Yang ZY, Seaton KE, Berman PW, Alpert MD, Evans DT, O'Connell RJ, Francis D, Sinangil F, Lee C, Nitayaphan S, Rerks-Ngarm S, Kaewkungwal J, Pitisuttithum P, Tartaglia J, Pinter A, Zolla-Pazner S, Gilbert PB, Nabel GJ, Michael NL, Kim JH, Montefiori DC, Haynes BF, Tomaras GD. 2014. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci Transl Med 6:228ra239.
17. Tomaras GD, Ferrari G, Shen X, Alam SM, Liao HX, Pollara J, Bonsignori M, Moody MA, Fong Y, Chen X, Poling B, Nicholson CO, Zhang R, Lu X, Parks R, Kaewkungwal J, Nitayaphan S, Pitisuttithum P, Rerks-Ngarm S, Gilbert PB, Kim JH, Michael NL, Montefiori DC, Haynes BF. 2013. Vaccine-induced plasma IgA specific for the C1 region of the HIV-1 envelope blocks binding and effector function of IgG. Proc Natl Acad Sci U S A 110: 9019-9024. https://doi.org/10.1073/pnas.1301456110.
18. Flynn BJ, Kastenmuller K, Wille-Reece U, Tomaras GD, Alam M, Lindsay RW, Salazar AM, Perdiguero B, Gomez CE, Wagner R, Esteban M, Park CG, Trumpfheller C, Keler T, Pantaleo G, Steinman RM, Seder R. 2011. Immunization with HIV Gag targeted to dendritic cells followed by recombinant New York vaccinia virus induces robust T-cell immunity in nonhuman primates. Proc Natl Acad Sci U S A 108:7131-7136. https://doi.org/10.1073/pnas.1103869108.
19. Wille-Reece U, Flynn BJ, Loré K, Koup RA, Miles AP, Saul A, Kedl RM, Mattapallil JJ, Weiss WR, Roederer M, Seder RA. 2006. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J Exp Med 213:1249-1258.
20. Park H, Adamson L, Ha T, Mullen K, Hagen SI, Nogueron A, Sylwester AW, Axthelm MK, Legasse AI, Piatak M, Jr, Lifson JD, McElrath JM, Picker LJ, Seder RA. 2013. Polyinosinic-polycytidylic acid is the most effective TLR adjuvant for SIV Gag protein-induced T cell responses in nonhuman primates. J Immunol 190:4103-4115. https://doi.org/10.4049/jimmunol.1202958.
21. Flamar AL, Zurawski S, Scholz F, Gayet I, Ni L, Li XH, Klechevsky E, Quinn J, Oh S, Kaplan DH, Banchereau J, Zurawski G. 2012. Noncovalent assembly of anti-dendritic cell antibodies and antigens for evoking immune responses in vitro and in vivo. J Immunol 189:2645-2655. https://doi.org/10.4049/jimmunol.1102390.
22. Li D, Romain G, Flamar AL, Duluc D, Dullaers M, Li XH, Zurawski S, Bosquet N, Palucka AK, Le Grand R, O'Garra A, Zurawski G, Banchereau J, Oh S. 2012. Targeting self-and foreign antigens to dendritic cells via DC-ASGPR generates IL-10-producing suppressive CD4+ T cells. J Exp Med 209:109-121. https://doi.org/10.1084/jem.20110399.
23. Skinner JA, Zurawski SM, Sugimoto C, Vinet-Oliphant H, Vinod P, Xue Y, Russell-Lodrigue K, Albrecht RA, Garcia-Sastre A, Salazar AM, Roy CJ, Kuroda MJ, Oh S, Zurawski G. 2014. Immunologic characterization of a rhesus macaque H1N1 challenge model for candidate influenza virus vaccine assessment. Clin Vaccine Immunol 21:1668-1680. https://doi.org/10.1128/CVI.00547-14.
24. Kibler KV, Gomez CE, Perdiguero B, Wong S, Huynh T, Holechek S, Arndt W, Jimenez V, Gonzalez-Sanz R, Denzler K, Haddad EK, Wagner R, Sekaly RP, Tartaglia J, Pantaleo G, Jacobs BL, Esteban M. 2011. Improved NYVAC-based vaccine vectors. PLoS One 6:e25674. https://doi.org/10.1371/journal.pone.0025674.
25. Montefiori DC. 2009. Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol Biol 485:395-405. https://doi.org/10.1007/978-1-59745-170-3_26.
26. Sarzotti-Kelsoe M, Daniell X, Todd CA, Bilska M, Martelli A, LaBranche C, Perez LG, Ochsenbauer C, Kappes JC, Rountree W, Denny TN, Montefiori DC. 2014. Optimization and validation of a neutralizing antibody assay for HIV-1 in A3R5 cells. J Immunol Methods 409:147-160. https://doi.org/10.1016/j.jim.2014.02.013.
27. Todd CA, Greene KM, Yu X, Ozaki DA, Gao H, Huang Y, Wang M, Li G, Brown R, Wood B, D'Souza MP, Gilbert P, Montefiori DC, Sarzotti-Kelsoe M. 2012. Development and implementation of an international proficiency testing program for a neutralizing antibody assay for HIV-1 in TZM-bl cells. J Immunol Methods 375:57-67. https://doi.org/10.1016/j.jim.2011.09.007.
28. Huang Y, Gilbert PB, Montefiori DC, Self SG. 2009. Simultaneous evaluation of the magnitude and breadth of a left and right censored multivariate response, with application to HIV vaccine development. Stat Biopharm Res 1:81-91. https://doi.org/10.1198/sbr.2009.0008.
29. Tomaras GD, Yates NL, Liu P, Qin L, Fouda GG, Chavez LL, Decamp AC, Parks RJ, Ashley VC, Lucas JT, Cohen M, Eron J, Hicks CB, Liao HX, Self SG, Landucci G, Forthal DN, Weinhold KJ, Keele BF, Hahn BH, Greenberg ML, Morris L, Karim SS, Blattner WA, Montefiori DC, Shaw GM, Perelson AS, Haynes BF. 2008. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J Virol 82:12449-12463. https://doi.org/10.1128/JVI.01708-08.
30. Liao HX, Bonsignori M, Alam SM, McLellan JS, Tomaras GD, Moody MA, Kozink DM, Hwang KK, Chen X, Tsao CY, Liu P, Lu X, Parks RJ, Montefiori DC, Ferrari G, Pollara J, Rao M, Peachman KK, Santra S, Letvin NL, Karasavvas N, Yang ZY, Dai K, Pancera M, Gorman J, Wiehe K, Nicely NI, Rerks-Ngarm S, Nitayaphan S, Kaewkungwal J, Pitisuttithum P, Tartaglia J, Sinangil F, Kim JH, Michael NL, Kepler TB, Kwong PD, Mascola JR, Nabel GJ, Pinter A, Zolla-Pazner S, Haynes BF. 2013. Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38:176-186. https://doi.org/10.1016/j.immuni.2012.11.011.
31. Gaschen B, Taylor J, Yusim K, Foley B, Gao F, Lang D, Novitsky V, Haynes B, Hahn BH, Bhattacharya T, Korber B. 2002. Diversity considerations in HIV-1 vaccine selection. Science 296:2354-2360. https://doi.org/10.1126/science.1070441.
32. Liao HX, Sutherland LL, Xia SM, Brock ME, Scearce RM, Vanleeuwen S, Alam SM, McAdams M, Weaver EA, Camacho Z, Ma BJ, Li Y, Decker JM, Nabel GJ, Montefiori DC, Hahn BH, Korber BT, Gao F, Haynes BF. 2006. A group M consensus envelope glycoprotein induces antibodies that neutralize subsets of subtype B and C HIV-1 primary viruses. Virology 353:268-282. https://doi.org/10.1016/j.virol.2006.04.043.
33. Tomaras GD, Binley JM, Gray ES, Crooks ET, Osawa K, Moore PL, Tumba N, Tong T, Shen X, Yates NL, Decker J, Wibmer CK, Gao F, Alam SM, Easterbrook P, Abdool Karim S, Kamanga G, Crump JA, Cohen M, Shaw GM, Mascola JR, Haynes BF, Montefiori DC, Morris L. 2011. Polyclonal B cell responses to conserved neutralization epitopes in a subset of HIV-1-infected individuals. J Virol 85:11502-11519. https://doi.org/10.1128/JVI.05363-11.
34. Gottardo R, Bailer RT, Korber BT, Gnanakaran S, Phillips J, Shen X, Tomaras GD, Turk E, Imholte G, Eckler L, Wenschuh H, Zerweck J, Greene K, Gao H, Berman PW, Francis D, Sinangil F, Lee C, Nitayaphan S, Rerks-Ngarm S, Kaewkungwal J, Pitisuttithum P, Tartaglia J, Robb ML, Michael NL, Kim JH, Zolla-Pazner S, Haynes BF, Mascola JR, Self S, Gilbert P, Montefiori DC. 2013. Plasma IgG to linear epitopes in the V2 and V3 regions of HIV-1 gp120 correlate with a reduced risk of infection in the RV144 vaccine efficacy trial. PLoS One 8:e75665. https://doi.org/10.1371/journal.pone.0075665.
35. Shen X, Duffy R, Howington R, Cope A, Sadagopal S, Park H, Pal R, Kwa S, Ding S, Yang OO, Fouda GG, Le Grand R, Bolton D, Esteban M, Phogat S, Roederer M, Amara RR, Picker LJ, Seder RA, McElrath MJ, Barnett S, Permar SR, Shattock R, DeVico AL, Felber BK, Pavlakis GN, Pantaleo G, Korber BT, Montefiori DC, Tomaras GD. 2015. Vaccine-induced linear epitope-specific antibodies to simian immunodeficiency virus SIVmac239 envelope are distinct from those induced to the human immunodeficiency virus type 1 envelope in nonhuman primates. J Virol 89:8643-8650. https://doi.org/10.1128/JVI.03635-14.
36. Donaldson MM, Kao SF, Eslamizar L, Gee C, Koopman G, Lifton M, Schmitz JE, Sylwester AW, Wilson A, Hawkins N, Self SG, Roederer M, Foulds KE. 2012. Optimization and qualification of an 8-color intracellular cytokine staining assay for quantifying T cell responses in rhesus macaques for pre-clinical vaccine studies. J Immunol Methods 386:10-21. https://doi.org/10.1016/j.jim.2012.08.011.
37. Foulds KE, Donaldson M, Roederer M. 2012. OMIP-005: quality and phenotype of antigen-responsive rhesus macaque T cells. Cytometry A 81:360-361.
38. Pollara J, Hart L, Brewer F, Pickeral J, Packard BZ, Hoxie JA, Komoriya A, Ochsenbauer C, Kappes JC, Roederer M, Huang Y, Weinhold KJ, Tomaras GD, Haynes BF, Montefiori DC, Ferrari G. 2011. High-throughput quantitative analysis of HIV-1 and SIV-specific ADCC-mediating antibody responses. Cytometry A 79:603-612.
39. Weatherall D (ed).2006. The use of non-human primates in research. https://royalsociety.org/topics-policy/publications/2006/weatherall-report/.