Potent and broadly reactive HIV-2 neutralizing antibodies elicited by a vaccinia virus vector prime-C2V3C3 polypeptide boost immunization strategy

Journal of Virology

Volumn 84, Issue 23, 2010, Pages 12429-12436

  Marcelino, José Maria ^a   Borrego, Pedro ^b,c   Rocha, Cheila ^b,c   Barroso, Helena ^b,c   Quintas, Alexandre ^b   Novo, Carlos ^b   Taveira, Nuno ^b,c,d  

^a INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^b INSTITUTO SUPERIOR DE CIÊNCIAS DA SAÚDE EGAS MONIZ   (Portugal)

^c RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^d INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 125; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; NEUTRALIZING ANTIBODY; POLYPEPTIDE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VACCINIA VIRUS VECTOR; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN; VIRUS VECTOR;

ACTIVE IMMUNIZATION; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; DRUG POTENCY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 2; IMMUNOGENICITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, NEUTRALIZING; DNA PRIMERS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENETIC VECTORS; HELA CELLS; HIV INFECTIONS; HIV-2; HUMANS; IMMUNIZATION, SECONDARY; IMMUNOPRECIPITATION; MICE; MICE, INBRED BALB C; MUTAGENESIS; NEUTRALIZATION TESTS; RECOMBINANT PROTEINS; VACCINIA VIRUS;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; MUS; VACCINIA VIRUS;

EID: 78049524372     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01102-10     Document Type: Article

References (58)

1. Andersson, S., B. Makitalo, R. Thorstensson, G. Franchini, J. Tartaglia, K. Limbach, E. Paoletti, P. Putkonen, and G. Biberfeld. 1996. Immunogenicity and protective efficacy of a human immunodeficiency virus type 2 recombinant canarypox (ALVAC) vaccine candidate in cynomolgus monkeys. J. Infect. Dis. 174:977-985.
2. Arnold, K., L. Bordoli, J. Kopp, and T. Schwede. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modeling. Bioinformatics 22:195-201. (Pubitemid 43205406)
3. Babas, T., S. Benichou, D. Guetard, L. Montagnier, and E. Bahraoui. 1994. Specificity of antipeptide antibodies produced against V2 and V3 regions of the external envelope of human immunodeficiency virus type 2. Mol. Immunol. 31:361-369.
4. Barouch, D. H. 2008. Challenges in the development of an HIV-1 vaccine. Nature 455:613-619.
5. Barouch, D. H., K. L. O'Brien, N. L. Simmons, S. L. King, P. Abbink, L. F. Maxfield, Y. H. Sun, A. La Porte, A. M. Riggs, D. M. Lynch, S. L. Clark, K. Backus, J. R. Perry, M. S. Seaman, A. Carville, K. G. Mansfield, J. J. Szinger, W. Fischer, M. Muldoon, and B. Korber. Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys. Nat. Med. 16:319-323.
6. Bjorling, E., K. Broliden, D. Bernardi, G. Utter, R. Thorstensson, F. Chiodi, and E. Norrby. 1991. Hyperimmune antisera against synthetic peptides representing the glycoprotein of human immunodeficiency virus type 2 can mediate neutralization and antibody-dependent cytotoxic activity. Proc. Natl. Acad. Sci. U. S. A. 88:6082-6086.
7. Bjorling, E., F. Chiodi, G. Utter, and E. Norrby. 1994. Two neutralizing domains in the V3 region in the envelope glycoprotein gp125 of HIV type 2. J. Immunol. 152:1952-1959. (Pubitemid 24075729)
8. Bjorling, E., G. Scarlatti, A. von Gegerfelt, J. Albert, G. Biberfeld, F. Chiodi, E. Norrby, and E. M. Fenyo. 1993. Autologous neutralizing antibodies prevail in HIV-2 but not in HIV-1 infection. Virology 193:528-530.
9. Blaak, H., P. H. Boers, R. A. Gruters, H. Schuitemaker, M. E. van der Ende, and A. D. Osterhaus. 2005. CCR5, GPR15, and CXCR6 are major coreceptors of human immunodeficiency virus type 2 variants isolated from individuals with or without plasma viremia. J. Virol. 79:1686-1700.
10. Borrego, P., J. M. Marcelino, C. Rocha, M. Doroana, F. Antunes, F. Maltez, P. Gomes, C. Novo, H. Barroso, and N. Taveira. 2008. The role of the humoral immune response in the molecular evolution of the envelope C2, V3, and C3 regions in chronically HIV-2-infected patients. Retrovirology 5:78.
11. Bottiger, B., A. Karlsson, P. A. Andreasson, A. Naucler, C. M. Costa, E. Norrby, and G. Biberfeld. 1990. Envelope cross-reactivity between human immunodeficiency virus types 1 and 2 detected by different serological methods: correlation between cross-neutralization and reactivity against the main neutralizing site. J. Virol. 64:3492-3499.
12. Buonaguro, L., L. Racioppi, M. L. Tornesello, C. Arra, M. L. Visciano, B. Biryahwaho, S. D. Sempala, G. Giraldo, and F. M. Buonaguro. 2002. Induction of neutralizing antibodies and cytotoxic T lymphocytes in BALB/c mice immunized with virus-like particles presenting a gp120 molecule from a HIV-1 isolate of clade A. Antivir. Res. 54:189-201.
13. Cavaco-Silva, P., N. C. Taveira, L. Rosado, M. H. Lourenco, J. Moniz-Pereira, N. W. Douglas, R. S. Daniels, and M. O. Santos-Ferreira. 1998. Virological and molecular demonstration of human immunodeficiency virus type 2 vertical transmission. J. Virol. 72:3418-3422.
14. Chen, B., E. M. Vogan, H. Gong, J. J. Skehel, D. C. Wiley, and S. C. Harrison. 2005. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433:834-841.
15. Davenport, M. P., L. Loh, J. Petravic, and S. J. Kent. 2008. Rates of HIV immune escape and reversion: implications for vaccination. Trends Microbiol. 16:561-566.
16. Davison, A. J., and B. Moss. 1990. New vaccinia virus recombination plasmids incorporating a synthetic late promoter for high level expression of foreign proteins. Nucleic Acids Res. 18:4285-4286.
17. de Silva, T. I., M. Cotten, and S. L. Rowland-Jones. 2008. HIV-2: the forgotten AIDS virus. Trends Microbiol. 16:588-595.
18. Dey, B., M. Pancera, K. Svehla, Y. Shu, S. H. Xiang, J. Vainshtein, Y. Li, J. Sodroski, P. D. Kwong, J. R. Mascola, and R. Wyatt. 2007. Characterization of human immunodeficiency virus type 1 monomeric and trimeric gp120 glycoproteins stabilized in the CD4-bound state: antigenicity, biophysics, and immunogenicity. J. Virol. 81:5579-5593.
19. Franchini, G., M. Robert-Guroff, J. Tartaglia, A. Aggarwal, A. Abimiku, J. Benson, P. Markham, K. Limbach, G. Hurteau, J. Fullen, et al. 1995. Highly attenuated HIV type 2 recombinant poxviruses, but not HIV-2 recombinant Salmonella vaccines, induce long-lasting protection in rhesus macaques. AIDS Res. Hum. Retrovir. 11:909-920.
20. Gaucher, D., R. Therrien, N. Kettaf, B. R. Angermann, G. Boucher, A. Filali-Mouhim, J. M. Moser, R. S. Mehta, D. R. Drake III, E. Castro, R. Akondy, A. Rinfret, B. Yassine-Diab, E. A. Said, Y. Chouikh, M. J. Cameron, R. Clum, D. Kelvin, R. Somogyi, L. D. Greller, R. S. Balderas, P. Wilkinson, G. Pantaleo, J. Tartaglia, E. K. Haddad, and R. P. Sekaly. 2008. Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J. Exp. Med. 205:3119-3131.
21. Geiben-Lynn, R., J. R. Greenland, K. Frimpong-Boateng, and N. L. Letvin. 2008. Kinetics of recombinant adenovirus type 5, vaccinia virus, modified vaccinia Ankara virus, and DNA antigen expression in vivo and the induction of memory T-lymphocyte responses. Clin. Vaccine Immunol. 15:691-696.
22. Gilljam, G. 1993. Envelope glycoproteins of HIV-1, HIV-2, and SIV purified with Galanthus nivalis agglutinin induce strong immune responses. AIDS Res. Hum. Retrovir. 9:431-438.
23. Gomez, C. E., J. L. Najera, V. Jimenez, K. Bieler, J. Wild, L. Kostic, S. Heidari, M. Chen, M. J. Frachette, G. Pantaleo, H. Wolf, P. Liljestrom, R. Wagner, and M. Esteban. 2007. Generation and immunogenicity of novel HIV/AIDS vaccine candidates targeting HIV-1 Env/Gag-Pol-Nef antigens of clade C. Vaccine 25:1969-1992.
24. Handley, L., R. M. Buller, S. E. Frey, C. Bellone, and S. Parker. 2009. The new ACAM2000 vaccine and other therapies to control orthopoxvirus outbreaks and bioterror attacks. Expert Rev. Vaccines 8:841-850.
25. Harari, A., P. A. Bart, W. Stohr, G. Tapia, M. Garcia, E. Medjitna-Rais, S. Burnet, C. Cellerai, O. Erlwein, T. Barber, C. Moog, P. Liljestrom, R. Wagner, H. Wolf, J. P. Kraehenbuhl, M. Esteban, J. Heeney, M. J. Frachette, J. Tartaglia, S. McCormack, A. Babiker, J. Weber, and G. Pantaleo. 2008. An HIV-1 clade C DNA prime, NYVAC boost vaccine regimen induces reliable, polyfunctional, and long-lasting T-cell responses. J. Exp. Med. 205:63-77.
26. Holmgren, B., Z. da Silva, P. Vastrup, O. Larsen, S. Andersson, H. Ravn, and P. Aaby. 2007. Mortality associated with HIV-1, HIV-2, and HTLV-1 single and dual infections in a middle-aged and older population in Guinea-Bissau. Retrovirology 4:85.
27. Hovav, A. H., M. W. Panas, C. E. Osuna, M. J. Cayabyab, P. Autissier, and N. L. Letvin. 2007. The impact of a boosting immunogen on the differentiation of secondary memory CD8+ T cells. J. Virol. 81:12793-12802.
28. Jobb, G. 2008. TREEFINDER version of October 2008 ed. Distributed by the author. G. Jobb, Munich, Germany.
29. Johnston, M. I., and A. S. Fauci. 2007. An HIV vaccine: evolving concepts. N. Engl. J. Med. 356:2073-2081.
30. Keele, B. F., E. E. Giorgi, J. F. Salazar-Gonzalez, J. M. Decker, K. T. Pham, M. G. Salazar, C. Sun, T. Grayson, S. Wang, H. Li, X. Wei, C. Jiang, J. L. Kirchherr, F. Gao, J. A. Anderson, L. H. Ping, R. Swanstrom, G. D. Tomaras, W. A. Blattner, P. A. Goepfert, J. M. Kilby, M. S. Saag, E. L. Delwart, M. P. Busch, M. S. Cohen, D. C. Montefiori, B. F. Haynes, B. Gaschen, G. S. Athreya, H. Y. Lee, N. Wood, C. Seoighe, A. S. Perelson, T. Bhattacharya, B. T. Korber, B. H. Hahn, and G. M. Shaw. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 105:7552-7557.
31. Leligdowicz, A., and S. Rowland-Jones. 2008. Tenets of protection from progression to AIDS: lessons from the immune responses to HIV-2 infection. Expert Rev. Vaccines 7:319-331. (Pubitemid 351520020)
32. Lizeng, Q., P. Skott, S. Sourial, C. Nilsson, S. S. Andersson, M. Ehnlund, N. Taveira, and E. Bjorling. 2003. Serum immunoglobulin A (IgA)-mediated immunity in human immunodeficiency virus type 2 (HIV-2) infection. Virology 308:225-232. (Pubitemid 36434230)
33. Locher, C. P., S. A. Witt, B. M. Ashlock, P. Polacino, S. L. Hu, S. Shiboski, A. M. Schmidt, M. B. Agy, D. M. Anderson, S. I. Staprans, J. zur Megede, and J. A. Levy. 2004. Human immunodeficiency virus type 2 DNA vaccine provides partial protection from acute baboon infection. Vaccine 22:2261-2272.
34. Luke, W., G. Voss, C. Stahl-Hennig, C. Coulibaly, P. Putkonen, H. Petry, and G. Hunsmann. 1993. Protection of cynomolgus macaques (Macaca fascicularis) against infection with the human immunodeficiency virus type 2 strain ben (HIV-2ben) by immunization with the virion-derived envelope glycoprotein gp130. AIDS Res. Hum. Retrovir. 9:387-394.
35. Mackett, M., G. L. Smith, and B. Moss. 1985. The construction and characterization of vaccinia virus recombinants expressing foreign genes, p. 191-212. In D. M. Glover (ed.), DNA cloning. IRL Press, Oxford, United Kingdom.
36. MacNeil, A., A. D. Sarr, J. L. Sankale, S. T. Meloni, S. Mboup, and P. Kanki. 2007. Direct evidence of lower viral replication rates in vivo in human immunodeficiency virus type 2 (HIV-2) infection than in HIV-1 infection. J. Virol. 81:5325-5330. (Pubitemid 46744441)
37. Marcelino, J. M., H. Barroso, F. Goncalves, S. M. Silva, C. Novo, P. Gomes, R. Camacho, and N. Taveira. 2006. Use of a new dual-antigen enzyme-linked immunosorbent assay to detect and characterize the human antibody response to the human immunodeficiency virus type 2 envelope gp125 and gp36 glycoproteins. J. Clin. Microbiol. 44:607-611.
38. Marcelino, J. M., C. Nilsson, H. Barroso, P. Gomes, P. Borrego, F. Maltez, L. Rosado, M. Doroana, F. Antunes, and N. Taveira. 2008. Envelope-specific antibody response in HIV-2 infection: C2V3C3-specific IgG response is associated with disease progression. AIDS 22:2257-2265.
39. Matheron, S., S. Pueyo, F. Damond, F. Simon, A. Lepretre, P. Campa, R. Salamon, G. Chene, and F. Brun-Vezinet. 2003. Factors associated with clinical progression in HIV-2 infected-patients: the French ANRS cohort. AIDS 17:2593-2601.
40. Matsushita, S., S. Matsumi, K. Yoshimura, T. Morikita, T. Murakami, and K. Takatsuki. 1995. Neutralizing monoclonal antibodies against human immunodeficiency virus type 2 gp120. J. Virol. 69:3333-3340.
41. McKnight, A., C. Shotton, J. Cordell, I. Jones, G. Simmons, and P. R. Clapham. 1996. Location, exposure, and conservation of neutralizing and nonneutralizing epitopes on human immunodeficiency virus type 2 SU glycoprotein. J. Virol. 70:4598-4606.
42. Montefiori, D., Q. Sattentau, J. Flores, J. Esparza, and J. Mascola. 2007. Antibody-based HIV-1 vaccines: recent developments and future directions. PLoS Med. 4:e348.
43. Mulligan, M. J., G. D. Ritter, Jr., M. A. Chaikin, G. V. Yamshchikov, P. Kumar, B. H. Hahn, R. W. Sweet, and R. W. Compans. 1992. Human immunodeficiency virus type 2 envelope glycoprotein: differential CD4 interactions of soluble gp120 versus the assembled envelope complex. Virology 187:233-241.
44. Myagkikh, M., S. Alipanah, P. D. Markham, J. Tartaglia, E. Paoletti, R. C. Gallo, G. Franchini, and M. Robert-Guroff. 1996. Multiple immunizations with attenuated poxvirus HIV type 2 recombinants and subunit boosts required for protection of rhesus macaques. AIDS Res. Hum. Retrovir. 12:985-992.
45. Patterson, L. J., B. Peng, A. G. Abimiku, K. Aldrich, L. Murty, P. D. Markham, V. S. Kalyanaraman, W. G. Alvord, J. Tartaglia, G. Franchini, and M. Robert-Guroff. 2000. Cross-protection in NYVAC-HIV-1-immunized/HIV-2-challenged but not in NYVAC-HIV-2-immunized/SHIV-challenged rhesus macaques. AIDS 14:2445-2455.
46. Reeves, J. D., S. Hibbitts, G. Simmons, A. McKnight, J. M. Azevedo-Pereira, J. Moniz-Pereira, and P. R. Clapham. 1999. Primary human immunodeficiency virus type 2 (HIV-2) isolates infect CD4-negative cells via CCR5 and CXCR4: comparison with HIV-1 and simian immunodeficiency virus and relevance to cell tropism in vivo. J. Virol. 73:7795-7804.
47. Robert-Guroff, M., K. Aldrich, R. Muldoon, T. L. Stern, G. P. Bansal, T. J. Matthews, P. D. Markham, R. C. Gallo, and G. Franchini. 1992. Cross-neutralization of human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus isolates. J. Virol. 66:3602-3608.
48. Rodriguez, S. K., A. D. Sarr, A. MacNeil, S. Thakore-Meloni, A. Gueye-Ndiaye, I. Traore, M. C. Dia, S. Mboup, and P. J. Kanki. 2007. Comparison of heterologous neutralizing antibody responses of human immunodeficiency virus type 1 (HIV-1)- and HIV-2-infected Senegalese patients: distinct patterns of breadth and magnitude distinguish HIV-1 and HIV-2 infections. J. Virol. 81:5331-5338.
49. + T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat. Med. 16:324-328.
50. Sarkar, G., and S. S. Sommer. 1990. The "megaprimer" method of site-directed mutagenesis. Biotechniques 8:404-407.
51. Schneider, J. A., S. A. Alam, M. Ackers, B. Parekh, H. Y. Chen, P. Graham, M. Gurwith, K. Mayer, and R. M. Novak. 2007. Mucosal HIV-binding antibody and neutralizing activity in high-risk HIV-uninfected female participants in a trial of HIV-vaccine efficacy. J. Infect. Dis. 196:1637-1644.
52. Shi, Y., E. Brandin, E. Vincic, M. Jansson, A. Blaxhult, K. Gyllensten, L. Moberg, C. Brostrom, E. M. Fenyo, and J. Albert. 2005. Evolution of human immunodeficiency virus type 2 coreceptor usage, autologous neutralization, envelope sequence and glycosylation. J. Gen. Virol. 86:3385-3396.
53. Taveira, N. C., F. Bex, A. Burny, D. Robertson, M. O. Ferreira, and J. Moniz-Pereira. 1994. Molecular characterization of the env gene from a non-syncytium-inducing HIV-2 isolate (HIV-2ALI). AIDS Res. Hum. Retrovir. 10:223-224.
54. Traincard, F., M. A. Rey-Cuille, I. Huon, S. Dartevelle, J. C. Mazie, and S. Benichou. 1994. Characterization of monoclonal antibodies to human immunodeficiency virus type 2 envelope glycoproteins. AIDS Res. Hum. Retrovir. 10:1659-1667.
55. Vogt, G., R. le Grand, B. Vaslin, F. Boussin, M. H. Auboyer, Y. Riviere, P. Putkonen, P. Sonigo, M. P. Kieny, M. Girard, et al. 1995. Heterologous HIV-2 challenge of rhesus monkeys immunized with recombinant vaccinia viruses and purified recombinant HIV-2 proteins. Vaccine 13:202-208.
56. Wei, X., J. M. Decker, H. Liu, Z. Zhang, R. B. Arani, J. M. Kilby, M. S. Saag, X. Wu, G. M. Shaw, and J. C. Kappes. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46:1896-1905.
57. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
58. Zhang, P. F., F. Cham, M. Dong, A. Choudhary, P. Bouma, Z. Zhang, Y. Shao, Y. R. Feng, L. Wang, N. Mathy, G. Voss, C. C. Broder, and G. V. Quinnan, Jr. 2007. Extensively cross-reactive anti-HIV-1 neutralizing antibodies induced by gp140 immunization. Proc. Natl. Acad. Sci. U. S. A. 104:10193-10198.