Sequential immunization with a subtype B HIV-1 envelope quasispecies partially mimics the in Vivo development of neutralizing antibodies

Journal of Virology

Volumn 85, Issue 11, 2011, Pages 5262-5274

  Malherbe, Delphine C ^a,b   Doria Rose, Nicole A ^b,g   Misher, Lynda ^b,h   Beckett, Travis ^b,c,h   Puryear, Wendy Blay ^b,c,i   Schuman, Jason T ^d   Kraft, Zane ^b   O'Malley, Jean ^e   Mori, Motomi ^e   Srivastava, Indresh ^f,g   Barnett, Susan ^f   Stamatatos, Leonidas ^b,c   Haigwood, Nancy L ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d GE Healthcare Life Sciences   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^f NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^g NATIONAL INSTITUTES OF HEALTH   (United States)

^h Trubion Pharmaceuticals   (United States)

ⁱ BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VIVO STUDY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RABBIT; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS ENVELOPE; VIRUS NEUTRALIZATION; VIRUS REPLICATION; VIRUS STRAIN;

AIDS VACCINES; ANIMALS; ANTIBODIES, NEUTRALIZING; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIV ANTIBODIES; HIV-1; HUMANS; IMMUNIZATION; MACACA MULATTA; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; RABBITS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 79956117053     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02419-10     Document Type: Article

References (63)

1. Anderson, D. E., M. P. Carlos, L. Nguyen, and J. V. Torres. 2001. Overcoming original (antigenic) sin. Clin. Immunol. 101:152-157.
2. Barnett, S. W., et al. 2001. The ability of an oligomeric human immunodeficiency virus type 1 (HIV-1) envelope antigen to elicit neutralizing antibodies against primary HIV-1 isolates is improved following partial deletion of the second hypervariable region. J. Virol. 75:5526-5540.
3. Blay, W. M., et al. 2006. Consistent patterns of change during the divergence of human immunodeficiency virus type 1 envelope from that of the inoculated virus in simian/human immunodeficiency virus-infected macaques. J. Virol. 80:999-1014.
4. Blish, C. A., et al. 2010. Comparative immunogenicity of subtype a human immunodeficiency virus type 1 envelope exhibiting differential exposure of conserved neutralization epitopes. J. Virol. 84:2573-2584.
5. Bower, J. F., X. Yang, J. Sodroski, and T. M. Ross. 2004. Elicitation of neutralizing antibodies with DNA vaccines expressing soluble stabilized human immunodeficiency virus type 1 envelope glycoprotein trimers conjugated to C3d. J. Virol. 78:4710-4719.
6. Buckner, C., et al. 2004. Priming B cell-mediated anti-HIV envelope responses by vaccination allows for the long-term control of infection in macaques exposed to a R5-tropic SHIV. Virology 320:167-180.
7. Burton, D. R., R. L. Stanfield, and I. A. Wilson. 2005. Antibody vs. HIV in a clash of evolutionary titans. Proc. Natl. Acad. Sci. U. S. A. 102:14943-14948.
8. Chackerian, B., L. M. Rudensey, and J. Overbaugh. 1997. Specific N-linked and O-linked glycosylation modifications in the envelope V1 domain of simian immunodeficiency virus variants that evolve in the host alter recognition by neutralizing antibodies. J. Virol. 71:7719-7727.
9. Cherpelis, S., et al. 2001. DNA vaccination with the human immunodeficiency virus type 1 SF162DeltaV2 envelope elicits immune responses that offer partial protection from simian/human immunodeficiency virus infection to CD8(+) T-cell-depleted rhesus macaques. J. Virol. 75:1547-1550.
10. Chohan, B., et al. 2005. Selection for human immunodeficiency virus type 1 envelope glycosylation variants with shorter V1-V2 loop sequences occurs during transmission of certain genetic subtypes and may impact viral RNA levels. J. Virol. 79:6528-6531.
11. Cole, K. S., et al. 1998. Common themes of antibody maturation to simian immunodeficiency virus, simian-human immunodeficiency virus, and human immunodeficiency virus type 1 infections. J. Virol. 72:7852-7859.
12. Corti, D., et al. 2010. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS One 5:e8805.
13. Crooks, E. T., et al. 2007. A comparative immunogenicity study of HIV-1 virus-like particles bearing various forms of envelope proteins, particles bearing no envelope and soluble monomeric gp120. Virology 366:245-262.
14. Derby, N. R., et al. 2007. Isolation and characterization of monoclonal antibodies elicited by trimeric HIV-1 Env gp140 protein immunogens. Virology 366:433-445.
15. Derby, N. R., et al. 2006. Antibody responses elicited in macaques immunized with human immunodeficiency virus type 1 (HIV-1) SF162-derived gp140 envelope immunogens: comparison with those elicited during homologous simian/human immunodeficiency virus SHIVSF162P4 and heterologous HIV-1 infection. J. Virol. 80:8745-8762.
16. Derdeyn, C. A., et al. 2004. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303:2019-2022.
17. Doria-Rose, N. A., et al. 2005. Human immunodeficiency virus type 1 subtype B ancestral envelope protein is functional and elicits neutralizing antibodies in rabbits similar to those elicited by a circulating subtype B envelope. J. Virol. 79:11214-11224.
18. Doria-Rose, N. A., et al. 2003. Multigene DNA priming-boosting vaccines protect macaques from acute CD4+-T-cell depletion after simian-human immunodeficiency virus SHIV89.6P mucosal challenge. J. Virol. 77:11563-11577.
19. Doria-Rose, N. A., et al. 2003. Multigene DNA prime-boost vaccines for SHIV89.6P. J. Med. Primatol. 32:218-228.
20. Frost, S. D., et al. 2005. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc. Natl. Acad. Sci. U. S. A. 102:18514-18519.
21. Gray, E. S., et al. 2007. Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. J. Virol. 81:6187-6196.
22. Haynes, B. F., and D. C. Montefiori. 2006. Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev. Vaccines 5:347-363.
23. Hofmann-Lehmann, R., et al. 2001. Postnatal passive immunization of neonatal macaques with a triple combination of human monoclonal antibodies against oral simian-human immunodeficiency virus challenge. J. Virol. 75: 7470-7480.
24. Katsamba, P. S., et al. 2006. Kinetic analysis of a high-affinity antibody/antigen interaction performed by multiple Biacore users. Anal. Biochem. 352:208-221.
25. Korber, B., et al. 2001. Evolutionary and immunological implications of contemporary HIV-1 variation. Br. Med. Bull. 58:19-42.
26. Kraft, Z., et al. 2007. Macaques infected with a CCR5-tropic simian/human immunodeficiency virus (SHIV) develop broadly reactive anti-HIV neutralizing antibodies. J. Virol. 81:6402-6411.
27. Kwong, P. D., et al. 2002. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420:678-682.
28. Li, M., et al. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccineelicited neutralizing antibodies. J. Virol. 79:10108-10125.
29. Li, Y., et al. 2007. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat. Med. 13:1032-1034.
30. Liu, M. A., and J. B. Ulmer. 2005. Human clinical trials of plasmid DNA vaccines. Adv. Genet. 55:25-40.
31. MacGregor, R. R., et al. 1998. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: safety and host response. J. Infect. Dis. 178:92-100.
32. Mahalanabis, M., V. M. Hirsch, and N. L. Haigwood. 2005. Infection with a molecularly cloned SIVsm virus elicits high titer homologous neutralizing antibodies with heterologous neutralizing activity. J. Med. Primatol. 34:253-261.
33. Mahalanabis, M., et al. 2009. Continuous viral escape and selection by autologous neutralizing antibodies in drug-naive human immunodeficiency virus controllers. J. Virol. 83:662-672.
34. Montefiori, D. C., et al. 2001. Induction of neutralizing antibodies and gag-specific cellular immune responses to an R5 primary isolate of human immunodeficiency virus type 1 in rhesus macaques. J. Virol. 75:5879-5890.
35. Moore, P. L., et al. 2006. Nature of nonfunctional envelope proteins on the surface of human immunodeficiency virus type 1. J. Virol. 80:2515-2528.
36. Moore, P. L., et al. 2009. Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog. 5:e1000598.
37. Nishimura, Y., et al. 2002. Determination of a statistically valid neutralization titer in plasma that confers protection against simian-human immunodeficiency virus challenge following passive transfer of high-titered neutralizing antibodies. J. Virol. 76:2123-2130.
38. Piantadosi, A., et al. 2009. Breadth of neutralizing antibody response to human immunodeficiency virus type 1 is affected by factors early in infection but does not influence disease progression. J. Virol. 83:10269-10274.
39. Poignard, P., et al. 2003. Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies. J. Virol. 77:353-365.
40. Rasmussen, R. A., D. C. Montefiori, H. L. Robinson, H. M. McClure, and R. M. Ruprecht. 2001. Heterologous neutralizing antibody induction in a simian-human immunodeficiency virus primate model: lack of original antigenic sin. J. Infect. Dis. 184:1603-1607.
41. Richman, D. D., T. Wrin, S. J. Little, and C. J. Petropoulos. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. U. S. A. 100:4144-4149.
42. Robinson, J. E., et al. 2010. Quaternary epitope specificities of anti-HIV-1 neutralizing antibodies generated in rhesus macaques infected by the simian/human immunodeficiency virus SHIVSF162P4. J. Virol. 84:3443-3453.
43. Rong, R., et al. 2009. Escape from autologous neutralizing antibodies in acute/early subtype C HIV-1 infection requires multiple pathways. PLoS Pathog. 5:e1000594.
44. Sagar, M., X. Wu, S. Lee, and J. Overbaugh. 2006. Human immunodeficiency virus type 1 V1-V2 envelope loop sequences expand and add glycosylation sites over the course of infection, and these modifications affect antibody neutralization sensitivity. J. Virol. 80:9586-9598.
45. Sather, D. N., et al. 2009. Factors associated with the development of crossreactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J. Virol. 83:757-769.
46. Scheid, J. F., et al. 2009. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458:636-640.
47. Shibata, R., et al. 1999. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat. Med. 5:204-210.
48. Srivastava, I. K., et al. 2003. Purification, characterization, and immunogenicity of a soluble trimeric envelope protein containing a partial deletion of the V2 loop derived from SF162, an R5-tropic human immunodeficiency virus type 1 isolate. J. Virol. 77:11244-11259.
49. Steckbeck, J. D., et al. 2006. Dynamic evolution of antibody populations in a rhesus macaque infected with attenuated simian immunodeficiency virus identified by surface plasmon resonance. J. Med. Primatol. 35:248-260.
50. Steimer, K. S., C. J. Scandella, P. V. Skiles, and N. L. Haigwood. 1991. Neutralization of divergent HIV-1 isolates by conformation-dependent human antibodies to Gp120. Science 254:105-108.
51. Vaine, M., et al. 2008. Improved induction of antibodies against key neutralizing epitopes by human immunodeficiency virus type 1 gp120 DNA prime-protein boost vaccination compared to gp120 protein-only vaccination. J. Virol. 82:7369-7378.
52. Vaine, M., S. Wang, A. Hackett, J. Arthos, and S. Lu. 2010. Antibody responses elicited through homologous or heterologous prime-boost DNA and protein vaccinations differ in functional activity and avidity. Vaccine 28:2999-3007.
53. Vaine, M., et al. 2010. Profiles of human serum antibody responses elicited by three leading HIV vaccines focusing on the induction of Env-specific antibodies. PLoS One 5:e13916.
54. VanCott, T. C., et al. 1997. Antibodies with specificity to native gp120 and neutralization activity against primary human immunodeficiency virus type 1 isolates elicited by immunization with oligomeric gp160. J. Virol. 71:4319-4330.
55. Walker, L. M., et al. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289.
56. Wang, S., et al. 2008. Cross-subtype antibody and cellular immune responses induced by a polyvalent DNA prime-protein boost HIV-1 vaccine in healthy human volunteers. Vaccine 26:3947-3957.
57. Wei, X., et al. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46:1896-1905.
58. Wei, X., et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
59. Wrammert, J., et al. 2008. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453:667-671.
60. Wu, X., et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861.
61. Yang, X., R. Wyatt, and J. Sodroski. 2001. Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers. J. Virol. 75:1165-1171.
62. Zhao, J., et al. 2009. Preclinical studies of human immunodeficiency virus/AIDS vaccines: inverse correlation between avidity of anti-Env antibodies and peak postchallenge viremia. J. Virol. 83:4102-4111.
63. Zhou, T., et al. 2010. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329:811-817.