Envelope variable region 4 is the first target of neutralizing antibodies in early simian immunodeficiency virus mac251 infection of rhesus monkeys

Journal of Virology

Volumn 86, Issue 13, 2012, Pages 7052-7059

  Yeh, Wendy W ^a   Brassard, Laura M ^a   Miller, Caroline A ^a   Basavapathruni, Aravind ^a   Zhang, Jinrong ^a   Rao, Srinivas S ^b   Nabel, Gary J ^b   Mascola, John R ^b   Letvin, Norman L ^a   Seaman, Michael S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; GENE SEQUENCE; HUMORAL IMMUNITY; IMMUNOGENICITY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING; RECEPTOR GENE; RHESUS MONKEY; SEQUENCE ANALYSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SITE DIRECTED MUTAGENESIS; TZM BL RECEPTOR GENE; VIRUS ACTIVATION; VIRUS ENVELOPE; VIRUS IMMUNITY; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; EPITOPES, B-LYMPHOCYTE; GENE PRODUCTS, ENV; MACACA MULATTA; MALE; MUTANT PROTEINS; NEUTRALIZATION TESTS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84864133994     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00107-12     Document Type: Article

References (45)

1. Baba TW, et al. 2000. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat. Med. 6:200 -206.
2. Babas T, et al. 1995. Specificity and neutralizing capacity of three monoclonal antibodies produced against the envelope glycoprotein of simian immunodeficiency virus isolate 251. Virology 211:339 -344.
3. Basavapathruni A, et al. 2010. Envelope vaccination shapes viral envelope evolution following simian immunodeficiency virus infection in rhesus monkeys. J. Virol. 84:953-963.
4. Burns DP, Collignon C, Desrosiers RC. 1993. Simian immunodeficiency virus mutants resistant to serum neutralization arise during persistent infection of rhesus monkeys. J. Virol. 67:4104-4113.
5. Burns DP, Desrosiers RC. 1991. Selection of genetic variants of simian immunodeficiency virus in persistently infected rhesus monkeys. J. Virol. 65:1843-1854.
6. Chackerian B, Rudensey LM, Overbaugh J. 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.
7. Chakrabarti BK, et al. 2002. Modifications of the human immunodeficiency virus envelope glycoprotein enhance immunogenicity for genetic immunization. J. Virol. 76:5357-5368.
8. Chen B, et al. 2005. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433:834-841.
9. Choi WS, et al. 1994. Effects of natural sequence variation on recognition by monoclonal antibodies neutralize simian immunodeficiency virus infectivity. J. Virol. 68:5395-5402.
10. Conley AJ, et al. 1996. The consequence of passive administration of an anti-human immunodeficiency virus type 1 neutralizing monoclonal antibody before challenge of chimpanzees with a primary virus isolate. J. Virol. 70:6751- 6758.
11. Emini EA, et al. 1992. Prevention of HIV-1 infection in chimpanzees by gp120 V3 domain-specific monoclonal antibody. Nature 355:728 -730.
12. Hessell AJ, et al. 2009. Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat. Med. 15: 951-954.
13. Hessell AJ, et al. 2009. Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog. 5:e1000433. doi:10.1371/journal.ppat.1000433.
14. Hessell AJ, et al. 2010. Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by simian-human immunodeficiency virus SHIVBa-L. J. Virol. 84:1302- 1313.
15. Javaherian K, et al. 1992. The principal neutralization determinant of simian immunodeficiency virus differs from that of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U. S. A. 89:1418 -1422.
16. Johnson WE, et al. 2002. A replication-competent, neutralizationsensitive variant of simian immunodeficiency virus lacking 100 amino acids of envelope. J. Virol. 76:2075-2086.
17. Johnson WE, et al. 2003. Assorted mutations in the envelope gene of simian immunodeficiency virus lead to loss of neutralization resistance against antibodies representing a broad spectrum of specificities. J. Virol. 77:9993-10003.
18. Jurkiewicz E, et al. 1997. Identification of the V1 region as a linear neutralizing epitope of the simian immunodeficiency virus SIVmac envelope glycoprotein. J. Virol. 71:9475-9481.
19. Keele BF, et al. 2009. Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J. Exp. Med. 206:1117-1134.
20. Kinsey NE, et al. 1996. Antigenic variation of SIV: mutations in V4 alter the neutralization profile. Virology 221:14 -21.
21. Kwong PD, et al. 2000. Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure 8:1329 -1339.
22. Kwong PD, et al. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
23. Lavine CL, et al. 2011. High-mannose glycan-dependent epitopes are frequently targeted in broad neutralizing antibody responses during infection of human immunodeficiency virus type 1. J. Virol. 86:2153-2164.
24. Letvin NL, et al. 2006. Preserved CD4_ central memory T cells and survival in vaccinated SIV-challenged monkeys. Science 312:1530 -1533.
25. Letvin NL, et al. 2011. Immune and genetic correlates of vaccine protection against mucosal infection by SIV in monkeys. Sci. Transl. Med. 3:81ra36.
26. Li Y, et al. 2008. Removal of a single N-linked glycan in human immunodeficiency virus type 1 gp120 results in an enhanced ability to induce neutralizing antibody responses. J. Virol. 82:638-651.
27. Mascola JR, et al. 1999. Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J. Virol. 73:4009-4018.
28. Mascola JR, et al. 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.
29. Moore PL, et al. 2008. The c3-v4 region is a major target of autologous neutralizing antibodies in human immunodeficiency virus type 1 subtype C infection. J. Virol. 82:1860 -1869.
30. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, DC.
31. Overbaugh J, Rudensey LM. 1992. Alterations in potential sites for glycosylation predominate during evolution of the simian immunodeficiency virus envelope gene in macaques. J. Virol. 66:5937-5948.
32. Overbaugh J, Rudensey LM, Papenhausen MD, Benveniste RE, Morton WR. 1991. Variation in simian immunodeficiency virus env is confined to V1 and V4 during progression to simian AIDS. J. Virol. 65:7025-7031.
33. Parren PW, et al. 2001. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75:8340- 8347.
34. Petry H, Pekrun K, Hunsmann G, Jurkiewicz E, Luke W. 2000. Naturally occurring V1-env region variants mediate simian immunodeficiency virus SIVmac escape from high-titer neutralizing antibodies induced by a protective subunit vaccine. J. Virol. 74:11145-11152.
35. Prince AM, et al. 1991. Prevention of HIV infection by passive immunization with HIV immunoglobulin. AIDS Res. Hum. Retrovir. 7:971-973.
36. Ren X, Sodroski J, Yang X. 2005. An unrelated monoclonal antibody neutralizes human immunodeficiency virus type 1 by binding to an artificial epitope engineered in a functionally neutral region of the viral envelope glycoproteins. J. Virol. 79:5616 -5624.
37. Rerks-Ngarm S, et al. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209 -2220.
38. Rudensey LM, Kimata JT, Long EM, Chackerian B, Overbaugh J. 1998. Changes in the extracellular envelope glycoprotein of variants that evolve during the course of simian immunodeficiency virus SIVMne infection affect neutralizing antibody recognition, syncytium formation, and macrophage tropism but not replication, cytopathicity, or CCR-5 coreceptor recognition. J. Virol. 72:209 -217.
39. Rybarczyk BJ, et al. 2004. Correlation between env V1/V2 region diversification and neutralizing antibodies during primary infection by simian immunodeficiency virus sm in rhesus macaques. J. Virol. 78: 3561-3571.
40. Sato S, et al. 2008. Potent antibody-mediated neutralization and evolution of antigenic escape variants of simian immunodeficiency virus strain SIVmac239 in vivo. J. Virol. 82:9739 -9752.
41. 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.
42. Torres JV, et al. 1993. An epitope on the surface envelope glycoprotein (gp130) of simian immunodeficiency virus (SIVmac) involved in viral neutralization and T cell activation. AIDS Res. Hum. Retrovir. 9:423- 430.
43. Walker LM, et al. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470.
44. Wei X, et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
45. Yeh WW, et al. 2010. Autologous neutralizing antibodies to the transmitted/founder viruses emerge late after simian immunodeficiency virus SIVmac251 infection of rhesus monkeys. J. Virol. 84:6018-6032.