Complement-mediated virus infectivity neutralisation by HLA antibodies is associated with sterilising immunity to SIV challenge in the macaque model for HIV/AIDS

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Page, Mark ^a   Quartey Papafio, Ruby ^a   Robinson, Mark ^a   Hassall, Mark ^a   Cranage, Martin ^b   Stott, James ^a   Almond, Neil ^a  

^a NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN ANTIBODY; HLA ANTIBODY; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN ANTIBODY; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; ARTICLE; COMPLEMENT SYSTEM; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MACACA FASCICULARIS; NONHUMAN; SEROLOGY; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VIRUS ENTRY; VIRUS INACTIVATION; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; COMPLEMENT SYSTEM PROTEINS; DISEASE MODELS, ANIMAL; HISTOCOMPATIBILITY ANTIGENS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNITY; MACACA FASCICULARIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TREATMENT OUTCOME; VACCINATION; VACCINES, INACTIVATED;

EID: 84895814574     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088735     Document Type: Article

References (56)

1. Barouch DH (2008) Challenges in the development of an HIV-1 vaccine. Nature 455: 613-619.
2. Karlsson Hedestam GB, Fouchier RAM, Phogat S, Burton DR, Sodroski J et al. (2008) The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat Rev Micro 6: 143-155.
3. Sattentau QJ, Moulard M, Brivet B, Botto F, Guillemot JC et al. (1999) Antibody neutralization of HIV-1 and the potential for vaccine design. Immunology Letters 66: 143-149. (Pubitemid 29136831)
4. Baba TW, Liska V, Hofmann-Lehmann R, Vlasak J, Xu W et al. (2000) Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nature Medicine 6: 200-206. (Pubitemid 30082366)
5. Barnett SW, Srivastava IK, Kan E, Zhou F, Goodsell A, et al. (2008) Protection of macaques against vaginal SHIV challenge by systemic or mucosal and systemic vaccinations with HIV-envelope. AIDS 22: 339-348.
6. Bower JF, Li Y, Wyatt R, Ross TM (2006) HIV-1 Envgp140 trimers elicit neutralizing antibodies without efficient induction of conformational antibodies. Vaccine 24: 5442-5451. (Pubitemid 43841937)
7. Hofmann-Lehmann R, Vlasak J, Rasmussen RA, Smith BA, Baba TW 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. (Pubitemid 32738005)
8. Mascola JR, Lewis MG, Stiegler G, Harris D, VanCott TC 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. (Pubitemid 29189846)
9. Liao HX, Lynch R, Zhou T, Gao F, Alam SM et al. (2013) Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496: 469-476.
10. Mouquet H, Nussenzweig MC (2013) HIV: Roadmaps to a vaccine. Nature 496: 441-442.
11. Carlson JR, McGraw TP, Keddie E, Yee JL, Rosenthal A et al. (1990) Vaccine protection of rhesus macaques against simian immunodeficiency virus infection. AIDS Res Hum Retroviruses 6: 1239-1246.
12. Cranage MP, Baskerville A, Ashworth LA, Dennis M, Cook N et al. (1992) Intrarectal challenge of macaques vaccinated with formalin-inactivated simian immunodeficiency virus. Lancet 339: 273-274.
13. Desrosiers RC, Wyand MS, Kodama T, Ringler DJ, Arthur LO et al. (1989) Vaccine protection against simian immunodeficiency virus infection. Proc Natl Acad Sci USA 86: 6353-6357. (Pubitemid 19210650)
14. Gardner M, Rosenthal A, Jennings M, Yee J, Antipa L et al. (1995) Passive Immunization of Rhesus Macaques against SIV Infection and Disease. AIDS Research and Human Retroviruses 11: 843-854.
15. Murphey-Corb M, Martin LN, vison-Fairburn B, Montelaro RC, Miller M et al. (1989) A formalin-inactivated whole SIV vaccine confers protection in macaques. Science 246: 1293-1297. (Pubitemid 20066712)
16. Stott EJ, Taffs F, Kitchin P, Chan WL, Mills KHG et al. (1990) Preliminary report: protection of cynomolgus macaques against simian immunodeficiency virus by fixed infected-cell vaccine. The Lancet 336: 1538-1541.
17. Arthur LO, Bess JW, Sowder RC, Benveniste RE, Mann DL et al. (1992) Cellular proteins bound to immunodeficiency viruses: implications for pathogenesis and vaccines. Science 258: 1935-1938. (Pubitemid 23026732)
18. Chan WL, Rodgers A, Hancock RD, Taffs F, Kitchin P et al. (1992) Protection in simian immunodeficiency virus-vaccinated monkeys correlates with anti-HLA class I antibody response. J Exp Med 176: 1203-1207.
19. Cranage MP, Polyanskaya N, McBride B, Cook N, Ashworth LA et al. (1993) Studies on the specificity of the vaccine effect elicited by inactivated simian immunodeficiency virus. AIDS Res Hum Retroviruses 9: 13-22. (Pubitemid 23055127)
20. Stott EJ (1991) Anti-cell antibody in macaques. Nature 353: 393.
21. Chan WL, Rodgers A, Grief C, Almond N, Ellis S et al. (1995) Immunization with class I human histocompatibility leukocyte antigen can protect macaques against challenge infection with SIVmac-32H. [Article]. AIDS 9: 223.
22. Arthur LO, Bess JW, Jr., Urban RG, Strominger JL, Morton WR et al. (1995) Macaques immunized with HLA-DR are protected from challenge with simian immunodeficiency virus. J Virol 69: 3117-3124.
23. Johnson RP, Lifson JD, Czajak SC, Cole KS, Manson KH et al. (1999) Highly attenuated vaccine strains of simian immunodeficiency virus protect against vaginal challenge: inverse relationship of degree of protection with level of attenuation. J Virol 73: 4952-4961. (Pubitemid 29246756)
24. Le Grand R, Vogt G, Vaslin B, Roques P, Theodoro Fdr et al. (1992) Specific and non-specific immunity and protection of macaques against SIV infection. Vaccine 10: 873-879.
25. Putkonen P, Nilsson C, Hild K, Benthin R, Cranage M et al. (1993) Whole inactivated SIV vaccine grown on human cells fails to protect against homologous SIV grown on simian cells. J Med Primatol 22: 100-103.
26. Wang Y, Tao L, Mitchell E, Bravery C, Berlingieri P et al. (1999) Alloimmunization elicits CD8+ T cell-derived chemokines, HIV suppressor factors and resistance to HIV infection in women. Nat Med 5: 1004-1009. (Pubitemid 29439570)
27. Leith JG, Clark DA, Matthews TJ, Rosenthal KL, Luscher MA et al. (2003) Assessing human alloimmunization as a strategy for inducing HIV type 1 neutralizing anti-HLA responses. AIDS Res Hum Retroviruses 19: 957-965. (Pubitemid 37476023)
28. Spruth M, Stoiber H, Kacani L, Schonitzer D, Dierich MP (1999) Neutralization of HIV Type 1 by Alloimmune Sera Derived from Polytransfused Patients. AIDS Research and Human Retroviruses 15: 533-543. (Pubitemid 29177849)
29. Page M, Ojugo A, Imami N, Hardy G, Gotch F et al. (2007) Specificity of antihuman leukocyte antigen antibody responses after immunization with Remune, an inactivated HIV-1 vaccine. AIDS 21: 375-377. (Pubitemid 46175053)
30. Cranage MP, Cook N, Johnstone P, Greenaway P, Kitchin PA, et al. (1990) SIV infection of rhesus macaques: in vivo titration of infectivity and development of an experimental vaccine. In: Scherjon S, Hoshino H, editors. Animal Models in AIDS. Elsevier Science. 103-113.
31. Hunsmann G, Dormont D, Le Grand R, Cranage M, Greenaway P et al. (1995) Protection of macaques against simian immunodeficiency virus infection with inactivated vaccines: comparison of adjuvants, doses and challenge viruses. Vaccine 13: 295-300.
32. Stott EJ, Thomas LH, Taylor G, Collins AP, Jebbett J, Crouch S (1984) A comparison of three vaccines against respiratory syncytial virus in calves. J Hyg (Lond) 93: 251-261. (Pubitemid 15207953)
33. Wei X, Decker JM, Wang S, Hui H, Kappes JC et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312. (Pubitemid 36378357)
34. Ranjbar S, Jones S, Stott EJ, Almond N (1997) The Construction and Evaluation of SIV/HIV Chimeras That Express the Envelope of European HIV Type 1 Isolates. AIDS Research and Human Retroviruses 13: 797-800. (Pubitemid 27225550)
35. Hirsch VM, Johnson PR (1994) Pathogenic diversity of simian immunodeficiency viruses. Virus Research 32: 183-203. (Pubitemid 24147716)
36. Hahn B, Manzari V, Colombini S, Franchini G, Gallo RC et al. (1983) Common site of integration of HTLV in cells of three patients with mature T-cell leukaemia-lymphoma. Nature 303: 253-256. (Pubitemid 13135530)
37. Akari H, Mori K, Terao K, Otani I, Fukasawa M et al. (1996) In vitro immortalization of Old World monkey T lymphocytes with Herpesvirus saimiri: its susceptibility to infection with simian immunodeficiency viruses. Virology 218: 382-388. (Pubitemid 26163832)
38. Stott EJ, Almond N, Kent K, Walker B, Hull R et al. (1998) Evaluation of a candidate human immunodeficiency virus type 1 (HIV-1) vaccine in macaques: effect of vaccination with HIV-1 gp120 on subsequent challenge with heterologous simian immunodeficiency virus-HIV-1 chimeric virus. J Gen Virol 79: 423-432. (Pubitemid 28115864)
39. Rose J, Silvera P, Flanagan B, Kitchin P, Almond N (1995) The development of PCR based assays for the detection and differentiation of simian immunodeficiency virus in vivo. Journal of Virological Methods 51: 229-239.
40. Stott EJ, Almond N, Kent KA, Chan WL, Cranage MP, et al. (1993) Animal models in the development of AIDS vaccines. Huitieme Colloque des Cent Gardes 131-137.
41. Hulskotte EG, Geretti AM, Siebelink KH, van Amerongen G, Cranage MP et al. (1995) Vaccine-induced virus-neutralizing antibodies and cytotoxic T cells do not protect macaques from experimental infection with simian immunodeficiency virus SIVmac32H (J5). J Virol 69: 6289-6296.
42. Spear GT, Takefman DM, Sullivan BL, Landay AL, Zolla-Pazner S (1993) Complement activation by human monoclonal antibodies to human immunodeficiency virus. J Virol 67: 53-59. (Pubitemid 23002963)
43. Spear GT, Takefman DM, Sullivan BL, Landay AL, Jennings MB et al. (1993) Anti-cellular Antibodies in Sera from Vaccinated Macaques Can Induce Complement-Mediated Virolysis of Human Immunodeficiency Virus and Simian Immunodeficiency Virus. Virology 195: 475-480.
44. Huber M, Fischer M, Misselwitz B, Manrique A, Kuster H et al. (2006) Complement lysis activity in autologous plasma is associated with lower viral loads during the acute phase of HIV-1 infection. PLoS Med 3: e441.
45. Sullivan BL, Knopoff EJ, Saifuddin M, Takefman DM, Saarloos MN et al. (1996) Susceptibility of HIV-1 plasma virus to complement-mediated lysis. Evidence for a role in clearance of virus in vivo. J Immunol 157: 1791-1798. (Pubitemid 126449124)
46. Sullivan BL, Takefman DM, Spear GT (1998) Complement can neutralize HIV-1 plasma virus by a C5-independent mechanism. Virology 248: 173-181 (Pubitemid 28417704)
47. Mouquet H, Scheid JF, Zoller MJ, Krogsgaard M, Ott RG et al. (2010) Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature 467: 591-595.
48. Valim YML, Lachmann PJ (1991) The effect of antibody isotype and antigenic epitope density on the complement-fixing activity of immune complexes: a systematic study using chimaeric anti-NIP antibodies with human Fc regions. Clinical & Experimental Immunology 84: 1-8.
49. Chojnacki J, Staudt T, Glass B, Bingen P, Engelhardt J et al. (2012) Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy. Science 338: 524-528.
50. Jiang H, Hester G, Liao L, Montefiori DC, Frank MM (2011) Mechanisms by which HIV envelope minimizes immunogenicity. Immunol Res 49: 147-158.
51. Hessell AJ, Hangartner L, Hunter M, Havenith CE, Beurskens FJ et al. (2007) Fc receptor but not complement binding is important in antibody protection against HIV. Nature 449: 101-104. (Pubitemid 47373775)
52. Montefiori D, Sattentau Q, Flores J, Esparza J, Mascola J et al. (2007) Antibody-Based HIV-1 Vaccines: Recent Developments and Future Directions. PLoS Med 4: e348.
53. Stott J, Almond N, Kent K, Kitchin P, Mills K, et al. (1994) Viral and cellular antigens induce protection against simian immunodeficiency virus infection of macaques. In: Biotechnology and AIDS Roma: Instituto Polignafico 151-160.
54. Morner A, Jansson M, Bunnik EM, Scholler J, Vaughan R et al. (2011) Immunization with Recombinant HLA Classes I and II, HIV-1 gp140, and SIV p27 Elicits Protection against Heterologous SHIV Infection in Rhesus Macaques. J Virol 85: 6442-6452.
55. Stoiber H, Pruenster M, Ammann CG, Dierich MP (2005) Complement-opsonized HIV: the free rider on its way to infection. Mol Immunol 42: 153-160. (Pubitemid 39361446)
56. Willey S, asa-Chapman M, O'Farrell S, Pellegrino P, Williams I et al. (2011) Extensive complement-dependent enhancement of HIV-1 by autologous non-neutralising antibodies at early stages of infection. Retrovirology 8: 16.