HIV-1 gp120 vaccine induces affinity maturation in both new and persistent antibody clonal lineages

Journal of Virology

Volumn 86, Issue 14, 2012, Pages 7496-7507

  Moody, M Anthony ^a   Yates, Nicole L ^a   Amos, Joshua D ^a   Drinker, Mark S ^a   Eudailey, Joshua A ^a   Gurley, Thaddeus C ^a   Marshall, Dawn J ^a   Whitesides, John F ^a   Chen, Xi ^a   Foulger, Andrew ^a   Yu, Jae Sung ^a   Zhang, Ruijun ^a   Meyerhoff, R Ryan ^a   Parks, Robert ^a   Scull, Julia Cavanaugh ^a   Wang, Lu ^a   Vandergrift, Nathan A ^a   Pickeral, Joy ^a   Pollara, Justin ^a   Kelsoe, Garnett ^a   Alam, S Munir ^a   Ferrari, Guido ^a   Montefiori, David C ^a   Voss, Gerald ^b   Liao, Hua Xin ^a   Tomaras, Georgia D ^a   Haynesa, Barton F ^a   more..

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b GLAXOSMITHKLINE BIOLOGICALS   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; MONOCLONAL ANTIBODY;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIVIRAL ACTIVITY; ARTICLE; B LYMPHOCYTE; CELL LINEAGE; CELL MATURATION; CELL SELECTION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGENICITY; MEMORY CELL; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; SOMATIC MUTATION; VACCINATION; VIRUS ENVELOPE; VIRUS ISOLATION;

AIDS VACCINES; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; B-LYMPHOCYTES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; IMMUNIZATION SCHEDULE; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGIC MEMORY; VACCINES, SUBUNIT;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84863754149     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00426-12     Document Type: Article

References (66)

1. Abu-Shakra M, Press J, Buskila D, Sukenik S. 2007. Influenza vaccination of patients with systemic lupus erythematosus: safety and immunogenicity issues. Autoimmun. Rev. 6:543-546.
2. Alam SM, et al. 2007. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J. Immunol. 178:4424-4435.
3. Alam SM, et al. 2008. Human immunodeficiency virus type 1 gp41 antibodies that mask membrane proximal region epitopes: antibody binding kinetics, induction, and potential for regulation in acute infection. J. Virol. 82:115-125.
4. Batista FD, Neuberger MS. 1998. Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity 8:751-759.
5. Baumgarth N, et al. 2000. B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J. Exp. Med. 192:271-280.
6. Belloni C, et al. 2002. No evidence of autoimmunity in 6-year-old children immunized at birth with recombinant hepatitis B vaccine. Pediatrics 110:e4. doi:10.1542/peds.110.1.e4.
7. Conti F, Rezai S, Valesini G. 2008. Vaccination and autoimmune rheumatic diseases. Autoimmun. Rev. 8:124 -128.
8. Ewing B, Green P. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8:186 -194.
9. Ewing B, Hillier L, Wendl MC, Green P. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175-185.
10. Felsenstein J. 2005. PHYLIP (phylogeny inference package), 3.6 ed. Department of Genome Sciences, University of Washington, Seattle, WA.
11. Gao F, et al. 2009. Cross-reactive monoclonal antibodies to multiple HIV-1 subtype and SIVcpz envelope glycoproteins. Virology 394:91-98.
12. Goepfert PA, et al. 2007. Durable HIV-1 antibody and T-cell responses elicited by an adjuvanted multi-protein recombinant vaccine in uninfected human volunteers. Vaccine 25:510 -518.
13. Gray D, MacLennan IC, Lane PJ. 1986. Virgin B cell recruitment and the lifespan of memory clones during antibody responses to 2,4-dinitrophenyl-hemocyanin. Eur. J. Immunol. 16:641- 648.
14. Gray ES, et al. 2011. Isolation of a monoclonal antibody that targets the alpha-2 helix of gp120 and represents the initial autologous neutralizingantibody response in an HIV-1 subtype C-infected individual. J. Virol. 85:7719 -7729.
15. Gray ES, et al. 2009. Antibody specificities associated with neutralization breadth in plasma from human immunodeficiency virus type 1 subtype C-infected blood donors. J. Virol. 83:8925- 8937.
16. Haynes BF, et al. 2005. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308:1906 -1908.
17. Haynes BF, Liao HX, Tomaras GD. 2010. Is developing an HIV-1 vaccine possible? Curr. Opin. HIV AIDS 5:362-367. 17a.
18. Haynes BF, Kelsoe G, Harrison SC, Kepler TB. 2012. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat. Biotechnol. 30:423- 433.
19. Karali Z, Basaranoglu ST, Karali Y, Oral B, Kilic SS. 2011. Autoimmunity and hepatitis A vaccine in children. J. Investig. Allergol. Clin. Immunol. 21:389 -393.
20. Katerinis I, et al. 2011. De novo anti-HLA antibody after pandemic H1N1 and seasonal influenza immunization in kidney transplant recipients. Am. J. Transplant. 11:1727-1733.
21. Kepler TB, Perelson AS. 1993. Somatic hypermutation in B cells: an optimal control treatment. J. Theor. Biol. 164:37- 64.
22. Kepler TB, et al. 2010. Chiropteran types I and II interferon genes inferred from genome sequencing traces by a statistical gene-family assembler. BMC Genomics 11:444. doi:10.1186/1471-2164-11-444.
23. Kim JH, Rerks-Ngarm S, Excler JL, Michael NL. 2010. HIV vaccines: lessons learned and the way forward. Curr. Opin. HIV AIDS 5:428-434.
24. Korber B, et al. 1998. Numbering Positions in HIV Relative to HXB2CG. Los Alamos National Laboratory, Los Alamos, NM. http://www.hiv.lanl .gov/content/sequence/HIV/REVIEWS/HXB2.html.
25. Leroux-Roels I, et al. 2010. Strong and persistent CD4+T-cell response in healthy adults immunized with a candidate HIV-1 vaccine containing gp120, Nef and Tat antigens formulated in three adjuvant systems. Vaccine 28:7016 -7024.
26. Liao HX, et al. 2011. Initial antibodies binding to HIV-1 gp41 in acutely infected subjects are polyreactive and highly mutated. J. Exp. Med. 208: 2237-2249.
27. Liao HX, et al. 2009. High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J. Virol. Methods 158:171-179.
28. Liao HX, et al. 2006. A groupMconsensus envelope glycoprotein induces antibodies that neutralize subsets of subtype B and C HIV-1 primary viruses. Virology 353:268 -282.
29. Martin F, Kearney JF. 2000. B-cell subsets and the mature preimmune repertoire. Marginal zone and B1 B cells as part of a " natural immune memory." Immunol. Rev. 175:70 -79.
30. Martinuc Porobic J, et al. 2005. Anti-phospholipid antibodies following vaccination with recombinant hepatitis B vaccine. Clin. Exp. Immunol. 142:377-380.
31. Mietzner B, et al. 2008. Autoreactive IgG memory antibodies in patients with systemic lupus erythematosus arise from nonreactive and polyreactive precursors. Proc. Natl. Acad. Sci. U. S. A. 105:9727-9732.
32. Mikell I, et al. 2011. Characteristics of the earliest cross-neutralizing antibody response to HIV-1. PLoS Pathog. 7:e1001251. doi:10.1371/ journal.ppat.1001251.
33. Millet A, Decaux O, Perlat A, Grosbois B, Jego P. 2009. Systemic lupus erythematosus and vaccination. Eur. J. Intern. Med. 20:236 -241.
34. Montefiori DC. 2005. Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. Curr. Protoc. Immunol. Chapter 12, unit 12.11. doi:10.1002/0471142735.im1211s64.
35. Moody MA, et al. 2011. H3N2 Influenza infection elicits more cross-reactive and less clonally expanded anti-hemagglutinin antibodies than influenza vaccination. PLoS One 6:e25797. doi:10.1371/journal.pone.0025797.
36. Morihara K, Arakawa Y, Takenaka H, Morihara T, Katoh N. 2011. Systemic lupus erythematosus following vaccination against 2009 influenza A (H1N1). Lupus 20:775-776.
37. Morris L, et al. 2011. Isolation of a human anti-HIV gp41 membrane proximal region neutralizing antibody by antigen-specific single B cell sorting. PLoS One 6:e23532. doi:10.1371/journal.pone.0023532.
38. Mouquet H, et al. 2010. Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature 467:591-595.
39. Mouquet H, Warncke M, Scheid JF, Seaman MS, Nussenzweig MC. 2012. Enhanced HIV-1 neutralization by antibody heteroligation. Proc. Natl. Acad. Sci. U. S. A. 109:875- 880.
40. Munshaw S, Kepler TB. 2010. SoDA2: a Hidden Markov Model approach for identification of immunoglobulin rearrangements. Bioinformatics 26: 867-872.
41. Ochsenbein AF, et al. 1999. Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:2156 -2159.
42. Pollara J, et al. 2011. High-throughput quantitative analysis of HIV-1 and SIV-specific ADCC-mediating antibody responses. Cytometry A 79:603- 612.
43. 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.
44. Scheid JF, et al. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333:1633-1637.
45. Shlomchik M, et al. 1990. Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation. J. Exp. Med. 171:265- 292.
46. Smith K, et al. 2009. Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat. Protoc. 4:372-384.
47. Smith TF, Waterman MS. 1981. Identification of common molecular subsequences. J. Mol. Biol. 147:195-197.
48. Stamatatos L, Morris L, Burton DR, Mascola JR. 2009. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat. Med. 15:866-870.
49. Tiller T, et al. 2007. Autoreactivity in human IgG_ memory B cells. Immunity 26:205-213.
50. Tomaras GD, et al. 2011. Polyclonal B Cell responses to conserved neutralization epitopes in a subset of HIV-1-infected individuals. J. Virol. 85:11502-11519.
51. Tomaras GD, Haynes BF. 2010. Strategies for eliciting HIV-1 inhibitory antibodies. Curr. Opin. HIV AIDS 5:421- 427.
52. Tomaras GD, et al. 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.
53. Toplak N, Avcin T. 2009. Influenza and autoimmunity. Ann. N. Y. Acad. Sci. 1173:619-626.
54. Toplak N, et al. 2008. Autoimmune response following annual influenza vaccination in 92 apparently healthy adults. Autoimmun. Rev. 8:134 -138.
55. Van Damme P, et al. 2001. Long-term persistence of antibodies induced by vaccination and safety follow-up, with the first combined vaccine against hepatitis A and B in children and adults. J. Med. Virol. 65:6 -13.
56. Verkoczy L, Kelsoe G, Moody MA, Haynes BF. 2011. Role of immune mechanisms in induction of HIV-1 broadly neutralizing antibodies. Curr. Opin. Immunol. 23:383-390.
57. Volpe JM, Cowell LG, Kepler TB. 2006. SoDA: implementation of a 3D alignment algorithm for inference of antigen receptor recombinations. Bioinformatics 22:438-444.
58. Walker LM, et al. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470.
59. Wardemann H, et al. 2003. Predominant autoantibody production by early human B cell precursors. Science 301:1374 -1377.
60. Wrammert J, et al. 2011. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J. Exp. Med. 208:181-193.
61. Wrammert J, et al. 2008. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453:667- 671.
62. Wu X, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856 - 861.
63. Xiao X, et al. 2009. Germline-like predecessors of broadly neutralizing antibodies lack measurable binding to HIV-1 envelope glycoproteins: implications for evasion of immune responses and design of vaccine immunogens. Biochem. Biophys. Res. Commun. 390:404-409.
64. Yates NL, et al. 2011. Multiple HIV-1-specific IgG3 responses decline during acute HIV-1: implications for detection of incident HIV infection. AIDS 25:2089 -2097.
65. Yu X, et al. 2008. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455:532-536.
66. Zhang J, Shakhnovich EI. 2010. Optimality of mutation and selection in germinal centers. PLoS Comput. Biol. 6:e1000800. doi:10.1371/ journal.pcbi.1000800.