Tools to therapeutically harness the human antibody response

Nature Reviews Immunology

Volumn 12, Issue 10, 2012, Pages 709-719

  Wilson, Patrick C ^a   Andrews, Sarah F ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INFLUENZA VACCINE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY VRC01; MONOCLONAL ANTIBODY VRC02; MONOCLONAL ANTIBODY VRC03; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VACCINE;

2009 H1N1 INFLUENZA; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL IMMORTALIZATION; DRUG ISOLATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; IMMUNOTHERAPY; INFLUENZA VIRUS; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; INFLUENZA VIRUS A H5N1; MEMORY CELL; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; REVIEW; SPANISH INFLUENZA; TECHNOLOGY; VACCINATION; VIRUS INFECTION; VIRUS STRAIN;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY FORMATION; B-LYMPHOCYTES; EPITOPES; HUMANS; VIRUS DISEASES;

EID: 84866679186     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri3285     Document Type: Review

References (96)

1. Casadevall, A., Dadachova, E. & Pirofski, L. A. Passive antibody therapy for infectious diseases. Nature Rev. Microbiol. 2, 695-703 (2004).
2. Kohler, G. & Milstein, C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256, 495-497 (1975).
3. Winter, G. & Harris, W. J. Humanized antibodies. Immunol. Today 14, 243-246 (1993).
4. Carter, P. J. Potent antibody therapeutics by design. Nature Rev. Immunol. 6, 343-357 (2006).
5. Chan, A. C. & Carter, P. J. Therapeutic antibodies for autoimmunity and inflammation. Nature Rev. Immunol. 10, 301-316 (2010).
6. Weiner, L. M., Surana, R. & Wang, S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nature Rev. Immunol. 10, 317-327 (2010).
7. Bradbury, A. R., Sidhu, S., Dubel, S. & McCafferty, J. Beyond natural antibodies: the power of in vitro display technologies. Nature Biotech. 29, 245-254 (2011).
8. Jin, A. et al. A rapid and efficient single-cell manipulation method for screening antigen-specific antibody-secreting cells from human peripheral blood. Nature Med. 15, 1088-1092 (2009).
9. Corti, D. et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333, 850-856 (2011).
10. Walker, L. M. et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289 (2009).
11. + plasmablasts in the human gut are antigen-specific. J. Clin. Invest. 121, 1946-1955 (2011).
12. Marasco, W. A. & Sui, J. The growth and potential of human antiviral monoclonal antibody therapeutics. Nature Biotech. 25, 1421-1434 (2007).
13. Marks, J. D. et al. By-passing immunization: building high affinity human antibodies by chain shuffling. Biotechnology 10, 779-783 (1992).
14. Steinitz, M., Klein, G., Koskimies, S. & Makel, O. EB virus-induced B lymphocyte cell lines producing specific antibody. Nature 269, 420-422 (1977).
15. Burioni, R. et al. Monoclonal antibodies isolated from human B cells neutralize a broad range of H1 subtype influenza A viruses including swine-origin influenza virus (S-OIV). Virology 399, 144-152 (2010).
16. Habersetzer, F. et al. Characterization of human monoclonal antibodies specific to the hepatitis C virus glycoprotein E2 with in vitro binding neutralization properties. Virology 249, 32-41 (1998).
17. Atlaw, T., Kozbor, D. & Roder, J. C. Human monoclonal antibodies against Mycobacterium leprae. Infect. Immun. 49, 104-110 (1985).
18. Cole, S. P., Campling, B. G., Atlaw, T., Kozbor, D. & Roder, J. C. Human monoclonal antibodies. Mol. Cell. Biochem. 62, 109-120 (1984).
19. Buchacher, A. et al. Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res. Hum. Retroviruses 10, 359-369 (1994).
20. Traggiai, E. et al. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nature Med. 10, 871-875 (2004).
21. Krause, J. C. et al. A broadly neutralizing human monoclonal antibody that recognizes a conserved, novel epitope on the globular head of the influenza H1N1 virus hemagglutinin. J. Virol. 85, 10905-10908 (2011).
22. Corti, D. et al. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest. 120, 1663-1673 (2010).
23. Krause, J. C. et al. Human monoclonal antibodies to pandemic 1957 H2N2 and pandemic 1968 H3N2 influenza viruses. J. Virol. 86, 6334-6340 (2012).
24. Yu, X. et al. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455, 532-536 (2008).
25. Bonsignori, M. et al. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J. Virol. 85, 9998-10009 (2011).
26. Corti, D. et al. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS ONE 5, e8805 (2010).
27. Walker, L. M. et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477, 466-470 (2011).
28. Macagno, A. et al. Isolation of human monoclonal antibodies that potently neutralize human cytomegalovirus infection by targeting different epitopes on the gH/gL/UL128-131A complex. J. Virol. 84, 1005-1013 (2010).
29. Beltramello, M. et al. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8, 271-283 (2010).
30. Dejnirattisai, W. et al. Cross-reacting antibodies enhance dengue virus infection in humans. Science 328, 745-748 (2010).
31. Smith, S. A. et al. Persistence of circulating memory B cell clones with potential for dengue virus disease enhancement for decades following infection. J. Virol. 86, 2665-2675 (2012).
32. Schieffelin, J. S. et al. Neutralizing and non-neutralizing monoclonal antibodies against dengue virus E protein derived from a naturally infected patient. Virol. J. 7, 28 (2010).
33. de Alwis, R. et al. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc. Natl Acad. Sci. USA 109, 7439-7444 (2012).
34. de Alwis, R. et al. In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl. Trop. Dis. 5, e1188 (2011).
35. Warter, L. et al. Chikungunya virus envelope-specific human monoclonal antibodies with broad neutralization potency. J. Immunol. 186, 3258-3264 (2011).
36. Collarini, E. J. et al. Potent high-affinity antibodies for treatment and prophylaxis of respiratory syncytial virus derived from B cells of infected patients. J. Immunol. 183, 6338-6345 (2009).
37. Yu, X., McGraw, P. A., House, F. S. & Crowe, J. E. Jr. An optimized electrofusion-based protocol for generating virus-specific human monoclonal antibodies. J. Immunol. Methods 336, 142-151 (2008).
38. Kwakkenbos, M. J. et al. Generation of stable monoclonal antibody-producing B cell receptor-positive human memory B cells by genetic programming. Nature Med. 16, 123-128 (2010).
39. Wardemann, H. et al. Predominant autoantibody production by early human B cell precursors. Science 301, 1374-1377 (2003).
40. Wardemann, H. & Nussenzweig, M. C. B-cell self-tolerance in humans. Adv. Immunol. 95, 83-110 (2007).
41. + human circulating memory B cells and bone marrow plasma cells. Proc. Natl Acad. Sci. USA 108, 18044-18048 (2011).
42. Meffre, E. The establishment of early B cell tolerance in humans: lessons from primary immunodeficiency diseases. Ann. NY Acad. Sci.1246, 1-10 (2011).
43. - human naive B cells contain mostly autoreactive unresponsive clones. Blood 115, 5026-5036 (2010).
44. Duty, J. A. et al. Functional anergy in a subpopulation of naive B cells from healthy humans that express autoreactive immunoglobulin receptors. J. Exp. Med. 206, 139-151 (2009).
45. Smith, K. et al. Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nature Protoc. 4, 372-384 (2009).
46. Casali, P., Inghirami, G., Nakamura, M., Davies, T. F. & Notkins, A. L. Human monoclonals from antigen-specific selection of B lymphocytes and transformation by EBV. Science 234, 476-479 (1986).
47. Weitkamp, J. H. et al. Generation of recombinant human monoclonal antibodies to rotavirus from single antigen-specific B cells selected with fluorescent virus-like particles. J. Immunol. Methods 275, 223-237 (2003).
48. Tiller, T. et al. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329, 112-124 (2008).
49. Scheid, J. F. et al. A method for identification of HIV gp140 binding memory B cells in human blood. J. Immunol. Methods 343, 65-67 (2009).
50. Di Niro, R. et al. Rapid generation of rotavirus-specific human monoclonal antibodies from small-intestinal mucosa. J. Immunol. 185, 5377-5383 (2010).
51. Di Niro, R. et al. High abundance of plasma cells secreting transglutaminase 2-specific IgA autoantibodies with limited somatic hypermutation in celiac disease intestinal lesions. Nature Med. 18, 441-445 (2012).
52. Scheid, J. F. et al. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458, 636-640 (2009).
53. Scheid, J. F. et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333, 1633-1637 (2011).
54. Mouquet, H. et al. Memory B cell antibodies to HIV-1 gp140 cloned from individuals infected with clade A and B viruses. PLoS ONE 6, e24078 (2011).
55. Wu, X. et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329, 856-861 (2010).
56. Wu, X. et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333, 1593-1602 (2011).
57. Whittle, J. R. et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc. Natl Acad. Sci. USA 108, 14216-14221 (2011).
58. Poulsen, T. R., Meijer, P. J., Jensen, A., Nielsen, L. S. & Andersen, P. S. Kinetic, affinity, and diversity limits of human polyclonal antibody responses against tetanus toxoid. J. Immunol. 179, 3841-3850 (2007).
59. Liao, H. X. et al. High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J. Virol. Methods 158, 171-179 (2009).
60. Bernasconi, N. L., Traggiai, E. & Lanzavecchia, A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298, 2199-2202 (2002).
61. Brokstad, K. A., Cox, R. J., Olofsson, J., Jonsson, R. & Haaheim, L. R. Parenteral influenza vaccination induces a rapid systemic and local immune response. J. Infect. Dis. 171, 198-203 (1995).
62. Sasaki, S. et al. Comparison of the influenza virus-specific effector and memory B-cell responses to immunization of children and adults with live attenuated or inactivated influenza virus vaccines. J. Virol. 81, 215-228 (2007).
63. Wrammert, J. et al. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453, 667-671 (2008).
64. Wrammert, J. et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J. Exp. Med. 208, 181-193 (2011).
65. Meijer, P. J. et al. Isolation of human antibody repertoires with preservation of the natural heavy and light chain pairing. J. Mol. Biol. 358, 764-772 (2006).
66. Poulsen, T. R., Jensen, A., Haurum, J. S. & Andersen, P. S. Limits for antibody affinity maturation and repertoire diversification in hypervaccinated humans. J. Immunol. 187, 4229-4235 (2011).
67. Sasaki, S. et al. Limited efficacy of inactivated influenza vaccine in elderly individuals is associated with decreased production of vaccine-specific antibodies. J. Clin. Invest. 121, 3109-3119 (2011).
68. Moody, M. A. et al. H3N2 influenza infection elicits more cross-reactive and less clonally expanded anti-hemagglutinin antibodies than influenza vaccination. PLoS ONE 6, e25797 (2011).
69. Reddy, S. T. & Georgiou, G. Systems analysis of adaptive immunity by utilization of high-throughput technologies. Curr. Opin. Biotechnol. 22, 584-589 (2011).
70. Krause, J. C. et al. Epitope-specific human influenza antibody repertoires diversify by B cell intraclonal sequence divergence and interclonal convergence. J. Immunol. 187, 3704-3711 (2011).
71. Cheung, W. C. et al. A proteomics approach for the identification and cloning of monoclonal antibodies from serum. Nature Biotech. 30, 447-452 (2012).
72. Kaur, K., Sullivan, M. & Wilson, P. C. Targeting B cell responses in universal influenza vaccine design. Trends Immunol. 32, 524-531 (2011).
73. Okuno, Y., Isegawa, Y., Sasao, F. & Ueda, S. A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J. Virol. 67, 2552-2558 (1993).
74. Ekiert, D. C. et al. Antibody recognition of a highly conserved influenza virus epitope. Science 324, 246-251 (2009).
75. Sui, J. et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nature Struct. Mol. Biol. 16, 265-273 (2009).
76. + memory B cells. PLoS ONE 3, e3942 (2008).
77. Xu, R. et al. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328, 357-360 (2010).
78. Thomson, C. A. et al. Pandemic H1N1 influenza infection and vaccination in humans induces cross-protective antibodies that target the hemagglutinin stem. Front. Immunol. 3, 1-19 (2012).
79. Li, G.-M. et al. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc. Natl Acad. Sci. USA 21 May 2012 (doi:10.1073/pnas.1118979109).
80. McMichael, A. J., Borrow, P., Tomaras, G. D., Goonetilleke, N. & Haynes, B. F. The immune response during acute HIV-1 infection: clues for vaccine development. Nature Rev. Immunol. 10, 11-23 (2010).
81. Pantophlet, R. & Burton, D. R. GP120: target for neutralizing HIV-1 antibodies. Annu. Rev. Immunol. 24, 739-769 (2006).
82. Moir, S., Malaspina, A. & Fauci, A. S. Prospects for an HIV vaccine: leading B cells down the right path. Nature Struct. Mol. Biol. 18, 1317-1321 (2011).
83. Kwong, P. D. & Wilson, I. A. HIV-1 and influenza antibodies: seeing antigens in new ways. Nature Immunol. 10, 573-578 (2009).
84. Simek, M. D. et al. Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J. Virol. 83, 7337-7348 (2009).
85. McLellan, J. S. et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-343 (2011).
86. Diskin, R. et al. Increasing the potency and breadth of an HIV antibody by using structure-based rational design. Science 334, 1289-1293 (2011).
87. Pejchal, R. et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334, 1097-1103 (2011).
88. Haynes, B. F., Kelsoe, G., Harrison, S. C. & Kepler, T. B. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nature Biotech. 30, 423-433 (2012).
89. Doria-Rose, N. A. et al. Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J. Virol. 83, 188-199 (2009).
90. Sather, D. N. et al. Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J. Virol. 83, 757-769 (2009).
91. Mouquet, H. et al. Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature 467, 591-595 (2010).
92. Zhou, T. et al. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445, 732-737 (2007).
93. Simmons, C. P. et al. Prophylactic and therapeutic efficacy of human monoclonal antibodies against H5N1 influenza. PLoS Med. 4, e178 (2007).
94. Hu, H. et al. A human antibody recognizing a conserved epitope of H5 hemagglutinin broadly neutralizes highly pathogenic avian influenza H5N1 viruses. J. Virol. 86, 2978-2989 (2012).
95. Kashyap, A. K. et al. Combinatorial antibody libraries from survivors of the Turkish H5N1 avian influenza outbreak reveal virus neutralization strategies. Proc. Natl Acad. Sci. USA 105, 5986-5991 (2008).
96. Tian, C. et al. Immunodominance of the VH1-46 antibody gene segment in the primary repertoire of human rotavirus-specific B cells is reduced in the memory compartment through somatic mutation of nondominant clones. J. Immunol. 180, 3279-3288 (2008).