Identification of antigen-specific B cell receptor sequences using public repertoire analysis

Journal of Immunology

Volumn 194, Issue 1, 2015, Pages 252-261

  Trück, Johannes ^a,d   Ramasamy, Maheshi N ^a   Galson, Jacob D ^a   Rance, Richard ^b   Parkhill, Julian ^b   Lunter, Gerton ^c   Pollard, Andrew J ^a   Kelly, Dominic F ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; GROUP C MENINGOCOCCAL POLYSACCHARIDE VACCINE; HAEMOPHILUS INFLUENZAE TYPE B VACCINE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN M; MENINGOCOCCUS VACCINE; MENITORIX; TETANUS TOXOID; UNCLASSIFIED DRUG; BACTERIAL POLYSACCHARIDE; BACTERIUM ANTIBODY; HAEMOPHILUS INFLUENZAE TYPE B POLYSACCHARIDE VACCINE; HAEMOPHILUS VACCINE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; MENINGOCOCCAL GROUP C POLYSACCHARIDE; MENINGOCOCCAL GROUP C POLYSACCHARIDE-TETANUS TOXOID CONJUGATE; VACCINE;

ADULT; AGED; AMINO ACID SEQUENCE; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; HUMAN; HUMAN EXPERIMENT; IMMUNOGENICITY; INFLUENZA B; INFLUENZA VACCINATION; NORMAL HUMAN; SEQUENCE ANALYSIS; TETANUS; TETANUS PROPHYLAXIS; VACCINATION REACTION; ADOLESCENT; B LYMPHOCYTE; BACTERIAL CAPSULE; GENETICS; HAEMOPHILUS INFLUENZAE TYPE B; HIGH THROUGHPUT SEQUENCING; IMMUNOLOGY; MIDDLE AGED; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AMINO ACID SEQUENCE; ANTIBODIES, BACTERIAL; B-LYMPHOCYTES; BACTERIAL CAPSULES; HAEMOPHILUS INFLUENZAE TYPE B; HAEMOPHILUS VACCINES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN M; MENINGOCOCCAL VACCINES; MIDDLE AGED; POLYSACCHARIDES, BACTERIAL; RECEPTORS, ANTIGEN, B-CELL; SEQUENCE ANALYSIS, PROTEIN; TETANUS TOXOID; VACCINES, COMBINED; VACCINES, CONJUGATE; YOUNG ADULT;

EID: 84919667651     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401405     Document Type: Article

References (60)

1. Tonegawa, S. 1983. Somatic generation of antibody diversity. Nature 302: 575-581.
2. Glanville, J., W. Zhai, J. Berka, D. Telman, G. Huerta, G. R. Mehta, I. Ni, L. Mei, P. D. Sundar, G. M. Day, et al. 2009. Precise determination of the diversity of a combinatorial antibody library gives insight into the human immunoglobulin repertoire. Proc. Natl. Acad. Sci. USA 106: 20216-20221.
3. Ohno, S., N. Mori, and T. Matsunaga. 1985. Antigen-binding specificities of antibodies are primarily determined by seven residues of VH. Proc. Natl. Acad. Sci. USA 82: 2945-2949.
4. Noel, D., T. Bernardi, I. Navarro-Teulon, M. Marin, J. P. Martinetto, F. Ducancel, J. C. Mani, B. Pau, M. Piechaczyk, and M. Biard-Piechaczyk. 1996. Analysis of the individual contributions of immunoglobulin heavy and light chains to the binding of antigen using cell transfection and plasmon resonance analysis. J. Immunol. Methods 193: 177-187.
5. Xu, J. L., and M. M. Davis. 2000. Diversity in the CDR3 region of V(H) is sufficient for most antibody specificities. Immunity 13: 37-45.
6. Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader, L. A. Bemben, J. Berka, M. S. Braverman, Y. J. Chen, Z. Chen, et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors [Published erratum appears in 2006 Nature 441: 120]. Nature 437: 376-380.
7. Georgiou, G., G. C. Ippolito, J. Beausang, C. E. Busse, H. Wardemann, and S. R. Quake. 2014. The promise and challenge of high-throughput sequencing of the antibody repertoire. Nat. Biotechnol. 32: 158-168.
8. Galson, J. D., A. J. Pollard, J. Truck, and D. F. Kelly. 2014. Studying the antibody repertoire after vaccination: Practical applications. Trends Immunol. 35: 319-331.
9. Boyd, S. D., B. A. Gaëta, K. J. Jackson, A. Z. Fire, E. L. Marshall, J. D. Merker, J. M. Maniar, L. N. Zhang, B. Sahaf, C. D. Jones, et al. 2010. Individual variation in the germline Ig gene repertoire inferred from variable region gene rearrangements. J. Immunol. 184: 6986-6992.
10. Boyd, S. D., E. L. Marshall, J. D. Merker, J. M. Maniar, L. N. Zhang, B. Sahaf, C. D. Jones, B. B. Simen, B. Hanczaruk, K. D. Nguyen, et al. 2009. Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci. Transl. Med. 1: 12ra23.
11. Wu, Y. C., D. Kipling, H. S. Leong, V. Martin, A. A. Ademokun, and D. K. Dunn-Walters. 2010. High-throughput immunoglobulin repertoire analysis distinguishes between human IgM memory and switched memory B-cell populations. Blood 116: 1070-1078.
12. Briney, B. S., J. R.Willis, B. A. McKinney, and J. E. Crowe, Jr. 2012. High-throughput antibody sequencing reveals genetic evidence of global regulation of the naïve and memory repertoires that extends across individuals. Genes Immun. 13: 469-473.
13. Prabakaran, P., Z. Zhu, W. Chen, R. Gong, Y. Feng, E. Streaker, and D. S. Dimitrov. 2012. Origin, diversity, and maturation of human antiviral antibodies analyzed by high-throughput sequencing. Front. Microbiol. 3: 277.
14. Fernández-Sánchez, A., M. García-Ocan a, and J. R. de los Toyos. 2009. Mouse monoclonal antibodies to pneumococcal C-polysaccharide backbone show restricted usage of VH-DH-JH gene segments and share the same kappa chain. Immunol. Lett. 123: 125-131.
15. Kolibab, K., S. L. Smithson, A. K. Shriner, S. Khuder, S. Romero-Steiner, G. M. Carlone, and M. A. Westerink. 2005. Immune response to pneumococcal polysaccharides 4 and 14 in elderly and young adults. I. Antibody concentrations, avidity and functional activity. Immun. Ageing 2: 10.
16. Zhou, J., K. R. Lottenbach, S. J. Barenkamp, A. H. Lucas, and D. C. Reason. 2002. Recurrent variable region gene usage and somatic mutation in the human antibody response to the capsular polysaccharide of Streptococcus pneumoniae type 23F. Infect. Immun. 70: 4083-4091.
17. Wisnewski, A., L. Cavacini, and M. Posner. 1996. Human antibody variable region gene usage in HIV-1 infection. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 11: 31-38.
18. Binley, J. M., E. A. Lybarger, E. T. Crooks, M. S. Seaman, E. Gray, K. L. Davis, J. M. Decker, D. Wycuff, L. Harris, N. Hawkins, et al. 2008. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82: 11651-11668.
19. Tian, C., G. K. Luskin, K. M. Dischert, J. N. Higginbotham, B. E. Shepherd, and J. E. J. Crowe, Jr. 2008. 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.
20. Chardes, T., N. Chapal, D. Bresson, C. Bes, V. Giudicelli, M. P. Lefranc, and S. Péraldi-Roux. 2002. The human anti-thyroid peroxidase autoantibody repertoire in Graves' and Hashimoto's autoimmune thyroid diseases. Immunogenetics 54: 141-157.
21. Parameswaran, P., Y. Liu, K. M. Roskin, K. K. Jackson, V. P. Dixit, J. Y. Lee, K. L. Artiles, S. Zompi, M. J. Vargas, B. B. Simen, et al. 2013. Convergent antibody signatures in human dengue. Cell Host Microbe 13: 691-700.
22. Jackson, K. J., Y. Liu, K. M. Roskin, J. Glanville, R. A. Hoh, K. Seo, E. L. Marshall, T. C. Gurley, M. A. Moody, B. F. Haynes, et al. 2014. Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements. Cell Host Microbe 16: 105-114.
23. Insel, R. A., A. Kittelberger, and P. Anderson. 1985. Isoelectric focusing of human antibody to the Haemophilus influenzae b capsular polysaccharide: Restricted and identical spectrotypes in adults. J. Immunol. 135: 2810-2816.
24. Adderson, E. E., P. G. Shackelford, A. Quinn, P. M. Wilson, M. W. Cunningham, R. A. Insel, and W. L. Carroll. 1993. Restricted immunoglobulin VH usage and VDJ combinations in the human response to Haemophilus influenzae type b capsular polysaccharide. Nucleotide sequences of monospecific anti-Haemophilus antibodies and polyspecific antibodies cross-reacting with self antigens. J. Clin. Invest. 91: 2734-2743.
25. Silverman, G. J., and A. H. Lucas. 1991. Variable region diversity in human circulating antibodies specific for the capsular polysaccharide of Haemophilus influenzae type b. Preferential usage of two types of VH3 heavy chains. J. Clin. Invest. 88: 911-920.
26. Lucas, A. H., G. R. McLean, D. C. Reason, A. P. O'Connor, M. C. Felton, and K. D. Moulton. 2003. Molecular ontogeny of the human antibody repertoire to the Haemophilus influenzae type B polysaccharide: Expression of canonical variable regions and their variants in vaccinated infants. Clin. Immunol. 108: 119-127.
27. Lucas, A. H., and D. C. Reason. 1999. Polysaccharide vaccines as probes of antibody repertoires in man. Immunol. Rev. 171: 89-104.
28. Poulsen, T. R., P. J. Meijer, A. Jensen, L. S. Nielsen, and P. S. Andersen. 2007. Kinetic, affinity, and diversity limits of human polyclonal antibody responses against tetanus toxoid. J. Immunol. 179: 3841-3850.
29. Lavinder, J. J., Y. Wine, C. Giesecke, G. C. Ippolito, A. P. Horton, O. I. Lungu, K. H. Hoi, B. J. DeKosky, E. M. Murrin, M. M. Wirth, et al. 2014. Identification and characterization of the constituent human serum antibodies elicited by vaccination. Proc. Natl. Acad. Sci. USA 111: 2259-2264.
30. Goldblatt, D., A. R. Vaz, and E. Miller. 1998. Antibody avidity as a surrogate marker of successful priming by Haemophilus influenzae type b conjugate vaccines following infant immunization. J. Infect. Dis. 177: 1112-1115.
31. Romero-Steiner, S., P. F. Holder, P. Gomez de Leon, W. Spear, T. W. Hennessy, and G. M. Carlone. 2005. Avidity determinations for Haemophilus influenzae Type b anti-polyribosylribitol phosphate antibodies. Clin. Diagn. Lab. Immunol. 12: 1029-1035.
32. Brochet, X., M. P. Lefranc, and V. Giudicelli. 2008. IMGT/V-QUEST: The highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 36: W503-W508.
33. R Core Team. 2013. R Foundation for Statistical Computing. Available at: Http: // www.r-project.org/foundation/.
34. Wickham, H. W. 2009. ggplot2: Elegant graphics for data analysis. Springer, New York.
35. Adderson, E. E., P. G. Shackelford, A. Quinn, and W. L. Carroll. 1991. Restricted Ig H chain V gene usage in the human antibody response to Haemophilus influenzae type b capsular polysaccharide. J. Immunol. 147: 1667-1674.
36. Poulsen, T. R., A. Jensen, J. S. Haurum, and P. S. Andersen. 2011. Limits for antibody affinity maturation and repertoire diversification in hypervaccinated humans. J. Immunol. 187: 4229-4235.
37. Frölich, D., C. Giesecke, H. E. Mei, K. Reiter, C. Daridon, P. E. Lipsky, and T. Dörner. 2010. Secondary immunization generates clonally related antigenspecific plasma cells and memory B cells. J. Immunol. 185: 3103-3110.
38. DeKosky, B. J., G. C. Ippolito, R. P. Deschner, J. J. Lavinder, Y. Wine, B. M. Rawlings, N. Varadarajan, C. Giesecke, T. Dörner, S. F. Andrews, et al. 2013. High-throughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat. Biotechnol. 31: 166-169.
39. Faber, C., L. Shan, Z. Fan, L. W. Guddat, C. Furebring, M. Ohlin, C. A. Borrebaeck, and A. B. Edmundson. 1998. Three-dimensional structure of a human Fab with high affinity for tetanus toxoid. Immunotechnology 3: 253-270.
40. Li, G. M., C. Chiu, J. Wrammert, M. McCausland, S. F. Andrews, N. Y. Zheng, J. H. Lee, M. Huang, X. Qu, S. Edupuganti, et al. 2012. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly crossreactive memory B cells. Proc. Natl. Acad. Sci. USA 109: 9047-9052.
41. Krause, J. C., T. Tsibane, T. M. Tumpey, C. J. Huffman, B. S. Briney, S. A. Smith, C. F. Basler, and J. E. Crowe, Jr. 2011. Epitope-specific human influenza antibody repertoires diversify by B cell intraclonal sequence divergence and interclonal convergence. J. Immunol. 187: 3704-3711.
42. Hutchins, W. A., A. R. Adkins, T. Kieber-Emmons, and M. A. J. Westerink. 1996. Molecular characterization of a monoclonal antibody produced in response to a group C meningococcal polysaccharide peptide mimic. Mol. Immunol. 33: 503-510.
43. Smithson, S. L., N. Srivastava, W. A. Hutchins, and M. A. Westerink. 1999. Molecular analysis of the heavy chain of antibodies that recognize the capsular polysaccharide of Neisseria meningitidis in hu-PBMC reconstituted SCID mice and in the immunized human donor. Mol. Immunol. 36: 113-124.
44. Lunter, G., and M. Goodson. 2011. Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21: 936-939.
45. Wilming, L. G., J. G. Gilbert, K. Howe, S. Trevanion, T. Hubbard, and J. L. Harrow. 2008. The vertebrate genome annotation (Vega) database. Nucleic Acids Res. 36: D753-D760.
46. Ademokun, A., Y. C. Wu, V. Martin, R. Mitra, U. Sack, H. Baxendale, D. Kipling, and D. K. Dunn-Walters. 2011. Vaccination-induced changes in human B-cell repertoire and pneumococcal IgM and IgA antibody at different ages. Aging Cell 10: 922-930.
47. Jiang, N., J. He, J. A. Weinstein, L. Penland, S. Sasaki, X. S. He, C. L. Dekker, N. Y. Zheng, M. Huang, M. Sullivan, et al. 2013. Lineage structure of the human antibody repertoire in response to influenza vaccination. Sci. Transl. Med. 5: 171ra19.
48. Zhu, J., S. O'Dell, G. Ofek, M. Pancera, X. Wu, B. Zhang, Z. Zhang, J. C. Mullikin, M. Simek, D. R. Burton, et al; NISC Comparative Sequencing Program. 2012. Somatic Populations of PGT135-137 HIV-1-Neutralizing Antibodies Identified by 454 Pyrosequencing and Bioinformatics. Front. Microbiol. 3: 315.
49. Wu, X., T. Zhou, J. Zhu, B. Zhang, I. Georgiev, C. Wang, X. Chen, N. S. Longo, M. Louder, K. McKee, et al; NISC Comparative Sequencing Program. 2011. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333: 1593-1602.
50. Weitkamp, J. H., N. Kallewaard, K. Kusuhara, E. Bures, J. V. Williams, B. LaFleur, H. B. Greenberg, and J. E. Crowe, Jr. 2003. Infant and adult human B cell responses to rotavirus share common immunodominant variable gene repertoires. J. Immunol. 171: 4680-4688.
51. Rohatgi, S., D. Dutta, S. Tahir, and D. Sehgal. 2009. Molecular dissection of antibody responses against pneumococcal surface protein A: Evidence for diverse DH-less heavy chain gene usage and avidity maturation. J. Immunol. 182: 5570-5585.
52. Wrammert, J., K. Smith, J. Miller, W. A. Langley, K. Kokko, C. Larsen, N. Y. Zheng, I. Mays, L. Garman, C. Helms, et al. 2008. Rapid cloning of highaffinity human monoclonal antibodies against influenza virus. Nature 453: 667-671.
53. Wu, Y. C., D. Kipling, and D. K. Dunn-Walters. 2012. Age-Related Changes in Human Peripheral Blood IGH Repertoire Following Vaccination. Front. Immunol. 3: 193.
54. Vollmers, C., R. V. Sit, J. A. Weinstein, C. L. Dekker, and S. R. Quake. 2013. Genetic measurement of memory B-cell recall using antibody repertoire sequencing. Proc. Natl. Acad. Sci. USA 110: 13463-13468.
55. Liu, L., and A. H. Lucas. 2003. IGH V3-23∗03 differ in their capacity to form the canonical human antibody combining site specific for the capsular polysaccharide of Haemophilus influenzae type b. Immunogenetics 55: 336-338.
56. Oh, S. Y., D. Griffiths, T. John, Y. C. Lee, L. M. Yu, N. McCarthy, P. T. Heath, D. Crook, M. Ramsay, E. R. Moxon, and A. J. Pollard. 2008. School-Aged children: A reservoir for continued circulation of Haemophilus influenzae type b in the United Kingdom. J. Infect. Dis. 197: 1275-1281.
57. Herrmann, D. J., R. G. Hamilton, T. Barington, C. E. Frasch, G. Arakere, O. Mäkelä, L. A. Mitchell, J. Nagel, G. T. Rijkers, B. Zegers, et al. 1992. Quantitation of human IgG subclass antibodies to Haemophilus influenzae type b capsular polysaccharide. Results of an international collaborative study using enzyme immunoassay methodology. J. Immunol. Methods 148: 101-114.
58. Engström, P. E., S. Nava, S. Mochizuki, and G. Norhagen. 1995. Quantitative analysis of IgA-subclass antibodies against tetanus toxoid. J. Immunoassay 16: 231-245.
59. van Riet, E., K. Retra, A. A. Adegnika, C. M. Jol-van der Zijde, H. W. Uh, B. Lell, S. Issifou, P. G. Kremsner, M. Yazdanbakhsh, M. J. van Tol, and F. C. Hartgers. 2008. Cellular and humoral responses to tetanus vaccination in Gabonese children. Vaccine 26: 3690-3695.
60. Kroon, F. P., M. J. van Tol, C. M. Jol-van der Zijde, R. van Furth, and J. T. van Dissel. 1999. Immunoglobulin G (IgG) subclass distribution and IgG1 avidity of antibodies in human immunodeficiency virus-infected individuals after revaccination with tetanus toxoid. Clin. Diagn. Lab. Immunol. 6: 352-355.