Immunoglobulin analysis tool: A novel tool for the analysis of human and mouse heavy and light chain transcripts

Frontiers in Immunology

Volumn 3, Issue JUN, 2012, Pages 1-14

  Rogosch, Tobias ^a   Kerzel, Sebastian ^a   Hoi, Kam Hon ^b   Zhang, Zhixin ^c   Maier, Rolf F ^a   Ippolito, Gregory C ^d   Zemlin, Michael ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b The University of Texas at Austin   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Antibody repertoire; Deep sequencing; High throughput analysis; Immunoglobulin heavy chain gene; Immunoglobulin light chain gene; Rearrangement; Sequence analysis software; Somatic mutation

Indexed keywords

EID: 84874137715     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00176     Document Type: Article

References (80)

1. Ademokun, A., Wu, Y.C., Martin, V., Mitra, R., Sack, U., Baxendale, H., Kipling, D., and Dunn-Walters, D. K. (2011). Vaccination-induced changes in human B-cell repertoire and pneumococcal IgM and IgA antibody at different ages. Aging Cell 10, 922-930.
2. Alamyar, E., Giudicelli, V., Li, S., Duroux, P., and Lefranc, M. P. (2012). IMGT/HighV-QUEST: the IMGT® web portal for immunoglobulin (IG) or anti- body and T cell receptor (TR) analysis from NGS high throughput and deep sequencing. Immunome Res. 8, 26.
3. Arnaout, R., Lee, W., Cahill, P., Honan, T., Sparrow, T., Weiand, M., Nusbaum, C., Rajewsky, K., and Koralov, S. B. (2011). High-resolution description of anti-body heavy-chain repertoires in humans. PLoS ONE 6, e22365. doi:10.1371/journal.pone.0022365
4. Benichou, G., Yamada, Y., Yun, S.H., Lin, C., Fray, M., and Tocco, G. (2011). Immune recognition and rejection of allogeneic skin grafts. Immunotherapy 3, 757-770.
5. Berek, C., Griffiths, G. M., and Milstein, C. (1985). Molecular events during maturation of the immune response to oxazolone. Nature 316, 412-418.
6. Boyd, S. D., Marshall, E. L., Merker, J.D., Maniar, J.M., Zhang, L. N., Sahaf, B., Jones, C. D., Simen, B. B., Hanczaruk, B., Nguyen, K. D., Nadeau, K. C., Egholm, M., Miklos, D. B., Zehnder, J. L., and Fire, A. Z. (2009). Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci. Transl. Med. 1, 12ra23.
7. Brezinschek, H. P., Foster, S.J., Brezinschek, R.I., Dorner, T., Domiati-Saad, R., and Lipsky, P. E. (1997). Analysis of the human VH gene repertoire. Differential effects of selection and somatic hypermutation on human peripheral CD5(+)/IgM+ and CD5(-)/IgM+ B cells. J. Clin. Invest. 99, 2488-2501.
8. Brochet, X., Lefranc, M.P., and Giudicelli, V. (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.
9. Butler, J.E., Wertz, N., Weber, P., and Lager, K. M. (2008). Porcine reproductive and respiratory syndrome virus subverts repertoire development by proliferation of germlinencoded B cells of all isotypes bearing hydrophobic heavy chain CDR3. J. Immunol. 180, 2347-2356.
10. Chang, B., and Casali, P. (1994). The CDR1 sequences of a major proportion of human germline Ig VH genes are inherently susceptible to amino acid replacement. Immunol. Today 15, 367-373.
11. Coker, H.A., Harries, H.E., Banfield, G. K., Carr, V. A., Durham, S. R., Chevretton, E., Hobby, P., Sutton, B. J., and Gould, H. J. (2005). Biased use of VH5 IgE-positive B cells in the nasal mucosa in allergic rhinitis. J. Allergy Clin. Immunol. 116, 445-452.
12. Collis, A.V., Brouwer, A. P., and Martin, A. C. (2003). Analysis of the antigen combining site: correlations between length and sequence comosition of the hypervariable loops and the nature of the antigen. J. Mol. Biol. 325, 337-354.
13. Cuisinier, A.M., Gauthier, L., Boubli, L., Fougereau, M., and Ton- nelle, C. (1993). Mechanisms that generate human immunoglobulin diversity operate from the 8th week of gestation in fetal liver. Eur. J. Immunol. 23, 110-118.
14. Dahlke, I., Nott, D. J., Ruhno, J., Sewell, W. A., and Collins, A.M. (2006). Antigen selection in the IgE response of allergic and nonallergic individuals. J. Allergy Clin. Immunol. 117, 1477-1483.
15. Dorner, T., Brezinschek, H.P., Foster, S. J., Brezinschek, R.I., Farner, N. L., and Lipsky, P. E. (1998a). Delineation of selective influences shaping the mutated expressed human Ig heavy chain repertoire. J. Immunol. 160, 2831-2841.
16. Dorner, T., Foster, S.J., Farner, N.L., and Lipsky, P.E. (1998b). Immunoglobulin kappa chain receptor editing in systemic lupus erythematosus. J. Clin. Invest. 102, 688-694.
17. Dorner, T., and Lipsky, P. E. (2005). Molecular basis of immunoglobulin variable region gene usage in systemic autoimmunity. Clin. Exp. Med. 4, 159-169.
18. Eisenberg, D. (1984). Threedimensional structure of membrane and surface proteins. Annu. Rev. Biochem. 53, 595-623.
19. Feeney, A.J. (2011). Epigenetic regulation of antigen receptor gene rearrangement. Curr. Opin. Immunol. 23, 171-177.
20. Feeney, A.J., Atkinson, M.J., Cowan, M.J., Escuro, G., and Lugo, G. (1996). A defective Vkappa A2 allele in Navajos which may play a role in increased susceptibility to Haemophilus influenzae type b disease. J. Clin. Invest. 97, 2277-2282.
21. Frolich, D., Giesecke, C., Mei, H.E., Reiter, K., Daridon, C., Lipsky, P. E., and Dorner, T. (2010). Secondary immunization generates clonally related antigen-specific plasma cells and memory B cells. J. Immunol. 185, 3103-3110.
22. Giudicelli, V., Brochet, X., and Lefranc, M.P. (2011). IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb. Protoc. 2011, 695-715.
23. Glanville, J., Kuo, T.C., Von Budingen, H.C., Guey, L., Berka, J., Sundar, P. D., Huerta, G., Mehta, G. R., Oksenberg, J. R., Hauser, S. L., Cox, D. R., Rajpal, A., and Pons, J. (2011). Naive antibody gene-segment frequencies are heritable and unaltered by chronic lymphocyte ablation. Proc. Natl.Acad. Sci. U.S.A. 108, 20066-20071.
24. Glanville, J., Zhai, W., Berka, J., Telman, D., Huerta, G., Mehta, G. R., Ni, I., Mei, L., Sundar, P. D., Day, G. M., Cox, D., Rajpal, A., and Pons, J. (2009). Precise determination of the diversity of a combinatorial antibody library gives insight into the human immunoglobulin repertoire. Proc. Natl. Acad. Sci. U.S.A. 106, 20216-20221.
25. Gu, H., Kitamura, D., and Rajewsky, K. (1991). B cell development regu lated by gene rearrangement: arrest of maturation by membrane-bound D mu protein and selection of DH element reading frames. Cell 65, 47-54.
26. Hershberg, U., Uduman, M., Shlomchik, M. J., and Kleinstein, S. H. (2008). Improved methods for detecting selection by mutation analysis of IgV region sequences. Int. Immunol. 20, 683-694.
27. Ichihara, Y., Hayashida, H., Miyazawa, S., and Kurosawa, Y. (1989). Only DFL16, DSP2, and DQ52 gene families exist in mouse immunoglobulin heavy chain diversity gene loci, of which DFL16 and DSP2 originate from the same primordial DH gene. Eur. J. Immunol. 19, 1849-1854
28. Ippolito, G.C., Hon Hoi, K., Reddy, S. T., Carroll, S. M., Ge, X., Rogosch, T., Zemlin, M., Shultz, L. D., Ellington, A. D., Vandenberg, C. L., and Georgiou, G. (2012). Antibody repertoires in humanized NOD-scid- IL2Rg-null mice and human B cells reveals human-like diversification and tolerance checkpoints in the mouse. PLoS ONE. 7, e35497. doi: 10.1371/journal.pone.0035497
29. Ippolito, G.C.,Schelonka, R. L.,Zemlin, M., Ivanov, Ii, Kobayashi, R., Zemlin, C., Gartland, G. L., Nitschke, L., Pelkonen, J., Fujihashi, K., Rajewsky, K., and Schroeder, H. W. Jr. (2006). Forced usage of positively charged amino acids in immunoglobulin CDR-H3 impairs B cell development and antibody production. J. Exp. Med. 203, 1567-1578.
30. Jiang, N., Weinstein, J. A., Penland, L., White, R. A. III, Fisher, D. S., and Quake, S. R. (2011). Determinism and stochasticity during maturation of the zebrafish antibody repertoire. Proc. Natl. Acad. Sci. U.S.A. 108, 5348-5353.
31. Johnson, G., and Wu, T. T. (2000). Kabat database and its applications: 30 years after the first variability plot. Nucleic Acids Res. 28, 214-218.
32. Kabat, E.A., and Wu, T. T. (1991). Identical V region amino acid sequences and segments of sequences in antibodies of different specificities. Relative contributions of VH and VL genes, minigenes, and complementarity-determining regions to binding of antibody-combining sites. J. Immunol. 147, 1709-1719.
33. Kalinina, O., Doyle-Cooper, C. M., Miksanek, J., Meng, W., Prak, E. L., and Weigert, M. G. (2011). Alternative mechanisms of receptor editing in autoreactive B cells. Proc. Natl. Acad. Sci. U.S.A. 108, 7125-7130.
34. Kerzel, S., Rogosch, T., Struecker, B., Maier, R. F., and Zemlin, M. (2010). IgE transcripts in the circulation of allergic children reflect a classical antigen-driven B cell response and not a superantigen-like activation. J. Immunol. 185, 2253-2260.
35. Kolar, G.R., Yokota, T., Rossi, M. I., Nath, S. K., and Capra, J. D. (2004). Human fetal, cord blood, and adult lymphocyte progenitors have similar potential for generating B cells with a diverse immunoglobulin repertoire. Blood 104, 2981-2987.
36. Krishnan, M.R., Jou, N. T., and Marion, T. N. (1996). Correlation between the amino acid position of arginine in VH-CDR3 and specificity for native DNA among autoimmune antibodies. J. Immunol. 157, 2430-2439.
37. Kuroda, D., Shirai, H., Kobori, M., and Nakamura, H. (2008). Structural classification of CDR-H3 revisited: a lesson in antibody modeling. Proteins 73, 608-620.
38. Kurosaki, T., Shinohara, H., and Baba, Y. (2010). B cell signaling and fate decision. Annu. Rev. Immunol. 28, 21-55.
39. Kyte, J., and Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
40. Lefranc, M. P., Giudicelli, V., Ginestoux, C., Jabado-Michaloud, J., Folch, G., Bellahcene, F., Wu, Y., Gemrot, E., Brochet, X., Lane, J., Regnier, L., Ehrenmann, F., Lefranc, G., and Duroux, P. (2009). IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 37, D1006-D1012.
41. Logan, A.C., Gao, H., Wang, C., Sahaf, B.,Jones,C. D.,Marshall, E. L.,Buno, I., Armstrong, R., Fire, A. Z., Weinberg, K. I., Mindrinos, M., Zehnder, J. L., Boyd, S. D., Xiao, W., Davis, R. W., and Miklos, D. B. (2011). High-throughput VDJ sequencing for quantification of minimal residual disease in chronic lymphocytic leukemia and immune reconstitu- tion assessment. Proc. Natl.Acad. Sci. U.S.A. 108, 21194-21199.
42. Lossos, I.S., Tibshirani, R., Narasimhan, B., and Levy, R. (2000). The inference of antigen selection on Ig genes. J. Immunol. 165, 5122-5126.
43. Morea, V., Tramontano, A., Rustici, M., Chothia, C., and Lesk, A. M. (1998). Conformations of the third hypervariable region in the VH domain of immunoglobulins. J. Mol. Biol. 275, 269-294.
44. Morris, G.P., and Allen, P. M. (2012). How the TCR balances sensitivity and specificity for the recognition of self and pathogens. Nat. Immunol. 13, 121-128.
45. Padlan, E.A. (1994). Anatomy of the antibody molecule. Mol. Immunol. 31, 169-217.
46. Prabakaran, P., Chen, W., Singarayan, M. G., Stewart, C. C., Streaker, E., Feng, Y., and Dimitrov, D. S. (2012). Expressed antibody reper- toires in human cord blood cells: 454 sequencing and IMGT/HighV- QUEST analysis of germline gene usage, junctional diversity, and somatic mutations. Immunogenetics 64, 337-350.
47. Radic, M.Z., and Zouali, M. (1996). Receptor editing, immune diversifi cation, and self-tolerance. Immunity 5, 505-511.
48. Rajewsky, K. (1996). Clonal selection and learning in the antibody system. Nature 381, 751-758.
49. Ramsland, P.A., Kaushik, A., Marchalonis, J. J., and Edmundson, A. B. (2001). Incorporation of long CDR3s intoV domains: implications for the structural evolution of the antibody-combining site. Exp. Clin. Immunogenet. 18, 176-198.
50. Reddy, S.T., Ge, X., Miklos, A. E., Hughes, R. A., Kang, S. H., Hoi, K. H., Chrysostomou, C., Hunicke-Smith, S. P., Iverson, B. L., Tucker, P. W., Ellington, A. D., and Georgiou, G. (2010). Monoclonal antibodies isolated without screening by analyzing the variable-gene repertoire of plasma cells. Nat. Biotechnol. 28, 965-969.
51. Richl, P., Stern, U., Lipsky, P.E., and Girschick, H.J. (2008). The lambda gene immunoglobulin repertoire of human neonatal B cells. Mol. Immunol. 45, 320-327.
52. Rogosch, T., Kerzel, S., Sikula, L., Gentil, K., Liebetruth, M., Schlingmann, K. P., Maier, R. F., and Zemlin, M. (2010). Plasma cells and non- plasma B cells express differing IgE repertoires in allergic sensitization. J. Immunol. 184, 4947-4954.
53. Rosner, K., Winter, D. B., Tarone, R. E., Skovgaard, G. L., Bohr, V. A., and Gearhart, P. J. (2001). Third complementarity-determining region of mutatedVH immunoglobulin genes contains shorter V, D, J, P, and N components than non- mutated genes. Immunology 103, 179-187.
54. Sasso, E. H., Silverman, G. J., and Mannik, M. (1989). Human IgM mole- cules that bind staphylococcal protein A contain VHIII H chains. J. Immunol. 142, 2778-2783.
55. Schelonka, R. L., Tanner, J., Zhuang, Y., Gartland, G. L., Zemlin, M., and Schroeder, H. W. Jr. (2007). Categorical selection of the antibody repertoire in splenic B cells. Eur. J. Immunol. 37, 1010-1021.
56. Schroeder, H.W. Jr. (2006). Similarity and divergence in the development and expression of the mouse and human antibody repertoires. Dev. Comp. Immunol. 30, 119-135.
57. Schroeder, H.W. Jr., and Cavacini, L. (2010). Structure and function of immunoglobulins. J. Allergy Clin. Immunol. 125, S41-S52.
58. Schroeder, H.W. Jr., Hillson, J.L., and Perlmutter, R. M. (1987). Early restriction of the human antibody repertoire. Science 238, 791-793.
59. Schroeder, H.W. Jr., Zemlin, M., Khass, M., Nguyen, H. H., and Schelonka, R. L. (2010). Genetic control of DH reading frame and its effect on B-cell development and antigenspecific antibody production. Crit. Rev. Immunol. 30, 327-344.
60. Schroeder, H. W. Jr., Zhang, L., and Philips, J. B. III. (2001). Slow, programmed maturation of the immunoglobulin HCDR3 repertoire during the third trimester of fetal life. Blood 98, 2745-2751.
61. Shannon, C. E. (1997). The mathematical theory of communication, 1963. MD Comput. 14, 306-317.
62. Shirai, H., Kidera, A., and Nakamura, H. (1996). Structural classification of CDR-H3 in antibodies. FEBS Lett. 399, 1-8.
63. Shirai, H., Kidera, A., and Nakamura, H. (1999). H3-rules: identification of CDR-H3 structures in antibodies. FEBS Lett. 455, 188-197.
64. Snow, R. E., Chapman, C. J., Holgate, S. T.,and Stevenson,F. K. (1998). Clon- ally related IgE and IgG4 transcripts in blood lymphocytes of patients with asthma reveal differing patterns of somatic mutation. Eur. J. Immunol. 28, 3354-3361.
65. Souto-Carneiro, M. M., Sims, G.P., Girschik, H., Lee, J., and Lipsky, P. E. (2005). Developmental changes in the human heavy chain CDR3. J. Immunol. 175, 7425-7436.
66. Steininger, C., Widhopf, G. F. II, Ghia, E. M., Morello, C.S., Vanura, K., Sanders, R., Spector, D., Guiney, D., Jager, U., and Kipps, T. J. (2012). Recombinant antibodies encoded by IGHV1-69 react with pUL32, a phosphoprotein of cytomegalovirus and B-cell superantigen. Blood 119, 2293-2301.
67. Takhar, P., Corrigan, C. J., Smurthwaite, L., O'Connor, B. J., Durham, S. R., Lee, T. H., and Gould, H. J. (2007). Class switch recombination to IgE in the bronchial mucosa of atopic and nonatopic patients with asthma. J. Allergy Clin. Immunol. 119,213-218.
68. Tonegawa, S. (1983). Somatic generation of antibody diversity. Nature 302, 575-581.
69. Uduman, M., Yaari, G., Hershberg, U., Stern, J. A., Shlomchik, M. J., and Kleinstein, S. H. (2011). Detecting selection in immunoglobulin sequences. Nucleic Acids Res. 39, W499-W504.
70. Vale, A.M., Foote, J. B., Granato, A., Zhuang, Y., Pereira, R.M., Lopes, U. G., Bellio, M., Burrows, P. D., Schroeder, H. W. Jr., and Nobrega, A. (2012). A rapid and quantitative method for the evaluation of V gene usage,specificities and the clonal size of B cell repertoires. J. Immunol. Methods 376, 143-149.
71. Vrolix, K., Fraussen, J., Molenaar, P. C., Losen, M., Somers, V., Stinissen, P., De Baets, M. H., and Martinez-Martinez, P. (2010). The auto-antigen repertoire in myasthenia gravis. Autoimmunity 43, 380-400.
72. Wu, X., Zhou, T., Zhu, J., Zhang, B., Georgiev, I., Wang, C., Chen, X., Longo, N. S., Louder, M., Mckee, K., O'Dell, S., Perfetto, S., Schmidt, S. D., Shi, W., Wu, L., Yang, Y., Yang, Z. Y., Yang, Z., Zhang, Z., Bonsignori, M., Crump, J. A., Kapiga, S. H., Sam, N. E., Haynes, B. F., Simek, M., Burton, D. R., Koff, W. C., Doria-Rose, N. A., Connors, M., Mullikin, J. C., Nabel, G. J., Roederer, M., Shapiro, L., Kwong, P. D., and Mascola, J. R. (2011). Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333, 1593-1602.
73. Wu, Y.C., Kipling, D., Leong, H. S., Martin, V., Ademokun, A. A., and Dunn-Walters, D. K. (2010). Highthroughput immunoglobulin repertoire analysis distinguishes between human IgM memory and switched memory B-cell populations. Blood 116, 1070-1078.
74. Xu, J. L., and Davis, M. M. (2000). Diversity in the CDR3 region of V(H) is sufficient for most antiody specificities. Immunity 13, 37-45.
75. Zemlin, M., Bauer, K., Hummel, M., Pfeiffer, S., Devers, S., Zemlin, C., Stein, H., and Versmold, H. T. (2001). The diversity of rearranged immunoglobulin heavy chain variable region genes in peripheral blood B cells of preterm infants is restricted by short third complementarity-determining regions but not by limited gene segment usage. Blood 97, 1511-1513.
76. Zemlin, M., Hoersch, G., Zemlin, C., Pohl-Schickinger, A., Hummel, M., Berek, C., Maier, R. F., and Bauer, K. (2007). The postnatal maturation of the immunoglobulin heavy chain IgG repertoire in human preterm neonates is slower than in term neonates. J. Immunol. 178, 1180-1188.
77. Zemlin, M., Klinger, M., Link, J., Zemlin, C., Bauer, K., Engler, J. A., Schroeder, H. W. Jr., and Kirkham, P. M. (2003). Expressed murine and human CDR-H3 intervals of equal length exhibit distinct repertoires that differ in their amino acid composition and predicted range of structures. J. Mol. Biol. 334, 733-749.
78. Zhang, Z., Zemlin, M., Wang, Y.H., Munfus, D., Huye, L.E., Findley, H. W., Bridges, S. L., Roth, D. B., Burrows, P. D., and Cooper, M. D. (2003). Contribution of VH gene replacement to the primary B cell repertoire. Immunity 19, 21-31.
79. Zouali, M. (1995). B-cell superantigens: implications for selection of the human antibody repertoire. Immunol. Today 16, 399-405.
80. Zuckerman, N.S., Hazanov, H., Barak, M., Edelman, H., Hess, S., Shcolnik, H., Dunn-Walters, D., and Mehr, R. (2010). Somatic hypermutation and antigen-driven selection of B cells are altered in autoimmune diseases. J. Autoimmun. 35, 325-335.