Nucleotide insertions and deletions complement point mutations to massively expand the diversity created by somatic hypermutation of antibodies

Journal of Biological Chemistry

Volumn 289, Issue 48, 2014, Pages 33557-33567

  Bowers, Peter M ^a   Verdino, Petra ^a   Wang, Zhengyuan ^a   Da Silva Correia, Jean ^a   Chhoa, Mark ^a   Macondray, Griffin ^a   Do, Minjee ^a   Neben, Tamlyn Y ^a   Horlick, Robert A ^a   Stanfield, Robyn L ^b   Wilson, Ian A ^b   King, David J ^a  

^a AnaptysBio Inc   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; CONVOLUTIONAL CODES; NUCLEOTIDES;

ACTIVATION INDUCED CYTIDINE DEAMINASE; AFFINITY MATURATION; ANTIBODY BINDING; ANTIBODY MATURATION; CLONAL SELECTION; INSERTIONS AND DELETIONS; SOMATIC HYPERMUTATION; STRUCTURAL DETERMINATION;

ANTIBODIES;

ANTIBODY; CYTIDINE DEAMINASE; COMPLEMENTARITY DETERMINING REGION;

ANTIBODY AFFINITY; ANTIBODY STRUCTURE; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; COMPLEMENT SYSTEM; ENZYME ACTIVATION; GENE DELETION; GENE INSERTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INDEL MUTATION; MOLECULAR EVOLUTION; POINT MUTATION; SEQUENCE ANALYSIS; SOMATIC HYPERMUTATION; COMPLEMENTARITY DETERMINING REGION; FEMALE; GENETICS; MALE; METABOLISM;

COMPLEMENTARITY DETERMINING REGIONS; CYTIDINE DEAMINASE; FEMALE; HUMANS; INDEL MUTATION; MALE; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 84912062551     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.607176     Document Type: Article

References (49)

1. Peled, J. U., Kuang, F. L., Iglesias-Ussel, M. D., Roa, S., Kalis, S. L., Goodman, M. F., and Scharff, M. D. (2008) The biochemistry of somatic hypermutation. Annu. Rev. Immunol. 26, 481-511
2. Klein, F., Mouquet, H., Dosenovic, P., Scheid, J. F., Scharf, L., and Nussenzweig, M. C. (2013) Antibodies in HIV-1 vaccine development and therapy. Science 341, 1199-1204
3. Throsby, M., van den Brink, E., Jongeneelen, M., Poon, L. L., Alard, P., Cornelissen, L., Bakker, A., Cox, F., van Deventer, E., Guan, Y., Cinatl, J., ter Meulen, J., Lasters, I., Carsetti, R., Peiris, M., de Kruif, J., and Goudsmit, J. (2008) Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory cells. PLoS One. 3, e3942
4. Ekiert, D. C., Bhabha, G., Elsliger, M. A., Friesen, R. H., Jongeneelen, M., Throsby, M., Goudsmit, J., and Wilson, I. A. (2009) Antibody recognition of a highly conserved influenza virus epitope. Science 324, 246-251
5. Briney, B. S., Willis, J. R., and Crowe, J. E., Jr. (2012) Location and length distribution of somatic hypermutation-associated DNA insertions and deletions reveals regions of antibody structural plasticity. Genes Immun. 13, 523-529
6. Goossens, T., Klein, U., and Küppers, R. (1998) Frequent occurrence of deletion and duplications during somatic hypermutation: implications for oncogene translocations and heavy chain disease. Proc. Natl. Acad. Sci. U.S.A. 95, 2463-2468
7. Briney, B. S., and Crowe, J. E., Jr. (2013) Secondary mechanisms of diversification in the human antibody repertoire. Front. Immunol. 4, 42
8. Miura, Y., Chu, C. C., Dines, D. M., Asnis, S. E., Furie, R. A., and Chiorazzi, N. (2003) Diversification of the Ig variable region gene repertoire of synovial B lymphocytes by nucleotide insertion and deletion. Mol. Med. 9, 166-174
9. Wilson, P. C., de Bouteiller, O., Liu, Y.-J., Potter, K., Banchereau, J., Capra, J. D., and Pascual, V. (1998) Somatic hypermutation introduces insertions and deletions into immunoglobulin V genes. J. Exp. Med. 187, 59-70
10. de Wildt, R. M., van Venrooij, W. J., Winter, G., Hoet, R. M., and Tomlinson, I. M. (1999) Somatic insertions and deletions shape the human antibody repertoire. J. Mol. Biol. 294, 701-710
11. Reason, D. C., and Zhou, J. (2006) Codon insertion and deletion functions as a somatic diversification in human antibody repertoires. Biol. Direct. 1, 24
12. Zhou, C., Jacobsen, F. W., Cai, L., Chen, Q., and Shen, W. D. (2010) Development of a novel mammalian cell surface antibody display platform. mAbs 2, 508-518
13. Walker, L. M., Phogat, S. K., Chan-Hui, P. Y., Wagner, D., Phung, P., Goss, J. L., Wrin, T., Simek, M. D., Fling, S., Mitcham, J. L., Lehrman, J. K., Priddy, F. H., Olsen, O. A., Frey, S. M., Hammond, P. W., Protocol G Principal Investigators, Kaminsky, S., Zamb, T., Moyle, M., Koff, W. C., Poignard, P., and Burton, D. R. (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289
14. 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., NISC Comparative Sequencing Program, 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
15. Pejchal, R., Doores, K. J., Walker, L. M., Khayat, R., Huang, P. S., Wang, S. K., Stanfield, R. L., Julien, J. P., Ramos, A., Crispin, M., Depetris, R., Katpally, U., Marozsan, A., Cupo, A., Maloveste, S., Liu, Y., McBride, R., Ito, Y., Sanders, R. W., Ogohara, C., Paulson, J. C., Feizi, T., Scanlan, C. N., Wong, C. H., Moore, J. P., Olson, W. C., Ward, A. B., Poignard, P., Schief, W. R., Burton, D. R., and Wilson, I. A. (2011) A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334, 1097-1103
16. Krause, J. C., Ekiert, D. C., Tumpey, T. M., Smith, P. B., Wilson, I. A., and Crowe, J. E., Jr. (2011) An insertion mutation that distorts antibody binding site architecture enhances function of a human antibody. mBio 2, e00345-e00310
17. Ekiert, D. C., Kashyap, A. K., Steel, J., Rubrum, A., Bhabha, G., Khayat, R., Lee, J. H., Dillon, M. A., O'Neil, R. E., Faynboym, A. M., Horowitz, M., Horowitz, L., Ward, A. B., Palese, P., Webby, R., Lerner, R. A., Bhatt, R. R., and Wilson, I. A. (2012) Cross-neutralization of influenza A viruses mediated by a single antibody. Nature 489, 526-532
18. Bowers, P. M., Horlick, R. A., Kehry, M. R., Neben, T. Y., Tomlinson, G. L., Altobell, L., Zhang, X., Macomber, J. L., Krapf, I. P., Wu, B. F., McConnell, A. D., Chau, B., Berkebile, A. D., Hare, E., Verdino, P., and King, D. J. (2014) Mammalian cell display for the discovery and optimization of antibody therapeutics. Methods 65, 44-56
19. Bowers, P. M., Horlick, R. A., Neben, T. Y., Toobian, R. M., Tomlinson, G. L., Dalton, J. L., Jones, H. A., Chen, A., Altobell, L., 3rd., Zhang, X., Macomber, J. L., Krapf, I. P., Wu, B. F., McConnell, A., Chau, B., Holland, T., Berkebile, A. D., Neben, S. S., Boyle, W. J., and King, D. J. (2011) Coupling mammalian cell surface display with somatic hypermutation for the discovery and maturation of human antibodies. Proc. Natl. Acad. Sci. U.S.A. 108, 20455-20460
20. Horlick, R. A., Macomber, J. L., Bowers, P. M., Neben, T. Y., Tomlinson, G. L., Krapf, I. P., Dalton, J. L., Verdino, P., and King, D. J. (2013) Simultaneous surface display and secretion of proteins from mammalian cells facilitates efficient in vitro selection and maturation of antibodies. J. Biol. Chem. 288, 19861-19869
21. Ye, J., Ma, N., Madden, T. L., and Ostell, J. M. (2013) IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res. 41, W34-W40
22. Koboldt, D. C., Chen, K., Wylie, T., Larson, D. E., McLellan, M. D., Mardis, E. R., Weinstock, G. M., Wilson, R. K., and Ding, L. (2009) VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 25, 2283-2285
23. Smith, T. F., and Waterman, M. S. (1981) Identification of common molecular subsequences. J. Mol. Biol. 147, 195-197
24. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
25. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
26. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
27. McCoy, A. J., Grosse-Kunstleve, R. W., Storoni, L. C., and Read, R. J. (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458-464
28. Winn, M. D., Murshudov, G. N., and Papiz, M. Z. (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374, 300-321
29. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
30. Sale, J. E., and Neuberger, M. S. (1998) TdT-accessible breaks are scattered over the immunoglobulin V domain in a constitutively hypermutation B cell line. Immunity 9, 859-869
31. Stanfield, R., Cabezas, E., Satterthwait, A., Stura, E., Profy, A., and Wilson, I. (1999) Dual conformations for the HIV-1 gp120 V3 loop in complexes with different neutralizing fabs. Structure 7, 131-142
32. Rogozin, I. B., and Diaz, M. (2004) Cutting Edge: DGYW/WRCH is a better predictor of mutability at G:C bases in Ig hypermutation than the widely accepted RGYW/WRCY motif and probably reflects a two-step activation-induced cytidine deaminase-triggered process. J. Immunol. 172, 3382-3384
33. Dörner, T., Foster, S. J., Farner, N. L., and Lipsky, P. E. (1998) Somatic hypermutation of human immunoglobulin heavy chain genes: targeting of RGYW motifs on both DNA strands. Eur. J. Immunol. 28, 3384-3396
34. Bransteitter, R., Pham, P., Scharff, M. D., and Goodman, M. F. (2003) Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl. Acad. Sci. U.S.A. 100, 4102-4107
35. Chaudhuri, J., Tian, M., Khuong, C., Chua, K., Pinaud, E., and Alt, F. W. (2003) Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422, 726-730
36. Chothia, C., Lesk, A. M., Tramontano, A., Levitt, M., Smith-Gill, S. J., Air, G., Sheriff, S., Padlan, E. A., Davies, D., and Tulip, W. R. (1989) Conformations of immunoglobulin hypervariable regions. Nature 342, 877-883
37. Martin, A. C., and Thornton, J. M. (1996) Structural families of loops in homologous proteins: automatic classification, modelling, and application to antibodies. J. Mol. Biol. 263, 800-815
38. Wang, F., Ekiert, D. C., Ahmad, I., Yu, W., Zhang, Y., Bazirgan, O., Torkamani, A., Raudsepp, T., Mwangi, W., Criscitiello, M. F., Wilson, I. A., Schultz, P. G., and Smider, V. V. (2013) Reshaping antibody diversity. Cell 153, 1379-1393
39. Zhou, T., Georgiev, I., Wu, X., Yang, Z. Y., Dai, K., Finzi, A., Kwon, Y. D., Scheid, J. F. Shi, W., Xu, L., Yang, Y., Zhu, J., Nussenzweig, M. C., Sodroski, J., Shapiro, L., Nabel, G. J., Mascola, J. R., and Kwong, P. D, (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817
40. Breden, F., Lepik, C., Longo, N. S., Montero, M., Lipsky, P. E., and Scott, J. K. (2011) Comparison of antibody repertoires produced by HIV-1 infection, other chronic and acute infections, and systemic autoimmune disease. PLoS ONE 3, e16857
41. Hsing, M., and Cherkasov, A. (2008) Indel PDB: A database of structural insertions and deletions derived from sequence alignments of closely related proteins. BMC Bioinformatics 9, 293
42. Kim, R., and Guo, J. (2010) Systematic analysis of short internal indels and their impact on protein folding. BMC Struct. Biol. 10, 24
43. Light, S., Sagit, R., Ekman, D., and Elofsson, A. (2013a) Long indels are disordered: a study of disorder and indels in homologous eukaryotic proteins. Biochim. Biophys. Acta 1834, 890-897
44. Light, S., Sagit, R., Sachenkova, O., Ekman, D., and Elofsson, A. (2013) Protein expansion is primarily due to indels in intrinsically disordered regions. Mol. Biol. Evol. 30, 2645-2653
45. Zhang, Z., Huang, J., Wang, Z., Wang, L., and Gao, P. (2011) Impact of indels on the flanking regions in structural domains. Mol. Biol. Evol. 28, 291-301
46. Zhang, Z., Xing, C., Wang, L., Gong, B., and Liu, H. (2012) IndelFR: a database of indels in protein structures and their flanking regions. Nucleic Acids Res. 40, D512-D518
47. Bostrom, J., Yu, S. F., Kan, D., Appleton, B. A., Lee, C. V., Billeci, K., Man, W., Peale, F., Ross, S., Wiesmann, C., and Fuh, G. (2009) Variants of the antibody Herceptin that interact with HER2 and VEGF at the antigen binding site. Science 323, 1610-1614
48. Georgiev, I. S., Doria-Rose, N. A., Zhou, T., Kwon, Y. D., Staupe, R. P., Moquin, S., Chuang, G. Y., Louder, M. K., Schmidt, S. D., Altae-Tran, H. R., Bailer, R. T., McKee, K., Nason, M., O'Dell, S., Ofek, G., Pancera, M., Srivatsan, S., Shapiro, L., Connors, M., Migueles, S. A., Morris, L., Nishimura, Y., Martin, M. A., Mascola, J. R., and Kwong, P. D. (2013) Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science 340, 751-756
49. Kong, L., Lee, J. H., Doores, K. J., Murin, C. D., Julien, J. P., McBride, R., Liu, Y., Marozsan, A., Cupo, A., Klasse, P. J., Hoffenberg, S., Caulfield, M., King, C. R., Hua, Y., Le, K. M., Khayat, R., Deller, M. C., Clayton, T., Tien, H., Feizi, T., Sanders, R. W., Paulson, J. C., Moore, J. P., Stanfield, R. L., Burton, D. R., Ward, A. B., and Wilson, I. A. (2013) Supersite of immune vulnerability on the glycosylated face HIV-1 envelope glycoprotein gp120. Nat. Struct. Mol. Biol. 20, 796-803