The Diversity and Molecular Evolution of B-Cell Receptors during Infection

Molecular Biology and Evolution

Volumn 33, Issue 5, 2016, Pages 1147-1157

  Hoehn, Kenneth B ^a   Fowler, Anna ^b   Lunter, Gerton ^b   Pybus, Oliver G ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

B cell receptor; diversity; immunoglobulin; infection; molecular evolution

Indexed keywords

B LYMPHOCYTE RECEPTOR; IMMUNOGLOBULIN; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN;

ARTICLE; AUTOIMMUNE DISEASE; CELL MATURATION; INFECTION; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MUTATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; VIRUS INFECTION; ADAPTIVE IMMUNITY; ANTIBODY AFFINITY; B LYMPHOCYTE; GENETIC VARIATION; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; IMMUNOLOGY; METABOLISM; PROCEDURES;

ADAPTIVE IMMUNITY; ANTIBODY AFFINITY; B-LYMPHOCYTES; EVOLUTION, MOLECULAR; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOGLOBULINS; INFECTION; MEMBRANE PROTEINS; MUTATION; RECEPTORS, ANTIGEN, B-CELL;

EID: 84969930970     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw015     Document Type: Article

References (94)

1. Ademokun A, Wu Y-C, Martin V, Mitra R, Sack U, Baxendale H, Kipling D, Dunn-Walters DK. 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, Duroux P, Lefranc M-P, Giudicelli V. 2012. IMGTVR tools for the nucleotide analysis of immunoglobulin (IG) and T cell receptor (TR) V-(D)-J repertoires, polymorphisms, and IG mutations: IMGT/ V-QUEST and IMGT/HighV-QUEST for NGS. Methods Mol Biol. 882:569-604
3. Bashford-Rogers RJM, Palser AL, Huntly BJ, Rance R, Vassiliou GS, Follows GA, KellamP. 2013. Network properties derived from deep sequencing of human B-cell receptor repertoires delineate B-cell populations. Genome Res. 23:1874-1884
4. Benichou J, Ben-Hamo R, Louzoun Y, Efroni S. 2012. Rep-Seq: uncovering the immunological repertoire through next-generation sequencing. Immunology 135:183-191
5. Bercovici N, DuffourM-T, Agrawal S, SalcedoM, Abastado J-P. 2000. New methods for assessing T-cell responses. Clin Diagn Lab Immunol. 7:859-864
6. Boyd SD, Marshall EL, Merker JD, Maniar JM, Zhang LN, Sahaf B, Jones CD, Simen BB, Hanczaruk B, Nguyen KD, et al. 2009. Measurement and clinicalmonitoring of human lymphocyte clonality bymassively parallel V-D-J pyrosequencing. Sci Transl Med. 1(12):12ra23
7. Bush RM, Bender CA, Subbaro K, Cox NJ, FitchWM. 1999. Predicting the evolution of human influenza A. Science 286:1921-1925
8. Busse CE, Czogiel I, Braun P, Arndt PF, Wardemann H. 2014. Single-cell based high-throughput sequencing of full-length immunoglobulin heavy and light chain genes. Eur J Immunol. 44:597-603
9. Chen W, Prabakaran P, Zhu Z, Feng Y, Streaker ED, Dimitrov DS. 2012. Characterization of human IgG repertoires in an acute HIV-1 infection. Exp Mol Pathol. 93:399-407
10. DeKosky BJ, Ippolito GC, Deschner RP, Lavinder JJ, Wine Y, Rawlings BM, Varadarajan N, Giesecke C, Dorner T, Andrews SF, et al. 2013. Highthroughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat Biotechnol. 31:166-169
11. DeKosky BJ, Kojima T, Rodin A, Charab W, Ippolito GC, Ellington AD, Georgiou G. 2015. In-depth determination and analysis of the human paired heavy-and light-chain antibody repertoire. Nat Med. 21:86-91
12. Doria-Rose NA, Schramm CA, Gorman J,Moore PL, Bhiman JN, DeKosky BJ, Ernandes MJ, Georgiev IS, Kim HJ, Pancera M, et al. 2014. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509:55-62
13. Dunn-Walters DK, Belelovsky A, Edelman H, Banerjee M, Mehr R. 2002. The dynamics of germinal centre selection as measured by graphtheoretical analysis of mutational lineage trees. Dev Immunol. 9:233-243
14. Dunn-Walters DK, Spencer J. 1998. Strong intrinsic biases towards mutation and conservation of bases in human IgVH genes during somatic hypermutation prevent statistical analysis of antigen selection. Immunology 95:339
15. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797
16. Elhanati Y, Sethna Z, Marcou Q, Callan CG, Mora T, Walczak AM. 2015. Inferring processes underlying B-cell repertoire diversity. Philos Trans R Soc Lond B Biol Sci. 370:20140243
17. Felsenstein J. 1981. Evolutionary trees fromDNA sequences: amaximum likelihood approach. J Mol Evol. 17:368-376
18. Frost SDW, Murrell B, Hossain ASMM, Silverman GJ, Pond SLK. 2015. Assigning and visualizing germline genes in antibody repertoires. Philos Trans R Soc Lond B Biol Sci. 370:20140240
19. Furlong RF, Yang Z. 2008. Diversifying and purifying selection in the peptide binding region of DRB in mammals. J Mol Evol. 66:384-394
20. Gadagkar SR, Rosenberg MS, Kumar S. 2005. Inferring species phylogenies from multiple genes: concatenated sequence tree versus consensus gene tree. J Exp Zool B Mol Dev Evol. 304:64-74
21. Gadala-Maria D, Yaari G, Uduman M, Kleinstein SH. 2015. Automated analysis of high-throughput B-cell sequencing data reveals a high frequency of novel immunoglobulin V gene segment alleles. Proc Natl Acad Sci U S A. 112:E862-E870
22. Gaeta BA, Malming HR, Jackson KJL, Bain ME, Wilson P, Collins AM. 2007. iHMMune-align: hidden Markov model-based alignment and identification of germline genes in rearranged immunoglobulin gene sequences. Bioinformatics 23:1580-1587
23. Galson JD, Clutterbuck EA, Truck J, Ramasamy MN, Munz M, Fowler A, Cerundolo V, Pollard AJ, Lunter G, Kelly DF. 2015. BCR repertoire sequencing: different patterns of B-cell activation after two meningococcal vaccines. Immunol Cell Biol. 93:885-895
24. Galson JD, Pollard AJ, Truck J, Kelly DF. 2014. Studying the antibody repertoire after vaccination: practical applications. Trends Immunol. 35:319-331
25. Georgiou G, Ippolito GC, Beausang J, Busse CE, Wardemann H, Quake SR. 2014. The promise and challenge of high-throughput sequencing of the antibody repertoire. Nat Biotechnol. 32:158-168
26. Giudicelli V, Chaume D, Lefranc M-P. 2005. IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res. 33:D256-D261
27. Greiff V, Bhat P, Cook SC, Menzel U, Kang W, Reddy ST. 2015. A bioinformatic framework for immune repertoire diversity profiling enables detection of immunological status. Genome Med. 7:49
28. GrenfellBT, PybusOG, Gog JR,WoodJLN,Daly JM,MumfordJA, Holmes EC. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327-332
29. 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
30. Hershberg U, Luning Prak ET. 2015. The analysis of clonal expansions in normal and autoimmune B cell repertoires. Philos Trans R Soc Lond B Biol Sci. 370:20140239
31. Hershberg U, UdumanM, ShlomchikMJ, Kleinstein SH. 2008. Improved methods for detecting selection by mutation analysis of Ig V region sequences. Int Immunol. 20:683-694
32. Hoehn KB, Gall A, Bashford-Rogers R, Fidler SJ, Kaye S, Weber JN, McClure MO; SPARTAC Trial Investigators, Kellam P, Pybus OG. 2015. Dynamics of immunoglobulin sequence diversity in HIV-1 infected individuals. Philos Trans R Soc Lond B Biol Sci. 370:20140241
33. Huelsenbeck JP, Bull JJ, Cunningham CW. 1996. Combining data in phylogenetic analysis. Trends Ecol Evol. 11:152-158
34. Jackson KJL, Liu Y, Roskin KM, Glanville J, Hoh RA, Seo K, Marshall EL, Gurley TC, Moody MA, Haynes BF, et al. 2014. Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements. Cell Host Microbe 16:105-114
35. Jiang N, He J,Weinstein JA, Penland L, Sasaki S, He X-S, Dekker CL, Zheng N-Y, Huang M, Sullivan M, et al. 2013. Lineage structure of the human antibody repertoire in response to influenza vaccination. Sci Transl Med. 5(171):171ra19
36. Kepler TB. 2013. Reconstructing a B-cell clonal lineage. I. Statistical inference of unobserved ancestors. F1000Res. [Internet]. Available from: http://f1000research.com/articles/2-103/v1
37. Kepler TB, Munshaw S, Wiehe K, Zhang R, Yu J-S, Woods CW, Denny TN, Tomaras GD, Alam SM, Moody MA, et al. 2014. Reconstructing a B-cell clonal lineage. II. Mutation, selection, and affinity maturation. B Cell Biol. 5:170
38. Larimore K, McCormick MW, Robins HS, Greenberg PD. 2012. Shaping of human germline IgH repertoires revealed by deep sequencing. J Immunol. 189:3221-3230
39. Laserson U, Vigneault F, Gadala-Maria D, Yaari G, Uduman M, Heiden JAV, Kelton W, Jung ST, Liu Y, Laserson J, et al. 2014. High-resolution antibody dynamics of vaccine-induced immune responses. Proc Natl Acad Sci U S A. 111:4928-4933
40. Lefranc M-P, Giudicelli V, Ginestoux C, Jabado-Michaloud J, Folch G, Bellahcene F, Wu Y, Gemrot E, Brochet X, Lane J, et al. 2009. IMGT(R), the international ImMunoGeneTics information system(R). Nucleic Acids Res. 37:D1006-D1012
41. Lefranc M-P, Lefranc G. 2001. The Immunoglobulin FactsBook. London (United Kingdom): Academic Press
42. Lemey P, Kosakovsky Pond SL, Drummond AJ, Pybus OG, Shapiro B, Barroso H, Taveira N, Rambaut A. 2007. Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics. PLoS Comput Biol. 3:e29
43. Lemey P,Minin VN, Bielejec F, Pond SLK, Suchard MA. 2012. A counting renaissance: combining stochastic mapping and empirical Bayes to quickly detect amino acid sites under positive selection. Bioinformatics 28:3248-3256
44. Li A. 2004. Utilization of Ig heavy chain variable, diversity, and joining gene segments in children with B-lineage acute lymphoblastic leukemia: implications for the mechanisms of VDJ recombination and for pathogenesis. Blood 103:4602-4609
45. Liao H-X, Lynch R, Zhou T, Gao F, Alam SM, Boyd SD, Fire AZ, Roskin KM, Schramm CA, Zhang Z, et al. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496:469-476
46. Liu Y-J, Zhang J, Lane PJL, Chan Y-T, Maclennan ICM. 1991. Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur J Immunol. 21:2951-2962
47. Lu DR, Tan Y-C, Kongpachith S, Cai X, Stein EA, Lindstrom TM, Sokolove J, Robinson WH. 2014. Identifying functional anti-Staphylococcus aureus antibodies by sequencing antibody repertoires of patient plasmablasts. Clin Immunol. 152:77-89
48. Martins AJ, Tsang JS. 2014. Random yet deterministic: convergent immunoglobulin responses to influenza. Trends Microbiol. 22:488-489
49. McCoy CO, Bedford T,Minin VN, Bradley P, Robins H, Matsen FA. 2015. Quantifying evolutionary constraints on B-cell affinity maturation. Philos Trans R Soc Lond B Biol Sci. 370:20140244
50. Mora T, Walczak AM, Bialek W, Callan CG. 2010. Maximum entropy models for antibody diversity. Proc Natl Acad Sci U S A. 107:5405-5410
51. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553-563
52. Murphy K, Trivers P,Walport M. 2008. Janeway's immunobiology. 7th ed. New York: Garland Science
53. Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey J. 2004. Bayesian phylogenetic analysis of combined data. Syst Biol. 53:47-67
54. Parameswaran P, Liu Y, Roskin KM, Jackson KK, Dixit VP, Lee J-Y, Artiles K, Zompi S, Vargas MJ, Simen BB, et al. 2013. Convergent antibody signatures in human dengue. Cell Host Microbe 13:691-700
55. Parham P. 2009. The immune system. London: Garland Science
56. Parker J, Tsagkogeorga G, Cotton JA, Liu Y, Provero P, Stupka E, Rossiter SJ. 2013. Genome-wide signatures of convergent evolution in echolocating mammals. Nature 502:228-231
57. Peled JU, Kuang FL, Iglesias-Ussel MD, Roa S, Kalis SL, Goodman MF, Scharff MD. 2008. The biochemistry of somatic hypermutation. Annu Rev Immunol. 26:481-511
58. Reddy ST,GeX,MiklosAE, Hughes RA,Kang SH, HoiKH, Chrysostomou C, Hunicke-Smith SP, Iverson BL, Tucker PW, et al. 2010. Monoclonal antibodies isolated without screening by analyzing the variable-gene repertoire of plasma cells. Nat Biotechnol. 28:965-969
59. Retter I, Althaus HH, Munch R,MullerW. 2005. VBASE2, an integrative V gene database. Nucleic Acids Res. 33:D671-D674
60. Robins H. 2013. Immunosequencing: applications of immune repertoire deep sequencing. Curr Opin Immunol. 25:646-652
61. Robinson WH, Lindstrom TM, Cheung RK, Sokolove J. 2013.Mechanistic biomarkers for clinical decision making in rheumatic diseases. Nat Rev Rheumatol. 9:267-276
62. Sasaki S, He X-S, Holmes TH, Dekker CL, Kemble GW, Arvin AM, Greenberg HB. 2008. Influence of prior influenza vaccination on antibody and B-Cell responses. PLoS One 3:e2975
63. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Oliveira TYK, Pietzsch J, Fenyo D, Abadir A, Velinzon K, et al. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333:1633-1637
64. Shahaf G, BarakM, Zuckerman NS, Swerdlin N, Gorfine M, Mehr R. 2008. Antigen-driven selection in germinal centers as reflected by the shape characteristics of immunoglobulin gene lineage trees: a large-scale simulation study. J Theor Biol. 255:210-222
65. Shapiro GS, Aviszus K, Murphy J, Wysocki LJ. 2002. Evolution of Ig DNA sequence to target specific base positions within codons for somatic hypermutation. J Immunol. 168:2302-2306
66. Shapiro GS, Ellison MC, Wysocki LJ. 2003. Sequence-specific targeting of two bases on both DNA strands by the somatic hypermutation mechanism. Mol Immunol. 40:287-295
67. Six A,Mariotti-Ferrandiz E, ChaaraW,Magadan S, Pham H-P, LefrancMP, Mora T, Thomas-Vaslin V, Walczak AM, Boudinot P. 2013. The past, present, and future of immune repertoire biology-The rise of next-generation repertoire analysis. Front Immunol. 4:413
68. Smith DS, Creadon G, Jena PK, Portanova JP, Kotzin BL, Wysocki LJ. 1996. Di-and trinucleotide target preferences of somatic mutagenesis in normal and autoreactive B cells. J Immunol. 156:2642-2652
69. Sok D, Laserson U, Laserson J, Liu Y, Vigneault F, Julien J-P, Briney B, Ramos A, Saye KF, Le K, et al. 2013. The effects of somatic hypermutation on neutralization and binding in the PGT121 family of broadly neutralizing HIV antibodies. PLoS Pathog. 9:e1003754
70. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313
71. Stern JNH, Yaari G, Heiden JAV, Church G, Donahue WF, Hintzen RQ, Huttner AJ, Laman JD, Nagra RM, Nylander A, et al. 2014. B cells populating the multiple sclerosis brain mature in the draining cervical lymph nodes. Sci Transl Med. 6(248):248ra107
72. Tan Y-C, Blum LK, Kongpachith S, Ju C-H, Cai X, Lindstrom TM, Sokolove J, Robinson WH. 2014. High-throughput sequencing of natively paired antibody chains provides evidence for original antigenic sin shaping the antibody response to influenza vaccination. Clin Immunol. 151:55-65
73. Tan Y-C, Kongpachith S, BlumLK, Ju C-H, Lahey LJ, Lu DR, Cai X,Wagner CA, Lindstrom TM, Sokolove J, et al. 2014. Barcode-enabled sequencing of plasmablast antibody repertoires in rheumatoid arthritis. Arthritis Rheumatol. 66:2706-2715
74. Teng G, Papavasiliou FN. 2007. Immunoglobulin somatic hypermutation. Annu Rev Genet. 41:107-120
75. Thammavongsa V, Kim HK, Missiakas D, Schneewind O. 2015. Staphylococcal manipulation of host immune responses. Nat Rev Microbiol. 13:529-543
76. Truck J, Ramasamy MN, Galson JD, Rance R, Parkhill J, Lunter G, Pollard AJ, Kelly DF. 2015. Identification of antigen-specific B Cell receptor sequences using public repertoire analysis. J Immunol. 194:252-261
77. Uduman M, Shlomchik MJ, Vigneault F, Church GM, Kleinstein SH. 2014. Integrating B cell lineage information into statistical tests for detecting selection in Ig sequences. J Immunol. 192:867-874
78. Victora GD, Nussenzweig MC. 2012. Germinal centers. Annu Rev Immunol. 30:429-457
79. Volz EM, Koelle K, Bedford T. 2013. Viral phylodynamics. PLoS Comput Biol. 9:e1002947
80. von Budingen H-C, Kuo TC, SirotaM, van Belle CJ, Apeltsin L, Glanville J, Cree BA, Gourraud P-A, Schwartzburg A, Huerta G, et al. 2012. B cell exchange across the blood-brain barrier in multiple sclerosis. J Clin Invest. 122:4533-4543
81. Wang C, Liu Y, CavanaghMM, Saux SL, Qi Q, Roskin KM, Looney TJ, Lee J-Y, Dixit V, Dekker CL, et al. 2014. B-cell repertoire responses to varicella-zoster vaccination in human identical twins. Proc Natl Acad Sci U S A. 112(2):500-505
82. Wang C, Liu Y, Xu LT, Jackson KJL, Roskin KM, Pham TD, Laserson J, Marshall EL, Seo K, Lee J-Y, et al. 2014. Effects of aging, cytomegalovirus infection, and EBV infection on human B cell repertoires. J Immunol. 192:603-611
83. Wu X, Yang Z-Y, Li Y, Hogerkorp C-M, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861
84. Wu X, Zhang Z, SchrammCA, JoyceMG, Do Kwon Y, Zhou T, Sheng Z, Zhang B, O'Dell S, McKee K, et al. 2015. Maturation and diversity of the VRC01-antibody lineage over 15 years of chronic HIV-1 infection. Cell 161:470-485
85. Xu JL, Davis MM. 2000. Diversity in the CDR3 region of VH is sufficient for most antibody specificities. Immunity 13:37-45
86. Yaari G, Benichou JIC, Vander Heiden JA, Kleinstein SH, Louzoun Y. 2015. The mutation patterns in B-cell immunoglobulin receptors reflect the influence of selection acting at multiple time-scales. Philos Trans R Soc Lond B Biol Sci. 370:20140242
87. Yaari G, Kleinstein SH. 2015. Practical guidelines for B-cell receptor repertoire sequencing analysis. Genome Med. 7: Article 121
88. Yaari G, Uduman M, Kleinstein SH. 2012. Quantifying selection in highthroughput immunoglobulin sequencing data sets. Nucleic Acids Res. 40(17):e134
89. Yaari G, Vander Heiden JA, Uduman M, Gadala-Maria D, Gupta N, Stern JNH, O'Connor KC, Hafler DA, Laserson U, Vigneault F, et al. 2013.Models of somatic hypermutation targeting and substitution based on synonymousmutations from high-throughput immunoglobulin sequencing data. Front Immunol. 4: Article 358
90. Yang Z, Swanson WJ. 2002. Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes.Mol Biol Evol. 19:49-57
91. Ye J, Ma N, Madden TL, Ostell JM. 2013. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res. 41:W34-W40
92. Zhang J, Kumar S. 1997. Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol. 14:527-536
93. Zhou T, Zhu J, Wu X, Moquin S, Zhang B,Acharya P, Georgiev IS,Altae-Tran HR, Chuang G-Y, Joyce MG, et al. 2013. Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-Class antibodies. Immunity 39:245-258
94. Zhu J,Ofek G, Yang Y, Zhang B, LouderMK, Lu G, McKee K, PanceraM, Skinner J, Zhang Z, et al. 2013. Mining the antibodyome for HIV-1-neutralizing antibodies with next-generation sequencing and phylogenetic pairing of heavy/light chains. Proc Natl Acad Sci U S A. 110:6470-6475