Sequencing of the human IG light chain loci from a hydatidiform mole BAC library reveals locus-specific signatures of genetic diversity

Genes and Immunity

Volumn 16, Issue 1, 2015, Pages 24-34

  Watson, C T ^a,b   Steinberg, K M ^c,d   Graves, T A ^d   Warren, R L ^e   Malig, M ^c   Schein, J ^e   Wilson, R K ^d   Holt, R A ^e   Eichler, E E ^c,f   Breden, F ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b HESS CORPORATION   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d WASHINGTON UNIVERSITY   (United States)

^e BRITISH COLUMBIA CANCER AGENCY   (Canada)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTIG; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN;

ALLELE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CLONE; CONTROLLED STUDY; GENE LIBRARY; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; GENOME ANALYSIS; HAPLOIDY; HAPLOTYPE; HUMAN; HUMAN CELL; HYDATIDIFORM MOLE; IMMUNOGLOBULIN LIGHT CHAIN GENE; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOGENE; SEGMENTAL DUPLICATION; SINGLE NUCLEOTIDE POLYMORPHISM; FEMALE; GENETICS; IMMUNOGLOBULIN HEAVY CHAIN GENE; MOLECULAR GENETICS; PREGNANCY; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMOSOMES, ARTIFICIAL, BACTERIAL; FEMALE; GENES, IMMUNOGLOBULIN HEAVY CHAIN; GENES, IMMUNOGLOBULIN LIGHT CHAIN; HUMANS; HYDATIDIFORM MOLE; MOLECULAR SEQUENCE DATA; POLYMORPHISM, SINGLE NUCLEOTIDE; PREGNANCY;

EID: 84921612155     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2014.56     Document Type: Article

References (73)

1. Lefranc MP, Lefranc G. The Immunoglobulin Facts Book. Academic Press: London, 2001.
2. Tonegawa S. Somatic generation of antibody diversity. Nature 1983; 302: 575-581.
3. Boyd SD, Gaeta BA, Jackson KJ, Fire AZ, Marshall EL, Merker JD et al. Individual variation in the germline Ig gene repertoire inferred from variable region gene rearrangements. J Immunol 2010; 184: 6986-6992.
4. Glanville J, Kuo TC, von Budingen HC, Guey L, Berka J, Sundar PD et al. Naive antibody gene-segment frequencies are heritable and unaltered by chronic lymphocyte ablation. Proc Natl Acad Sci USA 2011; 108: 20066-20071.
5. Kidd MJ, Chen Z, Wang Y, Jackson KJ, Zhang L, Boyd SD et al. The inference of phased haplotypes for the immunoglobulin H chain V region gene loci by analysis of VDJ gene rearrangements. J Immunol 2012; 188: 1333-1340.
6. Watson CT, Steinberg KM, Huddleston J, Warren RL, Malig M, Schein J et al. Complete haplotype sequence of the human immunoglobulin heavy-chain variable, diversity, and joining genes and characterization of allelic and copy-number variation. Am J Hum Genet 2013; 92: 530-546.
7. Watson CT, Breden F. The immunoglobulin heavy chain locus: genetic variation, missing data, and implications for human disease. Genes Immun 2012; 13: 363-373.
8. Lefranc MP. Immunoglobulin and T cell receptor genes: IMGT((R)) and the birth and rise of immunoinformatics. Front Immunol 2014; 5: 22.
9. Feeney AJ, Atkinson MJ, Cowan MJ, Escuro G, Lugo G. A defective Vkappa A2 allele in Navajos which may play a role in increased susceptibility to haemophilus influenzae type b disease. J Clin Invest 1996; 97: 2277-2282.
10. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LM et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 2009; 16: 265-273.
11. Tsai F-J, Lee Y-C, Chang J-S, Huang L-M, Huang F-Y, Chiu N-C et al. Identification of novel susceptibility Loci for kawasaki disease in a Han chinese population by a genome-wide association study. PLoS ONE 2011; 6: e16853.
12. Frippiat JP, Williams SC, Tomlinson IM, Cook GP, Cherif D, Le Paslier D et al. Organization of the human immunoglobulin lambda light-chain locus on chromosome 22q11.2. Hum Mol Genet 1995; 4: 983-991.
13. Kawasaki K, Minoshima S, Schooler K, Kudoh J, Asakawa S, de Jong PJ et al. The organization of the human immunoglobulin lambda gene locus. Genome Res 1995; 5: 125-135.
14. Williams SC, Frippiat JP, Tomlinson IM, Ignatovich O, Lefranc MP, Winter G. Sequence and evolution of the human germline V lambda repertoire. J Mol Biol 1996; 264: 220-232.
15. Kawasaki K, Minoshima S, Nakato E, Shibuya K, Shintani A, Schmeits JL et al. One-megabase sequence analysis of the human immunoglobulin lambda gene locus. Genome Res. 1997; 7: 250-261.
16. Ruiz M, Pallares N, Contet V, Barbi V, Lefranc MP. The human immunoglobulin heavy diversity (IGHD) and joining (IGHJ) segments. Exp Clin Immunogenet 1999; 16: 173-184.
17. Ghanem N, Dariavach P, Bensmana M, Chibani J, Lefranc G, Lefranc MP. Polymorphism of immunoglobulin lambda constant region genes in populations from France, Lebanon and Tunisia. Exp Clin Immunogenet 1988; 5: 186-195.
18. Lefranc MP, Pallares N, Frippiat JP. Allelic polymorphisms and RFLP in the human immunoglobulin lambda light chain locus. Hum Genet 1999; 104: 361-369.
19. Taub RA, Hollis GF, Hieter PA, Korsmeyer S, Waldmann TA, Leder P. Variable amplification of immunoglobulin lambda light-chain genes in human populations. Nature 1983; 304: 172-174.
20. Cox JP, Tomlinson IM, Winter G. A directory of human germ-line V kappa segments reveals a strong bias in their usage. Eur J Immunol 1994; 24: 827-836.
21. Huber C, Huber E, Lautner-Rieske A, Schable KF, Zachau HG. The human immunoglobulin kappa locus. Characterization of the partially duplicated L regions. Eur J Immunol 1993; 23: 2860-2867.
22. Huber C, Schable KF, Huber E, Klein R, Meindl A, Thiebe R et al. The V kappa genes of the L regions and the repertoire of V kappa gene sequences in the human germ line. Eur J Immunol 1993; 23: 2868-2875.
23. Kawasaki K, Minoshima S, Nakato E, Shibuya K, Shintani A, Asakawa S et al. Evolutionary dynamics of the human immunoglobulin kappa locus and the germline repertoire of the Vkappa genes. Eur J Immunol 2001; 31: 1017-1028.
24. Osoegawa K, Mammoser AG, Wu C, Frengen E, Zeng C, Catanese JJ et al. A bacterial artificial chromosome library for sequencing the complete human genome. Genome Res 2001; 11: 483-496.
25. Juul L, Hougs L, Barington T. A new apparently functional IGVK gene (VkLa) present in some individuals only. Immunogenetics 1998; 48: 40-46.
26. Kay PH, Moriuchi J, Ma PJ, Saueracker E. An unusual allelic form of the immunoglobulin lambda constant region genes in the Japanese. Immunogenetics 1992; 35: 341-343.
27. Moraes Junta C, Passos GA. Genomic EcoRI polymorphism and cosmid sequencing reveal an insertion/deletion and a new IGLV5 allele in the human immunoglobulin lambda variable locus (22q11.2/IGLV). Immunogenetics 2003; 55: 10-15.
28. Frippiat JP, Dard P, Marsh S, Winter G, Lefranc MP. Immunoglobulin lambda light chain orphons on human chromosome 8q11.2. Eur J Immunol 1997; 27: 1260-1265.
29. Romo-Gonzalez T, Vargas-Madrazo E. Substitution patterns in alleles of immunoglobulin V genes in humans and mice. Mol Immunol 2006; 43: 731-744.
30. Pallares N, Lefebvre S, Contet V, Matsuda F, Lefranc MP. The human immunoglobulin heavy variable genes. Exp Clin Immunogenet 1999; 16: 36-60.
31. Genomes Project Consortium, Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM et al. An integrated map of genetic variation from 1092 human genomes. Nature 2012; 491: 56-65.
32. Brensing-Kuppers J, Zocher I, Thiebe R, Zachau HG. The human immunoglobulin kappa locus on yeast artificial chromosomes (YACs). Gene 1997; 191: 173-181.
33. Jaenichen HR, Pech M, Lindenmaier W, Wildgruber N, Zachau HG. Composite human VK genes and a model of their evolution. Nucleic Acids Res 1984; 12: 5249-5263.
34. Barbie V, Lefranc MP. The human immunoglobulin kappa variable (IGKV) genes and joining (IGKJ) segments. Exp Clin Immunogenet 1998; 15: 171-183.
35. Giudicelli V, Chaume D, Lefranc MP. IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res 2005; 33: D256-D261.
36. Bailey JA, Eichler EE. Primate segmental duplications: crucibles of evolution, diversity and disease. Nat Rev Genet 2006; 7: 552-564.
37. Eichler EE. Recent duplication, domain accretion and the dynamic mutation of the human genome. Trends Genet 2001; 17: 661-669.
38. Matsuda F, Ishii K, Bourvagnet P, Kuma K, Hayashida H, Miyata T et al. The complete nucleotide sequence of the human immunoglobulin heavy chain variable region locus. J Exp Med 1998; 188: 2151-2162.
39. Steinberg KM, Schneider VK, Graves-Lindsay TA, Fulton RS, Agarwala R, Huddleston J et al. Single haplotype assembly of the human genome from a hydatidiform mole. Genome Res (in press).
40. Sandve GK, Gundersen S, Rydbeck H, Glad IK, Holden L, Holden M et al. The Genomic HyperBrowser: inferential genomics at the sequence level. Genome Biol 2010; 11: R121.
41. Arndt PF, Hwa T, Petrov DA. Substantial regional variation in substitution rates in the human genome: importance of GC content, gene density, and telomerespecific effects. J Mol Evol 2005; 60: 748-763.
42. Collins AM, Wang Y, Singh V, Yu P, Jackson KJ, Sewell WA. The reported germline repertoire of human immunoglobulin kappa chain genes is relatively complete and accurate. Immunogenetics 2008; 60: 669-676.
43. Jackson KJL, Wang Y, Gaeta BA, Pomat W, Siba P, Rimmer J et al. Divergent human populations show extensive shared IGK rearrangements in peripheral blood B cells. Immunogenetics 2012; 64: 3-14.
44. Wang Y, Jackson KJ, Gaeta B, Pomat W, Siba P, Sewell WA et al. Genomic screening by 454 pyrosequencing identifies a new human IGHV gene and sixteen other new IGHV allelic variants. Immunogenetics 2011; 63: 259-265.
45. Eichler EE. Masquerading repeats: paralogous pitfalls of the human genome. Genome Res 1998; 8: 758-762.
46. Estivill X, Cheung J, Pujana MA, Nakabayashi K, Scherer SW, Tsui L-C. Chromosomal regions containing high-density and ambiguously mapped putative single nucleotide polymorphisms (SNPs) correlate with segmental duplications in the human genome. Hum Mol Genet 2002; 11: 1987-1995.
47. Nadel B, Tang A, Lugo G, Love V, Escuro G, Feeney AJ. Decreased frequency of rearrangement due to the synergistic effect of nucleotide changes in the heptamer and nonamer of the recombination signal sequence of the V kappa gene A2b, which is associated with increased susceptibility of Navajos to Haemophilus influenzae type b disease. J Immunol 1998; 161: 6068-6073.
48. Romo-Gonzalez T, Vargas-Madrazo E. Structural analysis of substitution patterns in alleles of human immunoglobulin VH genes. Mol Immunol 2005; 42: 1085-1097.
49. Pargent W, Schable KF, Zachau HG. Polymorphisms and haplotypes in the human immunoglobulin kappa locus. Eur J Immunol 1991; 21: 1829-1835.
50. Schaible G, Rappold GA, Pargent W, Zachau HG. The immunoglobulin kappa locus: polymorphism and haplotypes of Caucasoid and non-Caucasoid individuals. Hum Genet 1993; 91: 261-267.
51. Sharp AJ, Locke DP, McGrath SD, Cheng Z, Bailey JA, Vallente RU et al. Segmental duplications and copy-number variation in the human genome. Am J Hum Genet 2005; 77: 78-88.
52. Hurles ME. Gene conversion homogenizes the CMT1A paralogous repeats. BMC Genomics 2001; 2: 11.
53. Hallast P, Nagirnaja L, Margus T, Laan M. Segmental duplications and gene conversion: Human luteinizing hormone/chorionic gonadotropin beta gene cluster. Genome Res 2005; 15: 1535-1546.
54. Verrelli BC, Tishkoff SA. Signatures of selection and gene conversion associated with human color vision variation. Am J Hum Genet 2004; 75: 363-375.
55. Xu JL, Davis MM. Diversity in the CDR3 region of V(H) is sufficient for most antibody specificities. Immunity 2000; 13: 37-45.
56. Avnir Y, Tallarico AS, Zhu Q, Bennett AS, Connelly G, Sheehan J et al. Molecular signatures of hemagglutinin stem-directed heterosubtypic human neutralizing antibodies against influenza A viruses. PLoS Pathog 2014; 10: e1004103.
57. Tang X-C, Agnihothram SS, Jiao Y, Stanhope J, Graham RL, Peterson EC et al. Identification of human neutralizing antibodies against MERS-CoV and their role in virus adaptive evolution. Proc Natl Acad Sci USA 2014; 111: 2018-2026.
58. Gonzalez-Garay ML, Cranford SM, Braun MC, Doris PA. Diversity in the preimmune immunoglobulin repertoire of SHR lines susceptible and resistant to endorgan injury. Genes Immun 2014; 15: 528-533.
59. Zachau HG. The immunoglobulin kappa locus-or-what has been learned from looking closely at one-tenth of a percent of the human genome. Gene 1993; 135: 167-173.
60. Zachau HG. The immunoglobulin kappa genes. Immunologist 1996; 4: 49-54.
61. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215: 403-410.
62. Brochet X, Lefranc MP, Giudicelli V. 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 2008; 36: W503-W508.
63. Giudicelli V, Brochet X, Lefranc M-P. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb Protoc 2011; 2011: 695-715.
64. Alamyar E, Duroux P, Lefranc MP, Giudicelli V. IMGT((R)) 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 2012; 882: 569-604.
65. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26: 841-842.
66. Parsons JD. Miropeats: graphical DNA sequence comparisons. Comput Appl Biosci 1995; 11: 615-619.
67. Burge C, Karlin S. Prediction of complete gene structures in human genomic DNA. J Mol Biol 1997; 268: 78-94.
68. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5: R12.
69. Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics 2002; Chapter 2: Unit 2.3.
70. McGuire G, Wright F. TOPAL 2.0: improved detection of mosaic sequences within multiple alignments. Bioinformatics 2000; 16: 130-134.
71. Milne I, Wright F, Rowe G, Marshall DF, Husmeier D, McGuire G. TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 2004; 20: 1806-1807.
72. Bailey JA, Yavor AM, Massa HF, Trask BJ, Eichler EE. Segmental duplications: organization and impact within the current human genome project assembly. Genome Res 2001; 11: 1005-1017.
73. Bailey JA, Gu Z, Clark RA, Reinert K, Samonte RV, Schwartz S et al. Recent segmental duplications in the human genome. Science 2002; 297: 1003-1007.