Somatic hypermutation and antigen-driven selection of B cells are altered in autoimmune diseases

Journal of Autoimmunity

Volumn 35, Issue 4, 2010, Pages 325-335

  Zuckerman, Neta S ^a   Hazanov, Helena ^a   Barak, Michal ^a   Edelman, Hanna ^a   Hess, Shira ^a   Shcolnik, Hadas ^a   Dunn Walters, Deborah ^b   Mehr, Ramit ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Autoimmune diseases; Germinal center; Immunoglobulin (Ig); Multiple Sclerosis (MS); Rheumatoid Arthritis (RA); Sj gren's Syndrome (SS); Somatic hypermutation

Indexed keywords

ANTIGEN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN;

ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL EXPANSION; CELL LINEAGE; CELL SELECTION; CLINICAL ARTICLE; CONTROLLED STUDY; GERMINAL CENTER; HUMAN; HUMAN TISSUE; IMMUNOGLOBULIN VARIABLE REGION; LYMPHOID TISSUE; MICROENVIRONMENT; MULTIPLE SCLEROSIS; PATHOGENESIS; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SEQUENCE ANALYSIS; SJOEGREN SYNDROME; SOMATIC HYPERMUTATION;

ANTIBODY AFFINITY; AUTOANTIGENS; AUTOIMMUNE DISEASES; B-LYMPHOCYTES; CELL DIFFERENTIATION; CHORISTOMA; CLONAL DELETION; DNA MUTATIONAL ANALYSIS; GERMINAL CENTER; HUMANS; IMMUNOGLOBULIN VARIABLE REGION; MUTATION; ORGAN SPECIFICITY; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 77958142452     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2010.07.004     Document Type: Article

References (69)

1. Shlomchik M.J. Sites and stages of autoreactive B cell activation and regulation. Immunity 2008, 28(1):18-28.
2. William J., Euler C., Christensen S., Shlomchik M.J. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science 2002, 297(5589):2066-2070.
3. Sims G.P., Shiono H., Willcox N., Stott D.I. Somatic hypermutation and selection of B cells in thymic germinal centers responding to acetylcholine receptor in myasthenia gravis. J Immunol 2001, 167(4):1935-1944.
4. Stott D.I., Hiepe F., Hummel M., Steinhauser G., Berek C. Antigen-driven clonal proliferation of a cells within the target tissue of an autoimmune disease - the salivary glands of patients with Sjogren's syndrome. J Clin Invest 1998, 102(5):938-946.
5. Manzo A., Pitzalis C. Lymphoid tissue reactions in rheumatoid arthritis. Autoimmun Rev 2007, 7(1):30-34.
6. Kim H.J., Berek C. B cells in rheumatoid arthritis. Arthritis Res 2000, 2(2):126-131.
7. Weyand C.M., Goronzy J.J. Ectopic germinal center formation in rheumatoid synovitis. Ann N Y Acad Sci 2003, 987:140-149.
8. Itoh K., Meffre E., Albesiano E., Farber A., Dines D., Stein P., et al. Immunoglobulin heavy chain variable region gene replacement as a mechanism for receptor revision in rheumatoid arthritis synovial tissue B lymphocytes. J Exp Med 2000, 192(8):1151-1164.
9. Kim H.J., Krenn V., Steinhauser G., Berek C. Plasma cell development in synovial germinal centers in patients with rheumatoid and reactive arthritis. J Immunol 1999, 162(5):3053-3062.
10. Miura Y., Chu C.C., Dines D.M., Asnis S.E., Furie R.A., Chiorazzi N. Diversification of the Ig variable region gene repertoire of synovial B lymphocytes by nucleotide insertion and deletion. Mol Med 2003, 9(5-8):166-174.
11. Bridges S.L., Lee S.K., Johnson M.L., Lavelle J.C., Fowler P.G., Koopman W.J., et al. Somatic mutation and CDR3 lengths of immunoglobulin kappa light chains expressed in patients with rheumatoid arthritis and in normal individuals. J Clin Invest 1995, 96(2):831-841.
12. Gil Y., Levy-Nabot S., Steinitz M., Laskov R. Somatic mutations and activation-induced cytidine deaminase (AID) expression in established rheumatoid factor-producing lymphoblastoid cell line. Mol Immunol 2007, 44(4):494-505.
13. Franciotta D., Salvetti M., Lolli F., Serafini B., Aloisi F. B cells and multiple sclerosis. Lancet Neurol 2008, 7(9):852-858.
14. Monson N.L. The natural history of B cells. Curr Opin Neurol 2008, 21:S3-S8.
15. Monson N.L., Brezinschek H.P., Brezinschek R.I., Mobley A., Vaughan G.K., Frohman E.M., et al. Receptor revision and atypical mutational characteristics in clonally expanded B cells from the cerebrospinal fluid of recently diagnosed multiple sclerosis patients. J Neuroimmunol 2005, 158(1-2):170-181.
16. Qin Y.F., Duquette P., Zhang Y.P., Talbot P., Poole R., Antel J. Clonal expansion and somatic hypermutation of V-H genes of B cells from cerebrospinal fluid in multiple sclerosis. J Clin Invest 1998, 102(5):1045-1050.
17. Bohnhorst J.O., Bjorgan M.B., Thoen J.E., Natvig J.B., Thompson K.M. Bm1-Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjogren's syndrome. J Immunol 2001, 167(7):3610-3618.
18. Hansen A., Lipsky P.E., Dorner T. B cells in Sjogren's syndrome: indications for disturbed selection and differentiation in ectopic lymphoid tissue. Arthritis Res Ther 2007, 9(4):218.
19. Hansen A., Jacobi A., Pruss A., Kaufmann O., Scholze J., Lipsky P.E., et al. Comparison of immunoglobulin heavy chain rearrangements between peripheral and glandular B cells in a patient with primary Sjogren's syndrome. Scand J Immunol 2003, 57(5):470-479.
20. Dorner T., Hansen A., Jacobi A., Lipsky P.E. Immunglobulin repertoire analysis provides new insights into the immunopathogenesis of Sjogren's syndrome. Autoimmun Rev 2002, 1(3):119-124.
21. Kaschner S., Hansen A., Jacobi A., Reiter K., Monson N.L., Odendahl M., et al. Immunoglobulin V-lambda light chain gene usage in patients with Sjogren's syndrome. Arthritis Rheum 2001, 44(11):2620-2632.
22. Barak M., Zuckerman N.S., Edelman H., Unger R., Mehr R. IgTree(c): creating Immunoglobulin variable region gene lineage trees. J Immunol Methods 2008, 338(1-2):67-74.
23. Kocks C., Rajewsky K. Stepwise intraclonal maturation of antibody-affinity through somatic hypermutation. Proc Natl Acad Sci USA 1988, 85(21):8206-8210.
24. Manser T., Wysocki L.J., Margolies M.N., Gefter M.L. Evolution of antibody variable region structure during the immune-response. Immunol Rev 1987, 96:141-162.
25. Vora K.A., Tumas-Brundage K., Manser T. Contrasting the in situ behavior of a memory B cell clone during primary and secondary immune responses. J Immunol 1999, 163(8):4315-4327.
26. DunnWalters D.K., Boursier L., Ciclitira P.J., Spencer J.O. Immunoglobulin genes from human duodenal and colonic plasma cells are mutated. Biochem Soc Trans 1997, 25(2):S324.
27. DunnWalters D.K., Isaacson P.G., Spencer J. Sequence analysis of human IgV(H) genes indicates that ileal lamina propria plasma cells are derived from Peyer's patches. Eur J Immunol 1997, 27(2):463-467.
28. Shannon M., Mehr R. Reconciling repertoire shift with affinity maturation: the role of deleterious mutations. J Immunol 1999, 162(7):3950-3956.
29. Zuckerman N.S., Howard W.A., Bismuth J., Gibson K., Edelman H., Berrih-Aknin S., et al. Ectopic GC in the thymus of myasthenia gravis patients show characteristics of normal GC. Eur J Immunol 2010, 40(4):1150-1161.
30. Tabibian-Keissar H., Zuckerman N.S., Barak M., Dunn-Walters D.K., Steiman-Shimony A., Chowers Y., et al. B-cell clonal diversification and gut-lymph node trafficking in ulcerative colitis revealed using lineage tree analysis. Eur J Immunol 2008, 38(9):2600-2609.
31. Steiman-Shimony A., Edelman H., Hutzler A., Barak M., Zuckerman N.S., Shahaf G., et al. Lineage tree analysis of immunoglobulin variable-region gene mutations in autoimmune diseases: chronic activation, normal selection. Cell Immunol 2006, 244(2):130-136.
32. Steiman-Shimony A., Edelman H., Barak M., Shahaf G., Dunn-Walters D., Stott D.I., et al. Immunoglobulin variable-region gene mutational lineage tree analysis: application to autoimmune diseases. Autoimmun Rev 2006, 5(4):242-251.
33. Rada C., Ehrenstein M.R., Neuberger M.S., Milstein C. Hot spot focusing of somatic hypermutation in MSH2-deficient mice suggests two stages of mutational targeting. Immunity 1998, 9(1):135-141.
34. Odegard V.H., Schatz D.G. Targeting of somatic hypermutation. Nat Rev Immunol 2006, 6(8):573-583.
35. Di Nola J.M., Neuberger M.S. Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 2007, 76:1-22.
36. Neuberger M.S., Rada C. Somatic hypermutation: activation-induced deaminase for C/G followed by polymerase eta for A/T. J Exp Med 2007, 204(1):7-10.
37. Delbos F., Aoufouchi S., Faili A., Weill J.C., Reynaud C.A. DNA polymerase eta is the sole contributor of A/T modifications during immunoglobulin gene hypermutation in the mouse. J Exp Med 2007, 204(1):17-23.
38. Neuberger M.S., Di Noia J.M., Beale R.C.L., Williams G.T., Yang Z.Z., Rada C. Opinion - somatic hypermutation at A center dot T pairs: polymerase error versus dUTP incorporation. Nat Rev Immunol 2005, 5(2):171-178.
39. Rogozin I.B., Pavlov Y.I., Bebenek K., Matsuda T., Kunkel T.A. Somatic mutation hotspots correlate with DNA polymerase eta error spectrum. Nat Immunol 2001, 2(6):530-536.
40. Boursier L., Su W., Spencer J. Analysis of strand biased G-C hypermutation in human immunoglobulin V-lambda gene segments suggests that both DNA strands are targets for deamination by activation-induced cytidine deaminase. Mol Immunol 2004, 40(17):1273-1278.
41. Michael N., Martin T.E., Nicolae D., Kim N., Padjen K., Zhan P., et al. Effects of sequence and structure on the hypermutability of immunoglobulin genes. Immunity 2002, 16(1):123-134.
42. Weitkamp J.H., LaFleur B.J., Greenberg H.B., Crowe J.E. Natural evolution of a human virus-specific antibody gene repertoire by somatic hypermutation requires both hotspot-directed and randomly-directed processes. Hum Immunol 2005, 66(6):666-676.
43. Spencer J., Dunn-Walters D.K. Hypermutation at A-T base pairs: the A nucleotide replacement spectrum is affected by adjacent nucleotides and there is no reverse complementarity of sequences flanking mutated A and T nucleotides. J Immunol 2005, 175(8):5170-5177.
44. Storb U. DNA polymerases in immunity: profiting from errors. Nat Immunol 2001, 2(6):484-485.
45. Spencer J., Dunn M., Dunn-Walters D.K. Characteristics of sequences around individual nucleotide substitutions in IgV(H) genes suggest different GC and AT mutators. J Immunol 1999, 162(11):6596-6601.
46. Dorner T., Foster S.J., Farner N.L., Lipsky P.E. Somatic hypermutation of human immunoglobulin heavy chain genes: targeting of RGYW motifs on both DNA strands. Eur J Immunol 1998, 28(10):3384-3396.
47. Rogozin I.B., Diaz M. 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 2004, 172(6):3382-3384.
48. Boursier L., Su W., Spencer J. Imprint of somatic hypermutation differs in human immunoglobulin heavy and lambda chain variable gene segments. Mol Immunol 2003, 39(16):1025-1034.
49. Smith D.S., Creadon G., Jena P.K., Portanova J.P., Kotzin B.L., Wysocki L.J. Di- and trinucleotide target preferences of somatic mutagenesis in normal and autoreactive B cells. J Immunol 1996, 156(7):2642-2652.
50. Dunn-Walters D.K., Spencer J. Strong intrinsic biases towards mutation and conservation of bases in human IgV(H) genes during somatic hypermutation prevent statistical analysis of antigen selection. Immunology 1998, 95(3):339-345.
51. Mayorov V.I., Rogozin I.B., Adkison L.R., Gearhart P.J. DNA polymerase eta contributes to strand bias of mutations of A versus T in immunoglobulin genes. J Immunol 2005, 174(12):7781-7786.
52. Chang B., Casali P. The Cdr1 sequences of a major proportion of human germline Ig V-H genes are inherently susceptible to amino-acid replacement. Immunol Today 1994, 15(8):367-373.
53. Lossos I.S., Tibshirani R., Narasimhan B., Levy R. The inference of antigen selection on Ig genes. J Immunol 2000, 165(9):5122-5126.
54. Bose B., Sinha S. Problems in using statistical analysis of replacement and silent mutations in antibody genes for determining antigen-driven affinity selection. Immunology 2005, 116(2):172-183.
55. Hershberg U., Uduman M., Shlomchik M.J., Kleinstein S.H. Improved methods for detecting selection by mutation analysis of Ig V region sequences. Int Immunol 2008, 20(5):683-694.
56. Livingstone C.D., Barton G.J. Protein sequence alignments: a strategy for the hierarchical analysis of residue conservation. Comput Appl Biosci 1993, 9(6):745-756.
57. Betts M.J., Russell R.B. Amino acid properties and consequences of subsitutions. Bioinformatics for geneticists 2003, 289-314. Wiley. M.R. Barnes, I.C. Gray (Eds.).
58. Gause A., Gundlach K., Zdichavsky M., Jacobs G., Koch B., Hopf T., et al. The B-lymphocyte in rheumatoid-arthritis - analysis of rearranged V-kappa genes from B-cells infiltrating the synovial-membrane. Eur J Immunol 1995, 25(10):2775-2782.
59. Colombo M., Dono M., Gazzola P., Roncella S., Valetto A., Chiorazzi N., et al. Accumulation of clonally related B lymphocytes in the cerebrospinal fluid of multiple sclerosis patients. J Immunol 2000, 164(5):2782-2789.
60. Gellrich S., Rutz S., Borkowski A., Golembowski S., Gromnica-Ihle E., Sterry W., et al. Analysis of V-H-D-J(H) gene transcripts in B cells infiltrating the salivary glands and lymph node tissues of patients with Sjogren's syndrome. Arthritis Rheum 1999, 42(2):240-247.
61. Jacobi A.M., Hansen A., Kaufmann O., Pruss A., Burmester G.R., Lipsky P.E., et al. Analysis of immunoglobulin light chain rearrangements in the salivary gland and blood of a patient with Sjogren's syndrome. Arthritis Res 2002, 4(4).
62. Bhattacharya P., Grigera F., Rogozin I.B., McCarty T., Morse H.C., Kenter A.L. Identification of murine B cell lines that undergo somatic hypermutation focused to A:T and G:C residues. Eur J Immunol 2008, 38(1):227-239.
63. Le Panse R., Cizeron-Clairac G., Bismuth J., Berrih-Aknin S. Microarrays reveal distinct gene signatures in the thymus of seropositive and seronegative and the role of CC chemokine myasthenia gravis patients ligand 21 in thymic hyperplasia. J Immunol 2006, 177(11):7868-7879.
64. Meraouna A., Cizeron-Clairac G., Le Panse R., Bismuth J., Truffault F., Tallaksen C., et al. The chemokine CXCL13 is a key molecule in autoimmune myasthenia gravis. Blood 2006, 108(2):432-440.
65. Cupedo T., Mebius R.E. Cellular interactions in lymph node development. J Immunol 2005, 174(1):21-25.
66. Volpe J.M., Kepler T.B. Large-scale analysis of human heavy chain V(D)J recombination patterns. Immunome Res 2008, 4(1):3.
67. Banerjee M., Mehr R., Belelovsky A., Spencer J., Dunn-Walters D.K. Age- and tissue-specific differences in human germinal center B cell selection revealed by analysis of IgV(H) gene hypermutation and lineage trees. Eur J Immunol 2002, 32(7):1947-1957.
68. Abraham R.S., Manske M.K., Zuckerman N.S., Sohni A., Edelman H., Shahaf G., et al. Novel analysis of clonal diversification in blood b cell and bone marrow plasma cell clones in immunoglobulin light chain amyloidosis. J Clin Immunol 2007, 27(1):69-87.
69. Goossens T., Klein U., Kuppers R. Frequent occurrence of deletions and duplications during somatic hypermutation: implications for oncogene translocations and heavy chain disease. Proc Natl Acad Sci USA 1998, 95(5):2463-2468.