Abnormalities of B cell phenotype, immunoglobulin gene expression and the emergence of autoimmunity in Sjögren's syndrome

Arthritis Research

Volumn 4, Issue 6, 2002, Pages 360-371

  Dörner, Thomas ^a   Lipsky, Peter E ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

Autoimmunity; B cells; IgV gene usage; Lymphocytes; Sj gren's syndrome

Indexed keywords

AUTOANTIBODY;

ANTIBODY PRODUCTION; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; BLOOD; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOGLOBULIN GENE; IMMUNOGLOBULIN VARIABLE REGION; LYMPHOCYTE DEPLETION; LYMPHOCYTE SUBPOPULATION; MEMORY CELL; PAROTID GLAND; PATHOGENESIS; PHENOTYPE; REVIEW; SJOEGREN SYNDROME;

AUTOIMMUNITY; B-LYMPHOCYTES; GENE EXPRESSION; HUMANS; IMMUNOGLOBULIN VARIABLE REGION; PAROTID GLAND; PHENOTYPE; SJOGREN'S SYNDROME;

EID: 0036434840     PISSN: 14659905     EISSN: None     Source Type: Journal    
DOI: 10.1186/ar603     Document Type: Review

References (99)

1. Fox RI, Stern M, Michelson P: Update in Sjögren syndrome. Curr Opin Rheumatol 2000, 12:391-398.
2. Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, Daniels TE, Fox PC, Fox RI, Kassan SS, Pillemer SR, Talal N, Weisman MH: European Study Group on Classification Criteria for Sjögren's Syndrome. Assessment of the European classification criteria for Sjögren's syndrome in a series of clinically defined cases: results of a prospective multicentre study. The European Study Group on Diagnostic Criteria for Sjögren's Syndrome. Ann Rheum Dis 1996, 55:116-121.
3. Xanthou G, Tapinos NI, Polihronis M, Nezis IP, Margaritis LH, Moutsopoulos HM: CD4 cytotoxic and dendritic cells in the immunopathologic lesion of Sjögren's syndrome. Clin Exp Immunol 1999, 118:154.
4. Stott DI, Hiepe F, Hummel M, Steinhauser G, Berek C: Antigendriven clonal proliferation of B cells within the target tissue of an autoimmune disease. The salivary glands of patients with Sjögren's syndrome. J Clin Invest 1998, 1102:938-946.
5. Bodeutsch C, de Wilde PC, Kater L, van den Hoogen FH, Hene RJ, van Houwelingen JC, van de Putte LB, Vooijs GP: Monotypic plasma cells in labial salivary glands of patients with Sjögren's syndrome: prognosticator for systemic lymphoproliferative disease. J Clin Pathol 1993, 46:123-128.
6. Horsfall AC, Venables PJ, Allard SA, Maini RN: Co-existent anti-La antibodies and rheumatoid factors bear distinct idiotypic markers. Scand J Rheumatol 1988 (Suppl), 75:84-88.
7. Fox RI, Konttinen Y, Fisher A: Use of muscarinic agonists; in the treatment of Sjögren's syndrome. Clin Immunol 2001, 101:249-263.
8. Schröder AE, Greiner A, Seyfert C, Berek C: Differentiation of B cells in the nonlymphoid tissue of the synovial membrane of patients with rheumatoid arthritis. Proc Natl Acad Sci USA 1996, 93:221-225.
9. Meffre E, Davis E, Schiff C, Cunningham-Rundles C, Ivashkiv LB, Staudt LM, Young JW, Nussenzweig MC: Circulating human B cells that express surrogate light chains and edited receptors. Nat Immunol 2000, 1:207-213.
10. Amft N, Bowman SJ: Chemokines and cell trafficking in Sjögren's syndrome. Scand J Immunol 2001, 54:62-69.
11. Amft N, Curnow SJ, Scheel-Toellner D, Devadas A, Oates J, Crocker J, Hamburger J, Ainsworth J, Mathews J, Salmon M, Bowman SJ, Buckley CD: Ectopic expression of the B cell-attracting chemokine BCA-1 (CXCL13) on endothelial cells and within lymphold follicles contributes to the establishment of germinal center-like structures in Sjögren's syndrome. Arthritis Rheum 2001, 44:2633-2641.
12. Shi K, Hayashida K, Kaneko M, Hashimoto J, Tomita T, Lipsky PE, Yoshikawa H, Ochi T: Lymphold chemokine B cell-attracting chemokine-1 (CXCL13) is expressed in germinal center of ectopic lymphoid follicles within the synovium of chronic arthritis patients. J Immunol 2001, 166:650-655.
13. Halse A, Tengner P, Wahren-Herlenius M, Haga H, Jonsson R: Increased frequency of cells secreting interleukin-6 and interleukin-10 in peripheral blood of patients with primary Sjögrens syndrome. Scand J Immunol 1999, 49:533-528.
14. Moutsopoulos HM, Kordossis T: Sjögren's syndrome revisited: autoimmune epithelitis. Br J Rheumatol 1996, 35:204-206.
15. Taga K, Cherney B, Tosato G: IL-10 inhibits apoptotic cell death in human T cells starved of IL-2. Int Immunol 1993, 5:1599-1608.
16. Fox R, Kang HI, Ando D, Abrams J, Pisa E: Cytokine mRNA expression in salivary gland biopsies of Sjögrens syndrome. J Immunol 1994, 152:5532-5539.
17. Ngo VN, Korner H, Gunn MD, Schmidt KN, Riminton DS, Cooper MD, Browning JL, Sedgwick JD, Cyster JG: Lymphotoxin-αβ and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen. J Exp Med 1999, 189:403-412.
18. Gunn MD, Kyuwa S, Tam C, Kakiuchi T, Matsuzawa A, Williams LT, Nakano H: Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J Exp Med 1999, 189:451-460.
19. Cyster JG: Chemokines and cell migration in secondary lymphoid organs. Science 1999, 286:2098-2102.
20. Forster R, Mattis AE, Kremmer E, Wolf E, Brem G, Lipp M: A putative chemokines receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 1996, 87:1037-1047.
21. Luther SA, Lopez T, Bai W, Hanahan D, Cyster JG: BCA-1 expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 2000, 12:471-481.
22. Nanki T, Hayashida K, El-Gabalawy HS, Suson S, Shi K, Girschick HJ, Yavuz S, Lipsky PE: Stromal cell-derived factor-1-CXC chemokine receptor 4 interactions play a central role in CD4+ T cell accumulation in rheumatoid arthritis synovium. J Immunol 2000, 165:6590-6598.
23. Groom J, Kalled SL, Cutler AH, Olson C, Woodcock SA, Schneider P, Tschopp J, Cachero TG, Batten M, Wheway J, Mauri D, Cavill D, Gordon TP, Mackay CR, Mackay F: Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjögren's syndrome. J Clin Invest 2002, 109:59-68.
24. Zhang J, Roschke V, Baker KP, Wang Z, Alarcon GS, Fessler BJ, Bastian H, Kimberly RP, Zhou T: Cutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosus. J Immunol 2001, 166:6-10.
25. Dörner T, Lipsky PE: Immunoglobulin variable-region gene usage in systemic autoimmune diseases. Arthritis Rheum 2001, 44:2715-2727.
26. Brezinschek HP, Foster SJ, Dörner T, Brezinschek RI, Lipsky PE: Pairing of variable heavy and variable kappa chains in individual naive and memory B cells. J Immunol 1998, 160:4762-4767.
27. Brezinschek HP, Brezinschek RI, Lipsky PE: Analysis of the heavy chain repertoire of human peripheral blood B cells using single-cell polymerase chain reaction. J Immunol 1995, 155:190-202.
28. Brezinschek HP, Foster SJ, Brezinschek RI, Dörner T, Domiati-Saad R, Lipsky PE: Analysis of the human VH gene repertoire. Differential effects of selection and somatic hypermutation on peripheral CD5+/IgM+ and CD5-/IgM+ B cells. J Clin Invest 1997, 99:2488-2501.
29. Farner NL, Dörner T, Lipsky PE: Molecular mechanisms and selection influence the generation of the human VλJλ repertoire. J Immunol 1999, 162:2137-2145.
30. Foster SJ, Brezinschek HP, Brezinschek RI, Lipsky PE: Molecular mechanisms and selective influences that shape the kappa gene repertoire of IgM+ B cells. J Clin Invest 1997, 99:1614-1627.
31. Dörner T, Brezinschek HP, Brezinschek RI, Foster SJ, Domiati-Saad R, Lipsky PE: Analysis of the frequency and pattern of somatic mutations within non-productively rearranged human VH genes. J Immunol. 1997, 158:2779-2789.
32. Dörner T, Brezinschek HP, Foster SJ, Brezinschek RI, Farner NL, Lipsky PE: Comparable impact of mutational and selective influences in shaping the expressed repertoire of peripheral IgM+/CD5- and IgM+/CD5+ B cells. Eur J Immunol 1998; 28:657-668.
33. Odendahl M, Jacobi A, Hansen A, Feist E, Hiepe F, Burmester GR, Lipsky PE, Radbruch A, Dörner T: Disturbed peripheral B lymphocyte homeostasis. J Immunol 2000, 165:5970-5979.
34. Dörner T, Foster SJ, Farner NL, Lipsky PE: Immunoglobulin kappa chain receptor editing in systemic lupus erythematosus. J Clin Invest 1998, 102:688-694.
35. Dörner T, Farner NL, Lipsky PE: Immunoglobulin lambda and heavy chain gene usage in early untreated systemic lupus erythematosus suggests intensive B cell stimulation. J Immunol 1999, 163:1027-1036.
36. Heimbächer C, Hansen A, Pruss A, Jacobi A, Reiter K, Lipsky PE, Dörner T: Immunoglobulin Vκ light chain analysis in patients with Sjögren's syndrome. Arthritis Rheum 2001, 44:626-637.
37. Kaschner S, Hansen A, Jacobi A, Reiter K, Monson NL, Odendahl M, Burmester GR, Lipsky PE, Dörner T: Immunoglobulin Vλlight chain gene usage in patients with Sjögren's syndrome. Arthritis Rheum 2001, 44:2620-2632.
38. Jacobi AM, Hansen A, Kaufmann O, Burmester GR, Lipsky PE, Dörner T: Analysis of immunoglobulin light chain rearrangements in the salivary gland and blood of a patient with Sjögren's syndrome. Arthritis Res 2002, 4:R4.
39. Hansen A, Jacobi AM, Burmester GR, Lipsky PE, Dörner T: Comparison of heavy chain rearrangements in the blood and parotid gland of a patient with Sjögren's syndrome. Scand J Immunol 2002, in press.
40. Hansen A, Odendahl M, Reiter K, Jacobi AM, Feist E, Scholze J, Burmester GR, Lipsky PE, Dörner T: Evidence for the migration and accumulation of memory B cells in the salivary glands of patients with Sjögren's syndrome. Arthritis Rheum 2002, 46:2160-2171.
41. Dörner T, Kaschner S, Hansen A, Pruss A, Lipsky PE: Perturbations in the impact of mutational activity on Vλ genes in systemic lupus erythematosus. Arthritis Res 2001, 3:368-374.
42. de Wildt RM, Hoet RM, van Venrooij WJ, Tomlinson IM, Winter G: Analysis of heavy and light chain pairings indicates that receptor editing shapes the human antibody repertoire. Mol Biol 1999, 285:895-901.
43. Silberstein LE, Jefferies LC, Goldman J, Friedman D, Moore JS, Nowell PC, Roelcke D, Pruzanski W, Roudier J, Silverman GJ: Variable region gene analysis of pathologic human autoantibodies to the related i and I red blood cell antigens. Blood 1991, 78:2372-2386.
44. Dörner T, Heimbacher C, Farner NL, Lipsky PE: Enhanced mutational activity of Vκ gene rearrangements in systemic lupus erythematosus. Clin Immunol 1999, 92:188-196.
45. Pugh-Bernard AE, Silverman GJ, Cappione AJ, Villano ME, Ryan DH, Insel RA, Sanz I: Regulation of inherently autoreactive VH4-34 B cells in the maintenance of human B cell tolerance. J Clin Invest 2001, 108:1061-1070.
46. Yavuz S, Grammer AC, Yavuz AS, Nanki T, Lipsky PE: Comparative characteristics of mu chain and alpha chain transcripts expressed by individual tonsil plasma cells. Mol Immunol 2001, 38:19-34.
47. Kelsoe G: Life and death in germinal centers (Redux). Immunity 1996, 4:107-111.
48. Nemazee D, Weigert M: Revising B cell receptors. J Exp Med 2000, 191:1813-1817.
49. Girschick HJ, Grammer AC, Nanki T, Mayo M, Lipsky PE: RAG1 and RAG2 expression by B cell subsets from human tonsil and peripheral blood. J Immunol 2001, 166:377-386.
50. Lee J, Monson NL, Lipsky PE: The VλJλ repertoire in human fetal spleen: evidence for positive selection and extensive receptor editing. J Immunol 2000, 165:6322-6333.
51. Radic MZ, Zouali M: Receptor editing, immune diversification and self-tolerance. Immunity 1996, 5:505-511.
52. Bensimon C, Chastagner P, Zouali M: Human lupus anti-DNA autoantibodies undergo essentially primary Vκ gene rearrangements. EMBO J 1994, 13:2951-2962.
53. Chen C, Luning-Prak E, Weigert M: Editing disease-associated autoantibodies. Immunity 1997, 6:97-105.
54. Itoh K, Meffre E, Albesiano E, Farber A, Dines D, Stein P, Asnis SE, Furie RA, Jain RI, Chiorazzi N: Immunoglobulin heavy chain variable region gene replacement as a mechanism for receptor revision in rheumatoid arthritis synovial tissue B lymphocytes. J Exp Med 2000, 192:1151-1164.
55. Zhang Z, Wu X, Limbaugh BH, Bridges SL Jr: Expression of recombination-activating genes and terminal deoxynucleotidyl transferase and secondary rearrangement of immunoglobulin kappa light chains in rheumatoid arthritis synovial tissue. Arthritis Rheum 2001, 44:2275-2284.
56. Elagib KE, Borretzen M, Thompson KM, Natvig JB: Light chain variable (VL) sequences of rheumatoid factors (RF) in patients with primary Sjögren's syndrome (pSS): moderate contribution of somatic hypermutation. Scand J Immunol 1999, 50:492-498.
57. Bohnhorst J, Bjorgan MB, Thoen JE, Natvig JB, Thompson KM: 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 Sjögren's syndrome. J Immunol 2001, 167:3610-3618.
58. Bahler DW, Swerdlow SH: Clonal salivary gland infiltrates associated with myoepithelial sialadenitis (Sjögren's syndrome) begin as nonmalignant antigen-selected expansion. Blood 1998, 91:1864-1872.
59. Kipps TJ, Tomhave E, Chen PP, Fox RI: Molecular characterization of a major autoantibody-associated cross-reactive idiotype in Sjögren's syndrome. J Immunol 1989, 142:4261-4268.
60. Gellrich S, Rutz S, Borkowski A, Golembowski S, Gromnica-Ihle E, Sterry W, Jahn S: Analysis of V(H)-D-J(H) gene transcripts in B cells infiltrating the salivary glands and lymph node tissues of patients with Sjögren's syndrome. Arthritis Rheum 1999, 42:240-247.
61. Tomlinson IM, Cook GP, Walter G, Carter NP, Riethman H, Buluwela L, Rabbitts TH, Winter G: A complete map of the human immunoglobulin VH locus. Ann NY Acad Sci 1995, 764:43-46.
62. Insel RA, Adderson EE, Carroll WL: The repertoire of human antibody to the Haemophilus influenzae type b capsular polysaccharide. Int Rev Immunol 1992, 9:25-43.
63. Sun Y, Park MK, Kim J, Diamond B, Solomon A, Nahm MH: Repertoire of human antibodies against the polysaccharide capsule of Streptococcus pneumoniae serotype 6B. Infect Immun 1999, 67:1172-1179.
64. Ikematsu W, Kobarg J, Ikematsu H, Ichiyoshi Y, Casali P: Clonal analysis of a human antibody response. III. Nucleotide sequences of monoclonal IgM, IgG, and IgA to rabies virus reveal restricted Vκ gene utilization, junctional VκJκ and VλJλ diversity, and somatic hypermutation. J Immunol 1998, 161:2895-2905.
65. Deacon EM, Matthews JB, Potts AJ, Hamburger J, Mageed RA, Jefferis R: Expression of rheumatoid factor associated cross-reactive idiotypes by glandular B cells in Sjögren's syndrome. Clin Exp Immunol 1991, 83:280-285.
66. Martin T, Weber JC, Levallois H, Labouret N, Soley A, Koenig S, Korganow AS, Pasquali JC: Salivary gland lymphomas in patients with Sjögren's syndrome may frequently develop from rheumatoid factor B cells. Arthritis Rheum 2000, 43:908-916.
67. Bahler DW, Miklos JA, Swerdlow SH: Ongoing Ig gene hypermutation in salivary gland mucosa-associated lymphoid tissue-type lymphomas. Blood 1997, 89:3335-3344.
68. Klein U, Rajewsky K, Küppers R: Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med 1998, 188:1679-1689.
69. Miklos JA, Swerdlow SH, Bahler DW: Salivary gland mucosa associated lymphoid tissue lymphoma immunoglobulin VH genes show frequent use of V1-69 with distinctive CDR3 features. Blood 2000, 95:3878-3884.
70. Rosner K, Winter DB, Tarone RE, Skovgaard GL, Bohr VA, Gearhart PJ: Third complementarity-determining region of mutated VH immunoglobulin genes contains shorter V, D, J, P, and N components than non-mutated genes. Immunology 2001, 103:179-187.
71. Küppers R, Zhao M, Hansmann ML, Rajewsky K: Tracing B cell development in human germinal centres by molecular analysis of single cells picked from histological sections. EMBO J 1993, 12:4955-4967.
72. Arce E, Jackson DG, Gill MA, Bennett LB, Banchereau J, Pascual V: Increased frequency of pre-germinal center B cells and plasma cell precursors in the blood of children with systemic lupus erythematosus. J Immunol 2001, 167:2361-2369.
73. Agematsu K, Nagumo H, Yang FC, Nakazawa T, Fukushima K, Ito S, Sugita K, Mori T, Kobata T, Morimoto C: B cell subpopulations separated by CD27 and crucial collaboration of CD27+ B cells and helper T cells in immunoglobulin production. Eur J Immunol 1997, 27:2073-2079.
74. Tangye SG, Liu YJ, Aversa G, Phillips JH, de Vries JE: Identification of functional human splenic memory B cells by expression of CD148 and CD27. J Exp Med 1998, 188:1691-1703.
75. Agematsu K, Nagumo H, Oguchi Y, Nakazawa T, Fukushima K, Yasui K, Ito S, Kobata T, Morimoto C, Komiyama A: Generation of plasma cells from peripheral blood memory B cells: synergistic effect of interleukin-10 and CD27/CD70 interaction. Blood 1998, 91:173-180.
76. Nagumo H, Agematsu K, Shinozaki K, Hokibara. S, Ito S, Takamoto M, Nikaido T, Yasui K, Uehara Y, Yachie A: CD27/CD70 interaction augments IgE secretion by promoting the differentiation of memory B cells into plasma cells. J Immunol 1998, 161:6496-6502.
77. Shinozaki K, Yasui K, Agematsu K: Direct B/B-cell interactions in immunoglobulin synthesis. Clin Exp Immunol 2001, 124:386-391.
78. Nagumo H, Agematsu K, Kobayashi N, Shinozaki K, Hokibara S, Nagase H, Takamoto M, Yasui K, Sugane K, Komiyama A: The different process of class switching and somatic hypermutation; a novel analysis by CD27 naive B cells. Blood 2002, 99:567-575.
79. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T: Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000, 102:553-563.
80. Moir S, Malaspina A, Ogwaro KIM, Donoghue ET, Hallahan CW, Ehler LA, Liu S, Adelsberger J, Lapointe R, Hwu P: HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc Natl Acad Sci USA 2001, 98:10362-10367.
81. Widney D, Gundapp G, Said JW, van der Meijden M, Bonavida B, Demidem A, Trevisan C, Taylor J, Detels R, Martinez-Maza O: Aberrant expression of CD27 and soluble CD27 (sCD27) in HIV infection and in AIDS-associated lymphoma. Clin Immunol 1999, 93:114-123.
82. + memory B cell population in X-linked hyper-IgM syndrome. J Clin Invest 1998, 102:853-860.
83. Denz A, Eibel H, Illges H, Kienzle G, Schlesier M, Peter HH: Impaired up-regulation of CD86 in B cells of 'type A' common variable immunodeficiency patients. Eur J Immunol 2000, 30:1069-1077.
84. Ebo D, DeClerck LS, Bridts CH, Stevens WJ: Expression of CD5 and CD23 on B cells of patients with rheumatoid arthritis, systemic lupus erythernatosus and Sjögren's syndrome. Relationship with disease activity and treatment. In Vivo 1994, 8:577-580.
85. Zeher M, Suranyi P, Nagy G, Szegedi G: B cells expressing CD5 in minor labial salivary glands of patients with primary Sjögren's syndrome [comment]. Arthritis Rheum 1990, 33:453.
86. Brennan F, Plater-Zyberk C, Maini RN, Feldmann M: Coordinate expansion of 'fetal type' lymphocytes (TCRγΔ+T and CD5+B) in rheumatoid arthritis and primary Sjögren's syndrome. Clin Exp Immunol 1989, 77:175-178.
87. Plater-Zyberk C, Brennan FM, Feldmann M, Maini RN: 'Fetal-type' B and T lymphocytes in rheumatoid arthritis and primary Sjögren's syndrome. J Autoimmun 1989, Suppl. 2:233-241.
88. Foster HE, Calvert JE, Kelly CA, Griffiths ID: Levels of CD5+ B cells are not increased in probands or relatives in a family study of primary Sjögren's syndrome. Autoimmunity 1992, 12:207-214.
89. Dauphinee M, Tovar Z, Talal N: B cells expressing CD5 are increased in Sjögren's syndrome. Arthritis Rheum 1988, 31:642-647.
90. DiGiuseppe JA, Corio RL, Westra WH: Lymphoid infiltrates of the salivary glands: pathology, biology, and clinical significance. Curr Opin Oncol 1996; 8:232-237.
91. De Vita S, Boiocchi M, Sorrentino D, Carbone A, Avellini C: Characterization of prelymphomatous stages of B cell lymphoproliferation in Sjögren's syndrome. Arthritis Rheum 1997, 40:318-331.
92. Kassan SS, Thomas TL, Moutsoloulos HIM, Hoover R, Kimberly RP, Budman DR, Costa J, Decker JL, Cused TM: Increased risk of lymphoma in sicca syndrome. Ann Intern Med 1978, 89:888-892.
93. Chen PP, Olsen NJ, Yang PM, Soto-Gil RW, Olee T, Siminovitch KA, Carson DA: From human autoantibodies to the fetal antibody repertoire to B cell malignancy: it's a small world after all. Intern Rev Immunol 1990, 5:239-251.
94. Mackay IR, Rose NR: Autoimmunity and lymphoma: tribulations of B cells. Nat Immunol 2001, 2:793-795.
95. Bahler DW, Miklos JA, Swerdlow SH: Ongoing Ig gene hypermutation in salivary gland mucosa-associated lymphoid tissue type lymphomas. Blood 1997, 89:3335-3344.
96. Miklos JA, Swerdlow SH, Bahler DW: Salivary gland mucosa-associated lymphoid tissue lymphoma immunoglobulin VH genes show frequent use of V1-69 with distinctive CDR3 features. Blood 2000, 95:3878-3884.
97. van Oers MH, Pals ST, Evers LM, van der Schoot CE, Koopman G, Bonfrer JM, Hintzen RQ, von dem Borne AE, van Lier RA: Expression and release of CD27 in human B-cell malignancies. Blood 1993, 82:3430-3406.
98. Lens SM, Tesselaar K, van Oers MH, van Lier RA: Control of lymphocyte function through CD27-CD70 interactions. Semin Immunol 1998, 10:491-499.
99. Ruzickova S, Pruss A, Odendahl M, Wolbart K, Burmester GR, Dörner T, Hansen A: Chronic lymphocytic leukemia preceeded by cold agglutinin disease: intraclonal Ig light chain diversity in VH4-34 expressing single B cells. Blood 2002, in press.