B cells in Sjögren's syndrome: Indications for disturbed selection and differentiation in ectopic lymphoid tissue

Arthritis Research and Therapy

Volumn 9, Issue 4, 2007, Pages

  Hansen, Arne ^a   Lipsky, Peter E ^b   Dörner, Thomas ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CD20 ANTIBODY; CD27 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; CXCL13 CHEMOKINE; STROMAL CELL DERIVED FACTOR 1; CHEMOKINE RECEPTOR CXCR; UNCLASSIFIED DRUG;

AUTOIMMUNE DISEASE; B CELL LYMPHOMA; BLOOD; CD4+ T LYMPHOCYTE; CELL INFILTRATION; DISEASE PREDISPOSITION; FOLLICULAR DENDRITIC CELL; GENE MUTATION; HISTOPATHOLOGY; HUMAN; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOPATHOGENESIS; IMMUNOPHENOTYPING; LIGAND BINDING; MEMORY CELL; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; SALIVARY GLAND; SALIVARY GLAND BIOPSY; SIALOADENITIS; SJOEGREN SYNDROME; B LYMPHOCYTE; CELL DIFFERENTIATION; CHEMOTAXIS; CHORISTOMA; IMMUNOLOGY; LYMPHOCYTE SUBPOPULATION; LYMPHOID TISSUE; METABOLISM; PATHOLOGY;

B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CHEMOTAXIS; CHORISTOMA; HUMANS; LYMPHOCYTE SUBSETS; LYMPHOID TISSUE; RECEPTORS, CXCR; SALIVARY GLANDS; SIALADENITIS; SJOGREN'S SYNDROME;

EID: 36949031360     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2210     Document Type: Review

References (117)

1. Fox RI Sjögren's syndrome Lancet 2005, 366:321-331. 10.1016/ S0140-6736(05)66990-5 16039337
2. Kassan SS Moutsopoulos HM Clinical manifestations and early diagnosis of Sjögren syndrome Arch Intern Med 2004, 164:1275-1284. 10.1001/ archinte.164.12.1275 15226160
3. Hansen A Lipsky PE Dörner T Immunopathogenesis of primary Sjögren's syndrome: Implications for disease management and therapy Curr Opin Rheum 2005, 17:558-565. 10.1097/01.bor.0000172801.56744.c3
4. Mitsias DI Kapsogeorgou EK Moutsopoulos HM The role of epithelial cells in the initiation and perpetuation of autoimmune lesions: Lessons from Sjögren's syndrome (autoimmune epithelitis) Lupus 2006, 15:255-261. 10.1191/0961203306lu2290rr 16761498
5. Cisholm DM Mason DK Labial salivary gland biopsy in Sjögren's disease J Clin Pathol 1968, 21:656-660. 473887 5697370 10.1136/ jcp.21.5.656
6. Daniels TE Labial salivary gland biopsy in Sjögren's syndrome. Assessment as a diagnostic criterion in 362 suspected cases Arthritis Rheum 1984, 27:147-156. 10.1002/art.1780270205 6696772
7. Adamson TC Fox RI Frisman DM Howell FV Immmunohistologic analysis of lymphoid infiltrates in primary Sjögren's syndrome using monoclonal antibodies J Immunol 1983, 130:203-208. 6600176
8. Larsson A Bredberg A Henriksson G Manthorpe R Sallmyr A Immunohistochemistry of the B-cell component in lower lip salivary glands of Sjögren's syndrome and healthy subjects Scand J Immunol 2005, 61:98-107. 10.1111/j.0300-9475.2005.01540.x 15644129
9. 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, 118:154-163. 1905402 10540173 10.1046/j.1365-2249.1999.01037.x
10. Zeher M Adany R Nagy G Gomez R Szegedi G Macrophage containing factor XIII subunit a in salivary glands of patients with Sjögren's syndrome J Investig Allergol Clin Immunol 1991, 1:261-265. 1669586
11. James JA Harley JB Scofield RH Role of viruses in systemic lupus erythematosus and Sjögren's syndrome Curr Opin Rheumatol 2001, 13:370-376. 10.1097/00002281-200109000-00005 11604590
12. Fox RI Pearson G Vaughan JH Detection of Epstein-Barr virus-associated antigens and DNA in salivary gland biopsies from patients with Sjögren's syndrome J Immunol 1986, 137:3162-3168. 3021847
13. Nakamura H Kawakami A Tominaga M Hida A Yamasaki S Migita K Kawabe Y Nakamura T Eguchi K Relationship between Sjögren's syndrome and human T-lymphotropic virus type I infection: Follow-up study of 83 patients J Lab Clin Med 2000, 135:139-144. 10.1067/mlc.2000.103429 10695658
14. Triantafyllopoulou A Tapinos N Moutsopoulos HM Evidence for Coxsackievirus infection in primary Sjögren's syndrome Arthritis Rheum 2004, 50:2897-2902. 10.1002/art.20463 15457458
15. Bolstad AI Jonsson R Genetic aspects of Sjögren's syndrome Arthritis Res 2002, 4:353-359. 153844 12453311 10.1186/ar599
16. Saegusa K Ishimaru N Yanagi K Mishima K Arakaki R Suda T Saito I Hayashi Y Prevention and induction of autoimmune exocrinopathy is dependent on pathogenic autoantigen cleavage in murine Sjögren's syndrome J Immunol 2002, 169:1050-1057. 12097413
17. Nordmark G Alm GV Ronnblom L Mechanisms of disease: Primary Sjögren's syndrome and the type I interferon system Nat Clin Pract Rheumatol 2006, 2:262-269. 10.1038/ncprheum0173 16932699
18. Nagata Y Inoue H Yamada K Higashiyama H Mishima K Kizu Y Takeda I Mizuno F Hayashi Y Saito I Activation of Epstein-Barr virus by saliva from Sjögren's syndrome patients Immunology 2004, 111:223-229. 1782400 15027908 10.1111/j.0019-2805.2003.01795.x
19. Hagiwara E Pando J Ishigatsubo Y Klinman DM Altered frequency of type 1 cytokine secreting cells in the peripheral blood of patients with primary Sjögren's syndrome J Rheumatol 1998, 25:89-93. 9458209
20. Mitsias DI Tzioufas AG Veiopoulou C Zintzaras E Tassios IK Kogopoulou O Moutsopoulos HM Thyphronitis G The Th1/Th2 cytokine balance changes with the progress of the immunopathological lesion of Sjögren's syndrome Clin Exp Immunol 2002, 128:562-568. 1906267 12067313 10.1046/ j.1365-2249.2002.01869.x
21. Zintsaras E Voulgarelis M Moutsopoulos HM The risk of lymphoma development in autoimmune diseases: A meta-analysis Arch Intern Med 2005, 165:2337-2344. 10.1001/archinte.165.20.2337 16287762
22. 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. 11564773
23. Bohnhorst JO Bjorgan MB Thoen JE Jonsson R Natvig JB Thompson KM Abnormal B cell differentiation in primary Sjögren's syndrome results in a depressed percentage of circulating memory B cells and elevated levels of soluble CD27 that correlate with serum IgG concentration Clin Immunol 2002, 103:79-88. 10.1006/clim.2002.5199 11987988
24. Hansen A Odendahl M Reiter K Jacobi AM Feist E Scholze J Burmester GR Lipsky PE Dörner T Diminished peripheral blood memory B cells and accumulation of memory B cells in the salivary glands of patients with Sjögren's syndrome Arthritis Rheum 2002, 46:2160-2167. 10.1002/ art.10445 12209521
25. Hansen A Gosemann M Pruss A Reiter K Ruzickova S Lipsky PE Dörner T Abnormalities in peripheral B cell memory of patients with primary Sjögren's syndrome Arthritis Rheum 2004, 50:1897-1908. 10.1002/ art.20276 15188366
26. Hansen A Reiter K Ziprian T Jacobi A Hoffmann A Gosemann M Scholze J Lipsky PE Dörner T Dysregulation of chemokine receptor expression and function by B cells of patients with primary Sjögren's syndrome Arthritis Rheum 2005, 52:2109-2119. 10.1002/art.21129 15986367
27. Stott DI Hiepe F Hummel M Steinhauser G Berek C Antigen-driven 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, 102:938-946. 508959 9727062
28. Amft N Curnow SJ Scheel-Toellner D Devadas A Oates J Crocker J Hamburger J Ainsworth J Mathews J Salmon M Ectopic expression of the B cell-attracting chemokine BCA-1 (CXCL13) on endothelial cells and within lymphoid follicles contributes to the establishment of germinal center-like structures in Sjögren's syndrome Arthritis Rheum 2001, 44:2633-2641. 10.1002/ 1529-0131(200111)44:11<2633::AID-ART443>3.0.CO;2-9 11710719
29. Xanthou G Polihronis M Tzioufas AG Paikos S Sideras P Moutsopoulos HM 'Lymphoid' chemokine messenger RNA expression by epithelial cells in the chronic inflammatory lesion of the salivary glands of Sjögren's syndrome patients. Possible participation in lymphoid structure formation Arthritis Rheum 2001, 44:408-418. 10.1002/ 1529-0131(200102)44:2<408::AID-ANR60>3.0.CO;2-0 11229473
30. Salomonsson S Larsson P Tengnér P Mellquist E Hjelmström P Wahren-Herlenius M Expression of the B cell-attracting chemokine CXCL13 in the target organ and autoantibody production in ectopic lymphoid tissue in the chronic inflammatory disease Sjögren's syndrome Scand J Immunol 2002, 55:336-342. 10.1046/j.1365-3083.2002.01058.x 11967114
31. Barone F Bombardieri M Manzo A Blades MC Morgan PR Challacombe SJ Valesini G Pitzalis C Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjögren's syndrome Arthritis Rheum 2005, 52:1773-1784. 10.1002/ art.21062 15934082
32. Salomonsson S Jonsson MV Skarstein K Brokstad KA Hjelmström P Wahren-Herlenius M Jonsson R Cellular basis of ectopic germinal center formation and autoantibody production in the target organ of patients with Sjögren's syndrome Arthritis Rheum 2003, 48:3187-3201. 10.1002/ art.11311 14613282
33. Jonsson MV Szodoray P Jellestad S Jonsson R Skarstein K Association between circulating levels of the novel TNF family members APRIL and BAFF and lymphoid organization in primary Sjögren's syndrome J Clin Immunol 2005, 25:189-201. 10.1007/s10875-005-4091-5 15981083
34. Szodoray P Alex P Jonsson MV Knowlton N Dozmorov I Nakken B Delaleu N Jonsson R Centola M Distinct profiles of Sjögren's syndrome patients with ectopic salivary gland germinal centers revealed by serum cytokines and BAFF Clin Immunol 2005, 117:168-176. 10.1016/ j.clim.2005.06.016 16126006
35. Daridon C Pers JO Devauchelle V Martins-Cavalho C Hutin P Pennec YL Saraux A Youinouh P Identification of transitional type II B cells in the salivary glands of patients with primary Sjögren's syndrome Arthritis Rheum 2006, 54:2280-2288. 10.1002/art.21936 16802367
36. 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. 40210 8552609 10.1073/pnas.93.1.221
37. Hutloff A Buchner K Reiter K Baelde HJ Odendahl M Jacobi A Dörner T Kroczek RA Involvement of inducible costimulator in the exaggerated memory B cell and plasma cell generation in systemic lupus erythematosus Arthritis Rheum 2004, 50:3211-3220. 10.1002/art.20519 15476242
38. Hsi ED Singleton TP Svoboda SM Schnitzer B Ross CW Characterization of the lymphoid infiltrate in Hashimoto thyroiditis by immunohistochemistry and polymerase chain reaction for immunoglobulin heavy chain rearrangement Am J Clin Pathol 1998, 110:327-333. 9728607
39. Ansell SM Grant CS Habermann TM Primary thyroid lymphoma Semin Oncol 1999, 26:316-323. 10375088
40. Kordossis T Paikos S Aroni K Kitsanta P Dimitrakopoulos A Kavouklis E Alevizou V Kyriaki P Skopouli FN Moutsopoulos HM Prevalence of Sjögren's-like syndrome in a cohort of HIV-1-positive patients: descriptive pathology and immunopathology Br J Rheumatol 1998, 37:691-695. 10.1093/rheumatology/37.6.691 9667626
41. 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. 10.1006/clim.1999.4782 10527687
42. Scott CA Avellini C Desinan L Pirisi M Ferraccioli GF Bardus P Fabris C Casatta L Bartoli E Beltrami CA Chronic lymphocytic sialoadenitis in HCV-related chronic liver disease: Comparison of Sjögren's syndrome Histopathology 1997, 30:41-48. 10.1046/j.1365-2559.1997.d01-561.x 9023556
43. Arcaini L Burcheri S Rossi A Paulli M Bruno R Passamonti F Brusamolino E Molteni A Pulsoni A Cox MC Prevalence of HCV infection in nongastric marginal zone B-cell lymphoma of MALT Ann Oncol 2007, 18:346-350. 10.1093/annonc/mdl388 17071937
44. Maszzuccheli L Blaser A Kappeler A Scharli P Laissue JA Baggiolini M Uguccioni M BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma J Clin Invest 1999, 104:R49-R54. 481995 10562310
45. Fox RI Saito I Criteria for diagnosis of Sjögren's syndrome Rheum Dis Clin North Am 1994, 20:391-407. 8016418
46. Vitali C Bombardieri S Jonsson R Moutsopoulos HM Alexander EL Carsons SE Daniels TE Fox PC Fox RI Kassan SS the European Study Group on Classification Criteria for Sjögren's Syndrome Classification criteria for Sjögren's syndrome: A revised version of the European criteria proposed by the American-European consensus group Ann Rheum Dis 2002, 61:554-558. 1754137 12006334 10.1136/ard.61.6.554
47. Dawson LJ Stanbury J Venn N Hasdimir B Rogers SN Smith PM Antimuscarinic antibodies in primary Sjögren's syndrome reversibly inhibit the mechanism of fluid secretion by human submandibular salivary acinar cells Arthritis Rheum 2006, 54:1165-1173. 10.1002/art.21764 16572451
48. Jonsson MV Delaleu N Brokstad KA Berggreen E Skarstein K Impaired salivary gland function in NOD mice: Association with changes in cytokine profile but not with histopathologic changes in the salivary gland Arthritis Rheum 2006, 54:2300-2305. 10.1002/art.21945 16802370
49. Tsunawaki S Nakamura S Ohyama Y Sasaki M Ikebe-Hiroki A Hiraki A Kadena T Kawamura W Shinohara M Shirasuna K Possible function of salivary gland epithelial cells as nonprofessional antigen-presenting cells in the development of Sjögren's syndrome J Rheumatol 2002, 29:1884-1896. 12233883
50. Vogelsang P Jonsson MV Dalvin ST Appel S Role of dendritic cells in Sjögren's syndrome Scand J Immunol 2006, 64:219-226. 10.1111/ j.1365-3083.2006.01811.x 16918690
51. Dimitrou ID Kapsogeorgou EK Moutsopoulos HM Manoussakis MN CD40 on salivary gland epithelial cells: High constitutive expression by cultured cells from Sjögren's syndrome patients indicating their intrinsic activation Clin Exp Immunol 2002, 127:386-392. 1906327 11876766 10.1046/j.1365-2249.2002.01752.x
52. Ohlsson M Szodoray P Loro LL Johanessen AC Jonsson R CD40, CD154, Bax and Bcl-2 expression in Sjögren's syndrome salivary glands: A putative anti-apoptotic role during its effector phases Scand J Immunol 2002, 56:561-571. 10.1046/j.1365-3083.2002.01168.x 12472667
53. Groom J Kalled SL Cutler AH Olson C Woodcock SA Schneider P Tschopp J Cachero TG Batten M Wheway J Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjögren's syndrome J Clin Invest 2002, 109:59-68. 150825 11781351 10.1172/JCI200214121
54. Ittah M Miceli-Richard C Gottenberg JE Lavie F Lazure T Ba N Sellam J Lepajolec C Mariette X B-cell activating factor of the tumor necrosis factor family (BAFF) is expressed under stimulation by interferon in salivary gland epithelial cells in primary Sjögren's syndrome Arthritis Res Ther 2006, 8:R51. 1526588 16507175 10.1186/ar1912
55. Lavie F Miceli-Richard C Quillard J Roux S Leclerc P Mariette X Expression of BAFF (BLys) in T cell infiltrating labial salivary glands from patients with Sjögren's syndrome J Pathol 2004, 202:496-502. 10.1002/path.1533 15095277
56. Kelsoe G Life and death in germinal centers (Redux) Immunity 1996, 4:107-111. 10.1016/S1074-7613(00)80675-5 8624801
57. 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. 11086103
58. Shi K Hayashida K Kaneko M Hashimoto J Tomita T Lipsky PE Yoshikawa H Ochi T Lymphoid 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. 11123349
59. Weyand CM Kurtin PJ Goronzy JJ Ectopic lymphoid organogenesis. A fast track for autoimmunity Am J Pathol 2001, 159:787-793. 1850453 11549568
60. Cupedo T Mebius RE Role of chemokines in the development of secondary and tertiary lymphoid tissues Semin Immunol 2003, 15:243-248. 10.1016/ j.smim.2003.08.002 15001173
61. Manthorpe R Benoni C Jacobsson L Kirtava Z Larsson A Riedholm R Nyhagen C Tabery H Theander E Lower frequency of focal lip sialadenitis (focus score) in smoking patients. Can tobacco diminish the salivary gland involvement as judged by histological examination and anti-SSA/Ro and anti-SSB/La antibodies in Sjögren's syndrome? Ann Rheum Dis 2000, 59:54-60. 1752994 10627428 10.1136/ard.59.1.54
62. Wise CM Woodruff RD Minor salivary gland biopsies in patients investigated for primary Sjögren's syndrome. A review of 187 patients J Rheumatol 1993, 20:1515-1518. 8164207
63. Hyjek E Smith WJ Isaacson PG Primary B-cell lymphoma of salivary glands and its relationship to myoepithelial sialadenitis Hum Pathol 1988, 19:766-776. 10.1016/S0046-8177(88)80259-4 3136072
64. Jaffe ES Lymphoid lesions of the head and neck: A model of lymphocyte homing and lymphomagenesis Mod Pathol 2002, 15:255-263. 10.1038/ modpathol.3880521 11904341
65. Ioannidis JP Vassiliou VA Moutsopoulos HM Long-term risk of mortality and lymphoproliferative disease and predictive classification of primary Sjögren's syndrome Arthritis Rheum 2002, 46:741-747. 10.1002/ art.10221 11920410
66. Xu KP Katagiri S Takeuchi T Tsubota K Biopsy of labial salivary glands and lacrimal glands in the diagnosis of Sjögren's syndrome J Rheumatol 1997, 23:76-82. 8838512
67. Pijpe J Kalk WW van der Wal JE Vissink A Kluin PM Roodenburg JL Bootsma H Kallenberg CG Spijkervert FK Parotid gland biopsy compared to labial biopsy in the diagnosis of patients with primary Sjögren's syndrome Rheumatology.
68. Dörner T Lipsky PE Abnormalities of B cell phenotype, immunoglobulin gene expression and the emergence of autoimmunity in Sjögren's syndrome Arthritis Res 2002, 4:360-371. 153845 12453312 10.1186/ar603
69. Potter KN Mockridge CI Rahman A Buchan S Hamblin T Davidson B Isenberg DA Stevenson FK Disturbances in peripheral blood B cell subpopulations in autoimmune patients Lupus 2002, 11:872-877. 10.1191/0961203302lu309oa 12529053
70. + 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. 10.1084/jem.188.9.1679 9802980
71. 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. 10.1002/eji.1830270835 9295047
72. Shinozaki K Yasui K Agematsu K Direct B/B-cell interactions in immunoglobulin synthesis Clin Exp Immunol 2001, 124:386-391. 1906067 11472398 10.1046/j.1365-2249.2001.01518.x
73. 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. 10.1182/blood.V99.2.567 11781240
74. Odendahl M Mei H Hoyer BF Jacobi AM Hansen A Radbruch A Dörner T Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response Blood 2005, 105:1614-1621. 10.1182/blood-2004-07-2507 15507523
75. Odendahl M Jacobi A Hansen A Feist E Hiepe F Burmester GR Lipsky PE Radbruch A Dörner T Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus J Immunol 2000, 165:5970-5979. 11067960
76. Jacobi AM Odendahl M Reiter K Bruns A Burmester GR Radbruch A Valet G Lipsky PE Dörner T Correlation between circulating CD27high plasma cells and disease activity in patients with systemic lupus erythematosus Arthritis Rheum 2003, 48:1332-1342. 10.1002/art.10949 12746906
77. Mandl T Bredberg A Jacobsson LT Manthorpe R Henriksson G CD4+ lymphopenia - a frequent finding in anti-SSA antibody seropositive patients with primary Sjögren's syndrome J Rheumatol 2004, 31:726-728. 15088298
78. Gellrich S Rutz S Borkowski A Golembowski S Gromnica-Ihle E Sterry W Jahn S Analysis of VH-D-JH 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. 10.1002/ 1529-0131(199902)42:2<240::AID-ANR5>3.0.CO;2-I 10025917
79. Hansen A Jacobi A Pruss A Kaufmann O Scholze J Lipsky PE Dörner T Comparison of immunoglobulin heavy chain rearrangements between peripheral and glandular B cells in a patient with primary Sjögren's syndrome Scand J Immunol 2003, 57:470-479. 10.1046/ j.1365-3083.2003.01226.x 12753504
80. Jacobi AM Hansen A Kaufmann O Burmester GR Lipsky PE Dörner T Analysis of immunglobulin light chain rearrangements in the salivary gland and blood of a patient with Sjögren's syndrome Arthritis Res 2002, 4:R4. 125296 12106503 10.1186/ar423
81. Ansel KM Ngo VN Hyman PL Luther SA Forster R Sedgwick JD Browning JL Lipp M Cyster JG A chemokine-driven feedback loop organizes lymphoid follicles Nature 2000, 406:309-314. 10.1038/35018581 10917533
82. Dörner T Lipsky PE Signalling pathways in B cells: Implications for autoimmunity Curr Top Microbiol Immunol 2006, 305:213-240. 16724808
83. Horsfall AC Rose LM Maini RN Autoantibodiy synthesis in salivary glands of Sjögren's syndrome patients J Autoimmun 1989, 2:554-568. 10.1016/ 0896-8411(89)90189-3
84. Berra A Sterin-Borda L Bacman S Borda E Role of salivary IgA in the pathogenesis of Sjögren syndrome Clin Immunol 2002, 104:49-57. 10.1006/clim.2002.5228 12139947
85. Rutjes SA Utz PJ van der Heijden A Broekhuis C van Venrooij WJ Purin GJM The La (SS-B) autoantigen, a key protein in RNA biogenesis, is dephosphorylated and cleaved early during apoptosis Cell Death Differ 1999, 6:976-986. 10.1038/sj.cdd.4400571 10556975
86. Ohlsson M Jonsson R Brokstad KA Subcellular redistribution and surface exposure of the Ro52, Ro60 and La48 autoantigens during apoptosis in human ductal epithelial cells: A possible mechanism in the pathogenesis of Sjögren's syndrome Scand J Immunol 2002, 56:456-469. 10.1046/ j.1365-3083.2002.01072_79.x 12410795
87. Espinosa A Zhou W Ek M Hedlund M Brauner S Popovic K Horvath L Wallerskog T Mohamed O Nyberg F The Sjögren's syndrome-associated autoantigen Ro 52 is an E3 ligase that regulates proliferation and cell death J Immunol 2006, 176:6277-6285. 16670339
88. Namekawa T Kuroda K Kato T Yamamoto K Murata H Sakamaki T Nishioka K Iwamoto I Saitoh Y Sumida T Identification of Ro(SSA) 52 kDa reactive T cells in labial salivary glands from patients with Sjögren's syndrome J Rheumatol 1995, 22:2092-2099. 8596150
89. Tengnér P Halse AK Haga HJ Jonsson R Wahren-Herlenius M Detection of anti-Ro/SSA and anti-La/SSB autoantibody-producing cells in salivary glands from patients with Sjögren's syndrome Arthritis Rheum 1998, 41:2238-2248. 10.1002/ 1529-0131(199812)41:12<2238::AID-ART20>3.0.CO;2-V 9870881
90. Weller S Faili A Garcia C Braun MC Le Deist FF de Saint Basile GG Hermine O Fischer A Reynaud CA Weill JC CD40-CD40L independent Ig gene hypermutation suggests a second B cell diversification pathway in humans Proc Natl Acad Sci USA 2001, 98:1166-1170. 14726 11158612 10.1073/ pnas.98.3.1166
91. Obukhanych TV Nussenzweig MC T-independent type II immune responses generate memory B cells J Exp Med 2006, 203:305-310. 10.1084/ jem.20052036 16476769
92. Ng LG Ng CH Woehl B Sutherland AP Huo J Xu S Mackay F Lam KP BAFF costimulation of Toll-like receptor-activated B1 cells Eur J Immunol 2006, 36:1837-1846. 10.1002/eji.200635956 16791880
93. Dörner T Egerer K Feist E Burmester GR Rheumatoid factor revisited Curr Opin Rheumatol 2004, 16:246-253. 10.1097/00002281-200405000-00013 15103252
94. 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. 1535268 1899631
95. 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. 2542406
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. 10845923
97. 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. 10.1002/ 1529-0131(200004)43:4<908::AID-ANR24>3.0.CO;2-K 10765938
98. Hansen A Reiter K Pruss A Loddenkemper C Kaufmann O Jacobi AM Scholze J Lipsky PE Dörner T Dissemination of a Sjögren's syndrome-associated extranodal marginal-zone B cell lymphoma: circulating lymphoma cells and invariant mutational pattern of nodal Ig heavy and light chain variable-region gene rearrangements Arthritis Rheum 2006, 54:127-137. 10.1002/art.21558 16385504
99. Tzioufas AG Boumba DS Skopouli FN Moutsopoulos HM Mixed monoclonal cryoglobulinemia and monoclonal rheumatoid factor cross-reactive idiotypes as predictive factors for the development of lymphoma in primary Sjögren's syndrome Arthritis Rheum 1996, 39:767-772. 10.1002/art.1780390508 8639173
100. Voulgarelis M Dafni UG Isenberg DA Moutsopoulos HM the members of the European Concerted Action on Sjögren's syndrome Malignant lymphoma in primary Sjögren's syndrome. A multicenter, retrospective, clinical study by the European Concerted Action on Sjögren's syndrome Arthritis Rheum 1999, 42:1765-1772. 10.1002/ 1529-0131(199908)42:8<1765::AID-ANR28>3.0.CO;2-V 10446879
101. Theander E Manthorpe R Jacobsson LTH Mortality and causes of death in primary Sjögren's syndrome. A prospective cohort study Arthritis Rheum 2004, 50:1262-1269. 10.1002/art.20176 15077310
102. + memory B cell development J Exp Med 2006, 203:293-400. 10.1084/jem.20052033
103. Sutherland AP Mackay F Mackay CR Targeting BAFF: Immunomodulation for autoimmune diseases and lymphomas Pharmacol Ther 2006, 112:774-786. 10.1016/j.pharmthera.2006.06.002 16863659
104. Martin F Dixit VM Unraveling TACIt functions Nat Genet 2005, 37:793-794. 10.1038/ng0805-793 16049503
105. Szodoray P Jellestad S Alex P Zhou T Wilson PC Centola M Brun JG Jonsson R Programmed cell death of peripheral blood B cells determined by laser scanning cytometry in Sjögren's syndrome with special emphasis on BAFF J Clin Immunol 2004, 24:600-611. 10.1007/s10875-004-6240-7 15622444
106. Mariette X Roux S Zhang J Bengoufa D Lavie F Zhou T Kimberly R The level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjögren's syndrome Ann Rheum Dis 2003, 62:168-171. 1754442 12525388 10.1136/ard.62.2.168
107. Batten M Fletcher C Ng LG Groom J Wheway J Laabi Y Xin X Schneider P Tschopp J Mackay GR TNF deficiency fails to protect BAFF transgenic mice against autoimmunity and reveals a predisposition to B cell lymphoma J Immunol 2004, 172:812-822. 14707051
108. Manoussakis MN Tzioufas AG Pange PJE Moutsopoulos HM Serologic profiles in subgroups of patients with Sjögren's syndrome Scand J Rheumatol 1986, 61:89-92.
109. Radbruch A Muehlinghaus G Luger EO Inamine A Smith KG Dörner T Hiepe F Competence and competition: The challenge of becoming a long-lived plasma cell Nat Rev Immunol 2006, 6:741-750. 10.1038/nri1886 16977339
110. Wahren M Skarstein K Blange I Petterson I Jonsson R MRL/lpr mice produce anti-Ro 52,000 MW antibodies: Detection, analysis of specificity and site of production Immunology 1994, 83:9-15. 1415008 7821973
111. 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. 10.1002/ 1529-0131(200103)44:3<626::AID-ANR111>3.0.CO;2-T 11263777
112. Kaschner S Hansen A Jacobi A Reiter K Monson NL Odendahl M Burmester GR Lipsky PE Dörner T Immunoglobulin Vλ light chain gene usage in patients with Sjögren's syndrome Arthritis Rheum 2001, 44:2620-2632. 10.1002/ 1529-0131(200111)44:11<2620::AID-ART442>3.0.CO;2-M 11710718
113. Du M Diss TC Xu C Peng H Isaacson PG Pan L Ongoing mutation in MALT lymphoma immunoglobulin gene suggests that antigen stimulation plays a role in clonal expansion Leukemia 1996, 10:1190-1197. 8684001
114. 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. 10.1016/S0092-8674(00)00078-7 11007474
115. Bertorello R Cordone MP Contini P Rossi P Indiveri F Puppo F Cordone G Increased levels of interleukin-10 in saliva of Sjögren's syndrome patients. Correlation with disease activity Clin Exp Med 2004, 4:148-151. 10.1007/s10238-004-0049-9 15599664
116. Steinfeld SD Tant L Burmester GR Teoh NK Wegener WA Goldenberg DM Pradier O Epratuzumab (humanised anti-CD22 antibody) in primary Sjögren's syndrome: An open-label phase I/II study Arthritis Res Ther 2006, 8:R129. 1779377 16859536 10.1186/ar2018
117. Pijpe J van Imhoff GW Spijkervet FK Roodenburg JL Wolbink GJ Mansour K Vissink A Kallenberg CG Bootsma H Rituximab treatment in patients with Sjögren's syndrome: An open-label phase II study Arthritis Rheum 2005, 52:2740-2750. 10.1002/art.21260 16142737