The roles of B cells and their interactions with fibroblast-like synoviocytes in the pathogenesis of rheumatoid arthritis

International Archives of Allergy and Immunology

Volumn 155, Issue 3, 2011, Pages 205-211

  Wang, Qingtong ^a   Ma, Yukun ^a   Liu, Dandan ^a   Zhang, Lingling ^a   Wei, Wei ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

B cells; Cell contact; Fibroblast like synoviocyte; Rheumatoid arthritis

Indexed keywords

AUTOANTIBODY; CELL ADHESION MOLECULE; CHEMOKINE; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; CYTOKINE; RHEUMATOID FACTOR; TOLL LIKE RECEPTOR;

ANGIOGENESIS; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; ANTIGEN PRESENTING CELL; B LYMPHOCYTE; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; COMPLEMENT FIXATION; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; FIBROBLAST; HUMAN; IMMUNOPATHOGENESIS; INFLAMMATION; INFLAMMATORY CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SYNOVIOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; B-LYMPHOCYTES; CYTOKINES; HUMANS; LYMPHOCYTE ACTIVATION; MICE; SYNOVIAL MEMBRANE; T-LYMPHOCYTES;

EID: 79551525427     PISSN: 10182438     EISSN: 14230097     Source Type: Journal    
DOI: 10.1159/000321185     Document Type: Review

References (72)

1. Weyand CM, Goronzy JJ: Ectopic germinal center formation in rheumatoid synovitis. Ann NY Acad Sci 2003;987:140-149. (Pubitemid 36584016)
2. Pereira JP, Kelly LM, Cyster JG: Finding the right niche: B-cell migration in the early phases of T-dependent antibody responses. Int Immunol 2010;22:413-419.
3. Bartok B, Firestein GS: Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev 2010;233:233-255.
4. Weyand CM, Goronzy JJ, Takemura S, Kurtin PJ: Cell-cell interactions in synovitis: interactions between T cells and B cells in rheumatoid arthritis. Arthritis Res 2000;2:457-463. (Pubitemid 32224811)
5. McInnes IB, Leung BP, Liew FY: Cell-cell interactions in synovitis. Interactions between T lymphocytes and synovial cells. Arthritis Res 2000;2:374-378.
6. Nozaki Y, Nagare Y, Hino S, Yano T, Kishimoto K, Shimazu H, Ikoma S, Kinoshita K, Funauchi M: Therapeutic strategy and significance of serum rheumatoid factor in patients with rheumatoid arthritis during infliximab treatment. Nihon Rinsho Meneki Gakkai Kaishi 2010;33:135-141.
7. Song YW, Kang EH: Autoantibodies in rheumatoid arthritis: rheumatoid factors and anticitrullinated protein antibodies. QJM 2010;103:139-146.
8. López-Longo FJ, Sánchez-Ramón S, Carreño L: The value of anti-cyclic citrullinated peptide antibodies in rheumatoid arthritis: do they imply new risk factors? Drug News Perspect 2009;22:543-548.
9. Engelmann R, Brandt J, Eggert M, Karberg K, Krause A, Neeck G, Mueller-Hilke B: The anti-mutated citrullinated vimentin response classifies patients with rheumatoid arthritis into broad and narrow responders. J Rheumatol 2009;36:2670-2674.
10. Mewar D, Wilson AG: Autoantibodies in rheumatoid arthritis: a review. Biomed Pharmacother 2006;60:648-655.
11. Hoffmann MH, Tuncel J, Skriner K, Tohidast-Akrad M, Türk B, Pinol-Roma S, Serre G, Schett G, Smolen JS, Holmdahl R, Steiner G: The rheumatoid arthritis-associated autoantigen hnRNP-A2 (RA33) is a major stimulator of autoimmunity in rats with pristane-induced arthritis. J Immunol 2007;179:7568-7576.
12. Furuya T, Matsumoto I, Tsuchiya N, Hakoda M, Ichikawa N, Yago T, Higami K, Nanke Y, Sumida T, Kamatani N, Kotake S: Anti-glucose-6-phosphate isomerase, anti-cyclic citrullinated peptide antibodies and HLA-DRB1 genotypes in Japanese patients with early rheumatoid arthritis. Clin Exp Rheumatol 2008;26:918-921.
13. Auger I, Roudier C, Guis S, Balandraud N, Roudier J: HLA-DRB1*0404 is strongly associated with anticalpastatin antibodies in rheumatoid arthritis. Ann Rheum Dis 2007;66:1588-1593. (Pubitemid 350205445)
14. Steiner G: Auto-antibodies and autoreactive T-cells in rheumatoid arthritis: pathogenetic players and diagnostic tools. Clin Rev Allergy Immunol 2007;32:23-36.
15. Harris DP, Goodrich S, Gerth AJ, Peng SL, Lund FE: Regulation of IFN-γ production by B effector 1 cells: essential roles for T-bet and the IFN-γ receptor. J Immunol 2005;174:6781-6790. (Pubitemid 40705641)
16. Harris DP, Goodrich S, Mohrs K, Mohrs M, Lund FE: Cutting edge: the development of IL-4-producing B cells is controlled by IL-4, IL-4 receptor α, and Th2 cells. J Immunol 2005;175:7103-7107. (Pubitemid 41713402)
17. Kim HJ, Berek C: B cells in rheumatoid arthritis. Arthritis Res 2000;2:126-131.
18. Yanaba K, Bouaziz JD, Matsushita T, Magro CM, St Clair EW, Tedder TF: B-lymphocyte contributions to human autoimmune disease. Immunol Rev 2008;223:284-299. (Pubitemid 351986191)
19. Mizoguchi A, Bhan AK: A case for regulatory B cells. J Immunol 2006;176:705-710. (Pubitemid 43099663)
20. Nam EJ, Sa KH, You DW, Cho JH, Seo JS, Han SW, Park JY, Kim SI, Kyung HS, Kim IS, Kang YM: Up-regulated transforming growth factor beta-inducible gene h3 in rheumatoid arthritis mediates adhesion and migration of synoviocytes through alpha v beta3 integrin: regulation by cytokines. Arthritis Rheum 2006;54:2734-2744. (Pubitemid 44497752)
21. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM: B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002;3:944-950. (Pubitemid 35154008)
22. Amu S, Gjertsson I, Brisslert M: Functional characterization of murine CD25 expressing B cells. Scand J Immunol 2010;71:275-282.
23. Chan O, Shlomchik MJ: A new role for B cells in systemic autoimmunity: B cells promote spontaneous T cell activation in MRL-lpr/lpr mice. J Immunol 1998;160:51.
24. Lanzavecchia A: Antigen-specific interaction between T and B cells. Nature 1985;314:537-539.
25. Takemura S, Klimiuk PA, Braun A, Goronzy JJ, Weyand CM: T cell activation in rheumatoid synovium is B cell dependent. J Immunol 2001;167:4710.
26. Lee S, Ballow M: Monoclonal antibodies and fusion proteins and their complications: targeting B cells in autoimmune diseases. J Allergy Clin Immunol 2010;125:814-820.
27. O'Neill SK, Shlomchik MJ, Glant TT, Cao Y, Doodes PD, Finnegan A: Antigen-specific B cells are required as APCs and autoantibody-producing cells for induction of severe autoimmune arthritis. J Immunol 2005;174:3781-3788. (Pubitemid 40354091)
28. Linton PJ, Harbertson J, Bradley LM: A critical role for B cells in the development of memory CD4 cells. J Immunol 2000;165:5558-5565.
29. Shen H, Whitmire JK, Fan X, Shedlock DJ, Kaech SM, Ahmed R: A specific role for B cells in the generation of CD8 T cell memory by recombinant Listeria monocytogenes. J Immunol 2003;170:1443-1451. (Pubitemid 36139513)
30. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A: Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002;416:603-607. (Pubitemid 34406754)
31. Silverman GJ, Carson DA: Roles of B cells in rheumatoid arthritis. Arthritis Res Ther 2003;5(suppl 4):S1-S6. (Pubitemid 38239909)
32. Schaniel C, Pardali E, Sallusto F, Speletas M, Ruedl C, Shimizu T, Seidl T, Andersson J, Melchers F, Rolink AG, Sideras P: Activated murine B lymphocytes and dendritic cells produce a novel CC chemokine which acts selectively on activated T cells. J Exp Med 1998;188:451-463. (Pubitemid 28369135)
33. Schaniel C, Sallusto F, Ruedl C, Sideras P, Melchers F, Rolink AG: Three chemokines with potential functions in T lymphocytein-dependent and -dependent B lymphocyte stimulation. Eur J Immunol 1999;29:2934-2947. (Pubitemid 30099018)
34. Ghia P, Schaniel C, Rolink AG, Nadler LM, Cardoso AA: Human macrophage-derived chemokine (MDC) is strongly expressed following activation of both normal and malignant precursor and mature B cells. Curr Top Microbiol Immunol 1999;246:103-110. (Pubitemid 29225965)
35. Ghia P, Transidico P, Veiga JP, Schaniel C, Sallusto F, Matsushima K, Sallan SE, Rolink AG, Mantovani A, Nadler LM, Cardoso AA: Chemoattractants MDC and TARC are secreted by malignant B-cell precursors following CD40 ligation and support the migration of leukemia-specific T cells. Blood 2001;98:533-540.
36. Yu P, Wang Y, Chin RK, Martinez-Pomares L, Gordon S, Kosco-Vibois MH, Cyster J, Fu YX: B cells control the migration of a subset of dendritic cells into B cell follicles via CXC chemokine ligand 13 in a lymphotoxin-dependent fashion. J Immunol 2002;168:5117-5123. (Pubitemid 34495976)
37. Humby F, Bombardieri M, Manzo A, Kelly S, Blades MC, Kirkham B, Spencer J, Pitzalis C: Ectopic lymphoid structures support ongoing production of class-switched autoantibodies in rheumatoid synovium. PLoS Med 2009;6:e1.
38. Shrestha B, Hashiguchi T, Ito T, Miura N, Takenouchi K, Oyama Y, Kawahara K, Tancharoen S, Ki-I Y, Arimura N, Yoshinaga N, Noma S, Shrestha C, Nitanda T, Kitajima S, Arimura K, Sato M, Sakamoto T, Maruyama I: B cell-derived vascular endothelial growth factor A promotes lymphangiogenesis and high endothelial venule expansion in lymph nodes. J Immunol 2010;184:4819-4826.
39. Galligan CL, Siminovitch KA, Keystone EC, Bykerk V, Perez OD, Fish EN: Fibrocyte activation in rheumatoid arthritis. Rheumatology (Oxford) 2010;49:640-651.
40. Zhang Q, Wu J, Cao Q, Xiao L, Wang L, He D, Ouyang G, Lin J, Shen B, Shi Y, Zhang Y, Li D, Li N: A critical role of Cyr61 in interleukin-17-dependent proliferation of fibroblast-like synoviocytes in rheumatoid arthritis. Arthritis Rheum 2009;60:3602-3612.
41. Chaiamnuay S, Bridges SL Jr: The role of B cells and autoantibodies in rheumatoid arthritis. Pathophysiology 2005;12:203-216. (Pubitemid 41375643)
42. Kang YM, Kim SY, Kang JH, Han SW, Nam EJ, Kyung HS, Park JY, Kim IS: LIGHT up-regulated on B lymphocytes and monocytes in rheumatoid arthritis mediates cellular adhesion and metalloproteinase production by synoviocytes. Arthritis Rheum 2007;56:1106-1117.
43. Burger JA, Zvaifler NJ, Tsukada N, Firestein GS, Kipps TJ: Fibroblast-like synoviocytes support B-cell pseudoemperipolesis via a stromal cell-derived factor-1- and CD106 (VCAM-1)-dependent mechanism. J Clin Invest 2001;107:305-315. (Pubitemid 32157962)
44. Dechanet J, Merville P, Durand I, Banchereau J, Miossec P: The ability of synoviocytes to support terminal differentiation of activated B cells may explain plasma cell accumulation in rheumatoid synovium. J Clin Invest 1995;95:456-463.
45. Bradfield PF, Amft N, Vernon-Wilson E, Exley AE, Parsonage G, Rainger GE, Nash GB, Thomas AM, Simmons DL, Salmon M, Buckley CD: Rheumatoid fibroblast-like synoviocytes overexpress the chemokine stromal cell-derived factor 1 (CXCL12), which supports distinct patterns and rates of CD4+ and CD8+ T cell migration within synovial tissue. Arthritis Rheum 2003;48:2472-2482. (Pubitemid 37129424)
46. Minges Wols HA, Ippolito JA, Yu Z, Palmer JL, White FA, Le PT, Witte PL: The effects of microenvironment and internal programming on plasma cell survival. Int Immunol 2007;19:837-846. (Pubitemid 47241892)
47. Boyle DL, Shi Y, Gay S, Firestein GS: Regulation of CS1 fibronectin expression and function by IL-1 in endothelial cells. Cell Immunol 2000;200:1-7. (Pubitemid 30170074)
48. Carter RA, O'Donnell K, Sachthep S, Cicuttini F, Boyd AW, Wicks IP: Characterization of a human synovial cell antigen: VCAM-1 and inflammatory arthritis. Immunol Cell Biol 2001;79:419-428. (Pubitemid 34225136)
49. Morales-Ducret J, Wayner E, Elices MJ, Alvaro-Gracia JM, Zvaifler NJ, Firestein GS: Alpha 4/beta 1 integrin (VLA-4) ligands in arthritis: vascular cell adhesion molecule-1 expression in synovium and on fibroblast-like synoviocytes. J Immunol 1992;149:1424.
50. 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.
51. Takemura S, Braun A, Crowson C, Kurtin PJ, Cofield RH, O'Fallon WM, Goronzy JJ, Weyand CM: Lymphoid neogenesis in rheumatoid synovitis. J Immunol 2001;167:1072.
52. Ohata J, Zvaifler NJ, Nishio M, Boyle DL, Kalled SL, Carson DA, Kipps TJ: Fibroblast-like synoviocytes of mesenchymal origin express functional B cell-activating factor of the TNF family in response to proinflammatory cytokines. J Immunol 2005;174:864-870. (Pubitemid 40094281)
53. Boland JM, Folpe AL, Hornick JL, Grogg KL: Clusterin is expressed in normal synoviocytes and in tenosynovial giant cell tumors of localized and diffuse types: diagnostic and histogenetic implications. Am J Surg Pathol 2009;33:1225-1229.
54. Falgarone G, Chiocchia G: Chapter 8: clusterin - a multifacet protein at the crossroad of inflammation and autoimmunity. Adv Cancer Res 2009;104:139-170.
55. Devauchelle V, Essabbani A, De Pinieux G, Germain S, Tourneur L, Mistou S, Margottin-Goguet F, Anract P, Migaud H, Le Nen D, Lequerré T, Saraux A, Dougados M, Breban M, Fournier C, Chiocchia G: Characterization and functional consequences of underexpression of clusterin in rheumatoid arthritis. J Immunol 2006;177:6471-6479. (Pubitemid 44628866)
56. Take Y, Nakata K, Hashimoto J, Tsuboi H, Nishimoto N, Ochi T, Yoshikawa H: Specifically modified osteopontin in rheumatoid arthritis fibroblast-like synoviocytes supports interaction with B cells and enhances production of interleukin-6. Arthritis Rheum 2009;60:3591-3601.
57. Xu W, He B, Chiu A, Chadburn A, Shan M, Buldys M, Ding A, Knowles DM, Santini PA, Cerutti A: Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat Immunol 2007;8:294-303. (Pubitemid 46745379)
58. Reyes LI, León F, González P, Rozas MF, Labarca C, Segovia A, Neira O, Naves R: Dexamethasone inhibits BAFF expression in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Cytokine 2008;42:170-178.
59. Schneider P, MacKay F, Steiner V, Hofmann K, Bodmer JL, Holler N, Ambrose C, Lawton P, Bixler S, Acha-Orbea H, Valmori D, Romero P, Werner-Favre C, Zubler RH, Browning JL, Tschopp J: BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med 1999;189:1747-1756. (Pubitemid 29272691)
60. Mukhopadhyay A, Ni J, Zhai Y, Yu GL, Aggarwal BB: Identification and characterization of a novel cytokine, THANK, a TNF homologue that activates apoptosis, nuclear factor-kappaB, and c-Jun NH2-terminal kinase. J Biol Chem 1999;274:15978-15981.
61. Shu HB, Hu WH, Johnson H: TALL-1 is a novel member of the TNF family that is downregulated by mitogens. J Leukoc Biol 1999;65:680-683.
62. Moore PA, Belvedere O, Orr A, Pieri K, LaFleur DW, Feng P, Soppet D, Charters M, Gentz R, Parmelee D, Li Y, Galperina O, Giri J, Roschke V, Nardelli B, Carrell J, Sosnovtseva S, Greenfield W, Ruben SM, Olsen HS, Fikes J, Hilbert DM: BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science 1999;285:260-263. (Pubitemid 29330000)
63. Seyler TM, Park YW, Takemura S, Bram RJ, Kurtin PJ, Goronzy JJ, Weyand CM: BLyS and APRIL in rheumatoid arthritis. J Clin Invest 2005;115:3083-3092. (Pubitemid 41567573)
64. Hondowicz BD, Alexander ST, Quinn WJ 3rd, Pagán AJ, Metzgar MH, Cancro MP, Erikson J: The role of BLyS/BLyS receptors in anti-chromatin B cell regulation. Int Immunol 2007;19:465-475. (Pubitemid 46523394)
65. Messer L, Alsaleh G, Freyssinet JM, Zobairi F, Leray I, Gottenberg JE, Sibilia J, Toti-Orfanoudakis F, Wachsmann D: Microparticle-induced release of B-lymphocyte regulators by rheumatoid synoviocytes. Arthritis Res Ther 2009;11:R40.
66. Alsaleh G, Messer L, Semaan N, Boulanger N, Gottenberg JE, Sibilia J, Wachsmann D: BAFF synthesis by rheumatoid synoviocytes is positively controlled by alpha5beta1 integrin stimulation and is negatively regulated by tumor necrosis factor alpha and Toll-like receptor ligands. Arthritis Rheum 2007;56:3202-3214. (Pubitemid 47585415)
67. Taneda S, Segerer S, Hudkins KL, Cui Y, Wen M, Segerer M, Wener MH, Khairallah CG, Farr AG, Alpers CE: Cryoglobulinemic glomerulonephritis in thymic stromal lymphopoietin transgenic mice. Am J Pathol 2001;159:2355-2369. (Pubitemid 33104288)
68. Ozawa T, Koyama K, Ando T, Ohnuma Y, Hatsushika K, Ohba T, Sugiyama H, Hamada Y, Ogawa H, Okumura K, Nakao A: Thymic stromal lymphopoietin secretion of synovial fibroblasts is positively and negatively regulated by Toll-like receptors/nuclear factor-kappaB pathway and interferon-gamma/dexamethasone. Mod Rheumatol 2007;17:459-463.
69. Koyama K, Ozawa T, Hatsushika K, Ando T, Takano S, Wako M, Suenaga F, Ohnuma Y, Ohba T, Katoh R, Sugiyama H, Hamada Y, Ogawa H, Okumura K, Nakao A: A possible role for TSLP in inflammatory arthritis. Biochem Biophys Res Commun 2007;357:99-104. (Pubitemid 46574504)
70. Firestein GS: Evolving concepts of rheumatoid arthritis. Nature 2003;423:356-361.
71. De Vita S, Zaja F, Sacco S, De Candia A, Fanin R, Ferraccioli G: Efficacy of selective B cell blockade in the treatment of rheumatoid arthritis: evidence for a pathogenetic role of B cells. Arthritis Rheum 2002;46:2029-2033.
72. Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, Stevens RM, Shaw T: Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004;350:2572-2581. (Pubitemid 38758544)