Elevated production of B Cell Chemokine CXCL13 is correlated with systemic lupus erythematosus disease activity

Journal of Clinical Immunology

Volumn 30, Issue 1, 2010, Pages 45-52

  Wong, C K ^a   Wong, Purple T Y ^a   Tam, L S ^a   Li, Edmund K ^a   Chen, D P ^a   Lam, Christopher W K ^a,b  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b MACAU UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Macao)

Author keywords

B cells; B cell activating factor of the TNF family; Chemokines; CXCL13; Follicular helper T lymphocytes; Systemic lupus erythematosus

Indexed keywords

AZATHIOPRINE; B CELL ACTIVATING FACTOR; CD19 ANTIGEN; CHEMOKINE RECEPTOR CXCR5; CXCL13 CHEMOKINE; HYDROXYCHLOROQUINE; INTERLEUKIN 21; INTERLEUKIN 21 RECEPTOR; PREDNISOLONE;

ADULT; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; MALE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADULT; ANTIGENS, CD; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; BIOLOGICAL MARKERS; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL13; DISEASE PROGRESSION; FEMALE; HUMANS; INTERLEUKINS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; RECEPTORS, CXCR5; RECEPTORS, INTERLEUKIN-21;

EID: 77249098290     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-009-9325-5     Document Type: Article

References (45)

1. LD Heinlen MT McClain J Merrill, et al. 2007 Clinical criteria for systemic lupus erythematosus precede diagnosis, and associated autoantibodies are present before clinical symptoms Arthritis Rheum 56 2344 2351 10.1002/art.22665 17599763 1:CAS:528:DC%2BD2sXovFSgtbc%3D (Pubitemid 47173582)
2. BL Kotzin 1996 Systemic lupus erythematosus Cell 85 303 306 10.1016/S0092-8674(00)81108-3 8616885 1:CAS:528:DyaK28XivVyrs78%3D (Pubitemid 26160701)
3. JF Viallard JL Pellegrin V Ranchin, et al. 1999 Th1 (IL-2, interferon-gamma (IFN-gamma)) and Th2 (IL-10, IL-4) cytokine production by peripheral blood mononuclear cells (PBMC) from patients with systemic lupus erythematosus (SLE) Clin Exp Immunol 115 189 195 10.1046/j.1365-2249.1999.00766. x 9933441 1:CAS:528:DyaK1MXos1Kgtw%3D%3D (Pubitemid 29030384)
4. KM Ansel RBS Harris JG Cyster 2002 CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity Immunity 16 67 76 10.1016/S1074-7613(01)00257-6 11825566 1:CAS:528:DC%2BD38Xht1SmtLw%3D (Pubitemid 34143217)
5. JL Vissers FC Hartgers E Lindhout CG Figdor GJ Adema 2001 BLC (CXCL13) is expressed by different dendritic cell subsets in vitro and in vivo Eur J Immunol 31 1544 1549 10.1002/1521-4141(200105)31:5<1544::AID-IMMU1544>3.0. CO;2-I 11465112 1:CAS:528:DC%2BD3MXktVWisrw%3D (Pubitemid 32454703)
6. DF Legler M Loetscher RS Roos I Clark-Lewis M Baggiolini B Moser 1998 B cell-attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5 J Exp Med 187 655 660 10.1084/jem.187.4.655 9463416 1:CAS:528:DyaK1cXhtFCqurc%3D (Pubitemid 28093368)
7. KM Ansel VN Ngo PL Hyman, et al. 2000 A chemokine-driven positive feedback loop organizes lymphoid follicles Nature 406 309 314 10.1038/35018581 10917533 1:CAS:528:DC%2BD3cXlsFKgsLg%3D (Pubitemid 30604409)
8. P Schaerli K Willimann AB Lang M Lipp P Loetscher B Moser 2000 CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function J Exp Med 192 1553 1562 10.1084/jem.192.11.1553 11104798 1:CAS:528:DC%2BD3cXosF2ntr0%3D
9. DL Breitfeld L Ohl EK Kremmer, et al. 2000 Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production J Exp Med 192 1545 1551 10.1084/jem.192.11.1545 11104797 1:CAS:528:DC%2BD3cXosF2ntrw%3D
10. A Vogelzang HM McGuire D Yu J Sprent CR Mackay C King 2008 A fundamental role for interleukin-21 in the generation of T follicular helper cells Immunity 29 127 137 10.1016/j.immuni.2008.06.001 18602282 1:CAS:528:DC%2BD1cXptF2mtb8%3D
11. N Fazilleau L Mark LJ McHeyzer-Williams MG McHeyzer-Williams 2009 Follicular helper T cells: lineage and location Immunity 30 324 335 10.1016/j.immuni.2009.03.003 19303387 1:CAS:528:DC%2BD1MXltFSmtrY%3D
12. C King SG Tangye CR Mackay 2008 T follicular helper (TFH) cells in normal and dysregulated immune responses Annu Rev Immunol 26 741 766 10.1146/annurev.immunol.26.021607.090344 18173374 1:CAS:528:DC%2BD1cXltlWkt74%3D (Pubitemid 351600391)
13. CG Vinuesa SG Tangye B Moser CR Mackay 2005 Follicular B helper T cells in antibody responses and autoimmunity Nat Rev Immunol 5 853 865 10.1038/nri1714 16261173 1:CAS:528:DC%2BD2MXhtFKls7jK (Pubitemid 41581667)
14. R Spolski WJ Leonard 2007 Interleukin-21: basic biology and implications for cancer and autoimmunity Annu Rev Immunol 26 57 79 10.1146/annurev.immunol. 26.021607.090316 1:CAS:528:DC%2BD1cXltlWksLc%3D
15. RI Nurieva Y Chung D Hwang, et al. 2008 Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages Immunity 29 138 149 10.1016/j.immuni.2008.05.009 18599325 1:CAS:528:DC%2BD1cXptF2mtbw%3D
16. AH Sawalha KM Kaufman JA Kelly, et al. 2008 Genetic association of interleukin-21 polymorphisms with systemic lupus erythematosus Ann Rheum Dis 67 458 461 10.1136/ard.2007.075424 17720724 1:CAS:528:DC%2BD1cXltlSlu7Y%3D
17. K Hayakawa RR Hardy 2000 Development and function of B-1 cells Curr Opin Immunol 12 346 353 10.1016/S0952-7915(00)00098-4 10858035 1:CAS:528: DC%2BD3cXjsFeqtr8%3D (Pubitemid 30240547)
18. T Sato S Ishikawa K Akadegawa, et al. 2004 Aberrant B1 cell migration into the thymus results in activation of CD4 T cells through its potent antigen-presenting activity in the development of murine lupus Eur J Immunol 34 3346 3358 10.1002/eji.200425373 15495164 1:CAS:528:DC%2BD2cXhtFajtrzO (Pubitemid 40012154)
19. M Dauphinee Z Tovar N Talal 1988 B cells expressing CD5 are increased in Sjogren's syndrome Arthritis Rheum 31 642 647 10.1002/art.1780310509 3259883 1:STN:280:DyaL1c3ktVKisw%3D%3D
20. C Plater-Zyberk RN Maini K Lam TD Kennedy G Janossy 1985 A rheumatoid arthritis B cell subset expresses a phenotype similar to that in chronic lymphocytic leukemia Arthritis Rheum 28 971 976 10.1002/art.1780280903 3899124 1:STN:280:DyaL2MzgslWgug%3D%3D (Pubitemid 15020087)
21. T Ito S Ishikawa T Sato, et al. 2004 Defective B1 cell homing to the peritoneal cavity and preferential recruitment of B1 cells in the target organs in a murine model for systemic lupus erythematosus J Immunol 172 3628 3634 15004165 1:CAS:528:DC%2BD2cXhvVKju7s%3D
22. S Ishikawa T Sato M Abe, et al. 2001 Aberrant high expression of B lymphocyte chemokine (BLC/CXCL13) by C11b+CD11c+dendritic cells in murine lupus and preferential chemotaxis of B1 cells towards BLC J Exp Med 193 1393 1402 10.1084/jem.193.12.1393 11413194 1:CAS:528:DC%2BD3MXksFCnurw%3D (Pubitemid 32565968)
23. S Ishikawa K Matsushima 2007 Aberrant B1 cell trafficking in a murine model for lupus Front Biosci 12 1790 1803 10.2741/2188 17127421 1:CAS:528:DC%2BD28Xht1WgsbvP (Pubitemid 46846807)
24. M Batten J Groom TG Cachero, et al. 2000 BAFF mediates survival of peripheral immature B lymphocytes J Exp Med 192 1453 1466 10.1084/jem.192.10. 1453 11085747 1:CAS:528:DC%2BD3cXotlaisrk%3D (Pubitemid 30953883)
25. G Badr G Borhis EA Lefevre, et al. 2008 BAFF enhances chemotaxis of primary human B cells: a particular synergy between BAFF and CXCL13 on memory B cells Blood 111 2744 2754 10.1182/blood-2007-03-081232 18172003 1:CAS:528:DC%2BD1cXivFaktbs%3D
26. JR Groom CA Fletcher SN Walters, et al. 2007 BAFF and MyD88 signals promote a lupuslike disease independent of T cells J Exp Med 204 1959 1971 10.1084/jem.20062567 17664289 1:CAS:528:DC%2BD2sXptVyjsbo%3D (Pubitemid 47236330)
27. EM Tan AS Cohen JF Fries, et al. 1982 The 1982 revised criteria for the classification of systemic lupus erythematosus Arthritis Rheum 25 1271 1277 10.1002/art.1780251101 7138600 1:STN:280:DyaL3s%2FkvVCmtA%3D%3D (Pubitemid 13221242)
28. C Bombardier DD Gladman MB Urowitz D Caron CH Chang 1992 The Committee on Prognosis studies in SLE: Derivation of the SLEDAI: a disease activity index for lupus patients Arthritis Rheum 35 630 640 10.1002/art.1780350606 1599520 1:STN:280:DyaK383oslWrtg%3D%3D
29. C Mohan S Adams V Stanik SK Datta 1993 Nucleosome: a major immunogen for pathogenic autoantibody-inducing T cells of lupus J Exp Med 177 1367 1381 10.1084/jem.177.5.1367 8478612 1:CAS:528:DyaK3sXitFWhsL4%3D
30. Schiffer L, Kümpers P, Davalos-Misslitz AM et al. B-cell-attracting chemokine CXCL13 as a marker of disease activity and renal involvement in systemic lupus erythematosus (SLE). Nephrol Dial Transplant. 2009 doi: 10.1093/ndt/gfp343
31. I Rioja FJ Hughes CH Sharp, et al. 2008 Potential novel biomarkers of disease activity in rheumatoid arthritis patients: CXCL13, CCL23, transforming growth factor alpha, tumor necrosis factor receptor superfamily member 9, and macrophage colony-stimulating factor Arthritis Rheum 58 2257 2267 10.1002/art.23667 18668547 1:CAS:528:DC%2BD1cXhtVCjtbbJ
32. PC Fulkerson N Zimmermann LM Hassman FD Finkelman ME Rothenberg 2004 Pulmonary chemokine expression is coordinately regulated by STAT1, STAT6, and IFN-gamma J Immunol 173 7565 7574 15585884 1:CAS:528:DC%2BD2cXhtVCqurvJ
33. S Morimoto S Nakano T Watanabe, et al. 2007 Expression of B-cell activating factor of the tumour necrosis factor family (BAFF) in T cells in active systemic lupus erythematosus: the role of BAFF in T cell-dependent B cell pathogenic autoantibody production Rheumatology 46 1083 1086 10.1093/rheumatology/kem097 17500077 1:CAS:528:DC%2BD2sXosVSjtrY%3D (Pubitemid 47050608)
34. F Mackay P Schneider P Rennert J Browning 2003 BAFF AND APRIL: a tutorial on B cell survival Annu Rev Immunol 21 231 264 10.1146/annurev.immunol.21. 120601.141152 12427767 1:CAS:528:DC%2BD3sXjtF2isr0%3D (Pubitemid 37174532)
35. JA Bubier TJ Sproule O Foreman, et al. 2009 A critical role for IL-21 receptor signaling in the pathogenesis of systemic lupus erythematosus in BXSB-Yaa mice Proc Natl Acad Sci USA 106 1518 1523 10.1073/pnas.0807309106 19164519
36. MA Linterman RJ Rigby RK Wong, et al. 2009 Follicular helper T cells are required for systemic autoimmunity J Exp Med 206 561 576 10.1084/jem.20081886 19221396 1:CAS:528:DC%2BD1MXjsVaisbw%3D
37. L Adalid-Peralta A Mathian T Tran L Delbos I Durand-Gasselin D Berrebi M Peuchmaur J Couderc D Emilie S Koutouzov 2008 Leukocytes and the kidney contribute to interstitial inflammation in lupus nephritis Kidney Int 73 172 180 10.1038/sj.ki.5002625 17928821 1:CAS:528:DC%2BD2sXhsVyltL7I
38. LV Bagaeva P Rao JM Powers BM Segal 2006 CXC chemokine ligand 13 plays a role in experimental autoimmune encephalomyelitis J Immunol 176 7676 7685 16751415 1:CAS:528:DC%2BD28Xlt1CksLs%3D
39. K Shi K Hayashida M Kaneko, et al. 2001 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 166 650 655 11123349 1:CAS:528:DC%2BD3MXis1emtQ%3D%3D
40. R Magliozzi S Columba-Cabezas B Serafini F Aloisi 2004 Intracerebral expression of CXCL13 and BAFF is accompanied by formation of lymphoid follicle-like structures in the meninges of mice with relapsing experimental autoimmune encephalomyelitis J Neuroimmunol 148 11 23 10.1016/j.jneuroim.2003. 10.056 14975582 1:CAS:528:DC%2BD2cXht1yksL8%3D (Pubitemid 38229554)
41. HJ Ree ME Kadin M Kikuchi YH Ko J Suzumiya JH Go 1999 Bcl-6 expression in reactive follicular hyperplasia, follicular lymphoma, and angioimmunoblastic T-cell lymphoma with hyperplastic germinal centers: heterogeneity of intrafollicular T-cells and their altered distribution in the pathogenesis of angioimmunoblastic T-cell lymphoma Hum Pathol 30 403 411 10.1016/S0046-8177(99) 90115-6 10208461 1:CAS:528:DyaK1MXivVSruro%3D
42. R Sabahi JH Anolik 2006 B-cell-targeted therapy for systemic lupus erythematosus Drugs 66 1933 1948 10.2165/00003495-200666150-00004 17100405 (Pubitemid 44771932)
43. J Sun Z Li J Feng Y Li B Shen 2008 BAFF-targeting therapy, a promising strategy for treating autoimmune diseases Eur J Pharmacol 597 1 5 10.1016/j.ejphar.2008.08.027 18793632 1:CAS:528:DC%2BD1cXht1KmtbrM
44. JA Bubier SM Bennett TJ Sproule, et al. 2007 Treatment of BXSB-Yaa mice with IL-21R-Fc fusion protein minimally attenuates systemic lupus erythematosus Ann N Y Acad Sci 1110 590 601 10.1196/annals.1423.063 17911475 1:CAS:528:DC%2BD2sXht1GitLzI (Pubitemid 350043049)
45. B Zheng Z Ozen X Zhang, et al. 2005 CXCL13 neutralization reduces the severity of collagen-induced arthritis Arthritis Rheum 52 620 626 10.1002/art.20768 15692971 1:CAS:528:DC%2BD2MXit1Gjtbs%3D (Pubitemid 40216328)