Multiple sclerosis: BAFF and CXCL13 in cerebrospinal fluid

Multiple Sclerosis Journal

Volumn 17, Issue 7, 2011, Pages 819-829

  Ragheb, Samia ^a   Li, Yanfeng ^a   Simon, Kirk ^a   Vanhaerents, Stephen ^a   Galimberti, Daniela ^b   De Riz, Milena ^b   Fenoglio, Chiara ^b   Scarpini, Elio ^b   Lisak, Robert ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

BAFF; cerebrospinal fluid; CXCL13; IgG index; multiple sclerosis

Indexed keywords

B CELL ACTIVATING FACTOR; CHEMOKINE; CXCL13 CHEMOKINE; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 6;

ADULT; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL SURVIVAL; CEREBROSPINAL FLUID; CYTOKINE PRODUCTION; DISEASE COURSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HOMEOSTASIS; HUMAN; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NEUROLOGIC DISEASE; PATHOPHYSIOLOGY; RELAPSE; REMISSION;

EID: 79959494654     PISSN: 13524585     EISSN: 14770970     Source Type: Journal    
DOI: 10.1177/1352458511398887     Document Type: Article

References (56)

1. Wingerchuk DM, Lucchinetti CF, Noseworthy JH. Multiple sclerosis: current pathophysiological concepts. Lab Invest. 2001 ; 81: 263-281 (Pubitemid 32245059)
2. Frohman EM, Racke MK, Raine CS. Multiple sclerosis - the plaque and its pathogenesis. N Engl J Med. 2006 ; 354: 942-955
3. McQualter JL, Bernard CCA. Multiple sclerosis: a battle between destruction and repair. J Neurochem. 2007 ; 100: 295-306 (Pubitemid 46010991)
4. Axtell RC, Steinman L. Gaining entry to an uninflamed brain. Nat Immunol. 2009 ; 10: 453-455
5. Cross AH, Trotter JL, Lyons J-A. B cells and antibodies in CNS demyelinating disease. J Neuroimmunol. 2001 ; 112: 1-14
6. McLaughlin KA, Wucherpfennig KW. B cells and autoantibodies in the pathogenesis of multiple sclerosis and related inflammatory demyelinating diseases. Adv Immunol. 2008 ; 98: 121-149
7. Prineas JW. Multiple sclerosis: presence of lymphatic capillaries and lymphoid tissue in the brain and spinal cord. Science. 1979 ; 203: 1123-1125 (Pubitemid 9148091)
8. Serafini B, Rosicarelli B, Magliozzi R, Stigliano E, Aloisi F. Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol. 2004 ; 14: 164-174 (Pubitemid 38656388)
9. Magliozzi R, Howell O, Vora A, Serafini B, Nicholas R, Puopolo M, et al. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain. 2007 ; 130: 1089-1104 (Pubitemid 47355604)
10. Esiri MM. Immunoglobulin-containing cells in multiple sclerosis plaques. Lancet. 1977 ; 2: 478-478
11. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol. 2000 ; 47: 707-717 (Pubitemid 30390191)
12. Holmoy T. The discovery of oligoclonal bands: a 50-year anniversary. Eur Neurol. 2009 ; 62: 311-315
13. 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: 2782-2789 (Pubitemid 30115513)
14. Owens GP, Ritchie AM, Burgoon MP, Williamson RA, Corboy JR, Gilden DH. Single-cell repertoire analysis demonstrates that clonal expansion is a prominent feature of the B cell response in multiple sclerosis cerebrospinal fluid. J Immunol. 2003 ; 171: 2725-2733 (Pubitemid 37025586)
15. Owens GP, Bennett JL, Lassmann H, O'Connor KC, Ritchie AM, Shearer A, et al. Antibodies produced by clonally expanded plasma cells in multiple sclerosis cerebrospinal fluid. Ann Neurol. 2009 ; 65: 639-649
16. Compston DA, Morgan BP, Campell AK, Wilkins P, Cole G, Thomas ND, et al. Immunocytochemical localization of the terminal complement complex in multiple sclerosis. Neuropathol Appl Neurobiol. 1989 ; 15: 307-316 (Pubitemid 19208151)
17. Piddlesden SJ, Lassmann H, Zimprich F, Morgan BP, Linington C. The demyelinating potential of antibodies to myelin oligodendrocyte glycoprotein is related to their ability to fix complement. Am J Pathol. 1993 ; 143: 555-564 (Pubitemid 24058211)
18. Genain CP, Cannella B, Hauser SL, Raine CS. Identification of autoantibodies associated with myelin damage in multiple sclerosis. Nat Med. 1999 ; 5: 170-175 (Pubitemid 29068523)
19. Vyshkina T, Kalman B. Autoantibodies and neurodegeneration in multiple sclerosis. Lab Invest. 2008 ; 88: 796-807
20. Yanaba K, Bouaziz J-D, Matsushita T, Magro C, Clair EW, Tedder TF. B-lymphocyte contributions to human autoimmune disease. Immunol Rev. 2008 ; 223: 284-299 (Pubitemid 351986191)
21. Bar-Or A, Calabresi PA, Arnold D, Markowitz C, Shafer S, Kasper LH, et al. Rituximab in relapsing-remitting multiple sclerosis: a 72-week, open-label, phase I trial. Ann Neurol. 2008 ; 63: 395-400 (Pubitemid 351499869)
22. Hauser SL, Waubant E, Arnold DL, Vollmer T, Antel J, Fox RJ, et al. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N Engl J Med. 2008 ; 358: 676-688 (Pubitemid 351240747)
23. Moore PA, Belvedere O, Orr A, Pieri K, LaFleur DW, Feng P, et al. Blys: Member of the tumor necrosis factor family and B lymphocyte stimulator. Science. 1999 ; 285: 260-263 (Pubitemid 29330000)
24. Schneider P, MacKay F, Steiner V, Hofmann K, Bodmer J-L, Holler N, et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med. 1999 ; 189: 1747-1756 (Pubitemid 29272691)
25. Nardelli B, Belvedere O, Roschke V, Moore PA, Olsen HS, Migone TS, et al. Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood. 2001 ; 97: 198-204 (Pubitemid 32061261)
26. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, Schneider P, et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med. 1999 ; 190: 1697-1710 (Pubitemid 30002351)
27. Khare SD, Sarosi I, Xia X-Z, McCabe S, Miner K, Solovyev I, et al. Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc Natl Acad Sci U S A. 2000 ; 97: 3370-3375 (Pubitemid 30183309)
28. Gross JA, Dillon SR, Mudri S, Johnston J, Littau A, Roque R, et al. TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease: impaired B cell maturation in mice lacking Blys. Immunity. 2001 ; 15: 289-302 (Pubitemid 32816877)
29. Schiemann B, Gommerman JL, Vora K, Cachero TG, Shulga-Morskaya S, Dobles M, et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science. 2001 ; 293: 2111-2114 (Pubitemid 32848063)
30. Kalled SL, Ambrose C, Hsu YM. The biochemistry and biology of BAFF, APRIL and their receptors. Curr Dir Autoimmun. 2005 ; 8: 206-242
31. von Bulow GU, Bram RJ. NF-AT activation induced by a CAML-interacting member of the tumor necrosis factor receptor superfamily. Science. 1997 ; 278: 138-141 (Pubitemid 27446295)
32. Ng LG, Sutherland APR, Newton R, Qian F, Cachero TG, Scott ML, et al. B cell-activating factor belonging to the TNF family (BAFF)-R is the principal BAFF receptor facilitating BAFF costimulation of circulating T and B cells. J Immunol. 2004 ; 173: 807-817 (Pubitemid 38924255)
33. Magliozzi R, Columba-Cabezas S, Serafini B, Aloisi F. 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. 2004 ; 148: 11-23 (Pubitemid 38229554)
34. Huntington ND, Tomioka R, Clavarino C, Chow AM, Linares D, Mana P, et al. A BAFF antagonist suppresses experimental autoimmune encephalomyelitis by targeting cell-mediated and humoral immune responses. Int Immunol. 2006 ; 18: 1473-1485 (Pubitemid 44446825)
35. Xue X, Feng G, Li M, Qin X, Wu S, Zhang C, et al. Amelioration of experimental autoimmune encephalomyelitis by BLys autovaccine. Vaccine. 2008 ; 26: 2873-2881
36. Ragheb S, Lisak R, Lewis R, Van Stavern G, Gonzales F, Simon K. A potential role for B-cell activating factor in the pathogenesis of autoimmune myasthenia gravis. Arch Neurol. 2008 ; 65: 1358-1362
37. Krumbholz M, Theil D, Derfuss T, Rosenwald A, Schrader F, Monoranu C-M, et al. BAFF is produced by astrocytes and up-regulated in multiple sclerosis lesions and primary central nervous system lymphoma. J Exp Med. 2005 ; 201: 195-200 (Pubitemid 40189428)
38. McDonald WI, Compston A, Edan G, Goodkin D, Hartung H-P, Lublin FD, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol. 2001 ; 50: 121-127
39. Polman CH, Reingold SC, Edan G, Filippi M, Hartung H-P, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann Neurol. 2005 ; 58: 840-846 (Pubitemid 41746873)
40. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an Expanded Disability Status Scale (EDSS). Neurology. 1983 ; 33: 1444-1452 (Pubitemid 14237132)
41. Gunn MD, Ngo VN, Ansel M, Ekland EH, Cyster JG, Williams LT. A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature. 1998 ; 391: 799-803 (Pubitemid 28099679)
42. Legler DF, Loetscher M, Roos RS, Clark-Lewis I, Baggiolini M, Moser B. B cell-attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5. J Exp Med. 1998 ; 187: 655-660 (Pubitemid 28093368)
43. Krumbholz M, Theil D, Cepok S, Hemmer B, Kivisakk P, Ransohoff RM, et al. Chemokines in multiple sclerosis: CXCL12 and CXCL13 up-regulation is differentially linked to CNS immune cell recruitment. Brain. 2006 ; 129: 200-211 (Pubitemid 43063771)
44. Sellebjerg F, Bornsen L, Khademi M, Krakauer M, Olsson T, Frederiksen JL, et al. Increased cerebrospinal fluid concentrations of the chemokine CXCL13 in active MS. Neurology. 2009 ; 73: 2003-2010
45. Piccio L, Naismith RT, Trinkaus K, Klein RS, Parks BJ, Lyons JA, et al. Changes in B- and T-lymphocyte and chemokine levels with rituximab treatment in multiple sclerosis. Arch Neurol. 2010 ; 67: 707-714
46. Festa ED, Hankiewicz K, Kim S, Skurnick J, Wolansky LJ, Cook SD, et al. Serum levels of CXCL13 are elevated in active multiple sclerosis. Mult Scler. 2009 ; 15: 1271-1279
47. Piazza F, DiFrancesco JC, Fusco ML, Corti D, Pirovano L, Frigeni B, et al. Cerebrospinal fluid levels of BAFF and APRIL in untreated multiple sclerosis. J Neuroimmunol. 2010 ; 220: 104-107
48. Okada K, Matsushita T, Kira J-I, Tsuji S. B-cell activating factor of the TNF family is upregulated in neuromyelitis optica. Neurology. 2010 ; 74: 177-178
49. Serafini B, Severa M, Columba-Cabezas S, Rosicarelli B, Veroni C, Chiappetta G, et al. Epstein-Barr virus latent infection and BAFF expression in B cells in the multiple sclerosis brain: implications for viral persistence and intrathecal B-cell activation. J Neuropathol Exp Neurol. 2010 ; 69: 677-693
50. Zhang L, Zheng S, Wu H, Wu Y, Liu S, Fan M, et al. Identification of BLyS (B lymphocyte stimulator), a non-myelin-associated protein, as a functional ligand for Nogo-66 receptor. J Neurosci. 2009 ; 29: 6348-6352
51. Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol. 2006 ; 6: 205-217 (Pubitemid 43290990)
52. Badr G, Borhis G, Lefevre EA, Chaoul N, Deshayes F, Dessirier V, et al. BAFF enhances chemotaxis of primary human B cells: a particular synergy between BAFF and CXCL13 on memory B cells. Blood. 2008 ; 111: 2744-2754
53. Gandhi KS, McKay FC, Schibeci SD, Arthur JW, Heard RN, Stewart GJ, et al. BAFF is a biological response marker to IFN-β treatment in multiple sclerosis. J Interferon Cytokine Res. 2008 ; 28: 529-539
54. Krumbholz M, Faber H, Steinmeyer F, Hoffmann L-A, Kumpfel T, Pellkofer H, et al. Interferon-β increases BAFF levels in multiple sclerosis: implications for B cell autoimmunity. Brain. 2008 ; 131: 1455-1463 (Pubitemid 351806460)
55. Warabi Y, Matsumoto Y, Hayashi H. Interferon beta-1b exacerbates multiple sclerosis with severe optic nerve and spinal cord demyelination. J Neurol Sci. 2007 ; 252: 57-61 (Pubitemid 44909191)
56. Kim KS, Park JY, Jou I, Park SM. Functional implication of BAFF synthesis and release in gangliosides-stimulated microglia. J Leuko Biol. 2009 ; 86: 349-359