Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology

Brain

Volumn 130, Issue 4, 2007, Pages 1089-1104

  Magliozzi, Roberta ^a,b   Howell, Owain ^b   Vora, Abhilash ^b   Serafini, Barbara ^a   Nicholas, Richard ^b   Puopolo, Maria ^a   Reynolds, Richard ^b,c   Aloisi, Francesca ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

B cells; Demyelination; Ectopic follicles; Multiple sclerosis; Neurodegeneration

Indexed keywords

ADULT; AGED; ARTICLE; AUTOPSY; B LYMPHOCYTE; BRAIN CORTEX; BRAIN TISSUE; CELL ACTIVATION; CELL DEATH; CELL LOSS; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; DEMYELINATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; HUMORAL IMMUNITY; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOGENESIS; MALE; MENINX; MICROGLIA; MORPHOMETRICS; MULTIPLE SCLEROSIS; NEURITE; NEUROPATHOLOGY; PRIORITY JOURNAL; ADOLESCENT; CHILD; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; INFLAMMATION; METHODOLOGY; MIDDLE AGED; NERVE CELL; ONSET AGE; PATHOLOGY;

ADOLESCENT; ADULT; AGE OF ONSET; AGED; AGED, 80 AND OVER; B-LYMPHOCYTES; CEREBRAL CORTEX; CHILD; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MENINGES; MICROGLIA; MIDDLE AGED; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; NEURITES; NEURONS;

EID: 34249700046     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awm038     Document Type: Article

References (41)

1. Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 2006; 6: 205-17.
2. Archelos JJ, Storch MK, Hartung HP. The role of B cells and autoantibodies in multiple sclerosis. Ann Neurol 2000; 47: 694-706.
3. Baranzini SE, Jeong MC, Butunoi C, Murray RS, Bernard CC, Oksenberg JR. B cell repertoire diversity and clonal expansion in multiple sclerosis brain lesions. J Immunol 1999; 163: 5133-44.
4. Bö L, Vedeler CA, Nyland H, Trapp BD, Mörk SJ. Intracortical multiple sclerosis lesions are not associated with increased lymphocyte infiltration. Mult Scler 2003a; 4: 323-31.
5. Bö L, Vedeler CA, Nyland HI, Trapp BD, Mörk SJ. Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 2003b; 62: 723-32.
6. Bö L, Geurts J, Van der Valk P, Polman C, Barkhof F. Lack of correlation between cortical demyelination and white matter pathologic changes in multiple sclerosis. Arch Neurol 2007; 64: 74-80.
7. Brink BP, Veerhuis R, Breij EC, van der Valk P, Dijkstra D, Bö L. The pathology of multiple sclerosis is location-dependent: no significant complement activation is detected in purely cortical lesions. J Neuropathol Exp Neurol 2005; 64: 147-55.
8. Brownell B, Hughes JT. The distribution of plaques in the cerebrum in multiple sclerosis. J Neurol Neurosurg Psychiatry 1962; 25: 315-20.
9. Cepok S, Zhou D, Srivastava R, Nessler S, Stei S, Bussow K, et al. Identification of Epstein-Barr virus proteins as putative targets of the immune response in multiple sclerosis. J Clin Invest 2005; 115: 1352-60.
10. 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: 2782-9.
11. Colombo M, Dono M, Gazzola P, Chiorazzi N, Mancardi G, Ferrarini M. Maintenance of B lymphocyte-related clones in the cerebrospinal fluid of multiple sclerosis patients. Eur J Immunol 2003; 33: 3433-8.
12. Columba-Cabezas S, Griguoli M, Rosicarelli B, Magliozzi R, Ria F, Serafini B, et al. Suppression of established experimental autoimmune encephalomyelitis and formation of meningeal lymphoid follicles by lymphotoxin β receptor-Ig fusion protein. J Neuroimmunol 2006; 179: 76-86.
13. Corcione A, Casazza S, Ferretti E, Giunti D, Zappia E, Pistorio A, et al. Recapitulation of B cell differentiation in the central nervous system of patients with multiple sclerosis. Proc Natl Acad Sci USA 2004; 101: 11064-9.
14. Filippi M, Rocca MA. MRI evidence for multiple sclerosis as a diffuse disease of the central nervous system. J Neurol 2005; 252 (Suppl 5): V/16-V/24.
15. Frohman EM, Racke MK, Raine CS. Multiple sclerosis: the plaque and its pathogenesis. New Engl J Med 2006; 354: 942-55.
16. Gilden DH. Infectious causes of multiple sclerosis. Lancet Neurol 2005; 4: 195-202.
17. Kidd D, Barkhof F, McConnell R, Algra PR, Allen IV, Revesz T. Cortical lesions in multiple sclerosis. Brain 1999; 122: 17-26.
18. Kornek B, Storch MK, Weissert R, Wallström E, Stefferl A, Olsson T, et al. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am J Pathol 2000; 157: 267-76.
19. Kutzelnigg A, Lucchinetti CF, Stadelmann C, Bruck W, Rauschka H, Bergmann M, et al. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 2006; 128: 2705-12.
20. 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: 707-17.
21. Lumsden CE. The neuropathology of multiple sclerosis. In: Vinken PJ, Bruyn GW, editors. Handbook of clinical neurology. Multiple sclerosis and other demyelinating diseases. Amsterdam: North Holland; 1970. p. 217-309.
22. Magalhaes R, Stiehl P, Morawietz L, Berek C, Krenn V. Morphological and molecular pathology of the B cell response in synovitis of rheumatoid arthritis. Virchows Arch 2002; 441: 415-27.
23. 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.
24. 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: 2725-33.
25. Owens GP, Bennett JL, Gilden DH, Burgoon MP. The B cell response in multiple sclerosis. Neurol Res 2006; 28: 236-44.
26. Park CS, Choi YS. How do follicular dendritic cells interact intimately with B cells in the germinal center? Immunology 2005; 114: 2-10.
27. Peterson JW, Bö L, Mörk S, Chang A, Trapp BD. Transected neuritis, apoptotic neurons and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001; 50: 389-400.
28. Prineas JW, Graham JS. Multiple sclerosis: capping of surface immunoglobulin G on macrophages engaged in myelin breakdown. Ann Neurol 1981; 10: 149-58.
29. Prineas JW, Wright RG. Macrophages, lymphocytes, and plasma cells in the perivascular compartment in chronic multiple sclerosis. Lab Invest 1978; 38: 409-21.
30. Qin Y, Duquette P, Zhang Y, Talbot P, Poole R, Antel J. Clonal expansion and somatic hypermutation of V(H) genes of B cells from cerebrospinal fluid in multiple sclerosis. J Clin Invest 1998; 102: 1045-50.
31. Qin Y, Duquette P, Zhang Y, Olek M, Da RR, Richardson J, et al. Intrathecal B-cell clonal expansion, an early sign of humoral immunity, in the cerebrospinal fluid of patients with clinically isolated syndrome suggestive of multiple sclerosis. Lab Invest 2003; 83: 1081-8.
32. Rand KH, Houck H, Denslow ND, Heilman KM. Epstein-Barr virus nuclear antigen-1 (EBNA-1) associated oligoclonal bands in patients with multiple sclerosis. J Neurol Sci 2000; 173: 32-9.
33. Rennels ML, Gregory TF, Blaumanis OR, Fujimoto K, Grady PA. Evidence for a 'paravascular' fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 1985; 326: 47-63.
34. Roxanis I, Micklem K, McConville J, Newsom-Davis J, Willcox N. Thymic myoid cells and germinal center formation in myasthenia gravis; possible roles in pathogenesis. J Neuroimmunol 2002; 125: 185-97.
35. 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 progresive multiple sclerosis. Brain Pathol 2004; 14: 164-74.
36. Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005; 23: 683-747.
37. Storch MK, Piddlesden S, Haltia M, Iivanainen M, Morgan P, Lassmann H. Multiple sclerosis: in situ evidence for antibody- and complement-mediated demyelination. Ann Neurol 1998; 43: 465-71.
38. Tedeschi G, Lavorgna L, Russo P, Prinster A, Dinacci D, Savettieri G, et al. Brain atrophy and lesion load in a large population of patients with multiple sclerosis. Neurology 2005; 65: 280-5.
39. Tourtellotte WW, Walsh MJ, Baumhefner RW, Staugaitis SM, Shapshak P. The current status of multiple sclerosis intra-blood-brain-barrier IgG synthesis. Ann N Y Acad Sci 1984; 436: 52-67.
40. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Bö L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998; 338: 278-85.
41. Uccelli A, Aloisi F, Pistoia V. Unveiling the enigma of the CNS as a B-cell fostering environment. Trends Immunol 2005; 26: 254-9.