Abundant extracellular myelin in the meninges of patients with multiple sclerosis

Neuropathology and Applied Neurobiology

Volumn 35, Issue 3, 2009, Pages 283-295

  Kooi, E J ^a,b   Van Horssen, J ^b   Witte, M E ^b   Amor, S ^b,c   Bo L ^d   Dijkstra, C D ^b   Van Der Valk, P ^b   Geurts, J J G ^b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

Extracellular; Meninges; Multiple sclerosis; Myelin

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; CELL MARKER; CYCLIC NUCLEOTIDE; FORMALDEHYDE; MYELIN; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PROTEOLIPID PROTEIN;

ADOLESCENT; ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN TISSUE; CHILD; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LEUKODYSTROPHY; MACROPHAGE; MALE; MENINGITIS; MENINX; MULTIPLE SCLEROSIS; NEUROLOGIC DISEASE; OLIGODENDROGLIA; PARENCHYMA; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; STROKE;

ADOLESCENT; ADRENOLEUKODYSTROPHY; ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BRAIN; CHILD; CHILD, PRESCHOOL; DENDRITIC CELLS; EXTRACELLULAR SPACE; FEMALE; HUMANS; MACROPHAGES; MALE; MENINGES; MENINGITIS; MIDDLE AGED; MULTIPLE SCLEROSIS; MYELIN PROTEINS; MYELIN SHEATH; STROKE;

EID: 65349144858     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2008.00986.x     Document Type: Article

References (56)

1. Steinman L. Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system. Cell 1996 85 : 299 302 (Pubitemid 26160700)
2. Lassmann H. Neuropathology in multiple sclerosis: new concepts. Mult Scler 1998 4 : 93 8 (Pubitemid 28410031)
3. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med 2000 343 : 938 52
4. 't Hart BA, van Kooyk Y. Yin-Yang regulation of autoimmunity by DCs. Trends Immunol 2004 25 : 353 9 (Pubitemid 38780951)
5. de Vos AF, van Meurs M, Brok HP, Boven LA, Hintzen RQ, van der Valk P, Ravid R, Rensing S, Boon L, 't Hart BA, Laman JD. Transfer of central nervous system autoantigens and presentation in secondary lymphoid organs. J Immunol 2002 169 : 5415 23 (Pubitemid 35291638)
6. Fabriek BO, Zwemmer JN, Teunissen CE, Dijkstra CD, Polman CH, Laman JD, Castelijns JA. In vivo detection of myelin proteins in cervical lymph nodes of MS patients using ultrasound-guided fine-needle aspiration cytology. J Neuroimmunol 2005 161 : 190 4 (Pubitemid 40340888)
7. Wolvers DA, Coenen-de Roo CJ, Mebius RE, van der Cammen MJ, Tirion F, Miltenburg AM, Kraal G. Intranasally induced immunological tolerance is determined by characteristics of the draining lymph nodes: studies with OVA and human cartilage gp-39. J Immunol 1999 162 : 1994 8 (Pubitemid 29288817)
8. Preston SD, Steart PV, Wilkinson A, Nicoll JA, Weller RO. Capillary and arterial cerebral amyloid angiopathy in Alzheimer's disease: defining the perivascular route for the elimination of amyloid beta from the human brain. Neuropathol Appl Neurobiol 2003 29 : 106 17 (Pubitemid 36408329)
9. Szentistvanyi I, Patlak CS, Ellis RA, Cserr HF. Drainage of interstitial fluid from different regions of rat brain. Am J Physiol 1984 246 : F835 44 (Pubitemid 14075694)
10. Weller RO. Pathology of cerebrospinal fluid and interstitial fluid of the CNS: significance for Alzheimer disease, prion disorders and multiple sclerosis. J Neuropathol Exp Neurol 1998 57 : 885 94 (Pubitemid 28477999)
11. Yamada S, DePasquale M, Patlak CS, Cserr HF. Albumin outflow into deep cervical lymph from different regions of rabbit brain. Am J Physiol 1991 261 : H1197 204
12. Zhang ET, Richards HK, Kida S, Weller RO. Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol 1992 83 : 233 9
13. Harling-Berg CJ, Park TJ, Knopf PM. Role of the cervical lymphatics in the Th2-type hierarchy of CNS immune regulation. J Neuroimmunol 1999 101 : 111 27 (Pubitemid 29516453)
14. Galea I, Bechmann I, Perry VH. What is immune privilege (not)? Trends Immunol 2007 28 : 12 18
15. Hatterer E, Davoust N, er-Bazes M, Vuaillat C, Malcus C, Belin MF, Nataf S. How to drain without lymphatics? Dendritic cells migrate from the cerebrospinal fluid to the B-cell follicles of cervical lymph nodes. Blood 2006 107 : 806 12 (Pubitemid 43076409)
16. Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, Perry VH, Weller RO. Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 2008 34 : 131 44
17. Pashenkov M, Teleshova N, Kouwenhoven M, Smirnova T, Jin YP, Kostulas V, Huang YM, Pinegin B, Boiko A, Link H. Recruitment of dendritic cells to the cerebrospinal fluid in bacterial neuroinfections. J Neuroimmunol 2002 122 : 106 16 (Pubitemid 34075496)
18. Magliozzi R, Howell O, Vora A, Serafini B, Nicholas R, Puopolo M, Reynolds R, Aloisi F. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 2007 130 : 1089 104 (Pubitemid 47355604)
19. Matyszak MK, Perry VH. Demyelination in the central nervous system following a delayed-type hypersensitivity response to bacillus Calmette-Guerin. Neuroscience 1995 64 : 967 77
20. 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 74 (Pubitemid 38656388)
21. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991 82 : 239 59
22. Morris-Downes MM, Smith PA, Rundle JL, Piddlesden SJ, Baker D, Pham-Dinh D, Heijmans N, Amor S. Pathological and regulatory effects of anti-myelin antibodies in experimental allergic encephalomyelitis in mice. J Neuroimmunol 2002 125 : 114 24 (Pubitemid 34327460)
23. Bø L, Vedeler CA, Nyland HI, Trapp BD, Mork SJ. Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 2003 62 : 723 32 (Pubitemid 36870458)
24. van der Valk P, De Groot CJ. Staging of multiple sclerosis (MS) lesions: pathology of the time frame of MS. Neuropathol Appl Neurobiol 2000 26 : 2 10 (Pubitemid 30145301)
25. Herndon RM, Johnson M. A method for the electron microscopic study of cerebrospinal fluid sediment. J Neuropathol Exp Neurol 1970 29 : 320 30
26. Herndon RM, Kasckow J. Electron microscopic studies of cerebrospinal fluid sediment in demyelinating disease. Ann Neurol 1978 4 : 515 23 (Pubitemid 9098465)
27. Itoyama Y, Sternberger NH, Webster HD, Quarles RH, Cohen SR, Richardson EP Jr. Immunocytochemical observations on the distribution of myelin-associated glycoprotein and myelin basic protein in multiple sclerosis lesions. Ann Neurol 1980 7 : 167 77
28. Brück W, Schmied M, Suchanek G, Bruck Y, Breitschopf H, Poser S, Piddlesden S, Lassmann H. Oligodendrocytes in the early course of multiple sclerosis. Ann Neurol 1994 35 : 65 73 (Pubitemid 24027608)
29. Brück W, Porada P, Poser S, Rieckmann P, Hanefeld F, Kretzschmar HA, Lassmann H. Monocyte/macrophage differentiation in early multiple sclerosis lesions. Ann Neurol 1995 38 : 788 96
30. van der Goes A, Boorsma W, Hoekstra K, Montagne L, De Groot CJ, Dijkstra CD. Determination of the sequential degradation of myelin proteins by macrophages. J Neuroimmunol 2005 161 : 12 20 (Pubitemid 40347246)
31. Cserr HF, Ostrach LH. Bulk flow of interstitial fluid after intracranial injection of blue dextran 2000. Exp Neurol 1974 45 : 50 60
32. Abbott NJ. Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem Int 2004 45 : 545 52 (Pubitemid 38739482)
33. Bradbury MW, Cserr HF, Westrop RJ. Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Physiol 1981 240 : F329 36 (Pubitemid 11150142)
34. Cserr HF, Harling-Berg CJ, Knopf PM. Drainage of brain extracellular fluid into blood and deep cervical lymph and its immunological significance. Brain Pathol 1992 2 : 269 76
35. Kida S, Pantazis A, Weller RO. CSF drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance. Neuropathol Appl Neurobiol 1993 19 : 480 8 (Pubitemid 24010674)
36. Cserr HF, Knopf PM. Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view. Immunol Today 1992 13 : 507 12
37. Koh L, Zakharov A, Johnston M. Integration of the subarachnoid space and lymphatics: is it time to embrace a new concept of cerebrospinal fluid absorption? Cerebrospinal Fluid Res 2005 2 : 6
38. Weller RO, Engelhardt B, Phillips MJ. Lymphocyte targeting of the central nervous system: a review of afferent and efferent CNS-immune pathways. Brain Pathol 1996 6 : 275 88 (Pubitemid 26246383)
39. Knopf PM, Cserr HF, Nolan SC, Wu TY, Harling-Berg CJ. Physiology and immunology of lymphatic drainage of interstitial and cerebrospinal fluid from the brain. Neuropathol Appl Neurobiol 1995 21 : 175 80
40. Ling C, Sandor M, Fabry Z. In situ processing and distribution of intracerebrally injected OVA in the CNS. J Neuroimmunol 2003 141 : 90 8 (Pubitemid 37289000)
41. Mutlu L, Brandt C, Kwidzinski E, Sawitzki B, Gimsa U, Mahlo J, Aktas O, Nitsch R, van Zwam M, Laman JD, Bechmann I. Tolerogenic effect of fiber tract injury: reduced EAE severity following entorhinal cortex lesion. Exp Brain Res 2007 178 : 542 53 (Pubitemid 46569892)
42. Harling-Berg C, Knopf PM, Merriam J, Cserr HF. Role of cervical lymph nodes in the systemic humoral immune response to human serum albumin microinfused into rat cerebrospinal fluid. J Neuroimmunol 1989 25 : 185 93 (Pubitemid 19276908)
43. Flügel A, Berkowicz T, Ritter T, Labeur M, Jenne DE, Li Z, Ellwart JW, Willem M, Lassmann H, Wekerle H. Migratory activity and functional changes of green fluorescent effector cells before and during experimental autoimmune encephalomyelitis. Immunity 2001 14 : 547 60 (Pubitemid 32520866)
44. Lake J, Weller RO, Phillips MJ, Needham M. Lymphocyte targeting of the brain in adoptive transfer cryolesion-EAE. J Pathol 1999 187 : 259 65 (Pubitemid 29037057)
45. Phillips MJ, Weller RO, Kida S, Iannotti F. Focal brain damage enhances experimental allergic encephalomyelitis in brain and spinal cord. Neuropathol Appl Neurobiol 1995 21 : 189 200
46. Phillips MJ, Needham M, Weller RO. Role of cervical lymph nodes in autoimmune encephalomyelitis in the Lewis rat. J Pathol 1997 182 : 457 64 (Pubitemid 27317212)
47. Harling-Berg CJ, Knopf PM, Cserr HF. Myelin basic protein infused into cerebrospinal fluid suppresses experimental autoimmune encephalomyelitis. J Neuroimmunol 1991 35 : 45 51
48. Brabb T, von Dassow P, Ordonez N, Schnabel B, Duke B, Goverman J. In situ tolerance within the central nervous system as a mechanism for preventing autoimmunity. J Exp Med 2000 192 : 871 80
49. Olivares-Villagomez D, Wang Y, Lafaille JJ. Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis. J Exp Med 1998 188 : 1883 94 (Pubitemid 28536776)
50. Carson MJ, Reilly CR, Sutcliffe JG, Lo D. Mature microglia resemble immature antigen-presenting cells. Glia 1998 22 : 72 85 (Pubitemid 28038045)
51. Carson MJ. Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 2002 40 : 218 31 (Pubitemid 35337379)
52. Greter M, Heppner FL, Lemos MP, Odermatt BM, Goebels N, Laufer T, Noelle RJ, Becher B. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat Med 2005 11 : 328 34 (Pubitemid 40460562)
53. Serafini B, Rosicarelli B, Magliozzi R, Stigliano E, Capello E, Mancardi GL, Aloisi F. Dendritic cells in multiple sclerosis lesions: maturation stage, myelin uptake, and interaction with proliferating T cells. J Neuropathol Exp Neurol 2006 65 : 124 41 (Pubitemid 43755377)
54. Bø L, Vedeler CA, Nyland H, Trapp BD, Mork SJ. Intracortical multiple sclerosis lesions are not associated with increased lymphocyte infiltration. Mult Scler 2003 9 : 323 31 (Pubitemid 36958014)
55. Prineas JW, Wright RG. Macrophages, lymphocytes, and plasma cells in the perivascular compartment in chronic multiple sclerosis. Lab Invest 1978 38 : 409 21 (Pubitemid 8338235)
56. Serafini B, Rosicarelli B, Franciotta D, Magliozzi R, Reynolds R, Cinque P, Andreoni L, Trivedi P, Salvetti M, Faggioni A, Aloisi F. Dysregulated Epstein-Barr virus infection in the multiple sclerosis brain. J Exp Med 2007 204 : 2899 912 (Pubitemid 350179559)