Disease-specific molecular events in cortical multiple sclerosis lesions

Brain

Volumn 136, Issue 6, 2013, Pages 1799-1815

  Fischer, Marie Therese ^a   Wimmer, Isabella ^a   Höftberger, Romana ^b   Gerlach, Susanna ^a   Haider, Lukas ^a   Zrzavy, Tobias ^a   Hametner, Simon ^a   Mahad, Don ^c   Binder, Christoph J ^a   Krumbholz, Markus ^d   Bauer, Jan ^a   Bradl, Monika ^a   Lassmann, Hans ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

cortex; demyelination; gene expression; multiple sclerosis; neurodegeneration

Indexed keywords

ADOLESCENT; ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; AUTOPSY; B LYMPHOCYTE; BRAIN CORTEX LESION; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CHILD; COMPARATIVE STUDY; CONTROLLED STUDY; DENDRITE; DNA DAMAGE; DNA REPAIR; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MICROARRAY ANALYSIS; MICRODISSECTION; MICROGLIA; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NERVE FIBER; NERVE INJURY; NERVE REGENERATION; NEUROPATHOLOGY; OLIGODENDROGLIA; PRESCHOOL CHILD; PRIORITY JOURNAL; REMYELINIZATION; SCHOOL CHILD; TUBERCULOUS MENINGITIS;

EID: 84878828439     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt110     Document Type: Article

References (63)

1. Aboul-Enein F, Rauschka H, Kornek B, Stadelmann C, Stefferl A, Bruck W, et al. Preferential loss of myelin-associated glycoprotein reflects hypoxia-like white matter damage in stroke and inflammatory brain diseases. J Neuropath Exp Neurol 2003; 62: 25-33.
2. Albert M, Antel J, Bruck W, Stadelmann C. Extensive cortical remyelination in patients with chronic multiple sclerosis. Brain Pathol 2007; 17: 129-38.
3. Alvarez JI, Cayrol R, Prat A. Disruption of central nervous system barriers in multiple sclerosis. Biochim Biophys Acta 2011; 1812: 252-64.
4. Barnett MH, Prineas JW. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 2004; 55: 458-68.
5. Bauer J, Elger CE, Hans VH, Schramm J, Urbach H, Lassmann H, et al. Astrocytes are a specific immunological target in Rasmussen's encephalitis. Ann Neurol 2007; 62: 67-80.
6. Bian W, Harter K, Hammond-Rosenbluth KE, Lupo JM, Kelley DA, Vigneron DB, et al. A serial in vivo 7T magnetic resonance phase imaging study of white matter lesions in multiple sclerosis. Mult Scler 2012; 19: 69-75.
7. Bien CG, Bauer J, Deckwerth TL, Wiendl H, Deckert M, Wiestler OD, et al. Destruction of neurons by cytotoxic T cells: a new pathogenic mechanism in Rasmussen's encephalitis. Ann Neurol 2002; 51: 311-18.
8. Bo 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.
9. Breitschopf H, Suchanek G, Gould RM, Colman DR, Lassmann H. In situ hybridization with digoxigenin-labeled probes: sensitive and reliable detection method applied to myelinating rat brain. Acta Neuropathol 1992; 84: 581-7.
10. Campbell GR, Ziabreva I, Reeve AK, Krishnan KJ, Reynolds R, Howell O, et al. Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis. Ann Neurol 2011; 69: 481-92.
11. Caramia F, Tinelli E, Francia A, Pozzilli C. Cognitive deficits in multiple sclerosis: a review of functional MRI studies. Neurol Sci 2010; 31: S239-43.
12. Choi S, Howell OW, Carassiti D, Magliozzi R, Gveric D, Muraro PA, et al. Meningeal inflammation plays a role in the pathology of primary progressive multiple sclerosis. Brain 2012; 135: 2925-37.
13. Cunnea P, McMahon J, O'Connell E, Mashayekhi K, Fitzgerald U, McQuaid S. Gene expression analysis of the microvascular compartment in multiple sclerosis using laser microdissected blood vessels. Acta Neuropathol 2010; 119: 601-15.
14. Dutta R, Chang A, Doud MK, Kidd GJ, Ribaudo MV, Young EA, et al. Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients. Ann Neurol 2011; 69: 445-54.
15. Dutta R, McDonough J, Yin X, Peterson J, Chang A, Torres T, et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 2006; 59: 478-89.
16. Dutta R, Trapp BD. Mechanisms of neuronal dysfunction and degeneration in multiple sclerosis. Prog Neurobiol 2011; 93: 1-12.
17. Eisele S, Krumbholz M, Fischer MT, Mohan H, Junker A, Arzberger T, et al. Prospects of transcript profiling for mRNAs and microRNAs using formalin fixed paraffin embedded dissected autoptic multiple sclerosis lesions. Brain Pathol 2012; 22: 607-12.
18. Fischer MT, Sharma R, Lim JL, Haider L, Frischer JM, Drexhage J, et al. NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury. Brain 2012; 135: 886-99.
19. Geurts JJ, Bo L, Roosendaal SD, Hazes T, Daniels R, Barkhof F, et al. Extensive hippocampal demyelination in multiple sclerosis. J Neuropathol Exp Neurol 2007; 66: 819-27.
20. Gold R, Schmied M, Rothe G, Zischler H, Breitschopf H, Wekerle H, et al. Detection of DNA-fragmentation in apoptosis: application of in situ nick translation to cell culture systems and tissue sections. J Histochem Cytochem 1993; 41: 1023-30.
21. Graumann U, Reynolds R, Steck AJ, Schaeren-Wiemers N. Molecular changes in normal appearing white matter in multiple sclerosis are characteristic of neuroprotective mechanisms against hypoxic insult. Brain Pathol 2003; 13: 554-73.
22. Gray E, Thomas TL, Betmouni S, Scolding N, Love S. Elevated activity and microglial expression of myeloperoxidase in demyelinated cerebral cortex in multiple sclerosis. Brain Pathol 2008; 18: 86-95.
23. Haider L, Fischer MT, Frischer JM, Bauer J, Hoftberger R, Botond G, et al. Oxidative damage in multiple sclerosis lesions. Brain 2011; 134: 1914-24.
24. Hoftberger R, Fink S, Aboul-Enein F, Botond G, Olah J, Berki T, et al. Tubulin polymerization promoting protein (TPPP/p25) as a marker for oligodendroglial changes in multiple sclerosis. Glia 2010; 58: 1847-57.
25. Howell OW, Reeves CA, Nicholas R, Carassiti D, Radotra B, Gentleman SM, et al. Meningeal inflammation is widespread and linked to cortical pathology in multiple sclerosis. Brain 2011; 134: 2755-71.
26. Joller N, Peters A, Anderson AC, Kuchroo VK. Immune checkpoints in central nervous system autoimmunity. Immunol Rev 2012; 248: 122-39.
27. King G, Payne S, Walker F, Murray GI. A highly sensitive detection method for immunohistochemistry using biotinylated tyramine. J Pathol 1997; 183: 237-41.
28. Kolasinski J, Stagg CJ, Chance SA, DeLuca GC, Esiri MM, Chang EH, et al. A combined post-mortem MRI and quantitative histological study of multiple sclerosis pathology. Brain 2012; 135: 2938-51.
29. Kutzelnigg A, Faber-Rod JC, Bauer J, Lucchinetti CF, Sorensen PS, Laursen H, et al. Widespread demyelination in the cerebellar cortex in multiple sclerosis. Brain Pathol 2007; 17: 38-44.
30. 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 2005; 128: 2705-12.
31. Lassmann H, Bancher C, Breitschopf H, Wegiel J, Bobinski M, Jellinger K, et al. Cell death in Alzheimer's disease evaluated by DNA-fragmentation in situ. Acta Neuropathol 1995; 89: 35-41.
32. Lassmann H, Bruck W, Lucchinetti CF. The immunopathology of multiple sclerosis: an overview. Brain Pathol 2007; 17: 210-18.
33. Lassmann H, van Horssen J, Mahad D. Progressive multiple sclerosis: pathology and pathogenesis. Nat Rev Neurol 2012; 8: 647-56.
34. Liu JS, Zhao ML, Brosnan CF, Lee SC. Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am J Pathol 2001; 158: 2057-66.
35. Lock C, Hermans G, Pedotti R, Brendolan A, Schadt E, Garren H, et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 2002; 8: 500-8.
36. Lucchinetti CF, Popescu BF, Bunyan RF, Moll NM, Roemer SF, Lassmann H, et al. Inflammatory cortical demyelination in early multiple sclerosis. N Engl J Med 2011; 365: 2188-97.
37. Mahad D, Ziabreva I, Lassmann H, Turnbull D. Mitochondrial defects in acute multiple sclerosis lesions. Brain 2008; 131: 1722-35.
38. Magliozzi R, Howell OW, Reeves C, Roncaroli F, Nicholas R, Serafini B, et al. A gradient of neuronal loss and meningeal inflammation in multiple sclerosis. Ann Neurol 2010; 68: 477-93.
39. Marik C, Felts PA, Bauer J, Lassmann H, Smith KJ. Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity Brain 2007; 130: 2800-15.
40. Mitew S, Kirkcaldie MT, Halliday GM, Shepherd CE, Vickers JC, Dickson TC. Focal demyelination in Alzheimer's disease and transgenic mouse models. Acta Neuropathol 2010; 119: 567-77.
41. Moll NM, Rietsch AM, Ransohoff AJ, Cossoy MB, Huang D, Eichler FS, et al. Cortical demyelination in PML and MS: Similarities and differences. Neurology 2008; 70: 336-43.
42. Muller GJ, Stadelmann C, Bastholm L, Elling F, Lassmann H, Johansen FF. Ischemia leads to apoptosis-and necrosis-like neuron death in the ischemic rat hippocampus. Brain Pathol 2004; 14: 415-24.
43. Mycko MP, Papoian R, Boschert U, Raine CS, Selmaj KW. cDNA microarray analysis in multiple sclerosis lesions: detection of genes associated with disease activity. Brain 2003; 126: 1048-57.
44. Palinski W, Horkko S, Miller E, Steinbrecher UP, Powell HC, Curtiss LK, et al. Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-deficient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma. J Clin Invest 1996; 98: 800-14.
45. Peterson JW, Bo L, Mork S, Chang A, Trapp BD. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001; 50: 389-400.
46. 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: 555-64.
47. Polman CH, O'Connor PW, Havrdova E, Hutchinson M, Kappos L, Miller DH, et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 2006; 354: 899-910.
48. Prendergast CT, Anderton SM. Immune cell entry to central nervous system-current understanding and prospective therapeutic targets. Endocr Metab Immune Disord Drug Targets 2009; 9: 315-27.
49. Rocca MA, Filippi M. Functional MRI in multiple sclerosis. J Neuroimaging 2007; 17 (Suppl 1): 36S-41S.
50. Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011; 476: 214-19.
51. Schmidt F, van den Eijnden M, Pescini Gobert R, Saborio GP, Carboni S, Alliod C, et al. Identification of VHY/Dusp15 as a regulator of oligodendrocyte differentiation through systematic genomics approach. PLoS One 2012; 7: e40457.
52. Stam NJ, Vroom TM, Peters PJ, Pastoors EB, Ploegh HL. HLA-A-and HLA-B-specific monoclonal antibodies reactive with free heavy chains in western blots, in formalin-fixed, paraffin-embedded tissue sections and in cryo-immuno-electron microscopy. Int Immunol 1990; 2: 113-25.
53. Torkildsen O, Stansberg C, Angelskar SM, Kooi EJ, Geurts JJ, van der Valk P, et al. Upregulation of immunoglobulin-related genes in cortical sections from multiple sclerosis patients. Brain Pathol 2010; 20: 720-9.
54. Trapp BD, Stys PK. Virtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosis. Lancet Neurol 2009; 8: 280-91.
55. Tzartos JS, Friese MA, Craner MJ, Palace J, Newcombe J, Esiri MM, et al. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 2008; 172: 146-55.
56. van Horssen J, Schreibelt G, Drexhage J, Hazes T, Dijkstra CD, van der Valk P, et al. Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic Biol Med 2008; 45: 1729-37.
57. Vercellino M, Plano F, Votta B, Mutani R, Giordana MT, Cavalla P. Grey matter pathology in multiple sclerosis. J Neuropath Exp Neurol 2005; 64: 1101-7.
58. Veto S, Acs P, Bauer JK, Lassmann H, Berente Z, Setalo G Jr, et al. Inhibiting poly(ADP-ribose) polymerase: a potential therapy against oligodendrocyte death. Brain 2010; 133: 822-34.
59. Wegner C, Esiri MM, Chance SA, Palace J, Matthews PM. Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology 2006; 67: 960-7.
60. Whitney LW, Becker KG, Tresser NJ, Caballero-Ramos CI, Munson PJ, Prabhu VV, et al. Analysis of gene expression in mutiple sclerosis lesions using cDNA microarrays. Ann Neurol 1999; 46: 425-8.
61. Wisniewski HM, Bloom BR. Primary demyelination as a nonspecific consequence of a cell-mediated immune reaction. J Exp Med 1975; 141: 346-59.
62. Zarbock A, Kempf T, Wollert KC, Vestweber D. Leukocyte integrin activation and deactivation: novel mechanisms of balancing inflammation. J Mol Med (Berl) 2012; 90: 353-9.
63. Zeis T, Probst A, Steck AJ, Stadelmann C, Bruck W, Schaeren-Wiemers N. Molecular changes in white matter adjacent to an active demyelinating lesion in early multiple sclerosis. Brain Pathol 2009; 19: 459-66.