Early axonal damage and progressive myelin pathology define the kinetics of CNS histopathology in a mouse model of multiple sclerosis

Clinical Immunology

Volumn 149, Issue 1, 2013, Pages 32-45

  Recks, Mascha S ^a   Stormanns, Eva R ^a   Bader, Jonas ^a   Arnhold, Stefan ^b   Addicks, Klaus ^a   Kuerten, Stefanie ^a,c  

^a UNIVERSITY OF COLOGNE   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Axonal pathology; ; EAE; ; Electron microscopy; ; MOG:35 55; ; MS; Neurodegeneration;

Indexed keywords

MYELIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DEMYELINATING DISEASE; DNA IMMUNIZATION; FEMALE; HISTOPATHOLOGY; KINETICS; MICROSCOPY; MOUSE; MULTIPLE SCLEROSIS; NERVE FIBER; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; NORMAL APPEARING WHITE MATTER; PRIORITY JOURNAL; SYMPTOM; TISSUE SECTION; WHITE MATTER;

4% PARAFORMALDEHYDE/4% GLUTARALDEHYDE; AXONAL PATHOLOGY;; B6; C57BL/6; CENTRAL NERVOUS SYSTEM; CFA; CNS; COMPLETE FREUND'S ADJUVANT; CORTICOSPINAL TRACT; CST; DC; DORSAL COLUMN; EAE; EAE;; ELECTRON MICROSCOPY;; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FGF; FIBROBLAST GROWTH FACTOR; IFA; INCOMPLETE FREUND'S ADJUVANT; MBP; MBP-PLP FUSION PROTEIN; MOG; MOG:35-55;; MP4; MS; MULTIPLE SCLEROSIS; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NAWM; NEAREST NEIGHBOR NEUROFILAMENT DISTANCE; NEURODEGENERATION;; NNND; NORMAL-APPEARING WHITE MATTER; OLIGODENDROCYTE PRECURSOR CELLS; OPC; PFA-GA; PLP; PROTEOLIPID PROTEIN; VENTROLATERAL COLUMN; VLC;

ANIMALS; AXONS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; KINETICS; LUMBAR VERTEBRAE; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; MYELIN BASIC PROTEIN; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; RECOMBINANT FUSION PROTEINS; SPINAL CORD;

EID: 84880942446     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2013.06.004     Document Type: Article

References (49)

1. Goverman J., Brabb T. Rodent models of experimental allergic encephalomyelitis applied to the study of multiple sclerosis. Lab. Anim. Sci. 1996, 46:482-492.
2. Krishnamoorthy G., Wekerle H. EAE: an immunologist's magic eye. Eur. J. Immunol. 2009, 39:2031-2035.
3. Mix E., Meyer-Rienecker H., Zettl U.K. Animal models of multiple sclerosis for the development and validation of novel therapies - potential and limitations. J. Neurol. 2008, 255(Suppl. 6):7-14.
4. Ben-Nun A., Wekerle H., Cohen I.R. The rapid isolation of clonable antigen-specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis. Eur. J. Immunol. 1981, 11:195-199.
5. Stromnes I.M., Goverman J.M. Passive induction of experimental allergic encephalomyelitis. Nat. Protoc. 2006, 1:1952-1960.
6. Gold R., Linington C., Lassmann H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 2006, 129:1953-1971.
7. Bernard C.C., Johns T.G., Slavin A., Ichikawa M., Ewing C., Liu J., Bettadapura J. Myelin oligodendrocyte glycoprotein: a novel candidate autoantigen in multiple sclerosis. J. Mol. Med. 1997, 75:77-88.
8. Mendel I., Kerlero de Rosbo N., Ben-Nun A. A myelin oligodendrocyte glycoprotein peptide induces typical chronic experimental autoimmune encephalomyelitis in H-2b mice: fine specificity and T cell receptor V beta expression of encephalitogenic T cells. Eur. J. Immunol. 1995, 25:1951-1959.
9. Oliver A.R., Lyon G.M., Ruddle N.H. Rat and human myelin oligodendrocyte glycoproteins induce experimental autoimmune encephalomyelitis by different mechanisms in C57BL/6 mice. J. Immunol. 2003, 171:462-468.
10. Herrero-Herranz E., Pardo L.A., Gold R., Linker R.A. Pattern of axonal injury in murine myelin oligodendrocyte glycoprotein induced experimental autoimmune encephalomyelitis: implications for multiple sclerosis. Neurobiol. Dis. 2008, 30:162-173.
11. Kuerten S., Gruppe T.L., Laurentius L., Kirch C., Tary-Lehmann M., Lehmann P.V., Addicks K. Differential patterns of spinal cord pathology induced by MP4, MOG peptide 35-55, and PLP peptide 178-191 in C57BL/6 mice. APMIS 2011, 119:336-346.
12. Recks M.S., Addicks K., Kuerten S. Spinal cord histopathology of MOG peptide 35-55-induced experimental autoimmune encephalomyelitis is time- and score-dependent. Neurosci. Lett. 2011, 494:227-231.
13. Berard J.L., Wolak K., Fournier S., David S. Characterization of relapsing-remitting and chronic forms of experimental autoimmune encephalomyelitis in C57BL/6 mice. Glia 2010, 58:434-445.
14. Kuerten S., Kostova-Bales D.A., Frenzel L.P., Tigno J.T., Tary-Lehmann M., Angelov D.N., Lehmann P.V. MP4- and MOG:35-55-induced EAE in C57BL/6 mice differentially targets brain, spinal cord and cerebellum. J. Neuroimmunol. 2007, 189:31-40.
15. Kuerten S., Javeri S., Tary-Lehmann M., Lehmann P.V., Angelov D.N. Fundamental differences in the dynamics of CNS lesion development and composition in MP4- and MOG peptide 35-55-induced experimental autoimmune encephalomyelitis. Clin. Immunol. 2008, 129:256-267.
16. De Stefano N., Matthews P.M., Fu L., Narayanan S., Stanley J., Francis G.S., Antel J.P., Arnold D.L. Axonal damage correlates with disability in patients with relapsing-remitting multiple sclerosis. Results of a longitudinal magnetic resonance spectroscopy study. Brain 1998, 121:1469-1477.
17. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mörk S., Bö L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 1998, 338:278-285.
18. Chomiak T., Hu B. What is the optimal value of the g-ratio for myelinated fibers in the rat CNS? A theoretical approach. PLoS One 2009, 4:e7754.
19. Mao P., Reddy P.H. Is multiple sclerosis a mitochondrial disease?. Biochim. Biophys. Acta 2010, 1802:66-79.
20. Schon E.A., Manfredi G. Neuronal degeneration and mitochondrial dysfunction. J. Clin. Invest. 2003, 111(2011):303-312.
21. Lunn M.P., Crawford T.O., Hughes R.A., Griffin J.W., Sheikh K.A. Anti-myelin-associated glycoprotein antibodies alter neurofilament spacing. Brain 2002, 125:904-911.
22. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683-747.
23. Bitsch A., Schuchardt J., Bunkowski S., Kuhlmann T., Brück W. Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation. Brain 2000, 123:1174-1183.
24. Allen I.V., McQuaid S., Mirakhur M., Nevin G. Pathological abnormalities in the normal-appearing white matter in multiple sclerosis. Neurol. Sci. 2001, 22:141-144.
25. Allen I.V., Glover G., Anderson R. Abnormalities in the macroscopically normal white matter in cases of mild or spinal multiple sclerosis (MS). Acta Neuropathol. Suppl. 1981, 7:176-178.
26. Kutzelnigg A., Lucchinetti C.F., Stadelmann C., Brück W., Rauschka H., Bergmann M., Schmidbauer M., Parisi J.E., Lassmann H. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 2005, 128:2705-2712.
27. Gay D., Esiri M. Blood-brain barrier damage in acute multiple sclerosis plaques. Brain 1991, 114:557-572.
28. Evangelou N., Konz D., Esiri M.M., Smith S., Palace J., Matthews P.M. Regional axonal loss in the corpus callosum correlates with cerebral white matter lesion volume and distribution in multiple sclerosis. Brain 2000, 123:1845-1849.
29. Fu L., Matthews P.M., De Stefano N., Worsley K.J., Narayanan S., Francis G.S., Antel J.P., Wolfson C., Arnold D.L. Imaging axonal damage of normal-appearing white matter in multiple sclerosis. Brain 1998, 121:103-113.
30. Gruppe T.L., Recks M.S., Addicks K., Kuerten S. The extent of ultrastructural spinal cord pathology reflects disease severity in experimental autoimmune encephalomyelitis. Histol. Histopathol. 2012, 27:1163-1174.
31. Guy J., Ellis E.A., Hope G.M., Emerson S. Maintenance of myelinated fibre g ratio in acute experimental allergic encephalomyelitis. Brain 1991, 114:281-294.
32. Kuerten S., Lichtenegger F.S., Faas S., Angelov D.N., Tary-Lehmann M., Lehmann P.V. MBP-PLP fusion protein-induced EAE in C57BL/6 mice. J. Neuroimmunol. 2006, 177:99-111.
33. Tompkins S.M., Padilla J., Dal Canto M.C., Ting J.P., Van Kaer L., Miller S.D. De novo central nervous system processing of myelin antigen is required for the initiation of experimental autoimmune encephalomyelitis. J. Immunol. 2002, 168:4173-4183.
34. Bannerman P.G., Hahn A., Ramirez S., Morley M., Bönnemann C., Yu S., Zhang G.X., Rostami A., Pleasure D. Motor neuron pathology in experimental autoimmune encephalomyelitis: studies in THY1-YFP transgenic mice. Brain 2005, 128:1877-1886.
35. Brück W., Kuhlmann T., Stadelmann C. Remyelination in multiple sclerosis. J. Neurol. Sci. 2003, 206:181-185.
36. Stangel M. Remyelinating and neuroprotective treatments in multiple sclerosis. Expert Opin. Inv. Drug. 2004, 13:331-347.
37. Rottlaender A., Villwock H., Addicks K., Kuerten S. Neuro protective role of fibroblast growth factor-2 in experimental autoimmune encephalomyelitis. Immunology 2011, 133:370-378.
38. Goddard D.R., Berry M., Kirvell S.L., Butt A.M. Fibroblast growth factor-2 inhibits myelin production by oligodendrocytes in vivo. Mol. Cell. Neurosci. 2001, 18:557-569.
39. Aharoni R., Vainshtein A., Eilam R., From R., Shinder V., Arnon R. Distinct pathological patterns in relapsing-remitting and chronic models of experimental autoimmune enchephalomyelitis and the neuroprotective effect of glatiramer acetate. J. Autoimmun. 2011, 37:228-241.
40. Holmøy T. The immunology of multiple sclerosis: disease mechanisms and therapeutic targets. Minerva. Med. 2008, 99:119-140.
41. Lassmann H., Brück W., Lucchinetti C.F. The immunopathology of multiple sclerosis: an overview. Brain Pathol. 2007, 17:210-218.
42. Lassmann H. Mechanisms of inflammation induced tissue injury in multiple sclerosis. J. Neurol. Sci. 2008, 274:45-47.
43. Kuhlmann T., Lingfeld G., Bitsch A., Schuchardt J., Brück W. Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain 2002, 125:2202-2212.
44. Bjartmar A., Wujek J.R., Trapp B.D. Axonal loss in the pathology of MS: consequences for understanding the progressive phase of the disease. J. Neurol. Sci. 2003, 206:165-171.
45. Zeis T., Graumann U., Reynolds R., Schaeren-Wiemers N. Normal-appearing white matter in multiple sclerosis is in a subtle balance between inflammation and neuroprotection. Brain 2008, 131:288-303.
46. Tompkins S.M., Padilla J., Dal Canto M.C., Ting J.P., Van Kaer L., Miller S.D. De novo central nervous system processing of myelin antigen is required for the initiation of experimental autoimmune encephalomyelitis. J. Immunol. 2002, 168:4173-4183.
47. Khan O., Shen Y., Caon C., Bao F., Ching W., Reznar M., Buccheister A., Hu J., Latif Z., Tselis A., Lisak R. Axonal metabolic recovery and potential neuroprotective effect of glatiramer acetate in relapsing-remitting multiple sclerosis. Mult. Scler. 2005, 11:646-651.
48. Narayanan S., De Stefano N., Francis G.S., Arnaoutelis R., Caramanos Z., Collins D.L., Pelletier D., Arnason B.G.W., Antel J.P., Arnold D.L. Axonal metabolic recovery in multiple sclerosis patients treated with interferon beta-1b. J. Neurol. 2001, 248:979-986.
49. Neumann H. Molecular mechanisms of axonal damage in inflammatory central nervous system diseases. Curr. Opin. Neurol. 2003, 16:267-273.