Primary oligodendrocyte death does not elicit anti-CNS immunity

Nature Neuroscience

Volumn 15, Issue 4, 2012, Pages 543-550

  Locatelli, Giuseppe ^a   Wörtge, Simone ^b   Buch, Thorsten ^a,c   Ingold, Barbara ^d   Frommer, Friederike ^b   Sobottka, Bettina ^a   Krüger, Martin ^e   Karram, Khalad ^b   Bühlmann, Claudia ^a   Bechmann, Ingo ^e   Heppner, Frank L ^d   Waisman, Ari ^b   Becher, Burkhard ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CD11B ANTIGEN; CD45 ANTIGEN; HERMES ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PROTEOLIPID PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; BYSTANDER EFFECT; CELL ACTIVATION; CELL FUNCTION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEMYELINATION; IN VIVO STUDY; LYMPH NODE; MACROPHAGE; MICROGLIA; MOTOR DYSFUNCTION; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE;

ANIMALS; CELL DEATH; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE KNOCK-IN TECHNIQUES; MICE; MICE, TRANSGENIC; MULTIPLE SCLEROSIS; OLIGODENDROGLIA;

EID: 84859218293     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3062     Document Type: Article

References (50)

1. Compston, A. & Coles, A. Multiple sclerosis. Lancet 372, 1502-1517 (2008).
2. Lassmann, H., Bruck, W. & Lucchinetti, C.F. The immunopathology of multiple sclerosis: an overview. Brain Pathol. 17, 210-218 (2007).
3. Lucchinetti, C.F., Bruck, W. & Lassmann, H. Evidence for pathogenic heterogeneity in multiple sclerosis. Ann. Neurol. 56, 308 (2004).
4. Barnett, M.H. & Prineas, J.W. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 55, 458-468 (2004).
5. Barnett, M.H. & Sutton, I. The pathology of multiple sclerosis: a paradigm shift. Curr. Opin. Neurol. 19, 242-247 (2006).
6. Filippi, M., Rocca, M.A., Martino, G., Horsfield, M.A. & Comi, G. Magnetization transfer changes in the normal appearing white matter precede the appearance of enhancing lesions in patients with multiple sclerosis. Ann. Neurol. 43, 809-814 (1998).
7. Narayana, P.A., Doyle, T.J., Lai, D. & Wolinsky, J.S. Serial proton magnetic resonance spectroscopic imaging, contrast-enhanced magnetic resonance imaging, and quantitative lesion volumetry in multiple sclerosis. Ann. Neurol. 43, 56-71 (1998).
8. Kassmann, C.M. et al. Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nat. Genet. 39, 969-976 (2007).
9. Ip, C.W. et al. Immune cells contribute to myelin degeneration and axonopathic changes in mice overexpressing proteolipid protein in oligodendrocytes. J. Neurosci. 26, 8206-8216 (2006).
10. Buch, T. et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2, 419-426 (2005).
11. Hövelmeyer, N. et al. Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. J. Immunol. 175, 5875-5884 (2005).
12. Traka, M. et al. A genetic mouse model of adult-onset, pervasive central nervous system demyelination with robust remyelination. Brain 133, 3017-3029 (2010).
13. Pohl, H.B. et al. Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J. Neurosci. 31, 1069-1080 (2011).
14. van Zwam, M. et al. Surgical excision of CNS-draining lymph nodes reduces relapse severity in chronic-relapsing experimental autoimmune encephalomyelitis. J. Pathol. 217, 543-551 (2009).
15. de Vos, A.F. et al. Transfer of central nervous system autoantigens and presentation in secondary lymphoid organs. J. Immunol. 169, 5415-5423 (2002).
16. Fabriek, B.O. et al. In vivo detection of myelin proteins in cervical lymph nodes of MS patients using ultrasound-guided fine-needle aspiration cytology. J. Neuroimmunol. 161, 190-194 (2005).
17. Bettelli, E. et al. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197, 1073-1081 (2003).
18. Frommer, F. et al. Tolerance without clonal expansion: self-antigen-expressing B cells program self-reactive T cells for future deletion. J. Immunol. 181, 5748-5759 (2008).
19. Elgueta, R. et al. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol. Rev. 229, 152-172 (2009).
20. Ransohoff, R.M. & Perry, V.H. Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27, 119-145 (2009).
21. Carson, M.J. Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 40, 218-231 (2002).
22. Becher, B. & Antel, J.P. Comparison of phenotypic and functional properties of immediately ex vivo and cultured human adult microglia. Glia 18, 1-10 (1996).
23. Link, H. & Muller, R. Immunoglobulins in multiple sclerosis and infections of the nervous system. Arch. Neurol. 25, 326-344 (1971).
24. Herndon, R.M. & Kasckow, J. Electron microscopic studies of cerebrospinal fluid sediment in demyelinating disease. Ann. Neurol. 4, 515-523 (1978).
25. Prineas, J.W. & Wright, R.G. Macrophages, lymphocytes, and plasma cells in the perivascular compartment in chronic multiple sclerosis. Lab. Invest. 38, 409-421 (1978).
26. Urich, E., Gutcher, I., Prinz, M. & Becher, B. Autoantibody-mediated demyelination depends on complement activation, but not activatory Fc-receptors. Proc. Natl. Acad. Sci. USA 103, 18697-18702 (2006).
27. Gallucci, S. & Matzinger, P. Danger signals: SOS to the immune system. Curr. Opin. Immunol. 13, 114-119 (2001).
28. Mueller, D.L. Mechanisms maintaining peripheral tolerance. Nat. Immunol. 11, 21-27 (2010).
29. Sakaguchi, S. et al. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol. Rev. 212, 8-27 (2006).
30. Honjo, T., Nishizuka, Y., Kato, I. & Hayaishi, O. Adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis by diphtheria toxin. J. Biol. Chem. 246, 4251-4260 (1971).
31. Emerson, M.R., Biswas, S. & Le Vine, S.M. Cuprizone and piperonyl butoxide, proposed inhibitors of T-cell function, attenuate experimental allergic encephalomyelitis in SJL mice. J. Neuroimmunol. 119, 205-213 (2001).
32. Zatta, P. et al. Copper and zinc dismetabolism in the mouse brain upon chronic cuprizone treatment. Cell. Mol. Life Sci. 62, 1502-1513 (2005).
33. Elloso, M.M., Phiel, K., Henderson, R.A., Harris, H.A. & Adelman, S.J. Suppression of experimental autoimmune encephalomyelitis using estrogen receptor-selective ligands. J. Endocrinol. 185, 243-252 (2005).
34. Chernoff, G.F. Shiverer: an autosomal recessive mutant mouse with myelin deficiency. J. Hered. 72, 128 (1981).
35. Wang, H., Zhan, Y., Xu, L., Feuerstein, G.Z. & Wang, X. Use of suppression subtractive hybridization for differential gene expression in stroke: discovery of CD44 gene expression and localization in permanent focal stroke in rats. Stroke 32, 1020-1027 (2001).
36. Kim, M.D., Cho, H.J. & Shin, T. Expression of osteopontin and its ligand, CD44, in the spinal cords of Lewis rats with experimental autoimmune encephalomyelitis. J. Neuroimmunol. 151, 78-84 (2004).
37. Bédard, A., Tremblay, P., Chernomoretz, A. & Vallieres, L. Identification of genes preferentially expressed by microglia and upregulated during cuprizone-induced inflammation. Glia 55, 777-789 (2007).
38. Remington, L.T., Babcock, A.A., Zehntner, S.P. & Owens, T. Microglial recruitment, activation and proliferation in response to primary demyelination. Am. J. Pathol. 170, 1713-1724 (2007).
39. Hiremath, M.M., Chen, V.S., Suzuki, K., Ting, J.P. & Matsushima, G.K. MHC class II exacerbates demyelination in vivo independently of T cells. J. Neuroimmunol. 203, 23-32 (2008).
40. Adams, C.W., Poston, R.N. & Buk, S.J. Pathology, histochemistry and immunocytochemistry of lesions in acute multiple sclerosis. J. Neurol. Sci. 92, 291-306 (1989).
41. Maña, P. et al. Demyelination caused by the copper chelator cuprizone halts T cell-mediated autoimmune neuroinflammation. J. Neuroimmunol. 210, 13-21 (2009).
42. Griffiths, I. et al. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280, 1610-1613 (1998).
43. Yin, X. et al. Evolution of a neuroprotective function of central nervous system myelin. J. Cell Biol. 172, 469-478 (2006).
44. Lappe-Siefke, C. et al. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33, 366-374 (2003).
45. Berger, J. & Gartner, J. X-linked adrenoleukodystrophy: clinical, biochemical and pathogenetic aspects. Biochim. Biophys. Acta 1763, 1721-1732 (2006).
46. Haak, S. et al. IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J. Clin. Invest. 119, 61-69 (2009).
47. Weston, S.A. & Parish, C.R. New fluorescent dyes for lymphocyte migration studies. Analysis by flow cytometry and fluorescence microscopy. J. Immunol. Methods 133, 87-97 (1990).
48. Becher, B., Durell, B.G. & Noelle, R.J. Experimental autoimmune encephalitis and inflammation in the absence of interleukin-12. J. Clin. Invest. 110, 493-497 (2002).
49. Förster, I. & Rajewsky, K. Expansion and functional activity of Ly-1 + B cells upon transfer of peritoneal cells into allotype-congenic, newborn mice. Eur. J. Immunol. 17, 521-528 (1987).
50. Spergel, D.J., Kruth, U., Hanley, D.F., Sprengel, R. & Seeburg, P.H. GABA-and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J. Neurosci. 19, 2037-2050 (1999).