A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis

Nature Medicine

Volumn 17, Issue 4, 2011, Pages 495-499

  Nikić, Ivana ^a   Merkler, Doron ^b,c   Sorbara, Catherine ^a   Brinkoetter, Mary ^d   Kreutzfeldt, Mario ^b,c   Bareyre, Florence M ^a   Brück, Wolfgang ^b   Bishop, Derron ^d   Misgeld, Thomas ^e   Kerschensteiner, Martin ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^d BALL STATE UNIVERSITY   (United States)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; MOUSE; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE FIBER DEGENERATION; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; AXONS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FREE RADICAL SCAVENGERS; HUMANS; MACROPHAGE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, VIDEO; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE DEGENERATION; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES;

EID: 79953761792     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2324     Document Type: Article

References (40)

1. Hauser, S.L. & Oksenberg, J.R. The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron 52, 61-76 (2006) (Pubitemid 44466355)
2. Trapp, B.D. & Nave, K.A. Multiple sclerosis: an immune or neurodegenerative disorder? Annu. Rev. Neurosci. 31, 247-269 (2008)
3. Trapp, B.D. et al. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338, 278-285 (1998) (Pubitemid 28065253)
4. Lucchinetti, C. et al. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann. Neurol. 47, 707-17 (2000) (Pubitemid 30390191)
5. Trapp, B.D. & Stys, P.K. Virtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosis. Lancet Neurol. 8, 280-291 (2009)
6. Waxman, S.G. Axonal conduction and injury in multiple sclerosis: the role of sodium channels. Nat. Rev. Neurosci. 7, 932-941 (2006)
7. Pitt, D., Werner, P. & Raine, C.S. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 6, 67-70 (2000) (Pubitemid 30048528)
8. Medana, I., Martinic, M.A., Wekerle, H. & Neumann, H. Transection of major histocompatibility complex class I-induced neurites by cytotoxic T lymphocytes. Am. J. Pathol. 159, 809-815 (2001) (Pubitemid 32847171)
9. Smith, K.J., Kapoor, R., Hall, S.M. & Davies, M. Electrically active axons degenerate when exposed to nitric oxide. Ann. Neurol. 49, 470-476 (2001) (Pubitemid 32281330)
10. Lo, A.C., Saab, C.J., Black, J.A. & Waxman, S.G. Phenytoin protects spinal cord axons and preserves axonal conduction and neurological function in a model of neuroinflammation in vivo. J. Neurophysiol. 90, 3566-3571 (2003) (Pubitemid 37430046)
11. Friese, M.A. et al. Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat. Med. 13, 1483-1489 (2007) (Pubitemid 350224241)
12. Mathey, E.K. et al. Neurofascin as a novel target for autoantibody-mediated axonal injury. J. Exp. Med. 204, 2363-2372 (2007) (Pubitemid 47529322)
13. Bittner, S. et al. TASK1 modulates inflammation and neurodegeneration in autoimmune inflammation of the central nervous system. Brain 132, 2501-2516 (2009)
14. Kerschensteiner, M., Schwab, M.E., Lichtman, J.W. & Misgeld, T. In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat. Med. 11, 572-577 (2005) (Pubitemid 40685982)
15. Misgeld, T. & Kerschensteiner, M. In vivo imaging of the diseased nervous system. Nat. Rev. Neurosci. 7, 449-463 (2006) (Pubitemid 44012285)
16. Bartholomäus, I. et al. Effector T cell interactions with meningeal vascular structure in nascent autoimmune CNS lesions. Nature 462, 94-98 (2009)
17. Siffrin, V. et al. In vivo imaging of partially reversible TH17 cell-induced neuronal dysfunction in the course of encephalomyelitis. Immunity 33, 424-436 (2010)
18. Feng, G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51 (2000)
19. Misgeld, T., Kerschensteiner, M., Bareyre, F.M., Burgess, R.W. & Lichtman, J.W. Imaging axonal transport of mitochondria in vivo. Nat. Methods 4, 559-561 (2007) (Pubitemid 47214773)
20. Singbartl, K. et al. A CD2-green fluorescence protein-transgenic mouse reveals very late antigen-4-dependent CD8+ lymphocyte rolling in inflamed venules. J. Immunol. 166, 7520-7526 (2001) (Pubitemid 32525631)
21. Jung, S. et al. Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20, 4106-4114 (2000) (Pubitemid 30314508)
22. Kapoor, R., Davies, M., Blaker, P.A., Hall, S.M. & Smith, K.J. Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann. Neurol. 53, 174-180 (2003) (Pubitemid 36163998)
23. Smith, K.J. & Lassmann, H. The role of nitric oxide in multiple sclerosis. Lancet Neurol. 1, 232-241 (2002) (Pubitemid 37159185)
24. Lin, M.T. & Beal, M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795 (2006) (Pubitemid 44622683)
25. Coleman, M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 6, 889-898 (2005) (Pubitemid 41568730)
26. Franklin, R.J. & Ffrench-Constant, C. Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9, 839-855 (2008)
27. Coman, I. et al. Nodal, paranodal and juxtaparanodal axonal proteins during demyelination and remyelination in multiple sclerosis. Brain 129, 3186-3195 (2006) (Pubitemid 44871435)
28. Aboul-Enein, F., Weiser, P., Höftberger, R., Lassmann, H. & Bradl, M. Transient axonal injury in the absence of demyelination: a correlate of clinical disease in acute experimental autoimmune encephalomyelitis. Acta Neuropathol. 111, 539-547 (2006) (Pubitemid 43778958)
29. Das Sarma, J., Kenyon, L.C., Hingley, S.T. & Shindler, K.S. Mechanisms of primary axonal damage in a viral model of multiple sclerosis. J. Neurosci. 29, 10272-10280 (2009)
30. Kroemer, G., Galluzzi, L. & Brenner, C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87, 99-163 (2007) (Pubitemid 46209992)
31. Dutta, R. et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann. Neurol. 59, 478-489 (2006) (Pubitemid 43358068)
32. Mahad, D., Ziabreva, I., Lassmann, H. & Turnbull, D. Mitochondrial defects in acute multiple sclerosis lesions. Brain 131, 1722-1735 (2008) (Pubitemid 351957459)
33. Mahad, D.J. et al. Mitochondrial changes within axons in multiple sclerosis. Brain 132, 1161-1174 (2009)
34. Forte, M. et al. Cyclophilin D inactivation protects axons in experimental autoimmune encephalomyelitis, an animal model of multiple sclerosis. Proc. Natl. Acad. Sci. USA 104, 7558-7563 (2007) (Pubitemid 47185945)
35. Du, H. et al. Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer′s disease. Nat. Med. 14, 1097-1105 (2008)
36. D'Autréaux, B. & Toledano, M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8, 813-824 (2007) (Pubitemid 47462134)
37. Hooper, D.C. et al. Uric acid, a peroxynitrite scavenger, inhibits CNS inflammation, blood-CNS barrier permeability changes and tissue damage in a mouse model of multiple sclerosis. FASEB J. 14, 691-698 (2000) (Pubitemid 30198568)
38. Kizelsztein, P., Ovadia, H., Garbuzenko, O., Sigal, A. & Barenholz, Y. Pegylated nanoliposomes remote-loaded with the antioxidant tempamibe ameliorate experimental autoimmune encephalomyelitis. J. Neuroimmunol. 213, 20-25 (2009)
39. Lipton, S.A. Pathologically activated therapeutics for neuroprotection. Nat. Rev. Neurosci. 8, 803-808 (2007). (Pubitemid 47462118)
40. Abdul-Majid, K.B. et al. Screening of several H-2 congenic mouse strains identified H-2(q) mice as highly susceptible to MOG-induced EAE with minimal adjuvant requirement. J. Neuroimmunol. 111, 23-33 (2000).