Functional recovery of callosal axons following demyelination: a critical window

Neuroscience

Volumn 164, Issue 4, 2009, Pages 1407-1421

  Crawford, D K ^a   Mangiardi, M ^a   Xia, X ^a   Lopez Valdes H E ^a   Tiwari Woodruff, S K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

action potential; axon damage; neurodegeneration; nodal proteins; remyelination

Indexed keywords

CUPRIZONE; MYELIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DISEASE; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATION; DISEASE COURSE; FEMALE; FUNCTIONAL DISEASE; MOUSE; NERVE CONDUCTION; NERVE FIBER; NERVE REGENERATION; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; RANVIER NODE; REMYELINIZATION;

ACTION POTENTIALS; ANIMALS; ASTROCYTES; AXONS; CELL ADHESION MOLECULES, NEURONAL; CELL LINEAGE; CORPUS CALLOSUM; CUPRIZONE; DIET; FEMALE; KV1.2 POTASSIUM CHANNEL; MICE; MICE, TRANSGENIC; MICROGLIA; MYELIN SHEATH; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; RANVIER'S NODES; REGENERATION; SODIUM CHANNELS;

EID: 70449528528     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.09.069     Document Type: Article

References (55)

1. Armstrong R.C., Le T.Q., Flint N.C., Vana A.C., and Zhou Y.X. Endogenous cell repair of chronic demyelination. J Neuropathol Exp Neurol 65 (2006) 245-256
2. Arnett H.A., Mason J., Marino M., Suzuki K., Matsushima G.K., and Ting J.P. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 4 (2001) 1116-1122
3. Arroyo E.J., Sirkowski E.E., Chitale R., and Scherer S.S. Acute demyelination disrupts the molecular organization of peripheral nervous system nodes. J Comp Neurol 479 (2004) 424-434
4. Bando Y., Takakusaki K., Ito S., Terayama R., Kashiwayanagi M., and Yoshida S. Differential changes in axonal conduction following CNS demyelination in two mouse models. Eur J Neurosci 28 (2008) 1731-1742
5. Bhat M.A., Rios J.C., Lu Y., Garcia-Fresco G.P., Ching W., St. Martin M., Li J., Einheber S., Chesler M., Rosenbluth J., Salzer J.L., and Bellen H.J. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30 (2001) 369-383
6. Blakemore W.F. Observations on oligodendrocyte degeneration, the resolution of status spongiosus and remyelination in cuprizone intoxication in mice. J Neurocytol 1 (1972) 413-426
7. Blakemore W.F., and Franklin R.J. Remyelination in experimental models of toxin-induced demyelination. Curr Top Microbiol Immunol 318 (2008) 193-212
8. Chang A., Nishiyama A., Peterson J., Prineas J., and Trapp B.D. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20 (2000) 6404-6412
9. Chang A., Tourtellotte W.W., Rudick R., and Trapp B.D. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 346 (2002) 165-173
10. Coman I., Aigrot M.S., Seilhean D., Reynolds R., Girault J.A., Zalc B., and Lubetzki C. Nodal, paranodal and juxtaparanodal axonal proteins during demyelination and remyelination in multiple sclerosis. Brain 129 (2006) 3186-3195
11. Craner M.J., Kataoka Y., Lo A.C., Black J.A., Baker D., and Waxman S.G. Temporal course of upregulation of Na(v)1.8 in Purkinje neurons parallels the progression of clinical deficit in experimental allergic encephalomyelitis. J Neuropathol Exp Neurol 62 (2003) 968-975
12. Craner M.J., Newcombe J., Black J.A., Hartle C., Cuzner M.L., and Waxman S.G. Molecular changes in neurons in multiple sclerosis: altered axonal expression of Nav12 and Nav16 sodium channels and Na+/Ca2+ exchanger. Proc Natl Acad Sci U S A 101 (2004) 8168-8173
13. Crawford D.K., Mangiardi M., and Tiwari-Woodruff S.K. Assaying the functional effects of demyelination and remyelination: revisiting field potential recordings. J Neurosci Methods 182 (2009) 25-33
14. Einheber S., Bhat M.A., and Salzer J.L. Disrupted Axo-glial junctions result in accumulation of abnormal mitochondria at nodes of Ranvier. Neuron Glia Biol 2 (2006) 165-174
15. Evangelou N., Esiri M.M., Smith S., Palace J., and Matthews P.M. Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis. Ann Neurol 47 (2000) 391-395
16. Foster R.E., Kocsis J.D., Malenka R.C., and Waxman S.G. Lysophosphatidyl choline-induced focal demyelination in the rabbit corpus callosum. Electron-microscopic observations. J Neurol Sci 48 (1980) 221-231
17. Franklin K., and Paxinos G. The mouse brain. Stereotaxic coordinates (2001), Academic Press, San Diego, CA
18. Franklin R.J. Why does remyelination fail in multiple sclerosis?. Nat Rev Neurosci 3 (2002) 705-714
19. Fuss B., Afshari F.S., Colello R.J., and Macklin W.B. Normal CNS myelination in transgenic mice overexpressing MHC class I H-2L(d) in oligodendrocytes. Mol Cell Neurosci 18 (2001) 221-234
20. Groebe A., Clarner T., Baumgartner W., Dang J., Beyer C., and Kipp M. Cuprizone treatment induces distinct demyelination, astrocytosis, and microglia cell invasion or proliferation in the mouse cerebellum. Cerebellum 8 (2009) 163-174
21. Gudi V., Moharregh-Khiabani D., Skripuletz T., Koutsoudaki P.N., Kotsiari A., Skuljec J., Trebst C., and Stangel M. Regional differences between grey and white matter in cuprizone induced demyelination. Brain Res 1283 (2009) 127-138
22. Harsan L.A., Steibel J., Zaremba A., Agin A., Sapin R., Poulet P., Guignard B., Parizel N., Grucker D., Boehm N., Miller R.H., and Ghandour M.S. Recovery from chronic demyelination by thyroid hormone therapy: myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J Neurosci 28 (2008) 14189-14201
23. Hiremath M.M., Saito Y., Knapp G.W., Ting J.P., Suzuki K., and Matsushima G.K. Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice. J Neuroimmunol 92 (1998) 38-49
24. Iocca H.A., Plant S.R., Wang Y., Runkel L., O'Connor B.P., Lundsmith E.T., Hahm K., van Deventer H.W., Burkly L.C., and Ting J.P. TNF superfamily member TWEAK exacerbates inflammation and demyelination in the cuprizone-induced model. J Neuroimmunol 194 (2008) 97-106
25. Irvine K.A., and Blakemore W.F. Remyelination protects axons from demyelination-associated axon degeneration. Brain 131 (2008) 1464-1477
26. Islam M.S., Tatsumi K., Okuda H., Shiosaka S., and Wanaka A. Olig2-expressing progenitor cells preferentially differentiate into oligodendrocytes in cuprizone-induced demyelinated lesions. Neurochem Int 54 (2009) 192-198
27. Kotter M.R., Zhao C., van Rooijen N., and Franklin R.J. Macrophage-depletion induced impairment of experimental CNS remyelination is associated with a reduced oligodendrocyte progenitor cell response and altered growth factor expression. Neurobiol Dis 18 (2005) 166-175
28. Koutsoudaki P.N., Skripuletz T., Gudi V., Moharregh-Khiabani D., Hildebrandt H., Trebst C., and Stangel M. Demyelination of the hippocampus is prominent in the cuprizone model. Neurosci Lett 451 (2009) 83-88
29. Kutzelnigg A., and Lassmann H. Cortical lesions and brain atrophy in MS. J Neurol Sci 233 (2005) 55-59
30. Lassmann H., Bruck W., Lucchinetti C., and Rodriguez M. Remyelination in multiple sclerosis. Mult Scler 3 (1997) 133-136
31. Lindner M., Fokuhl J., Linsmeier F., Trebst C., and Stangel M. Chronic toxic demyelination in the central nervous system leads to axonal damage despite remyelination. Neurosci Lett 453 (2009) 120-125
32. Lindner M., Heine S., Haastert K., Garde N., Fokuhl J., Linsmeier F., Grothe C., Baumgartner W., and Stangel M. Sequential myelin protein expression during remyelination reveals fast and efficient repair after central nervous system demyelination. Neuropathol Appl Neurobiol 34 (2008) 105-114
33. Mallon B.S., Shick H.E., Kidd G.J., and Macklin W.B. Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci 22 (2002) 876-885
34. Mason J.L., Toews A., Hostettler J.D., Morell P., Suzuki K., Goldman J.E., and Matsushima G.K. Oligodendrocytes and progenitors become progressively depleted within chronically demyelinated lesions. Am J Pathol 164 (2004) 1673-1682
35. Mathis C., Denisenko-Nehrbass N., Girault J.A., and Borrelli E. Essential role of oligodendrocytes in the formation and maintenance of central nervous system nodal regions. Development 128 (2001) 4881-4890
36. Matsushima G.K., and Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 11 (2001) 107-116
37. Morales L.B., Loo K.K., Liu H.B., Peterson C., Tiwari-Woodruff S., and Voskuhl R.R. Treatment with an estrogen receptor alpha ligand is neuroprotective in experimental autoimmune encephalomyelitis. J Neurosci 26 (2006) 6823-6833
38. Mutsaers S.E., and Carroll W.M. Focal accumulation of intra-axonal mitochondria in demyelination of the cat optic nerve. Acta Neuropathol 96 (1998) 139-143
39. Norkute A., Hieble A., Braun A., Johann S., Clarner T., Baumgartner W., Beyer C., and Kipp M. Cuprizone treatment induces demyelination and astrocytosis in the mouse hippocampus. J Neurosci Res 87 (2009) 1343-1355
40. Plant S.R., Iocca H.A., Wang Y., Thrash J.C., O'Connor B.P., Arnett H.A., Fu Y.X., Carson M.J., and Ting J.P. Lymphotoxin beta receptor (Lt betaR): dual roles in demyelination and remyelination and successful therapeutic intervention using Lt betaR-Ig protein. J Neurosci 27 (2007) 7429-7437
41. Preston R.J., Waxman S.G., and Kocsis J.D. Effects of 4-aminopyridine on rapidly and slowly conducting axons of rat corpus callosum. Exp Neurol 79 (1983) 808-820
42. Rasband M.N., Trimmer J.S., Schwarz T.L., Levinson S.R., Ellisman M.H., Schachner M., and Shrager P. Potassium channel distribution, clustering, and function in remyelinating rat axons. J Neurosci 18 (1998) 36-47
43. Reeves T.M., Phillips L.L., and Povlishock J.T. Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Exp Neurol 196 (2005) 126-137
44. Rovaris M., Gambini A., Gallo A., Falini A., Ghezzi A., Benedetti B., Sormani M.P., Martinelli V., Comi G., and Filippi M. Axonal injury in early multiple sclerosis is irreversible and independent of the short-term disease evolution. Neurology 65 (2005) 1626-1630
45. Selmaj K., Brosnan C.F., and Raine C.S. Colocalization of lymphocytes bearing gamma Delta T-cell receptor and heat shock protein hsp65+ oligodendrocytes in multiple sclerosis. Proc Natl Acad Sci U S A 88 (1991) 6452-6456
46. Skripuletz T, Bussmann JH, Gudi V, Koutsoudaki PN, Pul R, Moharregh-Khiabani D, Lindner M, Stangel M (in press) Cerebellar cortical demyelination in the murine cuprizone model. Brain Pathol, in press.
47. Skripuletz T., Lindner M., Kotsiari A., Garde N., Fokuhl J., Linsmeier F., Trebst C., and Stangel M. Cortical demyelination is prominent in the murine cuprizone model and is strain-dependent. Am J Pathol 172 (2008) 1053-1061
48. Song S.K., Yoshino J., Le T.Q., Lin S.J., Sun S.W., Cross A.H., and Armstrong R.C. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26 (2005) 132-140
49. Stidworthy M.F., Genoud S., Suter U., Mantei N., and Franklin R.J. Quantifying the early stages of remyelination following cuprizone-induced demyelination. Brain Pathol 13 (2003) 329-339
50. Tiwari-Woodruff S., Beltran-Parrazal L., Charles A., Keck T., Vu T., and Bronstein J. K+ channel KV31 associates with OSP/claudin-11 and regulates oligodendrocyte development. Am J Physiol Cell Physiol 291 (2006) C687-C698
51. Tiwari-Woodruff S., Morales L.B., Lee R., and Voskuhl R.R. Differential neuroprotective and antiinflammatory effects of estrogen receptor (ER)alpha and ERbeta ligand treatment. Proc Natl Acad Sci U S A 104 (2007) 14813-14818
52. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., and Bo L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338 (1998) 278-285
53. Waxman S.G., and Ritchie J.M. Organization of ion channels in the myelinated nerve fiber. Science 228 (1985) 1502-1507
54. Williams A., Piaton G., Aigrot M.S., Belhadi A., Theaudin M., Petermann F., Thomas J.L., Zalc B., and Lubetzki C. Semaphoring 3A and 3F: key players in myelin repair in multiple sclerosis?. Brain 130 (2007) 2554-2565
55. Wolswijk G. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 125 (2002) 338-349