Axonal thinning and extensive remyelination without chronic demyelination in spinal injured rats

Journal of Neuroscience

Volumn 32, Issue 15, 2012, Pages 5120-5125

  Powers, Berit E ^a   Lasiene, Jurate ^a   Plemel, Jason R ^b   Shupe, Larry ^a   Perlmutter, Steve I ^a   Tetzlaff, Wolfram ^b   Horner, Philip J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEMYELINATION; FEMALE; IMMUNOHISTOCHEMISTRY; MATHEMATICAL MODEL; NERVE CONDUCTION; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL TRACT; RAT; REMYELINIZATION; RUBROSPINAL TRACT; SPINAL CORD INJURY;

ANIMALS; AXONS; CERVICAL VERTEBRAE; CONTUSIONS; DEMYELINATING DISEASES; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MYELIN SHEATH; NEURAL CONDUCTION; PYRAMIDAL TRACTS; RABBITS; RATS; SOFTWARE; SPINAL CORD INJURIES; THORACIC VERTEBRAE;

EID: 84859552165     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0002-12.2012     Document Type: Article

References (47)

1. Balentine JD (1978) Pathology of experimental spinal cord trauma. I. The necrotic lesion as a function of vascular injury. Lab Invest 39:236-253.
2. Biernaskie J, Sparling JS, Liu J, Shannon CP, Plemel JR, Xie Y, Miller FD, Tetzlaff W (2007) Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci 27:9545-9559.
3. Bjartmar C, Yin X, Trapp BD (1999) Axonal pathology in myelin disorders. J Neurocytol 28:383-395.
4. Blight AR (1983) Axonal physiology of chronic spinal cord injury in the cat: intracellular recording in vitro. Neuroscience 10:1471-1486.
5. Blight AR (1985) Delayed demyelination and macrophage invasion: a candidate for secondary cell damage in spinal cord injury. Cent Nerv Syst Trauma 2:299-315.
6. Blight AR (1991) Morphometric analysis of a model of spinal cord injury in guinea pigs, with behavioral evidence of delayed secondary pathology. J Neurol Sci 103:156-171.
7. Blight AR, Decrescito V (1986) Morphometric analysis of experimental spinal cord injury in the cat: the relation of injury intensity to survival of myelinated axons. Neuroscience 19:321-341.
8. Blight AR, Young W (1989) Central axons in injured cat spinal cord recover electrophysiological function following remyelination by Schwann cells. J Neurol Sci 91:15-34.
9. Bostock H, Sears TA (1976) Continuous conduction in demyelinated mammalian nerve fibers. Nature 263:786-787.
10. Bostock H, Sherratt RM, Sears TA (1978) Overcoming conduction failure in demyelinated nerve fibres by prolonging action potentials. Nature 274:385-387.
11. Brady ST, Witt AS, Kirkpatrick LL, de Waegh SM, Readhead C, Tu PH, Lee VM (1999) Formation of compact myelin is required for maturation of the axonal cytoskeleton. J Neurosci 19:7278-7288.
12. Bunge MB, Bunge RP, Ris H (1961) Ultrastructural study of remyelination in an experimental lesion in adult cat spinal cord. J Biophys Biochem Cytol 10:67-94.
13. Chomiak T, Hu B (2009) What is the optimal value of the g-ratio for myelinated fibers in the rat CNS? A theoretical approach. PLoS One 4:e7754.
14. Coleman MP, Perry VH (2002) Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci 25:532-537.
15. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS (1997) Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3:73-76.
16. de Waegh SM, Lee VM, Brady ST (1992) Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell 68:451-463.
17. Gensel JC, Tovar CA, Hamers FP, Deibert RJ, Beattie MS, Bresnahan JC (2006) Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J Neurotrauma 23:36-54.
18. Gledhill RF, McDonald WI (1977) Morphological characteristics of central demyelination and remyelination: a single-fiber study. Ann Neurol 1:552-560.
19. Gledhill RF, Harrison BM, McDonald WI (1973a) Demyelination and remyelination after acute spinal cord compression. Exp Neurol 38:472-487.
20. Gledhill RF, Harrison BM, McDonald WI (1973b) Pattern of remyelination in the CNS. Nature 244:443-444.
21. Griffiths IR, McCulloch MC (1983) Nerve fibres in spinal cord impact injuries. Part 1. Changes in the myelin sheath during the initial 5 weeks. J Neurol Sci 58:335-349.
22. Guest JD, Hiester ED, Bunge RP (2005) Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp Neurol 192:384-393.
23. Guízar-Sahagún G, Grijalva I, Salgado-Ceballos H, Espitia A, Orozco S, Ibarra A, Martínez A, Franco-Bourland RE, Madrazo I (2004) Spontaneous and induced aberrant sprouting at the site of injury is irrelevant to motor function outcome in rats with spinal cord injury. Brain Res 1013:143-151.
24. Harrington EP, Zhao C, Fancy SP, Kaing S, Franklin RJ, Rowitch DH (2010) Oligodendrocyte PTEN is required for myelin and axonal integrity, not remyelination. Ann Neurol 68:703-716.
25. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
26. Hsieh ST, Kidd GJ, Crawford TO, Xu Z, Lin WM, Trapp BD, Cleveland DW, Griffin JW (1994) Regional modulation of neurofilament organization by myelination in normal axons. J Neurosci 14:6392-6401.
27. Inman DM, Steward O (2003) Physical size does not determine the unique histopathological response seen in the injured mouse spinal cord. J Neurotrauma 20:33-42.
28. Irvine KA, Blakemore WF (2008) Remyelination protects axons from demyelination-associated axon degeneration. Brain 131:1464-1477.
29. Kakulas BA (1999) A review of the neuropathology of human spinal cord injury with emphasis on special features. J Spinal Cord Med 22:119-124.
30. Karimi-Abdolrezaee S, Eftekharpour E, Fehlings MG (2004) Temporal and spatial patterns of Kv1.1 and Kv1.2 protein and gene expression in spinal cord white matter after acute and chronic spinal cord injury in rats: implications for axonal pathophysiology after neurotrauma. Eur J Neurosci 19:577-589.
31. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, Griffiths IR, Nave KA (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33:366-374.
32. Lasiene J, Shupe L, Perlmutter S, Horner P (2008) No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. J Neurosci 28:3887-3896.
33. McDonald WI (1975) Mechanisms of functional loss and recovery in spinal cord damage. Ciba Found Symp 34:23-33.
34. McDonald WI, Ohlrich GD (1971) Quantitative anatomical measurements on single isolated fibres from the cat spinal cord. J Anat 110:191-202.
35. Mclntyre CC, Richardson AG, Grill WM (2002) Modeling the excitability of mammalian nerve fibers: influence of afterpotentials on the recovery cycle. J Neurophysiol 87:995-1006.
36. Nashmi R, Fehlings MG (2001) Changes in axonal physiology and morphology after chronic compressive injury of the rat thoracic spinal cord. Neuroscience 104:235-251.
37. Nashmi R, Jones OT, Fehlings MG (2000) Abnormal axonal physiology is associated with altered expression and distribution of Kv1.1 and Kv1.2 K+channels after chronic spinal cord injury. Eur J Neurosci 12:491-506.
38. Nave KA (2010) Myelination and support of axonal integrity by glia. Nature 468:244-252.
39. Pohl HB, Porcheri C, Mueggler T, Bachmann LC, Martino G, Riethmacher D, Franklin RJ, Rudin M, Suter U (2011) Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J Neurosci 31:1069-1080.
40. Rabchevsky AG, Sullivan PG, Scheff SW (2007) Temporal-spatial dynamics in oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury. Glia 55:831-843.
41. Sánchez I, Hassinger L, Paskevich PA, Shine HD, Nixon RA (1996) Oligodendroglia regulate the regional expansion of axon caliber and local accumulation of neurofilaments during development independently of myelin formation. J Neurosci 16:5095-5105.
42. Smith PM, Jeffery ND (2006) Histological and ultrastructural analysis of white matter damage after naturally-occurring spinal cord injury. Brain Pathol 16:99-109.
43. Soblosky JS, Song JH, Dinh DH (2001) Graded unilateral cervical spinal cord injury in the rat: evaluation of forelimb recovery and histological effects. Behav Brain Res 119:1-13.
44. Tom VJ, Steinmetz MP, Miller JH, Doller CM, Silver J (2004) Studies on the development and behavior of the dystrophic growth cone, the hallmark of regeneration failure, in an in vitro model of the glial scar and after spinal cord injury. J Neurosci 24:6531-6539.
45. Totoiu MO, Keirstead HS (2005) Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol 486:373-383.
46. Waxman SG (1980) Determinants of conduction velocity in myelinated nerve fibers. Muscle Nerve 3:141-150.
47. Waxman SG (1989) Demyelination in spinal cord injury. J Neurol Sci 91:1-14.