Experimental spinal cord injury: Wallerian degeneration in the dorsal column is followed by revascularization, glial proliferation, and nerve regeneration

Experimental Neurology

Volumn 147, Issue 1, 1997, Pages 159-171

  Zhang, Ziyin ^a,b   Guth, Lloyd ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b Asian and Middle Eastern Studies Program   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GLIA CELL; INFLAMMATORY INFILTRATE; MICROSCOPY; NERVE CRUSH; NERVE DEGENERATION; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY; VASCULARIZATION; WOUND HEALING;

EID: 0031239077     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1997.6590     Document Type: Article

References (63)

1. Aguayo A. J. Axonal regeneration from injured neurons in the adult mammalian central nervous system. Synaptic Plasticity. 1985;Guilford, New York. p. 457-484.
2. Balentine J. D. Pathology of experimental spinal cord trauma. I. The necrotic lesion as a function of vascular injury. Lab. Invest. 39:1978;236-253.
3. Bandtlow C. E., Schmidt M. F., Hassinger T. D., Schwab M. E., Kater S. B. Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones. Science. 259:1993;80-83.
4. Bartholdi D., Schwab M. E. Methylprednisolone inhibits early inflammatory processes but not ischemic cell death after experimental spinal cord lesion in the rat. Brain Res. 672:1995;177-186.
5. Blight A. R. Delayed demyelination and macrophage invasion: a candidate for secondary cell damage in spinal cord injury. Cent. Nerv. Syst. Trauma. 2:1985;299-315.
6. Blottner D., Baumgarten H. G. Neurotrophy and regeneration in vivo. Acta Anat. 150:1994;235-245.
7. Borgens R. B., Blight A. R., Murphy D. J., Stewart L. Transected dorsal column axons within the guinea pig spinal cord regenerate in the presence of an applied electric field. J. Comp. Neurol. 250:1986;168-180.
8. Bregman B. S., Kunkel-Bagden E., Schnell L., Dai H. N., Gao D., Schwab M. E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature. 378:1995;498-501.
9. Caroni P., Schwab M. E. Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron. 1:1988;85-96.
10. Das D. K. Cellular, biochemical and molecular aspects of reperfusion injury. Ann. N. Y. Acad. Sci. 723:1994;1-506.
11. de la Torre J. C., Boggan J. E. Neurophysiological recording in rat spinal cord trauma. Exp. Neurol. 70:1980;356-370.
12. de la Torre J. C., Goldsmith H. S. Increased blood flow enhances axon regeneration after spinal transection. Neurosci. Lett. 94:1988;269-273.
13. de la Torre J. C., Goldsmith H. S. Collagen-omental graft in experimental spinal cord transection. Acta Neurochir. 102:1990;152-163.
14. Demopoulos H. B., Flamm E. S., Pietronigro D. D., Sligmann M. L. The free radical pathology and the microcirculation in the major central nervous system disorders. Acta Physiol. Scand. Suppl. 492:1980;91-119.
15. Dingle J. T. Lysosomes: A Laboratory Handbook. 1972;Elsevier, New York.
16. Dusart I., Schwab M. E. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci. 6:1994;712-724.
17. Feringa E. R., Shuer L. M., Vahlsing H. L., Davis S. W. Regeneration of corticospinal axons in the rat. Ann. Neurol. 2:1977;315-321.
18. S. J. Comp. Neurol. 371:1996;469-484.
19. George R., Griffin J. Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: The dorsal radiculotomy model. Exp. Neurol. 129:1994;225-236.
20. Goetzl E. J., Lewis R. A., Lewis R. A., Rola-Pleszczynski M. Cellular generation, transport, and effects of eiconosoids. Ann. N.Y. Acad. Sci. 744:1994;1-340.
21. Goldsmith H. S., Steward E., Duckett S. Early application of pedicled omentum to the acutely traumatised spinal cord. Paraplegia. 23:1985;100-112.
22. Goldsmith H. S. Brain and spinal cord revascularization by omental transposition. Neurolog. Res. 16:1994;159-162.
23. Guth L., Barrett C. P., Donati E. J., Deshpande S. S., Albuquerque E. X. Histopathological reactions and axonal regeneration in the transected spinal cord of hibernating squirrels. J. Comp. Neurol. 203:1981;297-308.
24. Guth L., Zhang Z., Diprospero N. A., Joubin K., Fitch M. T. Spinal cord injury in the rat: Treatment with bacterial lipopolysaccharide and indomethacin enhances cellular repair and locomotor function. Exp. Neurol. 126:1994;76-87.
25. Guth L., Zhang Z., Roberts E. Key role for pregnenolone in combination therapy that promotes recovery after spinal cord injury. Proc. Natl. Acad. Sci. USA. 91:1994;12308-12312.
26. Hall E. D., Wolf D. L., Braughler J. M. Pathophysiology, consequences and pharmacological prevention of posttraumatic CNS ischemia. Gilad G. Processes of Recovery from Neural Trauma. 1986;63-73 Springer-Verlag, Berlin.
27. Hiraizumi Y., Transfeldt E. E., Kawahara N., Fiegel V. D., Knighton D., Sung J. H. The effect of growth factor formula (platelet derived wound healing formula) in experimental spinal cord injuries. J. Am. Paraplegia Soc. 15:1992;7-13.
28. Igarashi M., Strittmatter S. M., Vartanian T., Fishman M. C. Mediation by G proteins of signals that cause collapse of growth cones. Science. 259:1993;77-79.
29. Joosten E. A., Gribnau A. A. Astrocytes and guidance of outgrowing corticospinal tract axons in the rat. An immunocytochemical study using anti-vimentin and anti-glial fibrillary acidic protein. Neuroscience. 31:1989;439-452.
30. Joosten E. A., Schuitman R. L., Vermelis M. E., Dederen P. J. Postnatal development of the ipsilateral corticospinal component in rat spinal cord: A light and electron microscopic anterograde HRP study. J. Comp. Neurol. 326:1992;133-146.
31. Joosten E. A. Developmental expression of N-CAM epitopes in the rat spinal cord during corticospinal tract axon outgrowth and target innervation. Brain Res. 78:1994;226-236.
32. Knighton D. R., Ciresi K. F., Fiegel V. D., Austin L. L., Butler E. L. Classification and treatment of chronic nonhealing platelet-derived wound healing factors (PDWHF). Ann. Surg. 204:1986;322-329.
33. Knighton D. R., Ciresi K. F., Fiegel V. D., Schumerth S., Butler E. L., Cerra F. Stimulation of repair in chronic nonhealing cutaneous ulcers using platelet-derived wound healing formula. Surg. Gynecol. Obstet. 170:1990;56-60.
34. Linowiecki A. J. The comparative anatomy of the pyramidal tract. J. Comp. Neurol. 24:1914;509-530.
35. Lotan M., Schwartz M. Cross talk between the immune system and the nervous system in response to injury: Implications for regeneration. FASEB J. 8:1994;1026-1033.
36. Lowry O. H., Passonneau J. V., Hasselberger F. X., Schulz D. W. Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain. J. Biol. Chem. 239:1964;18-31.
37. Meyer M., Matsuoka I., Wetmore C., Olson L., Thoenen H. Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J. Cell Biol. 119:1992;45-54.
38. Miller C., Tsatas O., David S. Dibutyryl cAMP, interleukin-1b, and macrophage conditioned medium enhance the ability of astrocytes to promote neurite growth. J. Neurosci. Res. 38:1994;56-63.
39. Nathan C. F. Secretory products of macrophages. J. Clin. Invest. 79:1987;319-326.
40. Perry V. H., Brown M. C., Gordon S. The macrophage response to central and peripheral nerve injury: A possible role for macrophages in regeneration. J. Exp. Med. 165:1987;1218-1223.
41. Perry V. H., Lunn E. R., Brown M. C., Cahusac S., Gordon S. Evidence that the rate of Wallerian degeneration is controlled by a single autosomal dominant gene. Eur. J. Neurosci. 2:1990;408-413.
42. Perry V. H., Brown M. C., Lunn E. R., Tree P., Gordon S. Evidence that very slow Wallerian degeneration in C57BL/Ola mice is an intrinsic property of the peripheral nerve. Eur. J. Neurosci. 2:1990;802-808.
43. Perry V. H., Brown M. C., Lunn E. R. Very slow retrograde and Wallerian degeneration in the CNS of C57BL/Ola mice. Eur. J. Neurosci. 3:1991;102-105.
44. Perry V. H., Brown M. C. Macrophages and nerve regeneration. Curr. Opin. Neurobiol. 2:1992;679-682.
45. Peruche B., Krieglstein J. Mechanisms of drug actions against neuronal damage caused by ischemia - An overview. Prog. Neuropsychopharmacol. Biol. Psychiatr. 17:1993;21-70.
46. Pippenger M. A., Sims T. J., Gilmore S. A. Development of the rat corticospinal tract through an altered glial environment. Brain Res. 55:1990;43-50.
47. Ramon y Cajal S. Degeneration and Regeneration of the Nervous System. 1913;Oxford Univ. Press, London.
48. Rappolee D. A., Mark D., Banda M. J., Werb Z. Wound macrophages express TGF-a and other growth factors in vivo. Analysis by mRNA phenotyping. Science. 241:1988;708-712.
49. Rivlin A. S., Tator C. H. Regional spinal cord blood flow in rats after severe cord trauma. J. Neurosurg. 49:1978;844-853.
50. Schnell L., Schwab M. E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature. 343:1990;269-272.
51. Silver J., Ogawa M. Y. Postnatally induced formation of the corpus callosum in acallosal mice on glia-coated cellulose bridges. Science. 220:1983;1067-1069.
52. Smith G. M., Miller R. H., Silver J. Changing role of forebrain astrocytes during development, regenerative failure and induced regeneration upon transplantation. J. Comp. Neurol. 251:1986;23-43.
53. Sporn M. B., Roberts A. B. Peptide Growth Factors and Their Receptors. 1990;Springer-Verlag, Berlin.
54. Stanfield B. B. The corticospinal tract attains a normal configuration in the absence of myelin: observations in jimpy mutant mice. Neuron. 7:1991;249-256.
55. Sussman M. S., Bulkley G. B. Oxygen-derived free radicals in reperfusion injury. Packer L., Glazer A. N. Methods in Enzymology: Oxygen Radicals in Biological Systems. 1990;711-723 Academic Press, San Diego.
56. Tator C. H., Fehlings M. G. Review of the secondary injury theory of spinal cord trauma with emphasis on vascular mechanisms. J. Neurosurg. 75:1991;15-26.
57. Terashima T., Ochiishi T., Yamauchi T. Immunohistochemical detection of calcium/calmodulin-dependent protein kinase II in the spinal cord of the rat and monkey with special reference to the corticospinal tract. J. Comp. Neurol. 340:1994;469-479.
58. The'ry C., Chamak B., Mallat M. Cytotoxic effect of brain macrophages on developing neurons. Eur. J. Neurosci. 3:1991;1155-1164.
59. West N. R., Collins G. H. Relationship of Wallerian degeneration to regrowing axons. J. Neuropathol. Exp. Neurol. 50:1991;693-703.
60. Windle W. F. Regeneration of axons in the vertebrate central nervous system. Physiol. Rev. 36:1956;427-440.
61. s. J. Comp. Neurol. 371:1996;485-495.
62. Zhang Z., Guth L. Revascularization, wound healing and nerve regeneration in lesion caused by Wallerian degeneration after spinal cord injury. FASEB J. 10:1996;A130.
63. Zhang Z., Krebs C., Guth L. Experimental analysis of progressive necrosis after spinal cord trauma in the rat: The etiological role of inflammatory responses. Exp. Neurol. 143:1997.