Ascending sensory, but not other long-tract axons, regenerate into the connective tissue matrix that forms at the site of a spinal cord injury in mice

Journal of Comparative Neurology

Volumn 462, Issue 4, 2003, Pages 431-449

  Inman, Denise M ^a,b   Steward, Oswald ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Ascending sensory pathways; Corticospinal tract; Mice; Regeneration; Reticulospinal tract; Rubrospinal tract; Spinal cord injury; Sprouting; Wound healing

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CHONDROITIN SULFATE; DEXTRAN; NEUROFILAMENT PROTEIN; PROTEOGLYCAN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONNECTIVE TISSUE; CONTROLLED STUDY; CRUSH TRAUMA; EXTRACELLULAR MATRIX; FEMALE; IMMUNOHISTOCHEMISTRY; MESENCEPHALON; MOTOR CORTEX; MOUSE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RETICULOSPINAL TRACT; RUBROSPINAL TRACT; SENSORY NERVE; SPINAL CORD INJURY; SPINAL GANGLION; WOUND HEALING;

ANIMALS; AXONS; CALCITONIN GENE-RELATED PEPTIDE; CONNECTIVE TISSUE; FEMALE; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MESENCEPHALON; MICE; MICE, INBRED C57BL; MOTOR CORTEX; NERVE REGENERATION; NEURAL PATHWAYS; NEUROFILAMENT PROTEINS; PROTEOCHONDROITIN SULFATES; PYRAMIDAL TRACTS; SEROTONIN; SPINAL CORD; SPINAL CORD INJURIES;

EID: 0038460895     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10768     Document Type: Article

References (40)

1. Anderson EG. 1983. The serotonin system of the spinal cord. In: Davidoff RS, editor. Handbook of the spinal cord. New York: Marcel Dekker. p 241-274.
2. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, Faden AI, Hsu CY, Noble LJ, Salzman S, Young W. 1997. Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148:453-463.
3. Bovolenta P, Wandosell F, Nieto-Sampedro M. 1992a. Central neurite outgrowth over glial scar tissue in vitro. In: Letourneau PC, Macagno ER, editors. The nerve growth cone. New York: Raven Press. p 477-488.
4. Bovolenta P, Wandosell F, Nieto-Sampedro M. 1992b. CNS glial scar tissue: a source of molecules which inhibit central neurite outgrowth. In: Waxman SG, eEditor. Progress in brain research. New York: Elsevier Science Publishers. p 367-379.
5. Bunge RP. 1994 Clinical implications of recent advances in neurotrauma research. In: Salzman SA, Faden AI, editors. The neurobiology of CNS trauma. New York: Oxford University Press. p 329-339.
6. Chung K, Lee WT, Carlton SM. 1988. The effects of dorsal rhizotomy and spinal cord isolation on calcitonin gene-related peptide-labeled terminals in the rat lumbar dorsal horn. Neurosci Lett 90:27-32.
7. Chung K, Lee WT, Park MJ. 1993. Spinal projections of pelvic visceral afferents of the rat: a calcitonin gene-related peptide (CGRP) immunohistochemical study. J Comp Neurol 337:63-69.
8. Davies SJ, Goucher DR, Doller C, Silver J. 1999. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822.
9. Deckner M, Lindholm T, Cullheim S, Risling M. 2000. Differential expression of tenascin-c, tenascin-r, tenascin/J1, and tenascin-x in spinal cord scar tissue and in the olfactory system. Exp Neurol 166:350-362.
10. Dou CL, Levine JM. 1994. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 14:7616-7628.
11. Du S, Rubin A, Klepper S, Barrett C, Kim YC, Rhim HW, Lee EB, Park CW, Markelonis GJ, Oh TH. 1999. Calcium influx and activation of calpain I mediate acute reactive gliosis in injured spinal cord. Exp Neurol 157:96-105.
12. Edwards SB. 1975. Autoradiographic studies of the midbrain reticular formation: descending projections of nucleus cuneiformis. J Comp Neurol 161:341-358.
13. Fidler PS, Schuette K, Asher RA, Dobbertin A, Thornton SR, Calle-Patino Y, Muir E, Levine JM, Geller HM, Rogers JH, Faissner A, Fawcett JW. 1999. Comparing astrocytic cell lines that are inhibitory or permissive for axon growth: the major axon-inhibitory proteoglycan is NG2. J Neurosci 19:8778-8788.
14. Fishman PS, Kelly JP. 1984. The fate of severed corticospinal axons. Neurology 34:1161-1167.
15. Fitch MT, Silver J. 1997. Activated macrophages and the blood-brain barrier: inflammation after CNS injury leads to increases in putative inhibitory molecules. Exp Neurol 148:587-603.
16. s) that causes delayed Wallerian degeneration. J Comp Neurol 371:469-484.
17. Gibson SJ, Polak JM, Bloom SR, Sabate IM, Mulderry PM, Ghatei MA, McGregor GP, Morrison IM, Kelly JS, Evans RM, Rosenfeld MG. 1984. Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 4:3101-3111.
18. Guest JD, Hesse D, Schnell L, Schwab ME, Bunge MB, Bunge RP. 1997. Influence of IN-1 antibody and acidic FGF-fibrin glue on the response of injured corticospinal tract axons to human Schwann cell grafts. J Neurosci Res 50:888-905.
19. Hill CE, Beattie MS, Bresnahan JC. 2001. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol 171:153-169.
20. Houweling DA, Lankhorst AJ, Gispen WH, Baer PR, Joosten EAJ. 1998. Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partical functional recovery. Exp Neurol 153:49-59.
21. Jin Y, Tessler A, Fischer I, Houle JD. 2000. Fibroblasts genetically modified to produce BDNF support regrowth of chronically injured serotonergic axons. Neurorehabil Neural Repair 14:311-317.
22. Krenz NR, Weaver LC. 1998. Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience 85:443-458.
23. Labrador RO, Buti M, Navarro X. 1998. Influence of collagen and laminin gels concentration on nerve regeneration after resection and tube repair. Exp Neurol 149:243-252.
24. Ma M, Basso DM, Walters P, Stokes BT, Jakeman LB. 2001. Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse. Exp Neurol 169:239-254.
25. Marchand R, Woerly S, Bertrand L, Valdes N. 1993. Evaluation of two cross-linked collagen gels implanted in the transected spinal cord. Brain Res Bull 30:415-422.
26. Martin P. 1997. Wound healing - aiming for perfect skin regeneration. Science 276:75-81.
27. McKeon RJ, Hoke A, Silver J. 1995. Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 136:32-43.
28. Newton BW, Hamill RW. 1988. The morphology and distribution of rat serotonergic intraspinal neurons: an immunohistochemical study. Brain Res Bull 20:349-360.
29. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI. 2002. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34:885-893.
30. Pasterkamp RJ, Giger RJ, Ruitenberg M-J, Holtmaat AJGD, Wit JD, Winter FD, Verhaagen J. 1999. Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol Cell Neurosci 13:143-166.
31. Powell EM, Fawcett JW, Geller HM. 1997. Proteoglycans provide neurite guidance at an astrocyte boundary. Mol Cell Neurosci 10:27-42.
32. Qiu 0J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT. 2002. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903.
33. Saruhashi Y, Young W, Perkins R. 1996. The recovery of 5-HT immunoreactivity in lumbosacral spinal cord and locomotor function after thoracic hemisection. Exp Neurol 139:203-213.
34. Schnell L, Fearn S, Klassen H, Schwab ME, Perry VH. 1999. Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur J Neurosci 11:3648-3658.
35. Smith GM, Hale JH. 1997. Macrophage/microglia regulation of astrocytic tenascin: synergistic action of transforming growth factor-beta and basic fibroblast growth factor. J Neurosci 17:9624-9633.
36. Stadelmann WK, Digenis AG, Tobin GR. 1998. Physiology and healing dynamics of chronic cutaneous wounds. Am J Surg 176 (2A suppl):26S-38S.
37. Steward O. 1989. Reorganization of neuronal connections following CNS trauma: principles and experimental paradigms. J Neurotrauma 6:99-152.
38. Tobin GR. 1984. Studies of mesenchymal healing processes in central nervous system wounds. J Am Paraplegia Soc 7:49-51.
39. von Euler M, Janson AM, Larsen JO, Seiger A, Forno L, Bunge MB, Sundstrom E. 2002. Spontaneous axonal regeneration in rodent spinal cord after ischemic injury. J Neuropathol Exp Neurol 61:64-75.
40. s) that causes delayed Wallerian degeneration. J Comp Neurol 371:485-495.