Axonal regeneration of Clarke's neurons beyond the spinal cord injury scar after treatment with chondroitinase ABC

Experimental Neurology

Volumn 182, Issue 1, 2003, Pages 160-168

  Yick, Leung Wah ^a   Cheung, Pik To ^a   So, Kwok Fai ^a   Wu, Wutian ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Axotomy; Chondroitin sulfate; Proteoglycans; Regrowth; Spinal cord; Traumatic injury

Indexed keywords

CHONDROITIN ABC LYASE; DYE; EPITOPE; PROTEOCHONDROITIN SULFATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CERVICAL SPINAL CORD; CONTROLLED STUDY; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; FEMALE; IMMUNOREACTIVITY; NERVE CELL PLASTICITY; NERVE FIBER REGENERATION; NERVE REGENERATION; NEWBORN; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; RAT; SCAR; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; THORACIC SPINAL CORD;

EID: 0037757588     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(02)00052-3     Document Type: Article

References (46)

1. Aguayo A.J., David S., Bray G.M. Influences of the glial environment on the elongation of axons after injury transplantation studies in adult rodents . J. Exp. Biol. 95:1981;231-240.
2. Asher R.A., Morgenstern D.A., Shearer M.C., Adcock K.H., Pesheva P., Fawcett J.W. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J. Neurosci. 22:2002;2225-2236.
3. Barbeau H., Ladouceur M., Norman K.E., Pepin A., Leroux A. Walking after spinal cord injury evaluation, treatment, and functional recovery . Arch. Phys. Med. Rehab. 80:1999;225-235.
4. Bovolenta P., Fernaud-Espinosa I., Mendez-Otero R., Nieto-Sampedro M. Neurite outgrowth inhibitor of gliotic brain tissue. Mode of action and cellular localization, studied with specific monoclonal antibodies. Eur. J. Neurosci. 9:1997;977-989.
5. Bovolenta P., Wandosell F., Nieto-Sampedro M. CNS glial scar tissue a source of molecules which inhibit central neurite outgrowth . Prog. Brain Res. 94:1992;367-379.
6. Carri N.G., Perris R., Johansson S., Ebendal T. Differential outgrowth of retinal neurites on purified extracellular matrix molecules. J. Neurosci. Res. 19:1988;428-439.
7. Dou C.L., Levine J.M. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J. Neurosci. 14:1994;7616-7628.
8. Dou C.L., Levine J.M. Differential effects of glycosaminoglycans on neurite growth on laminin and L1 substrates. J. Neurosci. 15:1995;8053-8066.
9. Dow K.E., Ethell D.W., Steeves J.D., Riopelle R.J. Molecular correlates of spinal cord repair in the embryonic chick heparan sulfate and chondroitin sulfate proteoglycans . Exp. Neurol. 128:1994;233-238.
10. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res. Bull. 49:1999;377-391.
11. Fawcett J.W., Keynes R.J. Peripheral nerve regeneration. Annu. Rev. Neurosci. 13:1990;43-60.
12. Fidler P.S., Schuette K., Asher R.A., Dobbertin A., Thornton S.R., Calle-Patino Y., Muir E., Levine J.M., Geller H.M., Rogers J.H., Faissner A., Fawcett J.W. Comparing astrocytic cell lines that are inhibitory or permissive for axon growth the major axon-inhibitory proteoglycan is NG2 . J. Neurosci. 19:1999;8778-8788.
13. Fitch M.T., Silver J. Activated macrophages and the blood-brain barrier inflammation after CNS injury leads to increases in putative inhibitory molecules . Exp. Neurol. 148:1997;587-603.
14. Fouad K., Dietz V., Schwab M.E. Improving axonal growth and functional recovery after experimental spinal cord injury by neutralizing myelin associated inhibitors. Brain Res. Brain Res. Rev. 36:2001;204-212.
15. Haas C.A., Rauch U., Thon N., Merten T., Deller T. Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J. Neurosci. 19:1999;9953-9963.
16. Ichijo H., Kawabata I. Roles of the telencephalic cells and their chondroitin sulfate proteoglycans in delimiting an anterior border of the retinal pathway. J. Neurosci. 21:2001;9304-9314.
17. Kornegay J.N. Paraparesis (paraplegia), tetraparesis (tetraplegia), urinary/fecal incontinence. Spinal cord diseases. Probl. Vet. Med. 3:1991;363-377.
18. Krekoski C.A., Neubauer D., Zuo J., Muir D. Axonal regeneration into acellular nerve grafts is enhanced by degradation of chondroitin sulfate proteoglycan. J. Neurosci. 21:2001;6206-6213.
19. Lander C., Kind P., Maleski M., Hockfield S. A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J. Neurosci. 17:1997;1928-1939.
20. Landolt R.M., Vaughan L., Winterhalter K.H., Zimmermann D.R. Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration and axon outgrowth. Development. 121:1995;2303-2312.
21. Lazarov-Spiegler O., Solomon A.S., Schwartz M. Peripheral nerve-stimulated macrophages simulate a peripheral nerve-like regenerative response in rat transected optic nerve. Glia. 24:1998;329-337.
22. Lemons M.L., Howland D.R., Anderson D.K. Chondroitin sulfate proteoglycan immunoreactivity increases following spinal cord injury and transplantation. Exp. Neurol. 160:1999;51-65.
23. Levine J.M. Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J. Neurosci. 14:1994;4716-4730.
24. Liesi P., Kauppila T. Induction of type IV collagen and other basement-membrane-associated proteins after spinal cord injury of the adult rat may participate in formation of the glial scar. Exp. Neurol. 173:2002;31-45.
25. Mann M.D. Clarke's column and the dorsal spinocerebellar tract a review . Brain Behav. Evol. 7:1973;34-83.
26. Maxwell D.J., Christie W.M., Ottersen O.P., Storm-Mathisen J. Terminals of group Ia primary afferent fibres in Clarke's column are enriched with L-glutamate-like immunoreactivity. Brain Res. 510:1990;346-350.
27. Maxwell W.L., Irvine A., Strang R.H., Graham D.I., Adams J.H., Gennarelli T.A. Glycogen accumulation in axons after stretch injury. J. Neurocytol. 19:1990;235-241.
28. McKeon R.J., Hoke A., Silver J. Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp. Neurol. 136:1995;32-43.
29. McKeon R.J., Schreiber R.C., Rudge J.S., Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J. Neurosci. 11:1991;3398-3411.
30. Moon L.D.F., Asher R.A., Rhodes K.E., Fawcett J.W. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci. 4:2001;465-466.
31. Muir D., Engvall E., Varon S., Manthorpe M. Schwannoma cell-derived inhibitor of the neurite-promoting activity of laminin. J. Cell Biol. 109:1989;2353-2362.
32. Niederost B.P., Zimmermann D.R., Schwab M.E., Bandtlow C.E. Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans. J. Neurosci. 19:1999;8979-8989.
33. Oakley R.A., Lasky C.J., Erickson C.A., Tosney K.W. Glycoconjugates mark a transient barrier to neural crest migration in the chicken embryo. Development. 120:1994;103-114.
34. Pettway Z., Domowicz M., Schwartz N.B., Bronner-Fraser M. Age-dependent inhibition of neural crest migration by the notochord correlates with alterations in the S103L chondroitin sulfate proteoglycan. Exp. Cell Res. 225:1996;195-206.
35. Pettway Z., Guillory G., Bronner-Fraser M. Absence of neural crest cells from the region surrounding implanted notochords in situ. Dev. Biol. 142:1990;335-345.
36. Plant G.W., Bates M.L., Bunge M.B. Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-transected spinal cord interface. Mol. Cell. Neurosci. 17:2001;471-487.
37. Reier P.J., Perlow M.J., Guth L. Development of embryonic spinal cord transplants in the rat. Brain Res. 312:1983;201-219.
38. Ring C., Lemmon V., Halfter W. Two chondroitin sulfate proteoglycans differentially expressed in the developing chick visual system. Dev. Biol. 168:1995;11-27.
39. Schwab J.M., Frei E., Klusman I., Schnell L., Schwab M.E., Schluesener H.J. AIF-1 expression defines a proliferating and alert microglial/macrophage phenotype following spinal cord injury in rats. J. Neuroimmunol. 119:2001;214-222.
40. Schwartz M., Moalem G., Leibowitz-Amit R., Cohen I.R. Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci. 22:1999;295-299.
41. Sekhon L.H., Fehlings M.G. Epidemiology, demographics, and pathophysiology of acute spinal cord injury. Spine. 26:2001;S2-12.
42. Walmsley B. Central synaptic transmission studies at the connection between primary afferent fibres and dorsal spinocerebellar tract (DSCT) neurones in Clarke's column of the spinal cord . Prog. Neurobiol. 36:1991;391-423.
43. Wang X., Messing A., David S. Axonal and nonneuronal cell responses to spinal cord injury in mice lacking glial fibrillary acidic protein. Exp. Neurol. 148:1997;568-576.
44. Yick L.W., Wu W., So K.F., Yip H.K., Shum D.K. Chondroitinase ABC promotes axonal regeneration of Clarke's neurons after spinal cord injury. NeuroReport. 11:2000;1063-1067.
45. Zemlan F.P., Leonard C.M., Kow L.M., Pfaff D.W. Ascending tracts of the lateral columns of the rat spinal cord a study using the silver impregnation and horseradish peroxidase techniques . Exp. Neurol. 62:1978;298-334.
46. Zuo J., Neubauer D., Dyess K., Ferguson T.A., Muir D. Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp. Neurol. 154:1998;654-662.