Chondroitinase ABCI improves locomotion and bladder function following contusion injury of the rat spinal cord

Journal of Neurotrauma

Volumn 22, Issue 2, 2005, Pages 226-239

  Caggiano, Anthony O ^a   Zimber, Michael P ^a   Ganguly, Anindita ^a   Blight, Andrew R ^a   Gruskin, Elliott A ^a  

^a ACORDA THERAPEUTICS INC   (United States)

Author keywords

Bladder function; Functional recovery; Plasticity; Proteoglycan; Regeneration

Indexed keywords

CHONDROITIN ABC LYASE; CHONDROITIN ABCI LYASE; PROTEOCHONDROITIN SULFATE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASSO BEATTIE AND BRESNAHAN LOCOMOTOR RATING SCALE; BLADDER FUNCTION; CONTROLLED STUDY; DRUG EFFICACY; HISTOPATHOLOGY; LOCOMOTION; NERVE CELL PLASTICITY; NERVE FIBER REGENERATION; NONHUMAN; OPEN FIELD BEHAVIOR; RAT; RATING SCALE; RESIDUAL URINE; SPINAL CORD INJURY; THORACIC SPINAL CORD;

EID: 14744306466     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2005.22.226     Document Type: Article

References (75)

1. ARNER, A., MALMQVIST, U., and UVELIUS, B. (1990). Metabolism and force in hypertrophic smooth muscle from rat urinary bladder. Am. J. Physiol. 258, C923-C932.
2. ASHER, R.A., MORGENSTERN, D.A., MOON, L.D., and FAWCETT, J.W. (2001). Chondroitin sulphate proteoglycans: inhibitory components of the glial scar. Prog. Brain Res. 132, 611-619.
3. BASSO, D.M., BEATTIE, M.S., and BRESNAHAN, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
4. BLIGHT, A.R. (1994). Effects of silica on the outcome from experimental spinal cord injury: implication of macrophages in secondary tissue damage. Neuroscience 60, 263-273.
5. BLIGHT, A.R. (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.
6. BLIGHT, A.R. (1991). Morphometric analysis of blood vessels in chronic experimental spinal cord injury: hypervascularity and recovery of function. J. Neurol. Sci. 106, 158-174.
7. BLIGHT, A.R., COHEN, T.I., SAITO, K., and HEYES, M.P. (1995). Quinolinic acid accumulation and functional deficits following experimental spinal cord injury. Brain 118, 735-752.
8. BLIGHT, A.R., LEROY, E.C., JR., and HEYES, M.P. (1997). Quinolinic acid accumulation in injured spinal cord: time course, distribution, and species differences between rat and guinea pig. J. Neurotrauma 14, 89-98.
9. BRADBURY, E.J., MOON, L.D., POPAT, R.J., KING, V.R., BENNETT, G.S., PATEL, P.N., FAWCETT, J.W., and McMAHON, S.B. (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640.
10. BRITTIS, P.A., and SILVER, J. (1995). Multiple factors govern intraretinal axon guidance: a time-lapse study. Mol. Cell Neurosci. 6, 413-432.
11. BRUCKNER, G., SEEGER, G., BRAUER, K., HARTIG, W., KACZA, J., and BIGL, V. (1994). Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res. 658, 67-86.
12. BUKALO, O., SCHACHNER, M., and DITYATEV, A. (2001). Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104, 359-369.
13. BUSH, T.G., PUVANACHANDRA, N., HORNER, C.H., POLITO, A., OSTENFELD, T., SVENDSEN, C.N., MUCKE, L., JOHNSON, M.H., and SOFRONIEW, M.V. (1999). Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23, 297-308.
14. CAGGIANO, A.O., ZIMBER, M.P., GANGULY, A., MARTINEZ, M., BLIGHT, A.R., and GRUSKIN, E.A. (2003). Chondroitinase ABC I improves locomotor function after spinal cord contusion injury in the rat. Program no. 744.5 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience.
15. CARBONETTA, S., GRUVER, M.M., and TURNER, D.C. (1983). Nerve fiber growth in culture on fibronectin, collagen, and glycosaminoglycan substrates. J. Neurosci. 3, 2324-2335.
16. CHAU, C.H., SHUM, D.K., LI, H., PEI, J., LUI, Y. Y., WIRTHLlN, L., CHAN, Y.S., and XU, X.M. (2004). Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J. 18, 194-196.
17. CHEN, X.Y., and WOLPAW, J.R. (2002). Probable corticospinal tract control of spinal cord plasticity in the rat. J. Neurophysiol. 87, 645-652.
18. CURTIS, R., GREEN, D., LINDSAY, R.M., and WILKIN, G.P. (1993). Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J. Neurocytol. 22, 51-64.
19. DAVIES, S.J., GOUCHER, D.R., DOLLER, C., and SILVER, J. (1999). Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J. Neurosci. 19, 5810-5822.
20. DE GROAT, W.C. (1993). Anatomy and physiology of the lower urinary tract. Urol. Clin. North Am. 20, 383-401.
21. DE GROAT, W.C., ARAKI, I., VIZZARD, M.A., YOSHIYAMA, M., YOSHIMURA, N., SUGAYA, K., TAI, C., and ROPPOLO, J.R. (1998). Developmental and injury induced plasticity in the micturition reflex pathway. Behav. Brain Res. 92, 127-140.
22. DE GROAT, W.C., KAWATANI, M., HISAMITSU, T., CHENG, C.L., MA, C.P., THOR, K., STEERS, W., and ROPPOLO, J.R. (1990). Mechanisms underlying the recovery of urinary bladder function following spinal cord injury. J. Auton. Nerv. Syst. 30, S71-S77.
23. DOU, C.L., and LEVINE, J.M. (1994). Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J. Neurosci. 14, 7616-7628.
24. FAULKNER, J.R., HERRMANN, J.E., WOO, M.J., DOAN, N.B., and SOFRONIEW, M.V. (2003). Reactive astrocytes protect tissue and preserve function after spinal cord stab injury. Program no. 744.1. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience.
25. FAWCETT, J. (1994). Astrocytes and axon regeneration in the central nervous system. J. Neurol. 242, S25-S28.
26. GALEANO, C., JUBELIN, B., GERMAIN, L., and GUENETTE, L. (1986). Micturation reflexes in chronic spinalized cats: the underactive detrusor and detrusor-sphincter dyssynergia. Neurourol. Urodyn. 5, 45-63.
27. GANGULY, A., ZIMBER, M.P., ALARCON, X., MARTINEZ, M.E., NATIELLO, M., GRUSKIN, E.A., and BLIGHT, A.R. (2003). Behavioral characterization of the forceps compression model of spinal cord injury in rats. Program no. 744.7. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience.
28. GRUNER, J.A., YEE, A.K., and BLIGHT, A.R. (1996). Histological and functional evaluation of experimental spinal cord injury: evidence of a step-wise response to graded compression. Brain Res. 729, 90-101.
29. GRUNER, J.A., and YEE, A.K. (1999). 4-Aminopyridine enhances motor evoked potentials following graded spinal cord compression injury in rats. Brain Res. 816, 446-456.
30. GUTH, L. (1975). History of central nervous system regeneration research. Exp. Neurol. 48, 3-15.
31. GUTH, L., BARRETT, C.P., DONATI, E.J., ANDERSON, F.D., SMITH, M.V., and LIFSON, M. (1985). Essentiality of a specific cellular terrain for growth of axons into a spinal cord lesion. Exp. Neurol. 88, 1-12.
32. GUTH, L., BARRETT, C.P., DONATI, E.J., SMITH, M.V., LIFSON, M., and ROBERTS, E. (1985). Enhancement of axonal growth into a spinal lesion by topical application of tri-ethanolamine and cytosine arabinoside. Exp. Neurol. 88, 44-55.
33. HALL, E. (2001). Pharmacological treatment of acute spinal cord injury: how do we build on past success? J. Spinal Cord Med. 24, 142-146.
34. HAMAI, A., HASHIMOTO, N., MOCHIZUKI, H., KATO, F., MAKIGUCHI, Y., HORIE, K., and SUZUKI, S. (1997). Two distinct chondroitin sulfate ABC lyases. An endoeliminase yielding tetrasaccharides and an exoeliminase preferentially acting on oligosaccharides. J. Biol. Chem. 272, 9123-9130.
35. HAYES, C.H., and BYRON, A.K. (1997). Neurophathology of human spinal cord injury sustained in sports-related activities. J. Neurotrauma 14, 235-248.
36. HOKE, A., and SILVER, J. (1996). Proteoglycans and other repulsive molecules in glial boundaries during development and regeneration of the nervous system. Prog. Brain Res. 108, 149-163.
37. JONES, L.L., MARGOLIS, R.U., and TUSZYNSKI, M.H. (2003). The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp. Neurol. 182, 399-411.
38. JONES, L.L., and TUSZYNSKI, M.H. (2001). Chronic intrathecal infusions after spinal cord injury cause scarring and compression. Microsc. Res. Tech. 54, 317-324.
39. KAKIZAKI, H., and DE GROAT, W.C. (1997). Reorganization of somato-urethral reflexes following spinal cord injury in the rat. J. Urol. 158, 1562-1567.
40. KREKOSKI, C.A., NEUBAUER, D., ZUO, J., and MUIR, D. (2001). Axonal regeneration into acellular nerve grafts is enhanced by degradation of chondroitin sulfate proteoglycan. J. Neurosci. 21, 6206-6213.
41. KRUSE, M.N., BENNETT, B., and DE GROAT, W.C. (1994). Effect of urinary diversion on the recovery of micturition reflexes after spinal cord injury in the rat. J. Urol. 151, 1088-1091.
42. KRUSE, M.N, BELTON, A.L., and DE GROAT, W.C. (1993). Changes in bladder and external urethral sphincter function after spinal cord injury in the rat. Am. J. Physiol. 264, 1157-1163.
43. LUO, J., LI, N., ROBINSON, J.P., and SHI, R. (2002). The increase of reactive oxygen species and their inhibition in an isolated guinea pig spinal cord compression model. Spinal Cord 40, 656-665.
44. LUTH, H.J., FISCHER, J., and CELIO, M.R. (1992). Soybean lectin binding neurons in the visual cortex of the rat contain parvalbumin and are covered by glial nets. J. Neurocytol. 21, 211-221.
45. McEWEN, M.L., and STEHOUWER, D.J. (2001). Kinematic analysis of air-stepping of neonatal rats after mid-thoracic spinal cord compression. J. Neurotrauma 18, 1383-1397.
46. McGUIRE, E.J., and BRADY, S. (1979). Detrusor-sphincter dyssynergia. J. Urol. 121, 774-777.
47. McGUIRE, E.J., and MORRISSEY, S.G. (1982). The development of neurogenic vesical dysfunction after experimental spinal cord injury or sacral rhizotomy in non-human primates. J. Urol. 128, 1390-1393.
48. McKEON, R.J., SCHREIBER, R.C., RUDGE, J.S., and SILVER, J. (1991). 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, 3398-3411.
49. McKEON, R.J., HOKE, A., and SILVER, J. (1995). Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp. Neurol. 136, 32-43.
50. METZ, G.A.S., CURT, A., VAN DE MEENT, H., KLUSMAN, I., SCHWAB, M.E., and DIETZ, V. (2000). Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J. Neurotrauma 17, 1-17.
51. MOON, L.D., ASHER, R.A., RHODES, K.E., and FAWCETT, J.W. (2001). Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci. 4, 465-466.
52. MORGENSTERN, D.A., ASHER, R.A., and FAWCETT, J.W. (2002). Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 137, 313-332.
53. MURE, P.Y., GALDO, M, and COMPAGNONE, N. (2004). Bladder function after incomplete spinal cord injury in mice: quantifiable outcomes associated with bladder function and efficiency of dehydroepiandrosterone as a therapeutic adjunct. J. Neurosurg. 100, 56-61.
54. OOHIRA, A., MATSUI, F., and KATOH-SEMBA, R. (1991). Inhibitory effects of brain chondroitin sulfate proteoglycans on neurite outgrowth from PC12D cells. J. Neurosci. 11, 822-827.
55. PIZZORUSSO, T., MEDINI, P., BERARDI, N., CHIERZI, S., FAWCETT, J.W., and MAFFEI, L. (2002). Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251.
56. RAMON, S., DOMINGUEZ, R., RAMIREZ, L., PARAIRA, M., OLONA, M., CASTELLO, T., and GARCIA FERNANDEZ, L. (1997). Clinical and magnetic resonance imaging correlation in acute spinal cord injury. Spinal Cord 35, 664-673.
57. RAMON Y CAJAL, S. (1928). Degeneration and Regeneration of the Nervous System. Oxford University Press: London.
58. REIER, P.J., and HOULE, J.D. (1988). The glial scar: its bearing on axonal elongation and transplantation approaches to CNS repair, in: S.G. Waxman (ed.), Advances in Neurology. Raven Press: New York, pps. 87-138.
59. SHEFCHYK, S.J. (2002). Spinal cord neural organization controlling the urinary bladder and striated sphincter. Prog, Brain Res. 137, 71-82.
60. SILVER, J., and MILLER, J. (2004). Regeneration beyond the glial scar. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146-156.
61. SNOW, D.M., LEMMON, V., CARRINO, D.A., CAPLAN, A.I., and SILVER, J. (1990a). Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol. 109, 111-130.
62. SNOW, D.M., STEINDLER, D.A., and SILVER, J. (1990b). Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan in the development of an axon barrier. Dev. Biol. 138, 359-376.
63. SNOW, D.M., MULLINS, N., and HYNDS, D.L. (2001). Nervous system-derived chondroitin sulfate proteoglycans regulate growth cone morphology and inhibit neurite outgrowth: a light, epifluorescence, and electron microscopy study. Microsc. Res. Tech. 54, 273-286.
64. TESTER, N.J., PLAAS, A.H., and HOWLAND, D.R. (2003). Chondroitin sulfate glycosaminoglycans and the effects of chondroitinase ABC on behavioral and anatomical recovery following spinal cord injury in the adult cat. Program no. 744.17. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience.
65. UVELIUS, B., PERSSON, L., and MATTIASSON, A. (1984). Smooth muscle cell hypertrophy and hyperplasia in the rat detrusor after short-time infravesical outflow obstruction. J. Urol. 131, 173-176.
66. WEIN, A.J., and BARRETT, D.M. (1988). Voiding: Function and Dysfunction. Yearbook Medical: Chicago.
67. YICK, L.W., CHEUNG, P.T., SO, K.F., and WU, W. (2003). Axonal regeneration of Clarke's neurons beyond the spinal cord injury scar after treatment with chondroitinase ABC. Exp. Neurol. 182, 160-168.
68. YICK, L.W., WU, W., SO, K.F., YIP, H.K., and SHUM, D.K. (2000). Chondroitinase ABC promotes axonal regeneration of Clarke's neurons after spinal cord injury. Neuroreport 11, 1063-1067.
69. YOUNG, W. (2003). Spinal cord contusion models. Prog. Brain Res. 137, 231-255.
70. ZHANG, Z., and GUTH, L. (1997). Experimental spinal cord injury. Wallerian degeneration in the dorsal column is followed by revascularization, glial proliferation, and nerve regeneration. Exp. Neurol. 147, 159-171.
71. ZHANG, Z., KREBS, C.J., and GUTH, L. (1997). Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp. Neurol. 143, 141-152.
72. ZIMBER, M.P., NATIELLO, M., GANGULY, A., CAGGIANO, A.O., GICHURU, L.N., MARTINEZ, M.E., GRUSKIN, E.A., and BLIGHT, A.R. (2003). Histological characterization of a forceps compression model of spinal cord injury in rats. Program no. 744.8. Abstract Viewer/Itinary Planner. Washington, DC: Society for Neuroscience.
73. ZIMBER, M.P., NATIELLO, N., GRUSKIN, E., TSENG, T., and BLIGHT, A.R. (2002). Evaluation of a forceps compression model of SCI in rats. Symp. Natl. Int. Neurotrauma Soc. P202.
74. ZUO, J., NEUBAUER, D., DYESS, K., FERGUSON, T.A., and MUIR, D. (1998). Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp. Neurol. 154, 654-662.
75. ZUO, J., NEUBAUER, D., GRAHAM, J., KREKOSKI, C.A., FERGUSON, T.A., and MUIR, D. (2002). Regeneration of axons after nerve transection repair is enhanced by degradation of chondroitin sulfate proteoglycan. Exp. Neurol. 176, 221-228.