Chondroitinase ABC promotes recovery of adaptive limb movements and enhances axonal growth caudal to a spinal hemisection

Journal of Neuroscience

Volumn 31, Issue 15, 2011, Pages 5710-5720

  Jefferson, Stephanie C ^a,b,c   Tester, Nicole J ^a,b,c   Howland, Dena R ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN ABC LYASE; FLUOROGOLD; NEUROFILAMENT PROTEIN; SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR THERAPY; CAT; CONTROLLED STUDY; FEMALE; FORELIMB; HINDLIMB; IMMUNOREACTIVITY; KINEMATICS; LIMB MOVEMENT; LOCOMOTION; MOTOR COORDINATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; RED NUCLEUS; REFLEX; RUBROSPINAL TRACT; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; TASK PERFORMANCE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AXONS; AXOTOMY; BEHAVIOR, ANIMAL; CATS; CHONDROITIN ABC LYASE; DECEREBRATE STATE; FEMALE; FUNCTIONAL LATERALITY; HINDLIMB; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MOVEMENT; NERVE REGENERATION; PYRAMIDAL TRACTS; RED NUCLEUS; SPINAL CORD; SPINAL CORD INJURIES;

EID: 79955776756     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4459-10.2011     Document Type: Article

References (94)

1. Armstrong DM (1986) Supraspinal contributions to the initiation and control of locomotion in the cat. Prog Neurobiol 26:273-361.
2. Armstrong DM (1988) The supraspinal control of mammalian locomotion. J Physiol 405:1-37.
3. Armstrong DM, Marple-Horvat DE (1996) Role of the cerebellum and motor cortex in the regulation of visually controlled locomotion. Can J Physiol Pharmacol 74:443-455.
4. Banik NL, Matzelle DC, Gantt-Wilford G, Osborne A, Hogan EL (1997) Increased calpain content and progressive degradation of neurofilament protein in spinal cord injury. Brain Res 752:301-306.
5. Banik NL, Hogan EL, Powers JM, Whetstine LJ (1982) Degradation of cy-toskeletal proteins in experimental spinal cord injury. Neurochem Res 7:1465-1475.
6. Barbeau H, McCrea DA, O'Donovan MJ, Rossignol S, Grill WM, Lemay MA (1999) Tapping into spinal circuits to restore motor function. Brain Res Brain Res Rev 30:27-51.
7. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME (2004) The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 7:269-277.
8. Barrieŕe G, Leblond H, Provencher J, Rossignol S (2008) Prominent role of the spinal central pattern generatorinrecoveryof locomotion after partial spinal cord injuries. J Neurosci 28:3976-3987.
9. Behrman AL, Harkema SJ (2000) Locomotor training after human spinal cord injury: a series of case studies. Phys Ther 80:688-700.
10. Beloozerova IN, Sirota MG (1993) The role of the motor cortex in the control of vigour of locomotor movements in the cat. J Physiol 461:27-46.
11. Beloozerova IN, Farrell BJ, Sirota MG, Prilutsky BI (2010) Differences in movement mechanics, electromyographic, and motor cortex activity between accurate and nonaccurate stepping. J Neurophysiol 103:2285-2300.
12. Blagoveshchenskii ED, Pettersson LG, Perfil'ev SN (2005) Control of fine movements mediated by propriospinal neurons. Neurosci Behav Physiol 35:299-304.
13. Blaszczyk J, Loeb GE (1993) Why cats pace on the treadmill. Physiol Behav 53:501-507.
14. Boulenguez P, Vinay L (2009) Strategies to restore motor functions after spinal cord injury. Curr Opin Neurobiol 19:587-600.
15. Bradbury EJ, Carter LM (2011) Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain Res Bull 84:306-316.
16. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640.
17. Braughler JM, Hall ED, Means ED, Waters TR, Anderson DK (1987) Evaluation of an intensive methylprednisolone sodium succinate dosing regimen in experimental spinal cord injury. J Neurosurg 67:102-105.
18. Bregman BS (1987) Development of serotonin immunoreactivity in the rat spinal cord and its plasticity after neonatal spinal cord lesions. Brain Res 431:245-263.
19. Brückner G, Bringmann A, Härtig W, Köppe G, Delpech B, Brauer K (1998) Acute and long-lasting changes in extracellular-matrix condroitin-sulphate proteoglycans inducedbyinjectionofchondroitinase ABCinthe adult rat brain. Exp Brain Res 121:300-310.
20. Busch SA, Silver J (2007) The role of extracellular matrix in CNS regeneration. Cur Opin Neurobiol 17:120-127.
21. Busch SA, Horn KP, Silver DJ, Silver J (2009) Overcoming macrophage-mediated axonal dieback following CNS injury. J Neurosci 29:9967-9976.
22. Carter LM, McMahon SB, Bradbury EJ (2011) Delayed treatment with chondroitinase ABC reverses chronic atrophy of rubrospinal neurons following spinal cord injury. Exp Neurol 228:149-156.
23. Coss L, Chan AK, Goslow GE, Rasmussen S (1978) Ipsilateral limb variation in cats during overground locomotion. Brain Behav Evol 15:85-93.
24. Courtine G, Roy RR, Raven J, Hodgson J, McKay H, Yang H, Zhong H, Tuszynski MH, Edgerton VR (2005) Performance of locomotion and foot grasping following a unilateral thoracic corticospinal tract lesion in monkeys (Macaca mulatta). Brain 128:2338-2358.
25. Courtine G, Song B, Roy RR, Zhong H, Herrmann JE, Ao Y, Qi J, Edgerton VR, Sofroniew MV (2008) Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med 14:69-74.
26. Courtine G, Gerasimenko Y, van den Brand R, Yew A, Musienko P, Zhong H, Song B, Ao Y, Ichiyama RM, Lavrov I, Roy RR, Sofroniew MV, Edgerton VR (2009) Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci 12:1333-1342.
27. Crespo D, Asher RA, Lin R, Rhodes KE, Fawcett JW (2007) How does chon-droitinase promote functional recovery in the damaged CNS? Exp Neurol 206:159-171.
28. Cruse H, Warnecke H (1992) Coordination ofthe legsof aslow-walking cat. Exp Brain Res 89:147-156.
29. de Leon RD, Hodgson JA, Roy RR, Edgerton VR (1998) Locomotor capacity attributable to step training versus spontaneous recovery after spinaliza-tion in adult cats. J Neurophysiol 79:1329-1340.
30. de Leon RD, Roy RR, Edgerton VR (2001) Is the recovery of stepping following spinal cord injury mediated by modifying existing neural pathways or by generating new pathways? A perspective. Phys Ther 81:1904-1911.
31. Drew T, Jiang W, Kably B, Lavoie S (1996) Role of the motor cortex in the control of visually triggered gait modifications. Can J Physiol Pharmacol 74:426-442.
32. Drew T, Jiang W, Widajewicz W (2002) Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat. Brain Res Brain Res Rev 40:178-191.
33. Drew T, Prentice S, Schepens B (2004) Cortical and brainstem control of locomotion. Prog Brain Res 143:251-261.
34. Edgerton VR, Tillakaratne NJ, Bigbee AJ, de Leon RD, Roy RR (2004) Plasticity of the spinal neural circuitry after injury. Annu Rev Neurosci 27:145-167.
35. Eidelberg E, Nguyen LH, Deza LD (1986) Recovery of locomotor function after hemisection of the spinal cord in cats. Brain Res Bull 16:507-515.
36. Eisenstein BL, Postillion FG, Norgren KS, Wetzel MC (1977) Kinematics of treadmill galloping by cats. Behav Biol 21:89-106.
37. English AW (1979) Interlimb coordination during stepping in the cat: an electromyographic analysis. J Neurophysiol 42:229-243.
38. English AW (1980) Interlimb coordination during stepping in the cat: effects of dorsal column section. J Neurophysiol 44:270-279.
39. English AW (1985) Interlimb coordination during stepping in the cat: the role of the dorsal spinocerebellar tract. Exp Neurol 87:96-108.
40. English AW, Lennard PR (1982) Interlimb coordination during stepping in the cat: in-phase stepping and gait transitions. Brain Res 245:353-364.
41. Forssberg H, Grillner S, Halbertsma J (1980) The locomotion of the low spinal cat. I. Coordination within a hindlimb. Acta Physiol Scand 108:269-281.
42. Forssberg H, Grillner S, Halbertsma J, Rossignol S (1980) The locomotion of the low spinal cat. II. Interlimb coordination. Acta Physiol Scand 108:283-295.
43. García-Alías G, Barkhuysen S, Buckle M, Fawcett JW (2009) Chondroiti-nase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 12:1145-1151.
44. Gibson AR, Houk JC, Kohlerman NJ (1985) Magnocellular red nucleus activity during different types of limb movement in the macaque monkey. J Physiol 358:527-549.
45. Girgis J, Merrett D, Kirkland S, Metz GA, Verge V, Fouad K (2007) Reaching training in rats with spinal cord injury promotes plasticity and task specific recovery. Brain 130:2993-3003.
46. Giuliani CA, Smith JL (1987) Stepping behaviors in chronic spinal cats with one hindlimb deafferented. J Neurosci 7:2537-2546.
47. Górska T, Bem T, Majczyński H, Zmyslowski W (1993) Unrestrained walking in intact cats. Brain Res Bull 32:235-240.
48. Grillner S, Zangger P (1979) On the central generation of locomotion in the low spinal cat. Exp Brain Res 34:241-261.
49. Helgren ME, Goldberger ME (1993) The recovery of postural reflexes and locomotion following low thoracic hemisection in adult cats involves compensation by undamaged primary afferent pathways. Exp Neurol 123:17-34.
50. Hodgson JA, Roy RR, de Leon R, Dobkin B, Edgerton VR (1994) Can the mammalian lumbar spinal cord learn a motor task? Med Sci Sports Exerc 26:1491-1497.
51. Howard CV and Reed M (2005) Estimation of component volume and volume fraction. In: Unbiased stereology: advanced methods, Ed 2 (Howard CV and Reed M, eds), pp 53-64. New York: Garland Science/BIOS Scientific Publishers.
52. Howland DR, Bregman BS, Tessler A, Goldberger ME (1995) Transplants enhance locomotion in neonatal kittens whose spinal cords are transected: a behavioral and anatomical study. Exp Neurol 135:123-145.
53. Howland DR, Bregman BS, Tessler A, Goldberger ME (1995) Development of locomotor behavior in the spinal kitten. Exp Neurol 135:108-122.
54. Jakeman LB, Hoschouer EL, Basso DM (2011) Injured mice at the gym: review, results and considerations for combining chondroitinase and lo-comotor exercise to enhance recovery after spinal cord injury. Brain Res Bull 84:317-326.
55. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Schut D, Fehlings MG (2010) Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J Neurosci 30:1657-1676.
56. Kato M, Murakami S, Yasuda K, Hirayama H (1984) Disruption of fore-and hindlimb coordination during overground locomotion in cats with bilateral serial hemisection of the spinal cord. Neurosci Res 2:27-47.
57. Krajacic A, Weishaupt N, Girgis J, Tetzlaff W, Fouad K 2010 Training-induced plasticity in rats with cervical spinal cord injury: effects and side effects. Behav Brain Res 214:323-331.
58. Kwok JC, Afshari F, García-Alías G, Fawcett JW (2008) Proteoglycans in the central nervous system: plasticity, regeneration and their stimulation with chondroitinase ABC. Restor Neurol Neurosci 26:131-145.
59. Lajoie K, Andujar JE, Pearson K, Drew T (2010) Neurons in area 5 of the posterior parietal cortex in the cat contribute to interlimb coordination during visually guided locomotion: a role in working memory. J Neuro-physiol 103:2234-2254.
60. Lavoie S, Drew T (2002) Discharge characteristics of neurons in the red nucleus during voluntary gait modifications: a comparison with the motor cortex. J Neurophysiol 88:1791-1814.
61. Levin MF, Kleim JA, Wolf SL (2009) What do motor "recovery" and "compensation" mean in patients following stroke? Neurorehabil Neural Repair 23:313-319.
62. Liu YL, Guo YS, Xu L, Wu SY, Wu DX, Yang C, Zhang Y, Li CY (2009) Alternation of neurofilaments in immune-mediated injury of spinal cord motor neurons. Spinal Cord 47:166-170.
63. Lovely RG, Gregor RJ, Roy RR, Edgerton VR (1986) Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp Neurol 92:421-435.
64. Martin JE, Mather KS, Swash M, Garofalo O, Dale GE, Leigh PN, Anderton BH (1990) Spinal cord trauma in man: studies of phosphorylated neu-rofilament and ubiquitin expression. Brain 113:1553-1562.
65. Mewes K, Cheney PD (1994) Primate rubromotoneuronal cells: parametric relations and contribution to wrist movement. J Neurophysiol 72:14-30.
66. Miller S, Van Der Meché FG (1975) Movements of the forelimbs of the cat during stepping on a treadmill. Brain Res 91:255-269.
67. Miller S, van der Meché FG (1976) Coordinated stepping of all four limbs in the high spinal cat. Brain Res 109:395-398.
68. Miller S, Reitsma DJ, van der Meché FG (1973) Functional organization of long ascending propriospinal pathways linking lumbo-sacral and cervical segments in the cat. Brain Res 62:169-188.
69. Miller S, van Berkum R, van der Burg J, van der Meché FG (1973) Inter-limb co-ordination in stepping in the cat. J Physiol 230:30P-31P.
70. Miller S, Van Der Burg J, Van Der Meché F (1975) Coordination of movements of the hindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats. Brain Res 91:217-237.
71. Miller S, van Der Burg J, van Der Meché F (1975) Locomotion in the cat: basic programmes of movement. Brain Res 91:239-253.
72. Mori S, Matsui T, Kuze B, Asanome M, Nakajima K, Matsuyama K (1998) Cerebellar-induced locomotion: reticulospinal control of spinal rhythm generating mechanism in cats. Ann N Y Acad Sci 860:94-105.
73. Raineteau O, Schwab ME (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2:263-273.
74. Rossignol S, Dubuc R (1994) Spinal pattern generation. Curr Opin Neuro-biol 4:894-902.
75. Rossignol S, Chau C, Brustein E, Belanger M, Barbeau H, Drew T (1996) Locomotor capacities after complete and partial lesions ofthe spinal cord. Acta Neurobiol Exp (Wars) 56:449-463.
76. Rossignol S, Drew T, Brustein E, Jiang W (1999) Locomotor performance and adaptation after partial or complete spinal cord lesions in the cat. Prog Brain Res 123:349-365.
77. Rossignol S, Giroux N, Chau C, Marcoux J, Brustein E, Reader TA (2001) Pharmacological aids to locomotor training after spinal injury in the cat. J Physiol 533:65-74.
78. Rossignol S, Bouyer L, Barthélemy D, Langlet C, Leblond H (2002) Recovery of locomotion in the cat following spinal cord lesions. Brain Res Brain Res Rev 40:257-266.
79. Sandrow-Feinberg HR, Izzi J, Shumsky JS, Zhukareva V, Houle JD (2009) Forced exercise as a rehabilitation strategy after unilateral cervical spinal cord contusion injury. J Neurotrauma 26:721-731.
80. Schumacher PA, Eubanks JH, Fehlings MG (1999) Increased calpain I-mediated proteolysis, and preferential loss of dephosphorylated NF200, following traumatic spinal cord injury. Neuroscience 91:733-744.
81. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neu-rosci 5:146-156.
82. Stuart DC, Withey TP, Wetzel MC, Goslow GE (1973) Time constraints for interlimb-limb co-ordination in the cat during unrestrained locomotion. In: Control of posture and locomotion (Stein RB, Pearson KG, Smith RS, Redfore JB, eds), pp 537-560. New York: Plenum.
83. Tester NJ, Howland DR (2008) Chondroitinase ABC improves basic and skilled locomotion in spinal cord injured cats. Exp Neurol 209:483-496.
84. Tester NJ, Plaas AH, Howland DR (2007) Effect of body temperature on chondroitinase ABC's ability to cleave chondroitin sulfate glycosamino-glycans. J Neurosci Res 85:1110-1118.
85. Thomas SL, Gorassini MA (2005) Increases in corticospinal tract function by treadmill training after incomplete spinal cord injury. J Neurophysiol 94:2844-2855.
86. Tom VJ, Sandrow-Feinberg HR, Miller K, Santi L, Connors T, Lemay MA, Houlé JD (2009) Combining peripheral nerve grafts and chondroitinase promotes functional axonal regeneration in the chronically injured spinal cord. J Neurosci 29:14881-14890.
87. von Euler M, Janson AM, Larsen JO, Seiger A, Forno L, Bunge MB, Sund-ström E (2002) Spontaneous axonal regeneration in rodent spinal cord after ischemic injury. J Neuropathol Exp Neurol 61:64-75.
88. Wessels M, Lucas C, Eriks I, de Groot S (2010) Body weight-supported gait training for restoration of walking in people with an incomplete spinal cord injury: a systematic review. J Rehabil Med 42:513-519.
89. Wetzel MC, Stuart DG (1976) Ensemble characteristics of cat locomotion and its neural control. Prog Neurobiol 7:1-98.
90. Wetzel MC, Atwater AE, Wait JV, Stuart DC (1975) Neural implications of different profiles between treadmill and overground locomotion timings in cats. J Neurophysiol 38:492-501.
91. Wetzel MC, Anderson RC, Brady, RH, Norgren KS (1977) Kinematics of treadmill gallopingbycats III. Coordination during Gait Conversions and Implications for Neural Control. Behav Biol 21:107-127.
92. Whelan PJ (1996) Control of locomotion in the decerebrate cat. Prog Neu-robiol 49:481-515.
93. Widajewicz W, Kably B, Drew T (1994) Motor cortical activity during voluntary gait modifications in the cat. II. Cells related to the hindlimbs. J Neurophysiol 72:2070-2089.
94. Yick LW, So KF, Cheung PT, Wu WT (2004) Lithium chloride reinforces the regeneration-promoting effect of chondroitinase ABC on rubrospinal neurons after spinal cord injury. J Neurotrauma 21:932-943.