Chondroitinase ABC reduces time to muscle reinnervation and improves functional recovery after sciatic nerve transection in rats

Journal of Neurophysiology

Volumn 107, Issue 3, 2012, Pages 747-757

  Sabatier, Manning J ^a,b   To, Bao Ngoc ^a   Rose, Samuel ^a   Nicolini, Jennifer ^a   English, Arthur W ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CLAYTON STATE UNIVERSITY   (United States)

Author keywords

Compound muscle action potential; Electromyographic activity; H reflex; Kinematics; Locomotion

Indexed keywords

CHONDROITIN ABC LYASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAPHY; EVOKED RESPONSE; FEMALE; KINEMATICS; LOCOMOTION; MUSCLE ACTION POTENTIAL; MUSCLE REINNERVATION; NERVE TRANSECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE;

ACTION POTENTIALS; ANIMALS; CHONDROITIN ABC LYASE; ELECTROMYOGRAPHY; FEMALE; H-REFLEX; HINDLIMB; LOCOMOTION; MUSCLE, SKELETAL; NERVE REGENERATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SCIATIC NERVE; TREATMENT OUTCOME;

EID: 84855827862     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00887.2011     Document Type: Article

References (57)

1. Alvarez FJ, Bullinger KL, Titus HE, Nardelli P, Cope TC. Permanent reorganization of Ia afferent synapses on motoneurons after peripheral nerve injuries. Ann NY Acad Sci 1198: 231-241, 2010.
2. Beaumont E, Cloutier FC, Atlan M, Rouleau DM, Beaumont PH. Chondroitinase ABC and acute electrical stimulation are beneficial for muscle reinnervation after sciatic nerve transection in rats. Restor Neurol Neurosci 27: 297-305, 2009.
3. Bishop C. Neural Networks for Pattern Recognition. Oxford, UK: Oxford Univ. Press, 1995.
4. Bovolenta P, Wandosell F, Nieto-Sampedro M. Characterization of a neurite outgrowth inhibitor expressed after CNS injury. Eur J Neurosci 5: 454-465, 1993.
5. Brannstrom T, Kellerth JO. Changes in synaptology of adult cat spinal alpha-motoneurons after axotomy. Exp Brain Res 118: 1-13, 1998.
6. Braunewell KH, Pesheva P, McCarthy JB, Furcht LT, Schmitz B, Schachner M. Functional involvement of sciatic nerve-derived versican-and decorin-like molecules and other chondroitin sulphate proteoglycans in ECM-mediated cell adhesion and neurite outgrowth. Eur J Neurosci 7: 805-814, 1995.
7. Carlson-Kuhta P, Trank TV, Smith JL. Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking. J Neurophysiol 79: 1687-1701, 1998.
8. Castro-Lopes JM, Tavares I, Coimbra A. GABA decreases in the spinal cord dorsal horn after peripheral neurectomy. Brain Res 620: 287-291, 1993.
9. Chang YH, Auyang AG, Scholz JP, Nichols TR. Whole limb kinematics are preferentially conserved over individual joint kinematics after peripheral nerve injury. J Exp Biol 212: 3511-3521, 2009.
10. Diers-Fenger M, Kirchhoff F, Kettenmann H, Levine JM, Trotter J. AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: isolation, differentiation, and association with radial glia. Glia 34: 213-228, 2001.
11. Donelan JM, McVea DA, Pearson KG. Force regulation of ankle extensor muscle activity in freely walking cats. J Neurophysiol 101: 360-371, 2009.
12. Dou CL, Levine JM. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 14: 7616-7628, 1994.
13. Eccles JC, Libet B, Young RR. The behaviour of chromatolysed motoneurones studied by intracellular recording. J Physiol 143: 11-40, 1958.
14. English AW. Enhancing axon regeneration in peripheral nerves also increases functionally inappropriate reinnervation of targets. J Comp Neurol 490: 427-441, 2005.
15. English AW, Chen Y, Carp JS, Wolpaw JR, Chen XY. Recovery of electromyographic activity after transection and surgical repair of the rat sciatic nerve. J Neurophysiol 97: 1127-1134, 2007.
16. Fawcett JW, Keynes RJ. Peripheral nerve regeneration. Annu Rev Neurosci 13: 43-60, 1990.
17. Ferguson TA, Muir D. MMP-2 and MMP-9 increase the neurite-promoting potential of schwann cell basal laminae and are upregulated in degenerated nerve. Mol Cell Neurosci 16: 157-167, 2000.
18. Foehring RC, Sypert GW, Munson JB. Properties of self-reinnervated motor units of medial gastrocnemius of cat. I. Long-term reinnervation. J Neurophysiol 55: 931-946, 1986.
19. Gorassini MA, Prochazka A, Hiebert GW, Gauthier MJ. Corrective responses to loss of ground support during walking. I. Intact cats. J Neurophysiol 71: 603-610, 1994.
20. Gorio A, Vergani L, De Tollis A, Di Giulio AM, Torsello A, Cattaneo L, Muller EE. Muscle reinnervation following neonatal nerve crush. Interactive effects of glycosaminoglycans and insulin-like growth factor-I. Neuroscience 82: 1029-1037, 1998.
21. Gregor RJ, Smith DW, Prilutsky BI. Mechanics of slope walking in the cat: quantification of muscle load, length change, and ankle extensor EMG patterns. J Neurophysiol 95: 1397-1409, 2006.
22. Groves ML, McKeon R, Werner E, Nagarsheth M, Meador W, English AW. Axon regeneration in peripheral nerves is enhanced by proteoglycan degradation. Exp Neurol 195: 278-292, 2005.
23. Hamilton S, Hinkle M, Nicolini J, Rambo L, Rexwinkle A, Rose S, Sabatier M, Backus D, English A. Misdirection of regenerating axons and functional recovery following sciatic nerve injury in rats. J Comp Neurol 519: 21-33, 2011.
24. Hellgren J, Kellerth JO. A physiological study of the monosynaptic reflex responses of cat spinal alpha-motoneurons after partial lumbosacral deafferentation. Brain Res 488: 149-162, 1989.
25. Jones LL, Sajed D, Tuszynski MH. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci 23: 9276-9288, 2003.
26. Krekoski CA, Neubauer D, Zuo J, Muir D. Axonal regeneration into acellular nerve grafts is enhanced by degradation of chondroitin sulfate proteoglycan. J Neurosci 21: 6206-6213, 2001.
27. Maas H, Gregor RJ, Hodson-Tole EF, Farrell BJ, English AW, Prilutsky BI. Locomotor changes in length and EMG activity of feline medial gastrocnemius muscle following paralysis of two synergists. Exp Brain Res 203: 681-692, 2010.
28. MacGillivray TE. Fibrin sealants and glues. J Card Surg 18: 480-485, 2003.
29. Martin S, Levine AK, Chen ZJ, Ughrin Y, Levine JM. Deposition of the NG2 proteoglycan at nodes of Ranvier in the peripheral nervous system. J Neurosci 21: 8119-8128, 2001.
30. Mazzaro N, Grey MJ, Sinkjaer T. Contribution of afferent feedback to the soleus muscle activity during human locomotion. J Neurophysiol 93: 167-177, 2005.
31. McKeon RJ, Hoke A, Silver J. Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 136: 32-43, 1995.
32. McKeon RJ, Schreiber RC, Rudge JS, 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: 3398-3411, 1991.
33. Menovsky T, Beek JF. Laser, fibrin glue, or suture repair of peripheral nerves: a comparative functional, histological, and morphometric study in the rat sciatic nerve. J Neurosurg 95: 694-699, 2001.
34. Muir D, Engvall E, Varon S, Manthorpe M. Schwannoma cell-derived inhibitor of the neurite-promoting activity of laminin. J Cell Biol 109: 2353-2362, 1989.
35. Pearson KG, Collins DF. Reversal of the influence of group Ib afferents from plantaris on activity in medial gastrocnemius muscle during locomotor activity. J Neurophysiol 70: 1009-1017, 1993.
36. Prochazka A, Trend P, Hulliger M, Vincent S. Ensemble proprioceptive activity in the cat step cycle: towards a representative look-up chart. Prog Brain Res 80: 61-74, 1989.
37. Rasband WS, Image J, Bethesda, MD: National Institutes of Health, 1997-2006.
38. Roy RR, Hutchison DL, Pierotti DJ, Hodgson JA, Edgerton VR. EMG patterns of rat ankle extensors and flexors during treadmill locomotion and swimming. J Appl Physiol 70: 2522-2529, 1991.
39. Sabatier MJ, To BN, Nicolini J, English AW. Effect of axon misdirection on recovery of EMG activity and kinematics after peripheral nerve injury. Cells Tissues Organs 193: 298-309, 2011a.
40. Sabatier MJ, To BN, Nicolini J, English AW. Effect of slope and sciatic nerve injury on ankle muscle recruitment and hindlimb kinematics during walking in the rat. J Exp Biol 214: 1007-1016, 2011b.
41. Schieppati M. The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28: 345-376, 1987.
42. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan JG. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326: 592-596, 2009.
43. Sperry R. The effect of crossing nerves to antagonistic muscles in the hind limb of the rat. J Comp Neurol 75: 1-19, 1941.
44. Stoll G, Muller HW. Nerve injury, axonal degeneration and neural regeneration: basic insights. Brain Pathol 9: 313-325, 1999.
45. Sunderland S. Nerve and Nerve Injuries. London: Churchill Livingstone, 1978.
46. Sweeney JD, Ksienski DA, Mortimer JT. A nerve cuff technique for selective excitation of peripheral nerve trunk regions. IEEE Trans Biomed Eng 37: 706-715, 1990.
47. Tabb JS, Fanger GR, Wilson EM, Maue RA, Henderson LP. Suppression of sodium channel function in differentiating C2 muscle cells stably overexpressing rat androgen receptors. J Neurosci 14: 763-773, 1994.
48. Thota AK, Watson SC, Knapp E, Thompson B, Jung R. Neuromechanical control of locomotion in the rat. J Neurotrauma 22: 442-465, 2005.
49. Tona A, Perides G, Rahemtulla F, Dahl D. Extracellular matrix in regenerating rat sciatic nerve: a comparative study on the localization of laminin, hyaluronic acid, and chondroitin sulfate proteoglycans, including versican. J Histochem Cytochem 41: 593-599, 1993.
50. Trigg DJ, O'Grady KM, Bhattacharyya T, Reinke M, Toriumi DM. Peripheral nerve regeneration: comparison of laminin and acidic fibroblast growth factor. Am J Otolaryngol 19: 29-32, 1998.
51. Udina E, Cobianchi S, Allodi I, Navarro X. Effects of activity-dependent strategies on regeneration and plasticity after peripheral nerve injuries. Ann Anat 193: 347-353, 2011.
52. Valero-Cabre A, Navarro X. Changes in crossed spinal reflexes after peripheral nerve injury and repair. J Neurophysiol 87: 1763-1771, 2002.
53. Wall PD, Devor M. The effect of peripheral nerve injury on dorsal root potentials and on transmission of afferent signals into the spinal cord. Brain Res 209: 95-111, 1981.
54. Widmer CG, Carrasco DI, English AW. Differential activation of neuromuscular compartments in the rabbit masseter muscle during different oral behaviors. Exp Brain Res 150: 297-307, 2003.
55. Zuo J, Hernandez YJ, Muir D. Chondroitin sulfate proteoglycan with neurite-inhibiting activity is up-regulated following peripheral nerve injury. J Neurobiol 34: 41-54, 1998a.
56. Zuo J, Neubauer D, Dyess K, Ferguson TA, Muir D. Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp Neurol 154: 654-662, 1998b.
57. Zuo J, Neubauer D, Graham J, Krekoski CA, Ferguson TA, Muir D. Regeneration of axons after nerve transection repair is enhanced by degradation of chondroitin sulfate proteoglycan. Exp Neurol 176: 221-228, 2002.