Accelerating axon growth to overcome limitations in functional recovery after peripheral nerve injury

Neurosurgery

Volumn 65, Issue SUPPL. 4, 2009, Pages

  Gordon, Tessa ^a   Chan, K Ming ^a   Sulaiman, Olawale A R ^b   Udina, Esther ^a   Amirjani, Nasim ^a   Brushart, Thomas M ^c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b OCHSNER CLINIC FOUNDATION   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Accelerated axon regeneration; Carpal tunnel syndrome; Cyclic adenosine monophosphate and axon regeneration; Electrical stimulation; Peripheral nerve injury; Quantitative outcomes of nerve surgery; Schwann cell denervation

Indexed keywords

CYCLIC AMP; NEUROTROPHIC FACTOR; ROLIPRAM;

CARPAL TUNNEL SYNDROME; CONVALESCENCE; DENERVATION ATROPHY; ELECTROSTIMULATION; FEMORAL NERVE; HUMAN; MEDIAN NERVE; MUSCLE ATROPHY; MUSCLE REINNERVATION; NERVE FIBER DEGENERATION; NERVE FIBER GROWTH; NERVE FIBER TRANSECTION; NERVE REGENERATION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; REVIEW; UPREGULATION;

ANIMALS; CYCLIC AMP; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION THERAPY; GROWTH CONES; HUMANS; NERVE REGENERATION; PERIPHERAL NERVES; PERIPHERAL NERVOUS SYSTEM DISEASES; PHOSPHODIESTERASE INHIBITORS; RATS; RECOVERY OF FUNCTION; ROLIPRAM; TREATMENT OUTCOME;

EID: 70349753738     PISSN: 0148396X     EISSN: None     Source Type: Journal    
DOI: 10.1227/01.NEU.0000335650.09473.D3     Document Type: Review

References (79)

1. Aglah C, Gordon T, Chaves EP: An essential role of cyclic adenosine monophosphate and protein kinase A in neurite outgrowth in cultured rat motoneurons. Abstr Soc Neurosci 30:29, 2005 (abstr).
2. Aguayo AJ, Dickson R, Trecarten J, Attiwell M, Bray GM, Richardson P: Ensheathment and myelination of regenerating PNS fibers by transplanted optic-nerve glia. Neurosci Lett 9:97-104, 1978.
3. Ahlborn P, Schachner M, Irintchev A: One hour electrical stimulation accelerates functional recovery after femoral nerve repair. Exp Neurol 208:137-144, 2007.
4. Aitken JT, Sharman M, Young JZ: Maturation of peripheral nerve fibres with various peripheral connections. J Anat 81:1-22, 1947.
5. al Amood WS, Lewis DM, Schmalbruch H: Effects of chronic electrical stimulation on contractile properties of long-term denervated rat skeletal muscle. J Physiol 441:243-256, 1991.
6. Al-Majed AA, Brushart TM, Gordon T: Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. Eur J Neurosci 12:4381-4390, 2000.
7. Al-Majed AA, Neumann CM, Brushart TM, Gordon T: Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci 20:2602-2608, 2000.
8. Al-Majed AA, Tam SL, Gordon T: Electrical stimulation accelerates and enhances expression of regeneration-associated genes in regenerating rat femoral motoneurons. Cell Mol Neurobiol 24:379-402, 2004.
9. Borisov AB, Dedkov EI, Carlson BM: Interrelations of myogenic response, progressive atrophy of muscle fibers, and cell death in denervated skeletal muscle. Anat Rec 264:203-218, 2001.
10. Boyd JG, Gordon T: The neurotrophin receptors, trkB and p75, differentially regulate motor axonal regeneration. J Neurobiol 49:314-325, 2001.
11. Boyd JG, Gordon T: A dose-dependent facilitation and inhibition of peripheral nerve regeneration by brain-derived neurotrophic factor. Eur J Neurosci 15:613-626, 2002.
12. Boyd JG, Gordon T: Glial cell line-derived neurotrophic factor and brainderived neurotrophic factor sustain the axonal regeneration of chronically axotomized motoneurons in vivo. Exp Neurol 183:610-619, 2003.
13. Boyd JG, Gordon T: Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Mol Neurobiol 27:277-324, 2003.
14. Brushart TM, Hoffman PN, Royall RM, Murinson BB, Witzel C, Gordon T: Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. J Neurosci 22:6631-6638, 2002.
15. Brushart TM, Jari R, Verge V, Rohde C, Gordon T: Electrical stimulation restores the specificity of sensory axon regeneration. Exp Neurol 194:221-229, 2005.
16. Brushart TM, Tarlov EC, Mesulam MM: Specificity of muscle reinnervation after epineurial and individual fascicular suture of the rat sciatic nerve. J Hand Surg [Am] 8:248-253, 1983.
17. Busch SA, Silver J: The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 17:120-127, 2007.
18. Cai D, Qiu J, Cao Z, McAtee M, Bregman BS, Filbin MT: Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J Neurosci 21:4731-4739, 2001.
19. Cai D, Shen Y, De Bellard M, Tang S, Filbin MT: Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 22:89-101, 1999.
20. Cajal SR: Degeneration and Regeneration of the Nervous System (translated by RM May). New York, Oxford University Press, 1928.
21. Calancie B, Molano MR, Broton JG: EMG for assessing the recovery of voluntary movement after acute spinal cord injury in man. Clin Neurophysiol 115:1748-1759, 2004. (Pubitemid 38952942)
22. Carraro U, Catani C, Biral D: Selective maintenance of neurotrophically regulated proteins in denervated rat diaphragm. Exp Neurol 63:468-475, 1979.
23. Carraro U, Catani C, Dalla Libera L: Myosin light and heavy chains in rat gastrocnemius and diaphragm muscles after chronic denervation or reinnervation. Exp Neurol 72:401-412, 1981.
24. Carraro U, Rossini K, Mayr W, Kern H: Muscle fiber regeneration in human permanent lower motoneuron denervation: Relevance to safety and effectiveness of FES-training, which induces muscle recovery in SCI subjects. Artif Organs 29:187-191, 2005.
25. Danielsen N, Kerns JM, Holmquist B, Zhao Q, Lundborg G, Kanje M: Predegenerated nerve grafts enhance regeneration by shortening the initial delay period. Brain Res 666:250-254, 1994.
26. David S, Aguayo AJ: Axonal elongation into peripheral nervous-system "bridges" after central nervous-system injury in adult-rats. Science 214:931-933, 1981.
27. Davies SJ, Field PM, Raisman G: Regeneration of cut adult axons fails even in the presence of continuous aligned glial pathways. Exp Neurol 142:203-216, 1996.
28. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J: Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683, 1997.
29. Davies SJ, Goucher DR, Doller C, Silver J: Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822, 1999.
30. Duchenne de Boulogne: De L'Electrisation Localisé, et de son Application à La Physiologie, à La Pathologie et à La Thérapeutique. Paris, 1855.
31. Eberhardt KA, Irintchev A, Al-Majed AA, Simova O, Brushart TM, Gordon T, Schachner M: BDNF/TrkB signaling regulates HNK-1 carbohydrate expression in regenerating motor nerves and promotes functional recovery after peripheral nerve repair. Exp Neurol 198:500-510, 2006.
32. English AW, Meador W, Carrasco DI: Neurotrophin-4/5 is required for the early growth of regenerating axons in peripheral nerves. Eur J Neurosci 21:2624-2634, 2005.
33. English AW, Schwartz G, Meador W, Sabatier MJ, Mulligan A: Electrical stimulation promotes peripheral axon regeneration by enhanced neuronal neurotrophin signaling. Dev Neurobiol 67:158-172, 2007.
34. Fenrich K, Gordon T: Canadian Association of Neuroscience review: Axonal regeneration in the peripheral and central nervous systems-Current issues and advances. Can J Neurol Sci 31:142-156, 2004.
35. Filbin MT: Recapitulate development to promote axonal regeneration: Good or bad approach? Philos Trans R Soc Lond B Biol Sci 361:1565-1574, 2006.
36. Fu SY, Gordon T: Contributing factors to poor functional recovery after delayed nerve repair: Prolonged axotomy. J Neurosci 15:3876-3885, 1995.
37. Fu SY, Gordon T: Contributing factors to poor functional recovery after delayed nerve repair: Prolonged denervation. J Neurosci 15:3886-3895, 1995.
38. Fu SY, Gordon T: The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol 14:67-116, 1997.
39. Furey MJ, Midha R, Xu QG, Belkas J, Gordon T: Prolonged target deprivation reduces the capacity of injured motoneurons to regenerate. Neurosurgery 60:723-732, 2007.
40. Gao Y, Deng K, Hou J, Bryson JB, Barco A, Nikulina E, Spencer T, Mellado W, Kandel ER, Filbin MT: Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44:609-621, 2004.
41. Gordon T, Pattullo MC: Plasticity of muscle fiber and motor unit types. Exerc Sport Sci Rev 21:331-362, 1993.
42. Gordon T, Sulaiman O, Boyd JG: Experimental strategies to promote functional recovery after peripheral nerve injuries. J Peripher Nerv Syst 8:236-250, 2003.
43. Gordon T, Sulaiman O, Boyd JG: Experimental approaches to promote functional recovery after severe peripheral nerve injuries. Acta Chir Aust Eur Surg 37:193-203, 2005.
44. Gordon T, Yang JF, Ayer K, Stein RB, Tyreman N: Recovery potential of muscle after partial denervation: A comparison between rats and humans. Brain Res Bull 30:477-482, 1993.
45. Gutmann E, Guttmann L, Medawar PB, Young JZ: The rate of regeneration of nerve. J Exp Biol 19:14-44, 1942.
46. Hannila SS, Filbin MT: The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 209:321-332, 2007.
47. Kern H, Rossini K, Carraro U, Mayr W, Vogelauer M, Hoellwarth U, Hofer C: Muscle biopsies show that FES of denervated muscles reverses human muscle degeneration from permanent spinal motoneuron lesion. J Rehabil Res Dev 42 [Suppl 1]:43-53, 2005.
48. Kim DH, Cho YJ, Tiel RL, Kline DG: Outcomes of surgery in 1019 brachial plexus lesions treated at Louisiana State University Health Sciences Center. J Neurosurg 98:1005-1016, 2003.
49. Kim DH, Murovic JA, Tiel RL, Kline DG: Penetrating injuries due to gunshot wounds involving the brachial plexus. Neurosurg Focus 16:E3, 2004.
50. Kline DG, Hudson AR: Nerve Injuries: Operative Results for Major Nerve Injuries, Entrapments and Tumors. Philadelphia, W.B. Saunders, 1995.
51. Kline DG, Kim D, Midha R, Harsh C, Tiel R: Management and results of sciatic nerve injuries: A 24-year experience. J Neurosurg 89:13-23, 1998.
52. Liu BP, Cafferty WB, Budel SO, Strittmatter SM: Extracellular regulators of axonal growth in the adult central nervous system. Philos Trans R Soc Lond B Biol Sci 361:1593-1610, 2006.
53. Mackinnon SE, Doolabh VB, Novak CB, Trulock EP: Clinical outcome following nerve allograft transplantation. Plast Reconstr Surg 107:1419-1429, 2001.
54. McDonald JW, Becker D, Sadowsky CL, Jane JA Sr, Conturo TE, Schultz LM: Late recovery following spinal cord injury. Case report and review of the literature. J Neurosurg 97:252-265, 2002.
55. Nemoto K, Williams HB, Nemoto K, Lough J, Chiu RC: The effects of electrical stimulation on denervated muscle using implantable electrodes. J Reconstr Microsurg 4:251-257, 1988.
56. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI: Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34:885-893, 2002.
57. Nikulina E, Tidwell JL, Dai HN, Bregman BS, Filbin MT: The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc Natl Acad Sci U S A 101:8786-8790, 2004.
58. Nix WA, Hopf HC: Electrical stimulation of regenerating nerve and its effect on motor recovery. Brain Res 272:21-25, 1983.
59. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB: cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10:610-616, 2004.
60. Pockett S, Gavin RM: Acceleration of peripheral nerve regeneration after crush injury in rat. Neurosci Lett 59:221-224, 1985.
61. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT: Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903, 2002.
62. Qiu J, Cai D, Filbin MT: A role for cAMP in regeneration during development and after injury. Prog Brain Res 137:381-387, 2002.
63. Rafuse VF, Gordon T: Self-reinnervated cat medial gastrocnemius muscles. I. Comparisons of the capacity of regenerating nerves to form enlarged motor units after extensive peripheral nerve injuries. J Neurophysiol 75:268-281, 1996.
64. Rafuse VF, Gordon T: Self-reinnervated cat medial gastrocnemius muscles. II. Analysis of the mechanisms and significance of fiber type grouping in reinnervated muscles. J Neurophysiol 75:282-297, 1996.
65. Rafuse VF, Gordon T, Orozco R: Proportional enlargement of motor units after partial denervation of cat triceps surae muscles. J Neurophysiol 68:1261-1276, 1992.
66. Richardson PM, Issa VM, Aguayo AJ: Regeneration of long spinal axons in the rat. J Neurocytol 13:165-182, 1984.
67. Richardson PM, McGuinness UM, Aguayo AJ: Axons from CNS neurons regenerate into PNS grafts. Nature 284:264-265, 1980.
68. Rodriguez FJ, Verdú E, Ceballos D, Navarro X: Nerve guides seeded with autologous Schwann cells improve nerve regeneration. Exp Neurol 161:571-584, 2000.
69. Schmalbruch H, al-Amood WS, Lewis DM: Morphology of long-term denervated rat soleus muscle and the effect of chronic electrical stimulation. J Physiol 441:233-241, 1991.
70. Schwab ME: Nogo and axon regeneration. Curr Opin Neurobiol 14:118-124, 2004.
71. Simova O, Irintchev A, Mehanna A, Liu J, Dihné M, Bächle D, Sewald N, Loers G, Schachner M: Carbohydrate mimics promote functional recovery after peripheral nerve repair. Ann Neurol 60:430-437, 2006.
72. Sulaiman OA, Gordon T: Effects of short- and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia 32:234-246, 2000.
73. Sulaiman OA, Gordon T: Role of chronic Schwann cell denervation in poor functional recovery after peripheral nerve injuries and strategies to combat it. Neurosurgery 65 [Suppl 4]:A105-A114, 2009.
74. Sulaiman WA, Kline DG: Nerve surgery: A review and insights about its future. Clin Neurosurg 53:38-47, 2006.
75. Sulaiman OA, Boyd JG, Gordon T: Axonal regeneration in the peripheral system of mammals, in Kettenmann H, Ransom BR (eds): Neuroglia. Oxford, Oxford University Press, 2005, pp 454-466.
76. Sunderland S: Nerve and Nerve Injuries. Edinburgh, Livingstone, 1978.
77. Witzel C, Rohde C, Brushart TM: Pathway sampling by regenerating peripheral axons. J Comp Neurol 485:183-190, 2005.
78. You S, Petrov T, Chung PH, Gordon T: The expression of the low affinity nerve growth factor receptor in long-term denervated Schwann cells. Glia 20:87-100, 1997.
79. Zhang CG, Ma JJ, Terenghi G, Mantovani C, Wiberg M: Phrenic nerve transfer in the treatment of brachial plexus avulsion: An experimental study of nerve regeneration and muscle morphology in rats. Microsurgery 24:232-240, 2004.