Implantation of neurotrophic factor-treated sensory nerve graft enhances survival and axonal regeneration of motoneurons after spinal root avulsion

Journal of Neuropathology and Experimental Neurology

Volumn 68, Issue 1, 2009, Pages 94-101

  Chu, Tak Ho ^a   Li, Suk Yee ^b   Guo, Anchen ^a   Wong, Wai Man ^a   Yuan, Qiuju ^a   Wu, Wutian ^a,c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Avulsion; Brain derived neurotrophic factor; Ciliary neurotrophic factor; Glial cell line derived neurotrophic factor; Peripheral nerve graft; Pleiotrophin; Regeneration

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CILIARY NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; NEUROTROPHIC FACTOR; PLEIOTROPHIN; SYNDECAN 3; 2 HYDROXY 4,4' DIAMIDINOSTILBENE, METHANESULFONATE SALT; 2-HYDROXY-4,4'-DIAMIDINOSTILBENE, METHANESULFONATE SALT; DIAGNOSTIC AGENT; GROWTH FACTOR RECEPTOR; NERVE GROWTH FACTOR; STILBAMIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVULSION INJURY; CELL SURVIVAL; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; NERVE FIBER REGENERATION; NERVE GRAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SENSORY NERVE; SPINAL CORD MOTONEURON; SPINAL ROOT; TECHNIQUE; ANIMAL; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; METABOLISM; MOTONEURON; NERVE REGENERATION; PATHOLOGY; PERIPHERAL NERVE; PHYSIOLOGY; RADICULOPATHY; SPRAGUE DAWLEY RAT; TIME; TRANSPLANTATION;

ANIMALS; CELL SURVIVAL; DISEASE MODELS, ANIMAL; MALE; MOTOR NEURONS; NERVE GROWTH FACTORS; NERVE REGENERATION; PERIPHERAL NERVES; RADICULOPATHY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GROWTH FACTOR; STILBAMIDINES; TIME FACTORS;

EID: 64049090493     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31819344a9     Document Type: Article

References (59)

1. Narakas AO. The treatment of brachial plexus injuries. Int Orthop 1985; 9:29-36
2. Dunham EA. Obstetrical brachial plexus palsy. Orthop Nurs 2003;22: 106-16
3. Terzis JK, Vekris MD, Soucacos PN. Brachial plexus root avulsions. World J Surg 2001;25:1049-61
4. Koliatsos VE, Price WL, Pardo CA, et al. Ventral root avulsion: An experimental model of death of adult motor neurons. J Comp Neurol 1994;342:35-44
5. Wu W. Expression of nitric-oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry. Exp Neurol 1993;120:153-59
6. Bertelli JA, Ghizoni MF. Brachial plexus avulsion injury repairs with nerve transfers and nerve grafts directly implanted into the spinal cord yield partial recovery of shoulder and elbow movements. Neurosurgery 2003;52:1385-89
7. Carlstedt T. Functional recovery after ventral root avulsion and implantation in the spinal cord. Clin Neurol Neurosurg 1993;95(suppl): S109-S111
8. Carlstedt T, Grane P, Hallin RG, et al. Return of function after spinal cord implantation of avulsed spinal nerve roots. Lancet 1995;346: 1323-25
9. Hsu SP, Shih YH, Huang MC, et al. Repair of multiple cervical root avulsion with sural nerve graft. Injury 2004;35:896-907
10. Frostick SP, Yin Q, Kemp GJ. Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 1998;18:397-405
11. Hoke A, Redett R, Hameed H, et al. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci 2006;26: 9646-55
12. Carlstedt T, Anand P, Htut M, et al. Restoration of hand function and so called Bbreathing arm[ after intraspinal repair of C5-T1 brachial plexus avulsion injury. Case report. Neurosurg Focus 2004;16:E7
13. Gu HY, Chai H, Zhang JY, et al. Survival, regeneration and functional recovery of motoneurons in adult rats by reimplantation of ventral root following spinal root avulsion. Eur J Neurosci 2004;19:2123-31 (Pubitemid 38582201)
14. Chu TH, Du Y, Wu W. Motor nerve graft is better than sensory nerve graft for survival and regeneration of motoneurons after spinal root avulsion in adult rats. Exp Neurol 2008;212:562-65
15. David J. A practical approach to nerve grafting in the upper extremity. In: Slutsky DJ, Hentz VR, eds. Peripheral Nerve Surgery. Practical Applications in the Upper Extremity. Philadelphia, PA: Elsevier B.V., 2006:61-80
16. Millesi H. Nerve grafting. In: Slutsky DJ, Hentz VR, eds. Peripheral Nerve Surgery. Practical Applications in the Upper Extremity. Philadelphia, PA: Elsevier B.V., 2006:39-59
17. Sendtner M, Pei G, Beck M, et al. Developmental motoneuron cell death and neurotrophic factors. Cell Tissue Res 2000;301:71-84
18. Yin QW, Johnson J, Prevette D, et al. Cell death of spinal motoneurons in the chick embryo following deafferentation: Rescue effects of tissue extracts, soluble proteins, and neurotrophic agents. J Neurosci 1994;14: 7629-40
19. Ekestern E. Neurotrophic factors and amyotrophic lateral sclerosis. Neurodegener Dis 2004;1:88-100
20. Wu W, Li L, Yick LW, et al. GDNF and BDNF alter the expression of neuronal NOS, c-Jun, and p75 and prevent motoneuron death following spinal root avulsion in adult rats. J Neurotrauma 2003;20:603-12
21. Yin Q, Kemp GJ, Frostick SP. Neurotrophins, neurones and peripheral nerve regeneration. J Hand Surg [Br] 1998;23:433-37 (Pubitemid 28395753)
22. Oppenheim RW. Neurotrophic survival molecules for motoneurons: An embarrassment of riches. Neuron 1996;17:195-97
23. Chu TH, Wu W. Neurotrophic factor treatment after spinal root avulsion injury. Central Nervous System Agents in Medicinal Chemistry. 2009 (in press)
24. Levi-Montalcini R, Hamburger V. Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J Exp Zool 1951;116:321-61
25. Sendtner M, Holtmann B, Kolbeck R, et al. Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 1992;360:757-59
26. Oppenheim RW, Yin QW, Prevette D, et al. Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 1992;360:755-57
27. Henderson CE, Camu W, Mettling C, et al. Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 1993;363:266-70
28. Henderson CE, Phillips HS, Pollock RA, et al. GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science 1994;266:1062-64
29. Fine EG, Decosterd I, Papaloizos M, et al. GDNF and NGF released by synthetic guidance channels support sciatic nerve regeneration across a long gap. Eur J Neurosci 2002;15:589-601
30. Novikov L, Novikova L, Kellerth JO. Brain-derived neurotrophic factor promotes axonal regeneration and long-term survival of adult rat spinal motoneurons in vivo. Neuroscience 1997;79:765-74
31. Chai H, Wu W, So KF, et al. Long-term effects of a single dose of brain-derived neurotrophic factor on motoneuron survival following spinal root avulsion in the adult rat. Neurosci Lett 1999;274:147-50
32. Zhou LH, Wu W. Survival of injured spinal motoneurons in adult rat upon treatment with glial cell line-derived neurotrophic factor at 2 weeks but not at 4 weeks after root avulsion. J Neurotrauma 2006;23:920-27
33. Zhang J, Lineaweaver WC, Oswald T, et al. Ciliary neurotrophic factor for acceleration of peripheral nerve regeneration: An experimental study. J Reconstr Microsurg 2004;20:323-27
34. Siegel SG, Patton B, English AW. Ciliary neurotrophic factor is required for motoneuron sprouting. Exp Neurol 2000;166:205-12
35. English AW. Cytokines, growth factors and sprouting at the neuromuscular junction. J Neurocytol 2003;32:943-60
36. Lang EM, Schlegel N, Sendtner M, et al. Effects of root replantation and neurotrophic factor treatment on long-term motoneuron survival and axonal regeneration after C7 spinal root avulsion. Exp Neurol 2005;194: 341-54 (Pubitemid 40966994)
37. Wright MC, Son YJ. Ciliary neurotrophic factor is not required for terminal sprouting and compensatory reinnervation of neuromuscular synapses: Re-evaluation of CNTF null mice. Exp Neurol 2007;205: 437-48
38. Li YS, Milner PG, Chauhan AK, et al. Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity. Science 1990;250:1690-94
39. Li YS, Hoffman RM, Le Beau MM, et al. Characterization of the human pleiotrophin gene. Promoter region and chromosomal localization. J Biol Chem 1992;267:26011-16
40. Rauvala H. An 18-kd heparin-binding protein of developing brain that is distinct from fibroblast growth factors. EMBO J 1989;8:2933-41
41. Mi R, Chen W, Hoke A. Pleiotrophin is a neurotrophic factor for spinal motor neurons. Proc Natl Acad Sci U S A 2007;104:4664-69
42. Martin LJ, Kaiser A, Price AC. Motor neuron degeneration after sciatic nerve avulsion in adult rat evolves with oxidative stress and is apoptosis. J Neurobiol 1999;40:185-201
43. Wu W, Han K, Li L, et al. Implantation of PNS graft inhibits the induction of neuronal nitric oxide synthase and enhances the survival of spinal motoneurons following root avulsion. Exp Neurol 1994;129: 335-39
44. Gschwendtner A, Liu Z, Hucho T, et al. Regulation, cellular localization, and function of the p75 neurotrophin receptor (p75NTR) during the regeneration of facial motoneurons. Mol Cell Neurosci 2003;24:307-22
45. Jansen P, Giehl K, Nyengaard JR, et al. Roles for the proneurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat Neurosci 2007;10:1449-57
46. Wu W. Potential roles of gene expression change in adult rat spinal motoneurons following axonal injury: A comparison among c-jun, off-affinity nerve growth factor receptor (LNGFR), and nitric oxide synthase (NOS). Exp Neurol 1996;141:190-200
47. Chu TH, Wu WT. Nitric oxide synthase inhibitor attenuates number of regenerating spinal motoneurons in adult rats. Neuroreport 2006;17: 969-73
48. Hammarberg H, Piehl F, Risling M, et al. Differential regulation of trophic factor receptor mRNAs in spinal motoneurons after sciatic nerve transection and ventral root avulsion in the rat. J Comp Neurol 2000; 426:587-601
49. Huang EJ, Reichardt LF. Trk receptors: Roles in neuronal signal transduction. Annu Rev Biochem 2003;72:609-42
50. Novak KD, Prevette D, Wang S, et al. Hepatocyte growth factor/scatter factor is a neurotrophic survival factor for lumbar but not for other somatic motoneurons in the chick embryo. J Neurosci 2000;20:326-37
51. Muramatsu T. Midkine and pleiotrophin: Two related proteins involved in development, survival, inflammation and tumorigenesis. J Biochem 2002;132:359-71
52. Perez-Pinera P, Chang Y, Deuel TF. Pleiotrophin, a multifunctional tumor promoter through induction of tumor angiogenesis, remodeling of the tumor microenvironment, and activation of stromal fibroblasts. Cell Cycle 2007;6:2877-83
53. Carlstedt T. Approaches permitting and enhancing motoneuron regeneration after spinal cord, ventral root, plexus and peripheral nerve injuries. Curr Opin Neurol 2000;13:683-86
54. Gu YD, Chen DS, Zhang GM, et al. Long-term functional results of contralateral C7 transfer. J Reconstr Microsurg 1998;14:57-59
55. Midha R. Nerve transfers for severe brachial plexus injuries: A review. Neurosurg Focus 2004;16:E5
56. Zhang CW, Lu Q, You SW, et al. CNTF and BDNF have similar effects on retinal ganglion cell survival but differential effects on nitric oxide synthase expression soon after optic nerve injury. Invest Ophthalmol Vis Sci 2005;46:1497-503
57. Leaver SG, Cui Q, Plant GW, et al. AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells. Gene Ther 2006;13:1328-41
58. Blits B, Carlstedt TP, Ruitenberg MJ, et al. Rescue and sprouting of motoneurons following ventral root avulsion and reimplantation combined with intraspinal adenoassociated viral vector-mediated expression of glial cell line-derived neurotrophic factor or brain-derived neurotrophic factor. Exp Neurol 2004;189:303-16
59. Gouin A, Bloch-Gallego E, Tanaka H, et al. Transforming growth factor-beta 3, glial cell line-derived neurotrophic factor, and fibroblast growth factor-2, act in different manners to promote motoneuron survival in vitro. J Neurosci Res 1996;43:454-64