Bioengineered nerve regeneration and muscle reinnervation

Journal of Anatomy

Volumn 209, Issue 4, 2006, Pages 511-526

  Kingham, Paul J ^a   Terenghi, Giorgio ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Larynx; Nerve conduit; Neurotrophic factor; Peripheral nerve injury; Synkinesis

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; COLLAGEN; FIBROBLAST GROWTH FACTOR; FIBRONECTIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEU DIFFERENTIATION FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN 3; NEUROTROPHIN 4; POLYMER;

CELL FUNCTION; CELL SURVIVAL; CONFERENCE PAPER; CONVALESCENCE; DRUG DELIVERY SYSTEM; EXTRACELLULAR MATRIX; HUMAN; LARYNX; LARYNX MUSCLE; MUSCLE CELL; MUSCLE DENERVATION; MUSCLE POTENTIAL; MUSCLE REINNERVATION; NERVE FIBER REGENERATION; NERVE POTENTIAL; NERVE REGENERATION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RECURRENT LARYNGEAL NERVE; SKELETAL MUSCLE; TISSUE ENGINEERING;

AXONS; BIOCOMPATIBLE MATERIALS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LARYNX; MUSCLES; NERVE GROWTH FACTORS; NERVE REGENERATION; RECURRENT LARYNGEAL NERVE; TISSUE ENGINEERING;

EID: 33749171889     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2006.00623.x     Document Type: Conference Paper

References (152)

1. Abe K, Namikawa K, Honma M, et al. (2001) Inhibition of Ras extracellular-signal-regulated kinase (ERK) mediated signaling promotes ciliary neurotrophic factor (CNTF) expression in Schwann cells. J Neurochem 77, 700-703.
2. Abe S, Mizusawa I, Kanno K, et al. (2004) Induction of nerve growth factor mRNA in a rat dorsal root ganglion after application of a tourniquet. Acta Neuropathol (Berl) 108, 183-188.
3. Ahmed Z, Brown RA (1999) Adhesion, alignment, and migration of cultured Schwann cells on ultrathin fibronectin fibres. Cell Motil Cytoskeleton 42, 331-343.
4. Ahmed Z, Brown RA, Ljungberg C, Wiberg M, Terenghi G (1999) Nerve growth factor enhances peripheral nerve regeneration in non-human primates. Scand J Plast Reconstr Surg Hand Surg 33, 393-401.
5. Ahmed Z, Underwood S, Brown RA (2003) Nerve guide material made from fibronectin: Assessment of in vitro properties. Tissue Eng 9, 219-231.
6. Al-Majed AA, Tam SL, Gordon T (2004) Electrical stimulation accelerates and enhances expression of regeneration-associated genes in regenerating rat femoral motoneurons. Cell Mol Neurobiol 24, 379-402.
7. Amano T, Yamakuni T, Okabe N, Sakimura K, Takahashi Y (1991) Production of nerve growth factor in rat skeletal muscle. Neurosci Lett 132, 5-7.
8. Anzil AP, Wernig A (1989) Muscle fibre loss and reinnervation after long-term denervation. J Neurocytol 18, 833-845.
9. Arakawa Y, Sendtner M, Thoenen H (1990) Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: comparison with other neurotrophic factors and cytokines. J Neurosci 10, 3507-3515.
10. Araki K, Shiotani A, Watabe K, Saito K, Moro K, Ogawa K (2006) Adenoviral GDNF gene transfer enhances neurofunctional recovery after recurrent laryngeal nerve injury. Gene Ther 13, 296-303.
11. Archibald SJ, Krarup C, Shefner J, Li ST, Madison RD (1991) A collagen-based nerve guide conduit for peripheral nerve repair: An electrophysiological study of nerve regeneration in rodents and nonhuman primates. J Comp Neurol 306, 685-696.
12. Baichwal RR, Bigbee JW, DeVries GH (1988) Macrophage-mediated myelin-related mitogenic factor for cultured Schwann cells. Proc Natl Acad Sci USA 85, 1701-1705.
13. Bennett DL, Boucher TJ, Armanini MP, et al. (2000) The glial cell line-derived neurotrophic factor family receptor components are differentially regulated within sensory neurons after nerve injury. J Neurosci 20, 427-437.
14. Birchall MA, Bailey M, Barker EV, Rothkotter HJ, Otto K, Macchiarini P (2002) Model for experimental revascularized laryngeal allotransplantation. Br J Surg 89, 1470-1475.
15. Birchall M, Idowu B, Murison P, et al. (2004) Laryngeal abductor muscle reinnervation in a pig model. Acta Otolaryngol 124, 839-846.
16. Bobinac D, Malnar-Dragojevic D, Bajek S, Soic-Vranic T, Jerkovic R (2000) Muscle fiber type composition and morphometric properties of denervated rat extensor digitorum longus muscle. Croat Med J 41, 294-297.
17. Borisov AB, Dedkov EI, Carlson BM (2001) Interrelations of myogenic response, progressive atrophy of muscle fibers, and cell death in denervated skeletal muscle. Anat Rec 264, 203-218.
18. Boudreau-Lariviere C, Sveistrup H, Parry DJ, Jasmin BJ (1996) Ciliary neurotrophic factor: Regulation of acetylcholinesterase in skeletal muscle and distribution of messenger RNA encoding its receptor in synaptic versus extrasynaptic compartments. Neuroscience 73, 613-622.
19. Boyd JG, Gordon T (2001) The neurotrophin receptors, trkB and p75, differentially regulate motor axonal regeneration. J Neurobiol 49, 314-325.
20. Bryan DJ, Holway AH, Wang KK, et al. (2000) Influence of glial growth factor and Schwann cells in a bioresorbable guidance channel on peripheral nerve regeneration. Tissue Eng 6, 129-138.
21. Buller AJ, Eccles JC, Eccles RM (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J Physiol 150, 417-439.
22. Burazin TC, Gundlach AL (1998) Up-regulation of GDNFR-alpha and c-ret mRNA in facial motor neurons following facial nerve injury in the rat. Brain Res Mol Brain Res 55, 331-336.
23. Caiozzo VJ, Wu YZ, Baker MJ, Crumley R (2004) Effects of denervation on cell cycle control in laryngeal muscle. Arch Otolaryngol Head Neck Surg 130, 1056-1068.
24. Capsoni S, Ruberti F, Di Daniel E, Cattaneo A (2000) Muscular dystrophy in adult and aged anti-NGF transgenic mice resembles an inclusion body myopathy. J Neurosci Res 59, 553-560.
25. Carrasco DI, English AW (2003) Neurotrophin 4/5 is required for the normal development of the slow muscle fiber phenotype in the rat soleus. J Exp Biol 206, 2191-2200.
26. Carroll SL, Miller ML, Frohnert PW, Kim SS, Corbett JA (1997) Expression of neuregulins and their putative receptors, ErbB2 and ErbB3, is induced during Wallerian degeneration. J Neurosci 17, 1642-1659.
27. Chen GQ, Wu Q (2005) The application of polyhydroxyalkanoates as tissue engineering materials. Biomaterials 26, 6565-6578.
28. Chen X, Mao Z, Liu S, et al. (2005) Dedifferentiation of adult human myoblasts induced by ciliary neurotrophic factor in vitro. Mol Biol Cell 16, 3140-3151.
29. Ciardelli G, Chiono V (2006) Materials for peripheral nerve regeneration. Macromol Biosci 6, 13-26.
30. Costigan M, Befort K, Karchewski L, et al. (2002) Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3, 16.
31. Crumley RL (1983) Phrenic nerve graft for bilateral vocal cord paralysis. Laryngoscope 93, 425-428.
32. Crumley RL (1989) Laryngeal synkinesis: Its significance to the laryngologist. Ann Otol Rhinol Laryngol 98, 87-92.
33. Curtis R, Adryan KM, Zhu Y, Harkness PJ, Lindsay RM, DiStefano PS (1993) Retrograde axonal transport of ciliary neurotrophic factor is increased by peripheral nerve injury. Nature 365, 253-255.
34. Del Gaudio JM, Sciote JJ (1997) Changes in myosin expression in denervated laryngeal muscle. Ann Otol Rhinol Laryngol 106, 1076-1081.
35. Deng YS, Zhong JH, Zhou XF (2000) BDNF is involved in sympathetic sprouting in the dorsal root ganglia following peripheral nerve injury in rats. Neurotox Res 1, 311-322.
36. Dulor JP, Cambon B, Vigneron P, et al. (1998) Expression of specific white adipose tissue genes in denervation-induced skeletal muscle fatty degeneration. FEBS Lett 439, 89-92.
37. English AW, Meador W, Carrasco DI (2005) Neurotrophin-4/5 is required for the early growth of regenerating axons in peripheral nerves. Eur J Neurosci 21, 2624-2634.
38. Erck C, Meisinger C, Grothe C, Seidl K (1998) Regulation of nerve growth factor and its low-affinity receptor (p75NTR) during myogenic differentiation. J Cell Physiol 176, 22-31.
39. Escandon E, Soppet D, Rosenthal A, et al. (1994) Regulation of neurotrophin receptor expression during embryonic and postnatal development. J Neurosci 14, 2054-2068.
40. Falls DL (2003) Neuregulins and the neuromuscular system: 10 years of answers and questions. J Neurocytol 32, 619-647.
41. Fenrich K, Gordon T (2004) 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.
42. Ferri CC, Moore FA, Bisby MA (1998) Effects of facial nerve injury on mouse motoneurons lacking the p75 low-affinity neurotrophin receptor. J Neurobiol 34, 1-9.
43. Fex S (1970) Functioning remobilization of vocal cords in cats with permanent recurrent laryngeal nerve paresis. Acta Otolaryngol 69, 294-301.
44. Fu AK, Ip FC, Lai KO, Tsim KW, Ip NY (1997) Muscle-derived neurotrophin-3 increases the aggregation of acetylcholine receptors in neuron-muscle co-cultures. Neuroreport 8, 3895-3900.
45. Funakoshi H, Frisen J, Barbany G, et al. (1993) Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123, 455-465.
46. Funakoshi H, Belluardo N, Arenas E, et al. (1995) Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science 268, 1495-1499.
47. Gacek RR, Malmgren LT, Lyon MJ (1977) Localization of adductor and abductor motor nerve fibers to the larynx. Ann Otol Rhinol Laryngol 86, 771-776.
48. Garratt AN, Britsch S, Birchmeier C (2000) Neuregulin, a factor with many functions in the life of a schwann cell. Bioessays 22, 987-996.
49. George EB, Glass JD, Griffin JW (1995) Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J Neurosci 15, 6445-6452.
50. Gillingwater TH, Thomson D, Ribchester RR (2004) Myo-GDNF increases non-functional polyinnervation of reinnervated mouse muscle. Neuroreport 15, 21-25.
51. Goding GS Jr, Al-Sharif KI, McLoon LK (2005) Myonuclear addition to uninjured laryngeal myofibers in adult rabbits. Ann Otol Rhinol Laryngol 114, 552-557.
52. Grant GA, Goodkin R, Kliot M (1999) Evaluation and surgical management of peripheral nerve problems. Neurosurgery 44, 825-839; discussion 839-840.
53. Griesbeck O, Parsadanian AS, Sendtner M, Thoenen H (1995) Expression of neurotrophins in skeletal muscle: Quantitative comparison and significance for motoneuron survival and maintenance of function. J Neurosci Res 42, 21-33.
54. Grimpe B, Silver J (2002) The extracellular matrix in axon regeneration. Prog Brain Res 137, 333-349.
55. Grossman EJ, Roy RR, Talmadge RJ, Zhong H, Edgerton VR (1998) Effects of inactivity on myosin heavy chain composition and size of rat soleus fibers. Muscle Nerve 21, 375-389.
56. Grotzinger J, Kurapkat G, Wollmer A, Kalai M, Rose-John S (1997) The family of the IL-6-type cytokines: Specificity and promiscuity of the receptor complexes. Proteins 27, 96-109.
57. Grounds MD, White JD, Rosenthal N, Bogoyevitch MA (2002) The role of stem cells in skeletal and cardiac muscle repair. J Histochem Cytochem 50, 589-610.
58. Gupta SK, Poduslo JF, Mezei C (1988) Temporal changes in PO and MBP gene expression after crush-injury of the adult peripheral nerve. Brain Res 464, 133-141.
59. Hall S (2005) The response to injury in the peripheral nervous system. J Bone Joint Surg Br 87, 1309-1319.
60. Hammarberg H, Piehl F, Cullheim S, Fjell J, Hokfelt T, Fried K (1996) GDNF mRNA in Schwann cells and DRG satellite cells after chronic sciatic nerve injury. Neuroreport 7, 857-860.
61. Hammarberg H, Piehl F, Risling M, Cullheim S (2000) Differential regulation of trophic factor receptor mRNAs in spinal motoneurons after sciatic nerve transection and ventral root avulsion in the rat. J Comp Neurol 426, 587-601.
62. Hazari A, Wiberg M, Johansson-Ruden G, Green C, Terenghi G (1999a) A resorbable nerve conduit as an alternative to nerve autograft in nerve gap repair. Br J Plast Surg 52, 653-657.
63. Hazari A, Johansson-Ruden G, Junemo-Bostrom K, et al. (1999b) A new resorbable wrap-around implant as an alternative nerve repair technique. J Hand Surg [Br]24, 291-295.
64. Henderson CE, Camu W, Mettling C, et al. (1993) Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363, 266-270.
65. Henderson CE, Phillips HS, Pollock RA, et al. (1994) GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266, 1062-1064.
66. Ho PR, Coan GM, Cheng ET, et al. (1998) Repair with collagen tubules linked with brain-derived neurotrophic factor and ciliary neurotrophic factor in a rat sciatic nerve injury model. Arch Otolaryngol Head Neck Surg 124, 761-766.
67. Hoh JF (2005) Laryngeal muscle fibre types. Acta Physiol Scand 183, 133-149.
68. Hoke A, Gordon T, Zochodne DW, Sulaiman OA (2002) A decline in glial cell-line-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp Neurol 173, 77-85.
69. Hudson TW, Evans GR, Schmidt CE (1999) Engineering strategies for peripheral nerve repair. Clin Plast Surg 26, 617-628.
70. Ito Y, Yamamoto M, Li M, Doyu M, et al. (1998) Differential temporal expression of mRNAs for ciliary neurotrophic factor (CNTF), leukemia inhibitory factor (LIF), interleukin-6 (IL-6), and their receptors (CNTFR alpha, LIFR beta, IL-6R alpha and gp130) in injured peripheral nerves. Brain Res 793, 321-327.
71. Iwase T, Jung CG, Bae H, Zhang M, Soliven B (2005) Glial cell line-derived neurotrophic factor-induced signaling in Schwann cells. J Neurochem 94, 1488-1499.
72. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF (1991) The trk proto-oncogene product: A signal transducing receptor for nerve growth factor. Science 252, 554-558.
73. Katoh-Semba R, Kaisho Y, Shintani A, Nagahama M, Kato K (1996) Tissue distribution and immunocytochemical localization of neurotrophin-3 in the brain and peripheral tissues of rats. J Neurochem 66, 330-337.
74. Kingham PJ, Birchall MA, Burt R, Jones A, Terenghi G (2005a) Reinnervation of laryngeal muscles: A study of changes in myosin heavy chain expression. Muscle Nerve 32, 761-766.
75. Kingham PJ, Birchall MA, Terenghi G (2005b) Neurotrophin expression in laryngeal muscles following denervation and reinnervation. J Peri Nerv Sys 10 (Suppl.), 41.
76. Kirsch M, Terheggen U, Hofmann HD (2003) Ciliary neurotrophic factor is an early lesion-induced retrograde signal for axotomized facial motoneurons. Mol Cell Neurosci 24, 130-138.
77. Kitahara AK, Suzuki Y, Qi P, et al. (1999) Facial nerve repair using a collagen conduit in cats. Scand J Plast Reconstr Surg Hand Surg 33, 187-193.
78. Kopp DM, Trachtenberg JT, Thompson WJ (1997) Glial growth factor rescues Schwann cells of mechanoreceptors from denervation-induced apoptosis. J Neurosci 17, 6697-6706.
79. Labrador RO, Buti M, Navarro X (1998) Influence of collagen and laminin gels concentration on nerve regeneration after resection and tube repair. Exp Neurol 149, 243-252.
80. Lee DA, Zurawel RH, Windebank AJ (1995) Ciliary neurotrophic factor expression in Schwann cells is induced by axonal contact. J Neurochem 65, 564-568.
81. Leibrock J, Lottspeich F, Hohn A, et al. (1989) Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341, 149-152.
82. Levi-Montalcini R, Hamburger V (1951) Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J Exp Zool 116, 321-361.
83. Lie DC, Weis J (1998) GDNF expression is increased in denervated human skeletal muscle. Neurosci Lett 250, 87-90.
84. Lomo T, Westgaard RH, Dahl HA (1974) Contractile properties of muscle: control by pattern of muscle activity in the rat. Proc R Soc Lond B Biol Sci 187, 99-103.
85. MacLennan AJ, Neitzel KL, Devlin BK, et al. (2000) In vivo localization and characterization of functional ciliary neurotrophic factor receptors which utilize JAK-STAT signaling. Neuroscience 99, 761-772.
86. Mahanthappa NK, Anton ES, Matthew WD (1996) Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth. J Neurosci 16, 4673-4683.
87. Malmgren LT, Jones CE, Bookman LM (2001) Muscle fiber and satellite cell apoptosis in the aging human thyroarytenoid muscle: A stereological study with confocal laser scanning microscopy. Otolaryngol Head Neck Surg 125, 34-39.
88. Matheson CR, Carnahan J, Urich JL, Bocangel D, Zhang TJ, Yan Q (1997) Glial cell line-derived neurotrophic factor (GDNF) is a neurotrophic factor for sensory neurons: Comparison with the effects of the neurotrophins. J Neurobiol 32, 22-32.
89. McKay Hart A, Brannstrom T, Wiberg M, Terenghi G (2002) Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat: timecourse of cell death and elimination. Exp Brain Res 142, 308-318.
90. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H (1992) Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: Different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol 119, 45-54.
91. Michel RN, Parry DJ, Dunn SE (1996) Regulation of myosin heavy chain expression in adult rat hindlimb muscles during short-term paralysis: comparison of denervation and tetrodotoxin-induced neural inactivation. FEBS Lett 391, 39-44.
92. Midha R, Munro CA, Dalton PD, Tator CH, Shoichet MS (2003) Growth factor enhancement of peripheral nerve regeneration through a novel synthetic hydrogel tube. J Neurosurg 99, 555-565.
93. Minghetti L, Goodearl AD, Mistry K, Stroobant P (1996) Glial growth factors I-III are specific mitogens for glial cells. J Neurosci Res 43, 684-693.
94. Mittal S, Cohen A, Maysinger D (1994) In vitro effects of brain derived neurotrophic factor released from microspheres. Neuroreport 5, 2577-2582.
95. Mohanna PN, Terenghi G, Wiberg M (2005) Composite PHB-GGF conduit for long nerve gap repair: A long-term evaluation. Scand J Plast Reconstr Surg Hand Surg 39, 129-137.
96. Mootoosamy RC, Dietrich S (2002) Distinct regulatory cascades for head and trunk myogenesis. Development 129, 573-583.
97. Mosahebi A, Fuller P, Wiberg M, Terenghi G (2002) Effect of allogeneic Schwann cell transplantation on peripheral nerve regeneration. Exp Neurol 173, 213-223.
98. Mosahebi A, Woodward B, Wiberg M, Martin R, Terenghi G (2001) Retroviral labeling of Schwann cells: In vitro characterization and in vivo transplantation to improve peripheral nerve regeneration. Glia 34, 8-17.
99. Mosahebi A, Wiberg M, Terenghi G (2003) Addition of fibronectin to alginate matrix improves peripheral nerve regeneration in tissue-engineered conduits. Tissue Eng 9, 209-218.
100. Motoyoshi K, Hyodo M, Yamagata T, Gyo K (2004) Restoring vocal fold movement after transection and immediate suturing of the recurrent laryngeal nerve with local application of basic fibroblast growth factor: An experimental study in the rat. Laryngoscope 114, 1247-1252.
101. Nagano M, Suzuki H (2003) Quantitative analyses of expression of GDNF and neurotrophins during postnatal development in rat skeletal muscles. Neurosci Res 45, 391-399.
102. Nitta A, Ohmiya M, Jin-nouchi T, et al. (1999) Endogenous neurotrophin-3 is retrogradely transported in the rat sciatic nerve. Neuroscience 88, 679-685.
103. Noden DM (1983) The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am J Anat 168, 257-276.
104. Omura T, Sano M, Omura K, et al. (2005) Different expressions of BDNF, NT3, and NT4 in muscle and nerve after various types of peripheral nerve injuries. J Peripher Nerv Syst 10, 293-300.
105. Paniello RC, West SE, Lee P (2001) Laryngeal reinnervation with the hypoglossal nerve. I. Physiology, histochemistry, electromyography, and retrograde labeling in a canine model. Ann Otol Rhinol Laryngol 110, 532-542.
106. Parkinson DB, Langner K, Namini SS, Jessen KR, Mirsky R (2002) beta-Neuregulin and autocrine mediated survival of Schwann cells requires activity of Ets family transcription factors. Mol Cell Neurosci 20, 154-167.
107. Pego AP, Poot AA, Grijpma DW, Feijen J (2001) Copolymers of trimethylene carbonate and epsilon-caprolactone for porous nerve guides: Synthesis and properties. J Biomater Sci Polym Ed 12, 35-53.
108. Perie S, St Guily JL, Callard P, Sebille A (1997) Innervation of adult human laryngeal muscle fibers. J Neurol Sci 149, 81-86.
109. Perry VH, Brown MC, Gordon S (1987) The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J Exp Med 165, 1218-1223.
110. Reusch RN (1995) Low molecular weight complexed poly (3-hydroxybutyrate): A dynamic and versatile molecule in vivo. Can J Microbiol 41 (Suppl. 1), 50-54.
111. Rhee HS, Lucas CA, Hoh JF (2004) Fiber types in rat laryngeal muscles and their transformations after denervation and reinnervation. J Histochem Cytochem 52, 581-590.
112. Saika T, Senba E, Noguchi K, et al. (1991) Effects of nerve crush and transection on mRNA levels for nerve growth factor receptor in the rat facial motoneurons. Brain Res Mol Brain Res 9, 157-160.
113. Saito K, Shiotani A, Watabe K, Moro K, Fukuda H, Ogawa K (2003) Adenoviral GDNF gene transfer prevents motoneuron loss in the nucleus ambiguus. Brain Res 962, 61-67.
114. Sanuki T, Yumoto E, Komori M, Hyodo M (2000) Expression of fibroblast growth factor-2 in the nucleus ambiguus following recurrent laryngeal nerve injury in the rat. Laryngoscope 110, 2128-2134.
115. Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: Gene regulation and functional significance. Physiol Rev 76, 371-423.
116. Seddon HJ (1943) Three types of nerve injury. Brain 66, 237-288.
117. Sendtner M, Carroll P, Holtmann B, Hughes RA, Thoenen H (1994) Ciliary neurotrophic factor. J Neurobiol 25, 1436-1453.
118. Sendtner M, Holtmann B, Hughes RA (1996) The response of motoneurons to neurotrophins. Neurochem Res 21, 831-841.
119. Shiotani A, Flint PW (1998) Myosin heavy chain composition in rat laryngeal muscles after denervation. Laryngoscope 108, 1225-1229.
120. Siegel SG, Patton B, English AW (2000) Ciliary neurotrophic factor is required for motoneuron sprouting. Exp Neurol 166, 205-212.
121. Simon M, Terenghi G, Green CJ, Coulton GR (2000) Differential effects of NT-3 on reinnervation of the fast extensor digitorum longus (EDL) and the slow soleus muscle of rat. Eur J Neurosci 12, 863-871.
122. Simon M, Mann D, Coulton G, Terenghi G (2002) Differential tyrosine kinase C mRNA distribution in extensor digitorum longus and soleus motoneurons in adult rats: Effect of axotomy and neurotrophin-3 treatment. Neurosci Lett 320, 9-12.
123. Simon M, Porter R, Brown R, Coulton GR, Terenghi G (2003) Effect of NT-4 and BDNF delivery to damaged sciatic nerves on phenotypic recovery of fast and slow muscles fibres. Eur J Neurosci 18, 2460-2466.
124. Smith GM, Rabinovsky ED, McManaman JL, Shine HD (1993) Temporal and spatial expression of ciliary neurotrophic factor after peripheral nerve injury. Exp Neurol 121, 239-247.
125. Sobue G, Yamamoto M, Doyu M, Li M, Yasuda T, Mitsuma T (1998) Expression of mRNAs for neurotrophins (NGF, BDNF, and NT-3) and their receptors (p75NGFR, trk, trkB, and trkC) in human peripheral neuropathies. Neurochem Res 23, 821-829.
126. Squinto SP, Stitt TN, Aldrich TH, et al. (1991) trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65, 885-893.
127. Sterne GD, Brown RA, Green CJ, Terenghi G (1997a) Neurotrophin-3 delivered locally via fibronectin mats enhances peripheral nerve regeneration. Eur J Neurosci 9, 1388-1396.
128. Sterne GD, Coulton GR, Brown RA, Green CJ, Terenghi G (1997b) Neurotrophin-3-enhanced nerve regeneration selectively improves recovery of muscle fibers expressing myosin heavy chains 2b. J Cell Biol 139, 709-715.
129. Sundback CA, Shyu JY, Wang Y, et al. (2005) Biocompatibility analysis of poly (glycerol sebacate) as a nerve guide material. Biomaterials 26, 5454-5464.
130. Sunderland S (1951) A classification of peripheral nerve injuries producing loss of function. Brain 74, 491-516.
131. Tang S, Shen YJ, DeBellard ME, et al. (1997) Myelin-associated glycoprotein interacts with neurons via a sialic acid binding site at ARG118 and a distinct neurite inhibition site. J Cell Biol 138, 1355-1366.
132. Terenghi G (1999) Peripheral nerve regeneration and neurotrophic factors. J Anat 194, 1-14.
133. Toews AD, Barrett C, Morell P (1998) Monocyte chemoattractant protein 1 is responsible for macrophage recruitment following injury to sciatic nerve. J Neurosci Res 53, 260-267.
134. Tonra JR, Curtis R, Wong V, et al. (1998) Axotomy upregulates the anterograde transport and expression of brain-derived neurotrophic factor by sensory neurons. J Neurosci 18, 4374-4383.
135. Utley DS, Lewin SL, Cheng ET, Verity AN, Sierra D, Terris DJ (1996) Brain-derived neurotrophic factor and collagen tubulization enhance functional recovery after peripheral nerve transection and repair. Arch Otolaryngol Head Neck Surg 122, 407-413.
136. Viguie CA, Lu DX, Huang SK, Rengen H, Carlson BM (1997) Quantitative study of the effects of long-term denervation on the extensor digitorum longus muscle of the rat. Anat Rec 248, 346-354.
137. Wang L, Copray S, Brouwer N, Meek MF, Kernell D (2002) Regional distribution of slow-twitch muscle fibers after reinnervation in adult rat hindlimb muscles. Muscle Nerve 25, 805-815.
138. Wang MC, Forsberg NE (2000) Effects of ciliary neurotrophic factor (CNTF) on protein turnover in cultured muscle cells. Cytokine 12, 41-48.
139. Wehrwein EA, Roskelley EM, Spitsbergen JM (2002) GDNF is regulated in an activity-dependent manner in rat skeletal muscle. Muscle Nerve 26, 206-211.
140. Wells DG, McKechnie BA, Kelkar S, Fallon JR (1999) Neurotrophins regulate agrin-induced postsynaptic differentiation. Proc Natl Acad Sci USA 96, 1112-1117.
141. Wheeler EF, Bothwell M (1992) Spatiotemporal patterns of expression of NGF and the low-affinity NGF receptor in rat embryos suggest functional roles in tissue morphogenesis and myogenesis. J Neurosci 12, 930-945.
142. Whitworth IH, Brown RA, Dore C, Green CJ, Terenghi G (1995) Orientated mats of fibronectin as a conduit material for use in peripheral nerve repair. J Hand Surg [Br]20, 429-436.
143. Wiberg M, Terenghi G (2003) Will it be possible to produce peripheral nerves? Surg Technol Int 11, 303-310.
144. Wong V, Arriaga R, Ip NY, Lindsay RM (1993) The neurotrophins BDNF, NT-3 and NT-4/5, but not NGF, up-regulate the cholinergic phenotype of developing motor neurons. Eur J Neurosci 5, 466-474.
145. Wu YZ, Crumley RL, Armstrong WB, Caiozzo VJ (2000) New perspectives about human laryngeal muscle: Single-fiber analyses and interspecies comparisons. Arch Otolaryngol Head Neck Surg 126, 857-864.
146. Yao M, Moir MS, Wang MZ, To MP, Terris DJ (1999) Peripheral nerve regeneration in CNTF knockout mice. Laryngoscope 109, 1263-1268.
147. Yoshii S, Oka M (2001) Collagen filaments as a scaffold for nerve regeneration. J Biomed Mater Res 56, 400-405.
148. Zealear DL, Billante CR, Courey MS, et al. (2003) Reanimation of the paralyzed human larynx with an implantable electrical stimulation device. Laryngoscope 113, 1149-1156.
149. Zhang JY, Luo XG, Xian CJ, Liu ZH, Zhou XF (2000) Endogenous BDNF is required for myelination and regeneration of injured sciatic nerve in rodents. Eur J Neurosci 12, 4171-4180.
150. Zhang CG, Ma JJ, Terenghi G, Mantovani C, Wiberg M (2004) 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.
151. Zhou XF, Deng YS, Chie E, et al. (1999) Satellite-cell-derived nerve growth factor and neurotrophin-3 are involved in noradrenergic sprouting in the dorsal root ganglia following peripheral nerve injury in the rat. Eur J Neurosci 11, 1711-1722.
152. Zwick M, Teng L, Mu X, Springer JE, Davis BM (2001) Overexpression of GDNF induces and maintains hyperinnervation of muscle fibers and multiple end-plate formation. Exp Neurol 171, 342-350.