Biology and pathology of nonmyelinating schwann cells

GLIA

Volumn 56, Issue 14, 2008, Pages 1518-1531

  Griffin, John W ^a   Thompson, Wesley J ^b  

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

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Demyelination; Nonmyelinating Schwann cell; Remak bundle; Sprouting and regeneration; Terminal Schwann cell

Indexed keywords

ANIMAL; CYTOLOGY; HUMAN; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE REGENERATION; NEUROMUSCULAR SYNAPSE; NONMYELINATED NERVE; PATHOPHYSIOLOGY; PERIPHERAL NERVOUS SYSTEM; PHYSIOLOGY; REVIEW; SCHWANN CELL; SYMPATHETIC NERVE; ULTRASTRUCTURE;

ANIMALS; HUMANS; NERVE FIBERS, UNMYELINATED; NERVE REGENERATION; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; PERIPHERAL NERVOUS SYSTEM; SCHWANN CELLS; SYMPATHETIC FIBERS, POSTGANGLIONIC; WALLERIAN DEGENERATION;

EID: 58849126462     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20778     Document Type: Article

References (137)

1. Aguayo AJ, Bray GM. 1975. Experimental pathology of unmyelinated nerve fibers. In: Dyck PJ, Thomas PK, Lambert EH, editors. Peripheral neuropathy. Philadelphia: Saunders.
2. Aguayo AJ, Epps J, Charron L, Bray GM. 1976. Multipotentiality of Schwann cells in cross anastomosed and grafted myelinated and unmyelinated nerves: Quantitative microscopy and radioautography. Brain Res 104:1-20.
3. Aguayo AJ, Peyronnard JM, Bray GM. 1973. A quantitative ultrastructural study of regeneration from isolated proximal stumps of transected unmyelinated nerves. J Neuropathol Exp Neurol 32:256-270.
4. Astrow SH, Qiang H, Ko CP. 1998. Perisynaptic Schwann cells at neuromuscular junctions revealed by a novel monoclonal antibody. J Neurocytol 27:667-681.
5. Astrow SH, Son YJ, Thompson WJ. 1994. Differential neural regulation of a neuromuscular junction-associated antigen in muscle fibers and Schwann cells. J Neurobiol 25:937-952.
6. Birks R, Huxley HE, Katz B. 1960a. The fine structure of the neuromuscular junction of the frog. J Physiol 150:134-144.
7. Birks R, Katz B, Miledi R. 1960b. Physiological and structural changes at the amphibian myoneural junction, in the course of nerve degeneration. J Physiol 150:145-168.
8. Bishop DL, Misgeld T, Walsh MK, Gan WB, Lichtman JW. 2004. Axon branch removal at developing synapses by axosome shedding. Neuron 44:651-661.
9. Bradley WG, Asbury AK. 1970. Duration of synthesis phase in neurilemma cells in mouse sciatic nerve during degeneration. Dev Neurol 26:275-282.
10. Brockes JP, Fields KL, Raff MC. 1979. Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve. Brain Res 165:105-118.
11. Brown MC, Holland RL, Hopkins WG. 1981. Motor nerve sprouting. Annu Rev Neurosci 4:17-42.
12. Brown MC, Jansen JK, Van Essen D. 1976. Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol 261:387-422.
13. 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.
14. Cauna N. 1959. The mode of termination of the sensory nerves and its significance. J Comp Neurol 113:169-199.
15. Clemence A, Mirsky R, Jessen KR. 1989. Non-myelin-forming Schwann cells proliferate rapidly during Wallerian degeneration in the rat sciatic nerve. J Neurocytol 18:185-192.
16. Cook MR, Bishop DI. 2004. Structural correlates to synapse reoccupation and axon regeneration at the neuromuscular junction. Soc Neurosci Abs 30:618.610.
17. Court FA, Gillingwater TH, Melrose S, Sherman DL, Greenshields K, Morton AJ, Harris JB, Willison HJ, Ribchester RR. Identity, developmental restriction and reactivity of extralaminar cells capping mouse neuromuscular junctions. J Cell Sci (in press).
18. Court FA, Sherman DL, Pratt T, Garry EM, Ribchester RR, Cottrell DF, Fleetwood-Walker SM, Brophy PJ. 2004. Restricted growth of Schwann cells lacking Cajal bands slows conduction in myelinated nerves. Nature 431:191-195.
19. Couteaux R. 1960. Motor end-plate structure. In: Bourne GH, editor. The structure and function of muscle. New York: Academic Press. pp 337-380.
20. Cragg SJ, Nicholson C, Kume-Kick J, Tao L, Rice ME. 2001. Dopaminemediated volume transmission in midbrain is regulated by distinct extracellular geometry and uptake. J Neurophysiol 85:1761-1771.
21. Diamond J, Holmes M, Coughlin M. 1992. Endogenous NGF, nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J Neurosci 12:1454-1466.
22. Dyck PJ, Lambert EH, Nichols PC. 1971. Quantitative measurement of sensation related to compound action potential and number and sizes of myelinated and unmyelinated fibers of sural nerve in health, Friedrich's ataxia, hereditary sensory neuropathy, and tabes dorsalis. In: Cobb WA, editor. Handbook of electroencephalography and clinical neurophysiology, Vol. 9. Amsterdam: Elsevier. pp 83-118.
23. Eames RA, Gamble HJ. 1970. Schwann cell relationships in normal human cutaneous nerves. J Anat 106:417-435.
24. Ebenezer GJ, McArthur JC, Thomas D, Murinson B, Hauer P, Polydefkis M, Griffin JW. 2007. Denervation of skin in neuropathies: The sequence of axonal and Schwann cell changes in skin biopsies. Brain 130:2703-2714.
25. Engel AG, Lambert EH, Santa T. 1973. Study of long-term anticholinesterase therapy. Effects on neuromuscular transmission and on motor end-plate fine structure. Neurology 23:1273-1281.
26. Feng G, Krejci E, Molgo J, Cunningham JM, Massoulie J, Sanes JR. 1999. Genetic analysis of collagen Q: Roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function. J Cell Biol 144:1349-1360.
27. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
28. Feng Z, Ko CP. 2008. Schwann cells promote synaptogenesis at the neuromuscular junction via transforming growth factor (TGF)-b1. J Neurosci (in press).
29. Ferri CC, Bisby MA. 1999. Improved survival of injured sciatic nerve Schwann cells in mice lacking the p75 receptor. Neurosci Lett 272: 191-194.
30. Garcia A, Combarros O, Calleja J, Berciano J. 1998. Charcot-Marie- Tooth disease type 1A with 17p duplication in infancy and early childhood: A longitudinal clinical and electrophysiologic study. Neurology 50:1061-1067.
31. Garcia ML, Lobsiger CS, Shah SB, Deerinck TJ, Crum J, Young D, Ward CM, Crawford TO, Gotow T, Uchiyama Y, Ellisman MH, Calcutt NA, Cleveland DW. 2003. NF-M is an essential target for the myelin-directed ''outside-in'' signaling cascade that mediates radial axonal growth. J Cell Biol 163:1011-1020.
32. Georgiou J, Robitaille R, Trimble WS, Charlton MP. 1994. Synaptic regulation of glial protein expression in vivo. Neuron 12:443-455.
33. Glass JD, Brushart TM, George EB, Griffin JW. 1993. Prolonged survival of transected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon. J Neurocytol 22:311-321.
34. Griffin JW, Drucker N, Gold BG, Rosenfeld J, Benzaquen M, Charnes LR, Fahnestock KE, Stocks EA. 1987. Schwann cell proliferation and migration during paranodal demyelination. J Neurosci 7:682- 699.
35. Griffin JW, Stocks EA, Fahnestock K, van Praagh A, Trapp BD. 1990. Schwann cell proliferation following lysolecithin-induced demyelination. J Neurocytol 19:367-384.
36. Grinspan JB, Marchionni MA, Reeves M, Coulaloglou M, Scherer SS. 1996. Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: Neuregulin receptors and the role of neuregulins. J Neurosci 16:6107-6118.
37. Gutmann E, Young JZ. 1944. The re-innervation of muscle after various periods of atrophy. J Anat 78:15-43.
38. Harrisingh MC, Perez-Nadales E, Parkinson DB, Malcolm DS, Mudge AW, Lloyd AC. 2004. The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation. EMBO J 23:3061-3071.
39. Hayworth CR, Moody SE, Chodosh LA, Krieg P, Rimer M, Thompson WJ. 2006. Induction of neuregulin signaling in mouse schwann cells in vivo mimics responses to denervation. J Neurosci 26:6873-6884.
40. Heath JW. 1982. Double myelination of axons in the sympathetic nervous system. J Neurocytol 11:249-262.
41. Hess DM, Scott MO, Potluri S, Pitts EV, Cisterni C, Balice-Gordon RJ. 2007. Localization of TrkC to Schwann cells and effects of neurotrophin- 3 signaling at neuromuscular synapses. J Comp Neurol 501: 465-482.
42. Heuser JE, Reese TS. 1973. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315-344.
43. Hillarp N, Olivecrona H. 1946. The role played by the axon and the Schwann cells in the degree of myelination of the peripheral nerve fibre. Acta Anat 2:17-32.
44. Hisanaga S, Hirokawa N. 1989. The effects of dephosphorylation on the structure of the projections of neurofilament. J Neurosci 9:959-966.
45. Hoke A, Redett R, Hameed H, Jari R, Zhou C, Li ZB, Griffin JW, Brushart TM. 2006. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci 26:9646-9655.
46. Holland NR, Crawford TO, Hauer P, Cornblath DR, Griffin JW, McArthur JC. 1998. Small-fiber sensory neuropathies: Clinical course and neuropathology of idiopathic cases. Ann Neurol 44:47-59.
47. Hsieh ST, Choi S, Lin WM, Chang YC, McArthur JC, Griffin JW. 1996. Epidermal denervation and its effects on keratinocytes and Langerhans cells. J Neurocytol 25:513-524.
48. Hsieh ST, Kidd GJ, Crawford TO, Xu Z, Lin WM, Trapp BD, Cleveland DW, Griffin JW. 1994. Regional modulation of neurofilament organization by myelination in normal axons. J Neurosci 14:6392- 6401.
49. Huang JK, Phillips GR, Roth AD, Pedraza L, Shan W, Belkaid W, Mi S, Fex-Svenningsen A, Florens L, Yates JR III, Colman DR. 2005. Glial membranes at the node of Ranvier prevent neurite outgrowth. Science 310:1813-1817.
50. Jahromi BS, Robitaille R, Charlton MP. 1992. Transmitter release increases intracellular calcium in perisynaptic Schwann cells in situ. Neuron 8:1069-1077.
51. Jirmanova I. 1975. Ultrastructure of motor end-plates during pharmacologically- induced degeneration and subsequent regeneration of skeletal muscle. J Neurocytol 4:141-155.
52. Julien JP, Mushynski WE. 1983. The distribution of phosphorylation sites among identified proteolytic fragments of mammalian neurofilaments. J Biol Chem 258:4019-4025.
53. Kang H, Lubischer JL, Newman CS, Thompson WJ, Krieg PA. 2000. In vivo imaging of terminal Schwann cells using GFP expressing transgenic mice. Soc Neurosci Abs 26:703.2.
54. Kang H, Tian L, Son YJ, Zuo Y, Procaccino D, Love F, Hayworth C, Trachtenberg J, Mikesh M, Sutton L, Ponomareva O, Mignone J, Enikolopov G, Rimer M, Thompson W. 2007. Regulation of the intermediate filament protein nestin at rodent neuromuscular junctions by innervation and activity. J Neurosci 27:5948-5957.
55. Karpati G, Engel WK. 1968. ''Type grouping'' in skeletal muscles after experimental reinnervation. Neurology 18:447-455.
56. Konishi T. 1985. Electrical excitability of motor nerve terminals in the mouse. J Physiol 366:411-421.
57. Konishi T. 1994. Activity-dependent regulation of inwardly rectifying potassium currents in non-myelinating Schwann cells in mice. J Physiol 474:193-202.
58. Krajewski KM, Lewis RA, Fuerst DR, Turansky C, Hinderer SR, Garbern J, Kamholz J, Shy ME. 2000. Neurological dysfunction and axonal degeneration in Charcot-Marie-Tooth disease type 1A. Brain 123:1516-1527.
59. Letinsky MS, Fischbeck KH, McMahan UJ. 1976. Precision of reinnervation of original postsynaptic sites in frog muscle after a nerve crush. J Neurocytol 5:691-718.
60. Lewis RA, Sumner AJ. 1999. Electrophysiologic features of inherited demyelinating neuropathies: A reappraisal. Ann N Y Acad Sci 883: 321-335.
61. Love FM, Son YJ, Thompson WJ. 2003. Activity alters muscle reinnervation and terminal sprouting by reducing the number of Schwann cell pathways that grow to link synaptic sites. J Neurobiol 54:566- 576.
62. Love FM, Thompson WJ. 1998. Schwann cells proliferate at rat neuromuscular junctions during development and regeneration. J Neurosci 18:9376-9385.
63. Lubischer JL, Bebinger DM. 1999. Regulation of terminal Schwann cell number at the adult neuromuscular junction. J Neurosci 19: RC46.
64. Lubischer JL, Thompson WJ. 1999. Neonatal partial denervation results in nodal but not terminal sprouting and a decrease in efficacy of remaining neuromuscular junctions in rat soleus muscle. J Neurosci 19:8931-8944.
65. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. 2006. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50:869- 881.
66. Manitt C, Colicos MA, Thompson KM, Rousselle E, Peterson AC, Kennedy TE. 2001. Widespread expression of netrin-1 by neurons and oligodendrocytes in the adult mammalian spinal cord. J Neurosci 21:3911-3922.
67. McMahan UJ, Spitzer NC, Peper K. 1972. Visual identification of nerve terminals in living isolated skeletal muscle. Proc R Soc Lond B Biol Sci 181:421-430.
68. Mehta A, Reynolds ML, Woolf CJ. 1993. Partial denervation of the medial gastrocnemius muscle results in growth-associated protein-43 immunoreactivity in sprouting axons and Schwann cells. Neuroscience 57:433-442.
69. Meier C, Parmantier E, Brennan A, Mirsky R, Jessen KR. 1999. Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor, neurotrophin-3, and platelet-derived growth factor-BB. J Neurosci 15:3847-3859.
70. Miledi R, Slater CR. 1968. Electrophysiology and electron-microscopy of rat neuromuscular junctions after nerve degeneration. Proc R Soc Lond B Biol Sci 169:289-306.
71. Miledi R, Slater CR. 1970. On the degeneration of rat neuromuscular junctions after nerve section. J Physiol 207:507-528.
72. Milner LD, Rafuse VF, Landmesser LT. 1998. Selective fasciculation and divergent pathfinding decisions of embryonic chick motor axons projecting to fast and slow muscle regions. J Neurosci 18:3297-3313.
73. Miner JH, Go G, Cunningham J, Patton BL, Jarad G. 2006. Transgenic isolation of skeletal muscle and kidney defects in laminin b2 mutant mice: Implications for Pierson syndrome. Development 133: 967-975.
74. Morfini G, Szebenyi G, Brown H, Pant HC, Pigino G, DeBoer S, Beffert U, Brady ST. 2004. A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. EMBO J 23: 2235-2245.
75. Murinson BB, Archer DR, Li Y, Griffin JW. 2005a. Degeneration of myelinated efferent fibers prompt mitosis in Schwann cells of uninjured C-fiber afferents. J Neurosci 25:1179-1187.
76. Murinson BB, Griffin JW. 2004. C-fiber structure varies with location in peripheral nerve. J Neuropathol Exp Neurol 63:246-254.
77. Murinson BB, Hoffman PN, Banihashemi MR, Meyer RA, Griffin JW. 2005b. C-fiber (Remak) bundles contain both isolectin B4-binding and calcitonin gene-related peptide-positive axons. J Comp Neurol 484:392-402.
78. Nageotte J. 1922. L'Organisation de la matiere dans ses rapports avec la vie. Libraire F, Alcan, Paris.
79. Nehlig A, Coles JA. 2007. Cellular pathways of energy metabolism in the brain: Is glucose used by neurons or astrocytes? Glia 55:1238- 1250.
80. Nguyen QT, Sanes JR, Lichtman JW. 2002. Pre-existing pathways promote precise projection patterns. Nat Neurosci 5:861-867.
81. Nishimune H, Sanes JR, Carlson SS. 2004. A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432:580-587.
82. Nixon RA, Paskevich PA, Sihag RK, Thayer CY. 1994. Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: Influences on regional neurofilament accumulation, interneurofilament spacing, and axon caliber. J Cell Biol 126:1031-1046.
83. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP. 1995. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/ laminin b2. Nature 374:258-262.
84. Oaklander AL, Miller MS, Spencer PS. 1987. Rapid anterograde spread of premitotic activity along degenerating cat sciatic nerve. J Neurochem 48:111-114.
85. Ochea J, Mair WGP. 1969. The normal sural nerve in man. I. Ultrastructure and numbers of fibres and cells. Acta Neuropathol 13:197- 216.
86. Patton BL, Chiu AY, Sanes JR. 1998. Synaptic laminin prevents glial entry into the synaptic cleft. Nature 393:698-701.
87. Pellegrino RG, Politis MJ, Ritchie JM, Spencer PS. 1986. Events in degenerating cat peripheral nerve: Induction of Schwann cell S phase and its relation to nerve fibre degeneration. J Neurocytol 15:17-28.
88. Peng HB, Yang JF, Dai Z, Lee CW, Hung HW, Feng ZH, Ko CP. 2003. Differential effects of neurotrophins and schwann cell-derived signals on neuronal survival/growth and synaptogenesis. J Neurosci 23: 5050-5060.
89. Peng YB, Ringkamp M, Campbell JN, Meyer RA. 1999. Electrophysiological assessment of the cutaneous arborization Adelta-fiber nociceptors. J Neurophysiol 82:1164-1177.
90. Peper K, Dreyer F, Sandri C, Akert K, Moor H. 1974. Structure and ultrastructure of the frog motor endplate. A freeze-etching study. Cell Tissue Res 149:437-455.
91. Perez VJ, Moore BW. 1968. Wallerian degeneration in rabbit tibial nerve: Changes in amounts of the S-100 protein. J Neurochem 15: 971-977.
92. Peters A, Muir AR. 1959. The relationship between axons and Schwann cells during development of peripheral nerves in the rat. Q J Exp Physiol Cogn Med Sci 44:117-130.
93. Petratos S, Butzkueven H, Shipham K, Cooper H, Bucci T, Reid K, Lopes E, Emery B, Cheema SS, Kilpatrick TJ. 2003. Schwann cell apoptosis in the postnatal axotomized sciatic nerve is mediated via NGF through the low-affinity neurotrophin receptor. J Neuropathol Exp Neurol 62:398-411.
94. Pinard A, Levesque S, Vallee J, Robitaille R. 2003. Glutamatergic modulation of synaptic plasticity at a PNS vertebrate cholinergic synapse. Eur J Neurosci 18:3241-3250.
95. Quick DC, Kennedy WR, Donaldson L. 1979. Dimensions of myelinated nerve fibers near the motor and sensory terminals in cat tenuissimus muscles. Neuroscience 4:1089-1096.
96. Rajan B, Polydefkis M, Hauer P, Griffin JW, McArthur JC. 2003. Epidermal reinnervation after intracutaneous axotomy in man. J Comp Neurol 457:24-36.
97. Rao MV, Campbell J, Yuan A, Kumar A, Gotow T, Uchiyama Y, Nixon RA. 2003. The neurofilament middle molecular mass subunit carboxyl- terminal tail domains is essential for the radial growth and cytoskeletal architecture of axons but not for regulating neurofilament transport rate. J Cell Biol 163:1021-1031.
98. Reddy LV, Koirala S, Sugiura Y, Herrera AA, Ko CP. 2003. Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron 40:563-580.
99. Reist NE, Smith SJ. 1992. Neurally evoked calcium transients in terminal Schwann cells at the neuromuscular junction. Proc Natl Acad Sci USA 89:7625-7629.
100. Remak R. 1838. Observationes anatomicae et microscopicae de systematis nervosi structura. Berlin: Suptibus Formis Reimerianis.
101. Reynolds ML, Woolf CJ. 1992. Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. J Neurocytol 21:50-66.
102. Robert A, Jirounek P. 1994. Uptake of potassium by nonmyelinating Schwann cells induced by axonal activity. J Neurophysiol 72:2570-2579.
103. Robert A, Jirounek P. 1998. Axonal and glial currents activated during the post-tetanic hyperpolarization in non-myelinated nerve. Pflugers Arch 436:529-537.
104. Robertson JD. 1956. The ultrastructure of a reptilian myoneural junction. J Biophys Biochem Cytol 2:381-394.
105. Robitaille R. 1998. Modulation of synaptic efficacy and synaptic depression by glial cells at the frog neuromuscular junction. Neuron 21: 847-855.
106. Sanes JR, Hunter DD, Green TL, Merlie JP. 1990. S-laminin. Cold Spring Harb Symp Quant Biol 55:419-430.
107. Simpson SA, Young JZ. 1945. Regeneration of fibre diameter after cross-unions of visceral and somatic nerves. J Anat 79:48-65.
108. Smith RS, Koles ZJ. 1970. Myelinated nerve fibers: Computed effect of myelin thickness on conduction velocity. Am J Physiol 219:1256-1286.
109. Son Y-J, Thompson WJ. 1995a. Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14:133-141.
110. Son Y-J, Thompson WJ. 1995b. Schwann cell processes guide regeneration of peripheral axons. Neuron 14:125-132.
111. Stoll G, Griffin JW, Li CY, Trapp BD. 1989. Wallerian degeneration in the peripheral nervous system: Participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 18:671-683.
112. Sulaiman OA, Gordon T. 2000. Effects of short- and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia 32:234-246.
113. Sulaiman OA, Midha R, Munro CA, Matsuyama T, Al-Majed A, Gordon T. 2002. Chronic Schwann cell denervation and the presence of a sensory nerve reduce motor axonal regeneration. Exp Neurol 176:342- 354.
114. Syroid DE, Maycox PJ, Soilu-Hanninen M, Petratos S, Bucci T, Burrola P, Murray S, Cheema S, Lee KF, Lemke G, Kilpatrick TJ. 2000. Induction of postnatal schwann cell death by the low-affinity neurotrophin receptor in vitro and after axotomy. J Neurosci 20:5741-5747.
115. Taniuchi M, Clark HB, Schweitzer JB, Johnson EM. 1988. Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: Ultrastructural location, suppression by axonal contact, and binding properties. J Neurosci 8:664-681.
116. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, Xu X, Esper RM, Loeb JA, Shrager P, Chao MV, Falls DL, Role L, Salzer JL. 2005. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47:681-694.
117. Theriault M, Dort J, Sutherland G, Zochodne DW. 1998. A prospective quantitative study of sensory deficits after whole sural nerve biopsies in diabetic and nondiabetic patients. Surgical approach and the role of collateral sprouting. Neurology 50:480-484.
118. Todd KJ, Auld DS, Robitaille R. 2007. Neurotrophins modulate neuronglia interactions at a vertebrate synapse. Eur J Neurosci 25:1287-1296.
119. Trachtenberg JT, Thompson WJ. 1996. Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379:174-177.
120. Trachtenberg JT, Thompson WJ. 1997. Nerve terminal withdrawal from rat neuromuscular junctions induced by neuregulin and Schwann cells. J Neurosci 17:6243-6255.
121. Trapp BD, Quarles RH. 1982. Presence of the myelin-associated glycoprotein correlates with alterations in the periodicity of peripheral myelin. J Cell Biol 92:877-882.
122. Ullian EM, Harris BT, Wu A, Chan JR, Barres BA. 2004. Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture. Mol Cell Neurosci 25:241-251.
123. Vega C, Martiel JL, Drouhault D, Burckhart MF, Coles JA. 2003. Uptake of locally applied deoxyglucose, glucose and lactate by axons and Schwann cells of rat vagus nerve. J Physiol 546:551-564.
124. Vega C, Poitry-Yamate CL, Jirounek P, Tsacopoulos M, Coles JA. 1998. Lactate is released and taken up by isolated rabbit vagus nerve during aerobic metabolism. J Neurochem 71:330-337.
125. Walsh MK, Lichtman JW. 2003. In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron 37:67-73.
126. Wang SS, Shultz JR, Burish MJ, Harrison KH, Hof PR, Towns LC, Wagers MW, Wyatt KD. 2008. Functional trade-offs in white matter axonal scaling. J Neurosci 28:4047-4056.
127. Watts RJ, Hoopfer ED, Luo L. 2003. Axon pruning during Drosophila metamorphosis: Evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38:871-885.
128. Waxman SG. 1980. Determinants of conduction velocity in myelinated nerve fiber. Muscle Nerve 3:141-150.
129. Weddell G, Guttmann L, Gutman E. 1941. The local extension of nerve fibres into denervated areas of skin. J Neurol Psychiatry 4: 206-225.
130. Weinberg HJ, Spencer PS. 1975. Studies on the control of myelogenesis. I. Myelination of regenerating axons after entry into a foreign myelinated nerve. J Neurocytol 4:395-418.
131. Wyatt KD, Tanapat P, Wang SS. 2005. Speed limits in the cerebellum: Constraints from myelinated and unmyelinated parallel fibers. Eur J Neurosci 21:2285-2290.
132. Yang JF, Cao G, Koirala S, Reddy LV, Ko CP. 2001. Schwann cells express active agrin and enhance aggregation of acetylcholine receptors on muscle fibers. J Neurosci 21:9572-9584.
133. Yin X, Crawford TO, Griffin JW, Tu P, Lee VMY, Li C, Roder J, Trapp BD. 1998. Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J Neurosci 18:1953-1962.
134. Young P, Nie J, Wang X, McGlade CJ, Rich MM, Feng G. 2005. LNX1 is a perisynaptic Schwann cell specific E3 ubiquitin ligase that interacts with ErbB2. Mol Cell Neurosci 30:238-248.
135. Zanazzi G, Einheber S, Westreich R, Hannocks MJ, Bedell-Hogan D, Marchionni MA, Salzer JL. 2001. Glial growth factor/neuregulin inhibits Schwann cell myelination and induces demyelination. J Cel Biol 152:1289-1299.
136. Zhou L, Zhang CL, Messing A, Chiu SY. 1998. Temperature-sensitive neuromuscular transmission in Kv1.1 null mice: Role of potassium channels under the myelin sheath in young nerves. J Neurosci 18:7200-7215.
137. Zuo Y, Lubischer JL, Kang H, Tian L, Mikesh M, Marks A, Scofield VL, Maika S, Newman C, Krieg P, Thompson WJ. 2004. Fluorescent proteins expressed in mouse transgenic lines mark subsets of glia, neurons, macrophages, and dendritic cells for vital examination. J Neurosci 24:10999-11009.