Neuregulin-1 controls an endogenous repair mechanism after spinal cord injury

Brain

Volumn 139, Issue 5, 2016, Pages 1394-1416

  Bartus, Katalin ^a   Galino, Jorge ^b   James, Nicholas D ^a   Hernandez Miranda, Luis R ^c   Dawes, John M ^b   Fricker, Florence R ^b   Garratt, Alistair N ^c,d   McMahon, Stephen B ^a   Ramer, Matt S ^e   Birchmeier, Carmen ^c   Bennett, David L H ^b   Bradbury, Elizabeth J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

axon degeneration; demyelination; remyelination; spinal cord injury; transgenic model

Indexed keywords

CELL DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN; MYELIN; NEU DIFFERENTIATION FACTOR; ISOPROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AXON; CELL PROLIFERATION; CONTROLLED STUDY; CONTUSION; DEMYELINATION; DORSAL ROOT; FEMALE; IMMUNOHISTOCHEMISTRY; INCLINED BEAM WALKING TEST; LOCOMOTION; MOUSE; NERVE CONDUCTION; NERVE FIBER DEGENERATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; RAT; REMYELINIZATION; SCHWANN CELL; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; ANIMAL; BIOSYNTHESIS; CONVALESCENCE; DEMYELINATING DISEASE; GENETICS; METABOLISM; MOTOR PERFORMANCE; MUTANT MOUSE STRAIN; MYELIN SHEATH; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD; SPINAL CORD REGENERATION; ULTRASTRUCTURE;

ANIMALS; AXONS; CELL PROLIFERATION; DEMYELINATING DISEASES; FEMALE; MICE; MICE, MUTANT STRAINS; MOTOR SKILLS; MYELIN SHEATH; NEURAL CONDUCTION; NEUREGULIN-1; PROTEIN ISOFORMS; RATS; RECOVERY OF FUNCTION; SCHWANN CELLS; SPINAL CORD; SPINAL CORD INJURIES; SPINAL CORD REGENERATION;

EID: 84966665275     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aww039     Document Type: Article

References (107)

1. Assinck PL, Duncan G, Plemel J, Lee M, Liu J, Bergles D, et al. PDGFR--positive progenitor cells form myelinating oligodendrocytes and Schwann cells following contusion spinal cord injury. Society for Neuroscience Abstract 2015, Program No. 338.03. Chicago; 2015.
2. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 2006; 23: 635-59. May;
3. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, et al. Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 1997; 148: 453-63.
4. Beattie MS, Harrington AW, Lee R, Kim JY, Boyce SL, Longo FM, et al. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 2002; 36: 375-86.
5. Bermingham-McDonogh O, Xu YT, Marchionni MA, Scherer SS. Neuregulin expression in PNS neurons: isoforms and regulation by target interactions. Mol Cell Neurosci 1997; 10: 184-95.
6. Birchmeier C, Nave KA. Neuregulin-1, a key axonal signal that drives Schwann cell growth and differentiation. Glia 2008; 56: 1491-7.Nov 1;
7. Bjartmar C, Kidd G, Mork S, Rudick R, Trapp BD. Neurological disability correlates with spinal cord axonal loss and reduced N-acetyl aspartate in chronic multiple sclerosis patients. Ann Neurol 2000, 48, 893-901.
8. Black JA, Waxman SG, Smith KJ. Remyelination of dorsal column axons by endogenous Schwann cells restores the normal pattern of Nav1.6 and Kv1.2 at nodes of Ranvier. Brain 2006; 129: 1319-29.
9. Blight AR, Decrescito V. Morphometric analysis of experimental spinal cord injury in the cat: the relation of injury intensity to survival of myelinated axons. Neuroscience 1986; 19: 321-41. Sep;
10. Blight AR, Young W. Central axons in injured cat spinal cord recover electrophysiological function following remyelination by Schwann cells. J Neurol Sci 1989; 91: 15-34. Jun;
11. Bresnahan JC. An electron-microscopic analysis of axonal alterations following blunt contusion of the spinal cord of the rhesus monkey (Macaca mulatta). J Neurol Sci 1978; 37: 59-82. Jun;
12. Brinkmann BG, Agarwal A, Sereda MW, Garratt AN, Muller T, Wende H, et al. Neuregulin-1/ErbB signaling serves distinct functions in myelination of the peripheral and central nervous system. Neuron 2008; 59: 581-95.
13. Bruce JH, Norenberg MD, Kraydieh S, Puckett W, Marcillo A, Dietrich D. Schwannosis: role of gliosis and proteoglycan in human spinal cord injury. J Neurotrauma 2000; 17: 781-8. Sep;
14. Bunge MB, Bunge RP, Ris H. Ultrastructural study of remyelination in an experimental lesion in adult cat spinal cord. J Biophys Biochem Cytol 1961; 10: 67-94. May;
15. Bunge RP Bunge MB, Rish H. Electron microscopic study of demyelination in an experimentally induced lesion in adult cat spinal cord. J Biophys Biochem Cytol 1960; 7: 685-96.
16. Bunge RP, Puckett WR, Becerra JL, Marcillo A, Quencer RM. Observations on the pathology of human spinal cord injury: a review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv Neurol 1993; 59: 75-89.
17. Buss A, Pech K, Merkler D, Kakulas BA, Martin D, Schoenen J, et al. Sequential loss of myelin proteins during Wallerian degeneration in the human spinal cord. Brain 2005; 128: 356-64. Feb;
18. Butt AM, Berry M. Oligodendrocytes and the control of myelination in vivo: new insights from the rat anterior medullary velum. J Neurosci Res 2000; 59: 477-88.
19. Butt AM, Ibrahim M, Ruge FM, Berry M. Biochemical subtypes of oligodendrocyte in the anterior medullary velum of the rat as revealed by the monoclonal antibody Rip. Glia 1995; 14: 185-97.
20. Calvo M, Zhu N, Tsantoulas C, Ma Z, Grist J, Loeb JA, et al. Neuregulin-ErbB signaling promotes microglial proliferation and chemotaxis contributing to microgliosis and pain after peripheral nerve injury. J Neurosci 2010; 30: 5437-50.
21. Cannon B. Sensation and loss. Nature 2013; 503: S2-3.
22. Carroll SL, Miller ML, Frohnert PW, Kim SS, Corbett JA. Expression of neuregulins and their putative receptors, ErbB2 and ErbB3, is induced during Wallerian degeneration. J Neurosci 1997; 17: 1642-59.
23. Cheret C, Willem M, Fricker FR, Wende H, Wulf-Goldenberg A, Tahirovic S, et al. Bace1 and Neuregulin-1 cooperate to control formation and maintenance of muscle spindles. EMBO J 2013; 32: 2015-28.
24. Chevalier Z, Kennedy P, Sherlock O. Spinal cord injury, coping and psychological adjustment: a literature review. Spinal Cord 2009; 47: 778-82.
25. Cohen JA, Yachnis AT, Arai M, Davis JG, Scherer SS. Expression of the neu proto-oncogene by Schwann cells during peripheral nerve development and Wallerian degeneration. J Neurosci Res 1992; 31: 622-34.
26. Corfas G, Rosen KM, Aratake H, Krauss R, Fischbach GD. Differential expression of ARIA isoforms in the rat brain. Neuron 1995; 14: 103-15.
27. Cornbrooks CJ, Carey DJ, McDonald JA, Timpl R, Bunge RP. In vivo and in vitro observations on laminin production by Schwann cells. Proc Natl Acad Sci USA 1983; 80: 3850-4. Jun;
28. Croslan DR, Schoell MC, Ford GD, Pulliam JV, Gates A, Clement CM, et al. Neuroprotective effects of neuregulin-1 on B35 neuronal cells following ischemia. Brain Res 2008; 1210: 39-47.
29. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 1997; 3: 73-6. Jan;
30. Dietz V, Fouad K. Restoration of sensorimotor functions after spinal cord injury. Brain 2014; 137: 654-67.
31. Duncan ID, Brower A, Kondo Y, Curlee JF Jr, Schultz RD. Extensive remyelination of the CNS leads to functional recovery. Proc Natl Acad Sci USA 2009; 106: 6832-6.
32. Elkhal A, Tunggal L, Aumailley M. Fibroblasts contribute to the deposition of laminin 5 in the extracellular matrix. Exp Cell Res 2004; 296: 223-30.
33. Falls DL. Neuregulins: functions, forms, and signaling strategies. Exp Cell Res 2003; 284: 14-30.
34. Fawcett JW, Curt A, Steeves JD, Coleman WP, Tuszynski MH, Lammertse D, et al. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: spontaneous recovery after spinal cord injury and statistical power needed for therapeutic clinical trials. Spinal Cord 2007; 45: 190-205.
35. Fehlings MG, Skaf G. A review of the pathophysiology of cervical spondylotic myelopathy with insights for potential novel mechanisms drawn from traumatic spinal cord injury. Spine 1998; 23: 2730-7.
36. Felts PA, Smith KJ. Conduction properties of central nerve fibers remyelinated by Schwann cells. Brain Res 1992; 574: 178-92.
37. Felts PA, Smith KJ. Blood-brain barrier permeability in astrocyte-free regions of the central nervous system remyelinated by Schwann cells. Neuroscience 1996; 75: 643-55.
38. Fitch MT, Silver J. CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp Neurol 2008; 209: 294-301.
39. Fleck D, van Bebber F, Colombo A, Galante C, Schwenk BM, Rabe L, et al. Dual cleavage of neuregulin 1 type III by BACE1 and ADAM17 liberates its EGF-like domain and allows paracrine signaling. J Neurosci 2013; 33: 7856-69.
40. Franklin RJ, Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008; 9: 839-55.
41. Fricker FR, Antunes-Martins A, Galino J, Paramsothy R, La Russa F, Perkins J, et al. Axonal neuregulin 1 is a rate limiting but not essential factor for nerve remyelination. Brain 2013; 136: 2279-97.
42. Fricker FR, Bennett DL. The role of neuregulin-1 in the response to nerve injury. Future Neurol 2011; 6: 809-22.
43. Fricker FR, Lago N, Balarajah S, Tsantoulas C, Tanna S, Zhu N, et al. Axonally derived neuregulin-1 is required for remyelination and regeneration after nerve injury in adulthood. J Neurosci 2011; 31: 3225-33.
44. Fricker FR, Zhu N, Tsantoulas C, Abrahamsen B, Nassar MA, Thakur M, et al. Sensory axon-derived neuregulin-1 is required for axoglial signaling and normal sensory function but not for long-term axon maintenance. J Neurosci 2009; 29: 7667-78. Jun 17;
45. Garratt AN, Voiculescu O, Topilko P, Charnay P, Birchmeier C. A dual role of erbB2 in myelination and in expansion of the schwann cell precursor pool. J Cell Biol 2000; 148: 1035-46.
46. Gaudet AD, Popovich PG. Extracellular matrix regulation of inflammation in the healthy and injured spinal cord. Exp Neurol 2014; 258: 24-34.
47. Gauthier MK, Kosciuczyk K, Tapley L, Karimi-Abdolrezaee S. Dysregulation of the neuregulin-1-ErbB network modulates endogenous oligodendrocyte differentiation and preservation after spinal cord injury. Eur J Neurosci 2013; 38: 2693-715.
48. Ghatak NR, Hirano A, Doron Y, Zimmerman HM. Remyelination in multiple sclerosis with peripheral type myelin. Arch Neurol 1973; 29: 262-7.
49. Guest JD, Hiester ED, Bunge RP. Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp Neurol 2005; 192: 384-93.
50. Hagg T, Oudega M. Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 2006; 23: 264-80.
51. Harrison BM, Gledhill RF, McDonald WJ. Remyelination after transient compression of the spinal cord. Proc Aust Assoc Neurol 1975; 12: 117-22.
52. Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 2002; 244: 305-18.
53. Hippenmeyer S, Shneider NA, Birchmeier C, Burden SJ, Jessell TM, Arber S. A role for neuregulin1 signaling in muscle spindle differentiation. Neuron 2002; 36: 1035-49.
54. Hopman AH, Ramaekers FC, Speel EJ. Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochrome-labeled tyramides and their application for In situ hybridization using CARD amplification. J Histochem Cytochem 1998; 46: 771-7.
55. Hu X, Hicks CW, He W, Wong P, Macklin WB, Trapp BD, et al. Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 2006; 9: 1520-5.
56. Iaci JF, Ganguly A, Finklestein SP, Parry TJ, Ren J, Saha S, et al. Glial growth factor 2 promotes functional recovery with treatment initiated up to 7 days after permanent focal ischemic stroke. Neuropharmacology 2010; 59: 640-9.
57. Irvine KA, Blakemore WF. Remyelination protects axons from demyelination-associated axon degeneration. Brain 2008; 131: 1464-77.
58. Itoyama Y, Ohnishi A, Tateishi J, Kuroiwa Y, Webster HD. Spinal cord multiple sclerosis lesions in Japanese patients: Schwann cell remyelination occurs in areas that lack glial fibrillary acidic protein (GFAP). Acta Neuropathol 1985; 65: 217-23.
59. James ND, Bartus K, Grist J, Bennett DL, McMahon SB, Bradbury EJ. Conduction failure following spinal cord injury: functional and anatomical changes from acute to chronic stages. J Neurosci 2011; 31: 18543-55.
60. Jasmin L, Janni G, Moallem TM, Lappi DA, Ohara PT. Schwann cells are removed from the spinal cord after effecting recovery from paraplegia. J Neurosci 2000; 20: 9215-23.
61. Kakulas BA. A review of the neuropathology of human spinal cord injury with emphasis on special features. J Spinal Cord Med 1999; 22: 119-24.
62. Kanagal SG, Muir GD. Effects of combined dorsolateral and dorsal funicular lesions on sensorimotor behaviour in rats. Exp Neurol 2008; 214: 229-39.
63. Koles ZJ, Rasminsky M. A computer simulation of conduction in demyelinated nerve fibres. J Physiol 1972; 227: 351-64.
64. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012; 487: 443-8.
65. Li L, Cleary S, Mandarano MA, Long W, Birchmeier C, Jones FE. The breast proto-oncogene, HRGalpha regulates epithelial proliferation and lobuloalveolar development in the mouse mammary gland. Oncogene 2002; 21: 4900-7.
66. Lovas G, Szilagyi N, Majtenyi K, Palkovits M, Komoly S. Axonal changes in chronic demyelinated cervical spinal cord plaques. Brain 2000; 123: 308-17.
67. Lundgaard I, Luzhynskaya A, Stockley JH, Wang Z, Evans KA, Swire M, et al. Neuregulin and BDNF induce a switch to NMDA receptordependent myelination by oligodendrocytes. PLoS Biol 2013; 11: e1001743.
68. Makinodan M, Rosen KM, Ito S, Corfas G. A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 2012; 337: 1357-60.
69. McDonald JW, Belegu V. Demyelination and remyelination after spinal cord injury. J Neurotrauma 2006; 23: 345-59.
70. McDonald WI. Mechanisms of functional loss and recovery in spinal cord damage. Ciba Found Symp 1975; 34: 23-33.
71. McGavern DB, Murray PD, Rivera-Quinones C, Schmelzer JD, Low PA, Rodriguez M. Axonal loss results in spinal cord atrophy, electrophysiological abnormalities and neurological deficits following demyelination in a chronic inflammatory model of multiple sclerosis. Brain 2000; 123: 519-31.
72. Mei L, Nave KA. Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases. Neuron 2014; 83: 27-49.
73. Meyer D, Birchmeier C. Multiple essential functions of neuregulin in development. Nature 1995; 378: 386-90.
74. Meyer D, Yamaai T, Garratt A, Riethmacher-Sonnenberg E, Kane D, Theill LE, et al. Isoform-specific expression and function of neuregulin. Development 1997; 124: 3575-86.
75. Monteiro de Castro G, Deja NA, Ma D, Zhao C, Franklin RJ. Astrocyte activation via Stat3 signaling determines the balance of oligodendrocyte versus schwann cell remyelination. Am J Pathol 2015; 185: 2431-40. Sep;
76. Nashmi R, Fehlings MG. Changes in axonal physiology and morphology after chronic compressive injury of the rat thoracic spinal cord. Neuroscience 2001; 104: 235-51.
77. Nave KA, Salzer JL. Axonal regulation of myelination by neuregulin 1. Curr Opin Neurobiol 2006; 16: 492-500.
78. Nave KA, Werner HB. Myelination of the nervous system: mechanisms and functions. Annu Rev Cell Dev Biol 2014; 30: 503-33.
79. Newbern J, Birchmeier C. Nrg1/ErbB signaling networks in Schwann cell development and myelination. Semin Cell Dev Biol 2010; 21: 922-8.
80. Norenberg MD, Smith J, Marcillo A. The pathology of human spinal cord injury: defining the problems. J Neurotrauma 2004; 21: 429-40.
81. Oudega M, Bradbury EJ, Ramer MS. Combination therapies. Handb Clin Neurol 2012; 109: 617-36.
82. Papastefanaki F, Matsas R. From demyelination to remyelination: the road toward therapies for spinal cord injury. Glia 2015; 63: 1101-25.
83. Penderis J, Woodruff RH, Lakatos A, Li WW, Dunning MD, Zhao C, et al. Increasing local levels of neuregulin (glial growth factor-2) by direct infusion into areas of demyelination does not alter remyelination in the rat CNS. Eur J Neurosci 2003; 18: 2253-64.
84. Perlin JR, Lush ME, Stephens WZ, Piotrowski T, Talbot WS. Neuronal Neuregulin 1 type III directs Schwann cell migration. Development 2011; 138: 4639-48.
85. Plemel JR, Keough MB, Duncan GJ, Sparling JS, Yong VW, Stys PK, et al. Remyelination after spinal cord injury: is it a target for repair Prog Neurobiol 2014; 117: 54-72.
86. Potter PJ. Disordered control of the urinary bladder after human spinal cord injury: what are the problems Progr Brain Res 2006; 152: 51-7.
87. Raineteau O, Schwab ME. Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2001; 2: 263-73.
88. Ramer LM, Ramer MS, Bradbury EJ. Restoring function after spinal cord injury: towards clinical translation of experimental strategies. Lancet Neurol 2014; 13: 1241-56.
89. Ravenscroft A, Ahmed YS, Burnside IG. Chronic pain after SCI: a patient survey. Spinal Cord 2000; 38: 611-14.
90. Salic A, Mitchison TJ. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci USA 2008; 105: 2415-20.
91. Schwab ME, Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 1996; 76: 319-70. Apr
92. Siegenthaler MM, Tu MK, Keirstead HS. The extent of myelin pathology differs following contusion and transection spinal cord injury. J Neurotrauma 2007; 24: 1631-46.
93. Sims TJ, Durgun MB, Gilmore SA. Schwann cell invasion of ventral spinal cord: the effect of irradiation on astrocyte barriers. J Neuropathol Exp Neurol 1998; 57: 866-73.
94. Smith KJ, Blakemore WF, McDonald WI. Central remyelination restores secure conduction. Nature 1979; 280: 395-6.
95. Soderblom C, Luo X, Blumenthal E, Bray E, Lyapichev K, Ramos J, et al. Perivascular fibroblasts form the fibrotic scar after contusive spinal cord injury. J Neurosci 2013; 33: 13882-7.
96. Stassart RM, Fledrich R, Velanac V, Brinkmann BG, Schwab MH, Meijer D, et al. A role for Schwann cell-derived neuregulin-1 in remyelination. Nat Neurosci 2013; 16: 48-54.
97. Takeoka A, Vollenweider I, Courtine G, Arber S. Muscle spindle feedback directs locomotor recovery and circuit reorganization after spinal cord injury. Cell 2014; 159: 1626-39.
98. Taveggia C, Thaker P, Petrylak A, Caporaso GL, Toews A, Falls DL, et al. Type III neuregulin-1 promotes oligodendrocyte myelination. Glia 2008; 56: 284-93.
99. Waxman SG. Demyelination in spinal cord injury. J Neurol Sci 1989; 91: 1-14.
100. Waxman SG, Utzschneider DA, Kocsis JD. Enhancement of action potential conduction following demyelination: experimental approaches to restoration of function in multiple sclerosis and spinal cord injury. Prog Brain Res 1994; 100: 233-43.
101. Weidner N, Tuszynski MH. Spontaneous plasticity in the injured spinal cord-implications for repair strategies. Mol Psychiatry 2002; 7: 9-11.
102. Willem M, Garratt AN, Novak B, Citron M, Kaufmann S, Rittger A, et al. Control of peripheral nerve myelination by the beta-secretase BACE1. Science 2006; 314: 664-6.
103. Woodruff RH, Franklin RJ. Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide, and complement/anti-galactocerebroside: a comparative study. Glia 1999; 25: 216-28.
104. Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, et al. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 2001; 30: 399-410.
105. Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, et al. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 2010; 6: 578-90.
106. Zeng C, Pan F, Jones LA, Lim MM, Griffin EA, Sheline YI, et al. Evaluation of 5-ethynyl-2'-deoxyuridine staining as a sensitive and reliable method for studying cell proliferation in the adult nervous system. Brain Res 2010; 1319: 21-32.
107. Zhang JF, Zhao FS, Wu G, Kong QF, Sun B, Cao J, et al. Therapeutic effect of co-transplantation of neuregulin-1-transfected Schwann cells and bone marrow stromal cells on spinal cord hemisection syndrome. Neurosci Lett 2011; 497: 128-33.