Use of stem cells to augment nerve injury repair

Neurosurgery

Volumn 65, Issue SUPPL. 4, 2009, Pages

  Walsh, Sarah ^a   Midha, Rajiv ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Chronic nerve injury; Denervation; Nerve regeneration; Schwann cells; Skin derived stem cells

Indexed keywords

ADULT; ADULT STEM CELL; CELL COUNT; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELL THERAPY; CLINICAL PRACTICE; DENERVATION; HUMAN; MOTOR PERFORMANCE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE REGENERATION; NONHUMAN; OUTCOME ASSESSMENT; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVIEW; SCHWANN CELL; STEM CELL TRANSPLANTATION;

ANIMALS; GRAFT SURVIVAL; HUMANS; NERVE REGENERATION; NEUROSURGICAL PROCEDURES; PERIPHERAL NERVES; PERIPHERAL NERVOUS SYSTEM DISEASES; RECOVERY OF FUNCTION; SCHWANN CELLS; SKIN; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 70350663143     PISSN: 0148396X     EISSN: None     Source Type: Journal    
DOI: 10.1227/01.NEU.0000335651.93926.2F     Document Type: Review

References (80)

1. Amoh Y, Li L, Campillo R, Kawahara K, Katsuoka K, Penman S, Hoffman RM: Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci USA 102:17734-17738, 2005.
2. Azizi SA, Stokes D, Augelli BJ, Digirolamo C, Prockop DJ: Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats-Similarities to astrocyte grafts. Proc Natl Acad Sci USA 95:3908-3913, 1998.
3. Biernaskie J, Sparling JS, Liu J, Shannon CP, Plemel JR, Xie Y, Miller FD, Tetzlaff W: Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci 27:9545-9559, 2007.
4. Bowden RE, Gutmann E: Denervation and re-innervation of human voluntary muscle. Brain 67:273-313, 1944.
5. Bunge MB, Bunge RP, Kleitman N, Dean AC: Role of peripheral nerve extracellular matrix in Schwann cell function and neurite regeneration. Dev Neurosci 11:348-360, 1989.
6. Bungner OV: Uber die Degenerations und Regenerations-vorgange am Nerven nach Verletzungen [in German]. Beitr Pathol Anat 10:321-387, 1891.
7. 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 17:1642-1659, 1997.
8. Chen CJ, Ou YC, Liao SL, Chen WY, Chen SY, Wu CW, Wang CC, Wang WY, Huang YS, Hsu SH: Transplantation of bone marrow stromal cells for peripheral nerve repair. Exp Neurol 204:443-453, 2007.
9. Chernousov MA, Carey DJ: Schwann cell extracellular matrix molecules and their receptors. Histol Histopathol 15:593-601, 2000.
10. Dedkov EI, Kostrominova TY, Borisov AB, Carlson BM: Survival of Schwann cells in chronically denervated skeletal muscles. Acta Neuropathol 103:565-574, 2002.
11. De Medinaceli L, Rawlings RR: Is it possible to predict the outcome of peripheral nerve injuries? A probability model based on prospects for regenerating neurites. Biosystems 20:243-258, 1987.
12. Dezawa M, Takahashi I, Esaki M, Takano M, Sawada H: Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bonemarrow stromal cells. Eur J Neurosci 14:1771-1776, 2001.
13. Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, Barnabé-Heider F, Biernaskie J, Junek A, Kobayashi NR, Toma JG, Kaplan DR, Labosky PA, Rafuse V, Hui CC, Miller FD: A dermal niche for multipotent adult skinderived precursor cells. Nat Cell Biol 6:1082-1093, 2004.
14. Fu SY, Gordon T: Contributing factors to poor functional recovery after delayed nerve repair: Prolonged axotomy. J Neurosci 15:3876-3885, 1995.
15. Fu SY, Gordon T: Contributing factors to poor functional recovery after delayed nerve repair: Prolonged denervation. J Neurosci 15:3886-3895, 1995.
16. Fu SY, Gordon T: The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol 14:67-116, 1997.
17. Gordon T, Fu SY: Long-term response to nerve injury. Adv Neurol 72:185-199, 1997.
18. Guénard V, Kleitman N, Morrissey TK, Bunge RP, Aebischer P: Syngeneic Schwann cells derived from adult nerves seeded in semipermeable guidance channels enhance peripheral nerve regeneration. J Neurosci 12:3310-3320, 1992.
19. Guénard V, Rosenbaum T, Gwynn LA, Doetschman T, Ratner N, Wood PM: Effect of transforming growth factor-beta 1 and -beta 2 on Schwann cell proliferation on neurites. Glia 13:309-318, 1995.
20. Guest JD, Rao A, Olson L, Bunge MB, Bunge RP: The ability of human Schwann cell grafts to promote regeneration in the transected nude rat spinal cord. Exp Neurol 148:502-522, 1997.
21. Hall SM, Kent AP, Curtis R, Robertson D: Electron microscopic immunocytochemistry of GAP-43 within proximal and chronically denervated distal stumps of transected peripheral nerve. J Neurocytol 21:820-831, 1992.
22. Hynes NM, Bain JR, Thoma A, Veltri K, Maguire JA: Preservation of denervated muscle by sensory protection in rats. J Reconstr Microsurg 13:337-343, 1997. (Pubitemid 27328629)
23. Jessen KR, Mirsky R: Signals that determine Schwann cell identity. J Anat 200:367-376, 2002.
24. Keilhoff G, Stang F, Goihl A, Wolf G, Fansa H: Transdifferentiated mesenchymal stem cells as alternative therapy in supporting nerve regeneration and myelination. Cell Mol Neurobiol 26:1235-1252, 2006.
25. Kelsey JL, Praemer A, Nelson L, Felberg A, Rice LM: Upper Extremity Disorders: Frequency, Impact, and Cost. New York, Churchill Livingstone, 1997.
26. Kingham PJ, Kalbermatten DF, Mahay D, Armstrong SJ, Wiberg M, Terenghi G: Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol 207:267-274, 2007.
27. Kline DG, Hudson AR: Nerve Injuries: Operative Results from Major Nerve Injuries, Entrapments, and Tumors. Philadelphia, W.B. Saunders Co., 1995.
28. Kobayashi J, Mackinnon SE, Watanabe O, Ball DJ, Gu XM, Hunter DA, Kuzon WM Jr: The effect of duration of muscle denervation on functional recovery in the rat model. Muscle Nerve 20:858-866, 1997.
29. Küry P, Stoll G, Müller HW: Molecular mechanisms of cellular interactions in peripheral nerve regeneration. Curr Opin Neurol 14:635-639, 2001.
30. La Fleur M, Underwood JL, Rappolee DA, Werb Z: Basement membrane and repair of injury to peripheral nerve: Defining a potential role for macro - phages, matrix metalloproteinases, and tissue inhibitor of metalloproteinases- 1. J Exp Med 184:2311-2326, 1996.
31. Li H, Terenchi G, Hall SM: Effects of delayed re-innervation on the expression of c-erbB receptors by chronically denervated rat Schwann cells in vivo. Glia 20:333-347, 1997.
32. Love FM, Thompson WJ: Schwann cells proliferate at rat neuromuscular junctions during development and regeneration. J Neurosci 18:9376-9385, 1998.
33. Ma J, Novikov LN, Wiberg M, Kellerth JO: Delayed loss of spinal motoneurons after peripheral nerve injury in adult rats: A quantitative morphological study. Exp Brain Res 139:216-223, 2001.
34. MacDonald SC, Fleetwood IG, Hochman S, Dodd JG, Cheng GK, Jordan LM, Brownstone RM: Functional motor neurons differentiating from mouse multipotent spinal cord precursor cells in culture and after transplantation into transected sciatic nerve. J Neurosurg 98:1094-1103, 2003.
35. Mahanthappa NK, Anton ES, Matthew WD: Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth. J Neurosci 16:4673-4683, 1996.
36. Marchesi C, Pluderi M, Colleoni F, Belicchi M, Meregalli M, Farini A, Parolini D, Draghi L, Fruguglietti ME, Gavina M, Porretti L, Cattaneo A, Battistelli M, Prelle A, Moggio M, Borsa S, Bello L, Spagnoli D, Gaini SM, Tanzi MC, Bresolin N, Grimoldi N, Torrente Y: Skin-derived stem cells transplanted into resorbable guides provide functional nerve regeneration after sciatic nerve resection. Glia 55:425-438, 2007. (Pubitemid 46247128)
37. Martini R: Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J Neurocytol 23:1-28, 1994.
38. McKenzie IA, Biernaskie J, Toma JG, Midha R, Miller FD: Skin-derived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J Neurosci 26:6651-6660, 2006.
39. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H: 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, 1992.
40. Midha R, Kline DG: Evaluation of the neuroma in continuity, in Omer GE, Spinner M, Van Beek AL (eds): Management of Peripheral Nerve Problems. Philadelphia, W.B. Saunders Co., 1998, pp 319-327.
41. Midha R, Mackay MS: Peripheral nerve suture techniques, in Rengachary SS (ed): Neurosurgical Operative Atlas. Chicago, AANA Publishing, 1999, pp 261-269.
42. Midha R, Mackinnon SE, Becker LE: The fate of Schwann cells in peripheral nerve allografts. J Neuropathol Exp Neurol 53:316-322, 1994.
43. Midha R, Munro CA, Chan S, Nitising A, Xu QG, Gordon T: Regeneration into protected and chronically denervated peripheral nerve stumps. Neurosurgery 57:1289-1299, 2005.
44. Millesi H, Meissl G, Berger A: The interfascicular nerve-grafting of the median and ulnar nerves. J Bone Joint Surg Am 54:727-750, 1972.
45. Mirsky R, Jessen KR: The neurobiology of Schwann cells. Brain Pathol 9:293-311, 1999.
46. Noble J, Munro CA, Prasad VS, Midha R: Analysis of upper and lower extremity peripheral nerve injuries in a population of patients with multiple injuries. J Trauma 45:116-122, 1998.
47. 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.
48. Pellegrino RG, Spencer PS: Schwann cell mitosis in response to regenerating peripheral axons in vivo. Brain Res 341:16-25, 1985.
49. Prockop DJ: Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74, 1997.
50. Rahmatullah M, Schroering A, Rothblum K, Stahl RC, Urban B, Carey DJ: Synergistic regulation of Schwann cell proliferation by heregulin and forskolin. Mol Cell Biol 18:6245-6252, 1998.
51. Ramón y Cajal S: Degeneration and Regeneration of the Nervous System. London, Oxford University Press, 1928.
52. Ridley AJ, Davis JB, Stroobant P, Land H: Transforming growth factors-beta 1 and beta 2 are mitogens for rat Schwann cells. J Cell Biol 109:3419-3424, 1989.
53. Samii M, Carvalho GA, Nikkhah G, Penkert G: Surgical reconstruction of the musculocutaneous nerve in traumatic brachial plexus injuries. J Neurosurg 87:881-886, 1997. (Pubitemid 27508594)
54. Samii A, Carvalho GA, Samii M: Brachial plexus injury: Factors affecting functional outcome in spinal accessory nerve transfer for the restoration of elbow flexion. J Neurosurg 98:307-312, 2003.
55. Scherer SS, Salzer JL: Axon-Schwann cell interactions during peripheral nerve degeneration and regeneration, in Jessen KR, Richardson WD (eds): Glial Cell Development. Oxford, Bios Scientific, 1996, pp 169-196.
56. Seddon HJ: Surgical Disorders of the Peripheral Nerves. Baltimore, Williams & Wilkins, 1972.
57. Sieber-Blum M, Grim M, Hu YF, Szeder V: Pluripotent neural crest stem cells in the adult hair follicle. Dev Dyn 231:258-269, 2004. (Pubitemid 39238052)
58. Son YJ, Thompson WJ: Schwann cell processes guide regeneration of peripheral axons. Neuron 14:125-132, 1995.
59. 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.
60. Sulaiman OA, Gordon T: Transforming growth factor-beta and forskolin attenuate the adverse effects of long-term Schwann cell denervation on peripheral nerve regeneration in vivo. Glia 37:206-218, 2002.
61. Sulaiman OA, Midha R, Munro CA, Matsuyama T, Al Majed A, Gordon T: Chronic Schwann cell denervation and the presence of a sensory nerve reduce motor axonal regeneration. Exp Neurol 176:342-354, 2002. (Pubitemid 35193351)
62. Sunderland S: Rate of regeneration in human peripheral nerves: Analysis of interval between injury and onset of recovery. Arch Neurol Psychiatry 58:251-295, 1947.
63. Sunderland S: Capacity of reinnervated muscles to function efficiently after prolonged denervation. AMA Arch Neurol Psychiatry 64:755-771, 1950.
64. Sunderland S: Nerves and Nerve Injuries. New York, Churchill Livingstone, 1978.
65. Sunderland S: Nerve Injuries and Their Repair: A Critical Appraisal. New York, Churchill Livingstone, 1991.
66. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB: Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22:6670-6681, 2002.
67. Taniuchi M, Clark HB, Schweitzer JB, Johnson EM Jr: Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerve: Ultrastructural location, suppression by axonal contact, and binding properties. J Neurosci 8:664-681, 1988.
68. Tetzlaff W, Alexander SW, Miller FD, Bisby MA: Response of facial and rubrospinal neurons to axotomy: Changes in mRNA expression for cytoskeletal proteins and GAP-43. J Neurosci 11:2528-2544, 1991.
69. Tofaris GK, Patterson PH, Jessen KR, Mirsky R: Denervated Schwann cells attract macrophages by secretion of leukemia inhibitory factor (LIF) and monocyte chemoattractant protein-1 in a process regulated by interleukin-6 and LIF. J Neurosci 22:6696-6703, 2002.
70. Tohill M, Mantovani C, Wiberg M, Terenghi G: Rat bone marrow mesenchymal stem cells express glial markers and stimulate nerve regeneration. Neurosci Lett 362:200-203, 2004.
71. Toma JG, McKenzie IA, Bagli D, Miller FD: Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23:727-737, 2005.
72. Toma JG, Akhavan M, Fernandes KJ, Barnabé-Heider F, Sadikot A, Kaplan DR, Miller FD: Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778-784, 2001.
73. Trachtenberg JT, Thompson WJ: Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379:174-177, 1996.
74. Unsicker K, Krieglstein K: Co-activation of TGF-ss and cytokine signaling pathways are required for neurotrophic functions. Cytokine Growth Factor Rev 11:97-102, 2000.
75. Unsicker K, Strelau J: Functions of transforming growth factor-beta isoforms in the nervous system. Cues based on localization and experimental in vitro and in vivo evidence. Eur J Biochem 267:6972-6975, 2000.
76. Vitry S, Bertrand JY, Cumano A, Dubois-Dalcq M: Primordial hematopoietic stem cells generate microglia but not myelin-forming cells in a neural environment. J Neurosci 23:10724-10731, 2003.
77. Weinberg HJ, Spencer PS: The fate of Schwann cells isolated from axonal contact. J Neurocytol 7:555-569, 1978.
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 P, He X, Liu K, Zhao F, Fu Z, Zhang D, Zhang Q, Jiang B: Bone marrow stromal cells differentiated into functional Schwann cells in injured rats sciatic nerve. Artif Cells Blood Substit Immobil Biotechnol 32:509-518, 2004.
80. Zou J, Ferguson TA, Hernandez YJ, Stetler-Stevenson WG, Muir D: Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite-inhibiting chondroitin sulfate proteoglycan. J Neurosci 18:5203-5211, 1998.