Schwann cell transplantation: A repair strategy for spinal cord injury?

Progress in Brain Research

Volumn 201, Issue , 2012, Pages 295-312

  Wiliams, Ryan R ^a   Bunge, Mary Bartlett ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Neurotrophins; PSA NCAM; Reactive astrocytes; Schwann cell combination therapy; Schwann cell astrocyte boundary assay; Schwann cell spinal cord interface

Indexed keywords

CYCLIC AMP; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; METHYLPREDNISOLONE; N ACETYLGALACTOSAMINE 4 SULFATASE; NERVE CELL ADHESION MOLECULE; NEUROTROPHIN;

ARTICLE; ASTROCYTE; CELL TRANSPLANTATION; HUMAN; LOCOMOTION; NERVE FIBER; NONHUMAN; OLFACTORY ENSHEATHING CELL; PRIORITY JOURNAL; SCHWANN CELL; SPINAL CORD INJURY;

EID: 84870152106     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/B978-0-444-59544-7.00014-7     Document Type: Chapter

References (90)

1. Afshari F.T., Fawcett J.W. Astrocyte-Schwann-cell coculture systems. Methods Mol. Biol. 2012, 814:381-391.
2. Afshari F.T., Kwok J.C., Fawcett J.W. Astrocyte-produced ephrins inhibit Schwann cell migration via VAV2 signaling. J. Neurosci. 2010, 30:4246-4255.
3. Afshari F.T., Kwok J.C., White L., Fawcett J.W. Schwann cell migration is integrin-dependent and inhibited by astrocyte-produced aggrecan. Glia 2010, 58:857-869.
4. Afshari F.T., Kwok J.C., Fawcett J.W. Analysis of Schwann-astrocyte interactions using in vitro assays. J. Vis. Exp. 2011, 47:2214.
5. Alto L.T., Havton L.A., Conner J.M., Hollis E.R., Blesch A., Tuszynski M.H. Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nat. Neurosci. 2009, 12:1106-1113.
6. Bamber N.I., Li H., Lu X., Oudega M., Aebischer P., Xu X.M. Neurotrophins, BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur. J. Neurosci. 2001, 13:257-268.
7. Basso D.M., Beattie M.S., Bresnahan J.C. A new, sensitive and reliable locomotor scale for open field testing in rats. J. Neurotrauma 1995, 12:1-21.
8. Basso D.M., Beattie M.S., Bresnahan J.C., Anderson D.K., Faden A.I., Gruner J.A., Holford T.R., Hsu C.Y., Noble L.J., Nockels R., Perot P.L., Salzman S.K., Young W. MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter Animal Spinal Cord Injury Study. J. Neurotrauma 1996, 13:343-359.
9. Basso D.M., Fisher L.C., Anderson A.J., Jakeman L.B., McTigue D.M., Popovich P.G. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 2006, 23:635-659.
10. Blakemore W.F., Franklin R.J. Transplantation options for therapeutic central nervous system remyelination. Cell Transplant. 2000, 9:289-294.
11. Bradbury E.J., Carter L.M. Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain Res. Bull. 2011, 84:306-316.
12. Bunge R.P. Changing uses of nerve tissue culture 1950-1975. The Nervous System, Volume 1, The Basic Neuroscience 1975, 31-42. Raven Press, New York. D.B. Tower (Ed.).
13. Bunge M.B. Novel combination strategies to repair the injured mammalian spinal cord. J. Spinal Cord Med. 2008, 31:262-269.
14. Bunge M.B., Wood P.M. Realizing the maximum potential of Schwann cells to promote recovery from spinal cord injury. Handbook of Clinical Neurology, Spinal Cord Trauma 2012, vol. 109. Elsevier, New York, (Chapter 34), p. 300. third ed. J. Verhaagan, J.W. McDonald (Eds.).
15. Bunge M.B., Williams A.K., Wood P.M., Uitto J., Jeffrey J.J. Comparison of nerve cell and nerve cell plus Schwann cell cultures, with particular emphasis on basal lamina and collagen formation. J. Cell Biol. 1980, 84:184-202.
16. Bunge M.B., Williams A.K., Wood P.M. Neuron-Schwann cell interaction in basal lamina formation. Dev. Biol. 1982, 92:449-460.
17. Bunge M.B., Holets V.R., Bates M.L., Clarke T.S., Watson B.D. Characterization of photochemically induced spinal cord injury in the rat by light and electron microscopy. Exp. Neurol. 1994, 127:76-93.
18. Casella G.T.B., Bunge R.P., Wood O.M. Improved method for harvesting human Schwann cells from mature peripheral nerve and expansion in vitro. Glia 1996, 17:327-338.
19. Chau C.H., Shum D.K., Li H., Pei J., Lui Y.Y., Wirthlin L., Chan Y.S., Xu X.M. Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J. 2004, 18:194-196.
20. Chen A., Xu X.M., Kleitman N., Bunge M.B. Methylprednisolone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp. Neurol. 1996, 138:261-276.
21. Davies J.E., Huang C., Proschel C., Noble M., Mayer-Proschel M., Davies S.J. Astrocytes derived from glial-restricted precursors promote spinal cord repair. J. Biol. 2006, 5:7.
22. Deng L.X., Hu J., Liu N., Wang X., Smith G.M., Wen X., Xu X.M. GDNF modifies reactive astrogliosis allowing robust axonal regeneration through Schwann cell-seeded guidance channels after spinal cord injury. Exp. Neurol. 2011, 229:238-250.
23. Eldridge C.F., Bunge M.B., Bunge R.P. Differentiation of axon-related Schwann cells in vitro: II. Control of myelin formation by basal lamina. J. Neurosci. 1989, 9:625-638.
24. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res. Bull. 1999, 49:377-391.
25. Fortun J., Hill C.E., Bunge M.B. Combinatorial strategies with Schwann cell transplantation to improve repair of the injured spinal cord. Neurosci. Lett. 2009, 456(3):124-132.
26. Fouad K., Schnell L., Bunge M.B., Schwab M.E., Liebscher T., Pearse D.D. Combining Schwann cell bridges and olfactory ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J. Neurosci. 2005, 25:1169-1178.
27. Fraher J.P. The transitional zone and CNS regeneration. J. Anat. 1999, 194:161-182.
28. Ghosh M., Tuesta L.M., Puentes R., Patel S., Melendez K., El Maarouf A., Rutishauser U., Pearse D.D. Extensive cell migration, axon regeneration, and improved function with polysialic acid-modified Schwann cells after spinal cord injury. Glia 2012, 60:979-992.
29. Gilmore S.A., Sims T.J. Patterns of Schwann cell myelination of axons within the spinal cord. J. Chem. Neuroanat. 1993, 6:191-199.
30. Golden K.L., Pearse D.D., Blits B., Garg M., Oudega M., Wood P.M., Bunge M.B. Transduced Schwann cells promote axon growth and myelination after spinal cord injury. Exp. Neurol. 2007, 207:203-217.
31. Golding J., Shewan D., Cohen J. Maturation of the mammalian dorsal root entry zone-from entry to no entry. Trends Neurosci. 1997, 20:303-308.
32. Grimpe B., Pressman Y., Lupa M.D., Horn K.P., Bunge M.B., Silver J. The role of proteoglycans in Schwann cell/astrocyte interactions and in regeneration failure at PNS/CNS interfaces. Mol. Cell. Neurosci. 2005, 28:18-29.
33. Guest J.D., Rao A., Olson L., Bunge M.B., Bunge R.P. The ability of human Schwann cell grafts to promote regeneration in the transected nude rat spinal cord. Exp. Neurol. 1997, 148:502-522.
34. Hill C.E., Hurtado A., Blits B., Bahr B.A., Wood P.M., Bunge M.B. Early necrosis and apoptosis of Schwann cells transplanted into the injured rat spinal cord. Eur. J. Neurosci. 2007, 26:1433-1445.
35. Houle J.D., Tom V.J., Mayes D., Wagoner G., Phillips N., Silver J. Combining an autologous peripheral nervous system " bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J. Neurosci. 2006, 26:7405-7415.
36. Hurtado A., Cregg J.M., Wang H.B., Wendell D.F., Oudega M., Gilbert R.J., McDonald J.W. Robust CNS regeneration after complete spinal cord transection using aligned poly-L-lactic acid microfibers. Biomaterials 2011, 32:6068-6079.
37. Iannotti C., Li H.Y., Yan P., Lu X.B., Wirthlin L., Xu X.M. Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Exp. Neurol. 2003, 183:379-393.
38. Iwashita Y., Fawcett J.W., Crang A.J., Franklin R.J., Blakemore W.F. Schwann cells transplanted into normal and X-irradiated adult white matter do not migrate extensively and show poor long-term survival. Exp. Neurol. 2000, 164:292-302.
39. Jones L.L., Margolis R.U., Tuszynski M.H. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp. Neurol. 2003, 182:399-411.
40. Kanno H., Pressman Y., Moody A., Berg R., Pearse D.D., Bunge M.B. Combined engineering of Schwann cell implants to secrete neurotrophin and chondroitinase promotes axonal regeneration and locomotion after spinal cord injury 2012.
41. Lakatos A., Franklin R.J., Barnett S.C. Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 2000, 32:214-225.
42. Lakatos A., Barnett S.C., Franklin R.J. Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Exp. Neurol. 2003, 184:237-246.
43. Levi A.D.O. Characterization of the technique involved in isolating Schwann cells from adult human peripheral nerve. J. Neurosci. Methods 1996, 68:21-26.
44. Levi A.D.O., Bunge R.P., Lofgren J.A., Meima L., Hefti F., Nikolics K., Sliwkowski M.X. The influence of heregulins on human Schwann cells proliferation. J. Neurosci. 1995, 15:1329-1340.
45. Luo J., Bo X., Wu D., Yeh J., Richardson P.M., Zhang Y. Promoting survival, migration, and integration of transplanted Schwann cells by over-expressing polysialic acid. Glia 2011, 59:424-434.
46. Matthews M.A., St Onge M.F., Faciane C.L., Gelderd J.B. Axon sprouting into segments of rat spinal cord adjacent to the site of a previous transection. Neuropathol. Appl. Neurobiol. 1979, 5:181-196.
47. McPhail L.T., Plunet W.T., Das P., Ramer M.S. The astrocytic barrier to axonal regeneration at the dorsal root entry zone is induced by rhizotomy. Eur. J. Neurosci. 2005, 21:267-270.
48. Meijs M.F.L., Timmers L., Pearse D.D., Tresco P.A., Bates M.L., Joosten E.A.J., Bunge M.B., Oudega M. Basic fibroblast growth factor promotes neuronal survival but not behavioral recovery in the transected and Schwann cell implanted rat thoracic spinal cord. J. Neurotrauma 2004, 21:1415-1430.
49. Morrissey T.K., Kleitman N., Bunge R.P. Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J. Neurosci. 1991, 11:2433-2442.
50. Noble M., Davies J.E., Mayer-Pröschel M., Pröschel C., Davies S.J. Precursor cell biology and the development of astrocyte transplantation therapies: lessons from spinal cord injury. Neurotherapeutics 2011, 8:677-693.
51. Oudega M., Xu X.M. Schwann cell transplantation for repair of the adult spinal cord. J. Neurotrauma 2006, 23:453-467.
52. Oudega M., Vargas C.G., Weber A.B., Kleitman N., Bunge M.B. Long-term effects of methylprednisolone following transection of adult rat spinal cord. Eur. J. Neurosci. 1999, 11:2453-2464.
53. Papastefanaki F., Chen P., Lavdas A.A., Thornaidou D., Schachner M., Matsas R. Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain 2007, 130:2159-2174.
54. Pearse D.D., Bunge M.B. Designing cell- and gene-based regeneration strategies to repair the injured spinal cord. J. Neurotrauma 2006, 23:438-452.
55. Pearse D.D., Pereira F.C., Marcillo A.E., Bates M.L., Berrocal Y.A., Filbin M.T., Bunge M.B. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat. Med. 2004, 10:610-616.
56. Pearse D.D., Sanchez A.R., Pereira F.C., Andrade C.M., Puzis R., Pressman Y., Golden K.L., Kitay B.M., Blits B., Wood P.M., Bunge M.B. Transplantation of Schwann cells and/or olfactory ensheathing glia into the contused spinal cord: survival, migration, axon association and functional recovery. Glia 2007, 55:976-1000.
57. Plant G.W., Bates M.L., Bunge M.B. Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-transected spinal cord interface. Mol. Cell. Neurosci. 2001, 17:471-487.
58. Ramer M.S., Priestley J.V., McMahon S.B. Functional regeneration of sensory axons into the adult spinal cord. Nature 2000, 403:312-316.
59. Ramer M.S., McMahon S.B., Priestley J.V. Axon regeneration across the dorsal root entry zone. Prog. Brain Res. 2001, 132:621-639.
60. Ramer M.S., Duraisingam I., Priestley J.V., McMahon S.B. Two-tiered inhibition of axon regeneration at the dorsal root entry zone. J. Neurosci. 2001, 21:2651-2660.
61. Ramer M.S., Bishop T., Dockery P., Mobarak M.S., O'Leary D., Fraher J.P., Priestley J.V., McMahon S.B. Neurotrophin-3-mediated regeneration and recovery of proprioception following dorsal rhizotomy. Mol. Cell. Neurosci. 2002, 19:239-249.
62. Ramón-Cueto A., Plant G.W., Avila J., Bunge M.B. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J. Neurosci. 1998, 18:3803-3815.
63. Richardson P.M., Issa V.M. Peripheral injury enhances central regeneration of primary sensory neurones. Nature 1984, 309:791-793.
64. Richardson P.M., Issa V.M., Aguayo A.J. Regeneration of long spinal axons in the rat. J. Neurocytol. 1984, 13:165-182.
65. Rutkowski J.L., Tenekoon G.I., McGillicuddy J.E. Selective culture of mitotically active human Schwann cells from adult sural nerves. Ann. Neurol. 1992, 31:580-586.
66. Saberi H., Moshayedi P., Aghayan H.R., Arjmand B., Hosseini S.K., Emami-Razavi S.H., Rahimi-Movaghar V., Raza M., Firouzi M. Treatment of chronic thoracic spinal cord injury patients with autologous Schwann cell transplantation: an interim report on safety considerations and possible outcomes. Neurosci. Lett. 2008, 443:46-50.
67. Saberi H., Firouzi M., Habibi Z., Moshayedi P., Aghayan H.R., Arjmand B., Hosseini K., Razavi H.E., Yekaninejad M.S. Safety of intramedullary Schwann cell transplantation for postrehabilitation spinal cord injuries: 2-year follow-up of 33 cases. J. Neurosurg. Spine 2011, 15:515-525.
68. Schaal S.M., Kitay B.M., Cho K.S., Lo T.P., Barakat D.J., Marcillo A.E., Sanchez A.R., Andrade C.M., Pearse D.D. Schwann cell transplantation improves reticulospinal axon growth and forelimb strength after severe cervical spinal cord contusion. Cell Transplant. 2007, 16:207-228.
69. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
70. Smith G.M., Miller R.H., Silver J. Changing role of forebrain astrocytes during development, regenerative failure, and induced regeneration upon translation. J. Comp. Neurol. 1986, 251:23-43.
71. Sofroniew M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009, 32:638-647.
72. Steinmetz M.P., Horn K.P., Tom V.J., Miller J.H., Busch S.A., Nair D., Silver D.J., Silver J. Chronic enhancement of the intrinsic growth capacity of sensory neurons combined with the degradation of inhibitory proteoglycans allows functional regeneration of sensory axons through the dorsal root entry zone in the mammalian spinal cord. J. Neurosci. 2005, 25:8066-8076.
73. Steward O., Zheng B., Tessier-Lavigne M. False resurrections: distinguishing regenerated from spared axons in the injured central nervous system. J. Comp. Neurol. 2003, 459:1-8.
74. Takami T., Oudega M., Bates M.L., Wood P.M., Kleitman N., Bunge M.B. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J. Neurosci. 2002, 22:6670-6681.
75. Tang X., Davies J.E., Davies S.J. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J. Neurosci. Res. 2003, 71:427-444.
76. Taylor L., Jones L., Tuszynski M.H., Blesch A. Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord. J. Neurosci. 2006, 26:9713-9721.
77. Tetzlaff W., Okon E.B., Karimi-Abdolrezaee S., Hill C.E., Sparling J.S., Plemel J.R., Plunet W.T., Tsai E.C., Baptiste D., Smithson L.J., Kawaja M.D., Fehlings M.G., Kwon B.K. A systematic review of cellular transplantation therapies for spinal cord injury. J. Neurotrauma 2011, 28:1611-1682.
78. Tuszynski M.H., Weidner N., McCormack M., Miller I., Powell H., Conner J. Grafts of genetically modified Schwann cells to the spinal cord: survival, axon growth, and myelination. Cell Transplant. 1998, 7:187-196.
79. Urfer R., Tsoulfas P., Soppet D., Escandón E., Parada L.F., Presta L.G. The binding epitopes of neurotrophin-3 to its receptors trkC and gp75 and the design of a multifunctional human neurotrophin. EMBO J. 1994, 13:5896-5909.
80. Vavrek R., Pearse D.D., Fouad K. Neuronal populations capable of regeneration following a combined treatment in rats with spinal cord transection. J. Neurotrauma 2007, 24:1667-1673.
81. White R.E., Jakeman L.B. Don't fence me in: harnessing the beneficial roles of astrocytes for spinal cord repair. Restor. Neurol. Neurosci. 2008, 26:197-214.
82. Wilby M.J., Muir E.M., Fok-Seang J., Gour B.J., Blaschuk O.W., Fawcett J.W. N-Cadherin inhibits Schwann cell migration on astrocytes. Mol. Cell. Neurosci. 1999, 14:66-84.
83. Williams R.R., Pearse D.D., Bunge M.B. The importance of implanted Schwann cells and host astrocyte interactions in providing a permissive hindlimb movements after SCI 2012.
84. Wood P.M., Bunge R.P. Evidence that sensory axons are mitogenic for Schwann cells. Nature 1975, 256:662-664.
85. Xu X.M., Guénard V., Kleitman N., Bunge M.B. Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol. 1995, 351:145-160.
86. Xu X.M., Guénard V., Kleitman N., Aebischer P., Bunge M.B. Combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 1995, 134:261-272.
87. Xu X.M., Chen A., Guénard V., Kleitman N., Bunge M.B. Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J. Neurocytol. 1997, 26:1-16.
88. Xu X.M., Zhang S.X., Li H.Y., Aebischer P., Bunge M.B. Regrowth of axons into the distal spinal cord through a Schwann cell seeded mini-channel implanted into hemisected adult rat spinal cord. Eur. J. Neurosci. 1999, 11:1723-1740.
89. Zhang Y., Ghadiri-Sani M., Zhang X., Richardson P.M., Yeh J., Bo X. Induced expression of polysialic acid in the spinal cord promotes regeneration of sensory axons. Mol. Cell. Neurosci. 2007, 35:109-119.
90. Zhang Y., Zhang X., Wu D., Verhaagen J., Richardson P.M., Yeh J., Bo X. Lentiviral-mediated expression of polysialic acid in spinal cord and conditioning lesion promote regeneration of sensory axons into spinal cord. Mol. Ther. 2007, 15:1796-1804.