The ability of human schwann cell grafts to promote regeneration in the transected nude rat spinal cord

Experimental Neurology

Volumn 148, Issue 2, 1997, Pages 502-522

  Guest, James D ^a   Rao, Arundathi ^a   Olson, Les ^a   Bunge, Mary Bartlett ^a   Bunge, Richard P ^a  

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

Author keywords

Anterograde tracing; CNS regeneration; Human Schwann cell transplantation; Inflammation; Propriospinal neurons; Retrograde tracing; Spinal cord injury; Transition zone

Indexed keywords

MATRIGEL; METHYLPREDNISOLONE; POLYACRYLONITRILE; POLYVINYLCHLORIDE;

ADOLESCENT; ADULT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL TRANSPLANTATION; CHILD; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SCHWANN CELL; SENSORY NERVE CELL; SPINAL CORD INJURY; SPINAL CORD NERVE CELL;

EID: 0031417671     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1997.6693     Document Type: Article

References (104)

1. Aebischer P., Guénard V., Winn S. R., Valentini R. F., Galletti P. M. Blind-ended semipermeable guidance channels support peripheral nerve regeneration in the absence of a distal nerve stump. Brain Res. 454:1988;179-187.
2. Aebischer P., Guénard V., Brace S. Peripheral nerve regeneration through blind-ended semipermeable guidance channels: effect of the molecular weight cutoff. J. Neurosci. 9:1989;3590-3595.
3. Aebischer P., Guénard V., Valentini R. F. The morphology of regenerating peripheral nerves is modulated by the surface microgeometry of polymeric guidance channels. Brain Res. 531:1990;211-218.
4. Aguayo A. J. Axonal regeneration from injured neurons in the adult mammalian central nervous system. Synaptic Plasticity. 1985;Guilford, New York. p. 457-483.
5. Alvarez-Buylla A., Vicario D. Simple microcomputer system for mapping tissue sections with the light microscope. J. Neurosci. Methods. 25:1988;165-173.
6. Barnard J. W., Carpenter W. Lack of regeneration in spinal cord of rat. J. Neurophysiol. 13:1950;223-228.
7. Baron-Van Evercooren A., Gansmuller A., Clerin E., Gumpel M. Hoechst 33342 a suitable fluorescent marker for Schwann cells after transplantation in the mouse spinal cord. Neurosci. Lett. 131:1991;241-244.
8. Basso D. M., Beattie M. S., Bresnahan J. C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma. 12:1995;1-21.
9. Berry M., Carlile J., Hunter A. Peripheral nerve explants grafted into the vitreous body of the eye promote the regeneration of retinal ganglion cell axons severed in the optic nerve. J. Neurocytol. 25:1996;147-170.
10. Bregman B. S. Spinal cord transplants permit the growth of serotonergic axons across the site of neonatal spinal cord transection. Dev. Brain Res. 34:1987;265-279.
11. Bregman B. S., Kunkel-Bagden E., Reier P. J., Dai H. N., McAtee M., Gao D. Recovery of function after spinal cord injury: Mechanisms underlying transplant-mediated recovery of function differ after spinal cord injury in newborn and adult rats. Exp. Neurol. 123:1993;3-16.
12. Broton J. G., Nikolic Z., Suys S., Calancie B. Kinematic analysis of limb position during locomotion in rats. J. Neurotrauma. 13:1996;409-416.
13. Broton J. G., Xu X. M., Bunge M. B., Lutton S., Cuthbert T., Calancie B. Hindlimb movements of adult rats with transected spinal cords. Soc. Neurosci. Abstr. 22:1996;1096.
14. Cabasso F. Hollow fiber membranes. Other K. Encyclopedia of Chemical Technology. 1980;492-517 Wiley, New York.
15. Carlstedt T., Cullheim M., Risling M., Ulfhake B. Nerve fiber regeneration across the PNS-CNS interface at the root-spinal cord junction. Brain Res. Bull. 22:1989;93-102.
16. Carter D. A., Bray G. M., Aguayo A. J. Regenerated retinal ganglion cell axons can form well-differentiated synapses in the superior colliculus of adult hamsters. J. Neurosci. 9:1989;4042-4050.
17. Casella G. T. B., Bunge R. P., Wood P. M. Improved method for harvesting human Schwann cells from mature peripheral nerve and expansion in vitro. Glia. 17:1996;327-338.
18. 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. 138:1996;261-276.
19. Cheng B., Mattson M. P. NT-3 and BDNF protect CNS neurons against metabolic/excitotoxic insults. Brain Res. 640:1994;56-67.
20. Cheng H., Cao Y., Olson L. Spinal cord repair in adult paraplegic rats: Partial restoration of hindlimb function. Science. 273:1996;510-513.
21. Cho E. Y. P., So K. F. Regrowth of retinal ganglion cell axons into a peripheral nerve graft in the adult hamster is enhanced by a concurrent optic nerve crush. Exp. Brain Res. 78:1989;567-574.
22. Cho E. Y. P., So K. F. Characterization of the sprouting response of axon-like processes from retinal ganglion cells after axotomy in adult hamsters: A model using intravitreal implantation of a peripheral nerve. J. Comp. Neurol. 21:1992;589-603.
23. Cohen A. H., Mackler S. A., Selzer M. E. Behavioral recovery following spinal transection: Functional regeneration in the lamprey CNS. Trends Neurosci. 11:1988;227-231.
24. Davidoff L. M., Ransohoff J. Absence of spinal cord regeneration in the cat. J. Neurophysiol. 11:1948;9-11.
25. Faktorovich E. G., Steinberg R. H., Yasumura D., Matthes M. T., Lavail M. M. Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature. 347:1990;83-86.
26. Fernandez E., Pallini R. Connective tissue scarring in experimental spinal cord lesions: Significance of dural continuity and role of epidural tissues. Acta Neurochirurgica. 76:1985;145-148.
27. Forman D. S., McQuarrie I. G., Graftstein B., Edwards D. L. Effect of a conditioning lesion on axonal regeneration and recovery of function. Flohr H., Precht W. Lesion-Induced Neuronal Plasticity in Sensorimotor Systems. 1981;103-113 Springer-Verlag, New York.
28. Fraher J. P. The CNS-PNS transitional zone of the rat: Morphometric studies at cranial and spinal levels. Prog. Neurobiol. 38:1992;261-316.
29. Friedman B., Kleinfeld D., Ip N. Y., Verge V. M. K., Moulton R., Boland P., Zlotchenko E., Lindsay R., Liu L. BDNF and NT 4/5 exert neurotrophic influences on injured adult spinal motor neurons. J. Neurosci. 15:1995;1044-1056.
30. Gerfen C. R., Sawchenko P. E. An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: Immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res. 290:1984;219-238.
31. Ghirnikar R. S., Eng L. F. Chondroitin sulfate proteoglycan staining in astrocyte-Schwann cell co-cultures. Glia. 14:1995;145-152.
32. Guénard V., Kleitman N., Morrissey T. K., Bunge R. P., Aebischer P. Syngeneic Schwann cells derived from adult nerves seeded in semipermeable guidance channels enhance peripheral nerve regeneration. J. Neurosci. 12:1992;3310-3320.
33. Guest J. D., Bunge R. P. Human Schwann cells can enhance axonal regeneration and myelination in the nude rat spinal cord. Soc. Neurosci. Abstr. 20:1994;458.
34. Guest J. D., Bunge R. P. Functional studies of human Schwann cells transplanted to the nude rat spinal cord. J. Neurotrauma. 12:1995;427.
35. Guest J. D., Kleitman N., Aebischer P., Bunge M. B., Bunge R. P. Axonal regeneration into human Schwann cell grafts placed to span the transected spinal cord of the nude rat. Soc. Neurosci. Abstr. 22:1996;490.
36. J. D. Guest, P. Aebischer, K. Akong, M. B. Bunge, R. P. Bunge, 1997, Human Schwann cell transplants in transected nude rat spinal cord: graft survival, axonal regeneration, and myelination.
37. Guth L., Zhang Z., Diprospero N. A., Joubin K., Fitch M. Spinal cord injury in the rat: Treatment with bacterial lipopolysaccharide and indomethacin enhanced cellular repair and locomotor function. Exp. Neurol. 126:1994;76-87.
38. P. H. Gutin, D. Kim, L. Noble, R. P. Nockels, J. Yu, 1996, Treatment with NGF or BDNF accelerates recovery from acute traumatic spinal cord injury, Abstracts of the Annual Meeting of the American Association of Neurological Surgeons.
39. Iwashita Y., Kawaguchi S., Murata M. Restoration of function by replacement of spinal cord segments in the rat. Nature. 367:1994;167-170.
40. Jakeman L. B., Reier P. J. Axonal projections between fetal spinal cord transplants and the adult rat spinal cord: A neuroanatomical tracing study of local interactions. J. Comp. Neurol. 307:1991;311-334.
41. Johnson A. R., Gregson N. A., Wigley C. B., Berry M. The conditioning effect of optic nerve injury upon axonal regrowth from adult rat retinal ganglion cells explanted in vitro. Neurosci. Lett. 97:1989;63-68.
42. Jones C. J., Mosley S. M., Jeffrey I. J., Stoddart R. W. Elimination of the non-specific binding of avidin to tissue sections. Histochem. J. 19:1987;264-268.
43. Jordan L. M. Control of functional systems in the brainstem and spinal cord. Curr. Opin. Neurobiol. 2:1992;794-801.
44. Kao C. C., Chang L. W., Bloodworth J. M. B. Jr. Axonal regeneration across transected mammalian spinal cords: An electron microscopic study of delayed microsurgical nerve grafting. Exp. Neurol. 54:1977;591-615.
45. Kato M., Murakami S., Hirayama H., Hikino K. Recovery of postural control following chronic bilateral hemisections at different spinal cord levels in adult cats. Exp. Neurol. 90:1985;350-364.
46. Keirstead S. A., Rasminsky M., Fukuda Y., Carter D. A., Aguayo A. J., Vidal-Sanz M. Electrophysiological responses in hamster superior colliculus evoked by regenerating retinal axons. Science. 246:1989;255-258.
47. Koliatsos V. E., Price D. L., Gouras G. K., Cayouette M. H., Burton L. E., Winslow J. W. Highly selective effects of nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 on intact and injured basal forebrain magnocellular neurons. J. Comp. Neurol. 343:1994;247-262.
48. Krikorian J. G., Guth L., Donati E. J. Origin of the connective tissue scar in the transected rat spinal cord. Exp. Neurol. 72:1981;698-707.
49. Kromer L. F., Cornbrooks C. J. Transplants of Schwann cell cultures promote axonal regeneration in the adult mammalian brain. Proc. Natl. Acad. Sci. USA. 82:1985;6330-6334.
50. Levi A. D. O., Bunge R. P. Studies of myelin formation after transplantation of human Schwann cells into the severe combined immunodeficient mouse. Exp. Neurol. 130:1994;41-52.
51. Levi A. D. O., Sliwkowski M. X., Lofgren J., Hefti F., Bunge R. P. The influence of heregulins on human Schwann cell proliferation. J. Neurosci. 15:1995;1329-1340.
52. Lindvall O., Kokaia Z., Bengzon J., Elmér E., Kokaia M. Neurotrophins and brain insults. Trends Neurosci. 17:1994;490-496.
53. Lotan M., Solomon A., Ben-Bassat S., Schwartz M. Cytokines modulate the inflammatory response and change permissiveness to neuronal adhesion in injured mammalian central nervous system. Exp. Neurol. 126:1994;284-290.
54. Lu X., Richardson P. M. Inflammation near the nerve cell body enhances axonal regeneration. J. Neurosci. 11:1991;972-978.
55. Lu X., Richardson P. M. Changes in neuronal mRNAs induced by a local inflammatory reaction. J. Neurosci. Res. 41:1995;8-14.
56. Mansour-Robaey S., Clarke D. B., Wang Y. C., Bray G. M., Aguayo A. J. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc. Natl. Acad. Sci. USA. 91:1994;1632-1636.
57. Martin D., Schoenen J., Delree P., Rigo J. M., Rogister B., Leprince P., Moonen G. Syngeneic grafting of adult rat DRG-derived Schwann cells to the injured spinal cord. Brain Res. Bull. 30:1993;507-514.
58. McClellan A. D. Locomotor recovery in spinal-transected lamprey: Regenerated spinal coordinating neurons and mechanosensory inputs couple locomotor activity across a spinal lesion. Neuroscience. 35:1990;675-685.
59. McClellan A. D. Time course of locomotor recovery and functional regeneration in spinal cord-transected lamprey: In vitro preparations. J. Neurophysiol. 2:1994;847-860.
60. McKeon R. J., Silver J. Functional significance of glial-derived matrix during development and regeneration. Kettenmann H., Ransom B. R. Neuroglia. 1995;398-410 Oxford Univ. Press, Cambridge.
61. McKeon R. J., Schreiber R. C., Rudge J. S., Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS Injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J. Neurosci. 11:1991;3398-3411.
62. Meier C., Sollmann H. Glial outgrowth and central-type myelination of regenerating axons in spinal nerve roots following transection and suture: Light and electron microscopic study in the pig. Neuropathol. Appl. Neurobiol. 4:1978;21-35.
63. Meisel R. L., Rakerd B. Induction of hindlimb stepping movements in rats spinally transected as adults or neonates. Brain Res. 240:1982;353-356.
64. Menei P., Montero-Menei C., Whittemore S. R., Bunge M. B., Bunge R. P. Schwann cells genetically engineered to produce BDNF promote axonal regeneration of brainstem neurons across transected adult rat spinal cord. Soc. Neurosci Abstr. 22:1996;406.
65. Monsonego A., Hauben E., Solomon A. S., Yoles E., Schwartz M. Cytokine-modulated astrocytes transplanted into transected adult rat optic nerve facilitate recovery of visual response. Soc. Neurosci. Abstr. 22:1996;490.
66. Montero-Menei C. N., Pouplard-Barthelaix A., Gumpel M., Baron-Van Evercooren A. Pure Schwann cell suspension grafts promote regeneration of the lesioned septo-hippocampal cholinergic pathway. Brain Res. 570:1992;198-208.
67. Morrissey T. K., Kleitman N., Bunge R. P. Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J. Neurosci. 11:1991;2433-2442.
68. Morrissey T. K., Levi A. D. O., Nuijens A., Sliwkowski M. X., Bunge R. P. Axon-induced mitogenesis of human Schwann cells involves heregulin and p185 erbB2. Proc. Natl. Acad. Sci. USA. 92:1995;1431-1435.
69. Newton B. W., Hamill R. W. Immunohistochemical demonstration of serotinin neurons in autonomic regions of the rat spinal cord. Brain Res. 376:1986;155-163.
70. Newton B. W., Hamill R. W. The morphology and distribution of rat serotinergic intraspinal neurons: An immunohistochemical study. Brain Res. Bull. 20:1988;349-360.
71. Ng T. F., So K. F., Chung S. K. Influence of peripheral nerve grafts on the expression of GAP-43 in regenerating retinal ganglion cells in adult hamsters. J. Comp. Neurol. 24:1995;487-496.
72. Pindzola R. R., Doller C., Silver J. Putative inhibitory extracellular matrix molecules at the dorsal root entry zone during development and after root and sciatic nerve lesions. Dev. Biol. 156:1993;34-48.
73. Pleasure D., Kreider B., Sobue G., Ross A. H., Koprowski H., Sonnenfeld K. H., Rubenstein A. E. Schwann-like cells cultured from human dermal fibromas. Ann. NY Acad. Sci. 486:1986;227-240.
74. Ramón Y Cajal S. May R. M. Degeneration and Regeneration of the Nervous System. 1928;Oxford Univ. Press, New York.
75. Reier P. J., Bregman B. S., Wujek J. R. Intraspinal transplantation of embryonic spinal cord tissue in neonatal and adult rats. J. Comp. Neurol. 247:1986;275-296.
76. Richardson P. M., McGuinness U. M., Aguayo A. J. Axons from CNS grafts regenerate into PNS grafts. Nature. 284:1980;264-265.
77. Richardson P. M., McGuinness U. M., Aguayo A. J. Peripheral nerve autografts to the rat spinal cord: Studies with axonal tracing methods. Brain Res. 237:1982;147-162.
78. Richardson P. M., Issa V. M. K., Aguayo A. J. Regeneration of long spinal axons in the rat. J. Neurocytol. 13:1984;165-182.
79. Rivlin A. S., Tator C. H. Objective clinical assessment of motor function after experimental spinal cord injury in the rat. J. Neurosurg. 47:1977;577-581.
80. Rosina A. Rapid anterograde transport of the fluorescent tracer Fast-blue: A new method for tracing central connections. Neurosci. Lett. 33:1982;217-221.
81. Sauvé Y., Sawai H., Rasminsky M. Functional synaptic connections made by regenerated retinal ganglion cell axons in the superior colliculus of adult hamsters. J. Neurosci. 15:1995;665-675.
82. Sceats D. J., Friedman W. A., Sypert G. W., Ballinger W. E. Regeneration in peripheral nerve grafts to the cat spinal cord. Brain Res. 362:1986;149-156.
83. Schmued L., Kyriakidis K., Heimer L. In vivo anterograde and retrograde axonal transport of the fluorescent rhodamine-dextran-aime, Fluoro-ruby, within the CNS. Brain Res. 526:1990;127-134.
84. Selzer M. E. Mechanisms of functional recovery and regeneration after spinal cord transection in larval sea lamprey. J. Physiol. 277:1978;395-408.
85. Stelzner D. J., Cullen J. M. Do propriospinal projections contribute to hindlimb recovery when all long tracts are cut in neonatal or weanling rats? Exp. Neurol. 114:1991;193-205.
86. Stelzner D. J., Ershler W. B., Weber E. D. Effects of spinal transection in neonatal and weanling rats: Survival of function. Exp. Neurol. 46:1975;156-177.
87. Stensaas L. J., Partlow L. M., Burgess P. R., Horch K. W. Inhibition of regeneration: The ultrastructure of reactive astrocytes and abortive axon terminals in the transition zone of the dorsal root. Prog. Brain Res. 71:1984;457-467.
88. Stichel C. C., Lips K., Müller H. W. Transplantation of Schwann cell suspension promotes regeneration in the transected postcommissural fornix of adult rats. J. Neurotrauma. 12:1995;375.
89. Stichel C. C., Lips K., Wunderlich G., Müller H. W. Reconstruction of transected fornix in adult rat by Schwann cell suspension grafts. Exp. Neurol. 140:1996;21-36.
90. Sugar O., Gerard R. W. Spinal cord regeneration in the rat. J. Neurophysiol. 3:1940;1-19.
91. Tello F. La influencia del neurotrophismo en la regeneracion de los centros nerviosos. Trabajos del Laboratorio de Investigaciones Biologicas de la Universidad de Madrid. 9:1911;123-159.
92. Tetzlaff W., Kobayashi N. R., Giehl K. M. G., Tsui B. J., Cassar S. L., Bedard A. M. Response of rubrospinal and corticospinal neurons to injury and neurotrophins. Prog. Brain Res. 103:1994;271-286.
93. Tourtellotte W., Van Hoesen G. Computer-aided two-dimensional high-resolution axon tracing: an application using the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L). J. Neurosci. Methods. 41:1992;101-112.
94. Tseng G. F., Shu J., Huang S. J., Wang Y. J. A time-dependent loss of retrograde transport ability in distally axotomized rubrospinal neurons. Anat. Embryol. 191:1995;243-249.
95. Tuszynski M. H., Peterson D. A., Ray J., Baird A., Nakahara Y., Gage F. H. Fibroblasts genetically modified to produce nerve growth factor induce robust neuritic ingrowth after grafting to the spinal cord. Exp. Neurol. 126:1994;1-14.
96. Vidal-Sanz M., Bray G. M., Villegas-Pérez M. P., Thanos S., Aguayo A. J. Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J. Neurosci. 7:1987;2894-2909.
97. Wardrope J., Wilson D. H. Peripheral nerve grafting in the spinal cord: A histological and electrophysiological study. Paraplegia. 24:1986;370-378.
98. Windle W. F., Chambers W. W. Regeneration in the spinal cord of the cat and dog. J. Comp. Neurol. 93:1950;241-257.
99. Wrathall J. R., Rigamonti D. D., Braford M. R., Kao C. C. Reconstruction of the contused cat spinal cord by the delayed nerve graft technique and cultured peripheral non-neuronal cells. Acta Neuropathol. (Berlin). 57:1982;59-69.
100. Wright J. H. A rapid method for differential staining of blood films and malarial parasites. J. Med. Res. 7:1902;138-144.
101. Xu X. M., Guénard V., Kleitman N., Bunge M. B. Axonal regeneration into Schwann cell-seeded guidance ghannels grafted into transected adult rat spinal cord. J. Comp. Neurol. 351:1995;145-160.
102. Xu X. M., Guénard V., Kleitman N., Aebischer P., Bunge M. B. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 134:1995;261-272.
103. Xu X. M., Chen A., Guenard V., Kleitman N., Bunge M. B. Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of the transected adult rat spinal cord. J. Neurocytol. 26:1997;1-16.
104. Yakovleff A., Cabelguen J. M., Orsal D., Gimenz Y Ribotta M., Rajaofetra N., Drain M. J., Bussel B., Privat A. Fictive motor activities in adult chronic spinal rats transplanted with embryonic brainstem neurons. Exp. Brain. Res. 106:1995;69-78.