Combined demyelination plus Schwann cell transplantation therapy increases spread of cells and axonal regeneration following contusion injury

Journal of Neurotrauma

Volumn 21, Issue 6, 2004, Pages 775-788

  Azanchi, Roya ^a   Bernal, Giovanna ^a   Gupta, Ranjan ^b   Keirstead, Hans S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell spread; CNS regeneration; Immunological demyelination; Schwann cell transplantation; Spinal cord injury

Indexed keywords

GALACTOSYLCERAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXONAL INJURY; BRAIN INJURY; CELL POPULATION; CELL SUSPENSION; CELL TRANSPLANTATION; CONTROLLED STUDY; CONTUSION; DEMYELINATION; FEMALE; IMPLANTATION; LOCOMOTION; NERVE FIBER REGENERATION; NONHUMAN; PROSPECTIVE STUDY; RAT; SCHWANN CELL; SPINAL CORD INJURY; TISSUE DISTRIBUTION; TROPHIC LEVEL;

ANIMALS; ANTIBODIES; AXONS; CELL MOVEMENT; DEMYELINATING DISEASES; FEMALE; GALACTOSYLCERAMIDES; MYELIN SHEATH; NERVE REGENERATION; RATS; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS; SPINAL CORD INJURIES;

EID: 3042771510     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/0897715041269696     Document Type: Article

References (80)

1. ACHESON, A., BARKER, P.A., et al. (1991). Detection of brain-derived neurotrophic factor-like activity in fibroblasts and Schwann cells: inhibition by antibodies to NGF. Neuron 7, 265-275.
2. AKESSON, E., HOLMBERG, L., et al. (2001). Solid human embryonic spinal cord xenografts in acute and chronic spinal cord cavities: a morphological and functional study. Exp. Neurol. 170, 305-316.
3. AZIZI, S.A., STOKES, D., et al. (1998). Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats-similarities to astrocyte grafts. Proc. Natl. Acad. Sci. U S A 95, 3908-3913.
4. BANDTLOW, C.E., HEUMANN, R., et al. (1987). Cellular localization of nerve growth factor synthesis by in situ hybridization. EMBO J. 6, 891-899.
5. BASSO, D.M., BEATTIE, M.S., et al. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
6. BERNSTEIN-GORAL, H., and BREGMAN, B.S. (1993). Spinal cord transplants support the regeneration of axotomized neurons after spinal cord lesions at birth: a quantitative double-labeling study. Exp. Neurol. 123, 118-132.
7. BLAKEMORE, W.F. (1977). Remyelination of CNS axons by Schwann cells transplanted from the sciatic nerve. Nature 266, 68-69.
8. BLAKEMORE, W.F., and CRANG, A.J. (1985). The use of cultured autologous Schwann cells to remyelinate areas of persistent demyelination in the central nervous system. J. Neurol. Sci. 70, 207-223.
9. BORISOFF, J.F., PATAKY, D.M., et al. (2000). Raphe-spinal neurons display an age-dependent differential capacity for neurite outgrowth compared to other brainstem-spinal populations. Exp. Neurol. 166, 16-28.
10. BREGMAN, B.S. (1998). Regeneration in the spinal cord. Curr. Opin. Neurobiol. 8, 800-807.
11. BREGMAN, B.S., COUMANS, J.V., et al. (2002). Transplants and neurotrophic factors increase regeneration and recovery of function after spinal cord injury. Prog. Brain Res. 137, 257-273.
12. BREGMAN, B.S., and GOLDBERGER, M.E. (1982). Anatomical plasticity and sparing of function after spinal cord damage in neonatal cats. Science 217, 553-555.
13. BREGMAN, B.S., KUNKEL-BAGDEN, E., et al. (1989). Extension of the critical period for developmental plasticity of the corticospinal pathway. J. Comp. Neurol. 282, 355-370.
14. BREGMAN, B.S., KUNKEL-BAGDEN, E., et al. (1993). 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, 3-16.
15. BROCKES, J.P., FIELDS, K.L., et al. (1979). Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve. Brain Res. 165, 105-118.
16. BROUDE, E., McATEE, M., et al. (1999). Fetal spinal cord transplants and exogenous neurotrophic support enhance c-Jun expression in mature axotomized neurons after spinal cord injury. Exp. Neurol. 155, 65-78.
17. BUNGE, M.B. (2001). Bridging areas of injury in the spinal cord. Neuroscientist 7, 325-339.
18. CAO, Q.L., ONIFER, S.M., et al. (2002). Labeling stem cells in vitro for identification of their differentiated phenotypes after grafting into the CNS. Methods Mol. Biol. 198, 307-318.
19. CARONI, P., and SCHWAB, M.E. (1988). Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1, 85-96.
20. CHEN, A., XU, X.M., et al. (1996). Methylprednisolone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp. Neurol. 138, 261-276.
21. COUMANS, J.V., LIN, T.T., et al. (2001). Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J. Neurosci. 21, 9334-9344.
22. DEZAWA, M. (2002). Central and peripheral nerve regeneration by transplantation of Schwann cells and transdifferentiated bone marrow stromal cells. Anat. Sci. Int. 77, 12-25.
23. DEZAWA, M., and ADACHI-USAMI, E. (2000). Role of Schwann cells in retinal ganglion cell axon regeneration. Prog. Retin. Eye Res. 19, 171-204.
24. DYER, J.K., BOURQUE, J.A., et al. (1998). Regeneration of brainstem-spinal axons after lesion and immunological disruption of myelin in adult rat. Exp. Neurol. 154, 12-22.
25. FRANKLIN, R.J., and BLAKEMORE, W.F. (1993). Requirements for Schwann cell migration within CNS environments: a viewpoint. Int. J. Dev. Neurosci. 11, 641-649.
26. FRANZEN, R., SCHOENEN, J., et al. (1998). Effects of macrophage transplantation in the injured adult rat spinal cord: a combined immunocytochemical and biochemical study. J. Neurosci. Res. 51, 316-327.
27. FRIEDMAN, B., SCHERER, S.S., et al. (1992). Regulation of ciliary neurotrophic factor expression in myelin-related Schwann cells in vivo. Neuron 9, 295-305.
28. FRY, E.J., and SAUNDERS, N.R. (2000). Spinal repair in immature animals: a novel approach using the South American opossum Monodelphis domestica. Clin. Exp. Pharmacol. Physiol. 27, 542-547.
29. FULOP, Z.L., LESCAUDRON, L., et al. (1997). Astrocytes grafted into rat nucleus basalis magnocellularis immediately after ibotenic acid injection fail to survive and have no effect on functional recovery. Int. J. Neurosci. 90, 203-222.
30. GRILL, R., MURAI, K., et al. (1997). Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 17, 5560-5572.
31. GUEST, J.D., RAO, A., et al. (1997). The ability of human Schwann cell grafts to promote regeneration in the transected nude rat spinal cord. Exp. Neurol. 148, 502-522.
32. HASAN, S.J., KEIRSTEAD, H.S., et al. (1993). Axonal regeneration contributes to repair of injured brainstem-spinal neurons in embryonic chick. J. Neurosci. 13, 492-507.
33. HIMES, B.T., LIU, Y., et al. (2001). Transplants of cells genetically modified to express neurotrophin-3 rescue axotomized Clarke's nucleus neurons after spinal cord hemisection in adult rats. J. Neurosci. Res. 65, 549-564.
34. IWASHITA, Y., FAWCETT, J.W., et al. (2000). Schwann cells transplanted into normal and X-irradiated adult white matter do not migrate extensively and show poor long-term survival. Exp. Neurol. 164, 292-302.
35. JIN, Y., FISCHER, I., et al. (2002). Transplants of fibroblasts genetically modified to express BDNF promote axonal regeneration from supraspinal neurons following chronic spinal cord injury. Exp. Neurol. 177, 265-275.
36. KAPFHAMMER, J.P., and SCHWAB, M.E. (1994). Inverse patterns of myelination and GAP-43 expression in the adult CNS: neurite growth inhibitors as regulators of neuronal plasticity? J. Comp. Neurol. 340, 194-206.
37. KEIRSTEAD, H.S., DYER, J.K., et al. (1995). Axonal regeneration and physiological activity following transection and immunological disruption of myelin within the hatchling chick spinal cord. J. Neurosci. 15, 6963-6974.
38. KEIRSTEAD, H.S., HASAN, S.J., et al. (1992). Suppression of the onset of myelination extends the permissive period for the functional repair of embryonic spinal cord. Proc. Natl. Acad. Sci. USA 89, 11664-11668.
39. KEIRSTEAD, H.S., HUGHES, H.C., et al. (1998). A quantifiable model of axonal regeneration in the demyelinated adult rat spinal cord. Exp. Neurol. 151, 303-313.
40. KEIRSTEAD, H.S., MORGAN, S.V., et al. (1999). Enhanced axonal regeneration following combined demyelination plus schwann cell transplantation therapy in the injured adult spinal cord. Exp. Neurol. 159, 225-236.
41. KEIRSTEAD, H.S., PATAKY, D.M., et al. (1997). In vivo immunological suppression of spinal cord myelin development. Brain Res. Bull. 44, 727-734.
42. LESCAUDRON, L., FULOP, Z., et al. (2001). Behavioral and morphological consequences of primary astrocytes transplanted into the rat cortex immediately after nucleus basalis ibotenic lesion. Int. J. Neurosci. 106, 63-85.
43. LI, Y., FIELD, P.M., et al. (1997). Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277, 2000-2002.
44. LIU, Y., KIM, D., et al. (1999). Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J. Neurosci. 19, 4370-4387.
45. LOH, N.K., WOERLY, S., et al. (2001). The regrowth of axons within tissue defects in the CNS is promoted by implanted hydrogel matrices that contain BDNF and CNTF producing fibroblasts. Exp. Neurol. 170, 72-84.
46. MARTIN, D., SCHOENEN, J., et al. (1991). Grafts of syngenic cultured, adult dorsal root ganglion-derived Schwann cells to the injured spinal cord of adult rats: preliminary morphological studies. Neurosci. Lett. 124, 44-48.
47. McDONALD, J.W., and HOWARD, M.J. (2002). Repairing the damaged spinal cord: a summary of our early success with embryonic stem cell transplantation and remyelination. Prog. Brain Res. 137, 299-309.
48. McKERRACHER, L., DAVID, S., et al. (1994). Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13, 805-811.
49. MEYER, M., MATSUOKA, I., et al. (1992). 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.
50. MIYA, D., GISZTER, S., et al. (1997). Fetal transplants alter the development of function after spinal cord transection in newborn rats. J. Neurosci. 17, 4856-4872.
51. MLADINIC, M., and WINTZER, M. (2002). Changes in mRNA content of developing opossum spinal cord at stages when regeneration can and cannot occur after injury. Brain Res. Brain Res. Rev. 40, 317-324.
52. MONTGOMERY, C.T., TENAGLIA, E.A., et al. (1996). Axonal growth into tubes implanted within lesions in the spinal cords of adult rats. Exp. Neurol. 137, 277-290.
53. MUKHOPADHYAY, G., DOHERTY, P., et al. (1994). A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13, 757-767.
54. NEUMANN, S., and WOOLF, C.J. (1999). Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23, 83-91.
55. NICHOLLS, J., and SAUNDERS, N. (1996). Regeneration of immature mammalian spinal cord after injury. Trends Neurosci 19, 229-234.
56. OGAWA, Y., SAWAMOTO, K., et al. (2002). Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J. Neurosci. Res. 69, 925-933.
57. OLSON, L. (1997). Regeneration in the adult central nervous system: experimental repair strategies. Nat. Med. 3, 1329-1335.
58. OUDEGA, M., XU, X.M., et al. (1997). A combination of insulin-like growth factor-I and platelet-derived growth factor enhances myelination but diminishes axonal regeneration into Schwann cell grafts in the adult rat spinal cord. Glia 19, 247-258.
59. PAINO, C.L., FERNANDEZ-VALLE, C., et al. (1994). Regrowth of axons in lesioned adult rat spinal cord: promotion by implants of cultured Schwann cells. J. Neurocytol. 23, 433-452.
60. PINZON, A., CALANCIE, B., et al. (2001). Conduction of impulses by axons regenerated in a Schwann cell graft in the transected adult rat thoracic spinal cord. J. Neurosci. Res. 64, 533-541.
61. RABCHEVSKY, A.G., and STREIT, W.J. (1997). Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J. Neurosci. Res. 47, 34-48.
62. RAMON-CUETO, A., and AVILA, J. (1998). Olfactory ensheathing glia: properties and function. Brain Res. Bull. 46, 175-187.
63. RAMON-CUETO, A., CORDERO, M.I., et al. (2000). Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25, 425-435.
64. RAMON-CUETO, A., PLANT, G.W., et al. (1998). Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J. Neurosci. 18, 3803-3815.
65. RAPALINO, O., LAZAROV-SPIEGLER, O., et al. (1998). Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat. Med. 4, 814-821.
66. RENDE, M., MUIR, D., et al. (1992). Immunolocalization of ciliary neuronotrophic factor in adult rat sciatic nerve, Glia 5, 25-32.
67. RICHARDSON, P.M., MCGUINNESS, U.M., et al. (1982). Peripheral nerve autografts to the rat spinal cord: studies with axonal tracing methods. Brain Res. 237, 147-162.
68. SCHNELL, L., and SCHWAB, M.E., (1993). Sprouting and regeneration of lesioned corticospinal tract fibres in the adult rat spinal cord. Eur. J. Neurosci. 5, 1156-1171.
69. SCHWAB, M.E. (2002). Increasing plasticity and functional recovery of the lesioned spinal cord. Prog. Brain Res. 137, 351-359.
70. TAKAMI, T., OUDEGA, M., et al. (2002). Methylprednisolone and interleukin-10 reduce gray matter damage in the contused Fischer rat thoracic spinal cord but do not improve functional outcome. J. Neurotrauma 19, 653-666.
71. THALLMAIR, M., METZ, G.A., et al. (1998). Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat. Neurosci. 1, 124-131.
72. VIDAL-SANZ, M., BRAY, G.M., et al. (1991). Regenerated synapses persist in the superior colliculus after the regrowth of retinal ganglion cell axons. J. Neurocytol. 20, 940-952.
73. VIDAL-SANZ, M., BRAY, G.M., et al. (1987). Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J. Neurosci, 7, 2894-2909.
74. WANG, J.J., CHUAH, M.I., et al. (1995). Effects of astrocyte implantation into the hemisected adult rat spinal cord. Neuroscience 65, 973-981.
75. WEIDNER, N., BLESCH, A., et al. (1999). Nerve growth factor- hypersecreting Schwann cell grafts augment and guide spinal cord axonal growth and remyelinate central nervous system axons in a phenotypically appropriate manner that correlates with expression of L1. J. Comp. Neurol. 413, 495-506.
76. WIDENFALK, J., LUNDSTROMER, K., et al. (2001). Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J. Neurosci. 21, 3457-3475.
77. XU, X.M., CHEN, A., et al. (1997). Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J. Neurocytol. 26, 1-16.
78. XU, X.M., GUENARD, V., et al. (1995). A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 134, 261-272.
79. XU, X.M., GUENARD, V., et al. (1995). Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol. 351, 145-160.
80. XU, X.M., ZHANG, S.X., et al. (1999). Regrowth of axons into the distal spinal cord through a Schwann-cell-seeded minichannel implanted into hemisected adult rat spinal cord. Eur. J. Neurosci. 11, 1723-1740.