Transplantation of embryonic spinal cord-derived neurospheres support growth of supraspinal projections and functional recovery after spinal cord injury in the neonatal rat

Journal of Neuroscience Research

Volumn 81, Issue 4, 2005, Pages 457-468

  Nakamura, M ^a,b   Okano, H ^b,c   Toyama, Y ^b   Dai, H N ^a   Finn, T P ^a   Bregman, Barbara S ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b KEIO UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Neonate; Progenitor; Regeneration; Spinal cord injury; Transplantation

Indexed keywords

BROXURIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN STEM; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; ELECTRON MICROSCOPY; FETAL TISSUE TRANSPLANTATION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOPEROXIDASE STAINING; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE PROJECTION; NEURAL STEM CELL; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; SPINAL CORD TRANSPLANTATION;

ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; FEMALE; GRAFT SURVIVAL; NERVE FIBERS, MYELINATED; NERVE REGENERATION; NEURONS; OLIGODENDROGLIA; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; SYNAPSES;

EID: 24744459462     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20580     Document Type: Article

References (65)

1. Bernstein-Goral H, Bregman BS. 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.
2. Bernstein-Goral H, Diener PS, Bregman BS. 1997. Regenerating and sprouting axons differ in their requirements for growth after injury. Exp Neurol 148:51-72.
3. Blakemore WF, Chari DM, Gilson JM, Crang AJ. 2002. Modelling large areas of demyelination in the rat reveals the potential and possible limitations of transplanted glial cells for remyelination in the CNS. Glia 38:155-168.
4. Bregman BS. 1987a. Development of serotonin immunoreactivity in the rat spinal cord and its plasticity after neonatal spinal cord lesions. Brain Res 431:245-263.
5. Bregman BS. 1987b. Spinal cord transplants permit the growth of serotonergic axons across the site of neonatal spinal cord transection. Brain Res 431:265-279.
6. Bregman BS, Bernstein-Goral H. 1991. Both regenerating and late-developing pathways contribute to transplant-induced anatomical plasticity after spinal cord lesions at birth. Exp Neurol 112:49-63.
7. Bregman BS, Broude E, McAtee M, Kelley MS. 1998. Transplants and neurotrophic factors prevent atrophy of mature CNS neurons after spinal cord injury. Exp Neurol 149:13-27.
8. Bregman BS, Coumans JV, Dai HN, Kuhn PL, Lynskey J, McAtee M, Sandhu F. 2002. Transplants and neurotrophic factors increase regeneration and recovery of function after spinal cord injury. Prog Brain Res 137:257-273.
9. Bregman BS, Goldberger ME. 1982. Anatomical plasticity and sparing of function after spinal cord damage in neonatal cats. Science 217:553-555.
10. Bregman BS, Goldberger ME. 1983. Infant lesion effect: III. Anatomical correlates of sparing and recovery of function after spinal cord damage in newborn and adult cats. Brain Res 9:137-154.
11. Bregman BS, Kunkel-Bagden E, McAtee M, O'Neill A. 1989. Extension of the critical period for developmental plasticity of the corticospinal pathway. J Comp Neurol 282:355-370.
12. Bregman BS, Kunkel-Bagden E, Reier PJ, Dai HN, McAtee M, Gao D. 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.
13. Bregman BS, McAtee M, Dai HN, Kuhn PL. 1997. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp Neurol 148:475-494.
14. Bregman BS, Reier PJ. 1986. Neural tissue transplants rescue axotomized rubrospinal cells from retrograde death. J Comp Neurol 244:86-95.
15. Cao Q, Benton RL, Whittemore SR. 2002a. Stem cell repair of central nervous system injury. J Neurosci Res 68:501-510.
16. Cao QL, Howard RM, Dennison JB, Whittemore SR. 2002b. Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp Neurol 177:349-359.
17. Cao QL, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR. 2001. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 167:48-58.
18. Coumans JV, Lin TT, Dai HN, MacArthur L, McAtee M, Nash C, Bregman BS. 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.
19. Diener PS, Bregman BS. 1994. Neurotrophic factors prevent the death of CNS neurons after spinal cord lesions in newborn rats. Neuroreport 5:1913-1917.
20. Diener PS, Bregman BS. 1998. Fetal spinal cord transplants support growth of supraspinal and segmental projections after cervical spinal cord hemisection in the neonatal rat. J Neurosci 18:779-793.
21. Frederiksen K, McKay RD. 1988. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144-1151.
22. Frisen J, Johansson CB, Torok C, Risling M, Lendahl U. 1995. Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131:453-464.
23. Geller HM, Fawcett JW. 2002. Building a bridge: engineering spinal cord repair. Exp Neurol 174:125-136.
24. Groves AK, Barnett SC, Franklin RJ, Crang AJ, Mayer M, Blakemore WF, Noble M. 1993. Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells. Nature 362:453-455.
25. Han SS, Kang DY, Mujtaba T, Rao MS, Fischer I. 2002. Grafted lineage-restricted precursors differentiate exclusively into neurons in the adult spinal cord. Exp Neurol 177:360-375.
26. Han SS, Liu Y, Tyler-Polsz C, Rao MS, Fischer I. 2004. Transplantation of glial-restricted precursor cells into the adult spinal cord: survival, glial-specific differentiation, and preferential migration in white matter. Glia 45:1-16.
27. Hardy RJ, Friedrich VL Jr. 1996. Oligodendrocyte progenitors are generated throughout the embryonic mouse brain, but differentiate in restricted foci. Development 122:2059-2069.
28. Harper JM, Krishnan C, Darman JS, Deshpande DM, Peck S, Shats I, Backovic S, Rothstein JD, Kerr DA. 2004. Axonal growth of embryonic stem cell-derived motoneurons in vitro and in motoneuron-injured adult rats. Proc Natl Acad Sci USA 101:7123-7128.
29. Herrera J, Yang H, Zhang SC, Proschel C, Tresco P, Duncan ID, Luskin M, Mayer-Proschel M. 2001. Embryonic-derived glial-restricted precursor cells (GRP cells) can differentiate into astrocytes and oligodendrocytes in vivo. Exp Neurol 171:11-21.
30. Hill CE, Proschel C, Noble M, Mayer-Proschel M, Gensel JC, Beattie MS, Bresnahan JC. 2004. Acute transplantation of glial-restricted precursor cells into spinal cord contusion injuries: survival, differentiation, and effects on lesion environment and axonal regeneration. Exp Neurol 190:289-310.
31. Hughes SM, Lillien LE, Raff MC, Rohrer H, Sendtner M. 1988. Ciliary neurotrophic factor induces type-2 astrocyte differentiation in culture. Nature 335:70-73.
32. Inoue M, Honmou O, Oka S, Houkin K, Hashi K, Kocsis JD. 2003. Comparative analysis of remyelinating potential of focal and intravenous administration of autologous bone marrow cells into the rat demyelinated spinal cord. Glia 44:111-118.
33. Jakeman LB, Reier PJ, Bregman BS, Wade EB, Dailey M, Kastner RJ, Himes BT, Tessler A. 1989. Differentiation of substantia gelatinosa-like regions in intraspinal and intracerebral transplants of embryonic spinal cord tissue in the rat. Exp Neurol 103:17-33.
34. Joosten EA, Bar DP. 1999. Axon guidance of outgrowing corticospinal fibres in the rat. J Anat 194:15-32.
35. Kalyani A, Hobson K, Rao MS. 1997. Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev Biol 186:202-223.
36. Kilpatrick TJ, Bartlett PF. 1993. Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron 10:255-265.
37. Kunkel-Bagden E, Bregman BS. 1990. Spinal cord transplants enhance the recovery of locomotor function after spinal cord injury at birth. Exp Brain Res 81:25-34.
38. Kunkel-Bagden E, Dai HN, Bregman BS. 1992. Recovery of function after spinal cord hemisection in newborn and adult rats: differential effects on reflex and locomotor function. Exp Neurol 116:40-51.
39. Kunkel-Bagden E, Dai HN, Bregman BS. 1993. Methods to assess the development and recovery of locomotor function after spinal cord injury in rats. Exp Neurol 119:153-164.
40. Lee MY, Kim CJ, Shin SL, Moon SH, Chun MH. 1998. Increased ciliary neurotrophic factor expression in reactive astrocytes following spinal cord injury in the rat. Neurosci Lett 255:79-82.
41. Liu S, Qu Y, Stewart TJ, Howard MJ, Chakrabortty S, Holekamp TF, McDonald JW. 2000. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc Natl Acad Sci USA 97:6126-6131.
42. Liu Y, Wu Y, Lee JC, Xue H, Pevny LH, Kaprielian Z, Rao MS. 2002. Oligodendrocyte and astrocyte development in rodents: an in situ and immunohistological analysis during embryonic development. Glia 40:25-43.
43. Lu P, Jones LL, Snyder EY, Tuszynski MH. 2003. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol 181:115-129.
44. Marmur R, Kessler JA, Zhu G, Gokhan S, Mehler MF. 1998. Differentiation of oligodendroglial progenitors derived from cortical multipotent cells requires extrinsic signals including activation of gp10/LIFbeta receptors. J Neurosci 18:9800-9811.
45. Mayer M, Bhakoo K, Noble M. 1994. Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro. Development 120:143-153.
46. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D, Gottlieb DI, Choi DW. 1999. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5: 1410-1412.
47. Nakamura M, Bregman BS. 2001. Differences in neurotrophic factor gene expression profiles between neonate and adult rat spinal cord after injury. Exp Neurol 169:407-415.
48. Nakamura M, Houghtling RA, MacArthur L, Bayer BM, Bregman BS. 2003. Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp Neurol 184:313-325.
49. Nakamura M, Okano H, Miyat T, Ogawa Y, Dai HN, Bundesen LQ, Bregman BS. 2000. Neutralization of endogenous ciliary neurotrophic factor blocks the differentiation of spinal cord progenitor cells into astrocytes. Soc Neurosci Abstr 26:1341.
50. Namiki J, Tator CH. 1999. Cell proliferation and nestin expression in the ependyma of the adult rat spinal cord after injury. J Neuropathol Exp Neurol 58:489-498.
51. Nandi KN, Knight DS, Beal JA. 1993. Spinal neurogenesis and axon projection: a correlative study in the rat. J Comp Neurol 328:252-262.
52. Nikulina E, Tidwell JL, Dai HN, Bregman BS, Filbin MT. 2004. The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc Natl Acad Sci USA 101:8786-8790.
53. Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, Nakamura M, Bregman BS, Koike M, Uchiyama Y, Toyama Y, Okano H. 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.
54. Pfeifer K, Vroemen M, Blesch A, Weidner N. 2004. Adult neural progenitor cells provide a permissive guiding substrate for corticospinal axon growth following spinal cord injury. Eur J Neurosci 20:1695-1704.
55. Pousset F, Fournier J, Keane PE. 1997. Expression of cytokine genes during ontogenesis of the central nervous system. Ann N Y Acad Sci 814:97-107.
56. Raff MC, Lillien LE. 1988. Differentiation of a bipotential glial progenitor cell: what controls the timing and the choice of developmental pathway? J Cell Sci Suppl 10:77-83.
57. Rao MS, Noble M, Mayer-Proschel M. 1998. A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci USA 95:3996-4001.
58. Reier PJ, Bregman BS, Wujek JR. 1986. Intraspinal transplantation of embryonic spinal cord tissue in neonatal and adult rats. J Comp Neurol 247:275-296.
59. Reynolds B, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
60. Sendtner M, Stockli KA, Thoenen H. 1992. Synthesis and localization of ciliary neurotrophic factor in the sciatic nerve of the adult rat after lesion and during regeneration. J Cell Biol 118:139-148.
61. Stankoff B, Aigrot MS, Noel F, Wattilliaux A, Zalc B, Lubetzki C. 2002. Ciliary neurotrophic factor (CNTF) enhances myelin formation: a novel role for CNTF and CNTF-related molecules. J Neurosci 22: 9221-9227.
62. Stockli KA, Lillien LE, Naher-Noe M, Breitfeld G, Hughes RA, Raff MC, Thoenen H, Sendtner M. 1991. Regional distribution, developmental changes, and cellular localization of CNTF-mRNA and protein in the rat brain. J Cell Biol 115:447-459.
63. Teng YD, Lavik EB, Qu X, Park KI, Ourednik J, Zurakowski D, Langer R, Snyder EY. 2002. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc Natl Acad Sci USA 99:3024-3029.
64. Warf BC, Fok-Seang J, Miller RH. 1991. Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord. J Neurosci 11: 2477-2488.
65. Yan J, Welsh AM, Bora SH, Snyder EY, Koliatsos VE. 2004. Differentiation and tropic/trophic effects of exogenous neural precursors in the adult spinal cord. J Comp Neurol 480:101-114.