Spinal cord regeneration: Intrinsic properties and emerging mechanisms

Seminars in Cell and Developmental Biology

Volumn 13, Issue 5, 2002, Pages 361-368

  Chernoff, Ellen A G ^a   Sato, Kazuna ^a   Corn, Angela ^a   Karcavich, Rachel E ^a  

^a Biology SL332   (United States)

Author keywords

Amphibian regeneration; Ependymal cell; Neural stem cell; Neurogenesis; Spinal cord regeneration

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CADHERIN; EPHRIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NOTCH RECEPTOR; PROTEIN MUSASHI 1; RNA BINDING PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

AMPHIBIA; ARTICLE; EMBRYO DEVELOPMENT; GLIA; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHYLOGENY; PROTEIN LOCALIZATION; REGENERATION; SPINAL CORD INJURY; SPINAL GANGLION; STEM CELL;

AMPHIBIA; AVES; MAMMALIA; SAURURACEAE; SQUAMATA;

EID: 0036417289     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1084952102000927     Document Type: Article

References (68)

1. Steward O, Schauwecker PE, Guth L, Zhang Z, Fujika M, Inman D, Wrathall J, Kemperman G, Gage F, Saatman KE, Raghupathi R, McIntosh T (1999) Genetic approaches to neurotrauma research: Opportunities and potential pitfalls of murine models. Exp Neurol 157:19-42
2. Caroni P, Schwab ME (1988) Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1:85-96
3. Keirstead HS, Hasan SJ, Muir GD, Steeves JD (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
4. Kwon BK, Tetzlaff W (2001) Spinal cord regeneration: From gene to transplants. Spine 26(Suppl 24):S13-S22
5. Chernoff EAG (1996) Spinal cord regeneration: A phenomenon unique to urodeles? Int J Dev Biol 40:823-831
6. Clarke JDW, Ferretti P (1998) CNS regeneration in lower vertebrates, in Cellular and Molecular Basis of Regeneration (Ferretti P, Geraudie J, eds) pp. 255-269. Wiley, New York
7. Seitz A, Aglow E, Heber-Katz E (2002) Recovery from spinal cord injury: A new transection model in the C57Bl/6 mouse. J Neurosci Res 67:337-345
8. Anderson MJ, Waxman SG (1983) Caudal spinal cord of the teleost Sternarchus albifrons resembles regenerating cord. Anat Rec 205:85-92
9. Anderson MJ, Choy CY, Waxman SG (1986) Selforganization of ependyma in regenerating teleost spinal cord: Evidence from serial section reconstructions. J Embryol Exp Morphol 96:1-18
10. Yamada H, Miyake T, Kitamura T (1997) Proliferation and differentiation of ependymal cells after transection of the carp spinal cord. Zool Sci 14:331-338
11. Egar M, Singer M (1972) The role of ependyma in spinal cord regeneration in the urodele, Triturus. Exp Neurol 37:422-430
12. Singer M, Nordlander RH, Egar M (1979) Axonal guidance during embryogenesis and regeneration in the spinal cord of newt: The blueprint hypothesis of neuronal pathway patterning. J Comp Neurol 185:1-22
13. Stensaas LJ (1983) Regeneration in the spinal cord of the newt Notopthalmus (Triturus) pyrrhogaster, in Spinal Cord Reconstruction. (Kao CC, Bunge RP, Reier PJ, eds) pp. 121-149. Raven Press, New York
14. Egar M, Simpson SB, Singer M (1970) The growth and differentiation of the regenerating spinal cord of the lizard, Anolis carolinensis. J Morphol 131:131-152
15. Simpson SB Jr (1968) Morphology of the regenerated spinal cord in the lizard, Anolis carolinensis. J Comp Neurol 134:193-210
16. Duffy MT, Liebich DR, Garner LK, Hawrych A, Simpson SB Jr, Davis BM (1992) Axonal sprouting and frank regeneration in the lizard tail spinal cord: Correlation between changes in synaptic circuitry and axonal growth. J Comp Neurol 316:363-374
17. Alibardi L, Meyer-Rochow VB (1988) Ultrastructure of the neural component of the regenerating spinal cord in the tails of three species of New Zealand lizards. New Zealand J Zool 15:535-550
18. Forehand CJ, Farel PB (1982) Anatomical and behavioral recovery from the effects of spinal cord transection: Dependence on metamorphosis in anuran larvae. J Neurosci 2:654-662
19. Clarke JD, Tonge DA, Holder NH (1986) Stage-dependent restoration of sensory dorsal columns following spinal cord transection in anuran tadpoles. Proc R Soc Lond B Biol Sci 227:67-82
20. Holder N, Clarke JDW, Wilson S, Hunter K, Tonge DA (1989) Mechanisms controlling directed axon regeneration in the peripheral and central nervous systems of amphibians, in NATO Advanced Research Workshop on Recent Trends in Regeneration Research (1988: Athens, Greece) (Kiorstsis V, Koussoulakos S, Wallace H, eds) pp. 179-190. Plenum Press, New York
21. Beattie MS, Bresnahan JC, Lopate G (1990) Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs. J Neurobiol 21:1108-1122
22. Shimizu I, Oppenheim RW, O'Brien M, Shneiderman A (1990) Anatomical and functional recovery following spinal cord transection in the chick embryo. J Neurobiol 21:918-937
23. Hasan SJ, Keirstead HS, Muir GD, Steeves JD (1993) Axonal regeneration contributes to repair of injured brainstem-spinal neurons in embryonic chick. J Neurosci 13:492-507
24. Iwashita Y, Kawaguchi S, Murata M (1994) Restoration of function by replacement of spinal cord segments in the rat. Nature 367:167-170
25. Anderson MJ, Rossetto DL, Lorenz LA (1994) Neuronal differentiation in vitro from precursor cells of regenerating spinal cord of the adult teleost Apteronotus albifrons. Cell Tissue Res 278:243-248
26. O'Hara CM, Egar MW, Chernoff EAG (1992) Reorganization of the ependyma during axolotl spinal cord regeneration: Changes in intermediate filament and fibronectin expression. Dev Dyn 193:103-115
27. Zhang F, Clarke JDW, Ferretti P (2000) FGF-2 up-regulation and proliferation of neural progenitors in the regenerating amphibian spinal cord in vivo. Dev Bio 225:381-391
28. Benraiss A, Arsanto JP, Coulon J, Thouveny Y (1999) Neurogenesis during caudal spinal cord regeneration in adult newts. Dev Genes Evol 209:363-369
29. Holder N, Clarke JDW, Stephens N, Wilson SW, Orsi C, Bloomer T, Tonge DA (1991) Continuous growth of the motor system in the axolotl. J Comp Neurol 303:534-550
30. Davis BM, Duffy MT, Simpson SB Jr (1989) Bulbospinal and intraspinal connection in normal and regenerated salamander spinal cord. Exp Neurol 103:41-51
31. Clarke JDW, Alexander R, Holder N (1988) Regeneration of descending axons in the spinal cord of the axolotl. Neurosci Lett 89:1-6
32. Nordlander RH, Singer M (1978) The role of ependyma in regeneration of the spinal cord of the urodele amphibian tail. J Comp Neurol 180:349-374
33. Arsanto JP, Komorowski TE, Dupin F, Caubit X, Diano M, Geraudie J, Carlson BM, Thouveny Y (1992) Formation of the peripheral nervous system during tail regeneration in urodele amphibians: Ultrastructural and immunohistochemical studies of the origin of the cells. J Exp Zool 264:273-292
34. Chernoff EA, Henry LC, Spotts T (1998) An ependymal cell culture system for the study of spinal cord regeneration. Wound Repair Regen 6:403-412
35. Chernoff EAG, O'Hara CM, Bauerle D, Bowling M (2000) Matrix metalloproteinase production in regenerating axolotl spinal cord. Wound Repair Regen 8:282-291
36. Egar M, Singer M (1981) The role of ependyma in spinal cord regrowth, in Mechanisms of Growth Control (Becker RO, ed.) pp. 93-106. Charles Thomas Publisher, Springfield, IL
37. Chernoff EAG, Sato K, Smith RC (2001) Nrp-1 (Musashi) and Shh expression in ependymal cells of regenerating and non-regenerating Xenopus spinal cord. Mol Biol Cell 12:366a
38. Dow KE, Ethell DW, Steeves JD, Riopelle RJ (1994) The cellular correlates of spinal cord repair in the embryonic chick: Heparan sulphate and chondroitin sulphate proteoglycans. Exp Neurol 128:233-238
39. Reier PJ, Stensaas LJ, Guth L (1983) The astrocytic scar as an impediment to regeneration in the central nervous system, in Spinal Cord Reconstitution (Kao CC, Bunge RP, Reier PJ, eds) pp. 163-195. Raven Press, New York
40. Reier PJ, Houle JD (1988) The glial scar: Its bearing on axonal elongation and transplantation approaches to CNS repair. Adv Neurol 47:87-138
41. Pasterkamp RJ, Verhaagen J (2001) Emerging roles for semaphorins in neural regeneration. Brain Res Rev 35:36-54
42. Miranda JD, White LA, Marcillo AE, Willson CA, Jagid J, Whittemore SR (1999) Induction of Eph B3 after spinal cord injury. Exp Neurol 156:218-222
43. Holder N, Clarke JDW (1988) Is there a correlation between continuous neurogenesis and directed axon regeneration in the vertebrate nervous system? TINS 11:94-99
44. Butler EF, Ward MB (1967) Reconstitution of the spinal cord after ablation in adult Triturus. Dev Biol 15:464-486
45. Holder N, Clarke JDW, Kamalati T, Lane EB (1990) Heterogeneity in spinal radial glia demonstrated by intermediate filament expression and HRP labeling. J Neurocytol 19:915-928
46. Miller RH, Liuzzi FJ (1986) Regional specialization of the radial glial cells of the adult frog spinal cord. J Neurocytol 15:187-196
47. Caubit X, Riou JF, Coulon J, Arsanto JP, Benraiss A, Boucaut JC, Thouveny Y (1994) Tenascin expression in developing, adult and regenerating caudal spinal cord in the urodele amphibians. Int J Dev Biol 38(4):661-672
48. Caubit X, Arsanto JP, Figarella-Branger D, Thouveny Y (1993) Expression of polysialylated neural cell adhesion molecule (PSA-N-CAM) in developing, adult and regenerating caudal spinal cord of the urodele amphibians. Int J Dev Biol 37(2):327-336
49. Benraiss A, Caubit X, Arsanto JP, Coulon J, Nicolas S, Le Parco Y, Thouveny Y (1996) Clonal cell cultures from adult spinal cord of the amphibian urodele Pleurodeles waltl to study the identity and potentialities of cells during tail regeneration. Dev Dyn 205:135-149
50. Temple S (2001) The development of neural stem cells. Nature 414:112-117
51. Svendsen CN, Caldwell MA (2000) Neural stem cells in the developing central nervous system: Implications for cell therapy through transplantation, in Progress in Brain Research (Dunnett SB, Bjorklund A, eds) pp. 13-34. Elsevier, New York
52. O'Hara CM, Chernoff EAG (1994) Growth factor modulation of injury-reactive ependymal cell proliferation and migration. Tissue Cell 26:599-611
53. Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, Nakafuku M, Okano H (2001) The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol 21:3888-3900
54. Nakamura M, Okano H, Blendy JA, Montell C (1994) Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development. Neuron 13:67-81
55. Sakakibara S, Imai T, Hamaguchi K, Okabe M, Aruga J, Nakajima K, Yasutomi D, Nagata T, Kurihara Y, Uesugi S, Miyata T, Ogawa M, Mikoshiba K, Okano H (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176:230-242
56. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: Cell fate control and signal integration in development. Science 284:70-76
57. Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R (1999) Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J 18:2196-2207
58. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25-34
59. Morshead C, van der Kooy D (2001) A new "spin" on neural stem cells? Curr Opin Neurobiol 11:59-65
60. Momma S, Johansson CB, Frisen J (2000) Get to know your stem cells. Curr Opin Neurobiol 10:45-49
61. Bamber NI, Li H, Lu X, Oudega M, Aebischer P, Xu XM (2001) Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur J Neurosci 13:257-268
62. Altmann CR, Brivanlou AH (2001) Neural patterning in the vertebrate embryo. Int Rev Cytol 203:447-482
63. Nicolas S, Caubit X, Massacrier A, Cau P, Le Parco Y (1999) Two Nkx-3-related genes are expressed in the adult and regenerating central nervous system of the urodele Pleurodeles waltl. Dev Genet 24:319-328
64. Nicolas S, Massacrier A, Caubit X, Cau P, Le Parco Y (1996) A distal-less-like gene is induced in the regenerating central nervous system of the urodele Pleurodeles waltl. Mech Dev 56:209-220
65. Eggenschwiler JT, Espinoza E, Anderson KV (2001) Rab23 is an essential negative regulator of the mouse Sonic hedgehog pathway. Nature 412:194-198
66. Patten I, Placzek M (2000) The role of sonic hedgehog in neural tube patterning. Cell Mol Life Sci 57:1695-1708
67. Briscoe J, Ericson J (1999) The specification of neuronal identity by graded sonic hedgehog signaling. Semin Cell Dev Biol 10:353-362
68. Briscoe J, Pierani A, Jessell TM, Ericson J (2000) A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101:435-445