Regeneration and sprouting in the injured spinal cord: A decade of growth

Topics in Spinal Cord Injury Rehabilitation

Volumn 8, Issue 4, 2003, Pages 37-51

  Murray, Marion ^a   Tobias, Christopher A ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Gene therapy; Recovery of function; Regeneration; Sprouting; Transplantation

Indexed keywords

NEUROTROPHIC FACTOR; NEUROTROPHIN;

CENTRAL NERVOUS SYSTEM; CONVALESCENCE; FETAL TISSUE TRANSPLANTATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; NERVE CONDUCTION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GRAFT; NERVE SPROUTING; NERVE TRACT; NERVE TRANSPLANTATION; NONHUMAN; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SPINAL GANGLION; STEM CELL TRANSPLANTATION;

EID: 0037350506     PISSN: 10820744     EISSN: None     Source Type: Journal    
DOI: 10.1310/7UTM-HGYE-J9A0-4AB3     Document Type: Review

References (74)

1. Goldberger ME, Murray M, Tessler A. Sprouting and regeneration in the spinal cord: their roles in recovery of function after spinal injury. In: Gorio A, ed. Neuroprotection. New York: Raven Press; 1993:241-264.
2. David S, Aguayo AJ. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science. 1981;214:931-933.
3. Reier PJ, Bregman BS, Wujek JR. Intraspinal transplantation of embryonic spinal cord tissue in neonatal and adult rats. J Comp Neurol. 1986;247:275-296.
4. Polistena DC, Murray M, Goldberger ME. Plasticity of dorsal root and descending serotoninergic projections after partial deafferentation of the adult rat spinal cord. J Comp Neurol. 1990;299:349-363.
5. Murray M. Therapies to promote CNS repair. In: Ingoglia NA, Murray M, eds. Axonal Regeneration in the Central Nervous System. New York: Marcel Dekker; 2001.
6. Kim D, Schallert T, Liu Y, et al. Transplantation of genetically modified fibroblasts expressing BDNF in adult rats with a subtotal hemisection improves specific motor and sensory functions. Neurorehabil Neural Repair. 2001;15:141-150.
7. Murray M. Cellular transplants: steps toward restoration of function in spinal injured animals. Prog Brain Res. 2002.
8. Murray M, Kim D, Liu Y, Tobias C, Tessler A, Fischer I. Transplantation of genetically modified cells contributes to repair and recovery after spinal injury. Brain Res Rev. 2002;40:292-300.
9. Murray M, Fischer I, Smeraski C, Tessler A, Giszter S. Towards a definition of recovery of function. J Neurotrauma. In press.
10. Murray M, Goldberger ME. Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral lumbosacral dorsal rhizotomy in adult cats. J Neurosci. 1986;6:3205-3217.
11. McNeill DL, Carlton SM, Hulsebosch CE. Intraspinal sprouting of calcitonin gene-related peptide containing primary afferents after deafferentation in the rat. Exp Neurol. 1991;114:321-329.
12. Wang SD, Goldberger ME, Murray M. Plasticity of spinal systems after unilateral dorsal rhizotomy in the adult rat. J Comp Neurol. 1990;304:555-568.
13. Zhang B, Goldberger ME, Murray M. Proliferation of SP and 5HT containing terminals in lamina II of the rat spinal cord following dorsal rhizotomy: quantitative EM immunocytochemical studies. Exp Neurol. 1993;123:51-63.
14. Doubell TP, Mannion RJ, Woolf CJ. Intact sciatic myelinated primary afferent terminals collaterally sprout in the adult rat dorsal horn following section of a neighbouring peripheral nerve. J Comp Neurol. 1997;380:95-104.
15. Krenz NR, Weaver LC. Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience. 1998;85:443-458.
16. Wong ST, Atkinson BA, Weaver LC. Confocal microscopic analysis reveals sprouting of primary afferent fibers in rat dorsal horn after spinal cord injury. Neurosci Lett. 2000;296:65-68.
17. Tessler A, Himes BT, Artymyshyn R, Murray M, Goldberger ME. Spinal neurons mediate return of substance P following deafferentation of cat spinal cord. Brain Res. 1981;23:263-281.
18. Bernstein-Goral H, Diener PS, Bregman BS. Regenerating and sprouting axons differ in their requirements for growth after injury. Exp Neurol. 1997;148:51-72.
19. Weidner N, Ner A, Salimi N, Tuszynski MH. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. PNAS. 2001;98:3513-3518.
20. Fouad K, Pedersen V, Schwab ME, Brosamle C. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol. 2001;11:1766-1770.
21. Zeng BY, Anderson PN, Campbell G, Lieberman AR. Regenerative and other responses to injury in the retinal stump of the optic nerve in adult albino rats. J Anat. 1994;185:643-661.
22. Hill CE, Beattie MS, Bresnahan JC. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol. 2001;171:153-169.
23. Neumann S, Woolf CJ. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron. 1999;23:83-91.
24. Plant GW, Ramon-Cueto A, Bunge MB. Transplantation of Schwann cells and ensheathing glia to improve regeneration in adult spinal cord. In: Ingoglia NA, Murray M, eds. Axonal Regeneration in the Central Nervous System. New York: Marcel Dekker; 2001.
25. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB. Schwann cells 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.
26. Bregman BS, Kunkel-Bagden E, Reier PJ, Dai HN, 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. 1993;123:3-6.
27. Howland DR, Bregman BS, Tessler A, Goldberger ME. Transplants enhance locomotion in neonatal kittens whose spinal cords are transected. Exp Neurol. 1995;135:123-145.
28. Miya D, Tessler A, Giszter S, Mori F, Murray M. Fetal transplants alter the development of function after spinal cord transection in newborn rats. J Neurosci. 1997;17:4856-4872.
29. Itoh Y, Waldek RF, Tessler A, Pinter M. Regenerated dorsal root fibers form functional synapses in embryonic spinal cord transplants. J Neurophysiol. 1996;76:1236-1245.
30. Hase T, Kawaguchi S, Hayashi H, Nishio T, Mizoguchi A, Nakamura T. Spinal cord repair in neonatal rats: a correlation between axonal regeneration and functional recovery. Eur J Neurosci. 2002;15:969-974.
31. Han S, Fischer I. Neural stem cells and gene therapy: prospects for repairing the injured spinal cord. JAMA. 2000;293:2300-2301.
32. Rao MS. Multipotent and restricted precursors in the central nervous system. Anatomical Rec. 1999;137-148.
33. Chow SY, Moul J, Tobias C, et al. Characterization of multipotential stem cells from embryonic spinal cord in vitro and following intraspinal grafting. Brain Res. 2000;874:78-106.
34. Han SSW, Kang DY, Mjutaba T, Rao MS, Fischer I. Grafted lineage restricted precursors differentiate exclusively into neurons in the adult spinal cord. Exp Neurol. 2002;177.
35. McDonald JW, Liu X-Z, Qu Y, et al. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med. 1999;5:1410-1412.
36. Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002;418:41-49.
37. Akiyama Y, Radtke C, Kocsis JD. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J Neurosci. 2002;22(15):6623-6630.
38. Hofstetter CP, Schwarz EJ, Hess D, et al. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci USA. 2002;99(4):2199-2204.
39. Ramer MS, Bishop T, Dockery P, Mobarak MS, O'Leary D, Fraher JP. Neurotrophin-3 mediated regeneration and recovery of proprioception following dorsal rhizotomy. Mol Cell Neurosci. 2002;19:239-249.
40. Oudega M, Hagg T. Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord. Brain Res. 1999;818:431-438.
41. Zhang Y, Dijkhuizen PA, Anderson PN, Lieberman AR. NT3 delivered by adenovirus vector induces injured dorsal root axons to regenerate into the spinal cord of adult rats. J Neurosci Res. 1998;54:554-562.
42. Romero MI, Rangappa N, Garry MG, Smith GM. Functional regeneration of chronically injured sensory afferents into adult spinal cord after neurotrophin gene therapy. J Neurosci. 2001;21:8408-8416.
43. Coumans JV, Lin TT-S, Dai HN, et al. Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J Neurosci. 2001;21:9334-9344.
44. Grill RJ, Blesch A, Tuszinski MH. Robust growth of chronically injured spinal cord axons induced by grafts of genetically modified NGF secreting cells. Exp Neurol. 1997;148:444-452.
45. Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci. 1997;17:5560-5572.
46. Liu Y, Kim D, Himes BT, et al. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons. J Neurosci. 1999;19:4370-4387.
47. Tobias CA, Dhoot NO, Wheatley MA, Tessler A, Murray M, Fischer I. Grafting of encapsulated BDNF-producing fibroblasts into the injured spinal cord without immune suppression in adult rats. J Neurotrauma. 2001;18:287-301.
48. Tobias CA, Shumsky JS, Shibata M, et al. Delayed grafting of BDNF and NT-3 producing fibroblasts into the injured spinal cord stimulates sprouting, partially rescues axotomized red nucleus neurons from loss and atrophy and provides limited regeneration. 2002. Manuscript in preparation.
49. Tobias CA, Han SW, Shumsky JS, et al. Grafting of alginate encapsulated BDNF-producing fibroblasts permits recovery of function after spinal cord injury in the absence of immune suppression. Submitted for publication.
50. Fernandes KJL, Tetzlaff W. Gene expression in axotomized neurons: identifying the intrinsic determinants of axonal growth. In: Ingoglia NA, Murray M, eds. Axonal Regeneration in the Central Nervous System. New York: Marcel Dekker; 2001.
51. Plunet W, Kwon BK, Tetzlaff W. Promoting axonal regeneration in the central nervous system by enhancing the cell body response to axotomy. J Neurosci Res. 2002;68:1-6.
52. Bradbury EJ, Moon LDF, Popat RJ, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 2002;416:636-640.
53. Bomze HM, Bulsara KRE, Iskandar J, Caroni P, Pate Skene JH. Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nat Neurosci. 2001;4:38-44.
54. Gold BG. Neuroimunophilin ligands: evaluation of their therapeutic potential for the treatment of neurological disorders. Exp Opin Invest Drugs. 2000;9:2331-2341.
55. Madsen JR, MacDonald P, Irwin N, et al. Tacrolimus (FK506) increases neuronal expression of GAP-43 and improves functional recovery after spinal cord injury in rats. Exp Neurol. 1998;154:673-683.
56. Sugawara T, Itoh Y, Mizoi K. Immunosuppressants promote adult dorsal root regeneration into the spinal cord. NeuroReport. 1999;10:3949-3953.
57. Bavetta S, Hamlyn PJ, Burnstock G, Lieberman AR, Anderson PN. The effects of FK506 on dorsal columns axons following spinal cord injury in adult rats: neuroprotection and local regeneration. Exp Neurol. 1999;158:382-393.
58. Wang M-S, Gold BG. FK506 increases the regeneration of spinal cord axons in a predegenerated peripheral nerve autograft. J Spinal Cord Med. 1999;22:287-296.
59. Benowitz LI, Goldberg DE, Madsen JR, Soni D, Irwin N. Inosine stimulates extensive axon collateral growth in the rat corticospinal tract after injury. Proc Natl Acad Sci USA. 2001;96:13486-13490.
60. Chen P, Goldberg DE, Kolb B, Lanser M, Benowitz LI. Inosine induces axonal rewiring and improves behavioral outcome after stroke. PNAS. 2002;99:9031-9036.
61. Liu B, Strittmatter SM. Semaphorin-mediated axonal guidance via Rho-related G proteins. Curr Opin Cell Biol. 2001;13:619-626.
62. Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, McKerracher L. Rho signaling pathway targeted to promote spinal cord repair. J Neurosci. 2002;22:6570-6577.
63. Neumann S, Badke F, Tessier-Lavigne M, Basbaum AI. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron. 2002;34:885-893.
64. Cai D, Shen Y, DeBellard M, Tang S, Filbin MT. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanisms. Neuron. 1999;22:89-101.
65. Huang DW, McKerracher L, Braun PE, David S. A therapeutic vaccine approach to stimulate axon regeneration in the adult mammalian spinal cord. Neuron. 1999;24:639-647.
66. Schwab ME. Inhibition of axonal growth by the myelin-associated inhbitory proteins NI-35/250/Nogo A. In: Ingoglia NA, Murray M, eds. Axonal Regeneration in the Central Nervous System. New York: Marcel Dekker; 2001:411-424.
67. GrandPre T, Li S, Strittmatter SM. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature. 2002;417:547-551.
68. Wang KC, Koprivica V, Kim JA, et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature. 2002;417:941-944.
69. Bareyre FM, Haudenschild B, Schwab ME. Long-lasting sprouting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord. J Neurosci. 2002;22:7097-7110.
70. Raineteau O, Fouad K, Noth P, Thallmair M, Schwab ME. Functional switch between motor tracts in the presence of the mAB IN-1 in the adult rat. PNAS. 2001;98:6929-6934.
71. Liu BO, Fournier A, GrandPre T, Strittmatter SM. Myelin associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science. 2002;297:1190-1193.
72. Basso DM, Beattie M, Bresnahan J. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma.1995;12(1):1-21.
73. Houle J, Tessler A. Repair of chronic spinal cord injury. Exp Neurol. In press.
74. Tobias CA, Shumsky JS, Tumolo M, et al. Delayed transplantation of fibroblasts genetically modified to secrete BDNF and NT-3 into a spinal cord injury site is associated with limited recovery of function. Manuscript in preparation.