Delayed intervention with transplants and neurotrophic factors supports recovery of forelimb function after cervical spinal cord injury in adult rats

Journal of Neurotrauma

Volumn 23, Issue 5, 2006, Pages 617-634

  Lynskey, James V ^a   Sandhu, Faheen A ^a   Dai, Hail Ning ^a   McAtee, Marietta ^a   Slotkin, Jon R ^a   MacArthur, Linda ^a   Bregman, Barbara S ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Forelimb use; Functional recovery; Neurotrophin; Spinal cord injury

Indexed keywords

NEUROTROPHIC FACTOR; NEUROTROPHIN 3; SULFAMETHOXAZOLE; TRIMETHOPRIM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CERVICAL SPINE INJURY; CONTROLLED STUDY; DESCENDING RAPHE SPINAL TRACT; FEMALE; FETAL TISSUE TRANSPLANTATION; FORELIMB; IMMUNOHISTOCHEMISTRY; LIMB MOVEMENT; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE GROWTH; NONHUMAN; PYRAMIDAL NERVE CELL; RAT; RUBROSPINAL TRACT; SKILL; THERAPY DELAY;

ANIMALS; FEMALE; FETAL TISSUE TRANSPLANTATION; FORELIMB; NERVE GROWTH FACTORS; NERVE REGENERATION; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES;

EID: 33646565625     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2006.23.617     Document Type: Article

References (87)

1. ALSTERMARK, B., and KUMMEL, H. (1986). Transneuronal labelling of neurones projecting to forelimb motoneurons in cat performing different movements. Brain Res. 376, 387-391.
2. ALSTERMARK, B., KUMMEL, H., and TANTISIRA, B. (1987a). Monosynaptic raphespinal and reticulospinal projection to forelimb motoneurones in cats. Neurosci. Lett. 74, 286-290.
3. ALSTERMARK, B., KUMMEL, H., PINTER, M., and TANTISIRA, B. (1987b). Branching and termination of C3-C4 propriospinal neurones in the cervical spinal cord of the cat. Neurosci. Lett. 74, 291-296.
4. ALSTERMARK, B., KUMMEL, H., PINTER, M., and TANTISIRA, B. (1990). Integration in descending motor pathways controlling the forelimb in the cat. 17. Axonal projection and termination of C3-C4 propriospinal neurones in the Co-Th1 segments. Exp. Brain Res. 81, 447-461.
5. ANDERSON, P., CAMPBELL, G., ZHANG, Y., and LIEBERMAN, A. (1998) Cellular and molecular correlates of regeneration of adult mammalian CNS axons into peripheral nerve grafts. Prog. Brain Res. 117, 211-232.
6. BAMBER, N., LI, H., LU, X., OUDEGA, M., AEBISCHER, P., and XU, X. (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.
7. BARBEAU, H., and ROSSIGNOL, S. (1994). Enhancement of locomotor recovery following spinal cord injury. Curr. Opin. Neurobiol. 7, 517-524.
8. BENFEY, M., and AGUAYO, A. (1982). Extensive elongation of axons from rat brain into peripheral nerve grafts. Nature 296, 150-152.
9. BLITS, B., DIJKHUIZEN, P., BOER, G., and VERHAAGEN, J. (2000). Intercostal nerve implants transduced with an adenoviral vector encoding neurotrophin-3 promote regrowth of injured rat corticospinal tract fibers and improve hindlimb function. Exp. Neurol. 164, 25-37.
10. BLITS, B., OUDEGA, M., BOER, G., BARTLETT BUNGE, M., and VERHAAGEN, J. (2003). Adeno-associatetd viral vector-mediated neurotrophin gene transfer in the injured adult rat spinal cord improves hind-limb function. Neuroscience 118, 271-281.
11. BRADBURY, E., MOON, L., POPAT, R., et al. (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640.
12. BREGMAN, B. (1987). Spinal cord transplants permit the growth of serotonergic axons across the site of neonatal spinal cord transection. Dev. Brain Res. 34, 265-279.
13. BREGMAN, B., and REIER, P. (1986). Neural tissue transplants rescue axotomized rubrospinal cells from retrograde death. J. Comp. Neurol. 244, 86-95.
14. BREGMAN, B., McATEE, M., DAI, H.N., and KUHN, P. (1997). Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp. Neurol. 148, 475-494.
15. BREGMAN, B., BROUDE, E., McATEE, M., and KELLEY, M. (1998). Transplants and neurotrophic factors prevent atrophy of mature CNS neurons after spinal cord injury. Exp. Neurol. 149, 13-27.
16. BREGMAN, B., KUNKEL-BAGDEN, E., REIER, P., DAI, H., McATEE, M., and 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.
17. BREGMAN, B., KUNKEL-BAGDEN, E., SCHNELL, L., DAI, H.N., GAO, D., and SCHWAB, M. (1995). Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378, 498-501.
18. BROSAMLE, C., HUBER, A., FIEDLER, M., SKERRA, A., and SCHWAB, M. (2000). Regeneration of lesioned corticospinal tract fibers in the adult rat induced by a recombinant, humanized IN-1 antibody fragment. J. Neurosci. 20, 8061-8068.
19. CAO, L., LIU, L., CHEN, Z.-Y., et al. (2004). Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 127, 535-549.
20. CASTRO, A. (1972a). The effects of cortical ablations on digital usage in the rat. Brain Res. 37, 173-185.
21. CASTRO, A. (1972b). Motor performance in rats. The effects of pyramidal tract section. Brain Res. 44, 313-323.
22. CHAN, C., KHODARAHMI, K., LIU, J., et al. (2005). Dose-dependent beneficial and detrimental effects of ROCK inhibitor Y27632 on axonal sprouting and functional recovery after rat spinal cord injury. Exp. Neurol. 196, 352-364.
23. COUMANS, J., LIN, T.T.-S., DAI, H.N., 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.
24. DAVID, S., and AGUAYO, A. (1981). Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214, 931-933.
25. DIENER, P., and BREGMAN, B. (1998). Fetal spinal cord transplants support the development of target reaching and coordinated postural adjustments after neonatal cervical spinal cord injury. J. Neurosci. 18, 763-778.
26. EDGERTON, V., DE LEON, R., TILLAKARATNE, N., RECKTENWALD, M., HODGSON, J., and ROY, R. (1997). Use-dependent plasticity in spinal stepping and standing. Adv. Neurol. 72, 233-247.
27. FOUAD, K., SCHNELL, L., BUNGE, M., SCHWAB, M., LIEBSCHER, T., and PEARSE, D. (2005). Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J. Neurosci. 25, 1169-1178.
28. GAVIRIA, M., PRIVAT, A., D'ARBIGNY, P., KAMENKA, J., HATON, H., and OHANNA, F. (2000). Neuroprotective effects of a novel NMDA antagonist, Gacyclidine, after experimental contusive spinal cord injury in adult rats. Brain Res. 874, 200-209.
29. GRILL, R., MURAI, K., BLESCH, A., GAGE, F., and TUSZYNSKI, M. (1997). Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 17, 5560-5572.
30. GRILLNER, S. (1985). Neurobiological bases of rhythmic motor acts in invertebrates. Science 228, 143-149.
31. GRIMPE, B., and SILVER, J. (2004). A novel DNA enzyme reduces glycosaminoglycan chains in the glial scar and allows microtransplanted dorsal root ganglia to regenerate beyond lesions in the spinal cord. J. Neurosci. 24, 1393.
32. GUEST, J., HESSE, D., SCHNELL, L., SCHWAB, M., BUNGE, M., and BUNGE, R. (1997). Influence of IN-1 antibody and acidic FGF-fibrin glue on the response of injured corticospinal tract axons to human Schwann cell grafts. J. Neurosci. Res. 50, 888-905.
33. JIN, Y., FISCHER, L, TESSLER, A., and HOULE, J. (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.
34. JUVIN, L., SIMMERS, J., and MORIN, D. (2005). Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J. Neurosci. 25, 6025-6035.
35. KEYVAN-FOULADI, N., RAISMAN, G., and LI, Y. (2003). Functional repair of the corticospinal tract by delayed transplantation of olfactory ensheathing cells in adult rats. J. Neurosci. 23, 9428-9434.
36. KUCHLER, M., FOUAD, K., WEINMANN, O., SCHWAB, M., and RAINETEAU, O. (2002). Red nucleus projections to distinct motor neuron pools in the rat spinal cord. J. Comp. Neurol. 448, 349-359.
37. KWON, B., LIU, J., OSCHIPOK, L., TEH, J., LIU, Z., and TETZLAFF, W. (2004). Rubrospinal neurons fail to respond to brain-derived neurotrophic factor applied to the spinal cord injury site 2 months after cervical axotomy. Exp. Neurol. 189, 45-57.
38. LANSNER, A., KOTALESKI, J., and GRILLNER, S. (1998). Modeling of the spinal neuronal circuitry underlying locomotion in a lower vertebrate. Ann. N.Y. Acad. Sci. 860, 239-249.
39. LIANG, F., MORET, V., WIESENDANGER, M., and ROUILLER, E. (1991). Corticomotoneuronal connections in the rat: evidence from double-labeling of motoneurons and corticospinal axon arborizations. J. Comp. Neurol. 311, 356-366.
40. LIU, Y., KIM, D., HIMES, B., 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.
41. LU, P., JONES, L., and TUSZYNSKI, M. (2005). BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury. Exp. Neurol. 191, 344-360.
42. McKAY, H., BRANNSTRON, T., WILBERG, M., and TERENGHI, G. (2002). Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat: timecourse of cell death and elimination. Exp. Brain Res. 142, 308-318.
43. McKENNA, J., and WHISHAW, I. (1999). Complete compensation in skilled reaching success with associated impairments in limb synergies, after dorsal column lesion in the rat. J. Neurosci. 19, 1885-1894.
44. McKENNA, J., PRUSKY, G., and WHISHAW, I. (2000). Cervical motoneuron topography reflects the proximodistal organization of muscles and movement of the rat forelimb: a retrograde carbocyanine dye analysis. J. Comp. Neurol. 419, 286-296.
45. McTIGUE, D., HORNER, P., STOKES, B., and GAGE, F. (1998). Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 18, 5354-5365.
46. MENEI, P., MONTERO-MENEI, C., WHITTEMORE, S., BUNGE, R., and BUNGE, M. (1998). Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. Eur. J. Neurosci. 10,607-621.
47. METZ, G., DIETZ, V., SCHWAB, M., and VAN DE MEENT, H. (1998). The effects of unilateral pyramidal tract section on hindlimb motor performance in the rat. Behav. Brain Res. 96, 37-46.
48. MUIR, G., and WHISHAW, I. (1999). Complete locomotor recovery following corticospinal tract lesions: measurement of ground forces during overground locomotion in rats. Behav. Brain Res. 103, 45-53.
49. MUIR, G., and WHISHAW, I. (2000). Red nucleus lesions impair overground locomotion in rats: a kinematic analysis. Eur. J. Neurosci. 12, 1113-1122.
50. MURRAY, M., KIM, D., LIU, Y., TOBIAS, C., TESSLER, A., and FISCHER, I. (2002). Transplantation of genetically modified cells contributes to repair and recovery from spinal injury. Brain Res. Brain Res. Rev. 40, 292-300.
51. NOVIKOVA, L., NOVIKOV, L., and KELLERTH, J.-O. (2002). Differential effects of neurotrophins on neuronal survival and axonal regeneration after spinal cord injury in adult rats. J. Comp. Neurol. 452, 255-263.
52. OUDEGA, M., and HAGG, T. (1999). Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord. Brain Res. 818, 431-438.
53. PEARSON, K. (1995). Proprioceptive regulation of locomotion. Curr. Opin. Neurobiol. 5, 786-791.
54. PENCALET, P., OHANNA, F., POULAT, P., KAMENKA, J., and PRIVAT, A. (1993). Thienylphencyclidine protection for the spinal cord of adult rats against extension of lesions secondary to a photochemical injury. J. Neurosurg. 78,603-609.
55. PIECHARKA, D., KLEIM, J., and WHISHAW, I. (2005). Limits on recovery in the corticospinal tract of the rat: partial lesions impair skilled reaching and the toppographic representation of the forelimb in motor cortex. Brain Res. Bull. 66, 203-211.
56. RAINETEAU, O., FOUAD, K., NOTH, P., THALLMAIR, M., and SCHWAB, M. (2001). Functional switch between motor tracts in the presence of the mAb IN-1 in the adult rat. Proc. Natl. Acad. Sci. USA 98, 6929-6934.
57. RAMON-CUETO, A., CORDERO, M., SANTOS-BENITO, F., and AVILA, J. (2000). Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25, 425-435.
58. REH, T., and KALIL, K. (1982). Functional role of regrowing pyramidal tract fibers. J. Comp. Neurol. 211, 276-283.
59. REINER, A., VEENMAN, C., MEDINA, L., JIAO, Y., DEL MAR, N., and HONIG, M. (2000). Pathway tracing using biotinylated dextran amines. J. Neurosci. Methods 103, 23-37.
60. RIBOTTA, M., PROVENCHER, J., FERABOLI-LOHNHER, D., ROSSIGNOL, S., PRIVAT, A., and ORSAL, D. (2000). Activation of locomotion in adult chronic spinal rats is achieved by transplantation of embryonic raphe cells reinnervating a precise lumbar level. J. Neurosci. 20, 5144-5152.
61. ROSSIGNOL, S. (2000). Locomotion and its recovery after spinal injury. Curr. Opin. Neurobiol. 10, 708-716.
62. ROSSIGNOL, S., and DUBUC, R. (1994). Spinal pattern generation. Curr. Opin. Neurobiol. 4, 894-902.
63. RUITENBERG, M., PLANT, G., HAMERS, F., et al. (2003). Ex vivo adenoviral vector-mediated neurotrophin gene transfer to olfactory ensheathing glia: effects on rubrospinal tract regeneration, lesion size, and functional recovery after implantation in the injured rat spinal cord. J. Neurosci. 23, 7045-7058.
64. SCHALLERT, T., FLEMING, S., LEASURE, J., TILLERSON, J., and BLAND, S. (2000). CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39, 777-787.
65. SCHMIDT, B., and JORDAN, L. (2000). The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res. Bull. 53, 689-710.
66. SCHNELL, L., and SCHWAB, M. (1990). Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343, 269-272.
67. SCHNELL, L., SCHNEIDER, R., KOLBECK, R., BARDE, Y., and SCHWAB, M. (1994). Neurotrophin-3 enhances sprouting of corticospinal tract during development and after spinal cord lesion. Nature 367, 170-173.
68. SCHRIMSHER, G., and REIER, P. (1992). Forelimb motor performance following cervical spinal cord contusion injury in the rat. Exp. Neurol. 117, 287-298.
69. SCHRIMSHER, G., and REIER, P. (1993). Forelimb motor performance following dorsal column, dorsolateral funiculi, or ventrolateral funiculi lesions of the cervical spinal cord in the rat. Exp. Neurol. 120, 264-276.
70. STERNBERGER, L. (1979). The unlabeled antibody (PAP) method, introduction. J. Histochem. Cytochem. 27, 1657.
71. STOKES, B., and REIER, P. (1992). Fetal grafts alter chronic behavioral outcome after contusion damage to the adult rat spinal cord. Exp. Neurol. 116, 1-12.
72. THALLMAIR, M., METZ, G., Z'GRAGGEN, W., RAINETEAU, O., KARTJE, G., and SCHWAB, M. (1998). Neurite outgrowth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat. Neurosci. 1, 124-131.
73. TOBIAS, C., SHUMSKY, J., SHIBATA, M., et al. (2003). Delayed grafting of BDNF and NT-3 producing fibroblasts into an injured spinal cord stimulates sprouting, partiallly rescues axotomized red nucleus neurons from loss and atrophy, and provides limited regeneration. Exp. Neurol. 184, 97-113.
74. TOBIAS, C., HAN, S., SHUMSKY, J., et al. (2005). Alginate encapsulated BDNF-producing fibroblast grafts permit recovery of function after spinal cord injury in the absence of immune suppression. J. Neurotrauma 22, 138-156.
75. TUSZYNSKI, M., MURAI, K., BLESCH, A., GRILL, R., and MILLER, I. (1997). Functional characterization of NGF secreting cell grafts to the acutely injured spinal cord. Cell Transplant. 6, 361-368.
76. TUSZYNSKI, M., GRILL, R., JONES, L., et al. (2003). NT-3 gene delivery elicits growth of chronically injured corticospinal axons and modestly improves functional deficits after chronic scar resection. Exp. Neurol. 181, 47-56.
77. VON MEYENBURG, J., BROSAMLE, J., METZ, G., and SCHWAB, M. (1998). Regeneration and sprouting of chronically injured corticospinal tract fibers in adult rats promoted by NT-3 and the mAB IN-1, which neutralizes myelin-associated neurite growth inhibitors. Exp. Neurol. 154, 583-594.
78. WEIDNER, N., NER, A., SALIMI, N., and TUSZYNSKI, M. (2001). Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc. Natl. Acad. Sci. USA 98, 3513-3518.
79. WHISHAW, I., and GORNY, B. (1996). Does the red nucleus provide the tonic support against which fractionated movements occur? A study on forepaw movements used in skilled reaching by the rat. Behav. Brain Res. 74, 79-90.
80. WHISHAW, I., and METZ, G. (2002). Absence of impairments or recovery mediated by the uncrossed pyramidal tract in the rat versus enduring deficits produced by the crossed pyramidal tract. Behav. Brain Res. 134, 323-336.
81. WHISHAW, I., O'CONNOR, W., and DUNNETT, S. (1986). The contribution of the motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat. Brain 109, 805-843.
82. WHISHAW, I., GORNY, B., and SARNA, J. (1998). Paw and limb use in skilled and spontaneous reaching after pyrimidal red nucleus and combined lesions in the rat: behavioral and anatomical dissociations. Behav. Brain Res. 93, 167-183.
83. WHISHAW, I., PELLIS, S., CORNY, B., KOLB, B., and TETZLAFF, W. (1993). Proximal and distal impairments in rat forelimb use in reaching follow unilateral pyramidal tract lesions. Behav. Brain Res. 56, 59-76.
84. XU, X., GUENARD, V., KLEITMAN, N., AEBISCHER, P., and BUNGE, M. (1995). A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic cord. Exp. Neurol. 134, 261-272.
85. YE, J.-H., and HOULE, J. (1997). Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143, 70-81.
86. Z'GRAGGEN, W., METZ, G., KARTJE, G., THALLMAIR, M., and SCHWAB, M. (1998). Functional recovery and enhanced corticofugal plasticity after unilateral pyramidal tract lesion and blockade of myelin-associated neurite growth inhibitors in adult rats. J. Neurosci. 18, 4744-4757.
87. ZUO, J., NEUBAUER, D., DYESS, K., FERGUSON, T., and MUIR, D. (1998). Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp. Neurol. 154, 654-662.