Nerve growth factor delivery by gene transfer induces differential outgrowth of sensory, motor, and noradrenergic neurites after adult spinal cord injury

Experimental Neurology

Volumn 137, Issue 1, 1996, Pages 157-173

  Tuszynski, Mark H ^a,b   Gabriel, Katie ^a   Gage, Fred H ^c   Suhr, Steve ^c   Meyer, Scott ^a   Rosetti, Angela ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FIBROBLAST; GENE TRANSFER; MOTONEURON; NERVE GRAFT; NERVE GROWTH; NONHUMAN; NORADRENERGIC NERVE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; SENSORY NERVE; SPINAL CORD INJURY; ULTRASTRUCTURE;

EID: 0030054303     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1996.0016     Document Type: Article

References (108)

1. 125I-neurotrophin-3 binding to the mammalian brain. J. Neurosci. 13:733-743.
2. ARAKAWA, Y., M. SENDTNER, AND H. THOENEN. 1990. Survival effect of ciliary neurotrophic factor on chick embryonic motoneurons in culture: Comparison with other neurotrophic factors and cytokines. J. Neurosci. 10: 3507-3515.
3. ARENAS, E., AND H. PERSSON. 1994. Neurotrophin-3 prevents the death of adult central noradrenergic neurons in vivo. Nature 367: 368-371.
4. BARDE, Y. A. 1988. What, if anything, is a neurotrophic factor? Trends Neurosci. 11(8): 343-345.
5. BARRETT, G. L., AND P. F. BARTLETT. 1994. The p75 nerve growth factor receptor mediates survival or death depending on the stage of sensory neuron development. Proc. Natl. Acad. Sci. USA 91: 6501-6505.
6. BLOTTNER, D., W. BRUGGEMANN, AND K. UNSICKER. 1989. Ciliary neurotrophic factor supports target-deprived preganglionic sympathetic spinal cord neurons. Neurosci. Lett. 105: 316-320.
7. BREGMAN, B. S., E. KUNKEL-BAGDEN, P. J. REIER, H. N. DAI, M. MCATEE, AND D. GAO. 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.
8. BUNGE, M. B., R. P. BUNGE, N. KLEITMAN, AND A. C. DEAN. 1989. Role of peripheral nerve extracellular matrix in Schwann cell function and in neurite regeneration. Dev. Neurosci. 11: 348-360.
9. CARROLL, P., M. SENDTNER, M. MEYER, AND H. THOENEN. 1993. Rat ciliary neurotrophic factor (CNTF): Gene structure and regulation of mRNAlevels in glial cell cultures. Glia 9: 176-187.
10. CHEN, K., AND F. H. GAGE. 1995. Somatic gene transfer of NGF to the aged brain: Behavioral and morphological amelioration. J. Neurosci. 15: 2819-2825.
11. CHEN, Y.-S., L. T. WANG-BENNETT, AND N. J. COKER. 1989. Facial nerve regeneration in the silicone chamber: The influence of nerve growth factor. Exp. Neurol. 103: 52-60.
12. CLARK, F. M., AND H. K. PROUDFIT. 1993. The projections of noradrenergic neurons in the A5 catecholamine cell group to the spinal cord in the rat: Anatomical evidence that A5 neurons modulate nociception. Brain Res. 616: 200-210.
13. CLATTERBUCK, R. E., D. L. PRICE, AND V. E. KOLIATSOS. 1993. Ciliary neurotrophic factor prevents retrograde neuronal death in the adult central nervous system. Proc. Natl. Acad. Sci. USA 90: 2222-2226.
14. CLOWRY, G., K. SIERADZAN, AND G. VRBOVA. 1991. Transplants of embryonic motoneurones to adult spinal cord: Survival and innervation abilities. Trends. Neurosci. 14: 355-357.
15. COTMAN, C., CUMMINGS, B. J., AND PIKE, C. 1993. Molecular cascades in adaptive versus pathological plasticity. Pages 217-240 in A. Gorio, Ed., Neuroregeneration. Raven Press, New York.
16. DAVID, S., AND A. AGUAYO. 1981. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214: 931-933.
17. DOBREA, G. M., J. R. UNNERSTALL, AND M. S. RAO. 1992. The expression of CNTF message and immunoreactivity in the central and peripheral nervous system of the rat. Brain Res. Dev. Brain Res. 66: 209-219.
18. DUNCAN, I. D., J. P. HAMMANG, AND S. A. GILMORE. 1988. Schwann cell myelination of the myelin deficient spinal cord following X-irradiation. Glia 1:233-239.
19. EMERICH, D. F., J. P. HAMMANG, E. E. BAETGE, AND S. R. WINN. 1994. Implantation of polymer-encapsulated human nerve growth factor-secreting fibroblasts attenuates the behavioral and neuropathological consequences of quinolinic acid injections into rodent striatum. Exp. Neurol. 130: 141-150.
20. FAWCETT, J. W., AND R. J. KEYNES. 1990. Peripheral nerve regeneration. Annu. Rev. Neurosci. 13: 43-60.
21. FERNANDEZ, E., R. PALLINI, L. LAURETTI, D. MERCANTI, A. SERRA, AND P. CALISSANO. 1993. Spinal cord transection in adult rats: Effects of local infusion of nerve growth factor on the corticospinal axons. Neurosurgery 33: 889-893.
22. FISCHER, W., K. WICTORIN, A. BJORKLUND, L. R. WILLIAMS, S. VARON, AND F. H. GAGE. 1987. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329: 65-68.
23. FRANKLIN, R. J., AND W F. BLAKEMORE. 1990. The peripheral nervous system-central nervous system regeneration dichotomy: A role for glial cell transplantation. J. Cell Sci. 95: 185-190.
24. FRIEDMAN, B., D. KLEINFELD, N. Y. IP, V M. VERGE, R. MOULTON, P. BOLAND, E. ZLOTCHENKO, R. M. LINDSAY, AND L. LIU. 1995. BDNF and NT-4/5 exert neurotrophic influences on injured adult spinal motor neurons. J. Neurosci. 15: 1044-1056.
25. FRIEDMAN, B., S. S. SCHERER, J. S. RUDGE, M. HELGREN, D. MORRISEY, J. MCCLAIN, D. Y WANG, S. J. WIEGAND, M. E. FURTH, R. M. LINDSAY, ET AL. 1992. Regulation of ciliary neurotrophic factor expression in myelin-related Schwann cells in vivo. Neuron 9: 295-305.
26. FRIM, D. M., U. WULLNER, M. F. BEAL, AND O. ISACSON. 1994. Implanted NGF-producing fibroblasts induce catalase and modify ATP levels but do not affect glutamate receptor binding or NMDA receptor expression in the rat striatum. Exp. Neurol. 128: 172-180.
27. GAGE, F. H., P. BATCHELOR, K. S. CHEN, D. CHIN, G. A. HIGGINS, S. KOH, S. DEPUTY, M. B. ROSENBERG, W FISCHER, AND A. BJORKLUND. 1989. NGF receptor reexpression and NGF mediated cholinergic neuronal hypertrophy in the damaged adult neostriatum. Neuron 2: 1177-1184.
28. GOMEZ-PINILLA, F., J. W. LEE, AND C. W. COTMAN. 1992. Basic fibroblast growth factor in adult rat brain: Cell distribution and response to entorhinal lesion and fimbria-fornix transection. J. Neurosci. 12: 345-355.
29. HAGG, T., H. L. VAHLSING, M. MANTHROPE, AND S. VARON. 1990. Septohippocampal cholinergic axonal regeneration through peripheral nerve bridges: Quantification and temporal development. Exp. Neurol. 109: 153-163.
30. HALLBOOK, F., C. F. IBANEZ, AND H. PERSSON. 1991. Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6: 845-858.
31. HARMANN, P. A., K. CHUNG, R. P. BRINER, K. N. WESTLUND, AND S. M. CARLTON. 1988. Calcitonin gene-related peptide (CGRP) in the human spinal cord: A light and electron microscopic analysis. J. Comp. Neurol. 269: 371-380.
32. HEFTI, F. 1986. Nerve growth factor (NGF) promotes survival of septal cholinergic neurons after fimbrial transection. J. Neurosci. 6: 2155-2162.
33. HENDERSEN, C. E., H. S. PHILLIPS, R. A. POLLOCK, A. M. DAVIES, C. LEMEULLE, M. ARMANINI, L. C. SIMPSON, B. MOFFET, R. A. VANDLEN, V E. KOLIATSOS, AND A. ROSENTHAL. 1994. GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266: 1062-1064.
34. HENDERSON, J. T., N. A. SENIUK, AND J. C. RODER. 1994. Localization of CNTF immunoreactivity to neurons and astroglia in the CNS. Brain Res. Mol. Brain Res. 22: 151-165.
35. HIMES, B. T., M. E. GOLDBERGER, AND A. TESSLER. 1994. Grafts of fetal central nervous system tissue rescue axotomized Clarke's nucleus neurons in adult and neonatal operates. J. Comp. Neurol. 339: 117-131.
36. ISAACSON, L. G., B. N. SAFFRAN, AND K. A. CRUTCHER. 1990. Intracerebral NGF infusion induces hyperinnervation of cerebral blood vessels. Neurobiol. Aging 11:51-55.
37. ITOH, Y., AND A. TESSLER 1990. Regeneration of adult dorsal root axons into transplants of fetal spinal cord and brain: A comparison of growth and synapse formation in appropriate and inappropriate targets. J. Comp. Neurol. 302: 272-293.
38. JAKEMAN, L. B., P. J. REIER, B. S. BREGMAN, E. B. WADE, M. DAILEY, R. J. KASTNER, B. T. HIMES, AND A. TESSLER. 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.
39. KAWAJA, M., M. ROSENBERG, K. YOSHIDA, AND F. H. GAGE. 1992. Somatic gene transfer of nerve growth factor promotes the survival of axotomized septal neurons and the regeneration of their axons in adult rats. J. Neurosci. 12: 2849-2864.
40. KLEIN, R. 1994. Role of neurotrophins in mouse neuronal development. FASEB J. 8: 738-744.
41. KOLB, B., AND I. Q. WHISHAW. 1989. Plasticity in the neocortex: Mechanisms underlying recovery from early brain damage. Prog. Neurobiol 32: 235-276.
42. KOLIATSOS, V. E., R. E. CLATTERBUCK, J. W WINSLOW, M. H. CAYOUETTE, AND D. L. PRICE. 1993. Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10: 359-367.
43. KOLIATSOS, V. E., T. O. CRAWFORD, AND D. L. PRICE. 1991. Axotomy induces nerve growth factor receptor immunoreactivity in spinal cord motoneurons. Brain Res. 549: 297-304.
44. KOLIATSOS, V. E., H. J. NAUTA, R. E. CLATTERBUCK, D. M. HOLTZMAN, W. C. MOBLEY, AND D. L. PRICE. 1990. Mouse nerve growth factor prevents degeneration of axotomized basal forebrain cholinergic neurons in the monkey. J. Neurosci. 10: 3801-3813.
45. KORDOWER, J. H., AND M. S. FIANDACA. 1990. Response of the monkey cholinergic septohippocampal system to fornix transection: A histochemical and cytochemical analysis. J. Comp. Neurol. 298: 443-457.
46. KORSCHING, S. 1993. The neurotrophic factor concept: A reexamination. J. Neurosci. 13: 2739-2748.
47. KWIAT, G. C., AND A. I. BASBAUM. 1990. Organization of tyrosine hydroxylase-and serotonin-immunoreactive brainstem neurons with axon collaterals to the periqueductal gray and the spinal cord in the rat. Brain Res. 528: 83-94.
48. KWIAT, G. C., AND A. I. BASBAUM. 1992. The origin of brainstem noradrenergic and serotonergic projections to the spinal cord dorsal horn in the rat. Somatosens. Motor Res. 9: 157-173.
49. LEVI-MONTALCINI, R. 1987. The nerve growth factor 35 years later. Science 237: 1154-1162.
50. LI, Y., AND G. RAISMAN. 1993. Long axon growth from embryonic neurons transplanted into myelinated tracts of the adult rat spinal cord. Brain Res. 629: 115-127.
51. LIN, L. F., D. H. DOHERTY, J. D. LILE, S. BEKTESH, AND F. COLLINS. 1993. GDNF: A glial cell-line derived neurotrophic factor for midbrain dopaminergic neurons. Science 260: 1130-1132.
52. LONGO, F. M., E. G. HAYMAN, G. E. DAVIS, E. RUOSLAHTI, E. ENGVALL, M. MANTHORPE, AND S. VARON. 1984. Neurite-promoting factors and extracellular matrix components accumulating in vivo within nerve regeneration chambers. Brain Res. 309: 105-117.
53. MAGAL, E., P. BURNHAM, AND S. VARON. 1991. Effects of ciliary neuronotrophic factor on rat spinal cord neurons in vitro: Survival and expression of choline acetyltransferase and low-affinity nerve growth factor receptors. Brain Res. 63: 141-150.
54. MAISONPIERRE, P. C., L. BELLUSCIO, S. SQUINTO, N. Y. IP, M. E. FURTH, R. M. LINDSAY, AND G. D. YANCOPOULOS. 1990. Neurotrophin-3: A neurotrophic factor related to NGF and BDNF. Science 247: 1446-1451.
55. MANSOUR-ROBAEY, S., D. B. CLARKE, Y. C. WANG, G. M. BRAY, AND A. J. AGUAYO. 1994. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc. Natl. Acad. Sci. USA 91: 1632-1636.
56. MARCHAND, R., AND S. WOERLY. 1990. Transected spinal cords grafted with in situ self-assembled collage matrices. Neuroscience 36: 45-60.
57. MASU, Y., E. WOLF, B. HOLTMANN, M. SENDTNER, G. BREM, AND H. THOENEN. 1993. Disruption of the CNTF gene results in motor neuron degeneration. Nature 365: 27-32.
58. MCKERRACHER, L., S. DAVID, D. L. JACKSON, V. KOTTIS, R. J. DUNN, AND P. E. BRAUN. 1994. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13: 805-811.
59. MCMAHON, S. B., M. P. ARMANINI, L. H. LING, AND H. S. PHILLIPS. 1994. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12: 1161-1171.
60. MCMANAMAN, J. L., L. J. HAVERKAMP, AND R. W OPPENHEIM. 1991. Skeletal muscle proteins rescue motor neurons from cell death in vivo. Adv. Neurol. 56: 81-88.
61. MCMANAMAN, J. L., R. W OPPENHEIM, D. PREVETTE, AND D. MARCHETTI. 1990. Rescue of motoneurons from cell death by a purified skeletal muscle polypeptide: Effects of the ChAT development factor, CDF. Neuron 4: 891-898.
62. MCNEILL, D. L., S. CARLTON, AND C. E. HULSEBOSCH. 1991. Intraspinal sprouting of calcitonin gene-related peptide containing primary afferents after deafferentation in the rat. Exp. Neurol. 114: 321-329.
63. MEYER, M., I. MATSUOKA, C. WETMORE, L. OLSON, AND H. THOENEN. 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.
64. MILLER, A. D., AND C. BUTTIMORE. 1986. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol. Cell Biol. 6: 2895-2902.
65. MITSUMOTO, H., K. IKEDA, B. KLINKOSZ, J. CEDARBAUM, V. WONG, AND R. LINDSAY. 1994. Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF. Science 265: 1107-1110.
66. MIYATA, Y., Y. KASHIHARA, S. HOMMA, AND M. KUNO. 1986. Effects of nerve growth factor on the survival and synaptic function of Ia sensory neurons axotomized in neonatal rats. J. Neurosci. 6: 2012-2018.
67. PAXINOS, G. 1985. The Rat Nervous System. Academic Press, Sydney.
68. PIEHL, F., J. FRISEN, M. RISLING, T. HOKFELT, AND S. CULLHEIM. 1994. Increased trkB mRNA expression by axotomized motoneurones. NeuroReport 5: 697-700.
69. RABIZADEH, S., J. OH, L. T. ZHONG, J. YANG, C. M. BITLER, L. L. BUTCHER, AND D. E. BREDESEN. 1993. Induction of apoptosis by the low-affinity NGF receptor. Science 261: 345-348.
70. RAISMAN, G. 1978. What hope for repair of the brain? Ann. Neurol. 3: 101-106.
71. RAIVICH, G., A. ZIMMERMAN, ANDA. SUTTER. 1985. The spatial and temporal pattern of β NGF receptor expression in the developing chick embryo. EMBO J. 4: 637-644.
72. RAMON Y CAJAL, S. 1928. Degeneration and Regeneration of the Nervous System. Oxford Univ. Press, London.
73. REIER, P. J., D. K. ANDERSON, F. J. THOMPSON, AND B. T. STOKES. 1992. Neural tissue transplantation and CNS trauma: Anatomical and functional repair of the injured spinal cord. J. Neurotrauma 9(Suppl 1): S223-S248.
74. RENDE, M., T. HAGG, M. MANTHORPE, AND S. VARON. 1992. Nerve growth factor immunoreactivity in neurons of the normal adult rat spinal cord and its modulation after peripheral nerve lesions. J. Comp. Neurol. 319: 285-298.
75. RICHARDSON, P. M., U. M. MCGUINESS, AND A. J. AGUAYO. 1980. Axons from CNS neurons regenerate into PNS grafts. Nature 284: 264-265.
76. RICHARDSON, P. M., V. M. K. VERGE ISSA, AND R. J. RIOPELLE. 1986. Distribution of neuronal receptors for nerve growth factor in the rat. J. Neurosci. 6: 2312-2321.
77. ROSENBERG, M. B., T. FRIEDMANN, R. C. ROBERTSON, M. TUSZYNSKI, J. A. WOLFF, X. O. BREAKEFIELD, AND F. H. GAGE. 1988. Grafting genetically modified cells to the damaged brain: Restorative effects of NGF expression. Science 242: 1575-1578.
78. SALONEN, V., J. PELTONEN, M. ROYTTA, AND J. VITRANEN. 1987. Laminin in traumatized perpheral nerve: Basement membrane changes during degeneration and regeneration. J. Neurocytol. 16: 713-720.
79. SCHINSTINE, M., AND C. J. CORNBROOKS. 1990. Axotomy enhances the outgrowth of neurites from embryonic rat septal-basal forebrain neurons on a laminin substratum. Exp. Neurol. 108: 10-22.
80. SCHNELL, L., R. SCHNEIDER, R. KOLBECK, Y. A. BARDE, AND M. E. SCHWAB. 1994. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion [see comments]. Nature 367: 170-173.
81. SCHUMACHER, J. M., M. P. SHORT, B. T. HYMAN, X. O. BREAKEFIELD, AND O. ISACSON. 1991. Intracerebral implantation of nerve growth factor-producing fibroblasts protects striatum against neurotoxic levels of excitatory amino acids. Neuroscience 45: 561-570.
82. SCHWAB, M. E. 1990. Myelin-associated inhibitors of neurite growth and regeneration in the CNS. Trends Neurosci. 13: 452-456.
83. SENDTNER, M., B. HOLTMANN, R. KOLBECK, H. THOENEN, AND Y.-A. BARDE. 1992. Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 360: 757-759.
84. SENDTNER, M., G. W. KREUTZBERG, AND H. THOENEN. 1990. Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 345: 440.
85. SENDTNER, M., H. SCHMALBRUCH, K. A. STOCKLI, P. CARROL, G. W. KREUTZBERG, AND H. THOENEN. 1992. Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant neuronopathy. Nature 358: 502-504.
86. SKOFITSCH, G., AND D. M. JACOBWITZ. 1985. Quantitative distribution of calcitonin gene-related peptide in the rat central nervous system. Peptides 6: 1069-1073.
87. SOPPET, D., E. ESCANDON, J. MARAGOS, D. S. MIDDLEMAS, S. W. REID, J. BLAIR, L. E. BURTON, B. R. STANTON, D. R. KAPLAN, T. HUNTER, K. NIKOLICS, AND L. F. PARADA. 1991. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trk B tyrosine kinase receptor. Cell 65: 895-903.
88. SQUINTO, S. P., S. T. STITT, T. H. ALDRICH, S. DAVIS, S. M. BIANCO, C. RADZIEJEWSKI, D. J. GLASS, P. MASIAKOWSKI, M. E. FURTH, D. M. VALENZUELA, D. S. DISTEFANO, AND G. D. YANCOPOULOS. 1991. Trk B encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65: 885-893.
89. STOKES, B. T., AND P. J. REIER. 1992. Fetal grafts alter chronic behavioral outcome after contusion damage to the adult rat spinal cord. Exp. Neurol. 116: 1-12.
90. TANIUCHI, M., J. B. SCHWEIZER, AND E. M. JOHNSON. 1986. Nerve growth factor receptor molecules in rat brain. Proc. Natl. Acad. Sci. USA 83: 1950-1954.
91. TESSLER, A. 1991. Intraspinal transplants. Ann. Neurol. 29: 115-123.
92. THOMAS, P. K. 1989. Focal nerve injury: Guidance factors during axonal regeneration. Muscle Nerve 12: 796-802.
93. TUSZYNSKI, M. H., G. BUZSAKI, AND F. H. GAGE. 1990. NGF infusions combined with fetal hippocampal grafts enhance reconstruction of the lesioned septo-hippocampal projection. Neuroscience 36: 33-14.
94. TUSZYNSKI, M. H., AND F. H. GAGE. 1995. Maintaining the neuronal phenotype after injury in the adult CNS: Neurotrophic factors, axonal growth substrates and gene therapy. Mol. Neurobiol. 10: 151-167.
95. TUSZYNSKI, M. H., AND F. H. GAGE. 1995. Bridging grafts and transient NGF infusions promote long-term CNS neuronal rescue and partial functional recovery. Proc. Natl. Acad. Sci. USA 92: 4621-1625.
96. TUSZYNSKI, M. H., S. MEYER, Y NAKAHARA, K. GABRIEL, K. MURAI, J. RAY, M.-C. SENUT, AND F. H. GAGE. 1994. Fibroblasts and Schwann cells genetically modified to produce neurotrophic factors induce robust neuritic growth after transplantation to the spinal cord. Soc. Neurosci. Abstr. 20: 10.
97. TUSZYNSKI, M. H., D. A. PETERSON, J. RAY, A. BAIRD, Y. NAKAHARA, AND F. H. GAGE. 1994. Fibroblasts genetically modified to produce nerve growth factor induce robust neuritic ingrowth after grafting to the spinal cord. Exp. Neurol. 126: 1-14.
98. TUSZYNSKI, M. H., M. C. SENUT, J. RAY, H.-S. U, AND F. H. GAGE. 1994. Somatic gene transfer to the adult primate CNS: In vitro and in vivo characterization of cells genetically modified to secrete nerve growth factor. Neurobiol. Dis. 1: 67-78.
99. TUSZYNSKI, M. H., H. S. U, D. G. AMARAL, AND F. H. GAGE. 1990. Nerve growth factor infusion in primate brain reduces lesion-induced cholinergic neuronal degeneration. J. Neurosci. 10: 3604-3614.
100. WANG, S. D., M. E. GOLDBERGER, AND M. MURRAY. 1991. Plasticity of spinal systems after unilateral lumbosacral dorsal rhizotomy in the adult rat. J. Comp. Neurol. 304: 555-568.
101. WAYNE, D. B., AND M. B. HEATON. 1988. Retrograde transport of NGF by early chick embryo spinal cord motoneurons. Dev. Biol. 127: 220-223.
102. WESKAMP, G., AND U. OTTEN. 1987. An enzyme-linked immunoassay for nerve growth factor (NGF): A tool for studying regulatory mechanisms involved in NGF production in brain and in peripheral tissues. J. Neurochem. 48: 1779-1786.
103. WEWETZER, K., J. R. MACDONALD, F. COLLINS, AND K. UNSICKER. 1990. CNTF rescues motoneurons from ontogenetic cell death in vivo, but not in vitro. NeuroReport 1: 203-206.
104. WONG, V., R. ARRIEGA, N. Y. IP, AND R. M. LINDSAY. 1993. The neurotrophins BDNF, NT-3 and NT-4/5, but not NGF, upregulate the cholinergic neuronal phenotype of developing motor neurons. Eur. J. Neurosci. 5: 466-474.
105. YAKOVLEFF, A., A. ROBY-BRAMI, B. GUEZARD, H. MANSOUR, B. BUSSEL, AND A. PRIVAT. 1989. Locomotion in rats transplanted with noradrenergic neurons. Brain Res. Bull. 22: 115-121.
106. YAN, O., K. GRAY, J. SUN, C. FARRELL, D. PATEL, R. ROSENFELD, J. TALVENHEIMO, G. PIERCE, AND J. MILLER 1991. Retrograde transport of BDNF and NT-3 by spinal motoneurons. Soc. Neurosci. Abstr. 17: 1119.
107. YAN, Q., W. D. SNIDER, J. J. PINZONE, AND E. M. JOHNSON. 1988. Retrograde transport of nerve growth factor (NGF) in motoneurons of developing rats: Assessment of potential neurotrophic effects. Neuron 1: 335-343.
108. YIN, Q. W., J. JOHNSON, D. PREVETTE, AND R. W. OPPENHEIM. 1994. Cell death of spinal motoneurons in the chick embryo following deafferentation: Rescue effects of tissue extracts, soluble proteins, and neurotrophic agents. J. Neurosci. 14: 7629-7640.