Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord

Brain Research

Volumn 818, Issue 2, 1999, Pages 431-438

  Oudega, Martin ^a   Hagg, Theo ^b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Axotomy; Brain derived neurotrophic factor; Conditioning lesion; Nerve growth factor; Neurotrophin 3; Peripheral nerve graft

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIN 3;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NERVE GRAFT; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE; SPINAL CORD; THORACIC SPINAL CORD;

ANIMALS; AXONS; AXOTOMY; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; GANGLIA, SENSORY; NERVE GROWTH FACTORS; NERVE REGENERATION; NEUROTROPHIN 3; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 0033550707     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(98)01314-6     Document Type: Article

References (43)

1. Anderson K.D., Alderson R.F., Altar C.A., DiStefano P.S., Corcoran T.L., Lindsay R.M., Wiegand S.J. Differential distribution of exogenous BDNF, NGF, and NT-3 in the brain corresponds to the relative abundance and distribution of high-affinity and low-affinity neurotrophin receptors. J. Comp. Neurol. 357:1995;296-317.
2. Anton E.S., Weskamp G., Reichardt L.F., Matthew W.D. Nerve growth factor and its low affinity receptor promote Schwann cell migration. Proc. Natl. Acad. Sci. U.S.A. 91:1994;2795-2799.
3. Bothwell M. Functional interactions of neurotrophins and neurotrophin receptors. Annu. Rev. Neurosci. 18:1995;223-253.
4. Bregman B.S., Kunkel-Bagden E., Schnell L., Dai H.N., Gao D., Schwab M.E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature. 378:1995;498-501.
5. Cadelli D., Schwab M.E. Regeneration of lesioned septo-hippocampal acetylcholinesterase-positive axons is improved by antibodies against the myelin-associated neurite growth inhibitors NI-35/250. Eur. J. Neurosci. 3:1991;825-832.
6. Caroni P., Schwab M.E. Central nervous system regeneration: oligodendrocytes and myelin as non-permissive substrates for neurite growth. Prog. Brain. Res. 78:1988;363-370.
7. Casaccia-Bonnefil P., Carter B.D., Dobrowsky R.T., Chao M.V. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature. 383:1996;716-719.
8. Chao M.V., Hempstead B.L. p75 and Trk: a two-receptor system. Trends Neurosci. 18:1995;321-326.
9. Ciriaco E., Dall'Aglio C., Hannestad J., Huerta J.J., Laura R., Germana G., Vega J.A. Localization of Trk neurotrophin receptor-like proteins in avian primary lymphoid organs (thymus and bursa of Fabricius). J. Neuroimmunol. 69:1996;73-83.
10. Clary D.O., Reichardt L.F. An alternatively spliced form of the nerve growth factor receptor TrkA confers an enhanced response to neurotrophin 3. Proc. Natl. Acad. Sci. U.S.A. 91:1994;11133-11137.
11. Cohen R.I., Marmur R., Norton W.T., Mehler M.F., Kessler J.A. Nerve growth factor and neurotrophin-3 differentially regulate the proliferation and survival of developing rat brain oligodendrocytes. J. Neurosci. 16:1996;6433-6442.
12. Davies S.J.A., Fitch M.T., Memberg S.P., Hall A.K., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature. 390:1997;680-683.
13. Ehrhard P.B., Ganter U., Stalder A., Bauer J., Otten U. Expression of functional Trk protooncogene in human monocytes. Proc. Natl. Acad. Sci. U.S.A. 90:1993;5423-5427.
14. Fernandez E., Pallini R., Mercanti D. Effects of topically administrated nerve growth factor on axonal regeneration in peripheral nerve autografts implanted in the spinal cord of the rat. Neurosurgery. 26:1990;37-42.
15. Funakoshi H., Frisen J., Barbany G., Timmusk T., Zachrisson O., Verge V.M., Persson H. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J. Cell. Biol. 123:1993;455-465.
16. Frisen J., Verge V.M., Fried K., Risling M., Persson H., Trotter J., Hokfelt T., Lindholm D. Characterization of glial trkB receptors: differential response to injury in the central and peripheral nervous system. Proc. Natl. Acad. Sci. U.S.A. 90:1993;4971-4975.
17. Hagg T., Vahlsing H.L., Manthorpe M., Varon S. Nerve growth factor infusion into the denervated adult rat hippocampal formation promotes its cholinergic reinnervation. J. Neurosci. 10:1990;3087-3092.
18. Hagg T., Varon S., Louis J.C. Ciliary neurotrophic factor (CNTF) promotes low-affinity nerve growth factor receptor and CD4 expression by rat CNS microglia. J. Neuroimmunol. 48:1993;177-187.
19. Hannestad J., Levanti M.B., Vega J.A. Distribution of neurotrophin receptors in human palatine tonsils: an immunohistochemical study. J. Neuroimmunol. 58:1995;131-137.
20. Houle J.D. Regeneration of dorsal root axons is related to specific non-neuronal cells lining NGF-treated intraspinal nitrocellulose implants. Exp. Neurol. 118:1992;138-142.
21. Johnson E.M. Jr., Taniuchi M., Distefano P.S. Expression and possible function of nerve growth factor receptors on Schwann cells. Trends Neurosci. 11:1988;299-304.
22. Junier M.P., Suzuki F., Onteniente B., Peschanski M. Target-deprived CNS neurons express the NGF gene while reactive glia around their axonal terminals contain low and high affinity NGF receptors. Mol. Brain Res. 24:1994;247-260.
23. McMahon S.B., Armanini M.P., Ling L.H., Phillips H.S. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron. 12:1994;1161-1171.
24. Nakahara Y., Gage F.H., Tuszinski M.H. Grafts of fibroblasts genetically modified to produce NGF, BDNF, NT-3, or basic FGF elicit differential responses in the adult spinal cord. Cell Trans. 5:1996;191-204.
25. Oudega M., Varon S., Hagg T. Regeneration of adult rat sensory fibers into intraspinal nerve grafts: promoting effects of conditioning lesion and graft pre-degeneration. Exp. Neurol. 129:1994;194-206.
26. Oudega M., Hagg T. Nerve growth factor promotes regeneration of sensory axons into the adult rat spinal cord. Exp. Neurol. 140:1996;218-229.
27. Patterson J.T., Head P.A., McNeill D.L., Chung K., Coggeshall R.E. Ascending unmyelinated primary afferent fibers in the dorsal funiculus. J. Comp. Neurol. 290:1989;384-390.
28. Richardson P.M., Issa V.M.K. Peripheral injury enhances central regeneration of primary sensory neurons. Nature. 309:1984;791-793.
29. Rosenthal A., Goeddel D.V., Hsu T., Lewis M., Shih A., Laramee G.R., Nikolics K., Winslow J.W. Primary structure and biological activity of a novel human neurotrophic factor. Neuron. 4:1990;767-773.
30. Ryden M., Ibanez C.F. Binding of neurotrophin-3 to p75LNGFR, TrkA, and TrkB mediated by a single functional epitope distinct from that recognized by trkC. J. Biol. Chem. 271:1996;5623-5627.
31. Schnell L., Schwab M.E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature. 343:1990;269-272.
32. Schwab M.E., Kapfhammer J.P., Bandtlow C.E. Inhibitors of neurite growth. Annu. Rev. Neurosci. 16:1993;565-595.
33. Soppet D., Escandon E., Maragos J., Middlemas D.S., Reid S.W., Blair J., Burton L.E., Stanton B.R., Kaplan D.R., Hunter T., Nikolics K., Parada L.F. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell. 65:1991;895-903.
34. Squinto S.P., Stitt T.N., Aldrich T.H., Davis S., Bianco S.M., Radziejewski C., Glass D.J., Masiakowski P., Furth M.E., Valenzuela D.M., DiStefano P.S., Yancopoulos G.D. trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell. 65:1991;885-893.
35. Tamatani M., Senba E., Tohyama M. Calcitonin gene-related peptide and Substance P containing primary afferents in the dorsal column of the rat. Brain Res. 495:1989;122-130.
36. Tessarollo L., Tsoulfas P., Donovan M.J., Palko M.E., Blair-Flynn J., Hempstead B.L., Parada L.F. Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates trkC in normal cardiogenesis. Proc. Natl. Acad. Sci. U.S.A. 94:1997;14776-14781.
37. Tuszynski M.H., Gabriel K., Gage F.H., Suhr S., Meyer S., Rosetti A. Nerve growth factor delivery by gene transfer induces differential outgrowth of sensory, motor, and noradrenergic neurites after adult spinal cord injury. Exp. Neurol. 137:1996;157-173.
38. Wetmore C., Olson L. Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interaction. J. Comp. Neurol. 353:1995;143-159.
39. W.D. Willis, R.E. Coggeshal, Sensory Mechanisms of the Spinal Cord, Plenum, New York, 1991.
40. Windisch J.M., Marksteiner R., Lang M.E., Auer B., Schneider R. Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 bind to a single leucine-rich motif of TrkB. Biochemistry. 34:1995;11256-11263.
41. Wright D.E., Snider W.D. Neurotrophin receptor mRNA expression defines distinct populations of neurons in rat dorsal root ganglia. J. Comp. Neurol. 351:1995;329-338.
42. Wyatt S., Pinon L.G., Ernfors P., Davies A.M. Sympathetic neuron survival and TrkA expression in NT3-deficient mouse embryos. EMBO J. 16(11):1997;3115-3123.
43. Zhou X.F., Rush R.A. Endogenous brain-derived neurotrophic factor is anterogradely transported in primary sensory neurons. Neuroscience. 74:1993;945-953.