Continuous infusion of neurotrophin-3 triggers sprouting, decreases the levels of TrkA and TrkC, and inhibits epileptogenesis and activity-dependent axonal growth in adult rats

Neuroscience

Volumn 115, Issue 4, 2002, Pages 1295-1308

  Xu, B ^a   Michalski, B ^a   Racine, R J ^a   Fahnestock, M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Epilepsy; Kindling; Mossy fiber sprouting; Neurotrophic factors; Seizures; Trk receptors

Indexed keywords

NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN 3; NEUROTROPHIN 3 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CHOLINERGIC NERVE; CONTROLLED STUDY; DENTATE GYRUS; DOWN REGULATION; EPILEPTOGENESIS; INFUSION; MALE; MOLECULAR BIOLOGY; MOSSY FIBER; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR AFFINITY; SEIZURE; SPROUTING;

ANIMALS; CELL COUNT; CYTOCHROME C GROUP; DRUG ADMINISTRATION SCHEDULE; EPILEPSY; GROWTH CONES; KINDLING, NEUROLOGIC; MALE; MOLECULAR WEIGHT; MOSSY FIBERS, HIPPOCAMPAL; NEURONAL PLASTICITY; NEUROPIL; NEUROTROPHIN 3; PHOSPHORYLATION; RATS; RATS, LONG-EVANS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, TRKA; RECEPTOR, TRKB; RECEPTOR, TRKC; SEIZURES;

EID: 0037121674     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00384-6     Document Type: Article

References (92)

1. Adams B., Sazgar M., Osehobo P., Van der Zee C.E.E.M., Diamond J., Fahnestock M., Racine R.J. Nerve growth factor accelerates seizure development, enhances mossy fiber sprouting, and attenuates seizure-induced decreases in neuronal density in the kindling model of epilepsy. J. Neurosci. 17:1997;5288-5296.
2. Adams B., Vaccarella L., Fahnestock M., Racine R.J. The cholinergic system modulates kindling and kindling-induced mossy fiber sprouting. Synapse. 44:2002;132-138.
3. Adams B., Von Ling E., Vaccarella L., Ivy G.O., Fahnestock M., Racine R.J. Time course for kindling-induced changes in the hilar area of the dentate gyrus: reactive gliosis as a potential mechanism. Brain Res. 804:1998;331-336.
4. 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.
5. Asztely F., Kokaia M., Olofsdotter K., Ortegren U., Lindvall O.R. Afferent-specific modulation of short-term synaptic plasticity by neurotrophins in dentate gyrus. Eur. J. Neurosci. 12:2000;662-669.
6. Avila M.A., Varela-Nieto I., Romero G., Mato J.M., Giraldez F., Van De Water T.R., Represa J. Brain-derived neurotrophic factor and neurotrophin-3 support the survival and neuritogenesis response of developing cochleovestibular ganglion neurons. Dev. Biol. 159:1993;266-275.
7. Baker R.E., Dijkhuizen P.A., Van Pelt J., Verhaagen J. Growth of pyramidal, but not non-pyramidal, dendrites in long-term organotypic explants of neonatal rat neocortex chronically exposed to neurotrophin-3. Eur. J. Neurosci. 10:1998;1037-1044.
8. Barbacid M. Structural and functional properties of the TRK family of neurotrophin receptors. Ann. NY Acad. Sci. 766:1995;442-458.
9. Bengzon J., Kokaia Z., Ernfors P., Kokaia M., Leanze G., Nilsson O.G., Persson H., Lindvall O. Regulation of neurotrophin and TrkA, TrkB and TrkC tyrosine kinase receptor messenger RNA expression in kindling. Neuroscience. 53:1993;433-466.
10. Bertram E.H., Lothman E.W. Morphometric effects of intermittent kindled seizures and limbic status epilepticus in the dentate gyrus of the rat. Brain Res. 603:1993;25-31.
11. Berzaghi M.P., Gutierrez R., Heinemann U., Lindholm D., Thoenen H. Neurotrophins induce acute transmitter-mediated changes in brain electrical activities. Soc. Neurosci. Abstr. 21:1995;545.
12. Binder D.K., Routbort M.J., McNamara J.O. Immunohistochemical evidence of seizure-induced activation of trk receptors in the mossy fiber pathway of adult rat hippocampus. J. Neurosci. 19:1999;4616-4626.
13. Binder D.K., Routbort M.J., Ryan T.E., Yancopoulos G.D., McNamara J.O. Selective inhibition of kindling development by intraventricular administration of TrkB receptor body. J. Neurosci. 19:1999;1424-1436.
14. Bradbury E.J., Khemani S., King V.R., Priestley J.V., McMahon S.B. NT-3 promotes growth of lesioned adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur. J. Neurosci. 11:1999;3873-3883.
15. Carter B.D., Zirrgiebel U., Barde Y.A. Differential regulation of p21ras activation in neurons by nerve growth factor and brain-derived neurotrophic factor. J. Biol. Chem. 270:1995;21751-21757.
16. Conner J.M., Lauterborn J.C., Yan Q., Gall C.M., Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci. 17:1997;2295-2313.
17. Conover J.C., Yancopoulos G.D. Neurotrophin regulation of the developing nervous system: analyses of knockout mice. Rev. Neurosci. 8:1997;13-27.
18. Cordon-Cardo C., Tapley P., Jing S., Nanduri V., O'Rourke E., Lamballe F., Kovary K., Klein R., Jones K., Reichardt L., Barbacid M. The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell. 66:1991;173-183.
19. Croll S.D., Chesnutt C.R., Rudge J.S., Acheson A., Ryan T.E., Siuciak J.A., DiStefano P.S., Wiegand S.J., Lindsay R.M. Co-infusion with a TrkB-Fc receptor body carrier enhances BDNF distribution in the adult rat brain. Exp. Neurol. 152:1998;20-33.
20. Davies A.M. Neurotrophins: neurotrophic modulation of neurite growth. Curr. Biol. 10:2000;R198-R200.
21. Diamond J., Coughlin M., Holmes M. Endogenous NGF and nerve impuses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J. Neurosci. 12:1992;1454-1466.
22. Dijkhuizen P.A., Hermens W.T., Teunis M.A., Verhaagen J. Adenoviral vector-directed expression of neurotrophin-3 in rat dorsal root ganglion explants results in a robust neurite outgrowth response. J. Neurobiol. 33:1997;172-184.
23. Elmer E., Kokaia M., Ernfors P., Ferencz I., Kokaia Z., Lindvall O. Suppressed kindling epileptogenesis and perturbed BDNF and TrkB gene regulation in NT-3 mutant mice. Exp. Neurol. 145:1997;93-103.
24. Elmer E., Kokaia M., Kokaia Z., Ferencz I., Lindvall O. Delayed kindling development after rapidly recurring seizures: relation to mossy fiber sprouting and neurotrophin, GAP-43 and dynorphin gene expression. Brain Res. 712:1996;19-34.
25. Elmer E., Kokaia Z., Kokaia M., Carnahan J., Nawa H., Lindvall O. Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures. Neuroscience. 83:1998;351-362.
26. Ernfors P., Bengzon J., Kokaia Z., Persson H., Lindvall O. Increased levels of messenger RNA for neurotrophic factors in the brain during kindling epileptogenesis. Neuron. 7:1991;165-176.
27. Ernfors P., Wetmore C., Olson L., Persson H. Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron. 5:1990;511-526.
28. Fahnestock M., Zhu W. Expression of human prohormone convertase PC2 in a baculovirus-insect cell system. DNA Cell Biol. 18:1999;409-417.
29. Frank L., Ventimiglia R., Anderson K., Lindsay R.M., Rudge J.S. BDNF down-regulates neurotrophin responsiveness, TrkB protein and TrkB mRNA levels in cultured rat hippocampal neurons. Eur. J. Neurosci. 8:1996;1220-1230.
30. Frank L., Wiegand S.J., Siuciak J.A., Lindsay R.M., Rudge J.S. Effects of BDNF infusion on the regulation of TrkB protein and message in adult rat brain. Exp. Neurol. 145:1997;62-70.
31. Gall C.M. Seizure-induced changes in neurotrophin expression; implication for epilepsy. Exp. Neurol. 124:1993;150-166.
32. Gall C.M., Isackson P.J. Limbic Seizures increase neuronal production of messenger RNA for nerve growth factor. Science. 24:1989;758-761.
33. Gibbs R.B., Pfaff D.W. In situ hybridization detection of trkA mRNA in brain: distribution, colocalization with p75NGFR and up-regulation by nerve growth factor. J. Comp. Neurol. 341:1994;324-339.
34. Goddard G.V. Development of epileptic seizures through brain stimulation at low intensity. Nature. 214:1967;1020-1021.
35. Humpel C., Wetmore C., Olson L. Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience. 53:1993;909-918.
36. Inoue T., Hirai H., Onteniente B., Suzuki F. Correlated long-term increase of brain-derived neurotrophic factor and Trk B proteins in enlarged granule cells of mouse hippocampus after kainic acid injection. Neuroscience. 86:1998;723-728.
37. Isackson P.J., Huntsman M.M., Murray K.D., Gall C.M. BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron. 6:1991;937-948.
38. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662.
39. Katoh-Semba R., Takeuchi I.K., Inaguma Y., Ito H., Kato K. Brain-derived neurotrophic factor, nerve growth and neurotrophin-3 selected regions of the rat brain following kainic acid-induced seizure activity. Neurosci. Res. 35:1999;19-29.
40. Khurgel M., Racine R.J., Ivy G.O. Kindling causes changes in the composition of the astrocytic sytoskeleton. Brain Res. 592:1992;338-342.
41. Kim H.G., Wang T., Olafsson P., Lu B. Neurotrophin 3 potentiates neuronal activity and inhibits gamma-aminobutyratergic synaptic transmission in cortical neurons. Proc. Natl. Acad. Sci. USA. 91:1994;12341-12345.
42. Klein R., Conway D., Parada L.F., Barbacid M. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell. 61:1990;647-656.
43. Klein R., Martin-Zanca D., Barbacid M., Parada L.F. Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development. 109:1990;845-850.
44. Knüsel B., Gao H., Okazaki T., Yoshida Y., Mori N., Hefti F., Kaplan D.R. Ligand-induced down-regulation of TRK messenger RNA, protein and tyrosine phosphorylation in rat cortical neurons. Neuroscience. 78:1997;851-862.
45. Kokaia M., Asztelym F., Olofsdotter K., Sindreu C.B., Kullmann D.M., Lindvall O. Endogenous neurotrophin-3 regulates short-term plasticity at lateral perforant path-granule cell synapses. J. Neurosci. 18:1998;8730-8739.
46. Kokaia M., Ernfors P., Kokaia Z., Elmer E., Jaenisch R., Lindvall O. Suppressed epileptogenesis in BDNF mutant mice. Exp. Neurol. 133:1995;215-224.
47. Kokaia Z., Bengzon J., Metsis M., Kokaia M., Persson H., Lindvall O. Coexpression of neurotrophins and their receptors in neurons of the central nervous system. Proc. Natl. Acad. Sci. USA. 90:1993;6711-6715.
48. Kokaia Z., Kelly M.E., Elmer E., Kokaia M., McIntyre D.C., Lindvall O. Seizure-induced differential expression of messenger RNAs for neurotrophins and their receptors in genetically fast and slow kindling rats. Neuroscience. 75:1996;197-207.
49. Labelle C., Leclerc N. Exogenous BDNF, NT-3 and NT-4 differentially regulate neurite outgrowth in cultured hippocampal neurons. Dev. Brain Res. 123:2000;1-11.
50. Lahteinen S., Pitkanen A., Saarelainen T., Nissinen J., Koponen E., Castren E. Decreased BDNF signalling in transgenic mice reduces epileptogenesis. Eur. J. Neurosci. 15:2002;721-734.
51. Lamballe F., Klein R., Barbacid M. TrkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell. 66:1991;967-979.
52. Larmet Y., Reibel S., Carnahan J., Nawa H., Marescaux C., Depaulis A. Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. NeuroReport. 6:1995;1937-1941.
53. Levine E.S., Dreyfus C.F., Black I.B., Plummer M.R. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl. Acad. Sci. USA. 92:1995;8074-8077.
54. Li Y., Holtzman D.M., Kromer L.F., Kaplan D.R., Chua-Couzens J., Clary D.O., Knusel B., Mobley W.C. Regulation of TrkA and ChAT expression in developing rat basal forebrain: evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J. Neurosci. 15:1995;2888-2905.
55. Lindsay R.M., Wiegand S.J., Altar C.A., DiStefano P.S. Neurotrophins and brain insults. Trends Neurosci. 17:1994;490-496.
56. Lu B., Figurov A. Role of neurotrophins in synapse development and plasticity. Rev. Neurosci. 8:1997;1-12.
57. Maisonpierre P.C., Belluscio L., Friedman B., Alderson R.F., Wiegand S.J., Furth M.E., Lindsay R.M., Yancopoulos G.D. NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron. 5:1990;501-509.
58. Malgrange B., Lefebvre P.P., Martin D., Staecker H., Van de Water T.R., Moonen G. NT-3 has a tropic effect on process outgrowth by postnatal auditory neurones in vitro. NeuroReport. 17:1996;2495-2499.
59. McAllister A.K., Katz L.C., Lo D.C. Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci. 22:1999;295-318.
60. Mendell L.M. Neurotrophin action on sensory neurons in adults: an extension of the neurotrophic hypothesis. Pain. 6:(Suppl.):1999;S127-S132.
61. Merlio J.P., Ernfors P., Jaber M., Persson H. Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience. 51:1992;513-532.
62. Merlio J.P., Ernfors P., Kokaia Z., Middlemas D.S., Bengzon J., Kokaia M., Smith M.L., Siesjo B.K., Hunter T., Lindvall O., Persson H. Increased production of the TrkB protein tyrosine kinase receptor after brain insults. Neuron. 10:1993;151-164.
63. Mocchetti I., Wrathall J.R. Neurotrophic factors in central nervous system trauma. J. Neurotrauma. 12:1995;853-870.
64. Mohiuddin L., Fernandez K., Tomlinson D.R., Fernyhough P. Nerve growth factor and neurotrophin-3 enhance neurite outgrowth and up-regulate the levels of messenger RNA for growth-associated protein GAP-43 and T alpha 1 alpha-tubulin in cultured adult rat sensory neurones. Neurosci. Lett. 185:1995;20-23.
65. Morfini G., DiTella M.C., Feiguin F., Carri N., Caceres A. Neurotrophin-3 enhances neurite outgrowth in cultured hippocampal pyramidal neurons. J. Neurosci. Res. 39:1994;219-232.
66. Morimoto K., Sato K., Sato S., Yamada N., Hayabara T. Time-dependent changes in neurotrophic factor mRNA expression after kindling and long-term potentiation in rats. Brain Res. Bull. 45:1998;599-605.
67. Mudo G., Jiang X.H., Timmusk T., Bindoni M., Belluardo N. Change in neurotrophins and their receptor mRNAs in the rat forebrain after status epilepticus induced by pilocarpine. Epilepsia. 37:1996;198-207.
68. Mufson E.J., Kroin J.S., Sendera T.J., Sobreviela T. Distribution and retrograde transport of trophic factors in the central nervous system: functional implications for the treatment of neurodegenerative diseases. Prog. Neurobiol. 57:1999;451-484.
69. Osehobo P., Adams B., Sazgar M., Xu Y., Racine R.J., Fahnestock M. Brain-derived neurotrophic factor infusion delays amygdala and perforant path kindling without affecting paired-pulse measures of neuronal inhibition in adult rats. Neuroscience. 92:1999;1367-1375.
70. Paxinos, G., Watson, C., 1985. In: The Rat Brain in Stereotaxic Coordinates, 2nd Ed. Academic, Sydney.
71. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32:1972;281-294.
72. Rashid K., Van der Zee C.E., Ross G.M., Chapman C.A., Stanisz J., Riopelle R.J., Racine R.J., Fahnestock M. A nerve growth factor peptide retards seizure development and inhibits neuronal sprouting in a rat model of epilepsy. Proc. Natl. Acad. Sci. USA. 92:1995;9495-9499.
73. Reibel S., Larmet Y., Carnahan J., Marescaux C., Depaulis A. Endogenous control of hippocampal epileptogenesis: a molecular cascade involving brain-derived neurotrophic factor and neuropeptide Y. Epilepsia. 41:(Suppl 6):2000;S127-S133.
74. Reibel S., Larmet Y., Le B., Carnahan J., Marescaux C., Depaulis A. Brain-derived neurotrophic factor delays hippocampal kindling in the rat. Neuroscience. 100:2000;777-788.
75. Rocamora N., Palacios J.M., Mengod G. Limbic seizures induce a differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in the rat hippocampus. Mol. Brain Res. 13:1992;27-33.
76. Rudge J.S., Mather P.E., Pasnikowshi E.M., Cai N., Corcoran T., Acheson A., Anderson K., Lindsay R.M., Weigand S.J. Endogenous BDNF protein is increased in adult rat hippocampus after a kainic acid induced excitotoxic insult but exogenous BDNF is not neuroprotective. Exp. Neurol. 149:1998;398-410.
77. 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.
78. Scharfman H.E., Goodman J.H., Sollas A.L., Croll S.D. Spontaneous limbic seizures after intrahippocampal infusion of brain-derived neurotrophic factor. Exp. Neurol. 174:2002;201-214.
79. Schinder A.F., Poo M. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 23:2000;639-645.
80. Schnell L., Schneider R., Kolbeck R., Barde Y.A., Schwab M.E. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature. 367:1994;170-173.
81. Schuman E.M. Neurotrophin regulation of synaptic transmission. Curr. Opin. Neurobiol. 9:1999;105-109.
82. Sommerfeld M.T., Schweigreiter R., Barde Y.A., Hoppe E. Down-regulation of the neurotrophin receptor TrkB following ligand binding. J. Biol. Chem. 275:2000;8982-8990.
83. Soppet D., Escandon E., Maragos J., Middlemas D., Reid S., Blair J., Burton L., Stanton B., Kaplan D., Hunter T., Nikolics K., Parada L. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell. 65:1991;895-903.
84. Squinto S., Stitt T., Aldrich T., Davis S., Bianco S., Radziejewski C., Glass D., Masiakowski P., Furth M., Valenzuela D., DiStefano P., Yancopoulos G. TrkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell. 65:1991;885-893.
85. Terenghi G. Peripheral nerve regeneration and neurotrophic factors. J. Anat. 194:1999;1-14.
86. Thoenen H. Neurotrophins and activity-dependent plasticity. Prog. Brain Res. 128:2000;183-191.
87. Van der Zee C.E.E.M., Rashid K., Le K., Moore K.A., Stanisz J., Diamond J., Racine R.J., Fahnestock M. Intraventricular administration of antibodies to NGF retards kindling and blocks mossy fiber sprouting in adult rats. J. Neurosci. 15:1995;5316-5323.
88. Venero J.L., Knusel B., Beck K.D., Hefti F. Expression of neurotrophin and trk receptor genes in adult rats with fimbria transections: effect of intraventricular nerve growth factor and brain-derived neurotrophic factor administration. Neuroscience. 59:1994;797-815.
89. Watanabe Y., Johnson R.S., Butler L.S., Binder D.K., Spiegelman B.M., Papaioannou V.M., McNamara J.O. Null mutation of c-fos impairs structural and functional plasticities in the kindling model of epilepsy. J. Neurosci. 16:1996;3827-3836.
90. Yan Q., Matheson C., Sun J., Radeke M.J., Feinstein S.C., Miller J.A. Distribution of intracerebral ventricularly administered neurotrophins in rat brain and its correlation with trk receptor expression. Exp. Neurol. 127:1994;23-36.
91. Yan Q., Rosenfeld R.D., Matheson C.R., Hawkins N., Lopez O.T., Bennet L., Welcher A.A. Expression of brain-derived neurotrophic factor (BDNF) protein in the adult rat central nervous system. Neuroscience. 78:1997;431-448.
92. Zhou X.F., Rush R.A. Localization of neurotrophin-3-like immunoreactivity in the rat central nervous system. Brain Res. 643:1994;162-172.