Seizure-induced differential expression of messenger RNAs for neurotrophins and their receptors in genetically fast and slow kindling rats

Neuroscience

Volumn 75, Issue 1, 1996, Pages 197-207

  Kokaia, Z ^a   Kelly, M E ^b   Elmer E ^a   Kokaia, M ^a   McIntyre, D C ^b   Lindvall, O ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b CARLETON UNIVERSITY   (Canada)

Author keywords

epilepsy; in situ hybridization; kindling; neurotrophic factors; slow and fast kindlers

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPILEPSY; GENE EXPRESSION; IN SITU HYBRIDIZATION; KINDLING; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE;

EID: 0030572743     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00257-6     Document Type: Article

References (54)

1. Ayer-LeLievre C., Olson L., Ebendal T., Seiger A., Persson H. Expression of β-nerve growth factor in hippocampal neurons. Science. 240:1988;1339-1341.
2. Ballarín M., Ernfors P., Lindefors N., Persson H. Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Expl Neurol. 114:1991;35-43.
3. Bengzon J., Kokaia Z., Ernfors P., Kokaia M., Leanza 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;433-446.
4. Bengzon J., Söderström S., Kokaia Z., Kokaia M., Ernfors P., Persson H., Ebendal T., Lindvall O. Widespread increase of nerve growth factor protein in the rat forebrain after kindling-induced seizures. Brain Res. 587:1992;338-342.
5. Blöchl A., Thoenen H. Characterization of nerve growth factor (NGF) release from hippocampal neurons: evidence for a constitutive and an unconventional sodium-dependent regulated pathway. Eur. J. Neurosci. 7:1995;1220-1228.
6. Castrén E., Pitkänen M., Sirviö J., Parsadanian A., Lindholm D., Thoenen H., Riekkinen P. J. The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. NeuroReport. 4:1993;895-898.
7. DiStefano P. S., Friedman B., Radziejewski C., Alexander C., Boland P., Schick C. M., Lindsay R. M., Wiegand S. J. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron. 8:1992;983-993.
8. Dufresne C., Kelly M. E., McIntyre D. C. New fast and slow kindling rat strains. Epilepsia. 30:1989;652.
9. Dugich-Djordjevic M. M., Tocco G., Willoughby D. A., Najm I., Pasinetti G., Thompson R. F., Baudry M., Lapchak P. A., Hefti F. BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron. 8:1992;1127-1138.
10. Elmér E., Kokaia M., Ernfors P., Ferenz I., Kokaia Z., and Lindvall O. (1996) Suppressed kindling epileptogenesis and perturbed BDNF and TrkB gene regulation in NT-3 mutant mice. J. Neurosci. (Submitted).
11. Ernfors P., Bengzon J., Kokaia Z., Persson H., Lindvall O. Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron. 7:1991;165-176.
12. Ernfors P., Henschen A., Olson L., Persson H. Expression of nerve growth factor receptor messenger RNA is developmentally regulated and increased after axotomy in rat spinal cord motoneurons. Neuron. 2:1989;1605-1613.
13. Ernfors P., Ibáñez C. F., Ebendal T., Olson L., Persson H. Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: developmental and topographical expression in the brain. Proc. natn. Acad. Sci. U.S.A. 87:1990;5454-5458.
14. 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.
15. Falkenberg T., Metsis M., Timmusk T., Lindefors N. Entorhinal cortex regulation of multiple brain-derived neurotrophic factor promoters in the rat hippocampus. Neuroscience. 57:1993;891-896.
16. Funabashi T., Sasaki H., Kimura F. Intraventricular injection of antiserum to nerve growth factor delays the development of amygdaloid kindling. Brain Res. 458:1988;132-136.
17. Gall C., Murray K., Isackson P. J. Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus. Brain Res. 9:1991;113-123.
18. Gall C. M., Isackson P. J. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science. 245:1989;758-761.
19. Griesbeck O., Blöchl A., Carnahan J. F., Nawa H., Thoenen H. Characterization of brain-derived neurotrophic factor (BDNF) secretion from hippocampal neurons. Soc. Neurosci. Abstr. 21:1995;1046.
20. Hofer M., Paglusi S. R., Hohn A., Leibrock J., Barde Y.-A. Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. Eur. molec. Biol. Org. J. 9:1990;2459-2464.
21. 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.
22. 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.
23. Kang H., Schuman E. M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662.
24. Kim H. G., Wang T., Olafsson P., Lu B. Neurotrophin-3 potentiates neuronal activity and inhibits gamma-aminobutyratergic synaptic transmission in cortical neurons. Proc. natn. Acad. Sci. U.S.A. 91:1994;12341-12345.
25. Knipper M., Leung L. S., Zhao D., Rylett J. R. Short-term modulation of glutamatergic synapses an adult rat hippocampus by NGF. NeuroReport. 5:1994;2433-2436.
26. Kokaia M., Ernfors P., Kokaia Z., Elmér E., Jaenisch R., Lindvall O. Suppressed epileptogenesis in BDNF mutant mice. Expl Neurol. 133:1995;215-224.
27. Kokaia M., Ferencz I., Leanza G., Elmér E., Metsis M., Kokaia Z., Wiley R. G., Lindvall O. Immunolesioning of basal forebrain cholinergic neurons facilitates hippocampal kindling and perturbs neurotrophin messenger RNA regulation. Neuroscience. 70:1995;313-327.
28. 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. natn. Acad. Sci. U.S.A. 90:1993;6711-6715.
29. Kokaia Z., Zhao Q., Kokaia M., Elmér E., Metsis M., Smith M.-L., Siesjö B. K., Lindvall O. Regulation of brain-derived neurotrophic factor gene expression after transient middle cerebral artery occlusion with and without brain damage. Expl Neurol. 136:1995;73-88.
30. Korsching S., Auburger G., Heumann R., Scott J., Thoenen H. Levels of nerve growth factor and its mRNA in the central nervous system of the rat correlate with cholinergic innervation. Eur. molec. Biol. Org. J. 4:1985;1389-1393.
31. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. natn. Acad. Sci. U.S.A. 92:1995;8856-8860.
32. Lauterborn J. C., Isackson P. J., Gall C. M. Seizure-induced increases in NGF mRNA exhibit different time courses across forebrain regions and are biphasic in hippocampus. Expl Neurol. 125:1994;22-40.
33. Lessmann V., Gottmann K., Heumann R. BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. NeuroReport. 6:1994;21-25.
34. Lindvall O., Ernfors P., Bengzon J., Kokaia Z., Smith M.-L., Siesjö B. K., Persson H. Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc. natn. Acad. Sci. U.S.A. 89:1992;648-652.
35. Maisonpierre P. C., Belluscio L., Squinto S., Ip N. Y., Furth M. E., Lindsay R. M., Yancopolous G. D. Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science. 247:1990;1446-1451.
36. McNamara J. O., Bonhaus D. W. and Shin C. (1993) The kindling model of epilepsy. In Epilepsy: Models, Mechanisms and Concepts (ed. Schwartzkroin P. A.), pp. 27-47. Cambridge University Press, Cambridge.
37. Merlio J.-P., Ernfors P., Jaber M., Persson H. Molecular cloning of rat trkC and disribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience. 51:1992;513-532.
38. Merlio J.-P., Ernfors P., Kokaia Z., Middlemas D. S., Bengzon J., Kokaia M., Smith M.-L., Siesjö B. K., Hunter T., Lindvall O., Persson H. Increased production of TrkB protein tyrosine kinase receptor after brain insults. Neuron. 10:1993;151-164.
39. Middlemas D. S., Lindberg R. A., Hunter T. trkB, a neural receptor protein-tyrosine kinase: evidence for full-length and two truncated receptors. Molec. Cell Biol. 11:1991;143-153.
40. Miranda R. C., Sohrabji F., Toran-Allerand C. D. Neuronal colocalization of mRNAs for neurotrophins and their receptors in the developing central nervous system suggests a potential for autocrine interactions. Proc. natn. Acad. Sci. U.S.A. 90:1993;6439-6443.
41. Mudó G., Persson H., Timmusk T., Funakoshi H., Bindoni M., Belluardo N. Increased expression of trkB and trkC messenger RNAs in the rat forebrain after focal mechanical injury. Neuroscience. 57:1993;901-912.
42. Nawa H., Carnahan J., Gall C. BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disaccordance with mRNA levels. Eur. J. Neurosci. 7:1995;1527-1535.
43. Phillips H. S., Hains J. M., Laramee G. R., Rosenthal A., Winslow J. W. Widespread expression of BDNF but not NT-3 by target areas of basal forebrain cholinergic neurons. Science. 250:1990;290-294.
44. Racine R. J. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroenceph. clin. Neurophysiol. 32:1972;281-294.
45. Rennert P. D., Heinrich G. Nerve growth factor mRNA in brain: localization by in situ hybridization. Biochem. biophys. Res. Commun. 138:1986;813-818.
46. Rocamora N., Palacios J. M., Mengold 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. Brain Res. 13:1992;27-33.
47. Steingart M. O. (1983) The selective breeding of seizure-prone vs. seizure resistant rats based on amygdala kindling: behavioral, electrophysiological and pharmacological measures. Ph.D. Dissertation, Hamilton, Ontario.
48. Sun F. Y., Costa E., Mocchetti I. Adrenal steroids mediate the increase of hippocampal nerve growth factor biosynthesis following bicuculline convulsions. Neuropsychopharmacology. 8:1993;219-225.
49. Takeda A., Onodera H., Sugimoto A., Kogure K., Obinata M., Shibahara S. Coordinated expression of messenger RNAs for nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 in the rat hippocampus following transient forebrain ischemia. Neuroscience. 55:1993;23-31.
50. Thoenen H. Neurotrophins and neuronal plasticity. Science. 270:1995;593-598.
51. Van der Zee C. E. E., Rashid K., Le K., Moore K. A., Stanisz J., Diamond J., Racine R. J., Fahnestock M. Intraventricular administration of antibodies to nerve growth factor retards kindling and blocks mossy fiber sprouting in adult rats. J. Neurosci. 15:1995;5316-5323.
52. Wada J., Sato M., Corcoran M. Persistent seizure susceptibility and recurrent spontaneous seizures in kindled cats. Epilepsia. 15:1974;465-478.
53. Whittemore S. R., Friedman P. L., Larhammar D., Persson H., Gonzalez C. M., Holets V. R. Rat β-nerve growth factor sequence and site of synthesis in the adult hippocampus. J. Neurosci. 20:1988;403-410.
54. Zafra F., Castrén E., Thoenen H., Lindholm D. Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in the hippocampal neurons. Proc. natn. Acad. Sci. U.S.A. 88:1991;10037-10041.