Differential regulation by MK801 of immediate-early genes, brain-derived neurotrophic factor and trk receptor mRNA induced by a kindling after-discharge

Molecular Brain Research

Volumn 53, Issue 1-2, 1998, Pages 138-151

  Hughes, Paul E ^a   Young, Deborah ^b   Preston, Kerin M ^b   Yan, Qiao ^c   Dragunow, Michael ^b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c AMGEN INC   (United States)

Author keywords

Epilepsy; Fos; Neurotrophin; Rat; trkB; trkC

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DIZOCILPINE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TYROSINE KINASE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; GRANULE CELL; IMMEDIATE EARLY GENE; INTERNEURON; KINDLING; MALE; MOSSY FIBER; NONHUMAN; ONCOGENE C FOS; ONCOGENE C JUN; PRIORITY JOURNAL; RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DIZOCILPINE MALEATE; DNA-BINDING PROTEINS; EARLY GROWTH RESPONSE PROTEIN 1; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GENE EXPRESSION REGULATION; GENES, IMMEDIATE-EARLY; HIPPOCAMPUS; IMMEDIATE-EARLY PROTEINS; KINDLING, NEUROLOGIC; NEURONS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RATS, WISTAR; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, TRKA; RECEPTORS, NERVE GROWTH FACTOR; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0031931970     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(97)00288-X     Document Type: Article

References (73)

1. Bading H., Ginty D.D., Greenberg M.E. Regulation of gene expression in hippocampal neurons by distinct calcium signalling pathways. Science. 260:1993;181-186.
2. 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.
3. Cain D.P. Long-term potentiation and kindling: how similar are the mechanisms? Trends Neurosci. 12:1989;6-10.
4. Cole A.J., Saffen D.W., Baraban J.M., Worley P.F. Rapid increase of an immediate-early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature. 340:1989;474-476.
5. Cole A.J., Abu-Sharkra S., Saffen D.W., Baraban J.M., Worley P.F. Rapid rise in transcription factor mRNAs in rat brain after electroshock-induced seizures. J. Neurochem. 55:1990;1920-1927.
6. Comelli M.C., Seren M.S., Guidolin D., Manev R.M., Favaron M., Rimland J.M., Canella R., Negro A., Manev H. Photochemical stroke and brain-derived neurotrophic factor (BDNF) mRNA expression. NeuroReport. 3:1992;473-476.
7. B. Conner, D. Young, Q. Yan, R.L.M. Faull, B. Synek, M. Dragunow, Brain-derived neurotrophic factor is reduced in Alzheimers disease. Mol. Brain Res. (in press).
8. Conner J.M., Yan Q., Varon S. Distribution of brain-derived neurotrophic factor in the rat pituitary gland. NeuroReport. 7:1996;1937-1940.
9. 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.
10. Dragunow M., Faull R.L.M. MK-801 induces c-fos protein in thalamic and neocortical neurons of rat brain. Neurosci. Lett. 111:1990;39-45.
11. Dragunow M., Robertson H.A. Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature. 329:1987;441-442.
12. Dragunow M., Abraham W.C., Goulding M., Mason S.E., Robertson H.A., Faull R.L.M. Long-term potentiation and the induction of c-fos mRNA and proteins in the dentate gyrus of unanaesthetized rats. Neurosci. Lett. 101:1989;274-280.
13. Dragunow M., Currie R.W., Faull R.L.M., Robertson H.A., Jansen K. Immediate-early genes, kindling and long-term potentiation. Neurosci. Biobehav. Rev. 13:1989;301-313.
14. Dragunow M., Faull R.L.M., Jansen K.L.R. MK-801, an antagonist of NMDA receptors, inhibits injury-induced c-fos protein accumulation in rat brain. Neurosci. Lett. 109:1990;128-133.
15. Dragunow M., Yamada N., Bilkey D.K., Lawlor P. Induction of immediate-early gene proteins in dentate granule cells and somatostatin interneurons after hippocampal seizures. Mol. Brain Res. 13:1992;119-126.
16. Dragunow M., Beilharz E., Mason B., Lawlor P., Abraham W., Gluckman P. Brain-derived neurotrophic factor expression after long-term potentiation. Neurosci. Lett. 160:1993;232-236.
17. Dugich-Djordjevic M.M., Peterson C., Isono F., Ohsawa F., Widmer H.R., Denton T.L., Bennett G.L., Hefti F. Immunohistochemical visualisation of brain-derived neurotrophic factor in the rat brain. Eur. J. Neurosci. 7:1995;1831-1839.
18. 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.
19. Funabashi T., Saki H., Kimura F. Intraventricular injection of antiserum to nerve growth factor delays the development of amygdaloid kindling. Brain Res. 459:1988;132-136.
20. Gilbert M.E. The NMDA-receptor antagonist, MK-801, suppresses limbic kindling and kindled seizures. Brain Res. 463:1988;90-99.
21. Gilbert M.E., Mack C.M. The NMDA antagonist, MK-801, suppresses long-term potentiation, kindling, and kindling-induced potentiation in the perforant path of the unanaesthetized rat. Brain Res. 519:1990;89-96.
22. Goddard G.V. Development of epileptic seizures through brain stimulation at low intensity. Nature. 214:1967;1020-1021.
23. Gunn A.J., Dragunow M., Faull R.L.M., Gluckman P.D. Effects of hypoxia-ischaemia and seizures on neuronal and glial-like c-fos protein levels in the infant rat. Brain Res. 531:1990;105-116.
24. Gwag B.J., Springer J.E. Activation of NMDA receptors increases brain-derived neurotrophic factor (BDNF) mRNA expression in the hippocampal formation. NeuroReport. 5:1993;125-128.
25. Herrera D.G., Robertson H.A. N-methyl-D-aspartate receptors mediate activation of the c-fos proto-oncogene in a model of brain injury. Neuroscience. 35:1990;273-281.
26. Hopker V.H., Kjaer B., Varon S. Dopaminergic regulation of BDNF content in the pituitary intermediate lobe. NeuroReport. 8:1997;1089-1093.
27. Hughes P., Lawlor P., Dragunow M. Basal expression of Fos, Fos-related, Jun, and Krox 24 proteins in rat hippocampus. Mol. Brain Res. 13:1992;355-357.
28. Hughes P., Dragunow M., Beilharz E., Lawlor P., Gluckman P. MK801 induces immediate-early gene proteins and BDNF mRNA in rat cerebrocortical neurones. NeuroReport. 4:1993;183-186.
29. Hughes P., Beilharz E., Gluckman P., Dragunow M. Brain-derived neurotrophic factor is induced as an immediate-early gene following N-methyl-D-aspartate receptor activation. Neuroscience. 57:1993;319-328.
30. Hughes P., Young D., Dragunow M. MK801 sensitizes rats to pilocarpine induced limbic seizures and status epilepticus. NeuroReport. 4:1993;314-316.
31. Hughes P., Dragunow M. Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol. Rev. 47:1995;133-178.
32. Hughes P., Dragunow M. TrkC may be an inducible transcription factor target gene. NeuroReport. 6:1995;465-468.
33. Humpel C., Wetmore C., Olson L. Regulation of BDNF mRNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience. 53:1993;909-918.
34. 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.
35. Jonec V., Wasterlain C.G. Effect of inhibitors of protein synthesis on the development of kindled seizures in rats. Exp. Neurol. 66:1979;524-532.
36. Kang H., Schuman E.M. Long-lasting neurotrophin-enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662.
37. Kokaia M., Ernfors P., Kokaia Z., Elmer E., Jaenisch R., Lindvall O. Suppressed epileptogenesis in BDNF mutant mice. Exp. Neurol. 133:1995;215-224.
38. Kovary K., Bravo R. The jun and fos protein families are both required for cell cycle progression in fibroblasts. Mol. Cell. Biol. 11:1991;4466-4472.
39. Kovary K., Bravo R. Expression of different Jun and Fos proteins during the G0-G1 transition in mouse fibroblasts: in vitro and in vivo associations. Mol. Cell Biol. 11:1991;2451-2459.
40. Labiner D.M., Butler L.S., Cao Z., Hosford D.A., Shin C., McNamara J.O. Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing. J. Neurosci. 13:1993;744-751.
41. Larmet Y., Reibel S., Carnahan J., Nawa H., Marescaux C., Depaulis A. Protective effets of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. NeuroReport. 6:1995;1937-1941.
42. Lees G.J. Influence of ketamine on the neuronal death caused by NMDA in the rat hippocampus. Neuropharmacology. 34:1995;411-417.
43. McNamara J.O., Russell R.D., Rigsbee L., Bonhaus D.W. Anticonvulsant and antiepileptogenic actions of MK-801 in the kindling and electroshock models. Neuropharmacology. 27:1988;563-568.
44. Merlio J.P., Ernfors P., Jaber M., Persson H. Molecular cloning of rat trk C and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience. 51:1992;513-532.
45. Merlio J.P., Ernfors P., Kokaia Z., Middlemas D.S., Bengzon J., Kokaia M., Smit M.L., Siesjo B.K., Hunter T., Lindvall O., Persson H. Increased production of trk B protein tyrosine kinase receptor after brain insult. Neuron. 10:1993;151-164.
46. Middlemas D.S., Lindberg R.A., Hunter T.A. trkB, a neurol receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol. Cell Biol. 11:1991;143-153.
47. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Ann. Rev. Neurosci. 14:1991;421-451.
48. Morimoto K., Katayama K., Inoue K., Sato K. Effects of competitive and noncompetitive NMDA receptor antagonists on kindling and LTP. Pharm. Biochem. Behav. 40:1991;893-899.
49. Nawa H., Carnahan J., Gall C. BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur. J. Neurosci. 7:1995;1527-1535.
50. Olney J.W., Labruyere J., Price M.T. Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs. Science. 244:1989;1360-1362.
51. Olney J.W., Labruyere J., Wang G., Wozniak D.F., Price M.T., Sesma M.A. NMDA antagonist neurotoxicity: mechanism and prevention. Science. 254:1991;1515-1518.
52. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17:1997;3727-3738.
53. G. Paxinos, C. Watson, The Rat Brain in Stereotaxic Coordinates. Academic, Sydney.
54. Perlin J.B., Gerwin C.M., Panchision D.M., Vick R.S., Jakoi E.R., DeLorenzo R.J. Kindling produces long-lasting and selective changes in gene expression of hippocampal neurons. Proc. Natl. Acad. Sci. USA. 90:1993;1741-1745.
55. Pretel S., Applegate C.D., Piekut D.T. Activation of somatostatin-synthesizing neurons in the hippocampal formation through kindling-induced seizures. Hippocampus. 5:1995;40-51.
56. Racine R. Kindling: the first decade. Neurosurgery. 3:1978;234-252.
57. Rashid K., Van der Zee C.E.E.M., 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.
58. Sato K., Morimoto K., Okamoto M. Anticonvulsant action of a non-competitive antagonist of NMDA receptors (MK-801) in the kindling model of epilepsy. Brain Res. 463:1988;12-20.
59. Sharp J.W., Sagar S.M., Hisanaga K., Jasper P., Sharp F. The NMDA receptor mediates cortical induction of fos and fos-related antigens following cortical injury. Exp. Neurol. 109:1990;323-332.
60. Shin C., McNamara J.O., Morgan J.I., Curran T., Cohen D.R. Induction of c-fos mRNA expression by afterdischarge in the hippocampus of naive and kindled rats. J. Neurochem. 55:1990;1050-1055.
61. Shinoda H., Suzan Nadi N., Schwartz J.P. Alterations in somatostatin and proenkephalin mRNA in response to a single amygdaloid stimulation versus kindling. Mol. Brain Res. 11:1991;221-226.
62. Simonato M., Hosford D.A., Labiner D.M., Shin C., Mansbach H.H., McNamara J.O. Differential expression of immediate early genes in the hippocampus in the kindling model of epilepsy. Mol. Brain Res. 11:1991;115-124.
63. Sutula T., Koch J., Golarai G., Watanabe Y., McNamara J.O. NMDA receptor dependence of kindling and mossy fibre sprouting: evidence that the NMDA receptor regulates patterning of hippocampal circuits in the adult brain. J. Neurosci. 16:1996;7398-7406.
64. Szekely A.M., Barbaccia M.L., Alho H., Costa E. In primary cultures of cerebellar granule cells the activation of N-methyl-D-aspartate-sensitive glutamate receptors induces c-fos mRNA expression. Mol. Pharmacol. 35:1989;401-408.
65. Uemura Y., Kowall N.W., Beal M.F. Global ischemia induces NMDA receptor-mediated c-fos expression in neurons resistant to injury in gerbil hippocampus. Brain Res. 542:1991;343-347.
66. Valenzuela D.M., Maisonpierre P.C., Glass D.J., Rojas E., Nunez L., Kong Y., Gies D.R., Stitt T.N., Ip N.Y., Yancopoulos G.D. Alternative forms of rat trkC with different functional capabilities. Neuron. 10:1993;963-974.
67. 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.
68. Vezzani A., Wu H-Q., Moneta E., Samanin R. Role of N-methyl-D-aspartate-type receptors in the development and maintenance of hippocampal kindling in rats. Neurosci. Lett. 87:1988;63-68.
69. Wetmore C., Ernfors P., Persson H., Olson L. Localization of brain-derived neurotrophic factor mRNA to neurons in the brain by in situ hybridization. Exp. Neurol. 10:1990;141-152.
70. Williamson J.M., Lothman E.W. The effect of MK801 on kindled seizures: implications for use and limitations as an antiepileptic drug. Ann. Neurol. 26:1989;85-90.
71. Yan Q., Matheson C.R., Lopez O.T., Hawkins N., Rosenfeld R.D., Bennett L. Immunohistochemical study of the expression of brain-derived neurotrophic factor (BDNF) in the adult rat brain. Soc. Neurosci. Abstr. 20:1994;1306.
72. Yan Q., Rosenfeld R.D., Matheson C.R., Hawkins N., Lopez O.T., Bennett L., Welcher A.A. Expression of brain-derived neurotrophic factor (BDNF) protein in the adult rat CNS. Neuroscience. 78:1997;431-448.
73. Zafra F., Hengerer B., Leibrock J., Thoenen H., Lindholm D. Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9:1990;3545-3550.