NMDA receptor overstimulation triggers a prolonged wave of immediate early gene expression: Relationship to excitotoxicity

Experimental Neurology

Volumn 144, Issue 2, 1997, Pages 406-415

  Shan, Yuan ^a   Carlock, Leon R ^a   Walker, Paul D ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIZOCILPINE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; QUINOLINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; IMMEDIATE EARLY GENE; MALE; NONHUMAN; NORTHERN BLOTTING; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; RNA ANALYSIS;

EID: 18344415286     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1997.6427     Document Type: Article

References (93)

1. Aronin N., Chase K., Sagar S. M., Sharp F. R., DiFiglia M. N-methyl-D-aspartate receptor activation in the neostriatum increases c-fos and fos-related antigens selectively in medium-sized neurons. Neuroscience. 44:1991;409-420.
2. Bading H., Ginty D. G., Greenberg M. E. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science. 260:1993;181-186.
3. Bakker M. H. M., Foster A. C. An investigation of the mechanisms of delayed neurodegeneration caused by direct injection of quinolinate into the rat striatumin vivo. Neuroscience. 42:1991;387-395.
4. Beal M. F., Kowall N. W., Ellison D. W., Mazurek M. F., Swartz K. J., Martin J. B. Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid. Nature. 321:1986;168-170.
5. Beal M. F. Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann. Neurol. 31:1992;119-130.
6. Berretta S., Robertson H. A., Graybiel A. M. Dopamine and glutamate agonists stimulate neuron-specific expression of fos-like protein in the striatum. J. Neurophysiol. 68:1992;767-777.
7. Bhat R. V., Worley P. F., Cole A. J., Baraban J. M. Activation of the zinc finger encoding gene krox-20 in adult rat brain: comparison with zif/268. Mol. Brain Res. 13:1992;263-266.
8. Bhat R. V., Baraban J. M. Activation of transcription factor genes in striatum by cocaine: Role of both serotonin and dopamine systems. J. Pharmacol. Exp. Ther. 267:1993;496-505.
9. Cenci M. A., Campbell K., Wictorin K., Bjorklund A. Striatal c-fos induction by cocaine or apomorphine occurs preferentially in output neurons projecting to the substantia nigra in the rat. Eur. J. Neurosci. 4:1992;376-380.
10. Choi D. W. Ionic dependence of glutamate neurotoxicity. J. Neurosci. 7:1987;369-379.
11. Choi D. W. Glutamate neurotoxicity and diseases of the nervous system. Neuron. 1:1988;623-634.
12. Christy B. A., Lau L. F., Nathans D. A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with "zinc finger" sequences. Proc. Natl. Acad. Sci. USA. 85:1988;7857-7861.
13. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
14. 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.
15. Cole A. J., Bhat R. V., Patt C., Worley P. F., Baraban J. M. D1 dopamine receptor activation of multiple transcription factors in rat striatum. J. Neurochem. 58:1992;1420-1426.
16. Curran T., Peters G., Van Beveren C., Teich N. M., Verma I. M. FBJ murine osteosarcoma virus: Identification and molecular cloning of biologically active proviral DNA. J. Virol. 44:1982;674-682.
17. Curran T., MacConnell W. P., van Staaten F., Verma I. M. Structure of the FBJ murine osteosarcoma virus genome: Molecular cloning of its associated helper virus and the cellular homolog of the v-fos gene from mouse and human cells. Mol. Cell. Biol. 3:1983;914-921.
18. Dirnagl U., Tanabe J., Pulsinelli W. Pre- and post-treatment with MK-801 but not pretreatment alone reduces neocortical damage after focal cerebral ischemia in the rat. Brain Res. 527:1990;62-68.
19. Dragunow M., Robertson H. A. Generalized seizures induce c-fos protein(s) in mammalian neurons. Neurosci. Lett. 82:1987;157-161.
20. Dragunow M., Young D., Hughes P., MacGibbon G., Lawlor P., Singleton K., Sirimanne E., Beilharz E., Gluckman P. Is c-jun involved in nerve cell death following status epilepticus and hypoxic-ischaemic brain injury? Mol. Brain Res. 18:1993;347-352.
21. Dragunow M., Beilharz E., Sirimanne E., Lawlor P., Williams C., Bravo R., Gluckman P. Immediate early gene protein expression in neurons undergoing delayed death, but not necrosis, following hypoxic-ischaemic injury to the young rat brain. Mol. Brain Res. 25:1994;19-33.
22. Dubinsky J. M. Intracellular calcium levels during the period of delayed excitotoxicity. J. Neurosci. 13:1993;623-631.
23. Dubinsky J. M., Rothman S. M. Intracellular calcium concentrations during "chemical hypoxia" and excitotoxic neuronal injury. J. Neurosci. 11:1991;2545-2551.
24. Estus S., Zaks W. J., Freeman R. S., Gruda M., Bravo R., Johnson E. M. Jr. Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127:1994;1717-1727.
25. Evan G. I., Wyllie A. H., Gilbert C. S., Littlewood T. D., Land H., Brooks M., Waters C. M., Penn L. Z., Hancock D. C. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 69:1992;119-128.
26. Foster A. C., Gill R., Woodruff G. N. Neuroprotective effects of MK-801in vivo: J. Neurosci. 8:1988;4745-4754.
27. Frandsen A., Schousboe A. Excitatory amino acid-mediated cytotoxicity and calcium homeostasis in cultured neurons. J. Neurochem. 60:1993;1202-1211.
28. Freeman R. S., Estus S., Johnson E. M. Jr. Analysis of cell cycle-related gene expression in postmitotic neurons: Selective induction of cyclin D1 during programmed cell death. Neuron. 12:1994;343-355.
29. Fu L., Beckstead R. M. Cortical stimulation induces fos expression in striatal neurons. Neuroscience. 46:1992;329-334.
30. Garthwaite G., Garthwaite J. Neurotoxicity of excitatory amino acid receptor agonists in rat cerebellar slices: dependence on calcium concentration. Neurosci. Lett. 66:1986;193-198.
31. Gass P., Herdegen T., Bravo R., Kiessling M. Induction of immediate early gene encoded proteins in the rat hippocampus after bicuculline-induced seizures: differential expression of krox-24, fos and jun proteins. Neuroscience. 48:1992;315-324.
32. Gass P., Herdegen T., Bravo R., Kiessling M. Induction and suppression of immediate early genes in specific rat brain regions by the non-competitive N-methyl-D-aspartate receptor antagonist MK-801. Neuroscience. 53:1993;749-758.
33. Gass P., Spranger M., Herdegen T., Bravo R., Kock P., Hacke W., Kiessling M. Induction of FOS and JUN proteins after focal ischemia in the rat: differential effect of the N-methyl-D-aspartate receptor antagonist MK-801. Acta Neuropathol. 84:1992;545-553.
34. Graybiel A. M., Moratalla R., Robertson H. A. Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc. Natl. Acad. Sci. USA. 87:1991;6912-6916.
35. Ham J., Babij C., Whitfield J., Pfarr C. M., Lallemand D., Yaniv M., Rubin L. L. A c-jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron. 14:1995;927-939.
36. Hanley M. R. Proto-oncogenes in the nervous system. Neuron. 1:1988;175-182.
37. Hartley D. M., Choi D. W. Delayed rescue of N-methyl-D-aspartate receptor-mediated neuronal injury in cortical culture. J. Pharmacol. Exp. Therap. 250:1989;752-758.
38. Herdegen T., Brecht S., Mayer B., Leah J., Kummer W., Bravo R., Zimmermann M. Long-lasting expression of JUN and KROX transcription factors and nitric oxide synthase in intrinsic neurons of the rat brain following axotomy. J. Neurosci. 13:1993;4130-4145.
39. Hope B. T., Ketz M. B., Duman R. S., Nestler E. J. Chronic electroconvulsive seizure (ECS) treatment results in expression of a long-lasting AP-1 complex in brain with altered composition and characteristics. J. Neurosci. 14:1994;4318-4328.
40. 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.
41. Hunt C., Morimoto R. Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc. Natl. Acad. Sci. USA. 82:1985;6455-6459.
42. Johnston H. M., Morris B. J. Induction of c-fos gene expression is not responsible for increased proenkephalin mRNA levels in the hippocampal dentate gyrus following NMDA stimulation. Mol. Brain Res. 25:1994;147-150.
43. Kasof G. M., Mandelzys A., Maika S. D., Hammer R. E., Curran T., Morgan J. I. Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate-early gene response in c-fos-lacZ transgenic rats. J. Neurosci. 15:1995;4238-4249.
44. Krause J. E., Chirgwin J. M., Carter M. S., Xu Z. S., Hershey A. D. Three rat preprotachykinin mRNAs encode the neuropeptides substance P and neurokinin A. Proc. Natl. Acad. Sci. USA. 84:1987;881-885.
45. Lau L. F., Nathans D. Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proc. Natl. Acad. Sci. USA. 84:1987;1182-1186.
46. Lei S. Z., Zhang D., Abele A. E., Lipton S. A. Blockade of NMDA receptor-mediated mobilization of intracellular Ca+2 prevents neurotoxicity. Brain Res. 598:1992;196-202.
47. Lerea L. S., McNamara J. O. Ionotropic glutamate receptor subtypes activate c-fos transcription by distinct calcium-requiring intracellular signaling pathways. Neuron. 10:1993;31-41.
48. Lerea L. S., Butler L. S., McNamara J. O. NMDA and non-NMDA receptor-mediated increase of c-fos mRNA in dentate gyrus neurons involves calcium influx via different routes. J. Neurosci. 12:1992;2973-2981.
49. 2/1C. Neuroscience. 53:1993;457-463.
50. Li B. H., Rowland N. E. Dexfenfluramine induces fos-like immunoreactivity in discrete brain regions in rats. Brain Res. Bull. 31:1993;43-48.
51. Lucas D. R., Newhouse J. P. The toxic effect of sodium L-glutamate on the inner layers of the retina. Arch. Ophthalmol. 58:1957;193-201.
52. Meldrum B., Garthwaite J. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol. Sci. 11:1990;379-387.
53. McDonald J. W., Silverstein F. S., Johnston M. V. MK-801 protects the neonatal brain from hypoxic-ischemic damage. Eur. J. Pharmacol. 140:1987;359-361.
54. Micheals R. L., Rothman S. M. GLU neurotoxicity in vitro: antagonist pharmacology and intracellular calcium concentrations. J. Neurosci. 10:1990;283-292.
55. Miller A. D., Curran T., Verma I. M. c-fos protein can induce cellular transformation: a novel mechanism of activation of a cellular oncogene. Cell. 36:1984;51-60.
56. Moratalla R., Vickers E. A., Robertson H. A., Cochran B. H., Graybiel A. M. Coordinate expression of c-fos and jun-B is induced in the rat striatum by cocaine. J. Neurosci. 13:1993;423-433.
57. Morgan J. I., Cohen D. R., Hempstead J. L., Curran T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science. 237:1987;192-197.
58. Murphy T. H., Worley P. F., Baraban J. M. L-type voltage-sensitive calcium channels mediate synaptic activation of immediate early genes. Neuron. 7:1991;625-635.
59. Olney J. W., Sharpe L. G. Brain lesions in an infant rhesus monkey treated with monosodium glutamate. Science. 166:1969;386-388.
60. 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.
61. Olney J. W., Price M. T., Samson L., Labruyere J. The role of specific ions in glutamate neurotoxicity. Neurosci. Lett. 65:1986;76-71.
62. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 1986;Academic Press, New York.
63. Pennypacker K. R., Thai L., Hong J.-S., McMillian M. K. Prolonged expression of AP-1 transcription factors in the rat hippocampus after systemic kainate treatment. J. Neurosci. 14:1994;3998-4006.
64. Raghupathi R., McIntosh T. K. Regionally and temporally distinct patterns of induction of c-fos, c-jun and junB mRNAs following experimental brain injury in the rat. Mol. Brain Res. 37:1996;134-144.
65. Randall R. D., Thayer S. A. Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J. Neurosci. 12:1992;1882-1895.
66. Reiner A., Anderson K. D. The patterns of neurotransmitter and neuropeptide co-occurrence among striatal projection neurons: Conclusions based on recent findings. Brain Res. Rev. 15:1990;251-265.
67. Richard D., Rivest S., Rivier C. The 5-hydroxytryptamine agonist fenfluramine increases fos-like immunoreactivity in the brain. Brain Res. 594:1992;131-137.
68. Rothman S. M. The neurotoxicity of excitatory amino acids is produced by passive chloride influx. J. Neurosci. 5:1985;1483-1489.
69. Ryder K., Nathans D. Induction of protooncogene c-jun by serum growth factors. Proc. Natl. Acad. Sci. USA. 85:1988;8464-8467.
70. Ryder K., Lau L. F., Nathans D. A gene activated by growth factors is related to the oncogene v-jun. Proc. Natl. Acad. Sci. USA. 85:1986;1487-1491.
71. Saffen D. W., Cole A. J., Worley P. F., Christy B. A., Ryder K., Baraban J. M. Convulsant-induced increase in transcription factor messenger RNAs in rat brain. Proc. Natl. Acad. Sci. USA. 85:1988;7795-7799.
72. Schwarcz R., Whetsell W. O., Mangano R. M. Quinolinic acid: an endogenous metabolite that produces axon-sparing lesions in rat brain. Science. 219:1983;316-317.
73. Sharp F. R., Sagar S. M., Hicks K., Lowenstein D., Hisanaga K. c-fos mRNA, fos, and fos-related antigen induction by hypertonic saline and stress. J. Neurosci. 11:1991;2321-2331.
74. Sheng M., Greenberg M. E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron. 4:1990;477-485.
75. Sheng M., McFadden G., Greenberg M. E. Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron. 4:1990;571-582.
76. Smeyne R. J., Vendrell M., Hayward M., Baker S. J., Miao G. G., Schilling K., Robertson L. M., Curran T., Morgan J. I. Continuous c-fos expression presedes programmed cell death in vivo. Nature. 363:1993;166-169.
77. Snyder-Keller A. M. Striatal c-fos induction by drugs and stress in neonatally dopamine-depleted rats given nigral transplants: importance of NMDA activation and relevance to sensitization phenomena. Exp. Neurol. 113:1991;155-165.
78. Sonnenberg J. L., Mitchelmore C., Macgregor-Leon P. F., Hempstead J., Morgan J. I., Curran T. Glutamate receptor agonists increase the expression of fos, fra, and AP-1 DNA binding activity in the mammalian brain. J. Neurosci. Res. 24:1989;72-80.
79. Szekely A. M., Costa E. M., Grayson D. R. Transcriptional program coordination by N-methyl-D-aspartate-sensitive glutamate receptor stimulation in primary cultures of cerebellar neurons. Mol. Pharmacol. 38:1990;624-633.
80. +2. Brain Res. 607:1993;319-323.
81. 2+. Neuron. 11:1993;221-235.
82. Vaccarino F. M., Hayward M. D., Nestler E. J., Duman R. S., Tallman J. F. Differential induction of immediate early genes by excitatory amino acid receptor types in primary cultures of cortical and striatal neurons. Mol. Brain Res. 12:1992;233-241.
83. Virgili M., Migani P., Contestabile A., Barnabei O. Protection from kainic acid neuropathological syndrome by NMDA receptor antagonists: effect of MK-801 and CGP 39551 on neurotransmitter and glial markers. Neuropharmacol. 31:1992;469-474.
84. Walker P. D., Carlock L. R. Immediate early gene activation during the initial phases of the excitotoxic cascade. J. Neurosci. Res. 36:1993;588-595.
85. Walker P. D., Carlock L. R. Timing the excitotoxic induction of heat shock protein 70 transcription. NeuroReport. 4:1993;699-702.
86. Wang Z. Q., Ovitt C., Grigoriadis A. E., Steinlein U. M., Ruther U., Wagner E. F. Bone and haematopoietic defects in mice lacking c-fos. Nature. 360:1992;741-745.
87. Wessel T. C., Joh T. H., Volpe B. T. In situ hybridization analysis of c-fos and c-jun expression in the rat brain following transient forebrain ischemia. Brain Res. 567:1991;231-240.
88. Wieloch T. Hypoglycemia-induced neuronal damage prevented by an N-methyl-D-aspartate antagonist. Science. 230:1985;681-683.
89. Wong E. H. F., Kemp J. A., Priestly T., Knight A. R., Woodruff G. N., Iversen L. L. The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc. Natl. Acad. Sci. USA. 83:1986;7104-7108.
90. Woodburn V. L., Hayward N. J., Poat J. A., Woodruff G. N., Hughes J. The effect of dizocilpine and enadoline on immediate early gene expression in the gerbil global ischaemia model. Neuropharmacology. 32:1993;1047-1059.
91. Woodburn V. L., Oles R., Woodruff G. N., Hughes J. Anticonvulsant agents, dizocilpine maleate, enadoline and HA 966 have different effects on N-methyl-DL-aspartate-induced immediate early gene induction in mice. Neuroscience. 56:1993;703-709.
92. Worley P. F., Cole A. F., Saffen D. W., Baraban J. M. Regulation of immediate early genes in brain: role of NMDA receptor activation. Prog. Brain Res. 86:1990;277-285.
93. Yoshikawa K., Williams C., Sabol S. L. Rat brain preproenkephalin mRNA: cDNA cloning, primary structure, and distribution in the central nervous system. J. Biol. Chem. 259:1984;14301-14308.