Kainate induces the expression of the DNA damage-inducible gene, GADD45, in the rat brain

Neuroscience

Volumn 81, Issue 3, 1997, Pages 707-720

  Zhu, R L ^a   Graham, S H ^a   Jin, K ^a   Stetler, R A ^a   Simon, R P ^a   Chen, J ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; DNA damage; DNA repair; Epilepsy; Gene expression

Indexed keywords

KAINIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; DNA DAMAGE; DNA REPAIR; EPILEPSY; EXCISION; GENE EXPRESSION; GENE INDUCTION; IN SITU HYBRIDIZATION; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; DNA DAMAGE; GENE EXPRESSION REGULATION; GENETIC TECHNIQUES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KAINIC ACID; MALE; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; STAINING AND LABELING;

EID: 0031587272     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00205-4     Document Type: Article

References (64)

1. Ames B. N., Shigenaga M. K., Gold L. S. DNA lesions, inducible DNA repair, and cell division: three key factors in mutagenesis and carcinogenesis. Environ. Health Perspect. 101(Suppl. 5):1993;35-44.
2. Ames B. N., Shigenaga M. K., Hagen T. M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. natn. Acad. Sci. U.S.A. 90:1993;7915-7922.
3. Ayyagari R., Impellizzeri K. J., Yoder B. L., Gary S. L., Burgers P. M. A mutational analysis of the yeast proliferating cell nuclear antigen indicates distinct roles in DNA replication and DNA repair. Molec. cell. Biol. 15:1995;4420-4429.
4. Beilharz E. J., Williams C. E., Dragunow M., Sirimanne E. S., Gluckman P. D. Mechanisms of delayed cell death following hypoxic-ischemic injury in the immature rat: evidence for apoptosis during selective neuronal loss. Brain Res. Molec. Brain Res. 29:1995;1-14.
5. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 14:1985;375-403.
6. Ben-Ari Y., Tremblay E., Ottersen O. P. Injections of kainic acid into the amygdaloid complex of the rat: an electrographic, clinical and histological study in relation to the pathology of epilepsy. Neuroscience. 5:1980;515-528.
7. Ben-Ari Y., Tremblay E., Riche D., Ghilini G., Naquet R. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience. 6:1981;1361-1391.
8. Bugra K., Pollard H., Charton G., Moreau J., Ben-Ari Y., Khrestchatisky M. aFGF, bFGF and FLG mRNAs show distinct patterns of induction in the hippocampus following kainate-induced seizures. Eur. J. Neurosci. 6:1994;58-66.
9. Charriaut-Marlangue C., Margaill I., Represa A., Popovici T., Plotkine M., Ben-Ari Y. Apoptosis and necrosis after reversible focal ischemia: an in situ DNA fragmentation analysis. J. Cereb. Blood Flow Metab. 16:1996;186-194.
10. Chen J., Marsh T., Zhang J. S., Graham S. H. Expression of cyclooxygenase 2 in rat brain following kainate treatment. NeuroReport. 6:1995;245-248.
11. Chen J., Zhu R. L., Nakayama M., Kawaguchi K., Jin K., Stetler R. A., Simon R. P., Graham S. H. The apoptosis-effector gene, bax, is expressed in vulnerable hippocampal CA1 neurons following global ischemia. J. Neurochem. 67:1996;64-71.
12. Choi D. W. Glutamate neurotoxicity and diseases of the nervous system. Neuron. 1:1988;623-634.
13. Cosi C., Suzuki H., Milani D., Facci L., Menegazzi M., Vantini G., Kanai Y., Skaper S. D. Poly(ADP-ribose) polymerase: early involvement in glutamate-induced neurotoxicity in cultured cerebellar granule cells. J. Neurosci. Res. 39:1994;38-46.
14. Coyle J. T., Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 262:1993;689-695.
15. Dawson V. L., Dawson T. M., Bartley D. A., Uhl G. R., Snyder S. H. Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13:1993;2651-2661.
16. Didier M., Bursztajn S., Adamec E., Passani L., Nixon R. A., Coyle J. T., Wei J. Y., Berman S. A. DNA strand breaks induced by sustained glutamate excitotoxicity in primary neuronal cultures. J. Neurosci. 16:1996;2238-2250.
17. 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.
18. Fornace A. J. Jr. Mammalian genes induced by radiation; activation of genes associated with growth control. A. Rev. Genet. 26:1992;507-526.
19. Fornace A. J. Jr., Alamo I. Jr., Hollander M. C. DNA damage-inducible transcripts in mammalian cells. Proc. natn. Acad. Sci. U.S.A. 85:1988;8800-8804.
20. Fornace A. J. Jr., Nebert D. W., Hollander M. C., Luethy J. D., Papathanasiou M., Fargnoli J., Holbrook N. J. Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Molec. cell. Biol. 9:1989;4196-4203.
21. Fornace A. J., Jr, Papathanasiuo M. A., Hollander M. C., Farhangi E., Alamo I. J., Beckett M. A. and Weichselbaum R. R. (1991) Altered regulation of a human gene induced by ionizing radiation in tumor cell lines. In Radiation Research (eds Chapman J. D., Dewey W. C. and Whitmore G. F.), p. 213. Academic, San Diego.
22. Fornace A. J. Jr., Zmudzka B., Hollander M. C., Wilson S. H. Induction of beta-polymerase mRNA by DNA-damaging agents in Chinese hamster ovary cells. Molec. cell. Biol. 9:1989;851-853.
23. Fritz G., Tano K., Mitra S., Kaina B. Inducibility of the DNA repair gene encoding O6-methylguanine-DNA methyltransferase in mammalian cells by DNA-damaging treatments. Molec. cell. Biol. 11:1991;4660-4668.
24. Graham S. H., Chen J., Stetler R. A., Zhu R. L., Jin K. L., Simon R. P. Expression of the proto-oncogene bcl-2 is increased in rat brain following kainate-induced seizures. Restor. Neurol. Neurosci. 9:1996;243-250.
25. Hall P. A., Kearsey J. M., Coates P. J., Norman D. G., Warbrick E., Cox L. S. Characterisation of the interaction between PCNA and Gadd45. Oncogene. 10:1995;2427-2433.
26. Hollander M. C., Alamo I., Jackman J., Wang M. G., McBride O. W., Fornace A. J. Jr. Analysis of the mammalian GADD45 gene and its response to DNA damage. J. biol. Chem. 268:1993;24385-24393.
27. Holley J. A., Janssen Y. M., Mossman B. T., Taatjes D. J. Increased manganese superoxide dismutase protein in type II epithelial cells of rat lungs after inhalation of crocidolite asbestos or cristobalite silica. Am. J. Path. 141:1992;475-485.
28. Humpel C., Lippoldt A., Chadi G., Ganten D., Olson L., Fuxe K. Fast and widespread increase of basic fibroblast growth factor messenger RNA and protein in the forebrain after kainate-induced seizures. Neuroscience. 57:1993;913-922.
29. Jackman J., Alamo I. Jr., Fornace A. J. Jr. Genotoxic stress confers preferential and coordinate messenger RNA stability on the five GADD genes. Cancer Res. 54:1994;5656-5662.
30. Janssen Y. M., Marsh J. P., Absher M. P., Hemenway D., Vacek P. M., Leslie K. O., Borm P. J. and Mossman B. T. (1992) Expression of antioxidant enzymes in rat lungs after inhalation of asbestos or silica. J. biol. Chem. 267, 10,625-10,630.
31. Janssen Y. M., Van Houten B., Borm P. J., Mossman B. T. Cell and tissue responses to oxidative damage. Lab. Invest. 69:1993;261-274.
32. Jin K. L., Chen J., Kawaguchi K., Zhu R. L., Stetler R. A., Simon R. P., Graham S. H. Focal ischemia induces expression of the DNA damage-inducible gene GADD45 in the rat brain. NeuroReport. 7:1996;1797-1802.
33. Kastan M. B., Zhan Q., el-Deiry W. S., Carrier F., Jacks T., Walsh W. V., Plunkett B. S., Vogelstein B., Fornace A. J. Jr. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell. 71:1992;587-597.
34. Lau C. C., Pardee A. B. Mechanism by which caffeine potentiates lethality of nitrogen mustard. Proc. natn. Acad. Sci. U.S.A. 79:1982;2942-2946.
35. Lowe S. W., Schmitt E. M., Smith S. W., Osborne B. A., Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature. 362:1993;847-849.
36. MacManus J. P., Buchan A. M., Hill I. E., Rasquinha I., Preston E. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci. Lett. 164:1993;89-92.
37. Meldrum B. Possible therapeutic applications of antagonists of excitatory amino acid neurotransmitters. Clin. Sci. 68:1985;113-122.
38. 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.
39. Nitatori T., Sato N., Waguri S., Karasawa Y., Araki H., Shibanai K., Kominami E., Uchiyama Y. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15:1995;1001-1011.
40. Nitecka L., Tremblay E., Charton G., Bouillot J. P., Berger M. L., Ben-Ari Y. Maturation of kainic acid seizure-brain damage syndrome in the rat. II. Histopathological sequelae. Neuroscience. 13:1984;1073-1094.
41. Okada M., Sakaguchi T., Kawasaki K. Proliferating cell nuclear antigen in neurones - induction by UV irradiation. NeuroReport. 7:1996;1770-1772.
42. Olney J. W., Rhee V., Ho O. L. Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res. 77:1974;507-512.
43. Papathanasiou M. A., Kerr N. C., Robbins J. H., McBride O. W., Alamo I. Jr., Barrett S. F., Hickson I. D., Fornace A. J. Jr. Induction by ionizing radiation of the gadd45 gene in cultured human cells: lack of mediation by protein kinase C. Molec. cell. Biol. 11:1991;1009-1016.
44. Pollard H., Cantagrel S., Charriaut-Marlangue C., Moreau J., Ben-Ari Y. Apoptosis associated DNA fragmentation in epileptic brain damage. NeuroReport. 5:1994;1053-1055.
45. Pollard H., Charriaut-Marlangue C., Cantagrel S., Represa A., Robain O., Moreau J., Ben-Ari Y. Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience. 63:1994;7-18.
46. Popovici T., Represa A., Crepel V., Barbin G., Beaudoin M., Ben-Ari Y. Effects of kainic acid-induced seizures and ischemia on c-fos-like proteins in rat brain. Brain Res. 536:1990;183-194.
47. Portera-Cailliau C., Hedreen J. C., Price D. L., Koliatsos V. E. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15:1995;3775-3787.
48. Rothman S. M., Olney J. W. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19:1986;105-111.
49. 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. natn. Acad. Sci. U.S.A. 85:1988;7795-7799.
50. Sakhi S., Bruce A., Sun N., Tocco G., Baudry M., Schreiber S. S. p53 induction is associated with neuronal damage in the central nervous system. Proc. natn. Acad. Sci. U.S.A. 91:1994;7525-7529.
51. Sambrook J., Fritsch E. F. and Maniatis T. (1989) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
52. Satoh M. S., Lindahl T. Enzymatic repair of oxidative DNA damage. Cancer Res. 54:1994;1899s-1901s.
53. Schraufstatter I. U., Hyslop P. A., Hinshaw D. B., Spragg R. G., Sklar L. A., Cochrane C. G. Hydrogen peroxide-induced injury of cells and its prevention by inhibitors of poly(ADP-ribose) polymerase. Proc. natn. Acad. Sci. U.S.A. 83:1986;4908-4912.
54. Schreiber S. S., Tocco G., Najm I., Finch C. E., Johnson S. A., Baudry M. Absence of c-fos induction in neonatal rat brain after seizures. Neurosci. Lett. 136:1992;31-35.
55. Schwob J. E., Fuller T., Price J. L., Olney J. W. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience. 5:1980;991-1014.
56. Shivji K. K., Kenny M. K., Wood R. D. Proliferating cell nuclear antigen is required for DNA excision repair. Cell. 69:1992;367-374.
57. 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 precedes programmed cell death in vivo. Nature. 363:1993;166-169.
58. Smith M. L., Chen I. T., Zhan Q., Bae I., Chen C. Y., Gilmer T. M., Kastan M. B., PM O. C., Fornace A. J. Jr. Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science. 266:1994;1376-1380.
59. Stetler R. A., Kawaguchi K., Jin K. L., Zhu R. L., Graham S. H., Greenberg D. A., Chen J. The expression of the proliferating cell nuclear antigen mRNA and protein is upregulated in the rat hippocampus following global ischemia. Soc. Neurosci. Abstr. 22:1996;1670.
60. Tominaga T., Kure S., Narisawa K., Yoshimoto T. Endonuclease activation following focal ischemic injury in the rat brain. Brain Res. 608:1993;21-26.
61. Wood K. A., Youle R. J. The role of free radicals and p53 in neuron apoptosis in vivo. J. Neurosci. 15:1995;5851-5857.
62. Yoshida T., Schneider E. L., Mori N. Cloning of the rat Gadd45 cDNA and its mRNA expression in the brain. Gene. 151:1994;253-255.
63. Zhan Q., Bae I., Kastan M. B., Fornace A. J. Jr. The p53-dependent gamma-ray response of GADD45. Cancer Res. 54:1994;2755-2760.
64. Zhang J., Dawson V. L., Dawson T. M., Snyder S. H. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science. 263:1994;687-689.