Ionotropic and metabotropic glutamate receptor mediation of glucocorticoid-induced apoptosis in hippocampal cells and the neuroprotective role of synaptic N-methyl-D-aspartate receptors

Neuroscience

Volumn 121, Issue 1, 2003, Pages 123-131

  Lu, J ^a   Goula, D ^a   Sousa, N ^b   Almeida, O F X ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UNIVERSITY OF MINHO   (Portugal)

Author keywords

Glucocorticoids; Glutamate; Hippocampus; Ionotropic glutamate receptor; Metabotropic glutamate receptor; NMDA

Indexed keywords

ALPHA CYCLOPROPYL 4 PHOSPHONOPHENYLGLYCINE; ALPHA ETHYL 4 CARBOXYPHENYLGLYCINE; DEXAMETHASONE; DIZOCILPINE; DNA NUCLEOTIDYLEXOTRANSFERASE; GLUCOCORTICOID; IFENPRODIL; IONOTROPIC RECEPTOR; IONOTROPIC RECEPTOR ANTAGONIST; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR ANTAGONIST; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE; CELL PROTECTION; CELL STRUCTURE; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOTOXICITY; DNA STRAND BREAKAGE; DRUG MECHANISM; HIPPOCAMPUS; HISTOCHEMISTRY; MALE; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR BLOCKING;

EID: 0142091874     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00421-4     Document Type: Article

References (51)

1. Abraham I.M., Harkany T., Horvath K.M., Luiten P.G. Action of glucocorticoids on survival of nerve cells promoting neurodegeneration or neuroprotection? J Neuroendocrinol. 13:2001;749-760.
2. Ábrahám I., Juhász G., Kékesi K.A., Kovács K.J. Effect of intrahippocampal dexamethasone on the levels of amino acid transmitters and neuronal excitability. Brain Res. 733:1996;56-63.
3. Allen J.W., Vicini S., Faden A.I. Exacerbation of neuronal cell death by activation of group I metabotropic glutamate receptors role of NMDA receptors and arachidonic acid release . Exp Neurol. 169:2001;449-460.
4. Almeida O.F.X., Condé G.L., Crochemore C., Demeneix B.A., Fischer D., Hassan A.H., Meyer M., Holsboer F., Michaelidis T.M. Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. FASEB J. 14:2000;779-790.
5. Armanini M.P., Hutchins C., Stein B.A., Sapolsky R.M. Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Res. 532:1990;7-12.
6. Behl C., Lezoualc'h F., Trapp T., Widmann M., Skutella T., Holsboer F. Glucocorticoids enhance oxidative stress-induced cell death in hippocampal neurons in vitro. Endocrinology. 138:1997;101-106.
7. Bhargava A., Meijer O.C., Dallman M.F., Pearce D. Plasma membrane calcium pump isoform 1 gene expression is repressed by corticosterone and stress in rat hippocampus. J Neurosci. 20:2000;3129-3138.
8. Brandoli C., Sanna A., De Bernardi M.A., Follesa P., Brooker G., Mocchetti I. Brain-derived neurotrophic factor and basic fibroblast growth factor downregulate NMDA receptor function in cerebellar granule cells. J Neurosci. 18:1998;7953-7961.
9. Chenard B.L., Menniti F.S. Antagonists selective for NMDA receptors containing the NR2B subunit. Curr Pharm Des. 5:1999;381-404.
10. Choi D.W. Excitotoxicity on cultured cortical neurons. Ascher P., Christen Y., Choi D.W. Glutamate, cell death and memory. 1991;125-136 Springer-Verlag, Berlin.
11. Coyle J.T., Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 262:1993;689-695.
12. Crochemore, C (2000) Molecular mechanisms underlying corticosteroid influences on neural cell survival. PhD Thesis, Louis Pasteur University, Strasbourg, France.
13. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocrinol Rev. 19:1998;269-301.
14. Elliott E.M., Sapolsky R.M. Corticosterone impairs hippocampal neuronal calcium regulation-possible mediating mechanisms. Brain Res. 602:1993;84-90.
15. Glazner G.W., Mattson M.P. Differential effects of BDNG, ADNF9, and TNFalpha on levels of NMDA receptor subunits, calcium homeostasis, and neuronal vulnerability to excitotoxicity. Exp Neurol. 161:2000;442-452.
16. Goodman Y., Bruce A.J., Cheng B., Mattson M.P. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J Neurochem. 66:1996;1836-1844.
17. Gotti B., Duverger D., Bertin J., Carter C., Dupont R., Frost J., Gaudilliere B., MacKenzie E.T., Rousseau J., Scatton B., et al. Ifenprodil and SL 82.0715 as cerebral anti-ischemic agents I. Evidence for efficacy in models of focal cerebral ischemia . J Pharmacol Exp Ther. 247:1988;1211-1221.
18. Gould E., McEwen B.S., Tanapat P., Galea L.A., Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci. 17:1997;2492-2498.
19. Gursoy E., Cardounel A., Kalimi M. Pregnenolone protects mouse hippocampal (HT-22) cells against glutamate and amyloid beta protein toxicity. Neurochem Res. 26:2001;15-21.
20. Hardingham G.E., Fukunaga Y., Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci. 5:2002;405-414.
21. Hassan A.H., von Rosenstiel P., Patchev V.K., Holsboer F., Almeida O.F.X. Exacerbation of apoptosis in the dentate gyrus of the aged rat by dexamethasone and the protective role of corticosterone. Exp Neurol. 140:1996;43-52.
22. Heidinger V., Manzerra P., Wang X.Q., Strasser U., Yu S.P., Choi D.W., Behrens M.M. Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current mediation through the Pyk2/Src-family kinase pathway in cortical neurons . J Neurosci. 22:2002;5452-5461.
23. Joëls M. Corticosteroid actions in the hippocampus. J Neuroendocrinol. 13:2001;657-669.
24. Johnson E.A., O'Callaghan J.P., Miller D.B. Chronic treatment with supraphysiological levels of corticosterone enhances D-MDMA-induced dopaminergic neurotoxicity in the C57BL/6J female mouse. Brain Res. 933:2002;130-138.
25. Kemp J.A., McKernan R.M. NMDA receptor pathways as drug targets. Nat Neurosci. 5:(Suppl.):2002;1039-1042.
26. 2+ conductances relevance to brain aging . Proc Natl Acad Sci USA. 89:1992;8527-8531.
27. Li B., Chen N., Luo T., Otsu Y., Murphy T.H., Raymond L.A. Differential regulation of synaptic and extra-synaptic NMDA receptors. Nat Neurosci. 5:2002;833-834.
28. Li J.H., Wang Y.H., Wolfe B.B., Krueger K.E., Corsi L., Stocca G., Vicini S. Developmental changes in localization of NMDA receptor subunits in primary cultures of cortical neurons. Eur J Neurosci. 10:1998;1704-1715.
29. Linthorst A.C.E., Flachskamm C., Barden N., Holsboer F., Reul J.M.H.M. Glucocorticoid receptor impairment alters CNS responses to a psychological stressor an in vivo microdialysis study in transgenic mice . Eur J Neurosci. 12:2000;283-291.
30. Lipton S.A., Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med. 330:1994;613-622.
31. Maiese K., Ahmad I., TenBroeke M., Gallant J. Metabotropic glutamate receptor subtypes independently modulate neuronal intracellular calcium. J Neurosci Res. 55:1999;472-485.
32. Marini A.M., Rabin S.J., Lipsky R.H., Mocchetti I. Activity-dependent release of brain-derived neurotrophic factor underlies the neuroprotective effect of N-methyl-D-aspartate. J Biol Chem. 273:1998;29394-29399.
33. Masters J.N., Finch C.E., Sapolsky R.M. Glucocorticoid endangerment of hippocampal neurons does not involve deoxyribonucleic acid cleavage. Endocrinology. 124:1989;3083-3088.
34. McEwen B.S. The neurobiology of stress from serendipity to clinical relevance . Brain Res. 886:2000;172-189.
35. Miskevich F., Lu W., Lin S.Y., Constantine-Paton M. Interaction between metabotropic and NMDA subtypes of glutamate receptors in sprout suppression at young synapses. J Neurosci. 22:2002;226-238.
36. Moghaddam B., Bolinao M.L., Stein-Behrens B., Sapolsky R. Glucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res. 655:1994;251-254.
37. Nair S.M., Werkman T.R., Craig J., Finnell R., Joëls M., Eberwine J.H. Corticosteroid regulation of ion channel conductances and mRNA levels in individual hippocampal CA1 neurons. J Neurosci. 18:1998;2685-2696.
38. Nedergaard M., Takano T., Hansen A.J. Beyond the role of glutamate as a neurotransmitter. Nat Rev Neurosci. 3:2002;748-755.
39. Otani S., Daniel H., Takita M., Crepel F. Long-term depression induced by postsynaptic group II metabotropic glutamate receptors linked to phospholipase C and intracellular calcium rises in rat prefrontal cortex. J Neurosci. 22:2002;3434-3444.
40. Pin J.P., Duvoisin R. The metabotropic glutamate receptors structure and functions . Neuropharmacology. 34:1995;1-26.
41. Resink A., Villa M., Benke D., Hidaka H., Mohler H., Balazs R. Characterization of agonist-induced down-regulation of NMDA receptors in cerebellar granule cell cultures. J Neurochem. 66:1996;369-377.
42. Riccio A., Ginty D.D. What a privilege to reside at the synapse NMDA receptor signaling to CREB . Nat Neurosci. 5:2002;389-390.
43. Rossi D.J., Oshima T., Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature. 403:2000;316-321.
44. Roy M., Sapolsky R.M. The exacerbation of hippocampal excitotoxicity by glucocorticoids is not mediated by apoptosis. Neuroendocrinology. 77:2003;24-31.
45. Sapolsky R.M. The possibility of neurotoxicity in the hippocampus in major depression a primer on neuron death . Biol Psychiatry. 48:2000;755-765.
46. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 21:2000;55-89.
47. Snyder E.M., Philpot B.D., Huber K.M., Dong X., Fallon J.R., Bear M.F. Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat Neurosci. 4:2001;1079-1085.
48. Sousa N., Almeida O.F.X. Corticosteroids sculptors of the hippocampal formation . Rev Neurosci. 13:2002;59-84.
49. Stocca G., Vicini S. Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol. 507:(Pt 1):1998;13-24.
50. Tovar K.R., Westbrook G.L. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci. 19:1999;4180-4188.
51. Weiland N.G., Orchinik M., Tanapat P. Chronic corticosterone treatment induces parallel changes in N-methyl-D-aspartate receptor subunit messenger RNA levels and antagonist binding sites in the hippocampus. Neuroscience. 78:1997;653-662.