Mechanisms leading to disseminated apoptosis following NMDA receptor blockade in the developing rat brain

Neurobiology of Disease

Volumn 16, Issue 2, 2004, Pages 440-453

  Hansen, Henrik H ^a,b   Briem, Tim ^a   Dzietko, Mark ^a   Sifringer, Marco ^a   Voss, Alexander ^a   Rzeski, Wojciech ^c   Zdzisinska, Barbara ^c   Thor, Friederike ^d   Heumann, Rolf ^d   Stepulak, Andrzej ^a,e   Bittigau, Petra ^a   Ikonomidou, Chrysanthy ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e MEDICAL UNIVERSITY OF LUBLIN   (Poland)

Author keywords

Apoptosis; BDNF; CaMKIV; CREB; Development; ERK; MK801; Neurodegeneration; NMDA receptor; Ras

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIZOCILPINE; MITOGEN ACTIVATED PROTEIN KINASE 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEUROTROPHIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; CONTROLLED STUDY; ENZYME ACTIVITY; MOLECULAR MECHANICS; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RAT STRAIN; SIGNAL TRANSDUCTION; SUPPLEMENTATION;

AGE FACTORS; ANIMALS; APOPTOSIS; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DIZOCILPINE MALEATE; DOWN-REGULATION; EXCITATORY AMINO ACID ANTAGONISTS; GENE EXPRESSION; GYRUS CINGULI; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; NERVE DEGENERATION; NERVE GROWTH FACTORS; NEURONS; PROTO-ONCOGENE PROTEINS C-BCL-2; RAS PROTEINS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 2942532414     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.03.013     Document Type: Article

References (54)

1. Aamodt S.M., Constantine-Paton M. The role of neural activity in synaptic development and its implications for adult brain function. Adv. Neurol. 79:1999;133-144
2. Agmon A., O'Dowd D.K. NMDA receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition. J. Neurophysiol. 68:1992;345-349
3. Bayer S.A., Altman J., Russo R.J., Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology. 14:1993;83-144
4. Bellinger F.P., Wilce P.A., Bedi K.S., Wilson P. Long-lasting synaptic modification in the rat hippocampus resulting from NMDA receptor blockade during development. Synapse. 43:2002;95-101
5. Bhave S.V., Hoffmann P.L. Ethanol promotes apoptosis in cerebellar granule cells by inhibiting the trophic effect of NMDA. J. Neurochem. 68:1997;578-586
6. Bittigau P., Sifringer M., Genz K., Reith E., Pospischil D., Govindarajalu S., Dzietko M., Pesditschek S., Mai I., Dikranian K., Olney J.W., Ikonomidou C. Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc. Natl. Acad. Sci. U. S. A. 99:2002;15089-15094
7. Bonni A., Brunet A., West A.E., Datta S.R., Takasu M.A., Greenberg M.E. Cell survival promoted by the Ras-MAPK signaling pathway by transcription- dependent and -independent mechanisms. Science. 286:1999;1358-1362
8. Bourne H.R., Nicoll R. Molecular machines integrate coincident synaptic signals. Cell. 72:1993;55-75
9. Brooks W.J., Petit T.L., LeBoutillier J.C. Effect of chronic administration of NMDA antagonists on synaptic development. Synapse. 26:1997;104-113
10. Climent E., Pascual M., Renau-Piqueras J., Guerri C. Ethanol exposure enhances cell death in the developing cerebral cortex: role of brain-derived neurotrophic factor and its signaling pathways. J. Neurosci. Res. 68:2002;213-225
11. De Olmos J.S., Ingram W.R. An improved cupric-silver method for impregnation of axonal and terminal degeneration. Brain Res. 33:1971;523-529
12. Dikranian K., Ishimaru M.J., Tenkova T.I., Labruyere J., Qin Y.Q., Ikonomidou C., Olney J.W. Apoptosis in the in vivo mammalian forebrain. Neurobiol. Dis. 8:2001;359-379
13. Dobbing J., Sands J. The brain growth spurt in various mammalian species. Early Hum. Dev. 3:1979;70-84
14. Du K., Asahara H., Jhala U.S., Wagner B.L., Montminy M. Characterization of a CREB gain-of-function mutant with constitutive transcriptional activity in vivo. Mol. Cell. Biol. 20:2000;4320-4327
15. Dzietko M., Felderhoff-Mueser U., Sifringer M., Krutz B., Bittigau P., Thor F., Heumann R., Bührer C., Ikonomidou C., Hansen H.H. Erythropoietin protects the developing brain against N-methyl-D-aspartate receptor antagonist neurotoxicity. Neurobiol. Dis. 15:2004;177-187
16. Fedoroff S., Richardson A. Protocols for Neural Cell Culture. 1997;Humana Press, Totowa, NJ
17. Finkbeiner S. CREB couples neurotrophin signals to survival messages. Neuron. 25:2000;11-14
18. Friedman H.V., Bresler T., Garner C.C., Ziv N.E. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron. 27:2000;57-69
19. Gaiarsa J.L., Coradetti R., Ben-Ari Y. The allosteric glycine site of the N-methyl-D-aspartate receptor modulates GABAergic-mediated synaptic events in neonatal rat CA3 hippocampal neurons. Proc. Natl. Acad. Sci. U. S. A. 87:1990;343-346
20. Gundersen H.J.G., Bendtsen T.F., West M.J. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS. 96:1988;379-394
21. Hardingham G.E., Bading H. Coupling of extrasynaptic NMDA receptors to a CREB shut-off pathway is developmentally regulated. Biochim. Biophys. Acta. 1600:2002;148-153
22. Hardingham G.E., Bading H. The Yin and Yang of NMDA receptor signalling. Trends Neurosci. 26:2003;81-89
23. Hardingham G.E., Arnold F.J., Bading H. A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat. Neurosci. 4:2001;565-566
24. 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
25. Hestrin S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature. 357:1992;686-689
26. Heumann R., Goemans C., Bartsch D., Lingenhöhl K., Waldmeier P.C., Hengerer B., Allegrini P.R., Schellander K., Wagner E.F., Arendt T., Kamdem R.H., Obst-Pernberg K., Narz F., Wahle P., Berns H. Transgenic activation of Ras in neurons promotes hypertrophy and protects from lesion-induced degeneration. J. Cell Biol. 151:2000;1537-1548
27. Huttenlocher P.R. Synaptic density in human frontal cortex- developmental changes and effect of aging. Brain Res. 163:1979;195-205
28. Hwang J.-Y., Kim Y.H., Ahn Y.-H., Wie M.-B., Koh J.Y. N-methyl-D-aspartate receptor blockade induces neuronal apoptosis in cortical culture. Exp. Neurol. 159:1999;124-130
29. Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vöckler J., Dikranian K., Tenkova T.I., Stefovska V., Turski L., Olney J.W. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science. 283:1999;70-74
30. Ikonomidou C., Bittigau P., Ishimaru M.J., Wozniak D.F., Koch C., Genz K., Price M.T., Stefovska V., Hörster F., Tenkova T.I., Dikranian K., Olney J.W. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science. 287:2000;1056-1060
31. Impey S., Fong A.L., Wang Y., Cardineaux J.-R., Fass D.M., Obretian K., Wayman G.A., Storm D.R., Soderling T.R., Goodman R.H. Phosphorylation of CBP mediates transcriptional activation by neural activity and CaM kinase IV. Neuron. 34:2002;235-244
32. Ishimaru M.J., Ikonomidou C., Tenkova T.I., Der T.C., Dikranian K., Sesma M.A., Olney J.W. Distinguishing excitotoxic from apoptotic neurodegeneration in the developing rat brain. J. Comp. Neurol. 408:1999;461-476
33. Jevtovic-Todorovic V., Hartman R.E., Izumi Y., Benshoff N.D., Dikranian K., Zorumski C.F., Olney J.W., Wozniak D.F. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J. Neurosci. 23:2003;876-882
34. Kornhauser J.M., Cowan C.W., Shaywitz A.J., Dolmetsch R.E., Griffith E.C., Hu L.S., Haddad C., Xia Z., Greenberg M.E. CREB transcriptional activity in neurons is regulated by multiple calcium-specific phosphorylation events. Neuron. 34:2003;221-233
35. Lonze B.E., Riccio A., Cohen S., Ginty D.D. Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron. 34:2002;371-385
36. Mantamadiotis T., Lemberger T., Bleckmann S.C., Kern H., Kretz O., Villalba A.M., Tronche F., Kellendock C., Gau D., Kapfhammer J., Otto C., Schmid W., Schütz W. Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet. 31:2002;47-54
37. Mayr B., Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev., Mol. Cell Biol. 2:2001;599-609
38. Olney J.W., Wozniak D.F., Jevtovic-Todorovic V., Farber N.B., Bittigau P., Ikonomidou C. Drug-induced apoptotic neurodegeneration in the developing brain. Brain Pathol. 12:2002;488-498
39. Paul S., Wang T.C., Wang P., Lombroso P.J. NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling. Nat. Neurosci. 6:2003;34-42
40. Rauschecker J.P., Egert U., Kossel A. Effects of NMDA antagonists on developmental plasticity in kitten visual cortex. Int. J. Dev. Neurosci. 8:1990;425-435
41. Riccio A., Ahn S., Davenport C.M., Blendy J.A., Ginty D.D. Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science. 286:1999;2358-2361
42. Rudolph D., Tafuri A., Gass P., Hammerling G.J., Arnold B., Schutz G. Impaired fetal T cell development and perinatal lethality in mice lacking the cAMP response element binding protein. Proc. Natl. Acad. Sci. U. S. A. 95:1998;4481-4486
43. Shaywitz A.J., Greenberg M.E. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Ann. Rev. Biochem. 68:1999;821-861
44. Shieh P.B., Hu S.C., Bobb K., Timmusk T.G.A. Identification of a signalling pathway involved in calcium regulation of BDNF expression. Neuron. 20:1998;740
45. Simon D.K., Prusky G.T., O'Leary D.D., Constantine-Paton M. N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. Proc. Natl. Acad. Sci. U. S. A. 89:1992;10593-10597
46. Somers J.P., DeLoia J.A., Zeleznik A.J. Adenovirus-directed expression of a nonphosphorylatable mutant of CREB (cAMP response element-binding protein) adversely affects the survival, but not the differentiation, of rat granulosa cells. Mol. Endocrinol. 13:1999;1364-1372
47. Tao X., Finkbeiner S., Arnold D.B., Shaywitz A.J., Greenberg M.E. Calcium influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron. 20:1998;727-740
48. Tsumoto T., Hagihara K., Sato H., Hata Y. NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats. Nature. 327:1987;513-514
49. Vallano M.L. Developmental aspects of NMDA receptor function. Crit. Rev. Neurobiol. 12:1998;177-204
50. West A.E., Chen W.G., Dalva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., Takasu M.A., Tao X., Greenberg M.E. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. U. S. A. 98:2001;11024-11031
51. Wu G., Malinow R., Cline H.T. Maturation of a central glutamatergic synapse. Science. 274:1996;972-976
52. Wu G.Y., Deisseroth K., Tsien R.W. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. U. S. A. 98:2001;2808-2813
53. Yen L.-Y., Sibley J.R., Constantine-Paton M. Fine-structural alterations and clustering of developing synapses after chronic treatments with low levels of NMDA. J. Neurosci. 13:1993;4949-4960
54. Yoon W.J., Won S.J., Ryu B.R., Gwag B.J. Blockade of ionotropic glutamate receptors produces neuronal apoptosis through the Bax-cytochrome C-caspase pathway: the causative role of Ca2+ deficiency. J. Neurochem. 85:2003;525-533