Cellular and subcellular calcium accumulation during glutamate-induced injury in cerebellar granule neurons

Journal of Neurochemistry

Volumn 92, Issue 5, 2005, Pages 1081-1090

  Ward, Manus W ^a   Kushnareva, Yulia ^c   Greenwood, Sam ^b   Connolly, Christopher N ^b  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c BURNHAM INSTITUTE   (United States)

Author keywords

Calcium; Glutamate; Kainate; Mitochondria; NMDA; Pre conditioning

Indexed keywords

GLUTAMIC ACID; KAINIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CEREBELLUM; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; GRANULE CELL; MITOCHONDRION; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; RAT;

AGE FACTORS; ALAMETHICIN; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BRAIN DISEASES; CALCIUM; CALCIUM ISOTOPES; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CELL COUNT; CELL DEATH; CELL FRACTIONATION; CELLS, CULTURED; CEREBELLUM; DIAGNOSTIC IMAGING; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; FURA-2; GLUTAMIC ACID; GLYCINE; HYDRO-LYASES; INDOLES; INTRACELLULAR SPACE; IONOPHORES; MALE; MITOCHONDRIA; NEURONS; PROPIDIUM; QUINOXALINES; RATS; RATS, WISTAR; TIME FACTORS;

EID: 14844302655     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02928.x     Document Type: Article

References (43)

1. Aarts M., Iihara K., Wei W. L., Xiong Z. G., Arundine M., Cerwinski W., MacDonald J. F. and Tymianski M. (2003) A key role for TRPM7 channels in anoxic neuronal death. Cell 115, 863-877.
2. Addae J. I., Evans S. M., Ali N. and Stone T. W. (2000) NMDA-induced changes in a cortical network in vivo are prevented by AMPA. Brain Res. 869, 211-215.
3. Addae J. I., Youssef F. F. and Stone T. W. (2003) Neuroprotective role of learning in dementia: a biological explanation. J. Alz. Dis. 5, 91-104.
4. Allen N. J. and Artwell D. (2002) Modulation of ASIC channels in rat cerebellar Purkinje neurons by ischaemia-related signals. J. Physiol. 543, 521-529.
5. Andreyev A. and Fiskum G. (1999) Calcium induced release of mitochondrial cytochrome c by different mechanisms selective for brain versus liver. Cell Death Differ. 6, 825-832.
6. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A. and Nicotera P. (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
7. Arnaudeau S., Kelley W. L., Walsh J. V. Jr and Demaurex N. (2001) Mitochondria recycle Ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring 'endoplasmic reticulum regions. J. Biol. Chem. 276, 29 430-29 439.
8. Bond A., Lodge D., Hicks C. A., Ward M. A. and O'Neill M. J. (1999) NMDA receptor antagonism, but not AMPA receptor antagonism attenuates induced ischaemic tolerance in the gerbil hippocampus. Eur. J. Pharmacol. 380, 91-99.
9. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P. and Lipton S. A. (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl Acad. Sci. USA 92, 7162-7166.
10. Brocard J. B., Tassetto M. and Reynolds I. J. (2001) Quantitative evaluation of mitochondrial calcium content in rat cortical neurones following a glutamate stimulus. J. Physiol. 531, 793-805.
11. Budd S. L. and Nicholls D. G. (1996) Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 67, 2282-2291.
12. Castilho R. F., Hansson O., Ward M. W., Budd S. L. and Nicholls D. G. (1998). Mitochondrial control of acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurosci. 18, 10 277-10 286.
13. Castilho R. F., Ward M. W. and Nicholls D. G. (1999) Oxidative stress, mitochondrial fonction, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 72, 1394-1401.
14. Chalmers S. and Nicholls D. G. (2003) The relationship between free and total calcium concentrations in the matrix of liver and brain mitochondria. J. Biol. Chem. 278, 19 062-19 070.
15. Choi D. W. (1994) Glutamate receptors and the induction of excitotoxic neuronal death. Prog. Brain Res. 100, 47-51.
16. Courtney M. J., Lambert J. J. and Nicholls D. G. (1990) Glutamate-receptor-mediated regulation of the cytoplasmic free calcium level in cultured cerebellar granule cells. Biochem. Soc. Trans. 18, 420-421.
17. Csordas G. and Hajnoczky G. (2001) Sorting of calcium signals at the junctions of endoplasmic reticulum and mitochondria. Cell Calcium 29, 249-262.
18. Dajas-Bailador F. A., Lima P. A. and Wonnacott S. (2000) The alpha7 nicotinic acetylcholine receptor subtype mediates nicotine protection against NMDA excitotoxicity in primary hippocampal cultures through a Ca(2+) dependent mechanism. Neuropharmacology 39, 2799-2807.
19. Dajas-Bailador F. A., Soliakov L. and Wonnacott S. (2002) Nicotine activates the extracellular signal-regulated kinase 1/2 via the alpha7 nicotinic acetylcholine receptor and protein kinase A, in SH-SY5Y cells and hippocampal neurones. J. Neurochem. 80, 520-530.
20. Eimerl S. and Schramm M. (1994) The quantity of calcium that appears to induce neuronal death. J. Neurochem. 62, 1223-1226.
21. Hardingham G. E., Fukunaga Y. and Bading H. (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5, 405-414.
22. Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vockler J., Dikranian K., Tenkova T. I., Stefovska V., Turski L. and Olney J. W. (1999) Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283, 70-74.
23. Khaspekov L., Shamloo M., Victorov I. and Wieloch T. (1998) Sublethal in vitro glucose-oxygen deprivation protects cultured hippocampal neurons against a subsequent severe insult. Neuroreport 9, 1273-1276.
24. Lehninger A. L., Carafoli E. and Rossi C. S. (1967) Energy-linked ion movements in mitochondrial systems. Adv. Enzymol. Relat. Areas Mol. Biol. 29, 259-320.
25. Li J., Kato K., Ikeda J., Morita I. and Murota S. (2001) A narrow window for rescuing cells-by the inhibition of calcium influx and the importance of influx route in rat cortical neuronal cell death induced by glutamate. Neurosci. Lett. 304, 29-32.
26. Luetjens C. M., Bui N. T., Sengpiel B., Munstermann G., Poppe M., Krohn A. J., Bauerbach E., Krieglstein J. and Prehn J. H. (2000) Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J. Neurosci. 20, 5715-5723.
27. Nicholls D. and Akerman K. (1982) Mitochondrial calcium transport. Biochim. Biophys. Acta 683, 57-88.
28. Nicholls D. G. and Scott I. D. (1980) The role of mitochondria in the regulation of calcium ion transport in synaptosomes. Biochem. Soc. Trans. 8, 264-266.
29. Pugliese A. M., Latini S., Corradetti R. and Pedata F. (2003) Brief, repeated, oxygen-glucose deprivation episodes protect neurotransmission from a longer ischemic episode in the in vitro hippocampus: role of adenosine receptors. Br. J. Pharmacol. 140, 305-314.
30. Rego A. C., Ward M. W. and Nicholls D. G. (2001) Mitochondria control ampa/kainate receptor-induced cytoplasmic calcium deregulation in rat cerebellar granule cells. J. Neurosci. 21, 1893-1901.
31. Sattler R., Charlton M. P., Hafner M. and Tymianski M. (1998) Distinct influx pathways, not calcium load, determine neuronal vulnerability to calcium neurotoxicity. J. Neurochem. 71, 2349-2364.
32. Sedova M. and Blatter L. A. (2000) Intracellular sodium modulates mitochondrial calcium signaling in vascular endothelial cells. J. Biol. Chem. 275, 35 402-35 407.
33. Solenski N. J., diPierro C. G., Trimmer P. A., Kwan A. L., Helm G. A. and Helms G. A. (2002) Ultrastructural changes of neuronal mitochondria after transient and permanent cerebral ischemia. Stroke 33, 816-824.
34. Stone T. W. (2003) Pre-conditioning protection in the brain. Br. J. Pharmacol. 140, 229-230.
35. Stout A. K., Raphael H. M., Kanterewicz B. I., Klann E. and Reynolds I. J. (1998) Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat. Neurosci. 1, 366-373.
36. Tymianski M., Charlton M. P., Carlen P. L. and Tator C. H. (1993a) Secondary Ca2+ overload indicates early neuronal injury which precedes staining with viability indicators. Brain Res. 607, 319-323.
37. Tymianski M., Charlton M. P., Carlen P. L. and Tator C. H. (1993b) Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J. Neurosci. 13, 2085-2104.
38. Ward M. W., Rego A. C., Frenguelli B. G. and Nicholls D. G. (2000) Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurosci. 20, 7208-7219.
39. Weiss J. H. and Sensi S. L. (2000) Ca2+-Zn2+ permeable AMPA or kainate receptors: possible key factors in selective neurodegeneration. Trends Neurosci. 23, 365-371.
40. Yermolaieva O., Leonard A. S., Schnizler M. K., Abboud F. M. and Welsh M. J. (2004) Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc. Natl Acad. Sci. USA 101, 6752-6757.
41. Youssef F. F., Addae J. I., McRae A. and Stone T. W. (2001) Long-term potentiation protects rat hippocampal slices from the effects of acute hypoxia. Brain Res. 907, 144-150.
42. Zaugg M. and Schaub M. C. (2003) Signaling and cellular mechanisms in cardiac protection by ischemic and pharmacological preconditioning. J. Muscle Res. Cell Motil. 24, 219-249.
43. Zeron M. M., Hansson O., Chen N., Wellington C. L., Leavitt B. R., Brundin P., Hayden M. R. and Raymond L. A. (2002) Increased sensitivity to N-methyl-D-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 33, 849-860.