Impaired presynaptic cytosolic and mitochondrial calcium dynamics in aged compared to young adult hippocampal CA1 synapses ameliorated by calcium chelation

Neuroscience

Volumn 159, Issue 4, 2009, Pages 1300-1308

  Tonkikh, A A ^a   Carlen, P L ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

calcium chelation; calcium dynamics; mitochondrial uncoupling; presynaptic

Indexed keywords

BIS(O AMINOPHENOXY)ETHANE N,N,N,N TETRAACETIC ACID; CALCIUM; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CHELATING AGENT; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; UNCLASSIFIED DRUG;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CHELATION; CONTROLLED STUDY; CYTOSOL; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FLUORESCENCE; HIPPOCAMPUS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT;

AGING; ANIMALS; CALCIUM; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; CELL HYPOXIA; CENTRAL NERVOUS SYSTEM AGENTS; CHELATING AGENTS; CYTOPLASM; EGTAZIC ACID; ELECTRON TRANSPORT; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUCOSE; HIPPOCAMPUS; MITOCHONDRIA; PRESYNAPTIC TERMINALS; RATS; RATS, INBRED F344; SYNAPSES;

EID: 63549149635     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.12.057     Document Type: Article

References (48)

1. Abdel-Hamid K., and Tymianski M. Mechanisms and effects of intracellular calcium buffering on neuronal survival in organotypic hippocampal cultures exposed to anoxia/aglycemia or to excitotoxins. J Neurosci 17 (1997) 3538-3553
2. Bartnik B.L., Spigelman I., and Obenaus A. Cell-permeant calcium buffer induced neuroprotection after cortical devascularization. Exp Neurol 192 (2005) 357-364
3. Bianchi K., Rimessi A., Prandini A., Szabadkai G., and Rizzuto R. Calcium and mitochondria: mechanisms and functions of a troubled relationship. Biochim Biophys Acta Mol Cell Res 1742 (2004) 119-131
4. Billups B., and Forsythe I.D. Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci 22 (2002) 5840-5847
5. Campbell L.W., Hao S.Y., Thibault O., Blalock E.M., and Landfield P.W. Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J Neurosci 16 (1996) 6286-6295
6. Cuchillo-Ibanez I., Albillos A., Aldea M., Arroyo G., Fuentealba J., and Garcia A.G. Calcium entry, calcium redistribution, and exocytosis. Ann N Y Acad Sci 971 (2002) 108-116
7. Frantseva M.V., Carlen P.L., and Perez Velazquez J.L. Dynamics of intracellular calcium and free radical production during ischemia in pyramidal neurons. Free Radic Biol Med 31 (2001) 1216-1227
8. Hajnoczky G., Seitz M.B., and Thomas A.P. Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82 (1995) 415-424
9. Hajnoczky G., Csordas G., Das S., Garcia-Perez C., Saotome M., Roy S., and Yi M. Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca uptake in apoptosis. Cell Calcium 40 (2006) 553-560
10. Holtkamp M., Buchheim K., Siegmund H., and Meierkord H. Optical imaging reveals reduced seizure spread and propagation velocities in aged rat brain in vitro. Neurobiol Aging 24 (2003) 345-353
11. Jackson M.B., and Redman S.J. Calcium dynamics, buffering, and buffer saturation in the boutons of dentate granule-cell axons in the hilus. J Neurosci 23 (2003) 1612-1621
12. Lee S.K., Lee J.Y., Lee M.Y., Chung S.M., and Chung J.H. Advantages of Calcium Green-1 over other fluorescent dyes in measuring cytosolic calcium in platelets. Anal Biochem 273 (1999) 186-191
13. Lim M.S., Lim P.K., Gupta R., and Boelsterli U.A. Critical role of free cytosolic calcium, but not uncoupling, in mitochondrial permeability transition and cell death induced by diclofenac oxidative metabolites in immortalized human hepatocytes. Toxicol Appl Pharmacol 217 (2006) 322-331
14. 2+] in adult Alzheimer's disease mice. J Neurochem 105 (2008) 262-271
15. Maravall M., Mainen Z.F., Sabatini B.L., and Svoboda K. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys J 78 (2000) 2655-2667
16. 2+ homeostasis pathways, cell death and protection after oxygen-glucose-deprivation in organotypic hippocampal slice cultures. Neuroscience 128 (2004) 729-740
17. Martinez-Serrano A., Blanco P., and Satrustegui J. Calcium binding to the cytosol and calcium extrusion mechanisms in intact synaptosomes and their alterations with aging. J Biol Chem 267 (1992) 4672-4679
18. Mattson M.P., and Liu D. Energetics and oxidative stress in synaptic plasticity and neurodegenerative disorders. Neuromol Med 2 (2002) 215-231
19. Matveev V., Zucker R.S., and Sherman A. Facilitation through buffer saturation: constraints on endogenous buffering properties. Biophys J 86 (2004) 2691-2709
20. Mothet J.P., Fossier P., Meunier F.M., Stinnakre J., Tauc L., and Baux G. Cyclic ADP-ribose and calcium-induced calcium release regulate neurotransmitter release at a cholinergic synapse of Aplysia. J Physiol Lond 507 (1998) 405-414
21. 2+ modulation of glycinergic synaptic currents in rodent hypoglossal motoneurones. J Physiol Lond 569 (2005) 817-831
22. 2+ dynamics matter. J Physiol Lond 586 (2008) 2031
23. Nicholls D.G., Vesce S., Kirk L., and Chalmers S. Interactions between mitochondrial bioenergetics and cytoplasmic calcium in cultured cerebellar granule cells. Cell Calcium 34 (2003) 407-424
24. Niesen C., Charlton M., and Carlen P. Postsynaptic and presynaptic effects of the calcium chelator BAPTA on synaptic transmission in rat hippocampal dentate granule neurons. Brain Res 555 (1991) 319-325
25. i and membrane currents during impaired mitochondrial metabolism in dissociated rat hippocampal neurons. J Physiol Lond 507 (1998) 131-145
26. Ouanounou A., Zhang L., Charlton M.P., and Carlen P.L. Differential modulation of synaptic transmission by calcium chelators in young and aged hippocampal CA1 neurons: evidence for altered calcium homeostasis in aging. J Neurosci 19 (1999) 906-915
27. 2+ chelators in attenuation of synaptic transmission at hippocampal CA1 neurons. Neuroscience 75 (1996) 99-109
28. Parihar M., and Brewer G. Simultaneous age-related depolarization of mitochondrial membrane potential and increased mitochondrial reactive oxygen species production correlate with age-related glutamate excitotoxicity in rat hippocampal neurons. J Neurosci Res 85 5 (2007) 1018-1032
29. Pivovarova N.B., Pozzo-Miller L.D., Hongpaisan J., and Andrews S.B. Correlated calcium uptake and release by mitochondria and endoplasmic reticulum of CA3 hippocampal dendrites after afferent synaptic stimulation. J Neurosci 22 (2002) 10653-10661
30. Raza M., Deshpande L.S., Blair R.E., Carter D.S., Sombati S., and DeLorenzo R.J. Aging is associated with elevated intracellular calcium levels and altered calcium homeostatic mechanisms in hippocampal neurons. Neurosci Lett 418 (2007) 77-81
31. Regehr W.G., and Tank D.W. Selective fura-2 loading of presynaptic terminals and nerve cell processes by local perfusion in mammalian brain slice. J Neurosci Methods 37 (1991) 111-119
32. 2+ dynamics with genetically encoded bioluminescent reporters. Eur J Neurosci 21 3 (2005) 597-610
33. Rosenzweig E.S., and Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69 (2003) 143-179
34. 2+ affinity, chelator structure and binding kinetics. Neuroscience 75 (1996) 559-572
35. Stricker S.A., Centonze V.E., Paddock S.W., and Schatten G. Confocal microscopy of fertilization-induced calcium dynamics in sea urchin eggs. Dev Biol 149 (1992) 370-380
36. 2+]. J Neurophysiol 90 (2003) 491-502
37. i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J Neurosci 21 (2001) 9744-9756
38. Thibault O., and Landfield P.W. Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272 (1996) 1017-1020
39. Toescu E.C., and Verkhratsky A. Neuronal ageing from an intraneuronal perspective: roles of endoplasmic reticulum and mitochondria. Cell Calcium 34 (2003) 311-323
40. Tonkikh A., Janus C., El-Beheiry H., Pennefather P.S., Samoilova M., McDonald P., Ouanounou A., and Carlen P.L. Calcium chelation improves spatial learning and synaptic plasticity in aged rats. Exp Neurol 197 (2006) 291-300
41. Tsang C.W., Elrick D.B., and Charlton M.P. Alpha-latrotoxin releases calcium in frog motor nerve terminals. J Neurosci 20 (2000) 8685-8692
42. Tsien R.Y. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19 (1980) 2396-2404
43. Tsuji S.K., Tashiro K.S., Jun T., Kishimoto R., Yabe I., Yamagishi S., Takeuchi M., and Sasaki H. Proteasome inhibition induces selective motor neuron death in organotypic slice cultures. J Neurosci Res 82 (2005) 443-451
44. 2+ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron 11 (1993) 221-235
45. Wu S.H., and Kelly J.B. In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. III. Synaptic pharmacology. J Neurophysiol 75 (1996) 1271-1282
46. Yuste R., Majewska A., Cash S.S., and Denk W. Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J Neurosci 19 (1999) 1976-1987
47. 2+-ATPase by hydrogen peroxide and protection by calmodulin. Biochemistry 42 (2003) 12001-12010
48. 2+ indicators in frog skeletal muscle fibers. Biophys J 70 (1996) 896-916