Differential NMDA receptor-dependent calcium loading and mitochondrial dysfunction in CA1 vs. CA3 hippocampal neurons

Neurobiology of Disease

Volumn 37, Issue 2, 2010, Pages 403-411

  Stanika, Ruslan I ^a   Winters, Christine A ^a   Pivovarova, Natalia B ^a   Andrews, S Brian ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Calcium; Electron probe microanalysis; Excitotoxicity; Hippocampal slice cultures; Reactive oxygen species; Zinc

Indexed keywords

CALCIUM ION; CHELATING AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; REACTIVE OXYGEN METABOLITE; ZINC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CALCIUM TRANSPORT; CONTROLLED STUDY; CULTURE MEDIUM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HIPPOCAMPUS; NERVE CELL CULTURE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN ISCHEMIA; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; CALCIUM; CALCIUM SIGNALING; CAUSALITY; CELL RESPIRATION; ENERGY METABOLISM; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NERVE DEGENERATION; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 73049090241     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.10.020     Document Type: Article

References (53)

1. Aguirre C.C., and Baudry M. Progesterone reverses 17-β-estradiol-mediated neuroprotection and BDNF induction in cultured hippocampal slices. Eur. J. Neurosci. 29 (2009) 447-454
2. Badugu R., Garcia M., Bondada V., Joshi A., and Geddes J.W. N terminus of calpain 1 is a mitochondrial targeting sequence. J. Biol. Chem. 283 (2008) 3409-3417
3. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn G.W., Robbins J., and Molkentin J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434 (2005) 658-662
4. Bernardi P., Krauskopf A., Basso E., Petronilli V., Blachly-Dyson E., Di Lisa F., and Forte M.A. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J. 273 (2006) 2077-2099
5. Bickler P.E., and Hansen B.M. Hypoxia-tolerant neonatal CA1 neurons: relationship of survival to evoked glutamate release and glutamate receptor-mediated calcium changes in hippocampal slices. Brain Res. Dev. Brain Res. 106 (1998) 57-69
6. + channels. Neuron 41 (2004) 351-365
7. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., and Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 287 (2004) C817-833
8. Calderone A., Jover T., Mashiko T., Noh K.M., Tanaka H., Bennett M.V., and Zukin R.S. Late calcium EDTA rescues hippocampal CA1 neurons from global ischemia-induced death. J. Neurosci. 24 (2004) 9903-9913
9. Chinopoulos C., and Adam-Vizi V. Calcium, mitochondria and oxidative stress in neuronal pathology. Novel aspects of an enduring theme. FEBS J. 273 (2006) 433-450
10. Choi D.W. Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci. 18 (1995) 58-60
11. Coultrap S.J., Nixon K.M., Alvestad R.M., Valenzuela C.F., and Browning M.D. Differential expression of NMDA receptor subunits and splice variants among the CA1, CA3 and dentate gyrus of the adult rat. Brain Res. Mol. Brain Res. 135 (2005) 104-111
12. Cronberg T., Rytter A., and Wieloch T. Chelation of intracellular calcium reduces cell death after hyperglycemic in vitro ischemia in murine hippocampal slice cultures. Brain Res. 1049 (2005) 120-127
13. 2+-dependent reactive oxygen species accumulation. J. Neurochem. 106 (2008) 2184-2193
14. Dixon R.M., Mellor J.R., and Hanley J.G. Pick1-mediated glutamate receptor subunit 2 (GLUR2) trafficking contributes to cell death in oxygen/glucose deprived hippocampal neurons. J. Biol. Chem. 284 (2009) 14230-14235
15. 2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity. J. Physiol. 585 (2007) 741-758
16. 2+ and ROS. Front Biosci. 14 (2009) 1197-1218
17. 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
18. Frederickson C.J., Koh J.Y., and Bush A.I. The neurobiology of zinc in health and disease. Nat. Rev., Neurosci. 6 (2005) 449-462
19. Gee C.E., Benquet P., Raineteau O., Rietschin L., Kirbach S.W., and Gerber U. NMDA receptors and the differential ischemic vulnerability of hippocampal neurons. Eur. J. Neurosci. 23 (2006) 2595-2603
20. Gillessen T., Budd S.L., and Lipton S.A. Excitatory amino acid neurotoxicity. Adv. Exp. Med. Biol. 513 (2002) 3-40
21. Grishin A.A., Gee C.E., Gerber U., and Benquet P. Differential calcium-dependent modulation of NMDA currents in CA1 and CA3 hippocampal pyramidal cells. J. Neurosci. 24 (2004) 350-355
22. Jemmerson R., Dubinsky J.M., and Brustovetsky N. Cytochrome C release from CNS mitochondria and potential for clinical intervention in apoptosis-mediated CNS diseases. Antioxid. Redox Signal. 7 (2005) 1158-1172
23. Kirino T. Delayed neuronal death. Neuropathology 20 Suppl. (2000) S95-S97
24. 28k knockout mice. Neuroscience 85 (1998) 361-373
25. Kwak S., and Weiss J.H. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr. Opin. Neurobiol. 16 (2006) 281-287
26. Li V., Brustovetsky T., and Brustovetsky N. Role of cyclophilin D-dependent mitochondrial permeability transition in glutamate-induced calcium deregulation and excitotoxic neuronal death. Exp. Neurol. 218 (2009) 171-182
27. Lin D.T., and Huganir R.L. PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptor-induced internalization. J. Neurosci. 27 (2007) 13903-13908
28. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 30 (2007) 126-134
29. Mattiasson G., Friberg H., Hansson M., Elmer E., and Wieloch T. Flow cytometric analysis of mitochondria from CA1 and CA3 regions of rat hippocampus reveals differences in permeability transition pore activation. J. Neurochem. 87 (2003) 532-544
30. 2+ accumulation contributes to synaptic failure, mitochondrial depolarization, and cell death in an acute slice oxygen-glucose deprivation model of ischemia. J. Neurosci. 29 (2009) 1105-1114
31. 2+ microdomains in hippocampal neurons. J. Neurosci. 25 (2005) 558-565
32. 28k in temporal lobe epilepsy. J. Neurosci. 20 (2000) 1831-1836
33. Nicholls D.G. Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr. Mol. Med. 4 (2004) 149-177
34. Nicholls D.G. Mitochondrial calcium function and dysfunction in the central nervous system. Biochim. Biophys. Acta 1787 (2009) 1416-1424
35. Olney J.W., and Sharpe L.G. Brain lesions in an infant rhesus monkey treated with monsodium glutamate. Science 166 (1969) 386-388
36. Paoletti P., Vergnano A.M., Barbour B., and Casado M. Zinc at glutamatergic synapses. Neuroscience 158 (2009) 126-136
37. Perez Velazquez J.L., Frantseva M.V., and Carlen P.L. In vitro ischemia promotes glutamate-mediated free radical generation and intracellular calcium accumulation in hippocampal pyramidal neurons. J. Neurosci. 17 (1997) 9085-9094
38. Pivovarova N.B., Hongpaisan J., Andrews S.B., and Friel D.D. Depolarization-induced mitochondrial Ca accumulation in sympathetic neurons: spatial and temporal characteristics. J. Neurosci. 19 (1999) 6372-6384
39. 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
40. Pivovarova N.B., Nguyen H.V., Winters C.A., Brantner C.A., Smith C.L., and Andrews S.B. Excitotoxic calcium overload in a subpopulation of mitochondria triggers delayed death in hippocampal neurons. J. Neurosci. 24 (2004) 5611-5622
41. Pivovarova N.B., Stanika R.I., Watts C.A., Brantner C.A., Smith C.L., and Andrews S.B. Reduced calcium-dependent mitochondrial damage underlies the reduced vulnerability of excitotoxicity-tolerant hippocampal neurons. J. Neurochem. 104 (2008) 1686-1699
42. Pozzo-Miller L.D., Pivovarova N.B., Leapman R.D., Buchanan R.A., Reese T.S., and Andrews S.B. Activity-dependent calcium sequestration in dendrites of hippocampal neurons in brain slices. J. Neurosci. 17 (1997) 8729-8738
43. Pringle A.K., Iannotti F., Wilde G.J., Chad J.E., Seeley P.J., and Sundstrom L.E. Neuroprotection by both NMDA and non-NMDA receptor antagonists in in vitro ischemia. Brain Res. 755 (1997) 36-46
44. Rytter A., Cronberg T., Asztely F., Nemali S., and Wieloch T. Mouse hippocampal organotypic tissue cultures exposed to in vitro "ischemia" show selective and delayed CA1 damage that is aggravated by glucose. J. Cereb. Blood. Flow. Metab. 23 (2003) 23-33
45. Schinzel A.C., Takeuchi O., Huang Z., Fisher J.K., Zhou Z., Rubens J., Hetz C., Danial N.N., Moskowitz M.A., and Korsmeyer S.J. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 12005-12010
46. 28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1 (2002) 241-258
47. 28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J. Comp. Neurol. 280 (1989) 183-196
48. Starkov A.A., Chinopoulos C., and Fiskum G. Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36 (2004) 257-264
49. Stork C.J., and Li Y.V. Intracellular zinc elevation measured with a "calcium-specific" indicator during ischemia and reperfusion in rat hippocampus: a question on calcium overload. J. Neurosci. 26 (2006) 10430-10437
50. Wang J., Liu S., Fu Y., Wang J.H., and Lu Y. Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors. Nat. Neurosci. 6 (2003) 1039-1047
51. Ward M.W., Huber H.J., Weisova P., Dussmann H., Nicholls D.G., and Prehn J.H. Mitochondrial and plasma membrane potential of cultured cerebellar neurons during glutamate-induced necrosis, apoptosis, and tolerance. J. Neurosci. 27 (2007) 8238-8249
52. Yuen E.Y., Gu Z., and Yan Z. Calpain regulation of AMPA receptor channels in cortical pyramidal neurons. J. Physiol. 580 (2007) 241-254
53. Zhou M., and Baudry M. EUK-207, a superoxide dismutase/catalase mimetic, is neuroprotective against oxygen/glucose deprivation-induced neuronal death in cultured hippocampal slices. Brain Res. 1247 (2009) 28-37