Preconditioning induces tolerance by suppressing glutamate release in neuron culture ischemia models

Journal of Neurochemistry

Volumn 122, Issue 2, 2012, Pages 470-481

  Tauskela, Joseph S ^a   Aylsworth, Amy ^a   Hewitt, Melissa ^a   Brunette, Eric ^a   Mealing, Geoffrey A R ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

excitotoxicity; glutamate; neuroprotection; preconditioning; synaptic scaling; tolerance

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; OUABAIN; PARAQUAT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE; EXOCYTOSIS; FEMALE; ISCHEMIC PRECONDITIONING; MEMBRANE DEPOLARIZATION; NERVE CELL CULTURE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CELL HYPOXIA; CELL SIZE; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID TRANSPORTER 2; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUCOSE; GLUTAMIC ACID; ISCHEMIA; ISCHEMIC PRECONDITIONING; NEURONS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, GABA; RECEPTORS, PRESYNAPTIC; SODIUM; SODIUM-POTASSIUM-EXCHANGING ATPASE; VESICULAR GLUTAMATE TRANSPORT PROTEINS; ZINC;

STROPHANTHUS GRATUS;

EID: 84863321701     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07791.x     Document Type: Article

References (42)

1. Abe H., and, Nowak T. S., (2004) Induced hippocampal neuron protection in an optimized gerbil ischemia model: insult thresholds for tolerance induction and altered gene expression defined by ischemic depolarization. J. Cereb. Blood Flow Metab. 24, 84-97. (Pubitemid 38021272)
2. Bengtson C. P., Dick O., and, Bading H., (2008) A quantitative method to assess extrasynaptic NMDA receptor function in the protective effect of synaptic activity against neurotoxicity. BMC Neurosci. 9, 11.
3. Bigdeli M. R., Rahnema M., and, Khoshbaten A., (2009) Preconditioning with sublethal ischemia or intermittent normobaric hyperoxia up-regulates glutamate transporters and tumor necrosis factor-alpha converting enzyme in the rat brain. J. Stroke Cerebrovasc. Dis. 18, 336-342.
4. Cohen D., and, Segal M., (2009) Homeostatic presynaptic suppression of neuronal network bursts. J. Neurophysiol. 101, 2077-2088.
5. Cousin M. A., Nicholls D. G., and, Pocock J. M., (1995) Modulation of ion gradients and glutamate release in cultured cerebellar granule cells by ouabain. J. Neurochem. 64, 2097-2104.
6. Dave K. R., Lange-Asschenfeldt C., Raval A. P., Prado R., Busto R., Saul I., and, Perez-Pinzon M. A., (2005) Ischemic preconditioning ameliorates excitotoxicity by shifting glutamate/gamma-aminobutyric acid release and biosynthesis. J. Neurosci. Res. 82, 665-673. (Pubitemid 41740467)
7. DeFazio R. A., Raval A. P., Lin H. W., Dave K. R., Della-Morte D., and, Perez-Pinzon M. A., (2009) GABA synapses mediate neuroprotection after ischemic and epsilonPKC preconditioning in rat hippocampal slice cultures. J. Cereb. Blood Flow Metab. 29, 375-384.
8. Dick O., and, Bading H., (2010) Synaptic activity and nuclear calcium signaling protect hippocampal neurons from death signal-associated nuclear translocation of FoxO3a induced by extrasynaptic N-methyl-D-aspartate receptors. J. Biol. Chem. 285, 19354-19361.
9. Dirnagl U., Simon R. P., and, Hallenbeck J. M., (2003) Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 26, 248-254. (Pubitemid 36556155)
10. Erdo S. L., and, Michler A, (1990) GABA does not protect cerebro-cortical cultures against excitotoxic cell death. Eur. J. Pharmacol. 182, 203-206. (Pubitemid 20211605)
11. Fogal B., Trettel J., Uliasz T. F., Levine E. S., and, Hewett S. J., (2005) Changes in secondary glutamate release underlie the developmental regulation of excitotoxic neuronal cell death. Neuroscience 132, 929-942. (Pubitemid 40602529)
12. Grabb M. C., Lobner D., Turetsky D. M., and, Choi D. W., (2002) Preconditioned resistance to oxygen-glucose deprivation-induced cortical neuronal death: alterations in vesicular GABA and glutamate release. Neuroscience 115, 173-183. (Pubitemid 35232699)
13. 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. (Pubitemid 34454245)
14. Hartley D. M., and, Choi D. W., (1989) Delayed rescue of N-methyl-D-aspartate receptor-mediated neuronal injury in cortical culture. J. Pharmacol. Exp. Ther. 250, 752-758. (Pubitemid 19216169)
15. Hogins J., Crawford D. C., Jiang X., and, Mennerick S., (2011) Presynaptic silencing is an endogenous neuroprotectant during excitotoxic insults. Neurobiol. Dis. 43, 516-525.
16. Ikeda J., Terakawa S., Murota S., Morita I., and, Hirakawa K., (1996) Nuclear disintegration as a leading step of glutamate excitotoxicity in brain neurons. J. Neurosci. Res. 43, 613-622. (Pubitemid 26087395)
17. Kawahara K., Kosugi T., Tanaka M., Nakajima T., and, Yamada T., (2005) Reversed operation of glutamate transporter GLT-1 is crucial to the development of preconditioning-induced ischemic tolerance of neurons in neuron/astrocyte co-cultures. Glia 49, 349-359. (Pubitemid 40222913)
18. Kimura M., Sawada K., Miyagawa T., Kuwada M., Katayama K., and, Nishizawa Y., (1998) Role of glutamate receptors and voltage-dependent calcium and sodium channels in the extracellular glutamate/aspartate accumulation and subsequent neuronal injury induced by oxygen/glucose deprivation in cultured hippocampal neurons. J. Pharmacol. Exp. Ther. 285, 178-185. (Pubitemid 28207583)
19. Koh J. Y., and, Choi D. W., (1987) Effect of anticonvulsant drugs on glutamate neurotoxicity in cortical cell culture. Neurology 37, 319-322. (Pubitemid 17015512)
20. Kosugi T., Kawahara K., Yamada T., Nakajima T., and, Tanaka M., (2005) Functional significance of the preconditioning-induced down-regulation of glutamate transporter GLT-1 in neuron/astrocyte co-cultures. Neurochem. Res. 30, 1109-1116. (Pubitemid 41642153)
21. A receptor? Neurosci. Lett. 384, 87-92. (Pubitemid 40826623)
22. Lau D., and, Bading H., (2009) Synaptic activity-mediated suppression of p53 and induction of nuclear calcium-regulated neuroprotective genes promote survival through inhibition of mitochondrial permeability transition. J. Neurosci. 29, 4420-4429.
23. Lee J. M., Zipfel G. J., and, Choi D. W., (1999) The changing landscape of ischaemic brain injury mechanisms. Nature 399, A7-14. (Pubitemid 29295654)
24. Miyawaki T. F., Yokota H. F., Oguro K. F., Kato K. F., and, Shimazaki K., (2004) Ischemic preconditioning decreases intracellular zinc accumulation induced by oxygen-glucose deprivation in gerbil hippocampal CA1 neurons. Neurosci. Lett. 362, 216-219. (Pubitemid 38648945)
25. Monyer H., Giffard R. G., Hartley D. M., Dugan L. L., Goldberg M. P., and, Choi D. W., (1992) Oxygen or glucose deprivation-induced neuronal injury in cortical cell cultures is reduced by tetanus toxin. Neuron 8, 967-973.
26. A receptor activation attenuates excitotoxicity but exacerbates oxygen-glucose deprivation-induced neuronal injury in vitro. J. Cereb. Blood Flow Metab. 16, 1211-1218. (Pubitemid 26365372)
27. Mulholland P. J., Carpenter-Hyland E. P., Hearing M. C., Becker H. C., Woodward J. J., and, Chandler L. J., (2008) Glutamate transporters regulate extrasynaptic NMDA receptor modulation of Kv2.1 potassium channels. J. Neurosci. 28, 8801-8809.
28. Ohkuma S., Chen S. H., Katsura M., Chen D. Z., and, Kuriyama K., (1994) Muscimol prevents neuronal injury induced by NMDA. Jpn. J. Pharmacol. 64, 125-128. (Pubitemid 24091840)
29. 2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection. J. Neurosci. 25, 4279-4287. (Pubitemid 40628772)
30. ATP channels. J. Cereb. Blood Flow Metab. 19, 1296-1308. (Pubitemid 30013620)
31. Prass K., and, Dirnagl U., (1998) Glutamate antagonists in therapy of stroke. Restor. Neurol. Neurosci. 13, 3-10. (Pubitemid 28526916)
32. Ramnath R. R., Strange K., and, Rosenberg P. A., (1992) Neuronal injury evoked by depolarizing agents in rat cortical cultures. Neuroscience 51, 931-939.
33. A neurotransmission and cerebral ischemia. J. Neurochem. 77, 353-371. (Pubitemid 32303172)
34. Shimazaki K., Nakamura T., Nakamura K., Oguro K., Masuzawa T., Kudo Y., and, Kawai N., (1998) Reduced calcium elevation in hippocampal CA1 neurons of ischemia-tolerant gerbils. NeuroReport 9, 1875-1878. (Pubitemid 28289202)
35. Tauskela J. S., Mealing G., Comas T., Brunette E., Monette R., Small D. L., and, Morley P., (2003) Protection of cortical neurons against oxygen-glucose deprivation and N-methyl-D-aspartate by DIDS and SITS. Eur. J. Pharmacol. 464, 17-25. (Pubitemid 36205060)
36. 2+- dependent insults by metalloporphyrin catalytic antioxidants. J. Neurochem. 98, 1324-1342. (Pubitemid 44127805)
37. Tauskela J. S., Fang H., Hewitt M., Brunette E., Ahuja T., Thivierge J. P., Comas T., and, Mealing G. A., (2008) Elevated synaptic activity preconditions neurons against an in vitro model of ischemia. J. Biol. Chem. 283, 34667-34676.
38. Turrigiano G. G., Leslie K. R., Desai N. S., Rutherford L. C., and, Nelson S. B., (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892-896. (Pubitemid 28157666)
39. Ueda M., and, Nowak T. S., (2005) Protective preconditioning by transient global ischemia in the rat: components of delayed injury progression and lasting protection distinguished by comparisons of depolarization thresholds for cell loss at long survival times. J. Cereb. Blood Flow Metab. 25, 949-958. (Pubitemid 41061710)
40. Vidwans A. S., and, Hewett S. J., (2004) Enhanced release of synaptic glutamate underlies the potentiation of oxygen-glucose deprivation-induced neuronal injury after induction of NOS-2. Exp. Neurol. 190, 91-101. (Pubitemid 39335709)
41. Yamada T., Kawahara K., Kosugi K., and, Tanaka M., (2006) Nitric oxide produced during sublethal ischemia is crucial for the preconditioning-induced down-regulation of glutamate transporter GLT-1 in neuron/astrocyte co-cultures. Neurochemical Res. 31, 49-56. (Pubitemid 43234544)
42. Zhang M., Li W. B., Geng J. X., Li Q. J., Sun X. C., Xian X. H., Qi J., and, Li S. Q., (2007) The upregulation of glial glutamate transporter-1 participates in the induction of brain ischemic tolerance in rats. J. Cereb. Blood Flow Metab. 27, 1352-1368. (Pubitemid 46985352)