Na+ mechanism of δ-opioid receptor induced protection from anoxic K+ leakage in the cortex

Cellular and Molecular Life Sciences

Volumn 66, Issue 6, 2009, Pages 1105-1115

  Chao, D ^a   Balboni, G ^b,c   Lazarus, L H ^c   Salvadori, S ^d   Xia, Y ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAGLIARI   (Italy)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d UNIVERSITY OF FERRARA   (Italy)

Author keywords

opioid receptor; Anoxia; Cortex; Ionotropic glutamate receptor channels; K+ homeostasis; Na + channels

Indexed keywords

DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; IONOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM ION; SODIUM ION; TETRODOTOXIN; UFP 512; UNCLASSIFIED DRUG; VERATRIDINE;

ANIMAL TISSUE; ANOXIA; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; HISTOPATHOLOGY; MALE; NONHUMAN;

ANIMALS; CATIONS, MONOVALENT; CEREBRAL CORTEX; HYPOXIA, BRAIN; ION CHANNEL GATING; MALE; MICE; MICE, INBRED C57BL; NEURONS; POTASSIUM; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, OPIOID, DELTA; SODIUM; SODIUM CHANNELS; SODIUM-CALCIUM EXCHANGER;

EID: 62349101427     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-009-8759-5     Document Type: Article

References (53)

1. Ginsberg M. D. (2008) Neuroprotection for ischemic stroke: Past, present and future. Neuropharmacology 55, 363-389
2. Green A. R. (2008) Pharmacological approaches to acute ischaemic stroke: Reperfusion certainly, neuroprotection possibly. Br. J. Pharmacol. 153, S325-S338
3. Zhang J. H., Haddad G. G. and Xia Y. (2000) δ-, but not μ- and κ-, opioid receptor activation protects neocortical neurons from glutamate-induced excitotoxic injury. Brain Res. 885, 143-153
4. Zhang J. H., Gibney G. T., Zhao P. and Xia Y. (2002) Neuroprotective role of δ-opioid receptors in the cortical neurons. Am. J. Physiol. 282, C1225-C1234
5. Zhang J., Qian H., Zhao P., Hong S. S. and Xia Y. (2006) Rapid hypoxia preconditioning protects cortical neurons from glutamate toxicity through δ-opioid receptor. Stroke 37, 1094-1099
6. Ma M. C., Qian H., Ghassemi F., Zhao P. and Xia Y. (2005) Oxygen sensitive d-opioid receptor-regulated survival and death signals: Novel insights into neuronal preconditioning and protection. J. Biol. Chem. 280, 16208-16218
7. Borlongan C. V., Wang Y. and Su T. P. (2004) Delta opioid peptide (D-Ala 2, D-Leu 5) enkephalin: Linking hibernation and neuroprotection. Front. Biosci. 9, 3392-3398
8. Lim Y. J., Zheng S. and Zuo Z. (2004) Morphine preconditions Purkinje cells against cell death under in vitro simulated ischemia-reperfusion conditions. Anesthesiology 100, 562-568
9. Zhao P., Huang Y. and Zuo Z. (2006) Opioid preconditioning induces opioid receptor-dependent delayed neuroprotection against ischemia in rats. J. Neuropathol. Exp. Neurol. 65, 945-952
10. Su D. S., Wang Z. H., Zheng Y. J., Zhao Y. H. and Wang X. R. (2007) Dose-dependent neuroprotection of delta opioid peptide [D-Ala2, D-Leu5]enkephalin in neuronal death and retarded behavior induced by forebrain ischemia in rats. Neurosci. Lett. 423, 113-117
11. Charron C., Messier C. and Plamondon H. (2008) Neuroprotection and functional recovery conferred by administration of kappa- and delta- opioid agonists in a rat model of global ischemia. Physiol. Behav. 93, 502-511
12. Pamenter M. E. and Buck L. T. (2008) δ-opioid receptor antagonism induces NMDA receptor-dependent excitotoxicity in anoxic turtle cortex. J. Exp. Biol. 211, 3512-3517
13. + efflux and neuronal apoptosis. Science 284, 336-339
14. Yu S. P., Yeh C. H., Sensi S. L., Gwag B. J., Canzoniero L. M., Farhangrazi Z. S., Ying H. S., Tian M., Dugan L. L. and Choi D. W. (1997) Mediation of neuronal apoptosis by enhancement of outward potassium current. Science 278, 114-117
15. + release and cellular efflux in ischemic and apoptotic neuronal death. J. Neurochem. 86, 966-979
16. Wei L., Yu S. P., Gottron F., Snider B. J., Zipfei G. J. and Choi D. W. (2003) Potassium channel blockers attenuate hypoxia-and ischemia-induced neuronal death in vitro and in vivo. Stroke 34, 1281-1286
17. + homeostasis during anoxia and oxygen-glucose deprivation. J. Cereb. Blood Flow Metab. 27, 356-368
18. 2+ influx in the cortex during acute hypoxia. J. Cell. Physiol. 212, 60 -67
19. + entry in mouse cortex. Cereb. Cortex 18, 2217-2227
20. Friedman J. E. and Haddad G. G. (1994) Anoxia induces an increase in intracellular sodium in rat central neurons in vitro. Brain Res. 663, 329-334
21. Calabresi P., Marfia G. A., Centonze D., Pisani A. and Bernardi G. (1999) Sodium influx plays a major role in the membrane depolarization induced by oxygen and glucose deprivation in rat striatal spiny neurons. Stroke 30, 171-179
22. Banasiak K. J., Burenkova O. and Haddad G. G. (2004) Activation of voltage-sensitive sodium channels during oxygen deprivation leads to apoptotic neuronal death. Neuroscience 126, 31-44
23. 2+ homeostasis pathways, cell death and protection after oxygen-glucose-deprivation in organotypic hippocampal slice cultures. Neuroscience 128, 729-740
24. Sheldon C., Diarra A., Cheng Y. M. and Church J. (2004) Sodium influx pathways during and after anoxia in rat hippocampal neurons. J. Neurosci. 24, 11057-11069
25. Guatteo E., Mercuri N. B., Bernardi G. and Knöpfel T. (1998) Intracellular sodium and calcium homeostasis during hypoxia in dopamine neurons of rat substantia nigra pars compacta. J. Neurophysiol. 80, 2237-2243
26. Jiang C. and Haddad G. G. (1991) Effect of anoxia on intracellular and extracellular potassium activity in hypoglossal neurons in vitro. J. Neurophysiol. 66:103-111
27. +. Mol. Pharmacol. 56, 619-632
28. Lynch J. J. III, Yu S. P., Canzoniero L. M. T., Sensi S. L. and Choi D. W. (1995) Sodium channel blockers reduce oxygen-glucose deprivation-induced cortical neuronal injury when combined with glutamate receptor antagonists. J. Pharmacol. Exp. Ther. 273, 554-560
29. Fung M. L., Croning M. D. R. and Haddad G. G. (1999) Sodium homeostasis in rat hippocampal slices during oxygen and glucose deprivation: Role of voltage-sensitive sodium channels. Neurosci. Lett. 275, 41-44
30. Lopachin R. M., Gaughan C. L., Lehning E. J., Weber M. L. and Taylor C. P. (2001) Effects of ion channel blockade on the distribution of Na, K, Ca, and other elements in oxygen-glucose deprived CA1 hippocampal neurons. Neuroscience 103, 971-983
31. Raley-Susman K. M., Kass I. S., Cottrell J. E., Newman R. B., Chambers G. and Wang J. (2001) Sodium influx blockade and hypoxic damage to CA1 pyramidal neurons in rat hippocampal slices. J. Neurophysiol. 86, 2715-2726
32. 2+] elevations in cultured hippocampal CA1 neurons during anoxic depolarization. J. Neurochem. 100, 915-923
33. 2+ during a transient focal cerebral ischemia in the mouse. Cell Calcium 43, 482-491
34. + exchanger 1 null mutant mouse brain with epilepsy. Neurosci. Res. 53, 442-446
35. + exchanger 1 null mutant mouse. J. Neurophysiol. 89, 229-236
36. + channel expression in cortical neurons subjected to prolonged hypoxia in culture. Program No. 740. 6 SfN Abstract. Society for Neuroscience online
37. Ma M. C., Donnelly D. F. and Xia Y. (2004) Neuronal preconditioning inhibits hypoxia-induced sodium channel up-regulation via δ-opioid receptor. SfN Abstract. Society for Neuroscience online
38. Camacho A. and Massieu L. (2006) Role of glutamate transporters in the clearance and release of glutamate during ischemia and its relation to neuronal death. Arch. Med. Res. 37, 11-18
39. Mayer M. L. and Westbrook G. L. (1987) The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 28, 197-276
40. Tanaka E. and North R. A. (1994) Opioid actions on rat anterior cingulated cortex neurons in vitro. J. Neurosci. 14, 1106-1113
41. Ostermeier A. M., Schlosser B., Schwender D. and Sutor B. (2000) Activation of μ- and δ-opioid receptors causes presynaptic inhibition of glutamatergic excitation in neocortical neurons. Anesthesiology 93, 1053-1063
42. Wang X. M. and Mokha S. S. (1996) Opioids modulate N-methyl-D- aspartic acid (NMDA)-evoked responses of trigeminothalamic neurons. J. Neurophysiol. 76, 2093-2096
43. 2+ exchange currents in cortical neurons: Concomitant forward and reverse operation and effect of glutamate. Eur. J. Neurosci. 9, 1273-1281
44. Balboni G., Salvadori S., Guerrini R., Negri L., Giannini E., Jinsmaa Y., Bryant S. D. and Lazarus L. H. (2002) Potent δ-opioid receptor agonists containing the Dmt-Tic pharmacophore. J. Med. Chem. 45, 5556-5563
45. + channels in ion fluxes during hypoxia of rat hippocampal slices. J. Neurophysiol. 84, 1869-1880
46. + homeostasis protects organotypic hippocampal slice cultures from hypoxic/hypoglycemic injury. Neuropharmacology 39, 1779-1787
47. Kang X., Gu Q., Ding G. Chao D., Wang Y., Balboni G., Lazarus L. H. and Xia Y. (2008) Delta-opioid receptor activation and sodium channel inhibition in Xenopus oocytes. Acta Physiol. Sin. 60 (Suppl), 124
48. +] seen in rat dorsal hippocampus, in vivo, during transient hypoxia as measured by ion-selective microelectrodes. Br. J. Pharmacol. 100, 179
49. Vyklický L. Jr, Benveniste M. and Mayer M. L. (1990) Modulation of N-methyl-D-aspartic acid receptor desensitization by glycine in mouse cultured hippocampal neurons. J. Physiol. 428, 313-331
50. Wilding T. J. and Huettner J. E. (1997) Activation and desensitization of hippocampal kainate receptors. J. Neurosci. 17, 2713-2721
51. Law P-Y., Wong Y. H. and Loh H. H. (2000) Molecular mechanisms and regulation of opioid receptor signaling. Annu. Rev. Pharmacol. Toxicol. 40, 389-430
52. Szabo S. T., Machado-Vieira R., Yuan P., Wang Y., Wei Y., Falke C., Cirelli C., Tononi G., Manji H. K. and Du J. (2009) Glutamate receptors as targets of protein kinase C in the pathophysiology and treatment of animal models of Mania. Neuropharmacology 56, 47-55
53. Chen Y., Yu F. H., Surmeier D. J., Scheuer T. and Catterall W. A. (2006) Neuromodulation of Na+ channel slow inactivation via cAMP-dependent protein kinase and protein kinase C. Neuron 49, 409-420