Cortical δ-opioid receptors potentiate K+ homeostasis during anoxia and oxygen-glucose deprivation

Journal of Cerebral Blood Flow and Metabolism

Volumn 27, Issue 2, 2007, Pages 356-368

  Chao, Dongman ^a   Donnelly, David F ^a   Feng, Yin ^a   Bazzy Asaad, Alia ^a   Xia, Ying ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

opioid receptors; Extracellular potassium; Hypoxia; Ischemia; Neuronal protection; Protein kinases

Indexed keywords

CHELERYTHRINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR ANTAGONIST; ENKEPHALIN[2 DEXTRO ALANINE 5 DEXTRO LEUCINE]; GLUCOSE; NALTRINDOLE; OXYGEN; PHORBOL 13 ACETATE 12 MYRISTATE; POTASSIUM ION; SULFONAMIDE;

ANIMAL MODEL; ANIMAL TISSUE; ANOXIA; ARTICLE; BRAIN HYPOXIA; BRAIN SLICE; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; DENDRITIC CELL; ENZYME INHIBITION; EXCITOTOXICITY; GLUCOSE HOMEOSTASIS; MALE; MICROELECTRODE; MOLECULAR MECHANICS; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL;

ANALGESICS, OPIOID; ANIMALS; CEREBRAL CORTEX; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENKEPHALIN, LEUCINE-2-ALANINE; ENZYME INHIBITORS; EXTRACELLULAR SPACE; GLUCOSE; HOMEOSTASIS; HYPOXIA, BRAIN; INDICATORS AND REAGENTS; MALE; MICE; MICE, INBRED C57BL; NALTREXONE; POTASSIUM; PROTEIN KINASE C; RECEPTORS, OPIOID, DELTA; SIGNAL TRANSDUCTION;

EID: 33846423542     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.jcbfm.9600352     Document Type: Article

References (60)

1. 2+ currents in rat sensory neurons. J Neurosci 19:8337-48
2. + selective microelectrodes with low electrical membrane resistance. Neurosci Lett 74:221-6
3. Ammon-Treiber S, Stolze D, Schrõder H, Loh H, Hõllt V (2005) Effects of opioid antagonists and morphine in a hippocampal hypoxia/hypoglycemia model. Neuropharmacology 49:1160-9
4. Balboni G, Salvadori S, Guerrini R, Negri L, Giannini E, Jinsmaa Y, Bryant SD, Lazarus LH (2002) Potent δ-opioid receptor agonists containing the Dmt-Tic pharmacophore. J Med Chem 45:5556-63
5. Bausch SB, Patterson TA, Appleyard SM, Chavkin C (1995) Immunocytochemical localization of delta opioid receptors in mouse brain. J Chem Neuroanat 8:175-89
6. Borlongan CV, Wang Y, Su TP (2004) Delta opioid peptide (D-Ala 2, D-Leu 5) enkephalin: linking hibernation and neuroprotection. Front Biosci 9:3392-8
7. Boutin H, Dauphin F, MacKenzie ET, Jauzac P (1999) Differential time-course decreases in nonselective, μ-, δ-, and κ-opioid receptors after focal cerebral ischemia in mice. Stroke 30:1271-7
8. Chaki S, Muramatsu M, Otomo S (1994) Involvement of protein kinase C activation in regulation of acetylcholine release from rat hippocampal slices by minaprine. Neurochem Int 24:37-41
9. Erdemli G, Xu YZ, Krnjević K (1998) Potassium conductance causing hyperpolarization of CA1 hippocampal neurons during hypoxia. J Neurophysiol 80:2378-90
10. Galeffi F, Sah R, Pond BB, George A, Schwartz-Bloom RD (2004) Changes in intracellular chloride after oxygen-glucose deprivation of the adult hippocampal slice: effect of diazepam. J Neurosci 24:4478-88
11. Grega DS, Werz MA, Macdonald RL (1987) Forskolin and phorbol esters reduce the same potassium conductance of mouse neurons in culture. Science 235:345-8
12. Hansen AJ (1978) The extracellular potassium concentration in brain cortex following ischemia in hypo- and hyperglycemic rats. Acta Physiol Scand 102:324-9
13. Hansen AJ (1985) Effect of anoxia on ion distribution in the brain. Physiol Rev 65:101-48
14. Hauser KF, Gurwell JA, Turbek CS (1994) Morphine inhibits purkinje cell survival and dendritic differentiation in organotypic cultures of the mouse cerebellum. Exp Neurol 130:95-105
15. Hiller JM, Fan LQ (1996) Laminar distribution of the multiple opioid receptors in the human cerebral cortex. Neurochem Res 21:1333-45
16. Hu S, Sheng WS, Lokensgard JR, Peterson PK (2002) Morphine induces apoptosis of human microglia and neurons. Neuropharmacology 42:829-36
17. Huang H, Gao TM, Gong LW, Zhuang ZY, Li X (2001) Potassium channel blocker TEA prevents CA1 hippocampal injury following transient forebrain ischemia in adult rats. Neurosci Lett 305:83-6
18. Jiang C, Haddad GG (1991) Effect of anoxia on intracellular and extracellular potassium activity in hypoglossal neurons in vitro. J Neurophysiol 66:103-11
19. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045-56
20. Leenders AGM, Sheng ZH (2005) Modulation of neurotransmitter release by the second messenger-activated protein kinases: implications for presynaptic plasticity. Pharmacol Ther 105:69-84
21. Liao SL, Chen WY, Raung SL, Chen CJ (2003) Neuroprotection of nalolone against ischemic injury in rats: role of mu receptor antagonism. Neurosci Lett 345:169-72
22. Libien J, Sacktor TC, Kass IS (2005) Magnesium blocks the loss of protein kinase C, leads to a transient translocation of PKCa and PKCe, and improves recovery after anoxia in rat hippocampal slices. Mol Brain Res 136:104-11
23. Lim YJ, Zheng S, Zuo Z (2004) Morphine preconditions purkinje cells against cell death under in vitro simulated ischemia-reperfusion conditions. Anesthesiology 100:562-8
24. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431-568
25. + release and cellular efflux in ischemic and apoptotic neuronal death. J Neurochem 86:966-79
26. Lopachin RM, Gaughan CL, Lehning EJ, Weber ML, Taylor CP (2001) Effects of ion channel blockade on the distribution of Na, K, Ca, and other elements in oxygen-glucose deprived CA1 hippocampal neurons. Neuroscience 103:971-83
27. Lou LG, Pei G (1997) Modulation of protein kinase C and cAMP-dependent protein kinase by opioid. Biochem Biophys Res Commun 236:626-9
28. Ma MC, Qian H, Ghassemi F, Zhao P, Xia Y (2005) Oxygen sensitive δ-opioid receptor-regulated survival and death signals: novel insights into neuronal preconditioning and protection. J Biol Chem 280:16208-18
29. Majewski H, Iannazzo L (1998) Protein kinase C: a physiological mediator of enhanced transmitter output. Prog Neurobiol 55:463-75
30. Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ (1987) Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J Neurosci 7:2445-64
31. 2+ homeostasis pathways, cell death and protection after oxygen-glucose-deprivation in organotypic hippocampal slice cultures. Neuroscience 128:729-40
32. Mayfield KP, Kozak W, Malvin GM, Porreca F (1996) Hypoxia decreases opioid delta receptor expression in mouse brain. Neuroscience 72:785-9
33. Moore SD, Madamba SG, Schweitzer P, Siggins GR (1994) Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro. J Neurosci 14:809-20
34. + channels in ion fluxes during hypoxia of rat hippocampal slices. J Neurophysiol 84:1869-80
35. + concentrations, extra- and intracellular voltages, and the effect of TTX in hypoxic rat hippocampal slices. J Neurophysiol 83:735-45
36. Nieber K (1999) Hypoxia and neuronal function under in vitro conditions. Pharmacol Ther 82:71-86
37. Ostermeier AM, Schlösser B, Schwender D, Sutor B (2000) Activation of μ- and δ-opioid receptors causes presynaptic inhibition of glutamatergic excitation in neocortical neurons. Anesthesiology 93:1053-63
38. Raley-Susman KM, Kass IS, Cottrell JE, Newman RB, Chambers G, Wang J (2001) Sodium influx blockade and hypoxic damage to CA1 pyramidal neurons in rat hippocampal slices. J Neurophysiol 86:2715-26
39. Raval AP, Dave KR, Mochly-Rosen D, Sick TJ, Pérez-Pinzón MA (2003) εPKC is required for the induction of tolerance by ischemic and NMDA-mediated preconditioning in the organotypic hippocampal slice. J Neurosci 23:384-91
40. + in regulating hypoxic cerebral blood flow in the rat: effect of glibenclamide and ouabain. Am J Physiol 270:H45-52
41. Roberts Jr EL (1993) Glycolysis and recovery of potassium ion homeostasis and synaptic transmission in hippocampal slices after anoxia or stimulated potassium release. Brain Res 620:251-8
42. Selvatici R, Marino S, Piubello C, Rodi D, Beani L, Gandini E, Siniscalchi A (2002) Protein kinase C activity, translocation, and selective isoform subcellular redistribution in the rat cerebral cortex after in vitro ischemia. J Neurosci Res 71:64-71
43. Sick TJ, Rosenthal M, LaManna JC, Lutz PL (1982) Brain potassium ion homeostasis, anoxia, and metabolic inhibition in turtles and rats. Am J Physiol 243:R281-8
44. Stanzione P, Stefani A, Calabresi P, Mercuri NB, Bernardi G (1989) Met- and leu-enkephalins inhibit rat cortical neurons intracellularly recorded in vivo while morphine excites them: evidence for naloxone-sensitive and naloxone-insensitive effects. Exp Brain Res 77:302-8
45. 5-enkephalin immunoreactivity in rat insular cortex. Brain Res 700:25-39
46. Tanaka E, North RA (1994) Opioid actions on rat anterior cingulate cortex neurons in vitro. J Neurosci 14:1106-13
47. Tanaka K (2001) Alteration of second messengers during acute cerebral ischemia-adenylate cyclase, cyclic AMP-dependent protein kinase, and cyclic AMP response element binding protein. Prog Neurobiol 65:173-207
48. Thorlin T, Eriksson PS, Persson PAI, Åberg ND, Hansson E, Rönnbäck L (1998) Delta-opioid receptors on astroglial cells in primary culture: mobilization of intracellular free calcium via a pertussis sensitive G protein. Neuropharmacology 37:299-311
49. Toselli M, Tosetti P, Taglietti V (1999) Kinetic study of N-type calcium current modulation by δ-opioid receptor activation in the mammalian cell line NG108-15. Biophys J 76:2560-74
50. 2+ uptake and glutamate release in rat cerebral cortex in primary culture. J Neurochem 68:517-24
51. Wei L, Yu SP, Gottron F, Snider BJ, Zipfei GJ, Choi DW (2003) Potassium channel blockers attenuate hypoxia-and ischemia-induced neuronal death in vitro and in vivo. Stroke 34:1281-6
52. Xia Y, Haddad GG (2001) Major difference in the expression of μ- and δ-opioid receptors between turtle and rat brain. J Comp Neurol 436:202-10
53. + efflux in apoptosis induced by AMPA and kainate in mouse cortical neurons. Neuroscience 108:61-7
54. Yao L, Fan P, Jiang Z, Mailliard WS, Gordon AS, Diamond I (2003) Addicting drugs utilize a synergistic molecular mechanism in common requiring adenosine and Gi-βγ dimers. Proc Natl Acad Sci USA 100:14379-84
55. Yu SP, Yeh CH, Sensi SL, Gwag BJ, Canzoniero LM, Farhangrazi ZS, Ying HS, Tian M, Dugan LL, Choi DW (1997) Mediation of neuronal apoptosis by enchancement of outward potassium current. Science 278:114-7
56. + efflux and neuronal apoptosis. Science 284:336-9
57. Yuan A, Santi CM, Wei A, Wang Z-W, Pollak K, Nonet M, Kaczmarek L, Crowder CM, Salkoff L (2003) The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron 37:765-73
58. Zhang JH, Gibney GT, Zhao P, Xia Y (2002) Neuroprotective role of δ-opioid receptors in the cortical neurons. Am J Physiol Cell Physiol 282:C1225-34
59. Zhang JH, Haddad GG, Xia Y (2000) δ-, but not μ- and κ-, opioid receptor activation protects neocortical neurons from glutamate-induced excitotoxic injury. Brain Res 885:143-53
60. Zhang J, Qian H, Zhao P, Hong SS, Xia Y (2006) Rapid hypoxia preconditioning protects cortical neurons from glutamate toxicity through δ-opioid receptor. Stroke 37:1094-9