Examining protection from anoxic depolarization by the drugs dibucaine and carbetapentane using whole cell recording from CA1 neurons

Journal of Neurophysiology

Volumn 107, Issue 8, 2012, Pages 2083-2095

  White, Sean H ^a   Devin Brisson, C ^a   David Andrew, R ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Neuroprotection; Pyramidal; Stroke

Indexed keywords

CINCHOCAINE; PENTOXYVERINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN HYPOXIA; BRAIN INFARCTION; CONTROLLED STUDY; DEPOLARIZATION; DRUG BINDING; GRAY MATTER; HYPERPOLARIZATION; IN VIVO STUDY; LIGHT; MALE; MEMBRANE POTENTIAL; NERVE CELL EXCITABILITY; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STROKE; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; CELL HYPOXIA; CYCLOPENTANES; DIBUCAINE; MALE; NEURONS; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84859741482     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00701.2011     Document Type: Article

References (67)

1. Alonso G, Phan V, Guillemain I, Saunier M, Legrand A, Anoal M, Maurice T. Immunocytochemical localization of the sigma(1) receptor in the adult rat central nervous system. Neuroscience 97: 155-170, 2000.
2. Anderson TR, Jarvis CR, Biedermann AJ, Molnar C, Andrew RD. Blocking the anoxic depolarization protects without functional compromise following simulated stroke in cortical brain slices. J Neurophysiol 93: 963-979, 2005.
3. Andrew RD, Biedermann AJ, Anderson TR, Jarvis CR. Imaging and preventing spreading depression independent of cerebral blood flow. In: Brain Activation and CBF Control, edited by Tomita I, Kanno I, and Hamel E. Amsterdam: Elsevier Science, 2002, p. 421-437.
4. Andrew RD, Labron MW, Boehnke SE, Carnduff L, Kirov SA. Physiological evidence that pyramidal neurons lack functional water channels. Cereb Cortex 17: 787-802, 2007.
5. Astman N, Gutnick MJ, Fleidervish IA. Persistent sodium current in layer 5 neocortical neurons is primarily generated in the proximal axon. J Neurosci 26: 3465-3473, 2006.
6. Aydar E, Palmer CP, Klyachko VA, Jackson MB. The sigma receptor as a ligand-regulated auxiliary potassium channel subunit. Neuron 34: 399-410, 2002.
7. Back T, Ginsberg MD, Dietrich WD, Watson BD. Induction of spreading depression in the ischemic hemisphere following experimental middle cerebral artery occlusion: effect on infarct morphology. J Cereb Blood Flow Metab 16: 202-213, 1996.
8. Bekkers JM. Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large layer 5 cortical pyramidal neurons of the rat. J Physiol 525: 611-620, 2000.
9. Brown DA, Gahwiler BH, Griffith WH, Halliwell JV. Membrane currents in hippocampal neurons. Prog Brain Res 83: 141-160, 1990.
10. Busch E, Gyngell ML, Eis M, Hoehn-Berlage M, Hossmann KA. Potassium-induced cortical spreading depressions during focal cerebral ischemia in rats: contribution to lesion growth assessed by diffusion-weighted NMR and biochemical imaging. J Cereb Blood Flow Metab 16: 1090-1099, 1996.
11. 3H]batrachotoxinin-a 20 alpha-benzoate binding in a vesicular preparation from guinea pig cerebral cortex. Mol Pharmacol 23: 350-358, 1983.
12. Czeh G, Aitken PG, Somjen GG. Membrane currents in CA1 pyramidal cells during spreading depression (SD) and SD-like hypoxic depolarization. Brain Res 632: 195-208, 1993.
13. Dohmen C, Sakowitz OW, Fabricius M, Bosche B, Reithmeier T, Ernestus RI, Brinker G, Dreier JP, Woitzik J, Strong AJ, Graf R. Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 63: 720-728, 2008.
14. Douglas HD, Callaway JK, Sword J, Kirov SA, Andrew RD. Potent inhibition of anoxic depolarization by the sodium channel blocker dibucaine. J Neurophysiol 105: 1482-1494, 2011.
15. Fabricius M, Fuhr S, Bhatia R, Boutelle M, Hashemi P, Strong AJ, Lauritzen M. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 129: 778-790, 2006.
16. Farkas E, Pratt R, Sengpiel F, Obrenovitch TP. Direct, live imaging of cortical spreading depression and anoxic depolarisation using a fluorescent, voltage-sensitive dye. J Cereb Blood Flow Metab 28: 251-262, 2008.
17. Folbergrova J, Memezawa H, Smith ML, Siesjo BK. Focal and perifocal changes in tissue energy state during middle cerebral artery occlusion in normo- and hyperglycemic rats. J Cereb Blood Flow Metab 12: 25-33, 1992.
18. Fung ML, Croning MD, Haddad GG. Sodium homeostasis in rat hippocampal slices during oxygen and glucose deprivation: role of voltage-sensitive sodium channels. Neurosci Lett 275: 41-44, 1999.
19. Gundlach AL, Largent BL, Snyder SH. Autoradiographic localization of sigma receptor binding sites in guinea pig and rat central nervous system with (+)3H-3-(3-hydroxyphenyl)-N-(1-propyl)piperidine. J Neurosci 6: 1757-1770, 1986.
20. Hammarström AK, Gage PW. Oxygen-sensing persistent sodium channels in rat hippocampus. J Physiol 529: 107-118, 2000.
21. Hanner M, Moebius FF, Flandorfer A, Knaus HG, Striessnig J, Kempner E, Glossmann H. Purification, molecular cloning, and expression of the mammalian sigma1-binding site. Proc Natl Acad Sci USA 93: 8072-8077, 1996.
22. Hartings JA, Rolli ML, Lu XC, Tortella FC. Delayed secondary phase of peri-infarct depolarizations after focal cerebral ischemia: relation to infarct growth and neuroprotection. J Neurosci 23: 11602-11610, 2003.
23. Hayashi T, Maurice T, Su TP. Ca(2+) signaling via sigma(1)-receptors: novel regulatory mechanism affecting intracellular Ca(2+) concentration. J Pharmacol Exp Ther 293: 788-798, 2000.
24. Hernandez-Caceres J, Macias-Gonzalez R, Brozek G, Bures J. Systemic ketamine blocks cortical spreading depression but does not delay the onset of terminal anoxic depolarization in rats. Brain Res 437: 360-364, 1987.
25. Hille B. Modification of gating in voltage-sensitive channels. In: Ion Channels of Excitable Membranes. Sunderland, MA: Sinauer, 2001, p. 635-662.
26. 2+ channels? Br J Anaesth 78: 185-188, 1997.
27. Hoehn K, Watson TW, MacVicar BA. A novel, TTX-insensitive, slow sodium current in striatal and hippocampal neurons. Neuron 10: 543-552, 1993.
28. Ishihara K, Akbar M, Sasa M. Effects of OPC-24439, a sigma ligand, on neuronal activities in the hippocampus. Nihon Yakurigaku Zasshi 114: 204-208, 1999.
29. Jarvis CR, Anderson TR, Andrew RD. Anoxic depolarization mediates acute damage independent of glutamate in neocortical brain slices. Cereb Cortex 11: 249-259, 2001.
30. Jarvis CR, Lilge L, Vipond GJ, Andrew RD. Interpretation of intrinsic optical signals and calcein fluorescence during acute excitotoxic insult in the hippocampal slice. Neuroimage 10: 357-372, 1999.
31. Kaminogo M, Suyama K, Ichikura A, Onizuka M, Shibata S. Anoxic depolarization determines ischemic brain injury. Neurol Res 20: 343-348, 1998.
32. Kaneda M, Oyama Y, Ikemoto Y, Akaike N. Blockade of the voltagedependent sodium current in isolated rat hippocampal neurons by tetrodotoxin and lidocaine. Brain Res 484: 348-351, 1989.
33. Katnik C, Guerrero WR, Pennypacker KR, Herrera Y, Cuevas J. Sigma-1 receptor activation prevents intracellular calcium dysregulation in cortical neurons during in vitro ischemia. J Pharmacol Exp Ther 319: 1355-1365, 2006.
34. + channel inactivation gate peptides in phosphatidylserine suspensions as studied by 1H-NMR spectroscopy. Chem Pharm Bull (Tokyo) 48: 1293-1298, 2000.
35. + channel inactivation gate peptide as studied by 2H- and 1H-NMR spectroscopies. Biophys J 71: 1191-1207, 1996.
36. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 79: 1432-1568, 1999.
37. Maurice T, Su TP. The pharmacology of sigma-1 receptors. Pharmacol Ther 124: 195-206, 2009.
38. Muller M, Somjen GG. Intrinsic optical signals in rat hippocampal slices during hypoxia-induced spreading depression-like depolarization. J Neurophysiol 82: 1818-1831, 1999.
39. + channels in ion fluxes during hypoxia of rat hippocampal slices. J Neurophysiol 84: 1869-1880, 2000.
40. Murphy TH, Li P, Betts K, Liu R. Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J Neurosci 28: 1756-1772, 2008.
41. 14C]2-deoxyglucose phosphorylation. J Cereb Blood Flow Metab 6: 607-615, 1986.
42. Nedergaard M, Hansen AJ. Characterization of cortical depolarizations evoked in focal cerebral ischemia. J Cereb Blood Flow Metab 13: 568-574, 1993.
43. Nellgard B, Wieloch T. NMDA-receptor blockers but not NBQX, an AMPAreceptor antagonist, inhibit spreading depression in the rat brain. Acta Physiol Scand 146: 497-503, 1992.
44. +current in rat hippocampal neurones via protein kinase C. J Physiol 503: 479-488, 1997.
45. Obeidat AS, Andrew RD. Spreading depression determines acute cellular damage in the hippocampal slice during oxygen/glucose deprivation. Eur J Neurosci 10: 3451-3461, 1998.
46. Obeidat AS, Jarvis CR, Andrew RD. Glutamate does not mediate acute neuronal damage after spreading depression induced by O2/glucose deprivation in the ippocampal slice. J Cereb Blood Flow Metab 20: 412-422, 2000.
47. Obrenovitch TP, Urenjak J, Zilkha E, Jay TM. Excitotoxicity in neurological disorders-the glutamate paradox. Int J Dev Neurosci 18: 281-287, 2000.
48. + channel in rat hippocampal neurones. Br J Pharmacol 105: 63-70, 1992.
49. Polischuk TM, Jarvis CR, Andrew RD. Intrinsic optical signaling denoting neuronal damage in response to acute excitotoxic insult by domoic acid in the hippocampal slice. Neurobiol Dis 4: 423-437, 1998.
50. 3H]batrachotoxinin A 20-alpha-benzoate to sodium channels by local anesthetics. Mol Pharmacol 25: 219-227, 1984.
51. + channels by local anesthetics. Science 265: 1724-1728, 1994.
52. + currents in neurones: types, physiological roles and modulation. Trends Neurosci 19: 150-154, 1996.
53. Somjen GG. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81: 1065-1096, 2001.
54. + conductance in rat optic nerve axons. Proc Natl Acad Sci USA 90: 6976-6980, 1993.
55. Sugiyama K, Muteki T. Local anesthetics depress the calcium current of rat sensory neurons in culture. Anesthesiology 80: 1369-1378, 1994.
56. Takano K, Latour LL, Formato JE, Carano RA, Helmer KG, Hasegawa Y, Sotak CH, Fisher M. The role of spreading depression in focal ischemia evaluated by diffusion mapping. Ann Neurol 39: 308-318, 1996.
57. Tanaka E, Yamamoto S, Kudo Y, Mihara S, Higashi H. Mechanisms underlying the rapid depolarization produced by deprevation of oxygen and glucose in rat hippocampal CA1 neurons in vitro. J Neurophysiol 78: 891-902, 1997.
58. + currents that fail to inactivate. Trends Neurosci 16: 455-460, 1993.
59. Taylor CP, Weber ML, Gaughan CL, Lehning EJ, LoPachin RM. Oxygen/glucose deprivation in hippocampal slices: altered intraneuronal elemental composition predicts structural and functional damage. J Neurosci 19: 619-629, 1999.
60. Thompson RJ, Zhou N, MacVicar BA. Ischemia opens neuronal gap junction hemichannels. Science 312: 924-927, 2006.
61. + channels: a rational and effective strategy against ischemic brain damage. Pharmacol Rev 48: 21-67, 1996.
62. Weber ML, Taylor CP. Damage from oxygen and glucose deprivation in hippocampal slices is prevented by tetrodotoxin, lidocaine and phenytoin without blockade of action potentials. Brain Res 664: 167-177, 1994.
63. Wilke RA, Mehta RP, Lupardus PJ, Chen Y, Ruoho AE, Jackson MB. Sigma receptor photolabeling and sigma receptor-mediated modulation of potassium channels in tumor cells. J Biol Chem 274: 18387-18392, 1999.
64. Wong BY, Coulter DA, Choi DW, Prince DA. Dextrorphan and dextromethorphan, common antitussives, are antiepileptic and antagonize N-methyl-D-aspartate in brain slices. Neurosci Lett 85: 261-266, 1988.
65. Xie Y, Dengler K, Zacharias E, Wilffert B, Tegtmeier F. Effects of the sodium channel blocker tetrodotoxin (TTX) on cellular ion homeostasis in rat brain subjected to complete ischemia. Brain Res 652: 216-224, 1994.
66. Yamamoto S, Tanaka E, Shoji Y, Kudo Y, Inokuchi H, Higashi H. Factors that reverse the persistent depolarization produced by deprivation of oxygen and glucose in rat hippocampal CA1 neurons in vitro. J Neurophysiol 78: 903-911, 1997.
67. Zhang H, Cuevas J. Sigma receptor activation blocks potassium channels and depresses neuroexcitability in rat intracardiac neurons. J Pharmacol Exp Ther 313: 1387-1396, 2005.