Protein kinase Cγ mediates ethanol withdrawal hyper-responsiveness of NMDA receptor currents in spinal cord motor neurons

British Journal of Pharmacology

Volumn 144, Issue 3, 2005, Pages 301-307

  Li, Hui Fang ^a   Mochly Rosen, Daria ^a   Kendig, Joan J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium dependence; Ethanol withdrawal; Hyper responsiveness; Long term potentiation; NMDA; Protein kinase C

Indexed keywords

ALCOHOL; BICUCULLINE METHIODIDE; CYSTEINYLARGINYLLEUCYLVALYLLEUCYLALANYLSERINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C GAMMA; PROTEIN KINASE C INHIBITOR; STRYCHNINE; TETRODOTOXIN; UNCLASSIFIED DRUG; CENTRAL DEPRESSANT AGENT; PROTEIN KINASE C;

ALCOHOL WITHDRAWAL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NUCLEUS; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOPLASM; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MOTONEURON; NEWBORN; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SPINAL CORD MOTONEURON; ANIMAL; CELL MEMBRANE POTENTIAL; CELL NUCLEUS; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; ENZYMOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD; SPRAGUE DAWLEY RAT; WITHDRAWAL SYNDROME;

ANIMALS; CELL NUCLEUS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CYTOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; EXCITATORY POSTSYNAPTIC POTENTIALS; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE POTENTIALS; MOTOR NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 14644395589     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706033     Document Type: Article

References (49)

1. ABELIOVICH, A., CHEN, C., GODA, Y., SILVA, A.J., STEVENS, C.F. & TONEGAWA, S. (1993). Modified hippocampal long-term potentiation in PKC gamma-mutant mice. Cell, 75, 1253-1262.
2. ALLGAIER, C. (2002). Ethanol sensitivity of NMDA receptors. Neurochem. Int., 41, 377-382.
3. BOWERS, B.J. & WEHNER, J.M. (2001). Ethanol consumption and behavioral impulsivity are increased in protein kinase Cgamma null mutant mice. J. Neurosci., 21, RC180.
4. CHEN, L., WRIGHT, L.R., CHEN, C.H., OLIVER, S.F., WENDER, P.A. & MOCHLY-ROSEN, D. (2001). Molecular transporters for peptides: delivery of a cardioprotective epsilonPKC agonist peptide into cells and intact ischemic heart using a transport system, R(7). Chem. Biol., 8, 1123-1129.
5. DILDY-MAYFIELD, J.E. & HARRIS, R.A. (1995). Ethanol inhibits kainate responses of glutamate receptors expressed in Xenopus oocytes: role of calcium and protein kinase C. J. Neurosci., 15, 3162-3171.
6. FANG, Z., GONG, D., IONESCU, P., LASTER, M.J., EGER II, E.I. & KENDIG, J. (1997). Maturation decreases ethanol minimum alveolar anesthetic concentration (MAC) more than desflurane MAC in rats. Anesth. Analg., 84, 852-858.
7. FENG, J. & KENDIG, J.J. (1995a). N-methyl-D-aspartate receptors are implicated in hyperresponsiveness following naloxone reversal of alfentanil in isolated rat spinal cord. Neurosci. Lett., 189, 128-130.
8. FENG, J. & KENDIG, J.J. (1995b). Selective effects of alfentanil on nociceptive-related neurotransmission in neonatal rat spinal cord. Br. J. Anaesth., 74, 691-696.
9. GOLDSTEIN, D.B. & PAL, N. (1971). Alcohol dependence produced in mice by inhalation of ethanol: grading the withdrawal reaction. Science, 172, 288-290.
10. GROSSHANS, D.R. & BROWNING, M.D. (2001). Protein kinase C activation induces tyrosine phosphorylation of the NR2A and NR2B subunits of the NMDA receptor. J. Neurochem., 76, 737-744.
11. HARRIS, K.M., KONGSAMUT, S. & MILLER, R.J. (1986). Protein kinase C mediated regulation of calcium channels in PC-12 pheochromocytoma cells. Biochem. Biophys. Res. Commun., 134, 1298-1305.
12. HARRIS, R.A., MCQUILKIN, S.J., PAYLOR, R., ABELIOVICH, A., TONEGAWA, S. & WEHNER, J.M. (1995). Mutant mice lacking the gamma isoform of protein kinase C show decreased behavioral actions of ethanol and altered function of gamma-aminobutyrate type A receptors. Proc. Natl. Acad. Sci. U.S.A., 92, 3658-3662.
13. HASHIMOTO, T., ASE, K., SAWAMURA, S., KIKKAWA, U., SAITO, N., TANAKA, C. & NISHIZUKA, Y. (1988). Postnatal development of a brain-specific subspecies of protein kinase C in rat. J. Neurosci., 8, 1678-1683.
14. JIA, W.G., BEAULIEU, C., HUANG, F.L. & CYNADER, M.S. (1990). Cellular and subcellular localization of protein kinase C in cat visual cortex. Brain Res. Mol. Brain Res., 8, 311-317.
15. JOHNSON, J.A., GRAY, M.O., CHEN, C.H. & MOCHLY-ROSEN, D. (1996). A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J. Biol. Chem., 271, 24962-24966.
16. KIM, H.G., FOX, K. & CONNORS, B.W. (1995). Properties of excitatory synaptic events in neurons of primary somatosensory cortex of neonatal rats. Cereb. Cortex, 5, 148-157.
17. KOSE, A., ITO, A., SAITO, N. & TANAKA, C. (1990). Electron microscopic localization of gamma- and beta II-subspecies of protein kinase C in rat hippocampus. Brain Res., 518, 209-217.
18. LAI, C.C., CHANG, M.C. & LIN, H.H. (2004). Acute tolerance to ethanol inhibition of NMDA-induced responses in rat rostral ventrolateral medulla neurons. J. Biomed. Sci., 11, 482-492.
19. LI, H.F. & KENDIG, J.J. (2003a). Ethanol withdrawal hyper-responsiveness mediated by NMDA receptors in spinal cord motor neurons. Br. J. Pharmacol., 139, 73-80.
20. LI, H.F., WANG, M.Y., KNAPE, J. & KENDIG, J.J. (2003b). Ethanol tachyphylaxis in spinal cord motorneurons: role of metabotropic glutamate receptors. Br. J. Pharmacol., 138, 1417-1424.
21. LINDEN, D.J., WONG, K.L., SHEU, F.S. & ROUTTENBERG, A. (1988). NMDA receptor blockade prevents the increase in protein kinase C substrate (protein F1) phosphorylation produced by long-term potentiation. Brain Res., 458, 142-146.
22. LOZIER, A.P. & KENDIG, J.J. (1995). Long-term potentiation in an isolated peripheral nerve-spinal cord preparation. J. Neurophysiol., 74, 1001-1009.
23. LU, W.Y., XIONG, Z.G., LEI, S., ORSER, B.A., DUDEK, E., BROWNING, M.D. & MACDONALD, J.F. (1999). G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat. Neurosci., 2, 331-338.
24. MALINOW, R., SCHULMAN, H. & TSIEN, R.W. (1989). Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science, 245, 862-866.
25. MALMBERG, A.B., CHEN, C., TONEGAWA, S. & BASBAUM, A.I. (1997). Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science, 278, 279-283.
26. MAO, J., PRICE, D.D., PHILLIPS, L.L., LU, J. & MAYER, D.J. (1995). Increases in protein kinase C gamma immunoreactivity in the spinal cord dorsal horn of rats with painful mononeuropathy. Neurosci. Lett., 198, 75-78.
27. MARTIN, W.J., MALMBERG, A.B. & BASBAUM, A.I. (2001). PKCgamma contributes to a subset of the NMDA-dependent spinal circuits that underlie injury-induced persistent pain. J. Neurosci., 21, 5321-5327.
28. MCINTYRE, T.A., SOUDER, M.G., HARTL, M.W. & SHIBLEY, I.A. (1999). Ethanol-induced decrease of developmental PKC isoform expression in the embryonic chick brain. Brain Res. Dev. Brain Res., 117, 191-197.
29. MIKI, A. (1995). Developmental changes in the expression of alpha-, beta- and gamma-subspecies of protein kinase C at synapses in the ventral horn of the embryonic and postnatal rat spinal cord. Brain Res. Dev. Brain Res., 87, 46-54.
30. MIKI, A. (1996). Expression of alpha-, beta-, and gamma-subspecies of protein kinase C in the motor neurons in the embryonic and postnatal rat spinal cord. Neuroscience, 72, 805-814.
31. MIRSHAHI, T., ANDERS, D.L., RONALD, K.M. & WOODWARD, J.J. (1998). Intracellular calcium enhances the ethanol sensitivity of NMDA receptors through an interaction with the C0 domain of the NR1 subunit. J. Neurochem., 71, 1095-1107.
32. MORI, M., KOSE, A., TSUJINO, T. & TANAKA, C. (1990). Immunocytochemical localization of protein kinase C subspecies in the rat spinal cord: light and electron microscopic study. J. Comp. Neurol., 299, 167-177.
33. MORRISETT, R.A., REZVANI, A.M., OVERSTREET, D., JANOWSKY, D.S., WILSON, W.A. & SWARTZWELDER, H.S. (1990). MK-801 potently inhibits alcohol withdrawal seizures in rats. Eur. J. Pharmacol., 176, 103-105.
34. PEREZ-VELAZQUEZ, J.L., VALIANTE, T.A. & CARLEN, P.L. (1994). Changes in calcium currents during ethanol withdrawal in a genetic mouse model. Brain Res., 649, 305-309.
35. POLGAR, E., FOWLER, J.H., MCGILL, M.M. & TODD, A.J. (1999). The types of neuron which contain protein kinase C gamma in rat spinal cord. Brain Res., 833, 71-80.
36. RIPLEY, T.L., WHITTINGTON, M.A., BUTTERWORTH, A.R. & LITTLE, H.J. (1996). Ethanol withdrawal hyperexcitability in vivo and in isolated mouse hippocampal slices. Alcohol Alcohol., 31, 347-357.
37. SAITO, N. & SHIRAI, Y. (2002). Protein kinase Cgamma (PKCgamma): function of neuron specific isotype. J. Biochem. (Tokyo), 132, 683-687.
38. SCHECHTMAN, D. & MOCHLY-ROSEN, D. (2002). Isozyme-specific inhibitors and activators of protein kinase C. Methods Enzymol., 345, 470-489.
39. SIGGINS, G.R., MARTIN, G., ROBERTO, M., NIE, Z., MADAMBA, S. & DE LECEA, L. (2003). Glutamatergic transmission in opiate and alcohol dependence. Ann. NY Acad. Sci., 1003, 196-211.
40. STUBBS, C.D. & SLATER, S.J. (1999). Ethanol and protein kinase C. Alcohol. Clin. Exp. Res., 23, 1552-1560.
41. SUBRAMANIAM, S. & MCGONIGLE, P. (1994). Regional profile of developmental changes in the sensitivity of the N-methyl-D-aspartate receptor to polyamines. J. Neurochem., 62, 1408-1415.
42. THOMAS, M.P., MONAGHAN, D.T. & MORRISETT, R.A. (1998). Evidence for a causative role of N-methyl-D-aspartate receptors in an in vitro model of alcohol withdrawal hyperexcitability. J. Pharmacol. Exp. Ther., 287, 87-97.
43. WANG, M.Y. & KENDIG, J.J. (2000). Patch clamp studies of motor neurons in spinal cord slices: a tool for high-resolution analysis of drug actions. Acta Pharmacol Sin., 21, 507-515.
44. WANG, M.Y., RAMPIL, I.J. & KENDIG, J.J. (1999). Ethanol directly depresses AMPA and NMDA glutamate currents in spinal cord motor neurons independent of actions on GABAA or glycine receptors. J. Pharmacol. Exp. Ther., 290, 362-367.
45. WOLF, M., BURGESS, S., MISRA, U.K. & SAHYOUN, N. (1986). Postsynaptic densities contain a subtype of protein kinase C. Biochem. Biophys. Res. Commun., 140, 691-698.
46. WONG, S.M., FONG, E., TAUCK, D.L. & KENDIG, J.J. (1997). Ethanol as a general anesthetic: actions in spinal cord. Eur. J. Pharmacol., 329, 121-127.
47. WONG, S.M., TAUCK, D.L., FONG, E.G. & KENDIG, J.J. (1998). Glutamate receptor-mediated hyperexcitability after ethanol exposure in isolated neonatal rat spinal cord. J. Pharmacol. Exp. Ther., 285, 201-207.
48. WONG, S.M.E., SWEITZER, S.M, PETERS, M.C. & KENDIG, J.J. (2004). Hyperresponsiveness on washout of volatile anesthetics from isolated spinal cord compared to withdrawal from ethanol. Anethesia and Analgesia (in press).
49. ZISKIND-CONHAIM, L., GAO, B.X. & HINCKLEY, C. (2003). Ethanol dual modulatory actions on spontaneous postsynaptic currents in spinal motoneurons. J. Neurophysiol., 89, 806-813.