Molecular mechanisms of analgesia induced by opioids and ethanol: Is the GIRK channel one of the keys?

Neuroscience Research

Volumn 44, Issue 2, 2002, Pages 121-131

  Ikeda, Kazutaka ^a,b   Kobayashi, Toru ^c   Kumanishi, Toshiro ^c,d   Yano, Ryoji ^b   Sora, Ichiro ^a,e   Niki, Hiroaki ^b  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c NIIGATA UNIVERSITY   (Japan)

^d Niigata Longevity Research Institute   (Japan)

^e TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Analgesia; Ethanol; G protein activated inwardly rectifying potassium channel; Kir3; Opioid; Opioid receptor; Pain

Indexed keywords

ALCOHOL; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE LIPID; OPIATE; OPIATE RECEPTOR; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL; NARCOTIC ANALGESIC AGENT; POTASSIUM CHANNEL;

ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONTROLLED STUDY; KNOCKOUT MOUSE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PAIN ASSESSMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; ANIMAL; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; PAIN; PATHOPHYSIOLOGY;

ANALGESICS, OPIOID; ANIMALS; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; ETHANOL; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GTP-BINDING PROTEINS; HUMANS; MICE; MODELS, ANIMAL; PAIN; POTASSIUM CHANNELS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RECEPTORS, OPIOID;

EID: 0036781281     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-0102(02)00094-9     Document Type: Article

References (123)

1. Abel T., Nguyen P.V., Barad M., Deuel T.A., Kandel E.R., Bourtchouladze R. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell. 88:1997;615-626.
2. Basbaum A.I., Fields H.L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci. 7:1984;309-338.
3. Blednov Y.A., Stoffel M., Chang S.R., Harris R.A. Potassium channels as targets for ethanol: studies of G-protein-coupled inwardly rectifying potassium channel 2 (GIRK2) null mutant mice. J. Pharmacol. Exp. Ther. 298:2001;521-530.
4. Bowers B.J., Wehner J.M. Ethanol consumption and behavioral impulsivity are increased in protein kinase Cγ null mutant mice. J. Neurosci. 21:2001;RC 180.
5. Brown A.M., Birnbaumer L. Ionic channels and their regulation by G protein subunits. Annu. Rev. Physiol. 52:1990;197-213.
6. 2): a potent and specific agonist for morphine μ receptors. Science. 212:1981;75-77.
7. Chu B., Treistman S.N. Modulation of two cloned potassium channels by 1-alkanols demonstrates different cutoffs. Alcohol Clin. Exp. Res. 21:1997;1103-1107.
8. Connor M., Schuller A., Pintar J.E., Christie M.J. Mu-opioid receptor modulation of calcium channel current in periaqueductal grey neurons from C57BL6/J mice and mutant mice lacking MOR-1. Br. J. Pharmacol. 126:1999;1553-1558.
9. + current expressed in Xenopus oocytes. Proc. Natl. Acad. Sci. USA. 90:1993;6957-6960.
10. Covarrubias M., Vyas T.B., Escobar L., Wei A. Alcohols inhibit a cloned potassium channel at a discrete saturable site. Insights into the molecular basis of general anesthesia. J. Biol. Chem. 270:1995;19408-19416.
11. Covernton P.J., Connolly J.G. Differential modulation of rat neuronal nicotinic receptor subtypes by acute application of ethanol. Br. J. Pharmacol. 122:1997;1661-1668.
12. Deitrich R.A., Dunwiddie T.V., Harris R.A., Erwin V.G. Mechanism of action of ethanol: initial central nervous system actions. Pharmacol. Rev. 41:1989;489-537.
13. Diamond I., Gordon A.S. Cellular and molecular neuroscience of alcoholism. Physiol. Rev. 77:1997;1-20.
14. Dopico A.M., Chu B., Lemos J.R., Treistman S.N. Alcohol modulation of calcium-activated potassium channels. Neurochem. Int. 35:1999;103-106.
15. Doupnik C.A., Davidson N., Lester H.A. The inward rectifier potassium channel family. Curr. Opin. Neurobiol. 5:1995;268-277.
16. 2 (Tyr-W-MIF-1). Peptides. 13:1992;623-631.
17. Evans C.J., Keith D.E. Jr., Morrison H., Magendzo K., Edwards R.H. Cloning of a delta opioid receptor by functional expression. Science. 258:1992;1952-1955.
18. Fadda F., Rossetti Z.L. Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Prog. Neurobiol. 56:1998;385-431.
19. Filliol D., Ghozland S., Chluba J., Martin M., Matthes H.W., Simonin F., Befort K., Gaveriaux-Ruff C., Dierich A., Lemeur M., Valverde O., Maldonado R., Kieffer B.L. Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses. Nat. Genet. 25:2000;195-200.
20. Fuchs P.N., Roza C., Sora I., Uhl G., Raja S.N. Characterization of mechanical withdrawal responses and effects of mu-, delta- and kappa-opioid agonists in normal and mu-opioid receptor knockout mice. Brain Res. 821:1999;480-486.
21. Fukuda K., Kato S., Morikawa H., Shoda T., Mori K. Functional coupling of the delta-, mu-, and kappa-opioid receptors to MAP-kinase and arachidonate release in Chinese hamster ovary cells. J. Neurochem. 67:1996;1309-1316.
22. Gordon A.S., Yao L., Wu Z.L., Coe I.R., Diamond I. Ethanol alters the subcellular localization of delta- and epsilon-protein kinase C in NG108-15 cells. Mol. Pharmacol. 52:1997;554-559.
23. Harris R.A., Mcquilkin S.J., Paylor R., Abeliovich A., Tonegawa S., Wehner J.M. 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. USA. 92:1995;3658-3662.
24. 2+ channels. Neuroreport. 12:2001;2423-2427.
25. zα-deficient mice. Brain Res. 870:2000;10-19.
26. 2+ channels by G-protein beta gamma subunits. Nature. 380:1996;258-262.
27. A receptor modulators and alcohol in mice lacking PKCε Nat. Neurosci. 2:1999;997-1002.
28. 2 and its stabilization by Gβγ Nature. 391:1998;803-806.
29. + channel. Biochem. Biophys. Res. Commun. 208:1995;302-308.
30. + (GIRK) channels in opioid-induced analgesia. Neurosci. Res. 38:2000;113-116.
31. + (GIRK) channels and functional couplings of the opioid receptors with the GIRK1 channel. Ann. N.Y. Acad. Sci. 801:1996;95-109.
32. Ikeda K., Watanabe M., Ichikawa T., Kobayashi T., Yano R., Kumanishi T. Distribution of prepro-nociceptin/orphanin FQ mRNA and its receptor mRNA in developing and adult mouse central nervous systems. J. Comp. Neurol. 399:1998;139-151.
33. Ikeda K., Ichikawa T., Kobayashi T., Kumanishi T., Oike S., Yano R. Unique behavioural phenotypes of recombinant-inbred CXBK mice: partial deficiency of sensitivity to μ- and κ-agonists. Neurosci. Res. 34:1999;149-155.
34. Ikeda K., Kobayashi T., Ichikawa T., Kumanishi T., Niki H., Yano R. The untranslated region of μ-opioid receptor mRNA contributes to reduced opioid sensitivity in CXBK mice. J. Neurosci. 21:2001;1334-1339.
35. + (GIRK) channel. Brain Res. Mol. Brain Res. 45:1997;117-126.
36. Ikeda S.R. Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature. 380:1996;255-258.
37. Jeong S.W., Ikeda S.R. G protein α subunit Gαz couples neurotransmitter receptors to ion channels in sympathetic neurons. Neuron. 21:1998;1201-1212.
38. Jiang M., Gold M.S., Boulay G., Spicher K., Peyton M., Brabet P., Srinivasan Y., Rudolph U., Ellison G., Birnbaumer L. Multiple neurological abnormalities in mice deficient in the G protein Go. Proc. Natl. Acad. Sci. USA. 95:1998;3269-3274.
39. Jordan B.A., Devi L.A. G-protein-coupled receptor heterodimerization modulates receptor function. Nature. 399:1999;697-700.
40. + channel mRNAs are differentially expressed in the adult rat brain. J. Neurosci. 16:1996;3559-3570.
41. + channel in the rat. FEBS Lett. 348:1994;139-144.
42. Kieffer B.L. Recent advances in molecular recognition and signal transduction of active peptides: receptors for opioid peptides. Cell Mol. Neurobiol. 15:1995;615-635.
43. Kieffer B.L., Befort K., Gaveriaux-Ruff C., Hirth C.G. The delta-opioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization. Proc. Natl. Acad. Sci. USA. 89:1992;12048-12052.
44. 1B subunit of the voltage-dependent calcium channel. Mol. Cell Neurosci. 18:2001;235-245.
45. Kitchen I., Slowe S.J., Matthes H.W., Kieffer B. Quantitative autoradiographic mapping of mu-, delta- and kappa-opioid receptors in knockout mice lacking the mu-opioid receptor gene. Brain Res. 778:1997;73-88.
46. Kobayashi T., Ikeda K., Ichikawa T., Abe S., Togashi S., Kumanishi T. Molecular cloning of a mouse G-protein-activated K+ channel (mGIRK1) and distinct distributions of three GIRK (GIRK1, 2 and 3) mRNAs in mouse brain. Biochem. Biophys. Res. Commun. 208:1995;1166-1173.
47. + channels. Nat. Neurosci. 2:1999;1091-1097.
48. Konig M., Zimmer A.M., Steiner H., Holmes P.V., Crawley J.N., Brownstein M.J., Zimmer A. Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin. Nature. 383:1996;535-538.
49. +-channel proteins. Nature. 374:1995;135-141.
50. Krauss S.W., Ghirnikar R.B., Diamond I., Gordon A.S. Inhibition of adenosine uptake by ethanol is specific for one class of nucleoside transporters. Mol. Pharmacol. 44:1993;1021-1026.
51. Kubo Y., Reuveny E., Slesinger P.A., Jan Y.N., Jan L.Y. Primary structure and functional expression of a rat G-protein-coupled muscarinic potassium channel. Nature. 364:1993;802-806.
52. Law P.Y., Wong Y.H., Loh H.H. Molecular mechanisms and regulation of opioid receptor signaling. Annu. Rev. Pharmacol. Toxicol. 40:2000;389-430.
53. Lee J.W., Joshi S., Chan J.S., Wong Y.H. Differential coupling of mu-, delta-, and kappa-opioid receptors to Gα16-mediated stimulation of phospholipase C. J. Neurochem. 70:1998;2203-2211.
54. Leonoudakis D., Gray A.T., Winegar B.D., Kindler C.H., Harada M., Taylor D.M., Chavez R.A., Forsayeth J.R., Yost C.S. An open rectifier potassium channel with two pore domains in tandem cloned from rat cerebellum. J. Neurosci. 18:1998;868-877.
55. + channels. J. Biol. Chem. 270:1995;28660-28667.
56. Lewohl J.M., Wilson W.R., Mayfield R.D., Brozowski S.J., Morrisett R.A., Harris R.A. G-protein-coupled inwardly rectifying potassium channels are targets of alcohol action. Nat. Neurosci. 2:1999;1084-1090.
57. Li C., Peoples R.W., Weight F.F. Alcohol action on a neuronal membrane receptor: evidence for a direct interaction with the receptor protein. Proc. Natl. Acad. Sci. USA. 91:1994;8200-8204.
58. Li L.Y., Chang K.J. The stimulatory effect of opioids on MAP-kinase in Chinese hamster ovary cells transfected to express mu-opioid receptors. Mol. Pharmacol. 50:1996;599-602.
59. + channel proteins GIRK1 and GIRK2 and their altered expression in weaver brain. J. Neurosci. 16:1996;7137-7150.
60. Linder M.E., Gilman A.G. G proteins. Sci. Am. 267:(56-61):1992;55-64.
61. 3 receptors and the neural actions of alcohols: an increasingly exciting topic. Neurochem. Int. 35:1999;125-130.
62. 3 receptor-mediated ion current in neuroblastoma cells and isolated adult mammalian neurons. Mol. Pharmacol. 40:1991;263-270.
63. Lovinger D.M., White G., Weight F.F. Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science. 243:1989;1721-1724.
64. Lyon R.C., McComb J.A., Schreurs J., Goldstein D.B. A relationship between alcohol intoxication and the disordering of brain membranes by a series of short-chain alcohols. J. Pharmacol. Exp. Ther. 218:1981;669-675.
65. Mansour A., Fox C.A., Akil H., Watson S.J. Opioid receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci. 18:1995;22-29.
66. Matthes H.W., Smadja C., Valverde O., Vonesch J.L., Foutz A.S., Boudinot E., Denavit-Saubie M., Severini C., Negri L., Roques B.P., Maldonado R., Kieffer B.L. Activity of the delta-opioid receptor is partially reduced, whereas activity of the kappa-receptor is maintained in mice lacking the mu-receptor. J. Neurosci. 18:1998;7285-7295.
67. Matthes H.W., Maldonado R., Simonin F., Valverde O., Slowe S., Kitchen I., Befort K., Dierich A., Le Meur M., Dolle P., Tzavara E., Hanoune J., Roques B.P., Kieffer B.L. Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid receptor gene. Nature. 383:1996;819-823.
68. McCreery M.J., Hunt W.A. Physico-chemical correlates of alcohol intoxication. Neuropharmacology. 17:1978;451-461.
69. Meunier J.C., Mollereau C., Toll L., Suaudeau C., Moisand C., Alvinerie P., Butour J.L., Guillemot J.C., Ferrara P., Monsarrat B., Mazarguil H., Vassart G., Parmentier M., Costentin J. Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature. 377:1995;532-535.
70. A and glycine receptor function. Neurochem. Int. 35:1999;115-123.
71. Minami M., Satoh M. Molecular biology of the opioid receptors: structures, functions and distributions. Neurosci. Res. 23:1995;121-145.
72. Mitrovic I., Yi E., Margeta-Mitrovic M., Stoffel M., Basbaum A.I. Contribution of GIRK2 channels to morphine and clonidine antinociception: a possible mediator of sex differences. Soc. Neurosci. Abst. 26:2000;2188.
73. Miyakawa T., Yagi T., Kitazawa H., Yasuda M., Kawai N., Tsuboi K., Niki H. Fyn-kinase as a determinant of ethanol sensitivity: relation to NMDA-receptor function. Science. 278:1997;698-701.
74. Mollereau C., Parmentier M., Mailleux P., Butour J.L., Moisand C., Chalon P., Caput D., Vassart G., Meunier J.C. ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett. 341:1994;33-38.
75. 2+ channels. Trends Pharmacol. Sci. 22:2001;526-532.
76. Nagy L.E., Diamond I., Casso D.J., Franklin C., Gordon A.S. Ethanol increases extracellular adenosine by inhibiting adenosine uptake via the nucleoside transporter. J. Biol. Chem. 265:1990;1946-1951.
77. Narahashi T., Aistrup G.L., Marszalec W., Nagata K. Neuronal nicotinic acetylcholine receptors: a new target site of ethanol. Neurochem. Int. 35:1999;131-141.
78. Narita M., Mizoguchi H., Sora I., Uhl G.R., Tseng L.F. Absence of G-protein activation by mu-opioid receptor agonists in the spinal cord of mu-opioid receptor knockout mice. Br. J. Pharmacol. 126:1999;451-456.
79. + channels. Science. 272:1996;1950-1953.
80. Nestler E.J. Molecular neurobiology of addiction. Am. J. Addict. 10:2001;201-217.
81. Nestler E.J., Duman R.S. G proteins. Siegel G.J., Agranoff B.W., Albers R.W., Fisher S.K., Uhler M.D. Basic Neurochemistry. sixth ed. 1999;401-414 Lippincott-Raven, Philadelphia.
82. North R.A. Drug receptors and the inhibition of nerve cells. Br. J. Pharmacol. 98:1989;13-28.
83. Ozaki M., Hashikawa T., Ikeda K., Miyakawa Y., Ichikawa T., Ishihara Y., Kumanishi T., Yano R. Degeneration of pontine mossy fibers during cerebellar development in weaver mutant mice. Eur. J. Neurosci., in press.
84. Pan Z.Z., Williams J.T., Osborne P.B. Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro. J. Physiol. 427:1990;519-532.
85. + channels. Trends Neurosci. 24:2001;339-346.
86. Patil N., Cox D.R., Bhat D., Faham M., Myers R.M., Peterson A.S. A potassium channel mutation in weaver mice implicates membrane excitability in granule cell differentiation. Nat. Genet. 11:1995;126-129.
87. Peoples R.W., Li C., Weight F.F. Lipid vs protein theories of alcohol action in the nervous system. Annu. Rev. Pharmacol. Toxicol. 36:1996;185-201.
88. Pert C.B., Snyder S.H. Opiate receptor: demonstration in nervous tissue. Science. 179:1973;1011-1014.
89. Reimann F., Ashcroft F.M. Inwardly rectifying potassium channels. Curr. Opin. Cell Biol. 11:1999;503-508.
90. Reinscheid R.K., Nothacker H.P., Bourson A., Ardati A., Henningsen R.A., Bunzow J.R., Grandy D.K., Langen H., Monsma F.J. Jr., Civelli O. Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor. Science. 270:1995;792-794.
91. Reuveny E., Slesinger P.A., Inglese J., Morales J.M., Iniguez-Lluhi J.A., Lefkowitz R.J., Bourne H.R., Jan Y.N., Jan L.Y. Activation of the cloned muscarinic potassium channel by G protein beta gamma subunits. Nature. 370:1994;143-146.
92. Rubinstein M., Mogil J.S., Japon M., Chan E.C., Allen R.G., Low M.J. Absence of opioid stress-induced analgesia in mice lacking β-endorphin by site-directed mutagenesis. Proc. Natl. Acad. Sci. USA. 93:1996;3995-4000.
93. 2+ channel. EMBO J. 20:2001;2349-2356.
94. 2+ channel. Proc. Natl. Acad. Sci. USA. 97:2000;6132-6137.
95. Sharifi N., Diehl N., Yaswen L., Brennan M.B., Hochgeschwender U. Generation of dynorphin knockout mice. Brain Res. Mol. Brain Res. 86:2001;70-75.
96. + channel GIRK2. Proc. Natl. Acad. Sci. USA. 94:1997;923-927.
97. Simon M.I., Strathmann M.P., Gautam N. Diversity of G proteins in signal transduction. Science. 252:1991;802-808.
98. Simonin F., Valverde O., Smadja C., Slowe S., Kitchen I., Dierich A., Le Meur M., Roques B.P., Maldonado R., Kieffer B.L. Disruption of the κ-opioid receptor gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective κ-agonist U-50, 488H and attenuates morphine withdrawal. EMBO J. 17:1998;886-897.
99. Slater S.J., Cox K.J., Lombardi J.V., Ho C., Kelly M.B., Rubin E., Stubbs C.D. Inhibition of protein kinase C by alcohols and anaesthetics. Nature. 364:1993;82-84.
100. + channels. Neuron. 16:1996;321-331.
101. Sora I., Funada M., Uhl G.R. The mu-opioid receptor is necessary for [D-Pen2,D-Pen5]enkephalin-induced analgesia. Eur. J. Pharmacol. 324:1997a;R1-2.
102. Sora I., Li X.F., Funada M., Kinsey S., Uhl G.R. Visceral chemical nociception in mice lacking mu-opioid receptors: effects of morphine, SNC80 and U-50,488. Eur. J. Pharmacol. 366:1999;R3-5.
103. Sora I., Takahashi N., Funada M., Ujike H., Revay R.S., Donovan D.M., Miner L.L., Uhl G.R. Opiate receptor knockout mice define mu receptor roles in endogenous nociceptive responses and morphine-induced analgesia. Proc. Natl. Acad. Sci. USA. 94:1997b;1544-1549.
104. Tanaka C., Nishizuka Y. The protein kinase C family for neuronal signaling. Annu. Rev. Neurosci. 17:1994;551-567.
105. 3 receptor mRNA. Proc. Natl. Acad. Sci. USA. 90:1993;1430-1434.
106. Thiele T.E., Willis B., Stadler J., Reynolds J.G., Bernstein I.L., McKnight G.S. High ethanol consumption and low sensitivity to ethanol-induced sedation in protein kinase A-mutant mice. J. Neurosci. 20:2000;RC75.
107. Ueda H., Miyamae T., Hayashi C., Watanabe S., Fukushima N., Sasaki Y., Iwamura T., Misu Y. Protein kinase C involvement in homologous desensitization of delta-opioid receptor coupled to Gi1-phospholipase C activation in Xenopus oocytes. J. Neurosci. 15:1995;7485-7499.
108. Vaccarino A.L., Kastin A.J. Endogenous opiates. Peptides. 21:1999;1975-2034.
109. Wall P.D., Melzack R. Textbook of Pain. fourth ed. 1999;Churchill Livingstone, Edinburgh.
110. Walter H.J., Messing R.O. Regulation of neuronal voltage-gated calcium channels by ethanol. Neurochem. Int. 35:1999;95-101.
111. Wand G., Levine M., Zweifel L., Schwindinger W., Abel T. The cAMP-protein kinase A signal transduction pathway modulates ethanol consumption and sedative effects of ethanol. J. Neurosci. 21:2001;5297-5303.
112. Weight F.F., Li C., Peoples R.W. Alcohol action on membrane ion channels gated by extracellular ATP (P2X receptors). Neurochem. Int. 35:1999;143-152.
113. A receptors in rat hippocampal CA1 pyramidal neurons. J. Neurochem. 68:1997;1949-1959.
114. Wickman K., Nemec J., Gendler S.J., Clapham D.E. Abnormal heart rate regulation in GIRK4 knockout mice. Neuron. 20:1998;103-114.
115. Woodward J.J. Ionotropic glutamate receptors as sites of action for ethanol in the brain. Neurochem. Int. 35:1999;107-113.
116. Woodward J.J. Ethanol and NMDA receptor signaling. Crit. Rev. Neurobiol. 14:2000;69-89.
117. Xie W., Samoriski G.M., McLaughlin J.P., Romoser V.A., Smrcka A., Hinkle P.M., Bidlack J.M., Gross R.A., Jiang H., Wu D. Genetic alteration of phospholipase Cβ3 expression modulates behavioral and cellular responses to μ opioids. Proc. Natl. Acad. Sci. USA. 96:1999;10385-10390.
118. Xiong K., Li C., Weight F.F. Inhibition by ethanol of rat P2X(4) receptors expressed in Xenopus oocytes. Br. J. Pharmacol. 130:2000;1394-1398.
119. Zadina J.E., Hackler L., Ge L.J., Kastin A.J. A potent and selective endogenous agonist for the mu-opiate receptor. Nature. 386:1997;499-502.
120. + channels by distinct PtdIns(4,5)P2 interactions. Nat. Cell Biol. 1:1999;183-188.
121. + channels. Proc. Natl. Acad. Sci. USA. 98:2001;6482-6487.
122. Zhu Y., King M.A., Schuller A.G., Nitsche J.F., Reidl M., Elde R.P., Unterwald E., Pasternak G.W., Pintar J.E. Retention of supraspinal delta-like analgesia and loss of morphine tolerance in δ opioid receptor knockout mice. Neuron. 24:1999;243-252.
123. Zimmer A., Valjent E., Konig M., Zimmer A.M., Robledo P., Hahn H., Valverde O., Maldonado R. Absence of Δ-9-tetrahydrocannabinol dysphoric effects in dynorphin-deficient mice. J. Neurosci. 21:2001;9499-9505.