Potassium channels as molecular targets of endocannabinoids

References

• De Petrocellis L, Di Marzo V. Non-CB1, non-CB2 receptors for endocannabinoids, plant cannabinoids, and synthetic cannabimimetics: focus on G-protein-coupled receptors and transient receptor potential channels. J Neuroimmune Pharmacol. 2010;5(1):103–121.
   PubMed Web of Science ®Google Scholar
• De Petrocellis L, Nabissi M, Santoni G, et al. Actions and regulation of ionotropic cannabinoid receptors. Adv Pharmacol. 2017;80:249–289.
   PubMedGoogle Scholar
• Ibeas Bih C, Chen T, Nunn AV, et al. Molecular targets of cannabidiol in neurological disorders. Neurotherapeutics. 2015;12(4):699–730.
   PubMed Web of Science ®Google Scholar
• Oz M. Receptor-independent actions of cannabinoids on cell membranes: focus on endocannabinoids. Pharmacol Ther. 2006;111(1):114–144.
   PubMed Web of Science ®Google Scholar
• Burstein SH. The cannabinoid acids, analogs and endogenous counterparts. Bioorg Med Chem. 2014;22(10):2830–2843.
   PubMed Web of Science ®Google Scholar
• Gaoni Y, Mechoulam R. Isolation, structure, and partial synthesis of an active constituent of hashish. J Am Chem Soc. 1964;86(8):1646–1647.
   Web of Science ®Google Scholar
• Lu HC, Mackie K. An introduction to the endogenous cannabinoid system. Biol Psychiatry. 2016;79(7):516–525.
   PubMed Web of Science ®Google Scholar
• Maccarrone M, Bab I, Bíró T, et al. Endocannabinoid signaling at the periphery: 50 years after THC. Trends Pharmacol Sci. 2015;36(5):277–296.
   PubMed Web of Science ®Google Scholar
• Mechoulam R, Parker LA. The endocannabinoid system and the brain. Annu Rev Psychol. 2013;64:21–47.
   PubMed Web of Science ®Google Scholar
• Aizpurua-Olaizola O, Elezgarai I, Rico-Barrio I, et al. Targeting the endocannabinoid system: future therapeutic strategies. Drug Discov Today. 2017;22(1):105–110.
   Google Scholar
• Fraguas-Sánchez AI, Torres-Suárez AI. Medical use of cannabinoids. Drugs. 2018;78(16):1665–1703.
   PubMed Web of Science ®Google Scholar
• Devane WA, Hanus L, Breur A, et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science. 1992;258(5090):1946–1949.
   PubMed Web of Science ®Google Scholar
• Mechoulam R, Ben-Shabat S, Hanus L, et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol. 1995;50(1):83–90.
   PubMed Web of Science ®Google Scholar
• Sugiura T, Kondo S, Sukagawa A, et al. 2-Arachidonoylglycerol: a possible endogenous cannabinoid ligand in brain. Biochem Biophys Res Commun. 1995;215(1):89–97.
   PubMed Web of Science ®Google Scholar
• Howlett AC, Barth F, Bonner TI, et al. International union of pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev. 2002;54(2):161–202.
   PubMed Web of Science ®Google Scholar
• Fride E. Endocannabinoids in the central nervous system--an overview. Prostaglandins Leukot Essent Fatty Acids. 2002;66(2–3):221–233.
   PubMed Web of Science ®Google Scholar
• O’Sullivan SE. An update on PPAR activation by cannabinoids. Br J Pharmacol. 2016;173(12):1899–1910.
   PubMed Web of Science ®Google Scholar
• Pistis M, O’Sullivan SE. The role of nuclear hormone receptors in cannabinoid function. Adv Pharmacol. 2017;80:291–328.
   PubMedGoogle Scholar
• Van Der Stelt M, Di Marzo V. Anandamide as an intracellular messenger regulating ion channel activity. Prostaglandins Other Lipid Mediat. 2005;77(1–4):111–122.
   PubMed Web of Science ®Google Scholar
• Watkins AR. Cannabinoid interactions with ion channels and receptors. Channels (Austin). 2019;13(1):162–167.
   PubMed Web of Science ®Google Scholar
• González C, Baez-Nieto D, Valencia I, et al. K+ channels: function-structural overview. Compr Physiol. 2012;2(3):2087–2149.
   PubMed Web of Science ®Google Scholar
• Hille B. Ion channels of excitable membranes. 3rd ed. Sunderland, MA: Sinauer; 2001.
   Google Scholar
• Huang X, Jan LY. Targeting potassium channels in cancer. J Cell Biol. 2014;206(2):151–162.
   PubMed Web of Science ®Google Scholar
• Maljevic S, Lerche H. Potassium channels: a review of broadening therapeutic possibilities for neurological diseases. J Neurol. 2013;260(9):2201–2211.
   PubMed Web of Science ®Google Scholar
• Rubaiy HN. The therapeutic agents that target ATP-sensitive potassium channels. Acta Pharm. 2016;66(1):23–34.
   PubMed Web of Science ®Google Scholar
• Wickenden A. K+ channels as therapeutic drug targets. Pharmacol Ther. 2002;94(1–2):157–182.
   PubMed Web of Science ®Google Scholar
• Wulff H, Castle NA, Pardo LA. Voltage-gated potassium channels as therapeutic targets. Nat Rev Drug Discov. 2009;8(12):982–1001.
   PubMed Web of Science ®Google Scholar
• Maccarrone M, Bernardi G, Agrò AF, et al. Cannabinoid receptor signalling in neurodegenerative diseases: a potential role for membrane fluidity disturbance. Br J Pharmacol. 2011;163(7):1379–1390.
   PubMed Web of Science ®Google Scholar
• Oz M, Yang KH, Dinc M, et al. The endogenous cannabinoid anandamide inhibits cromakalim-activated K+ currents in follicle-enclosed xenopus oocytes. J Pharmacol Exp Ther. 2007;323(2):547–554.
   PubMed Web of Science ®Google Scholar
• Pertwee RG. Endocannabinoids and their pharmacological actions. Handb Exp Pharmacol. 2015;231:1–37.
   PubMedGoogle Scholar
• Ameri A. The effects of cannabinoids on the brain. Prog Neurobiol. 1999;58(4):315–348.
   PubMed Web of Science ®Google Scholar
• Lovinger DM. Presynaptic modulation by endocannabinoids. Handb Exp Pharmacol. 2008;184:435–477.
   Google Scholar
• Jackson WF. Potassium channels in regulation of vascular smooth muscle contraction and growth. Adv Pharmacol. 2017;78:89–144.
   PubMedGoogle Scholar
• Parmar N, Ho WS. N-arachidonoyl glycine, an endogenous lipid that acts as a vasorelaxant via nitric oxide and large conductance calcium-activated potassium channels. Br J Pharm. 2010;160(3):594–603.
   Web of Science ®Google Scholar
• Li Y, Zhang L, Wu Y, et al. Cannabinoids-induced peripheral analgesia depends on activation of BK channels. Brain Res. 2019;1711:23–28.
   PubMed Web of Science ®Google Scholar
• Sade H, Muraki K, Ohya S, et al. Activation of large-conductance, Ca2+-activated K+ channels by cannabinoids. Am J Physiol Cell Physiol. 2006;290(1):C77–C86.
   Web of Science ®Google Scholar
• Bondarenko AI, Panasiuk O, Okhai I, et al. Direct activation of Ca2+- and voltage-gated potassium channels of large conductance by anandamide in endothelial cells does not support the presence of endothelial atypical cannabinoid receptor. Eur J Pharmacol. 2017;805:14–24.
   PubMed Web of Science ®Google Scholar
• Bondarenko AI, Panasiuk O, Drachuk K, et al. The quest for endothelial atypical cannabinoid receptor: BKCa channels act as cellular sensors for cannabinoids in in vitro and in situ endothelial cells. Vascul Pharmacol. 2018;102:44–55.
   PubMed Web of Science ®Google Scholar
• Jan LY, Jan YN. Voltage-gated potassium channels and the diversity of electrical signalling. J Physiol. 2012;590(11):2591–2599.
   PubMed Web of Science ®Google Scholar
• Tamargo J, Caballero R, Gómez R, et al. Pharmacology of cardiac potassium channels. Cardiovasc Res. 2004;62(1):9–33.
   PubMed Web of Science ®Google Scholar
• Hiley CR. Endocannabinoids and the heart. J Cardiovasc Pharmacol. 2009;53(4):267–276.
   PubMed Web of Science ®Google Scholar
• Amorós I, Barana A, Caballero R, et al. Endocannabinoids and cannabinoid analogues block human cardiac Kv4.3 channels in a receptor-independent manner. J Mol Cell Cardiol. 2010;48(1):201–210.
   Web of Science ®Google Scholar
• Grant AO. Cardiac ion channels. Circ Arrhythm Electrophysiol. 2009;2(2):185–194.
   PubMed Web of Science ®Google Scholar
• Li Q, Ma HJ, Song SL, et al. Effects of anandamide on potassium channels in rat ventricular myocytes: a suppression of Ito and augmentation of KATP channels. Am J Physiol Cell Physiol. 2012;302(6):C924–C930.
   Web of Science ®Google Scholar
• Augustin SM, Lovinger DM. Functional relevance of endocannabinoid-dependent synaptic plasticity in the central nervous system. ACS Chem Neurosci. 2018;9(9):2146–2161.
   PubMed Web of Science ®Google Scholar
• Liss B, Franz O, Sewing S, et al. Tuning pacemaker frequency of individual dopaminergic neurons by Kv4.3L and KChip3.1 transcription. EMBO J. 2001;20(20):5715–5724.
   PubMed Web of Science ®Google Scholar
• Gantz SC, Bean BP. Cell-autonomous excitation of midbrain dopamine neurons by endocannabinoid-dependent lipid signaling. Neuron. 2017;93(6):1375–1387.
   Google Scholar
• Poling JS, Rogawski MA, Salem N Jr, et al. Anandamide, an endogenous cannabinoid, inhibits Shaker-related voltage-gated K+ channels. Neuropharmacology. 1996;35(7):983–991.
   Web of Science ®Google Scholar
• Nelson MT, Quayle JM. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol. 1995;268(4 Pt 1):C799–C822.
   Google Scholar
• Van den Bossche I, Vanheel B. Influence of cannabinoids on the delayed rectifier in freshly dissociated smooth muscle cells of the rat aorta. Br J Pharmacol. 2000;131(1):85–93.
   Web of Science ®Google Scholar
• Vignali M, Benfenati V, Caprini M, et al. The endocannabinoid anandamide inhibits potassium conductance in rat cortical astrocytes. Glia. 2009;57(7):791–806.
   PubMed Web of Science ®Google Scholar
• MacDonald PE, Wheeler MB. Voltage-dependent K+ channels in pancreatic β-cells: role, regulation and potential as therapeutic targets. Diabetologia. 2003;46(8):1046–1062.
   Web of Science ®Google Scholar
• Smith PA, Bokvist K, Arkhammar P, et al. Delayed rectifying and calcium-activated K+ channels and their significance for action potential repolarization in mouse pancreatic β-cells. J Gen Physiol. 1990;95(6):1041–1059.
   PubMed Web of Science ®Google Scholar
• Spivak CE, Kim W, Liu QR, et al. Blockade of β-cell KATP channels by the endocannabinoid, 2-arachidonoylglycerol. Biochem Biophys Res Commun. 2012;423(1):13–18.
   PubMed Web of Science ®Google Scholar
• Philipson LH, Hice RE, Schaefer K, et al. Sequence and functional expression in Xenopus oocytes of a human insulinoma and islet potassium channel. Proc Natl Acad Sci U S A. 1991;88(1):53–57.
   PubMed Web of Science ®Google Scholar
• Hardy AB, Fox JE, Giglou PR, et al. Characterization of Erg K+ channels in alpha- and beta-cells of mouse and human islets. J Biol Chem. 2009;284(44):30441–30452.
   PubMed Web of Science ®Google Scholar
• Herrington J, Sanchez M, Wunderler D, et al. Biophysical and pharmacological properties of the voltage-gated potassium current of human pancreatic β-cells. J Physiol. 2005;567(Pt 1):159–175.
   PubMed Web of Science ®Google Scholar
• Ravens U, Wettwer E. Ultra-rapid delayed rectifier channels: molecular basis and therapeutic implications. Cardiovasc Res. 2011;89(4):776–785.
   PubMed Web of Science ®Google Scholar
• Barana A, Amorós I, Caballero R, et al. Endocannabinoids and cannabinoid analogues block cardiac hKv1.5 channels in a cannabinoid receptor-independent manner. Cardiovasc Res. 2010;85(1):56–67.
   PubMed Web of Science ®Google Scholar
• Moreno-Galindo EG, Barrio-Echavarría GF, Vásquez JC, et al. Molecular basis for a high-potency open-channel block of Kv1.5 channel by the endocannabinoid anandamide. Mol Pharmacol. 2010;77(5):751–758.
   PubMed Web of Science ®Google Scholar
• Oliver D, Lien CC, Soom M, et al. Functional conversion between A-type and delayed rectifier K+ channels by membrane lipids. Science. 2004;304(5668):265–270.
   Web of Science ®Google Scholar
• Shepard PD, Canavier CC, Levitan ES. Ether-a-go-go-related gene potassium channels: what’s all the buzz about? Schizophr Bull. 2007;33(6):1263–1269.
   Google Scholar
• Sanguinetti MC, Tristani-Firouzi M. hERG potassium channels and cardiac arrhythmia. Nature. 2006;440(7083):463–469.
   PubMed Web of Science ®Google Scholar
• Lo YK, Chiang HT, Wu SN. Effect of arvanil (N-arachidonoyl-vanillyl-amine), a nonpungent anandamide-capsaicin hybrid, on ion currents in NG108-15 neuronal cells. Biochem Pharmacol. 2003;65(4):581–591.
   PubMed Web of Science ®Google Scholar
• Sirois JE, Lei Q, Talley EM. Lynch C 3rd, Bayliss DA. The TASK-1 two-pore domain K+ channel is a molecular substrate for neuronal effects of inhalation anesthetics. J Neurosci. 2000;20(17):6347–6354.
   PubMed Web of Science ®Google Scholar
• Maingret F, Patel AJ, Lazdunski M, et al. The endocannabinoid anandamide is a direct and selective blocker of the background K+ channel TASK-1. EMBO J. 2001;20(1–2):47–54.
   PubMed Web of Science ®Google Scholar
• Millar JA, Barratt L, Southan AP, et al. A functional role for the two-pore domain potassium channel TASK-1 in cerebellar granule neurons. Proc Natl Acad Sci U S A. 2000;97(7):3614–3618.
   PubMed Web of Science ®Google Scholar
• Chaperon F, Thiébot MH. Behavioral effects of cannabinoid agents in animals. Crit Rev Neurobiol. 1999;13(3):243–281.
   PubMedGoogle Scholar
• Dietrich A, McDaniel WF. Endocannabinoids and exercise. Br J Sports Med. 2004;38(5):536–541.
   PubMed Web of Science ®Google Scholar
• De Petrocellis L, Di Marzo V. An introduction to the endocannabinoid system: from the early to the latest concepts. Best Pract Res Clin Endocrinol Metab. 2009;23(1):1–15.
   PubMed Web of Science ®Google Scholar
• Li C, Jones PM, Persaud SJ. Cannabinoid receptors are coupled to stimulation of insulin secretion from mouse MIN6 β-cells. Cell Physiol Biochem. 2010;26(2):187–196.
   Google Scholar
• Matias I, Gonthier MP, Orlando P, et al. Regulation, function, and dysregulation of endocannabinoids in models of adipose and β-pancreatic cells and in obesity and hyperglycemia. J Clin Endocrinol Metab. 2006;91(8):3171–3180.
   Web of Science ®Google Scholar
• Hibino H, Inanobe A, Furutani K, et al. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev. 2010;90(1):291–366.
   PubMed Web of Science ®Google Scholar
• Nichols CG. KATP channels as molecular sensors of cellular metabolism. Nature. 2006;440(7083):470–476.
   Web of Science ®Google Scholar
• McTaggart JS, Clark RH, Ashcroft FM. The role of the KATP channel in glucose homeostasis in health and disease: more than meets the islet. J Physiol. 2010;588(Pt 17):3201–3209.
   PubMed Web of Science ®Google Scholar
• Nichols CG. Adenosine triphosphate-sensitive potassium currents in heart disease and cardioprotection. Card Electrophysiol Clin. 2016;8(2):323–335.
   PubMedGoogle Scholar
• Suzuki M, Sasaki N, Miki T, et al. Role of sarcolemmal KATP channels in cardioprotection against ischemia/reperfusion injury in mice. J Clin Invest. 2002;109(4):509–516.
   PubMed Web of Science ®Google Scholar
• Tinker A, Aziz Q, Li Y, et al. ATP-sensitive potassium channels and their physiological and pathophysiological roles. Compr Physiol. 2018;8(4):1463–1511.
   PubMed Web of Science ®Google Scholar
• Ashcroft FM. Adenosine 5’-triphosphate-sensitive potassium channels. Annu Rev Neurosci. 1988;11:97–118.
   PubMed Web of Science ®Google Scholar
• Honoré E, Hormone-regulated LM. K+ channels in follicle-enclosed oocytes are activated by vasorelaxing K+ channel openers and blocked by antidiabetic sulfonylureas. Proc Natl Acad Sci U S A. 1991;88(12):5438–5442.
   PubMed Web of Science ®Google Scholar
• Ho WSV, Kelly MEM. Cannabinoids in the cardiovascular system. Adv Pharmacol. 2017;80:329–366.
   PubMedGoogle Scholar
• Anumonwo JM, Lopatin AN. Cardiac strong inward rectifier potassium channels. J Mol Cell Cardiol. 2010;48(1):45–54.
   PubMed Web of Science ®Google Scholar
• Zygmunt PM, Petersson J, Andersson DA, et al. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature. 1999;400(6743):452–457.
   Web of Science ®Google Scholar
• Fan P. Cannabinoid agonists inhibit the activation of 5-HT3 receptors in rat nodose ganglion neurons. J Neurophysiol. 1995;73(2):907–910.
   Web of Science ®Google Scholar
• Oz M, Ravindran A, Diaz-Ruiz O, et al. The endogenous cannabinoid anandamide inhibits α7 nicotinic acetylcholine receptor-mediated responses in Xenopus oocytes. J Pharmacol Exp Ther. 2003;306(3):1003–1010.
   PubMed Web of Science ®Google Scholar
• Hejazi N, Zhou C, Oz M, et al. Δ9-tetrahydrocannabinol and endogenous cannabinoid anandamide directly potentiate the function of glycine receptors. Mol Pharmacol. 2006;69(3):991–997.
   PubMed Web of Science ®Google Scholar
• Chemin J, Monteil A, Perez-Reyes E, et al. Direct inhibition of T-type calcium channels by the endogenous cannabinoid anandamide. EMBO J. 2001;20(24):7033–7040.
   Web of Science ®Google Scholar
• Shimasue K, Urushidani T, Hagiwara M, et al. Effects of anandamide and arachidonic acid on specific binding of (+)-PN200-110, diltiazem and (-)-desmethoxyverapamil to L-type Ca2+ channel. Eur J Pharmacol. 1996;296(3):347–350.
   Web of Science ®Google Scholar
• Al Kury LT, Voitychuk OI, Yang KH, et al. Effects of the endogenous cannabinoid AEA on voltage-dependent sodium and calcium channels in rat ventricular myocytes. Br J Pharmacol. 2014;171(14):3485–3498.
   PubMed Web of Science ®Google Scholar
• Patel RR, Barbosa C, Brustovetsky T, et al. Aberrant epilepsy-associated mutant Nav1.6 sodium channel activity can be targeted with cannabidiol. Brain. 2016;139(Pt 8):2164–2181.
   PubMedGoogle Scholar
• Muller C, Lynch DL, Hurst DP, et al. A closer look at anandamide interaction with TRPV1. Front Mol Biosci. 2020;7:144.
   PubMed Web of Science ®Google Scholar
• Venkatachalam K, Montell C. TRP channels. Annu Rev Biochem. 2007;76:387–417.
   PubMed Web of Science ®Google Scholar
• Zamponi GW, Striessnig J, Koschak A, et al. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol Rev. 2015;67(4):821–870.
   PubMed Web of Science ®Google Scholar
• Avila G, de la Rosa JA, Monsalvo-Villegas A, et al. Ca2+ channels mediate bidirectional signaling between sarcolemma and sarcoplasmic reticulum in muscle cells. Cells. 2019;9(1):55.
   Web of Science ®Google Scholar
• Thompson AJ, Lester HA, Lummis SC. The structural basis of function in Cys-loop receptors. Q Rev Biophys. 2010;43(4):449–499.
   PubMed Web of Science ®Google Scholar
• Lynch JW. Molecular structure and function of the glycine receptor chloride channel. Physiol Rev. 2004;84(4):1051–1095.
   PubMed Web of Science ®Google Scholar
• Bouzat C, Lasala M, Nielsen BE, et al. Molecular function of α7 nicotinic receptors as drug targets. J Physiol. 2018;596(10):1847–1861.
   PubMed Web of Science ®Google Scholar
• Du C, Role LW. Differential modulation of nicotinic acetylcholine receptor subtypes and synaptic transmission in chick sympathetic ganglia by PGE2. J Neurophysiol. 2001;85(6):2498–2508.
   Web of Science ®Google Scholar
• Bruno MJ, Koeppe RE 2nd, Andersen OS. Docosahexaenoic acid alters bilayer elastic properties. Proc Natl Acad Sci USA. 2007;104(23):9638–9643.
   Web of Science ®Google Scholar
• Rimmerman N, Hughes HV, Bradshaw HB, et al. Compartmentalization of endocannabinoids into lipid rafts in a dorsal root ganglion cell line. Br J Pharmacol. 2008;153(2):380–389.
   PubMed Web of Science ®Google Scholar
• Carta M, Lanore F, Rebola N, et al. Membrane lipids tune synaptic transmission by direct modulation of presynaptic potassium channels. Neuron. 2014;81(4):787–799.
   Web of Science ®Google Scholar
• Lishko PV, Botchkina IL, Fedorenko A, et al. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell. 2010;140(3):327–337.
   Web of Science ®Google Scholar
• Sigel E, Baur R, Rácz I, et al. The major central endocannabinoid directly acts at GABAA receptors. Proc Natl Acad Sci U S A. 2011;108(44):18150–18155.
   PubMed Web of Science ®Google Scholar
• Bakas T, van Nieuwenhuijzen PS, Devenish SO, et al. The direct actions of cannabidiol and 2-arachidonoyl glycerol at GABAA receptors. Pharmacol Res. 2017;119:358–370.
   PubMed Web of Science ®Google Scholar