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Brain Structure and Function
Published in: Brain Structure and Function 1/2020

01-01-2020 | Cannabinoid | Review

Cannabinoids, TRPV and nitric oxide: the three ring circus of neuronal excitability

Authors: Giuditta Gambino, Valerio Rizzo, Giuseppe Giglia, Giuseppe Ferraro, Pierangelo Sardo

Published in: Brain Structure and Function | Issue 1/2020

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Abstract

Endocannabinoid system is considered a relevant player in the regulation of neuronal excitability, since it contributes to maintaining the balance of the synaptic ionic milieu. Perturbations to bioelectric conductances have been implicated in the pathophysiological processes leading to hyperexcitability and epileptic seizures. Cannabinoid influence on neurosignalling is exerted on classic receptor-mediated mechanisms or on further molecular targets. Among these, transient receptor potential vanilloid (TRPV) are ionic channels modulated by cannabinoids that are involved in the transduction of a plethora of stimuli and trigger fundamental downstream pathways in the post-synaptic site. In this review, we aim at providing a brief summary of the most recent data about the cross-talk between cannabinoid system and TRPV channels, drawing attention on their role on neuronal hyperexcitability. Then, we aim to unveil a plausible point of interaction between these neural signalling systems taking into consideration nitric oxide, a gaseous molecule inducing profound modifications to neural performances. From this novel perspective, we struggle to propose innovative cellular mechanisms in the regulation of hyperexcitability phenomena, with the goal of exploring plausible CB-related mechanisms underpinning epileptic seizures.
Literature
Adermark L, Lovinger DM (2007) Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step. Proc Natl Acad Sci USA 104:20564–20569PubMedCrossRefPubMedCentral
Aguiar DC, Moreira FA, Terzian AL, Fogac MV, Lisboa SF, Wotjakc CT et al (2014) Modulation of defensive behavior by transient receptor potential vanilloid type-1 (TRPV1) channels. Neurosci Biobehav Rev 46:418–428PubMedCrossRef
Ahern GP, Klyachko VA, Jackson MB (2002) CGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25(10):510–517PubMedCrossRef
Anwyl R (2009) Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharm 56(4):735–740CrossRef
Arancio O, Kandel ER, Hawkins RD (1995) Activity-dependent long-term enhancement of transmitter release by presynaptic 30, 50-cyclic GMP in cultured hippocampal neurons. Nature 376:74–80PubMedCrossRef
Ayala GF, Dichter M, Gumnit RJ, Matsumoto G, Spencer WA (1973) Genesis of epileptic interictal spikes: new knowledge of cortical feedback systems suggests a neurophysiological explanation of brief paroxysms. Brain Res 52:1–17PubMedCrossRef
Azad SC, Marsicano G, Eberlein I, Putzke J, Zieglgänsberger W, Spanagel R et al (2001) Differential role of the nitric oxide pathway on delta(9)-THC-induced central nervous system effects in the mouse. Eur J Neurosci 13(3):561–568PubMedCrossRef
Bacci A, Huguenard JR, Prince DA (2004) Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431:312–316PubMedCrossRef
Bahremand A, Nasrabady SE, Shafaroodi H, Ghasemi M, Dehpour AR (2009) Involvement of nitrergic system in the anticonvulsant effect of the cannabinoid CB(1) agonist ACEA in the pentylenetetrazole-induced seizure in mice. Epilepsy Res 84(2–3):110–119PubMedCrossRef
Banach M, Piskorska B, Czuczwar SJ, Borowicz KK (2011) Nitric oxide, epileptic seizures, and action of antiepileptic drugs. CNS Neurol Disord Drug Targets 10(7):808–819PubMedCrossRef
Batista P, Fogaça MV, Guimarães FS (2015) The endocannabinoid, endovanilloid and nitrergic systems could interact in the rat dorsolateral periaqueductal gray matter to control anxiety-like behaviors. Behav Brain Res 293:182–188PubMedCrossRef
Benko R, Lazar Z, Undi S, Illenyi L, Antal A, Horvath ÖP et al (2005) Inhibition of nitric oxide synthesis blocks the inhibitory response to capsaicin in intestinal circular muscle preparations from different species. Life Sci 76:2773–2782PubMedCrossRef
Bhaskaran MD, Smith BN (2010) Effects of TRPV1 activation on synaptic excitation in the dentate gyrus of a mouse model of temporal lobe epilepsy. Exp Neurol 223(2):529–536PubMedPubMedCentralCrossRef
Blair RE, Deshpande LS, Sombati S, Falenski KW, Martin BR, DeLorenzo RJ (2006) Activation of the cannabinoid type-1 receptor mediates the anticonvulsant properties of cannabinoids in the hippocampal neuronal culture models of acquired epilepsy and status epilepticus. J Pharmacol Exp Ther 317:1072–1078PubMedCrossRef
Borowicz KK, Luszczki J, Kleinrok Z, Czuczwar SJ (2000) 7-Nitroindazole, a nitric oxide synthase inhibitor, enhances the anticonvulsive action of ethosuximide and clonazepam against penthylenetetrazol-induced convulsions. J Neural Transm 107:1117–1126PubMedCrossRef
Braakman HM, van Oostenbrugge RJ, van Kranen-Mastenbroek VH, de Krom MC (2009) Rimonabant induces partial seizures in a patient with a history of generalized epilepsy. Epilepsia 50(9):2171–2172PubMedCrossRef
Bromfield EB, Cavazos JE, Sirven JI, editors (2006) An introduction to epilepsy. West Hartford (CT): American Epilepsy Society, chapter 2, clinical epilepsy
Brown SP, Brenowitz SD, Regehr WG (2003) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048–1057PubMedCrossRef
Burette A, Zabel U, Weinberg RJ, Schmidt HH, Valtschanoff JG (2002) Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J Neurosci 22(20):8961–8970PubMedPubMedCentralCrossRef
Cabral GA, Raborn ES, Griffin L, Dennis J, Marciano-Cabral F (2008) CB2 receptors in the brain: role in central immune function. Br J Pharmacol 153(2):240–251PubMedCrossRef
Carletti F, Ferraro G, Rizzo V, Cannizzaro C, Sardo P (2013) Antiepileptic effect of dimethyl sulfoxide in a rat model of temporal lobe epilepsy. Neurosci Lett 546:31–35PubMedCrossRef
Carletti F, Gambino G, Rizzo V, Ferraro G, Sardo P (2016b) Involvement of TRPV1 channels in the activity of the cannabinoid WIN 55,212-2 in an acute rat model of temporal lobe epilepsy. Epilepsy Res 122:56–65PubMedCrossRef
Carletti F, Gambino G, Rizzo V, Ferraro G, Sardo P (2017) Neuronal nitric oxide synthase is involved in CB/TRPV1 signalling: focus on control of hippocampal hyperexcitability. Epilepsy Res 138:18–25PubMedCrossRef
Carletti F, Rizzo V, Gambino G, De Caro V, Sutera FM, Li Giannola et al (2018) Comparative study of the effects exerted by N-valproyl-l-phenylalanine and N-valproyl-l-tryptophan on CA1 hippocampal epileptiform activity in rat. Curr Pharm Des 24:1849–1858PubMedCrossRef
Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824PubMedCrossRef
Cavanaugh DJ, Chesler AT, Jackson AC, Sigal YM, Yamanaka H, Grant R et al (2011) Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J Neurosci 31:5067–5077PubMedPubMedCentralCrossRef
Chamberlain SE, Jane DE, Jones RS (2012) Pre- and post-synaptic functions of kainate receptors at glutamate and GABA synapses in the rat entorhinal cortex. Hippocampus 22(3):555–576PubMedCrossRef
Chavez AE, Chiu CQ, Castillo PE (2010) TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Nat Neurosci 13:1511–1518PubMedPubMedCentralCrossRef
Chevaleyre V, Takahashi KA, Castillo PE (2006) Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 29:37–76PubMedCrossRef
Chiarlone A, Bellocchio L, Blazquez C, Resel E, Soria-Gomez E, Cannich A et al (2014) A restricted population of CB1 cannabinoid receptors with neuroprotective activity. Proc Natl Acad Sci 111:8257–8262PubMedCrossRefPubMedCentral
Cilio MR, Thiele E, Devinsky O (2014) The case for assessing cannabidiol in epilepsy. Epilepsia 55:787–790PubMedCrossRef
de Vasconcelos AP, Gizard F, Marescaux C, Nehlig A (2000) Role of nitric oxide in pentylenetetrazol-induced seizures: age-dependent effects in the immature rat. Epilepsia 41(4):363–371PubMedCrossRef
Del-Bel EA, Oliveira PR, Oliveira JA, Mishra PK, Jobe PC, Garcia-Cairasco N (1997) Anticonvulsant and proconvulsant roles of nitric oxide in experimental epilepsy models. Braz J Med Biol Res 30:971–979PubMedCrossRef
den Boon FS, Chameau P, Schaafsma-Zhao Q, van Aken W, Bari M, Oddi S et al (2012) Excitability of prefrontal cortical pyramidal neurons is modulated by activation of intracellular type-2 cannabinoid receptors. Proc Natl Acad Sci USA 109(9):3534–3539CrossRef
Derbenev AV, Monroe MJ, Glatzer NR, Smith BN (2006) Vanilloid-mediated heterosynaptic facilitation of inhibitory synaptic input to neurons of the rat dorsal motor nucleus of the vagus. J Neurosci 26:9666–9672PubMedPubMedCentralCrossRef
Deshpande LS, Sombati S, Blair RE, Carter DS, Martin BR, DeLorenzo RJ (2007) Cannabinoid CB1 receptor antagonists cause status epilepticus-like activity in the hippocampal neuronal culture model of acquired epilepsy. Neurosci Lett 411(1):11–16PubMedCrossRef
Doyle MW, Bailey TW, Jin Y-H, Andresen MC (2002) Vanilloid receptors presynaptically modulate visceral afferent synaptic transmission in nucleus tractus solitarius. J Neurosci 22:8222–8229PubMedPubMedCentralCrossRef
Feil R, Kleppisch T (2008) NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol 184:529–560CrossRef
Fernández-Ruiz J, Romero J, Velasco G, Tolón RM, Ramos JA, Guzmán M (2007) Cannabinoid CB2 receptor: a new target for controlling neural cell survival? Trends Pharmacol Sci 28(1):39–45PubMedCrossRef
Ferraro G, Sardo P (2004) Nitric oxide and brain hyperexcitability. Vivo 18:357–366
Ferraro G, Sardo P (2009) Cholecystokinin-8 sulfate modulates the anticonvulsant efficacy of vigabatrin in an experimental model of partial complex epilepsy in the rat. Epilepsia 50:721–730PubMedCrossRef
Fioravanti B, De Felice M, Stucky CL, Medler KA, Luo MC, Gardell LR et al (2008) Constitutive activity at the cannabinoid CB1 receptor is required for behavioral response to noxious chemical stimulation of TRPV1: antinociceptive actions of CB1 inverse agonists. J Neurosci 28:11593–11602PubMedPubMedCentralCrossRef
Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017–1066PubMedCrossRef
Fritschy JM, Kiener T, Bouilleret V, Loup F (1999) GABAergic neurons and GABAA-receptors in temporal lobe epilepsy. Neurochem Int 34:435–445PubMedCrossRef
Fu M, Xie Z, Zuo H (2009) TRPV1: a potential target for antiepileptogenesis. Med Hypotheses 73(1):100–102PubMedCrossRef
Galanopoulou AS (2007) Developmental patterns in the regulation of chloride homeostasis and GABAA receptor signaling by seizures. Epilepsia 48(Suppl 5):14–18PubMedCrossRef
Gambino G, Allegra M, Sardo P, Attanzio A, Tesoriere L, Livrea MA et al (2018) Brain distribution and modulation of neuronal excitability by indicaxanthin from Opuntia ficus indica administered at nutritionally-relevant amounts. Front Aging Neurosci 10:1–11CrossRef
Garzòn J, de la Torre-Madrid E, Rodrı´guez-Munoz M, Vicente-Sa´nchez A, Sa´nchez-Bla´zquez P (2009) Gz mediates the long-lasting desensitization of brain CB1 receptors and is essential for cross-tolerance with morphine. Mol Pain 5:11PubMedPubMedCentralCrossRef
Gerra G, Zaimovic A, Gerra ML, Ciccocioppo R, Cippitelli A, Serpelloni G et al (2010) Pharmacology and toxicology of Cannabis derivatives and endocannabinoid agonists. Recent Pat CNS Drug Discov 5(1):46–52PubMedCrossRef
Gibson HE, Page RS, Van Hook MJ, Kauer JA (2008) TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 57:746–759PubMedPubMedCentralCrossRef
Gonzalez-Reyes LE, Ladas TP, Chiang C, Durand DM (2013) TRPV1 antagonist capsazepine suppresses 4-AP-induced epileptiform activity in vitro and electrographic seizures in vivo. Exp Neurol 250:321–332PubMedPubMedCentralCrossRef
Grima G, Benz B, Do KB (2001) Glial-derived arginine, the nitric oxide precursor, protects neurons from NMDA-induced excitotoxicity. Eur J Neurosci 14:1762–1770PubMedCrossRef
Grueter BA, Brasnjo G, Malenka RC (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat Neurosci 13:1519–1525PubMedPubMedCentralCrossRef
Hara H, Ayata C, Huang PL, Waeber C, Ayata G, Fujii M et al (1997) [3H]L-NG-nitrine binding after transient focal ischemia and NMDA-induced excitotoxicity in type I and type III nitric oxide synthase null mice. J Cereb Blood Flow Metab 17:515–526PubMedCrossRef
Hillard CJ, Muthian S, Kearn CS (1999) Effects of CB(1) cannabinoid receptor activation on cerebellar granule cell nitric oxide synthase activity. FEBS Lett 459:277–281PubMedCrossRef
Hillard CJ, Jarrahian A (2005) Accumulation of anandamide: evidence for cellular diversity. Neuropharmacology 48:1072–1078PubMedCrossRef
Ho KW, Ward NJ, Calkins DJ (2012) TRPV1: A stress response protein in the central nervous system. Am J Neurodegener Dis 1:1–14PubMedPubMedCentral
Hofmann ME, Frazier CJ (2013) Marijuana, endocannabinoids, and epilepsy: potential and challenges for improved therapeutic intervention. Exp Neurol 244:43–50PubMedCrossRef
Hong S, Fan J, Kemmerer ES, Evans S, Li Y, Wiley JW (2009) Reciprocal changes in vanilloid (TRPV1) and endocannabinoid (CB1) receptors contribute to visceral hyperalgesia in the water avoidance stressed rat. Gut 58:202–210PubMedCrossRef
Hong Z, Tian Y, Yuan Y, Qi M, Li Y, Du Y et al (2016) Enhanced oxidative stress is responsible for TRPV4-induced neurotoxicity. Front Cell Neurosci 10:232PubMedPubMedCentral
Howlett AC (2005) Cannabinoid receptor signaling. Handb Exp Pharmacol 168:53–79CrossRef
Iannotti FA, Hill CL, Leo A, Alhusaini A, Soubrane C, Mazzarella E et al (2014) Nonpsychotropic plant cannabinoids, cannabidivarin (CBDV) and cannabidiol (CBD), activate and desensitize transient receptor potential vanilloid 1 (TRPV1) channels in vitro: potential for the treatment of neuronal hyperexcitability. ACS Chem Neurosci 5(11):1131–1141PubMedCrossRef
Jeske NA, Patwardhan AM, Gamper N, Price TJ, Akopian AN, Hargreaves KM (2006) Cannabinoid WIN 55,212-2 regulates TRPV1 phosphorylation in sensory neurons. J Biol Chem 281(43):32879–32890PubMedCrossRef
Jia YF, Li YC, Tang YP, Cao J, Wang L, Yang Y et al (2015) Interference of TRPV1 function altered the susceptibility of PTZ-induced seizures. Front Cell Neurosci 9:20PubMedPubMedCentralCrossRef
Jin Y-H, Bailey TW, Li BY, Schild JH, Andresen MC (2004) Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals. J Neurosci 24:4709–4717PubMedPubMedCentralCrossRef
Jones JD, Carney ST, Vrana KE, Norford DC, Howlett AC (2008) Cannabinoid receptor-mediated translocation of NO-sensitive guanylyl cyclase and production of cyclic GMP in neuronal cells. Neuropharmacology 54(1):23–30PubMedCrossRef
Katona I, Urbán GM, Wallace M, Ledent C, Jung KM, Piomelli D et al (2006) Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26:5628–5637PubMedPubMedCentralCrossRef
Kim SH, Won SJ, Mao XO, Ledent C, Jin K, Greenberg DA (2006a) Role for neuronal nitric-oxide synthase in cannabinoid-induced neurogenesis. J Pharmacol Exp Ther 319(1):150–154PubMedCrossRef
Kim SH, Won SJ, Mao XO, Jin K, Greenberg DA (2006b) Molecular mechanisms of cannabinoid protection from neuronal excitotoxicity. Mol Pharmacol 69(3):691–696PubMedCrossRef
Kiss JP (2000) Role of nitric oxide in the regulation of monoaminergic neurotransmission. Brain Res Bull 52:459–466PubMedCrossRef
Kiss JP, Vizi ES (2001) Nitric oxide: a novel link between synaptic and non synaptic transmission. Trends Neurosci 24:211–215PubMedCrossRef
Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717–727PubMedCrossRef
Leite JP, Neder L, Arisi GM, Carlotti CG, Assirati JA, Moreira JE (2005) Plasticity, synaptic strength, and epilepsy: what can we learn from ultrastructural data? Epilepsia 46(5):S134–S141CrossRef
Ligresti A, De Petrocellis L, Di Marzo V (2016) From phytocannabinoids to cannabinoid receptors and endocannabinoids: pleiotropic physiological and pathological roles through complex pharmacology. Physiol Rev 96(4):1593–1659PubMedCrossRef
Lisboa SF, Magesto AC, Aguiar JC, Resstel LB, Guimaraes FS (2013) Complex interaction between anandamide and the nitrergic system in the dorsolateral periaqueductal gray to modulate anxiety-like behavior in rats. Neuropharmacology 75:86–89PubMedCrossRef
Liu X, Miller MJ, Joshi MS, Sadowska-Krowicka H, Clark DA, Lancaster JR (1998) Diffusion-limited reaction of free nitric oxide with erythrocytes. J Biol Chem 273:18709–18713PubMedCrossRef
Ludányi A, Eross L, Czirják S, Vajda J, Halász P, Watanabe M et al (2008) Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J Neurosci 28:2976–2990PubMedPubMedCentralCrossRef
Lumme A, Soinila S, Sadienemi M, Halonen T, Vanhatalo S (2000) Nitric oxide synthase immunoreactivity in the rat hippocampus after status epilepticus induced by perforant pathway stimulation. Brain Res 871:303–310PubMedCrossRef
Makara JK, Katona I, Nyíri G, Németh B, Ledent C, Watanabe M et al (2007) Involvement of nitric oxide in depolarization-induced suppression of inhibition in hippocampal pyramidal cells during activation of cholinergic receptors. J Neurosci 27(38):10211–10222PubMedPubMedCentralCrossRef
Manna SS, Umathe SN (2012) Involvement of transient receptor potential vanilloid type 1 channels in the pro-convulsant effect of anandamide in pentylenetetrazole-induced seizures. Epilepsy Res 100(1–2):113–124PubMedCrossRef
Marinelli S, Vaughan CW, Christie MJ, Connor M (2002) Capsaicin activation of glutamatergic synaptic transmission in the rat locus coeruleus in vitro. J Physiol 543:531–540PubMedPubMedCentralCrossRef
Marinelli S, Di Marzo V, Berretta N, Matias I, Maccarrone M, Bernardi G et al (2003) Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J Neurosci 23:3136–3144PubMedPubMedCentralCrossRef
Marinelli S, Pacioni S, Bisogno T, Di Marzo V, Prince DA, Huguenard JR et al (2008) The endocannabinoid 2-arachidonoylglycerol is responsible for the slow self-inhibition in neocortical interneurons. J Neurosci 28:13532–13541PubMedPubMedCentralCrossRef
Marinelli S, Pacioni S, Cannich A, Marsicano G, Bacci A (2009) Self-modulation of neocortical pyramidal neurons by endocannabinoids. Nat Neurosci 12:1488–1490PubMedCrossRef
Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A et al (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302(5642):84–88PubMedCrossRef
Messeguer A, Planells-Cases R, Ferrer-Montiel A (2006) Physiology and pharmacology of the vanilloid receptor. Curr Neuropharm 4(1):1–15CrossRef
Mezey E, Toth ZE, Cortright DN, Arzubi MK, Krause JE, Elde R et al (2000) Distribution ofmRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc Natl Acad Sci USA 97:3655–3660PubMedCrossRefPubMedCentral
Micale V, Cristino L, Tamburella A, Petrosino S, Leggio GM, Drago F, Di Marzo V (2009) Anxiolytic effects in mice of a dual blocker of fatty acid amide hydrolase and transient receptor potential vanilloid type-1 channels. Neuropsychopharmacology 34(3):593–606PubMedCrossRef
Min R, Testa-Silva G, Heistek TS, Canto CB, Lodder JC, Bisogno T et al (2010) Diacylglycerol lipase is not involved in depolarization-induced suppression of inhibition at unitary inhibitory connections in mouse hippocampus. J Neurosci 30:2710–2715PubMedPubMedCentralCrossRef
Mohapatra DP, Nau C (2005) Regulation of Ca2+ -dependent desensitization in the vanilloid receptor TRPV1 by calcineurin and cAMP-dependent protein kinase. J Biol Chem 280:13424–13432PubMedCrossRef
Monory K, Massa F, Egertová M, Eder M, Blaudzun H, Westenbroek R et al (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51(4):455–466PubMedPubMedCentralCrossRef
Morgan NH, Stanford IM, Woodhall GL (2009) Functional CB2 type cannabinoid receptors at CNS synapses. Neuropharmacology 57(4):356–368PubMedCrossRef
Nazıroğlu M (2015) TRPV1 channel: a potential drug target for treating epilepsy. Curr Neuropharm 13(2):239–247CrossRef
Németh B, Ledent C, Freund TF, Hájos N (2008) CB1 receptor-dependent and -independent inhibition of excitatory postsynaptic currents in the hippocampus by WIN55,212-2. Neuropharmacology 54:51–57PubMedPubMedCentralCrossRef
Ohkuma S, Katsura M (2001) Nitric oxide and peroxynitrite as factors to stimulate neurotransmitter release in the CNS. Prog Neurobiol 64:97–108PubMedCrossRef
Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29(3):729–738PubMedCrossRef
Okere CO, Kaba H, Higuchi T (2000) Importance of endogenous nitric oxide synthase in the rat hypothalamus and amygdala in mediating the response to capsaicin. J Comp Neurol 423:670–686PubMedCrossRef
Oliveira MS, Skinner F, Arshadmansab MF, Garcia I, Mello CF, Knaus HG et al (2010) Altered expression and function of small-conductance (SK) Ca21-activated K1 channels in pilocarpine-treated epileptic rats. Brain Res 1348:187–199PubMedPubMedCentralCrossRef
Peters JH, McDougall SJ, Fawley JA, Smith SM, Andresen MC (2010) Primary afferent activation of thermosensitive TRPV1 triggers asynchronous glutamate release at central neurons. Neuron 65:657–669PubMedPubMedCentralCrossRef
Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64(1):51–68PubMedCrossRef
Przegalinski E, Baran L, Siwanowicz J (1996) The role of nitric oxide in chemically- and electrically-induced seizures in mice. Neurosci Lett 217:145–148PubMedCrossRef
Puente N, Cui Y, Lassalle O, Lafourcade M, Georges F, Venance L et al (2011) Polymodal activation of the endocannabinoid system in the extended amygdala. Nat Neurosci 14:1542–1547PubMedCrossRef
Quesada O, Hirsch J, Ben-Ari Y, Bernard C (1996) Redox sites of NMDA receptors can modulate epileptiform activity in hippocampal slices from kainic acid-treated rats. Neurosci Lett 212:171–174PubMedCrossRef
Rizzo V, Ferraro G, Carletti F, Lonobile G, Cannizzaro C, Sardo P (2009) Evidences of cannabinoids-induced modulation of paroxysmal events in an experimental model of partial epilepsy in the rat. Neurosci Lett 462(2):135–139PubMedCrossRef
Roberts JC, Davis JB, Benham CD (2004) [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res 995:176–183PubMedCrossRef
Rubino T, Realini N, Castiglioni C, Guidali C, Viganó D, Marras E et al (2008) Role in anxiety behavior of the endocannabinoid system in the prefrontal cortex. Cereb Cortex 18(6):1292–1301PubMedCrossRef
Saffarzadeh F, Eslamizade MJ, Ghadiri T, Modarres Mousavi SM, Hadjighassem M et al (2015) Effects of TRPV1 on the hippocampal synaptic plasticity in the epileptic rat brain. Synapse 69(7):375–383PubMedCrossRef
Sánchez-Blázquez P, Rodríguez-Muñoz M, Vicente-Sánchez A, Garzón J (2013) Cannabinoid receptors couple to NMDA receptors to reduce the production of NO and the mobilization of zinc induced by glutamate. Antioxid Redox Signal 19(15):1766–1782PubMedPubMedCentralCrossRef
Sardo P, Carletti F, D’Agostino S, Rizzo V, Ferraro G (2006) Involvement of nitric oxide-soluble guanylyl cyclase pathway in the control of maximal dentate gyrus activation in the rat. J Neural Transm 113(12):1855–1861PubMedCrossRef
Sardo P, Ferraro G (2007) Modulatory effects of nitric oxide-active drugs on the anticonvulsant activity of lamotrigine in an experimental model of partial complex epilepsy in the rat. BMC Neurosci 8:47PubMedPubMedCentralCrossRef
Sardo P, D’Agostino S, Rizzo V, Carletti F, Lonobile G, Ferraro G (2009) In the rat maximal dentate activation model of partial complex epilepsy, the anticonvulsant activity of levetiracetam is modulated by nitric oxide-active drugs. J Neural Transm 116(7):831–839PubMedCrossRef
Sardo P, Carletti F, D’Agostino S, Rizzo V, Lo Nobile G, Friscia S et al (2011) Nitric oxide-active compounds modulate the intensity of glutamate-evoked responses in the globus pallidus of the rat. Life Sci 88:1113–1120PubMedCrossRef
Sensi SL, Jeng JM (2004) Rethinking the excitotoxic ionic milieu: the emerging role of Zn (2+) in ischemic neuronal injury. Curr Mol Med 4:87–111PubMedCrossRef
Shen M, Thayer S (1999) Delta9-tetrahydrocannabinol acts as a partial agonist to modulate glutamatergic synaptic transmission between rat hippocampal neurons in culture. Mol Pharmacol 55:8–13PubMedCrossRef
Shoudai K, Peters JH, McDougall SJ, Fawley JA, Andresen MC (2010) Thermally active TRPV1 tonically drives central spontaneous glutamate release. J Neurosci 30:14470–14475PubMedPubMedCentralCrossRef
Soltesz I, Alger BE, Kzno M, Lee S-H, Lovinger DM, Ohno-Shosaku T et al (2015) Weeding out bad waves: towards selective cannabinoid circuit control in epilepsy. Nature Rev Neurosci 16:264–277CrossRef
Starowicz K, Maione S, Cristino L, Palazzo E, Marabese I, Rossi F et al (2007) Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathways. J Neurosci 27:13739–13749PubMedPubMedCentralCrossRef
Starowicz K, Cristino L, Di Marzo V (2008) TRPV1 receptors in the central nervous system: potential for previously unforeseen therapeutic applications. Curr Pharm Des 14:42–54PubMedCrossRef
Szallasi A, Blumberg PM (2007) Complex regulation of TRPV1 by vanilloids. In: Liedtke WB, Heller S (eds) TRP ion channel function in sensory transduction and cellular signaling cascades, 6th edn. CRC Press, Boca Raton
Tahmasebi L, Komaki A, Karamian R, Shahidi S, Sarihi A, Salehi I et al (2015) The interactive role of cannabinoid and vanilloid systems in hippocampal synaptic plasticity in rats. Eur J Pharmacol 757:68–73PubMedCrossRef
Toda N, Herman AG (2005) Gastrointestinal function regulation by nitrergic efferent nerves. Pharmacol Rev 57:315–338PubMedCrossRef
Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, Papp Z et al (2005) Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135:162–168PubMedCrossRef
Twitchell W, Brown S, Mackie K (1997) Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 78:43–501PubMedCrossRef
Uliana DL, Hott SC, Lisboa SF, Resstel LB (2016) Dorsolateral periaqueductal gray matter CB1 and TRPV1 receptors exert opposite modulation on expression of contextual fear conditioning. Neuropharmacology 103:257–269PubMedCrossRef
van der Stelt M, Di Marzo V (2005) Anandamide as an intracellular messenger regulating ion channel activity. Prostaglandins Other Lipid Mediat 77:111–122PubMedCrossRef
Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K et al (2005) Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310(5746):329–332PubMedCrossRef
Vicente-Sanchez A, Sanchez-Blazquez P, Rodriguez-Munoz M, Garzon J (2013) Hint1 protein cooperates with cannabinoid 1 receptor to negatively regulate glutamate nmda receptor activity. Mol Brain 6:42PubMedPubMedCentralCrossRef
Wallace MJ, Wiley JL, Martin BR, DeLorenzo RJ (2001) Assessment of the role of CB1 receptors in cannabinoid anticonvulsant effects. Eur J Pharmacol 428:51–57PubMedCrossRef
Wallace MJ, Martin BR, DeLorenzo RJ (2002) Evidence for a physiological role of endocannabinoids in the modulation of seizure threshold and severity. Eur J Pharmacol 452:295–301PubMedCrossRef
Wallace MJ, Blair RE, Falenski KW, Martin BR, DeLorenzo RJ (2003) The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J Pharm Exp Ther 307(1):129–137CrossRef
Wang W, Cao X, Liu C, Liu L (2012) Cannabinoid WIN 55,212-2 inhibits TRPV1 in trigeminal ganglion neurons via PKA and PKC pathways. Neurol Sci 33(1):79–85PubMedCrossRef
Wilson RI, Kunos G, Nicoll RA (2001) Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31:453–462PubMedCrossRef
Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588–659PubMedCrossRef
Wu Z, Chen SR, Pan HL (2005) Transient receptor potential vanilloid type 1 activation down-regulates voltage-gated calcium channels through calciumdependent calcineurin in sensory neurons. J Biol Chem 280:18142–18151PubMedCrossRef
Xing J, Li J (2007) TRPV1 receptor mediates glutamatergic synaptic input to dorsolateral periaqueductal gray (dl-PAG) neurons. J Neurophysiol 97(1):503–511PubMedCrossRef
Yang K, Kumamoto E, Furue H, Yoshimura M (1998) Capsaicin facilitates excitatory but not inhibitory synaptic transmission in substantia gelatinosa of the rat spinal cord. Neurosci Lett 255:135–138PubMedCrossRef
Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y et al (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2(11):596–607PubMedCrossRef
Zhuang SY, Bridges D, Grigorenko E, McCloud S, Boon A, Hampson RE et al (2005) Cannabinoids produce neuroprotection by reducing intracellular calcium release from ryanodine-sensitive stores. Neuropharmacology 48:1086–1096PubMedCrossRef
Zschenderlein C, Gebhardt C, von Bohlen Und Halbach O, Kulisch C, Albrecht D (2011) Capsaicin-induced changes in LTP in the lateral amygdala are mediated by TRPV1. PLoS ONE 6:e16116PubMedPubMedCentralCrossRef
Metadata
Title
Cannabinoids, TRPV and nitric oxide: the three ring circus of neuronal excitability
Authors
Giuditta Gambino
Valerio Rizzo
Giuseppe Giglia
Giuseppe Ferraro
Pierangelo Sardo
Publication date
01-01-2020
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-019-01992-9

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