Cross state-dependency of learning between tramadol and MK-801 in the mouse dorsal hippocampus: involvement of nitric oxide (NO) signaling pathway

Majid Jafari‐Sabet1, Shiva Amiri1, Ramin Ataee2
1Department of Pharmacology, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran
2Pharmaceutical Sciences Research Center, Mazandaran University of Medical Sciences, Sari, Iran

Tóm tắt

Từ khóa


Tài liệu tham khảo

Alijanpour S, Rezayof A, Zarrindast MR (2013) Dorsal hippocampal cannabinoid CB1 receptors mediate the interactive effects of nicotine and ethanol on passive avoidance learning in mice. Addict Biol 18:241–251

Athos J, Impey S, Pineda VV, Chen X, Storm DR (2002) Hippocampal CRE mediated gene expression is required for contextual memory formation. Nat Neurosci 5:1119–1120

Babalonis S, Lofwall MR, Nuzzo PA, Siegel AJ, Walsh SL (2013) Abuse liability and reinforcing efficacy of oral tramadol in humans. Drug Alcohol Depend 129:116–124

Barbosa J, Faria J, Queirós O, Moreira R, Carvalho F, Dinis-Oliveira RJ (2016) Comparative metabolism of tramadol and tapentadol: a toxicological perspective. Drug Metab Rev 15:1–16

Barros DM, Mello e Souza T, De David T, Choi H, Aguzzoli A, Madche C, Ardenghi P, Medina JH, Izquierdo I (2001) Simultaneous modulation of retrieval by dopaminergic D(1), beta-noradrenergic, serotonergic-1A and cholinergic muscarinic receptors in cortical structures of the rat. Behav Brain Res 124:1–7

Bassiony MM, Youssef UM, Hassan MS, Salah El-Deen GM, El-Gohari H, Abdelghani M, Abdalla A, Ibrahim DH (2017) Cognitive impairment and tramadol dependence. J Clin Psychopharmacol 37:61–66

Bodnar RJ (2016) Endogenous opiates and behavior: 2014. Peptides 75:18–70

Brigman JL, Wright T, Talani G, Prasad-Mulcare S, Jinde S, Seabold GK, Mathur P, Davis MI, Bock R, Gustin RM, Colbran RJ, Alvarez VA, Nakazawa K, Delpire E, Lovinger DM, Holmes A (2010) Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J Neurosci 30:4590–4600

Cai Z, Xiao F, Lee B, Paul IA, Rhodes PG (1999) Prenatal hypoxia-ischemia alters expression and activity of nitric oxide synthase in the young rat brain and causes learning deficits. Brain Res Bull 49:359–365

Cammarota M, Bevilaqua LR, Ardenghi P, Paratcha G, Levi de Stein M, Izquierdo I, Medina JH (2000) Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning: abolition by NMDA receptor blockade. Brain Res Mol Brain Res 76:36–46

Castellano C, Cestari V, Ciamei A (2001) NMDA receptors and learning and memory processes. Curr Drug Targets 2:273–283

Ceretta AP, Camera K, Mello CF, Rubin MA (2008) Arcaine and MK-801make recall state-dependent in rats. Psychopharmacology 201:405–411

Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 129:1659–1673

De Vries TJ, Shippenberg TS (2002) Neural systems underlying opiate addiction. J Neurosci 22:3321–3325

Epstein DH, Preston KL, Jasinski DR (2006) Abuse liability, behavioral pharmacology, and physical-dependence potential of opioids in humans and laboratory animals: lessons from tramadol. Biol Psychol 73:90–99

Feil R, Kleppisch T (2008) NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol 184:529–560

Ghasemzadeh Z, Rezayof A (2016) Role of hippocampal and prefrontal cortical signaling pathways in dextromethorphan effect on morphine-induced memory impairment in rats. Neurobiol Learn Mem 128:23–32

Harooni HE, Naghdi N, Sepehri H, Rohani AH (2009) The role of hippocampal nitric oxide (NO) on learning and immediate, short- and long-term memory retrieval in inhibitory avoidance task in male adult rats. Behav Brain Res 201:166–172

Harrod SB, Flint RW, Riccio DC (2001) MK-801 induced retrieval, but not acquisition, deficits for passive avoidance conditioning. Pharmacol Biochem Behav 69:585–593

Ishide T, Mancini M, Maher TJ, Chayaikul P, Ally A (2000) Rostral ventrolateral medulla opioid receptor activation modulates glutamate release and attenuates the exercise pressor reflex. Brain Res 865:177–185

Izquierdo I, Bevilaqua LR, Rossato JI, Bonini JS, Medina JH, Cammarota M (2006) Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci 29:496–505

Jafari-Sabet M (2006a) NMDA receptor blockers prevents the facilitatory effects of post-training intra-dorsal hippocampal NMDA and physostigmine on memory retention of passive avoidance learning in rats. Behav Brain Res 169:20–127

Jafari-Sabet M (2006b) NMDA receptor antagonists antagonize the facilitatory effects of post-training intra-basolateral amygdala NMDA and physostigmine on passive avoidance learning. Eur J Pharmacol 529:122–128

Jafari-Sabet M (2011) Involvement of dorsal hippocampal muscarinic cholinergic receptors on muscimol state-dependent memory of passive avoidance in mice. Life Sci 88:1136–1141

Jafari-Sabet M, Jannat-Dastjerdi I (2009) Muscimol state-dependent memory: involvement of dorsal hippocampal mu-opioid receptors. Behav Brain Res 202:5–10

Jafari-Sabet M, Karimi AM (2017) Cross state-dependency of learning between arachidonylcyclopropylamide (ACPA) and muscimol in the mouse dorsal hippocampus. Pharmacol Biochem Behav 163:66–73

Jafari-Sabet M, Zarrindast MR, Rezayat M, Rezayof A, Djahanguiri B (2005) The influence of NMDA receptor agonist and antagonist on morphine state-dependent memory of passive avoidance in mice. Life Sci 78:57–163

Jafari-Sabet M, Banafshe HR, Khodadadnejad MA (2013) Modulation of muscimol state-dependent memory by α2-adrenoceptors of the dorsal hippocampal area. Eur J Pharmacol 710:92–99

Jafari-Sabet M, Khodadadnejad MA, Ghoraba S, Ataee R (2014) Nitric oxide in the dorsal hippocampal area is involved on muscimol state-dependent memory in the step-down passive avoidance test. Pharmacol Biochem Behav 117:37–143

Jafari-Sabet M, Jafari-Sabet AR, Dizaji-Ghadim A (2016) Tramadol state-dependent memory: involvement of dorsal hippocampal muscarinic acetylcholine receptors. Behav Pharmacol 27:470–478

Jafari-Sabet M, Mofidi H, Attarian-Khosroshahi MS (2018) NMDA receptors in the dorsal hippocampal area are involved in tramadol state-dependent memory of passive avoidance learning in mice. Can J Physiol Pharmacol 96:45–50

Jamali-Raeufy N, Nasehi M, Ebrahimi-Ghiri M, Zarrindast MR (2011) Cross state-dependency of learning between WIN55, 212-2 and scopolamine in rat dorsal hippocampus. Neurosci Lett 491:227–231

Korpi ER, den Hollander B, Farooq U, Vashchinkina E, Rajkumar R, Nutt DJ, Hyytiä P, Dawe GS (2015) Mechanisms of action and persistent neuroplasticity by drugs of abuse. Pharmacol Rev 67:872–1004

Lanier RK, Lofwall MR, Mintzer MZ, Bigelow GE, Strain EC (2010) Physical dependence potential of daily tramadol dosing in humans. Psychopharmacology 211:457–466

Lansink CS, Goltstein PM, Lankelma JV, McNaughton BL, Pennartz CM (2009) Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol 7:e1000173

Ledo A, Frade J, Barbosa RM, Laranjinha J (2004) Nitric oxide in brain: diffusion, targets and concentration dynamics in hippocampal subregions. Mol Asp Med 25:75–89

de Lima MN, Laranja DC, Bromberg E, Roesler R, Schröder N (2005) Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats. Behav Brain Res 156:139–143

Lisman J (2003) Long-term potentiation: outstanding questions and attempted synthesis. Philos Trans Royal Soc London B: Bio Sci 358:829–842

Ma YY, Meng L, Guo CY, Han JS, Lee DY, Cui CL (2009) Dose- and time dependent, context-induced elevation of dopamine and its metabolites in the nucleus accumbens of morphine-induced CPP rats. Behav Brain Res 204:192–199

Majlessi N, Choopani S, Bozorgmehr T, Azizi Z (2008) Involvement of hippocampal nitric oxide in spatial learning in the rat. Neurobiol Learn Mem 90:413–419

Martin JL, Itzhak Y (2000) 7-Nitroindazole blocks nicotine-induced conditioned place preference but not LiCl-induced conditioned place aversion. Neuroreport 11:947–949

McGaugh JL (2013) Making lasting memories: remembering the significant. Proc Natl Acad Sci U S A 110:10402–10407

Naqvi S, Martin KJ, Arthur JS (2014) CREB phosphorylation at Ser133 regulates transcription via distinct mechanisms downstream of cAMP and MAPK signaling. Biochem J 458:469–479

Neves G, Cooke SF, Bliss TV (2008) Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 9:65–75

Nossaman VE, Ramadhyani U, Kadowitz PJ, Nossaman BD (2010) Advances in perioperative pain management: use of medications with dual analgesic mechanisms, tramadol & tapentadol. Anesthesiol Clin 28:647–666

O’Connor EC, Mead AN (2010) Tramadol acts as a weak reinforcer in the rat self-administration model, consistent with its low abuse liability in humans. Pharmacol Biochem Behav 96:279–286

Oliva P, Aurilio C, Massimo F, Grella A, Maione S, Grella E, Scafuro M, Rossi F, Berrino L (2002) The antinociceptive effect of tramadol in the formalin test is mediated by the serotonergic component. Eur J Pharmacol 445:179–185

Paoletti P, Neyton J (2007) NMDA receptor subunits: function and pharmacology. Curr Opin Pharmacol 7:39–47

Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic Press, New York

Place R, Farovik A, Brockmann M, Eichenbaum H (2016) Bidirectional prefrontal-hippocampal interactions support context-guided memory. Nat Neurosci 19:992–994

Peters J, De Vries TJ (2012) Glutamate mechanisms underlying opiate memories. Cold Spring Harb Perspect Med 2:a012088

Pittenger C, Huang YY, Paletzki RF, Bourtchouladze R, Scanlin H, Vronskaya S, Kandel ER (2002) Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34:447–462

Pu L, Bao GB, Xu NJ, Ma L, Pei G (2002) Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22:1914–1921

Rosa J, Myskiw JC, Furini CR, Sapiras GG, Izquierdo I (2014) Fear extinction can be made state-dependent on peripheral epinephrine: role of norepinephrine in the nucleus tractus solitarius. Neurobiol Learn Mem 113:55–61

Shen F, Wang XW, Ge FF, Li YJ, Cui CL (2016) Essential role of the NO signaling pathway in the hippocampal CA1 in morphine-associated memory depends on glutaminergic receptors. Neuropharmacology 102:216–228

Shiga Y, Minami K, Shiraishi M, Uezono Y, Murasaki O, Kaibara M, Shigematsu A (2002) The inhibitory effects of tramadol on muscarinic receptor-induced responses in Xenopus oocytes expressing cloned M(3) receptors. Anesth Analg 95:1269–1273

Shiraishi M, Minami K, Uezono Y, Yanagihara N, Shigematsu A (2001) Inhibition by tramadol of muscarinic receptor-induced responses in cultured adrenal medullary cells and in Xenopus laevis oocytes expressing cloned M1 receptors. J Pharmacol Exp Ther 299:255–260

Solati J (2011) Dorsal hippocampal N-methyl-D-aspartate glutamatergic and μ-opioidergic systems modulate anxiety behaviors in rats in a non-interactive manner. Kaohsiung J Med Sci 27:485–493

Wagner JJ, Etemad LR, Thompson AM (2001) Opioid-mediated facilitation of long-term depression in rat hippocampus. J Pharmacol Exp Ther 296:776–781

Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093–1097

Zarrindast MR, Rezayof A (2004) Morphine state-dependent learning: sensitization and interactions with dopamine receptors. Eur J Pharmacol 497:197–204

Zarrindast MR, Jafari-Sabet M, Rezayat M, Djahanguiri B, Rezayof A (2006a) Involvement of NMDA receptors in morphine state-dependent learning in mice. Int J Neurosci 116:731–743

Zarrindast MR, Nouraei N, Khallilzadeh A, Askari E (2006b) Influence of acute and sub-chronic nicotine pretreatment on morphine state-dependent learning. Behav Brain Res 173:268–273

Zarrindast MR, Ownegh V, Rezayof A, Ownegh F (2014) The involvement of dorsal hippocampus in dextromethorphan-induced state-dependent learning in mice. Pharmacol Biochem Behav 116:90–95

Zhang M, Jing L, Liu Q, Wen RT, Li JX, Li YL, Gong Q, Liang JH (2012) Tramadol induces conditioned place preference in rats: interactions with morphine and buprenorphine. Neurosci Lett 520:87–91