nach oben

Brain Structure and Function

Erschienen in:

26.06.2020 | Original Article

Direct administration of ifenprodil and citalopram into the nucleus accumbens inhibits cue-induced nicotine seeking and associated glutamatergic plasticity

verfasst von: Jonna M. Leyrer-Jackson, Jose A. Piña, Joseph McCallum, M. Foster Olive, Cassandra D. Gipson

Erschienen in: Brain Structure and Function | Ausgabe 7/2020

Einloggen, um Zugang zu erhalten

Abstract

Nicotine use disorder has been associated with glutamatergic alterations within the basal ganglia that might contribute to relapse. Specifically, initiation of cue-induced nicotine seeking produces rapid, transient synaptic potentiation (t-SP) in nucleus accumbens core (NAcore) medium spiny neurons (MSNs), defined as increases in spine head diameter and AMPA to NMDA current ratios (A/N). Ifenprodil, which inhibits nicotine reinstatement when administered systemically, antagonizes GluN2B-containing NMDA receptors, has affinity for serotonin receptors, and blocks serotonin transporters (SERT). The mechanisms underlying its therapeutic efficacy, however, remain unknown. Using pharmacological and genetic approaches, the current study examined the role of NAcore GluN2B receptors as well as SERT in mediating cue-induced nicotine seeking and associated MSN structure and physiology. Prior to reinstatement, rats received intra-NAcore injections of either ifenprodil, citalopram or artificial cerebral spinal fluid (15 min prior), or GluN2B or control siRNAs (3 consecutive days prior). Rats were sacrificed after a 15-min cue-induced reinstatement session for dendritic spine analysis, western blotting or whole-cell electrophysiology. Intra-NAcore ifenprodil blocked nicotine-seeking behavior and promoted a higher frequency of shorter spines on MSN dendrites. However, a decrease in membrane-bound GluN2B receptor expression did not prevent cue-induced nicotine seeking or associated MSN cell physiology. Interestingly, intra-NAcore citalopram, an SSRI, prevented cue-induced nicotine seeking. Together, these results indicate that the therapeutic effects of ifenprodil on cue-induced nicotine seeking may, in part, be due to its actions at SERT rather than GluN2B, which may be specific to nicotine-seeking as opposed to other drugs of abuse.

Nur mit Berechtigung zugänglich

Akashi K, Kakizaki T, Kamiya H, Fukaya M, Yamasaki M, Abe M, Natsume R, Watanabe M, Sakimura K (2009) NMDA receptor GluN2B (GluR epsilon 2/NR2B) subunit is crucial for channel function, postsynaptic macromolecular organization, and actin cytoskeleton at hippocampal CA3 synapses. J Neurosci 29(35):10869–10882. https://doi.org/10.1523/JNEUROSCI.5531-08.2009CrossRefPubMedPubMedCentral

Bell RF, Kalso EA (2018) Ketamine for pain management. Pain Rep 3(5):e674. https://doi.org/10.1097/PR9.0000000000000674CrossRefPubMedPubMedCentral

Bell RF, Dahl JB, Moore RA, Kalso E (2006) Perioperative ketamine for acute postoperative pain. Cochrane Database Syst Rev 1:CD004603. https://doi.org/10.1002/14651858.CD004603.pub2CrossRef

Bezchlibnyk-Butler K, Aleksic I, Kennedy SH (2000) Citalopram—a review of pharmacological and clinical effects. J Psychiatry Neurosci 25(3):241–254PubMedPubMedCentral

Bisaga A, Popik P, Bespalov AY, Danysz W (2000) Therapeutic potential of NMDA receptor antagonists in the treatment of alcohol and substance use disorders. Expert Opin Investig Drugs 9(10):2233–2248. https://doi.org/10.1517/13543784.9.10.2233CrossRefPubMed

Chen JP, van Praag HM, Gardner EL (1991) Activation of 5-HT3 receptor by 1-phenylbiguanide increases dopamine release in the rat nucleus accumbens. Brain Res 543(2):354–357CrossRef

Chenard BL, Shalaby IA, Koe BK, Ronau RT, Butler TW, Prochniak MA, Schmidt AW, Fox CB (1991) Separation of alpha 1 adrenergic and N-methyl-d-aspartate antagonist activity in a series of ifenprodil compounds. J Med Chem 34(10):3085–3090. https://doi.org/10.1021/jm00114a018CrossRefPubMed

Conrad KL, Tseng KY, Uejima JL, Reimers JM, Heng LJ, Shaham Y, Marinelli M, Wolf ME (2008) Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454(7200):118–121. https://doi.org/10.1038/nature06995CrossRefPubMedPubMedCentral

Dajas-Bailador F, Wonnacott S (2004) Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol Sci 25(6):317–324. https://doi.org/10.1016/j.tips.2004.04.006CrossRefPubMed

De Sarro GB, Bagetta G, Spagnolo C, Nistico G (1993) Antagonists of N-methyl-D-aspartate receptors block seizures induced by putrescine in the deep prepiriform. Neuropharmacology 32(1):43–50CrossRef

Dong Y, Nestler EJ (2014) The neural rejuvenation hypothesis of cocaine addiction. Trends Pharmacol Sci 35(8):374–383CrossRef

Elias GM, Elias LA, Apostolides PF, Kriegstein AR, Nicoll RA (2008) Differential trafficking of AMPA and NMDA receptors by SAP102 and PSD-95 underlies synapse development. Proc Natl Acad Sci USA 105(52):20953–20958. https://doi.org/10.1073/pnas.0811025106CrossRefPubMed

Foster Olive M, Del Franco AP, Gipson CD (2018) Diolistic labeling and analysis of dendritic spines. Methods Mol Biol 1727:179–200. https://doi.org/10.1007/978-1-4939-7571-6_14CrossRefPubMed

Gipson CD, Reissner KJ, Kupchik YM, Smith AC, Stankeviciute N, Hensley-Simon ME, Kalivas PW (2013a) Reinstatement of nicotine seeking is mediated by glutamatergic plasticity. Proc Natl Acad Sci USA 110(22):9124–9129. https://doi.org/10.1073/pnas.1220591110CrossRefPubMed

Gipson CD, Kupchik YM, Shen H, Reissner KJ, Thomas CA, Kalivas PW (2013b) Relapse induced by cues predicting cocaine depends on rapid, transient synaptic potentiation. Neuron. https://doi.org/10.1016/j.neuron.2013.01.00CrossRefPubMedPubMedCentral

Gipson CD, Kupchik YM, Kalivas PW (2014) Rapid, transient synaptic plasticity in addiction. Neuropharmacology 76(Pt B):276–286. https://doi.org/10.1016/j.neuropharm.2013.04.032CrossRefPubMed

Goenaga J, Powell GL, Leyrer-Jackson JM, Pina J, Phan S, Prakapenka AV, Koebele SV, Namba MD, McClure EA, Bimonte-Nelson HA, Gipson CD (2019) N-acetylcysteine yields sex-specific efficacy for cue-induced reinstatement of nicotine seeking. Addict Biol. https://doi.org/10.1111/adb.12711CrossRefPubMed

Halt AR, Dallapiazza RF, Zhou Y, Stein IS, Qian H, Juntti S, Wojcik S, Brose N, Silva AJ, Hell JW (2012) CaMKII binding to GluN2B is critical during memory consolidation. EMBO J 31(5):1203–1216. https://doi.org/10.1038/emboj.2011.482CrossRefPubMedPubMedCentral

Herman BH, Vocci F, Bridge P (1995) The effects of NMDA receptor antagonists and nitric oxide synthase inhibitors on opioid tolerance and withdrawal. Medication development issues for opiate addiction. Neuropsychopharmacology 13(4):269–293. https://doi.org/10.1016/0893-133X(95)00140-9CrossRefPubMed

Hitsman B, Spring B, Borrelli B, Niaura R, Papandonatos GD (2001) Influence of antidepressant pharmacotherapy on behavioral treatment adherence and smoking cessation outcome in a combined treatment involving fluoxetine. Exp Clin Psychopharmacol 9(4):355–362. https://doi.org/10.1037//1064-1297.9.4.355CrossRefPubMed

Hotulainen P, Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189(4):619–629. https://doi.org/10.1083/jcb.201003008CrossRefPubMedPubMedCentral

Huang YH, Lin Y, Mu P, Lee BR, Brown TE, Wayman G, Marie H, Liu W, Yan Z, Sorg BA, Schlüter OM, Zukin RS, Dong Y (2009) In vivo cocaine experience generates silent synapses. Neuron 63(1):40–47. https://doi.org/10.1016/j.neuron.2009.06.007CrossRefPubMedPubMedCentral

Hughes JR, Stead LF, Hartmann-Boyce J, Cahill K, Lancaster T (2014) Antidepressants for smoking cessation. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD000031.pub4CrossRefPubMedPubMedCentral

Inoue T, Li XB, Abekawa T, Kitaichi Y, Izumi T, Nakagawa S, Koyama T (2004) Selective serotonin reuptake inhibitor reduces conditioned fear through its effect in the amygdala. Eur J Pharmacol 497(3):311–316CrossRef

Knackstedt LA, LaRowe S, Mardikian P, Malcolm R, Upadhyaya H, Hedden S, Markou A, Kalivas PW (2009) The role of cysteine–glutamate exchange in nicotine dependence in rats and humans. Biol Psychiatry 65(10):841–845. https://doi.org/10.1016/j.biopsych.2008.10.040CrossRefPubMed

Kobayashi T, Washiyama K, Ikeda K (2006) Inhibition of G protein-activated inwardly rectifying K⁺ channels by ifenprodil. Neuropsychopharmacology 31(3):516–524. https://doi.org/10.1038/sj.npp.1300844CrossRefPubMed

Li Z, Chen Y (2019) Ketamine reduces pain and opioid consumption after total knee arthroplasty: a meta-analysis of randomized controlled studies. Int J Surg 70:70–83. https://doi.org/10.1016/j.ijsu.2019.08.026CrossRefPubMed

Ma YY, Chu NN, Guo CY, Han JS, Cui CL (2007) NR2B-containing NMDA receptor is required for morphine—but not stress-induced reinstatement. Exp Neurol 203(2):309–319. https://doi.org/10.1016/j.expneurol.2006.08.014CrossRefPubMed

Maksay G, Bíró T, Bugovics G (2005) Allosteric modulation of 5-HT3 serotonin receptors. Eur J Pharmacol 514(1):17–24. https://doi.org/10.1016/j.ejphar.2005.03.019CrossRefPubMed

Manepalli S, Surratt CK, Madura JD, Nolan TL (2012) Monoamine transporter structure, function, dynamics, and drug discovery: a computational perspective. AAPS J 14(4):820–831. https://doi.org/10.1208/s12248-012-9391-0CrossRefPubMedPubMedCentral

McCool BA, Lovinger DM (1995) Ifenprodil inhibition of the 5-hydroxytryptamine3 receptor. Neuropharmacology 34(6):621–629CrossRef

Miech R, Johnston L, O'Malley PM, Bachman JG, Patrick ME (2019) Adolescent vaping and nicotine use in 2017–2018—U.S. national estimates. N Engl J Med 380(2):192–193. https://doi.org/10.1056/NEJMc1814130CrossRefPubMed

Mineur YS, Picciotto MR (2009) Biological basis for the co-morbidity between smoking and mood disorders. J Dual Diagn 5(2):122–130CrossRef

Misra C, Brickley SG, Farrant M, Cull-Candy SG (2000) Identification of subunits contributing to synaptic and extrasynaptic NMDA receptors in Golgi cells of the rat cerebellum. J Physiol 524(Pt 1):147–162. https://doi.org/10.1111/j.1469-7793.2000.00147.xCrossRefPubMedPubMedCentral

Mulholland PJ, Chandler LJ, Kalivas PW (2016) Signals from the fourth dimension regulate drug relapse. Trends Neurosci. https://doi.org/10.1016/j.tins.2016.04.007CrossRefPubMedPubMedCentral

Overby PF, Daniels CW, Del Franco A, Goenaga J, Powell GL, Gipson CD, Sanabria F (2018) Effects of nicotine self-administration on incentive salience in male Sprague Dawley rats. Psychopharmacology 235(4):1121–1130. https://doi.org/10.1007/s00213-018-4829-4CrossRefPubMed

Papouin T, Ladepeche L, Ruel J, Sacchi S, Labasque M, Hanini M, Groc L, Pollegioni L, Mothet JP, Oliet SH (2012) Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150(3):633–646. https://doi.org/10.1016/j.cell.2012.06.029CrossRefPubMed

Patterson M, Yasuda R (2011) Signalling pathways underlying structural plasticity of dendritic spines. Br J Pharmacol 163(8):1626–1638. https://doi.org/10.1111/j.1476-5381.2011.01328.xCrossRefPubMedPubMedCentral

Paxinos G, Franklin KB (2013) The mouse brain in stereotaxic coordinates, 4th edn. Academic Press, Amsterdam, pp 31–231

Petralia RS (2012) Distribution of extrasynaptic NMDA receptors on neurons. Scientif World J 2012:267120. https://doi.org/10.1100/2012/267120CrossRef

Poleszak E, Wosko S, Serefko A, Wlaz A, Kasperek R, Dudka J, Wrobel A, Nowak G, Wlaz P (2014) The effects of ifenprodil on the activity of antidepressant drugs in the forced swim test in mice. Pharmacol Rep 66(6):1031–1036. https://doi.org/10.1016/j.pharep.2014.06.016CrossRefPubMed

Powell GL, Leyrer-Jackson JM, Goenaga J, Namba MD, Piña J, Spencer S, Stankeviciute N, Schwartz D, Allen NP, Del Franco AP, McClure EA, Olive MF, Gipson CD (2019) Chronic treatment with N-acetylcysteine decreases extinction responding and reduces cue-induced nicotine-seeking. Physiol Rep 7(1):e13958. https://doi.org/10.14814/phy2.13958CrossRefPubMedPubMedCentral

Russo SJ, Dietz DM, Dumitriu D, Morrison JH, Malenka RC, Nestler EJ (2010) The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci 33(6):267–276. https://doi.org/10.1016/j.tins.2010.02.002CrossRefPubMedPubMedCentral

Sanacora G, Frye MA, McDonald W, Mathew SJ, Turner MS, Schatzberg AF, Summergrad P, Nemeroff CB, American Psychiatric Association (APA) Council of Research Task Force on Novel Biomarkers, and Treatments (2017) A consensus statement on the use of ketamine in the treatment of mood disorders. JAMA Psychiatry 74(4):399–405. https://doi.org/10.1001/jamapsychiatry.2017.0080CrossRefPubMed

Schrantee A, Solleveld MM, Schwantje H, Bruin WB, Mutsaerts HMM, Adriaanse SM, Lucassen P, Booij J, Reneman L (2019) Dose-dependent effects of the selective serotonin reuptake inhibitor citalopram: a combined SPECT and phMRI study. J Psychopharmacol. https://doi.org/10.1177/0269881119836229CrossRefPubMedPubMedCentral

Schumann J, Matzner H, Michaeli A, Yaka R (2009) NR2A/B-containing NMDA receptors mediate cocaine-induced synaptic plasticity in the VTA and cocaine psychomotor sensitization. Neurosci Lett 461(2):159–162. https://doi.org/10.1016/j.neulet.2009.06.002CrossRefPubMed

Scofield MD, Heinsbroek JA, Gipson CD, Kupchik YM, Spencer S, Smith AC, Roberts-Wolfe D, Kalivas PW (2016a) The nucleus accumbens: mechanisms of addiction across drug classes reflect the importance of glutamate homeostasis. Pharmacol Rev 68(3):816–871. https://doi.org/10.1124/pr.116.012484CrossRefPubMedPubMedCentral

Scofield MD, Li H, Siemsen BM, Healey KL, Tran PK, Woronoff N, Boger HA, Kalivas PW, Reissner KJ (2016b) cocaine self-administration and extinction leads to reduced glial fibrillary acidic protein expression and morphometric features of astrocytes in the nucleus accumbens core. Biol Psychiatry 80(3):207–215. https://doi.org/10.1016/j.biopsych.2015.12.022CrossRefPubMed

Shen H, Moussawi K, Zhou W, Toda S, Kalivas PW (2011) Heroin relapse requires long-term potentiation-like plasticity mediated by NMDA2b-containing receptors. Proc Natl Acad Sci USA 108(48):19407–19412. https://doi.org/10.1073/pnas.1112052108CrossRefPubMed

Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368(6467):144–147. https://doi.org/10.1038/368144a0CrossRefPubMed

Shoaib M, Buhidma Y (2018) Why are antidepressant drugs effective smoking cessation aids? Current Neuropharmacol 16(4):426–437CrossRef

Sim-Selley LJ, Selley DE, Vogt LJ, Childers SR, Martin TJ (2000) Chronic heroin self-administration desensitizes mu opioid receptor-activated G-proteins in specific regions of rat brain. J Neurosci 20(12):4555–4562CrossRef

St Helen G, Havel C, Dempsey DA, Jacob P 3rd, Benowitz NL (2016) Nicotine delivery, retention and pharmacokinetics from various electronic cigarettes. Addiction 111(3):535–544. https://doi.org/10.1111/add.13183CrossRefPubMed

Stefanik MT, Kupchik YM, Kalivas PW (2016) Optogenetic inhibition of cortical afferents in the nucleus accumbens simultaneously prevents cue-induced transient synaptic potentiation and cocaine-seeking behavior. Brain Struct Funct 221(3):1681–1689. https://doi.org/10.1007/s00429-015-0997-8CrossRefPubMed

Stolerman IP, Jarvis MJ (1995) The scientific case that nicotine is addictive. Psychopharmacology 117(1):2–10 (discussion 14–20)CrossRef

Talbot JN, Geffert LM, Jorvig JE, Goldstein RI, Nielsen CL, Wolters NE, Amos ME, Munro CA, Dallman E, Mereu M, Tanda G, Katz JL, Indarte M, Madura JD, Choi H, Leak RK, Surratt CK (2016) Rapid and sustained antidepressant properties of an NMDA antagonist/monoamine reuptake inhibitor identified via transporter-based virtual screening. Pharmacol Biochem Behav 150–151:22–30. https://doi.org/10.1016/j.pbb.2016.08.007CrossRefPubMed

Tomek SE, Lacrosse AL, Nemirovsky NE, Olive MF (2013) NMDA receptor modulators in the treatment of drug addiction. Pharmaceuticals (Basel) 6(2):251–268. https://doi.org/10.3390/ph6020251CrossRef

van Zundert B, Yoshii A, Constantine-Paton M (2004) Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci 27(7):428–437. https://doi.org/10.1016/j.tins.2004.05.010CrossRefPubMed

Wang TW, Asman K, Gentzke AS, Cullen KA, Holder-Hayes E, Reyes-Guzman C, Jamal A, Neff L, King BA (2018) Tobacco product use among adults—United States, 2017. MMWR Morb Mortal Wkly Rep 67(44):1225–1232. https://doi.org/10.15585/mmwr.mm6744a2CrossRefPubMedPubMedCentral

Yao Y, Ju P, Liu H, Wu X, Niu Z, Zhu Y, Zhang C, Fang Y (2020) Ifenprodil rapidly ameliorates depressive-like behaviors, activates mTOR signaling and modulates proinflammatory cytokines in the hippocampus of CUMS rats. Psychopharmacology. https://doi.org/10.1007/s00213-020-05469-0CrossRefPubMed

Yoshimoto K, McBride WJ (1992) Regulation of nucleus accumbens dopamine release by the dorsal raphe nucleus in the rat. Neurochem Res 17(5):401–407CrossRef

Titel: Direct administration of ifenprodil and citalopram into the nucleus accumbens inhibits cue-induced nicotine seeking and associated glutamatergic plasticity
verfasst von: Jonna M. Leyrer-Jackson
Jose A. Piña
Joseph McCallum
M. Foster Olive
Cassandra D. Gipson
Publikationsdatum: 26.06.2020
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 7/2020
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-020-02103-9

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

16.04.2024 | Maligne primäre ZNS-Tumoren | Nachrichten

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Direct administration of ifenprodil and citalopram into the nucleus accumbens inhibits cue-induced nicotine seeking and associated glutamatergic plasticity

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Manche Gestagene können das Risiko für Meningeome erhöhen

Parkinson: Größere Studie bestätigt Genauigkeit von Hauttest

Simple Kortisontherapie stoppt primär progrediente Aphasie

Impostor-Syndrom häufig bei Hyperhidrose zu finden

Update Neurologie

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 7/2020

Serotonergic treatment normalizes midbrain dopaminergic neuron increase after periaqueductal gray stimulation

Male-specific features are reduced in Mecp2-null mice: analyses of vasopressinergic innervation, pheromone production and social behaviour

Expression of GPR55 and either cannabinoid CB1 or CB2 heteroreceptor complexes in the caudate, putamen, and accumbens nuclei of control, parkinsonian, and dyskinetic non-human primates

Postnatal exposure to an acoustically enriched environment alters the morphology of neurons in the adult rat auditory system

The effect of bilingualism on brain development from early childhood to young adulthood

Prelimbic cortical targets of ventromedial thalamic projections include inhibitory interneurons and corticostriatal pyramidal neurons in the rat

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Manche Gestagene können das Risiko für Meningeome erhöhen

Parkinson: Größere Studie bestätigt Genauigkeit von Hauttest

Simple Kortisontherapie stoppt primär progrediente Aphasie

Impostor-Syndrom häufig bei Hyperhidrose zu finden

Update Neurologie