Central Nervous System Agents in Medicinal Chemistry

Author(s): Fatemeh Babaei, Masoumeh Kourosh-Arami* and Mona Farhadi

DOI: 10.2174/1871524923666230816103223

NMDA Receptors in the Rat Paraventricular Thalamic Nucleus Reduce the Naloxone-induced Morphine Withdrawal

Page: [119 - 125] Pages: 7

  • * (Excluding Mailing and Handling)

Abstract

Background: NMDA receptors have a significant role in the development of opioid physical dependence. Evidence demonstrated that a drug of abuse enhances neuronal excitability in the Paraventricular Nucleus (PVT). The current research studied whether blocking NMDA receptors through the administration of MK801 in the PVT nucleus could affect the development of Morphine (Mor) dependence and hence the behavioral indices induced by morphine withdrawal in rats.

Methods: Male Wistar rats weighing 250-300 g were used. For induction of drug dependence, we injected Mor subcutaneously (s.c.) (6, 16, 26, 36, 46, 56, and 66 mg/kg, 2 ml/kg) at an interval of 24 hours for 7 days. Animals were divided into two groups in which the NMDA receptor antagonist, MK801 (20 mM in 0.1 ml), or its vehicle were applied into the PVT nucleus for 7 days before each Mor administration. On day 8, after injection of naloxone (Nal, 2.5 mg/kg, i.p.), withdrawal behaviors were checked for 25 min.

Results: The current results demonstrated that the blockade of the NMDA receptor in the PVT nucleus significantly increased withdrawal behaviors provoked by the application of Nal in morphinedependent (Mor-d) rats.

Conclusion: We concluded that the NMDA receptor in the PVT nucleus changes the development of Mor dependence.

Graphical Abstract

[1]
Choi, E.A.; McNally, G.P. Paraventricular thalamus balances danger and reward. J. Neurosci., 2017, 37(11), 3018-3029.
[http://dx.doi.org/10.1523/JNEUROSCI.3320-16.2017] [PMID: 28193686]
[2]
Dong, X.; Li, S.; Kirouac, G.J. Collateralization of projections from the paraventricular nucleus of the thalamus to the nucleus accumbens, bed nucleus of the stria terminalis, and central nucleus of the amygdala. Brain Struct. Funct., 2017, 222(9), 3927-3943.
[http://dx.doi.org/10.1007/s00429-017-1445-8] [PMID: 28528379]
[3]
Kirouac, G.J. Placing the paraventricular nucleus of the thalamus within the brain circuits that control behavior. Neurosci. Biobehav. Rev., 2015, 56, 315-329.
[http://dx.doi.org/10.1016/j.neubiorev.2015.08.005] [PMID: 26255593]
[4]
Li, S.; Kirouac, G.J. Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J. Comp. Neurol., 2008, 506(2), 263-287.
[http://dx.doi.org/10.1002/cne.21502] [PMID: 18022956]
[5]
Liu, Z.; Wang, Y.; Cai, L.; Li, Y.; Chen, B.; Dong, Y.; Huang, Y.H. Prefrontal cortex to accumbens projections in sleep regulation of reward. J. Neurosci., 2016, 36(30), 7897-7910.
[http://dx.doi.org/10.1523/JNEUROSCI.0347-16.2016] [PMID: 27466335]
[6]
Yeoh, J.W.; Morgan, H.J.; Brett, A.G.; Christopher, V.D. Electrophysiological characteristics of paraventricular thalamic (PVT) neurons in response to chronic cocaine exposure: Effects of cocaine-and amphetamine-regulated transcript (CART). Front. Behav. Neurosci., 2014, 8, 280.
[http://dx.doi.org/10.3389/fnbeh.2014.00280] [PMID: 25309361]
[7]
Browning, J.R.; Jansen, H.T.; Sorg, B.A. Inactivation of the paraventricular thalamus abolishes the expression of cocaine conditioned place preference in rats. Drug Alcohol Depend., 2014, 134, 387-390.
[http://dx.doi.org/10.1016/j.drugalcdep.2013.09.021] [PMID: 24139547]
[8]
Hamlin, A.S.; Clemens, K.J.; Choi, E.A.; McNally, G.P. Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking. Eur. J. Neurosci., 2009, 29(4), 802-812.
[http://dx.doi.org/10.1111/j.1460-9568.2009.06623.x] [PMID: 19200064]
[9]
James, M.H.; Charnley, J.L.; Jones, E.; Levi, E.M.; Yeoh, J.W.; Flynn, J.R.; Smith, D.W.; Dayas, C.V. Cocaine- and amphetamine-regulated transcript (CART) signaling within the paraventricular thalamus modulates cocaine-seeking behaviour. PLoS One, 2010, 5(9), e12980.
[http://dx.doi.org/10.1371/journal.pone.0012980] [PMID: 20886038]
[10]
Neumann, P.A.; Wang, Y.; Yan, Y.; Wang, Y.; Ishikawa, M.; Cui, R.; Huang, Y.H.; Sesack, S.R.; Schlüter, O.M.; Dong, Y. Cocaine-induced synaptic alterations in thalamus to nucleus accumbens projection. Neuropsychopharmacology, 2016, 41(9), 2399-2410.
[http://dx.doi.org/10.1038/npp.2016.52] [PMID: 27074816]
[11]
O’Brien, C.P. Anticraving medications for relapse prevention: A possible new class of psychoactive medications. Am. J. Psychiatry, 2005, 162(8), 1423-1431.
[http://dx.doi.org/10.1176/appi.ajp.162.8.1423] [PMID: 16055763]
[12]
Ong, Z.Y.; Liu, J.J.; Pang, Z.P.; Grill, H.J. Paraventricular thalamic control of food intake and reward: Role of glucagon-like peptide-1 receptor signaling. Neuropsychopharmacology, 2017, 42(12), 2387-2397.
[http://dx.doi.org/10.1038/npp.2017.150] [PMID: 28811669]
[13]
Arami, M.K.; Abdolrahman, S.; Seyyed, M.M.; Gila, M.; Mehrangiz, V.; Iraj, A. The effect of nucleus tractus solitarius nitric oxidergic neurons on blood pressure in diabetic rats. Iran. Biomed. J., 2006, 10(1), 15-19.
[14]
Malakouti, S.M.; Kourosh, A.M.; Sarihi, A.; Hajizadeh, S.; Behzadi, G.; Shahidi, S.; Komaki, A.; Heshmatian, B.; Vahabian, M. Reversible inactivation and excitation of nucleus raphe magnus can modulate tail blood flow of male Wistar rats in response to hypothermia. Iran. Biomed. J., 2008, 12(4), 203-208.
[PMID: 19079538]
[15]
Peyron, C.; Tighe, D.K.; van den Pol, A.N.; de Lecea, L.; Heller, H.C.; Sutcliffe, J.G.; Kilduff, T.S. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci., 1998, 18(23), 9996-10015.
[http://dx.doi.org/10.1523/JNEUROSCI.18-23-09996.1998] [PMID: 9822755]
[16]
Auerbach, S.; Fornal, C.; Jacobs, B.L. Response of serotonin-containing neurons in nucleus raphe magnus to morphine, noxious stimuli, and periaqueductal gray stimulation in freely moving cats. Exp. Neurol., 1985, 88(3), 609-628.
[http://dx.doi.org/10.1016/0014-4886(85)90075-5] [PMID: 3996512]
[17]
Olson, V.G.; Heusner, C.L.; Bland, R.J.; During, M.J.; Weinshenker, D.; Palmiter, R.D. Role of noradrenergic signaling by the nucleus tractus solitarius in mediating opiate reward. Science, 2006, 311(5763), 1017-1020.
[http://dx.doi.org/10.1126/science.1119311] [PMID: 16484499]
[18]
Bell, J.A.; Beglan, C.L. Co-treatment with MK-801 potentiates naloxone-predpitated morphine withdrawal in the isolated spinal cord of the neonatal rat. Eur. J. Pharmacol., 1995, 294(1), 297-301.
[http://dx.doi.org/10.1016/0014-2999(95)00548-X] [PMID: 8788444]
[19]
Kourosh-Arami, M.; Javan, M.; Semnanian, S. Inhibition of orexin receptor 1 contributes to the development of morphine dependence via attenuation of cAMP response element-binding protein and phospholipase Cβ3. J. Chem. Neuroanat., 2020, 108, 101801.
[http://dx.doi.org/10.1016/j.jchemneu.2020.101801] [PMID: 32404265]
[20]
Komaki, A.; Shahidi, S.; Sarihi, A.; Hasanein, P.; Lashgari, R.; Haghparast, A.; Salehi, I.; Arami, M.K. Effects of neonatal C-fiber depletion on interaction between neocortical short-term and long-term plasticity. Basic Clin. Neurosci., 2013, 4(2), 136-145.
[PMID: 25337340]
[21]
Kourosh-Arami, M.; Komaki, A.; Gholami, M. Addiction-induced plasticity in underlying neural circuits. Neurol. Sci., 2022, 43(3), 1605-1615.
[http://dx.doi.org/10.1007/s10072-021-05778-y] [PMID: 35064341]
[22]
Koyuncuoǧlu, H.; Dizdar, Y.; Aricioǧlu, F.; Sayin, Ü. Effects of MK 801 on morphine physical dependence: Attenuation and intensification. Pharmacol. Biochem. Behav., 1992, 43(2), 487-490.
[http://dx.doi.org/10.1016/0091-3057(92)90181-E] [PMID: 1438485]
[23]
Trujillo, K.A.; Akil, H. Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science, 1991, 251(4989), 85-87.
[http://dx.doi.org/10.1126/science.1824728] [PMID: 1824728]
[24]
Zhu, H.; Barr, G.A. Inhibition of morphine withdrawal by the NMDA receptor antagonist MK-801 in rat is age-dependent. Synapse, 2001, 40(4), 282-293.
[http://dx.doi.org/10.1002/syn.1051] [PMID: 11309844]
[25]
Paxinos, G.; Watson, C. A stereotaxic atlas of the rat brain; Academic: New York, 1998.
[26]
van den Pol, A.N. Hypothalamic hypocretin (orexin): Robust innervation of the spinal cord. J. Neurosci., 1999, 19(8), 3171-3182.
[http://dx.doi.org/10.1523/JNEUROSCI.19-08-03171.1999] [PMID: 10191330]
[27]
Kovacic, P.; Somanathan, R. Clinical physiology and mechanism of dizocilpine (MK-801): Electron transfer, radicals, redox metabolites and bioactivity. Oxid. Med. Cell. Longev., 2010, 3(1), 13-22.
[http://dx.doi.org/10.4161/oxim.3.1.10028] [PMID: 20716924]
[28]
Deiana, S.; Watanabe, A.; Yamasaki, Y.; Amada, N.; Kikuchi, T.; Stott, C.; Riedel, G. MK-801-induced deficits in social recognition in rats. Behav. Pharmacol., 2015, 26(8), 748-765.
[http://dx.doi.org/10.1097/FBP.0000000000000178] [PMID: 26287433]
[29]
Perdikaris, P.; Dermon, C.R. Behavioral and neurochemical profile of MK-801 adult zebrafish model: Forebrain β2-adrenoceptors contribute to social withdrawal and anxiety-like behavior. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2022, 115, 110494.
[http://dx.doi.org/10.1016/j.pnpbp.2021.110494] [PMID: 34896197]
[30]
Benturquia, N.; Le Guen, S.; Canestrelli, C.; Lagente, V.; Apiou, G.; Roques, B.P.; Noble, F. Specific blockade of morphine- and cocaine-induced reinforcing effects in conditioned place preference by nitrous oxide in mice. Neuroscience, 2007, 149(3), 477-486.
[http://dx.doi.org/10.1016/j.neuroscience.2007.08.003] [PMID: 17905521]
[31]
Sekiya, Y.; Nakagawa, T.; Ozawa, T.; Minami, M.; Satoh, M. Facilitation of morphine withdrawal symptoms and morphine-induced conditioned place preference by a glutamate transporter inhibitor dl-threo-β-benzyloxyaspartate in rats. Eur. J. Pharmacol., 2004, 485(1-3), 201-210.
[http://dx.doi.org/10.1016/j.ejphar.2003.11.062] [PMID: 14757142]
[32]
Anderson, E.M.; Valle-Pinero, A.Y.D.; Suckow, S.K.; Nolan, T.A.; Neubert, J.K.; Caudle, R.M. Morphine and MK-801 administration leads to alternative NMDAR1 splicing and associated changes in reward seeking behavior and nociception on an operant orofacial assay. Neuroscience, 2012, 214, 14.
[http://dx.doi.org/10.1016/j.neuroscience.2012.04.032] [PMID: 22531378]
[33]
Al-Hasani, R.; Bruchas, M.R. Molecular mechanisms of opioid receptor-dependent signaling and behavior. Anesthesiology, 2011, 115(6), 1363-1381.
[http://dx.doi.org/10.1097/ALN.0b013e318238bba6] [PMID: 22020140]
[34]
Rusin, K.I. Giovannucci, D.R.; Stuenkel, E.L.; Moises, H.C. κ-opioid receptor activation modulates Ca2+ currents and secretion in isolated neuroendocrine nerve terminals. J. Neurosci., 1997, 17(17), 6565-6574.
[http://dx.doi.org/10.1523/JNEUROSCI.17-17-06565.1997] [PMID: 9254669]
[35]
Zamponi, G.W.; Snutch, T.P. Modulation of voltage-dependent calcium channels by G proteins. Curr. Opin. Neurobiol., 1998, 8(3), 351-356.
[http://dx.doi.org/10.1016/S0959-4388(98)80060-3] [PMID: 9687363]
[36]
Zamponi, G.W.; Snutch, T.P. Modulating modulation: Crosstalk between regulatory pathways of presynaptic calcium channels. Mol. Interv., 2002, 2(8), 476-478.
[http://dx.doi.org/10.1124/mi.2.8.476] [PMID: 14993397]