A Nonrewarding NMDA Receptor Antagonist Impairs the Acquisition, Consolidation, and Expression of Morphine Conditioned Place Preference in Mice

Molecular Neurobiology

Volumn 54, Issue 1, 2017, Pages 710-721

  Tomazi, Lediane ^a   Mello, Carlos Fernando ^a   Schöffer, Ana Paula ^a   Girardi, Bruna Amanda ^a   Frühauf, Pâmella Karina Santana ^a   Rubin, Maribel Antonello ^a  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

Author keywords

Addiction; Arcaine; Conditioned place preference; Morphine; Spermidine

Indexed keywords

ARCAINE; MORPHINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SPERMIDINE; AMINO ACID RECEPTOR BLOCKING AGENT; NARCOTIC ANALGESIC AGENT;

ADULT; ANIMAL EXPERIMENT; ARTICLE; AVERSION; BINDING SITE; CONDITIONING; CONTROLLED STUDY; MALE; MOUSE; NONHUMAN; PLACE PREFERENCE; REWARD; ANIMAL; ANTAGONISTS AND INHIBITORS; CONDITIONED REFLEX; DOSE RESPONSE; DRUG EFFECTS; LOCOMOTION; PHYSIOLOGY;

ANALGESICS, OPIOID; ANIMALS; CONDITIONING, CLASSICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; LOCOMOTION; MALE; MICE; MORPHINE; RECEPTORS, N-METHYL-D-ASPARTATE; REWARD;

EID: 84954321696     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9678-0     Document Type: Article

References (105)

1. Koob GF (1998) Circuits, drugs, and drug addiction. Adv Pharmacol 42:978–982
2. Suzuki T, Yoshiike M, Mizoguchi H, Kamei J, Misawa M, Nagase H (1994) Blockade of delta-opioid receptors prevents morphine-induced place preference in mice. Jpn J Pharmacol 66:131–137
3. Suzuki T, Kato H, Tsuda M, Suzuki H, Misawa M (1999) Effects of the non-competitive NMDA receptor antagonist ifenprodil on the morphine-induced place preference in mice. Life Sci 64:151–156
4. Leshner AI, Koob GF (1999) Drugs of abuse and the brain. Proc Assoc Am Physicians 111:99–108
5. Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462
6. Ribeiro Do Couto B, Aguilar MA, Rodriguez-Arias M, Minarro J (2005) Long-lasting rewarding effects of morphine induced by drug primings. Brain Res 1050:53–63
7. Lin J, Liu L, Wen Q, Zheng C, Gao Y, Peng S, Tan Y, Li Y (2014) Rapamycin prevents drug seeking via disrupting reconsolidation of reward memory in rats. Int J Neuropsychopharmacol 17:127–136
8. Liu SB, Ma L, Guo HJ, Feng B, Guo YY, Li XQ, Sun WJ, Zheng LH, Zhao MG (2012) Gentiopicroside attenuates morphine rewarding effect through downregulation of GluN2B receptors in nucleus accumbens. CNS Neurosci Ther 18:652–658
9. Wise RA (1988) The neurobiology of craving: implications for the understanding and treatment of addiction. J Abnorm Psychol 97:118–132
10. Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24:97–129
11. Narita M, Matsushima Y, Niikura K, Takagi S, Nakahara K, Kurahashi K, Abe M, Saeki M, Asato M, Imai S, Ikeda K, Kuzumaki N, Suzuki T (2010) Implication of dopaminergic projection from the ventral tegmental area to the anterior cingulate cortex in mu-opioid-induced place preference. Addict Biol 15:434–447
12. Hnasko TS, Sotak BN, Palmiter RD (2005) Morphine reward in dopamine-deficient mice. Nature 438:854–857
13. Leone P, Pocock D, Wise RA (1991) Morphine-dopamine interaction: ventral tegmental morphine increases nucleus accumbens dopamine release. Pharmacol Biochem Behav 39:469–472
14. Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483–488
15. Zarrindast MR, Rezayof A, Sahraei H, Haeri-Rohani A, Rassouli Y (2003) Involvement of dopamine D1 receptors of the central amygdala on the acquisition and expression of morphine-induced place preference in rat. Brain Res 965:212–221
16. Rezayof A, Golhasani-Keshtan F, Haeri-Rohani A, Zarrindast MR (2007) Morphine-induced place preference: involvement of the central amygdala NMDA receptors. Brain Res 1133:34–41
17. Zarrindast MR, Jafari-Sabet M, Rezayat M, Djahanguiri B, Rezayof A (2006) Involvement of NMDA receptors in morphine state-dependent learning in mice. Intl J Neurosci 116:731–743
18. Nestler EJ (1996) Under siege: the brain on opiates. Neuron 16:897–900
19. Tzschentke TM, Schmidt WJ (2003) Glutamatergic mechanisms in addiction. Mol Psychiatry 8:373–382
20. Mazei-Robison MS, Nestler EJ (2012) Opiate-induced molecular and cellular plasticity of ventral tegmental area and locus coeruleus catecholamine neurons. Cold Spring Harb Perspect Med 2:a012070
21. Fields HL, Margolis EB (2015) Understanding opioid reward. Trends Neurosci 38:217–225
22. Jalabert M, Bourdy R, Courtin J, Veinante P, Manzoni OJ, Barrot M, Georges F (2011) Neuronal circuits underlying acute morphine action on dopamine neurons. Proc Natl Acad Sci U S A 108:16446–16450
23. Xi ZX, Stein EA (2002) GABAergic mechanisms of opiate reinforcement. Alcohol Alcohol 37:485–494
24. Danysz W, Kozela E, Parsons CG, Sladek M, Bauer T, Popik P (2005) Peripherally acting NMDA receptor/glycineB site receptor antagonists inhibit morphine tolerance. Neuropharmacology 48:360–371
25. Makarska-Bialek K, Kaminski RM, Czuczwar SJ (2005) Influence of the antagonist of the glycine site of NMDA receptors, MRZ 2/576, on the anticonvulsant activity of conventional antiepileptic drugs in mice. Pharmacol Rep 57:458–466
26. Backstrom P, Hyytia P (2006) Ionotropic and metabotropic glutamate receptor antagonism attenuates cue-induced cocaine seeking. Neuropsychopharmacology 31:778–786
27. Del Pozo E, Barrios M, Baeyens JM (1996) The NMDA receptor antagonist dizocilpine (MK-801) stereoselectively inhibits morphine-induced place preference conditioning in mice. Psychopharmacology 125:209–213
28. Huang EY, Liu TC, Tao PL (2003) Co-administration of dextromethorphan with morphine attenuates morphine rewarding effect and related dopamine releases at the nucleus accumbens. Naunyn Schmiedeberg’s Arch Pharmacol 368:386–392
29. Lue WM, Huang EY, Yang SN, Wong CS, Tao PL (2007) Post-treatment of dextromethorphan reverses morphine effect on conditioned place preference in rats. Synapse 61:420–428
30. Tzschentke TM, Schmidt WJ (1995) N-methyl-d-aspartic acid-receptor antagonists block morphine-induced conditioned place preference in rats. Neurosci Lett 193:37–40
31. Narita M, Aoki T, Suzuki T (2001) Mechanisms of morphine-induced rewarding effect: involvement of NMDA receptor subunits. Nihon Yakurigaku Zasshi 117:13–19
32. Ma YY, Guo CY, Yu P, Lee DY, Han JS, Cui CL (2006) The role of NR2B containing NMDA receptor in place preference conditioned with morphine and natural reinforcers in rats. Exp Neurol 200:343–355
33. 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 203:309–319
34. Chen SL, Hsu KY, Huang EY, Lu RB, Tao PL (2011) Low doses of dextromethorphan attenuate morphine-induced rewarding via the sigma-1 receptor at ventral tegmental area in rats. Drug Alcohol Depend 117:164–169
35. Hu L, Jing XH, Cui CL, Xing GG, Zhu B (2012) NMDA receptors in the midbrain play a critical role in dopamine-mediated hippocampal synaptic potentiation caused by morphine. Addict Biol 19:380–391
36. Balster RL (1987) Abuse potential evaluation of inhalants. Drug Alcohol Depend 19:7–15
37. Koek W, Woods JH, Winger GD (1988) MK-801, a proposed noncompetitive antagonist of excitatory amino acid neurotransmission, produces phencyclidine-like behavioral effects in pigeons, rats and rhesus monkeys. J Pharmacol Exp Ther 245:969–974
38. Willetts J, Balster RL, Leander JD (1990) The behavioral pharmacology of NMDA receptor antagonists. Trends Pharmacol Sci 11:423–428
39. Grotta J, Clark W, Coull B, Pettigrew LC, Mackay B, Goldstein LB, Meissner I, Murphy D, LaRue L (1995) Safety and tolerability of the glutamate antagonist CGS 19755 (Selfotel) in patients with acute ischemic stroke. Results of a phase IIa randomized trial. Stroke 26:602–605
40. Sveinbjornsdottir S, Sander JW, Upton D, Thompson PJ, Patsalos PN, Hirt D, Emre M, Lowe D, Duncan JS (1993) The excitatory amino acid antagonist D-CPP-ene (SDZ EAA-494) in patients with epilepsy. Epilepsy Res 16:165–174
41. Papp M, Moryl E, Maccecchini ML (1996) Differential effects of agents acting at various sites of the NMDA receptor complex in a place preference conditioning model. Eur J Pharmacol 317:191–196
42. Tzschentke TM (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56:613–672
43. Suzuki T, Kato H, Aoki T, Tsuda M, Narita M, Misawa M (2000) Effects of the non-competitive NMDA receptor antagonist ketamine on morphine-induced place preference in mice. Life Sci 67:383–389
44. Marglin SH, Milano WC, Mattie ME, Reid LD (1989) PCP and conditioned place preferences. Pharmacol Biochem Behav 33:281–283
45. Noda Y, Nabeshima T (2004) Involvement of signal transduction cascade via dopamine-D1 receptors in phencyclidine dependence. Ann N Y Acad Sci 1025:62–68
46. Shin EJ, Nah SY, Kim WK, Ko KH, Jhoo WK, Lim YK, Cha JY, Chen CF, Kim HC (2005) The dextromethorphan analog dimemorfan attenuates kainate-induced seizures via sigma1 receptor activation: comparison with the effects of dextromethorphan. Br J Pharmacol 144:908–918
47. Domino EF (2010) Taming the ketamine tiger. 1965. Anesthesiology 113:678–684
48. Miller SC (2011) Dextromethorphan to dextrorphan: a pathway towards abuse liability. Hum Psychopharmacol 26:89–90
49. Mony L, Zhu S, Carvalho S, Paoletti P (2011) Molecular basis of positive allosteric modulation of GluN2B NMDA receptors by polyamines. EMBO J 30:3134–3146
50. Mariani RK, Mello CF, Rosa MM, Ceretta AP, Camera K, Rubin MA (2011) Effect of naloxone and morphine on arcaine-induced state-dependent memory in rats. Psychopharmacology 215:483–491
51. Panos JJ, Rademacher DJ, Renner SL, Steinpreis RE (1999) The rewarding properties of NMDA and MK-801 (dizocilpine) as indexed by the conditioned place preference paradigm. Pharmacol Biochem Behav 64:591–595
52. Zarrindast MR, Lashgari R, Rezayof A, Motamedi F, Nazari-Serenjeh F (2007) NMDA receptors of dorsal hippocampus are involved in the acquisition, but not in the expression of morphine-induced place preference. Eur J Pharmacol 568:192–198
53. Tzschentke TM, Schmidt WJ (1997) Interactions of MK-801 and GYKI 52466 with morphine and amphetamine in place preference conditioning and behavioural sensitization. Behav Brain Res 84:99–107
54. Fukushiro DF, Alvarez Jdo N, Tatsu JA, de Castro JP, Chinen CC, Frussa-Filho R (2007) Haloperidol (but not ziprasidone) withdrawal enhances cocaine-induced locomotor activation and conditioned place preference in mice. Prog Neuropsychopharmacol Biol Psychiatry 31:867–872
55. Tahsili-Fahadan P, Yahyavi-Firouz-Abadi N, Khoshnoodi MA, Motiei-Langroudi R, Tahaei SA, Ghahremani MH, Dehpour AR (2006) Agmatine potentiates morphine-induced conditioned place preference in mice: modulation by alpha2-adrenoceptors. Neuropsychopharmacology 31:1722–1732
56. Signor C, Mello CF, Porto GP, Ribeiro DA, Rubin MA (2014) Spermidine improves fear memory persistence. Eur J Pharmacol 730:72–76
57. Ribeiro DA, Mello CF, Signor C, Rubin MA (2013) Polyaminergic agents modulate the reconsolidation of conditioned fear. Neurobiol Lear Mem 104C:9–15
58. Tabaeizadeh M, Motiei-Langroudi R, Mirbaha H, Esmaeili B, Tahsili-Fahadan P, Javadi-Paydar M, Ghaffarpour M, Dehpour AR (2013) The differential effects of OX1R and OX2R selective antagonists on morphine conditioned place preference in naive versus morphine-dependent mice. Behav Brain Res 237:41–48
59. Kao JH, Huang EY, Tao PL (2011) NR2B subunit of NMDA receptor at nucleus accumbens is involved in morphine rewarding effect by siRNA study. Drug Alcohol Depend 118:366–374
60. Bardo MT, Miller JS, Neisewander JL (1984) Conditioned place preference with morphine: the effect of extinction training on the reinforcing CR. Pharmacol Biochem Behav 21:545–549
61. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565–598
62. Kalivas PW (1993) Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Brain Res Rev 18:75–113
63. van Ree JM, Gerrits MA, Vanderschuren LJ (1999) Opioids, reward and addiction: an encounter of biology, psychology, and medicine. Pharmacol Rev 51:341–396
64. Papp M, Gruca P, Willner P (2002) Selective blockade of drug-induced place preference conditioning by ACPC, a functional NDMA-receptor antagonist. Neuropsychopharmacology 27:727–743
65. Bisaga A, Popik P (2000) In search of a new pharmacological treatment for drug and alcohol addiction: N-methyl-d-aspartate (NMDA) antagonists. Drug Alcohol Depend 59:1–15
66. Kim HS, Jang CG, Park WK (1996) Inhibition by MK-801 of morphine-induced conditioned place preference and postsynaptic dopamine receptor supersensitivity in mice. Pharmacol Biochem Behav 55:11–17
67. Yonghui L, Xigeng Z, Yunjing B, Xiaoyan Y, Nan S (2006) Opposite effects of MK-801 on the expression of food and morphine-induced conditioned place preference in rats. J Psychopharmacol 20:40–46
68. Li F, Wang XS, Dai RP, Zhang JY, Zhou XF, Hao W, Li CQ (2011) The activation of NMDA receptor-ERK pathway in the central amygdala is required for the expression of morphine-conditioned place preference in the rat. Neurotox Res 20:362–371
69. Fan Y, Niu H, Rizak JD, Li L, Wang G, Xu L, Ren H, Lei H, Yu H (2012) Combined action of MK-801 and ceftriaxone impairs the acquisition and reinstatement of morphine-induced conditioned place preference, and delays morphine extinction in rats. Neurosci Bull 28:567–576
70. Popik P, Danysz W (1997) Inhibition of reinforcing effects of morphine and motivational aspects of naloxone-precipitated opioid withdrawal by N-methyl-d-aspartate receptor antagonist, memantine. Behav Pharmacol 14:237–244
71. Popik P, Wrobel M, Rygula R, Bisaga A, Bespalov AY (2003) Effects of memantine, an NMDA receptor antagonist, on place preference conditioned with drug and nondrug reinforcers in mice. Behav Pharmacol 14:237–244
72. Ribeiro Do Couto B, Aguilar MA, Manzanedo C, Rodriguez-Arias M, Minarro J (2004) Effects of NMDA receptor antagonists (MK-801 and memantine) on the acquisition of morphine-induced conditioned place preference in mice. Prog Neuropsychopharmacol Biol Psychiatry 28:1035–1043
73. Gao C, Che LW, Chen J, Xu XJ, Chi ZQ (2003) Ohmefentanyl stereoisomers induce changes of CREB phosphorylation in hippocampus of mice in conditioned place preference paradigm. Cell Res 13:29–34
74. Ma YY, Yu P, Guo CY, Cui CL (2011) Effects of ifenprodil on morphine-induced conditioned place preference and spatial learning and memory in rats. Neurochem Res 36:383–391
75. Popik P, Kolasiewicz W (1999) Mesolimbic NMDA receptors are implicated in the expression of conditioned morphine reward. Naunyn Schmiedeberg’s Arch Pharmacol 359:288–294
76. Harris GC, Wimmer M, Byrne R, Aston-Jones G (2004) Glutamate-associated plasticity in the ventral tegmental area is necessary for conditioning environmental stimuli with morphine. Neuroscience 129:841–847
77. Wei XL, Su RB, Lu XQ, Liu Y, Yu SZ, Yuan BL, Li J (2005) Inhibition by agmatine on morphine-induced conditioned place preference in rats. Eur J Pharmacol 515:99–106
78. Zhu Y, King MA, Schuller AG, Nitsche JF, Reidl M, Elde RP, Unterwald E, Pasternak GW, Pintar JE (1999) Retention of supraspinal delta-like analgesia and loss of morphine tolerance in delta opioid receptor knockout mice. Neuron 24:243–252
79. Zhu H, Ho IK (1998) NMDA-R1 antisense oligonucleotide attenuates withdrawal signs from morphine. Eur J Pharmacol 352:151–156
80. Paoletti P (2011) Molecular basis of NMDA receptor functional diversity. Eur J Neurosci 33:1351–1365
81. Mori H, Mishina M (1995) Structure and function of the NMDA receptor channel. Neuropharmacology 34:1219–1237
82. Miyamoto H, Rahman MM, Chang C (2004) Molecular basis for the antiandrogen withdrawal syndrome. J Cel Biochem 91:3–12
83. Inoue M, Mishina M, Ueda H (2003) Locus-specific rescue of GluRepsilon1 NMDA receptors in mutant mice identifies the brain regions important for morphine tolerance and dependence. J Neurosci 23:6529–6536
84. Narita M, Aoki T, Suzuki T (2000) Molecular evidence for the involvement of NR2B subunit containing N-methyl-d-aspartate receptors in the development of morphine-induced place preference. Neuroscience 101:601–606
85. Rubin MA, Berlese DB, Stiegemeier JA, Volkweis MA, Oliveira DM, dos Santos TL, Fenili AC, Mello CF (2004) Intra-amygdala administration of polyamines modulates fear conditioning in rats. J Neurosci 24:2328–2334
86. Ceretta AP, Camera K, Mello CF, Rubin MA (2008) Arcaine and MK-801 make recall state-dependent in rats. Psychopharmacology 201:405–411
87. Rubin MA, Stiegemeier JA, Volkweis MA, Oliveira DM, Fenili AC, Boemo RL, Jurach A, Mello CF (2001) Intra-amygdala spermidine administration improves inhibitory avoidance performance in rats. Eur J Pharmacol 423:35–39
88. Camera K, Mello CF, Ceretta AP, Rubin MA (2007) Systemic administration of polyaminergic agents modulate fear conditioning in rats. Psychopharmacology 192:457–464
89. Berlese DB, Sauzem PD, Carati MC, Guerra GP, Stiegemeier JA, Mello CF, Rubin MA (2005) Time-dependent modulation of inhibitory avoidance memory by spermidine in rats. Neurobiol Learn Mem 83:48–53
90. da Rosa MM, Mello CF, Camera K, Ceretta AP, Ribeiro DA, Signor C, Rubin MA (2012) Opioid mechanisms are involved in the disruption of arcaine-induced amnesia by context pre-exposure. Neurobiol Learn Mem 97:294–300
91. Popik P, Mamczarz J, Fraczek M, Widla M, Hesselink M, Danysz W (1998) Inhibition of reinforcing effects of morphine and naloxone-precipitated opioid withdrawal by novel glycine site and uncompetitive NMDA receptor antagonists. Neuropharmacology 37:1033–1042
92. Kolesnikov YA, Pick CG, Ciszewska G, Pasternak GW (1993) Blockade of tolerance to morphine but not to kappa opioids by a nitric oxide synthase inhibitor. Proc Natl Acad Sci U S A 90:5162–5166
93. Moron JA, Gullapalli S, Taylor C, Gupta A, Gomes I, Devi LA (2010) Modulation of opiate-related signaling molecules in morphine-dependent conditioned behavior: conditioned place preference to morphine induces CREB phosphorylation. Neuropsychopharmacology 35:955–966
94. Huang MJ, Regunathan S, Botta M, Lee K, McClendon E, Yi GB, Pedersen ML, Berkowitz DB, Wang G, Travagli M, Piletz JE (2003) Structure-activity analysis of guanidine group in agmatine for brain agmatinase. Ann NY Acad Sci 1009:52–63
95. Bernstein HG, Derst C, Stich C, Pruss H, Peters D, Krauss M, Bogerts B, Veh RW, Laube G (2011) The agmatine-degrading enzyme agmatinase: a key to agmatine signaling in rat and human brain? Amino Acids 40:453–465
96. Shen F, Li YJ, Shou XJ, Cui CL (2012) Role of the NO/sGC/PKG signaling pathway of hippocampal CA1 in morphine-induced reward memory. Neurobiol Learn Mem 98:130–138
97. Shen F, Wang N, Qi C, Li YJ, Cui CL (2014) The NO/sGC/PKG signaling pathway in the NAc shell is necessary for the acquisition of morphine-induced place preference. Behav Neurosci 128:446–459
98. Gholami A, Haeri-Rohani A, Sahraie H, Zarrindast MR (2002) Nitric oxide mediation of morphine-induced place preference in the nucleus accumbens of rat. Eur J Pharmacol 449:269–277
99. Gholami A, Zarrindast MR, Sahraei H, Haerri-Rohani A (2003) Nitric oxide within the ventral tegmental area is involved in mediating morphine reward. Eur J Pharmacol 458:119–128
100. Kiyani A, Javadi-Paydar M, Mohammadkhani H, Esmaeili B, Dehpour AR (2011) Lithium chloride disrupts consolidation of morphine-induced conditioned place preference in male mice: the nitric oxide/cyclic GMP signaling pathway. Behav Brain Res 219:240–247
101. Manzanedo C, Aguilar MA, Do Couto BR, Rodriguez-Arias M, Minarro J (2009) Involvement of nitric oxide synthesis in sensitization to the rewarding effects of morphine. Neurosci Lett 464:67–70
102. Manzanedo C, Aguilar MA, Rodriguez-Arias M, Navarro M, Minarro J (2004) 7-Nitroindazole blocks conditioned place preference but not hyperactivity induced by morphine. Behav Brain Res 150:73–82
103. Sahraei H, Zarei F, Eidi A, Oryan S, Shams J, Khoshbaten A, Zarrindast MR (2007) The role of nitric oxide within the nucleus accumbens on the acquisition and expression of morphine-induced place preference in morphine sensitized rats. Eur J Pharmacol 556:99–106
104. Ma P, Liu H, Li H, Huang X, Chen L, Zhai H (2014) Involvement of the insular nitric oxide signaling pathway in the expression of morphine-induced conditioned place preference in rats. Neuroreport 25:641–646
105. Cadet JL (2014) Epigenetics of stress, addiction, and resilience: therapeutic implications. Mol Neurobiol. doi:10.1007/s12035-014-9040-y