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Interaction Between Central Opioidergic and Glutamatergic Systems on Food Intake in Neonatal Chicks: Role of NMDA, AMPA and mGLU1 Receptors

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Abstract

The present study was designed to examine the role of opioidergic and glutamatergic systems on feeding behavior in neonatal meat-type chicken. In experiment 1, FD3 neonatal broilers ICV injected with (A) saline, (B) DAMGO (µ-opioid receptor agonist, 125 pmol), (C) MK-801 (NMDA glutamate receptors antagonist, 15 nmol) and (D) combination of DAMGO plus MK-801. Experiments 2–5 were similar to experiment 1, except FD3 chicks ICV injected with CNQX (AMPA glutamate receptors antagonist, 390 nmol), AIDA (mGLU1 receptors antagonist, 2 nmol), LY341495 (mGLU2 receptors antagonist, 150 nmol) and UBP1112 (mGLU3 receptors antagonist, 2 nmol) instead of MK-801, respectively. In experiments 6–10, FD3 chicks ICV injected as the same as procedure to the experiments 1–5, except to inject with DPDPE (δ-opioid receptor agonist, 40 nmol) instead of the DAMGO. The experiments 11–15 were similar to the experiments 1–5, except neonatal broilers ICV injected with U-50488H (κ-opioid receptor agonist, 30 nmol) instead of DAMGO. Then the cumulative food intake measured until 120 min post injection. According to the results, ICV injection of DAMGO, significantly decreased food intake (P < 0.05) while DPDPE and U-50488H increased feeding behavior compared to the control group (P < 0.05). Co-injection of the DAMGO + MK-801 and DAMGO + AIDA, significantly decreased DAMGO-induced hypophagia in neonatal chicks (P < 0.05). Also, co-injection of the DPDPE + CNQX significantly amplified DPDPE induced feeding behavior (P < 0.05). These results suggested interconnection between central opioidergic and glutamatergic systems on feeding behavior mediates via µ- and δ-opioid receptor with NMDA, AMPA and mGLU1 receptors in FD3 neonatal broilers. These findings may shed light on the circuitry underlying interconnection between central opioidergic and glutamatergic systems on feeding behavior.

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References

  • Alimohammadi S, Zendehdel M, Babapour V (2015) Modulation of opioid-induced feeding behavior by endogenous nitric oxide in neonatal layer-type chicks. Vet Res Commun 39:105–113

    Article  PubMed  Google Scholar 

  • Baghbanzadeh A, Babapour V (2007) Glutamate ionotropic and metabotropic receptors affect feed intake in broiler cockerels. J Vet Res 62(4):125–129

    Google Scholar 

  • Beckerman MA, Glass MJ (2011) Ultrastructural relationship between the AMPA-GluR2 receptor subunit and the mu-opioid receptor in the mouse central nucleus of the amygdala. Exp Neurol 227(1):149–158

    Article  CAS  PubMed  Google Scholar 

  • Blevins JE, Stanley BG, Reidelberger RD (2002) DMSO as a vehicle for central injections: tests with feeding elicited by norepinephrine injected into the paraventricular nucleus. Pharmacol Biochem Behav 71:277–282

    Article  CAS  PubMed  Google Scholar 

  • Branch SY, Goertz RB, Sharpe AL, Pierce J, Roy S, Ko D, Paladini CA, Beckstead MJ (2013) Food Restriction Increases Glutamate receptor-mediated burst firing of dopamine neurons. J Neurosci 33(34):13861–13872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bungo T, Kawamura K, Izumi T, Dodo K, Ueda H (2004) Feeding responses to µ-, δ- and κ-opioid receptor agonists in the meat-type chick. Pharmacol Biochem Behav 78: 707–710

    Article  CAS  PubMed  Google Scholar 

  • Bungo T, Kawamura K, Izumi T, Dodo K, Ueda H (2005) Effects of various µ-, δ- and κ-opioid ligands on food intake in the meat-type chick. Physiol Behav 85:519–523

    Article  CAS  PubMed  Google Scholar 

  • Charles JR, Duva MA, Ramirez GJ, Lara RL, Yang CR, Stanley BG (2014) Activation of lateral hypothalamic mGlu1 and mGlu5 receptors elicits feeding in rats. Neuropharmacology 79:59–65

    Article  CAS  PubMed  Google Scholar 

  • Da Silva AA, Marino-Neto J, MA P (2003) Feeding induced by microinjections of NMDA and AMPA–kainite receptor antagonists into ventral striatal and ventral pallidal areas of the pigeon. Brain Res 966:76–83

    Article  CAS  PubMed  Google Scholar 

  • Davis JL, Masuoka DT, Gerbrandt LK, Cherkin A (1979) Autoradiographic distribution of l-proline in chicks after intracerebral injection. Physiol Behav 22:693–695

    Article  CAS  PubMed  Google Scholar 

  • Denbow DM (1994) Peripheral regulation of food intake in poultry. J Nutr 124:1349S–1354S

    Article  CAS  PubMed  Google Scholar 

  • Farahmandfar M, Karimian SM, Zarrindast MR, Kadivar M, Afrouzi H, Naghdi N (2011) Morphine sensitization increases the extracellular level of glutamate in CA1 of rat hippocampus via µ-opioid receptor. Neurosci Lett 494: 130–134

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, He X, Yang Y, Chao D, Lazarus LH, Xia Y (2012) Current research on opioid receptor function. Curr Drug Target 13(2):230–246

    Article  CAS  Google Scholar 

  • Filizola M, Devi LA (2013) Grand opening of structure-guided design for novel opioids. Trends Pharmacol Sci 34(1):6–12

    Article  CAS  PubMed  Google Scholar 

  • Furuse M (2002) Central regulation of food intake in the neonatal chick. Anim Sci J 73:83–94

    Article  CAS  Google Scholar 

  • Furuse M, Matsumoto M, Saito N, Sugahara K, Hasegawa S (1997) The central corticotropin-releasing factor and glucagon-like peptide-1 in food intake of the neonatal chick. Eur J Pharmacol 339:211–214

    Article  CAS  PubMed  Google Scholar 

  • Furuse M, Ando R, Bungo T, Ao R, ShimoJO M, Masuda Y (1999) Intracerebroventricular injection of orexins does not stimulate food intake in neonatal chicks. Br Poult Sci 40:698–700

    Article  CAS  PubMed  Google Scholar 

  • Garzón J, Rodríguez-Muñoz M, Sánchez-Blázquez P (2012) Direct association of mu-opioid and NMDA glutamate receptors supports their cross-regulation: molecular implications for opioid tolerance. Curr Drug Abuse Rev 5:199–226

    Article  PubMed  Google Scholar 

  • Glass MJ, Lane DA, Colago EE, Chan J, Schlussman SD, Zhou Y, Kreek MJ, Pickel VM (2008) Chronic administration of morphine is associated with a decrease in surface AMPA GluR1 receptor subunit in dopamine D1 receptor expressing neurons in the shell and non-D1 receptor expressing neurons in the core of the rat nucleus accumbens. Exp Neurol 210:750–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo M, Xu NJ, Li YT, Yang JY, Wu CF, Pei G (2005) Morphine modulates glutamate release in the hippocampal CA1 area in mice. Neurosci Lett 381: 12–15

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Wang HL, Xiang XH, Zhao Y (2009) The role of glutamate and its receptors in mesocorticolimbic dopaminergic regions in opioid addiction. Neurosci Biobehav Rev 33:864–873

    Article  CAS  PubMed  Google Scholar 

  • Hao Y, Yang JY, Wu CF, Wu MF (2007) Pseudoginsenoside-F11 decreases morphine-induced behavioral sensitization and extracellular glutamate levels in the medial prefrontal cortex in mice. Pharmacol Biochem Behav 86:660–666

    Article  CAS  PubMed  Google Scholar 

  • Hettes SR, GonzagaWJ, Heyming TW, Nguyen JK, Perez S, Stanley BG (2010) Stimulation of lateral hypothalamic AMPA receptors may induce feeding in rats. Brain Res 1346:112–120

    Article  CAS  PubMed  Google Scholar 

  • Kamali M, Sahraei H, Khosravi M, Hassanpour S, Yaribeygi H (2016) Asymmetric involvement of central and the peripheral NMDA glutamate receptors in the expression of withdrawal syndrome in morphine-dependent mice. Physiol Pharmacol 19: 274–284

    Google Scholar 

  • Kaneko K, Yoshikawa M, Ohinata K (2012) Novel orexigenic pathway prostaglandin D2-NPY system-involvement in orally active orexigenic δ opioid peptide. Neuropeptides 46:353–357

    Article  CAS  PubMed  Google Scholar 

  • Ladepeche L, Yang L, Bouchet D, Groc L (2013) Regulation of dopamine D1 receptor dynamics within the postsynaptic density of hippocampal glutamate synapses. PLoS ONE 8(9):e74512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Merrer J, Becker JAJ, Befort K, Kieffer BL (2009) Reward processing by the opioid system in the brain. Physiol Rev 89:1379–1412

    Article  CAS  PubMed  Google Scholar 

  • Lee CWS, Ho IK (2013) Pharmacological profiles of oligomerized μ-opioid receptors. Cells 2, 689–714. doi:10.3390/cells2040689

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu XJ, Salter MW (2010) Glutamate receptor phosphorylation and trafficking in pain plasticity in spinal cord dorsal horn. Eur J Neurosci 32:278–289

    Article  PubMed  PubMed Central  Google Scholar 

  • McFadden KL, Cornier MA, Tregellas JR (2014) The role of alpha-7 nicotinic receptors in food intake behaviors. Frontiers In Psychol 5(553):1–7

    Google Scholar 

  • Mena JD, Selleck RA, Baldo BA (2013) Mu-opioid stimulation in rat prefrontal cortex engages hypothalamic orexin/hypocretin-containing neurons, and reveals dissociable roles of nucleus accumbens and hypothalamus in cortically driven feeding. J Neurosci 33(47):18540–18552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minowa S, Ishihara S, Tsuchiya S, Horie S, Watanabe K, Murayama T (2003) Involvement of glutamate and c-amino-butyric acid receptor systems on gastric acid secretion induced by activation of κ-opioid receptors in the central nervous system in rats. Br J Pharmacol 138:1049–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitrano DA, Arnold C, Smith Y (2008) Subcellular and subsynaptic localization of group I metabotropic glutamate receptors in the nucleus accumbens of cocainetreated rats. Neurosci 154: 653–666

    Article  CAS  Google Scholar 

  • Novoseletsky N, Nussinovitch A, Friedman-Einat M (2011) Attenuation of food intake in chicks by an inverse agonist of cannabinoid receptor1 administered by either injection or ingestion in hydrocolloid carriers. Gen Comp Endocrinol 170:522–527

    Article  CAS  PubMed  Google Scholar 

  • Olanrewaju HA, Thaxton JP, Dozier WA, Purswell J, Roush WB, Branton SL (2006) A review of lighting programs for broiler production. Int J Poult Sci 5(4):301–308

    Article  Google Scholar 

  • Qi W, Ding D, Salvi RJ (2008) Cytotoxic effects of dimethyl sulphoxide (DMSO) on cochlear organotypic cultures. Hear Res 236:52–60

    Article  CAS  PubMed  Google Scholar 

  • Saito ES, Kaiya H, Tachibana T, Tomonaga S, Denbow DM, Kangawa K, Furuse M (2005) Inhibitory effect of ghrelin on food intake is mediated by the corticotropin-releasing factor system in neonatal chicks. Regul Pept 125:201–208

    Article  CAS  PubMed  Google Scholar 

  • Scavone JL, Asan E, Van Bockstaele EJ (2011) Unraveling glutamate-opioid receptor interactions using highresolution electron microscopy: implications for addictionrelated processes. Exp Neurol 229(2):207–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schotanus SM, Chergui K (2008) Dopamine D1 receptors and group I metabotropic glutamate receptors contribute to the induction of long-term potentiation in the nucleus accumbens. Neuropharmacol 54: 837–844

    Article  CAS  Google Scholar 

  • Sepehrizadeh Z, Bahrololoumi Shapourabadi M, Ahmadi S, Bozchlou Hashemi S, Zarrindast MR, Sahebgharani M (2008a) Decreased AMPA GluR2, but not GluR3, mRNA expression in rat amygdala and dorsal hippocampus following morphine-induced behavioural sensitization. Clin Exp Pharmacol Physiol 35:1321–1330

    Article  CAS  PubMed  Google Scholar 

  • Sepehrizadeh Z, Sahebgharani M, Ahmadi S, Shapourabadi MB, Bozchlou Hashemi S, Zarrindast MR (2008b) Morphine-induced behavioral sensitization increased the mRNA expression of NMDA receptor subunits in the rat amygdala. Pharmacol 81:333–343

    Article  CAS  Google Scholar 

  • Shojaei M, Zendehdel M, Babapour V, Charkhkar S, Hassanpour S (2015) Opioid-induced hypophagia is mediated by 5-HT2c receptors in neonatal layer-type chicken. Czech J Anim Sci 60(9):400–410

    Article  Google Scholar 

  • Steinman JL, Fujikawa DG, Wasterlain CG, Cherkin A, Morley JE (1987) The effects of adrenergic, opioid and pancreatic polypeptidergic compounds on feeding and other behaviors in neonatal leghorn chicks. Peptides 8: 585–592

    Article  CAS  PubMed  Google Scholar 

  • Taati M, Nayebzadeh H, Zendehdel M (2011) The effects of DLAP5 and glutamate on ghrelin-induced feeding behavior in 3-h food-deprived broiler cockerels. J Physiol Biochem 67:217–223

    Article  CAS  PubMed  Google Scholar 

  • Taheriyan MR, Baghbanzadeh A, Zendehdel M (2016) Dopamine- induced hypophagia is mediated via NMDA and mGlu1 receptors in chicken. Iranian J. Vet Med 10(3):191–199

    Google Scholar 

  • Tzschentke TM, Schmidt WJ (2003) Glutamatergic mechanisms in addiction. Mol Psychiatr 8:373–382

    Article  CAS  Google Scholar 

  • Van Tienhoven A, Juhasz LP (1962) The chicken telencephalon, diencephalon and mesencephalon in sterotaxic coordinates. J Comp Neurol 118:185–197

    Article  Google Scholar 

  • Xu NJ, Bao L, Fan HP, Bao GB, Pu L, Lu YJ, Wu CF, Zhang X, Pei G (2003) Morphine withdrawal increases glutamate uptake and surface expression of glutamate transporter GLT1 at hippocampal synapses. J Neurosci 23:4775–4784

  • Zendehdel M, Baghbanzadeh A, Babapour V, Cheraghi J (2009) The effects of bicuculline and muscimol on glutamate-induced feeding behaviour in broiler cockerels. J Comp Physiol A 195:715–720

    Article  CAS  Google Scholar 

  • Zendehdel M, Ghashghayi E, Hassanpour S, Baghbanzadeh A, Jonaidi H (2016) Interaction between opioidergic and dopaminergic systems on food intake in neonatal layer type chicken. Int J Pept Res Ther 22:83–92

    Article  CAS  Google Scholar 

  • Zendehdel M, Hassanpour S (2014) Ghrelin-induced hypophagia is mediated by the β2 adrenergic receptor in chicken. J Physiol Sci 64:383–391

    Article  CAS  PubMed  Google Scholar 

  • Zendehdel M, Hassanpour S, Babapour V, Charkhkar Mahdavi M (2015) Interaction between endocannabinoid and opioidergic systems regulates food intake in neonatal chicken. Int J Pept Res Ther 21:289–297

    Article  CAS  Google Scholar 

  • Zendehdel M, Taati M, Jonaidi H, Amini E (2012) The role of central 5-HT (2C) and NMDA receptors on LPS-induced feeding behavior in chickens. J Physiol Sci 62:413–419

    Article  CAS  PubMed  Google Scholar 

  • Zeni LA, Seidler HB, De Carvalho NA, Freitas CG, Marino-Neto J, Paschoalini MA (2000) Glutamatergic control of food intake in pigeons: effects of central injections of glutamate, NMDA, and AMPA receptor agonists and antagonists. Pharmacol Biochem Behav 65(1):67–74

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank the central laboratory (Dr. Rastegar Lab.) of the Faculty of Veterinary Medicine, University of Tehran for cooperation.

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Authors and Affiliations

  1. Department of Basic Sciences, Faculty of Veterinary Medicine, Science and Research Branch, Islamic Azad University, Tehran, Iran

    Mahshid Torkzaban, Negar Panahi & Shahin Hassanpour

  2. Department of Basic Sciences, Faculty of Veterinary Medicine, University of Tehran, P.O. Box: 14155-6453, Tehran, Iran

    Morteza Zendehdel & Vahab Babapour

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  1. Mahshid Torkzaban
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  2. Morteza Zendehdel
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  3. Vahab Babapour
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  4. Negar Panahi
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Correspondence to Morteza Zendehdel.

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All experiments were executed according to the Guide for the Care and Use of Laboratory Animals and were approved by the institutional animal ethics committee.

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Torkzaban, M., Zendehdel, M., Babapour, V. et al. Interaction Between Central Opioidergic and Glutamatergic Systems on Food Intake in Neonatal Chicks: Role of NMDA, AMPA and mGLU1 Receptors. Int J Pept Res Ther 24, 157–169 (2018). https://doi.org/10.1007/s10989-017-9601-9

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