Skip to main content

Cannabinoid–glutamate interactions in the regulation of food intake in neonatal layer- type chicks: role of glutamate NMDA and AMPA receptors

Abstract

The involvement of the endocannabinoid system in the brain functions is likely the conclusion of its capability to interact with specific neurotransmitters in several brain regions. The present study was designed to examine the role of the glutamatergic system on cannabinoid-induced hyperphagia in chicken. In this survey 10 experiments designed to investigate interaction of cannabinoidergic and glutamatergic systems on feeding behavior in neonatal chickens. In experiment 1, chicken were intracerebroventricular (ICV) injected with saline, 2-AG (2-Arachidonoylglycerol, 5.28 nmol, CB1 receptors agonist), MK-801(NMDA receptor antagonist, 15 nmol) and co-administration of 2-AG + MK-801. In experiment 2, injection of saline, 2-AG (5.28 nmol), CNQX) AMPA/kainate receptor antagonist, 390 nmol) and their combination (2-AG + CNQX) was done. In Experiment 3, injections were saline, 2-AG (5.28 nmol), AIDA)mGluR1 antagonist, 2 nmol) and 2-AG + AIDA. Experiments 4 and 5 were similar to experiment 3, except birds injected with LY341495 (mGLUR2 glutamate antagonist, 150 nmol) and UBP1112 (mGLUR3 glutamate antagonist, 2 nmol) instead of AIDA. Experiments 6–10 followed the procedure similar to experiments 1–5, except chickens received ICV injection of CB65 (CB2 receptor agonist, 3 nmol), instead of 2-AG. Then the cumulative food intake measured until 120 min post injection. According to the results, ICV injection of 2-AG and CB65 significantly increased food intake (P < 0.001). Co-injection of 2-AG and MK-801 significantly amplified hyperphagic effect of CB1 receptors agonist(P < 0.001). Moreover, co-administration of CB65 plus CNQX significantly increased CB65- induced hyperphagia in FD3 neonatal layer-type chickens (P < 0.001). These results suggest there is an interaction between endocannabinoids and glutamatergic systems via NMDA and AMPA receptors in feeding behavior of neonatal layer-type chickens.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

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(2):105–113

    Article  PubMed  Google Scholar 

  • Alizadeh A, Zendehdel M, Babapour V, Charkhkar S, Hassanpour S (2015) Role of cannabinoidergic system on food intake in neonatal layer-type chicken. Vet Res Commun 39:151–157

    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 

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

    CAS  Article  PubMed  Google Scholar 

  • Chen RZ, Frassetto A, Fong TM (2006) Effects of the CB1 cannabinoid receptor inverse agonist AM251 on food intake and body weight in mice lacking μ-opioid receptors. Brain Res 1108:176–178

    CAS  Article  PubMed  Google Scholar 

  • Ciranna L (2006) Serotonin as a modulator of glutamate- and GABAmediated neurotransmission: implications in physiological functions and in pathology. Curr Neuropharmacol 4:101–114

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Cota D, Marsicano G, Lutz B, Vicennati V, Stalla GK, Pasquali R, Pagotto U (2003) Endogenous cannabinoid system as a modulator of food intake. Int J Obes 27:289–301

    CAS  Article  Google Scholar 

  • D’Addario C, Micioni Di Bonaventura MV, Pucci M, Romano A, Gaetani S, Ciccocioppo R, Cifani C, Maccarrone M (2014) Endocannabinoid signaling and food addiction. Neurosci Biobehav Rev 47:203–224

    Article  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  PubMed  Google Scholar 

  • Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105

    CAS  Article  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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Di Marzo VGS, Wang L, Liu J, Batkai S, Jarai Z, Fezza F, Miura GI, Palmiter RD, Sugiura T, Kunos G (2001) Leptin regulated endocannabinoids are involved in maintaining food intake. Nature 410:822–825

    Article  PubMed  Google Scholar 

  • Duva MA, Siu A, Stanley BG (2005) The NMDA receptor antagonist MK-801 alters lipoprivic eating elicited by 2-mercaptoacetate. Physiol Behav 83:787–791

    CAS  Article  PubMed  Google Scholar 

  • Emadi L, Jonaidi H, Hosseini Amir Abad E (2011) The role of Central CB2 cannabinoid receptors on food intake in neonatal chicks. J Comp Physiol A 197:1143–1147

    CAS  Article  Google Scholar 

  • Ferna’ndez-Ruiz J, Herna’ndez M, JA R (2010) Cannabinoid–dopamine interaction in the pathophysiology and treatment of CNS disorders. CNS Neurosci Ther 16:72–91

    Article  Google Scholar 

  • Fowler CJ, Nilsson O, Andersson M, Disney G, Jacobsson SO, Tiger G (2001) Pharmacological properties of cannabinoid receptors in the avian brain: similarity of rat and chicken cannabinoid1 receptor recognition sites and expression of cannabinoid2 receptor-like immunoreactivity in the embryonic chick brain. Pharmacol Toxicol 88:213–222

    CAS  Article  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

    CAS  Article  PubMed  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

    CAS  Article  PubMed  Google Scholar 

  • Gerdeman G, Lovinger DM (2001) CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 85:468–471

    CAS  PubMed  Google Scholar 

  • Hampson RE, Miller F, Palchik G, Deadwyler SA (2011) Cannabinoid receptor activation modifies NMDA receptor mediated release of intracellular calcium: implications for endocannabinoid control of hippocampal neural plasticity. Neuropharmacology 60:944–952

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hassanpour S, Zendehdel M, Babapour V, Charkhkar S (2015) Endocannabinoid and nitric oxide interaction mediates food intake in neonatal chicken. Br Poult Sci 56(4):443–451

    CAS  Article  PubMed  Google Scholar 

  • Huang CC, Lo SW, Hsu KS (2001) Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol Lond 532:731–748

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Irving AJ, Rae MG, Coutts AA (2002) Cannabinoids on the brain. Sci World J 2:632–648

    CAS  Article  Google Scholar 

  • Irwin N, Hunter K, Frizzell N, Flatt PR (2008) Antidiabetic effects of sub-chronic administration of the cannabinoid receptor (CB1) antagonist, AM251, in obese diabetic (ob/ob) mice. Eur J Pharmacol 581:226–233

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Kangas BD, Delatte MS, Vemuri VK, Thakur GA, Nikas SP, Subramanian KV, Shukla VG, Makriyannis A, Bergman J (2013) Cannabinoid discrimination and antagonism by cb1 neutral and inverse agonist antagonists. J Pharmacol Exp Ther 344:561–567

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Levine AS (2006) The animal model in food intake regulation: examples from the opioid literature. Physiol Behav 89:92–96

    CAS  Article  PubMed  Google Scholar 

  • Lim CT, Kola B, Korbonits M (2010) AMPK as a mediator of hormonal signalling. J Mol Endocrinol 44:87–97

    CAS  Article  PubMed  Google Scholar 

  • Lin TY, Lu CW, Wu CC, Huang SK, Wang SJ (2015) Palmitoylethanolamide inhibits glutamate release in rat cerebrocortical nerve terminals. Int J Mol Sci 16:5555–5571

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Bhat M, Bowen WD, Cheng J (2009) Signaling pathways from cannabinoid receptor-1 activation to inhibition of N-methyl-D-aspartic acid mediated calcium influx and neurotoxicity in dorsal root ganglion neurons. J Pharmacol Exp Ther 331:1062–1070

    CAS  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 

  • López HH (2010) Cannabinoid–hormone interactions in the regulation of motivational processes. Horm Behav 58:100–110

    Article  PubMed  Google Scholar 

  • Nicoll RA, Alger BE (2004) The brain’s own marijuana. Sci Am 291:68–75

    Article  PubMed  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

    CAS  Article  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 

  • Onaivi ES, Carpio O, Ishiguro H, Schanz N, Uhl GR, Benno R (2008) Behavioral effects of CB2 cannabinoid receptor activation and its influence on food and alcohol consumption. Ann N Y Acad Sci 1139:426–433

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Onaivi ES, Ishiguro H, Gu S, Liu QR (2012) CNS effects of CB2 cannabinoid receptors: beyond neuro-immuno-cannabinoid activity. J Psychopharmacol 26:92–103

  • Parker KE, Johns HW, Floros TG, Will MJ (2014) Central amygdala opioid transmission is necessary for increased high-fat intake following 24-h food deprivation, but not following intraaccumbens opioid administration. Behav Brain Res 260:131–138

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Pertwee RG (2005) Pharmacological actions of cannabinoids. Handb Exp Pharmacol 168:1–51

    CAS  Article  PubMed  Google Scholar 

  • Reid CA, Bliss TVP (2000) Learning about kainate receptors. Tips 21:159–160

    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

    CAS  Article  PubMed  Google Scholar 

  • Sánchez-Blázquez P, Rodríguez-Muñoz M, Vicente-Sánchez A, Garzón J (2013a) Cannabinoid receptors couple to NMDA receptors to reduce the production of NO and the mobilization of zinc induced by glutamate. Antioxid Redox Signal 19:1766–1782

    Article  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Blázque P, Rodríguez-Muño M, Garzón J (2013b) The cannabinoid receptor 1 associates with NMDA receptors to produce glutamatergic hypofunction: implications in psychosis and schizophrenia. Front Pharmacol 4:169. doi:10.3389/fphar.2013.00169

  • Seyedali Mortezaei S, Zendehdel M, Babapour V, Hasani K (2013) The role of glutamatergic and GABAergic systems on serotonin- induced feeding behavior in chicken. Vet Res Commun 37:303–310

    Article  Google Scholar 

  • Sharkey KA, Darmani NA, Parker LA (2014) Regulation of nausea and vomiting by cannabinoids and the endocannabinoid system. Eur J Pharmacol 722:134–146

    CAS  Article  PubMed  Google Scholar 

  • Shiraishi J, Yanagita K, Fukumori R, Sugino T, Fujita M, Kawakami S, McMurtry JP, Bungo T (2011) Comparisons of insulin related parameters in commercial-type chicks: evidence for insulin resistance in broiler chicks. Physiol Behav 103:233–239

    CAS  Article  PubMed  Google Scholar 

  • Suarez J, Bermudez-Silva FJ, Mackie K, Ledent C, Zimmer A, Cravatt BF, de Fonseca FR (2008) Immunohistochemical description of the endogenous cannabinoid system in the rat cerebellum and functionally related nuclei. J Comp Neurol 509:400–421

    CAS  Article  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

    CAS  Article  PubMed  Google Scholar 

  • Tasca CI, Santos TG, Tavares RG, Battastini AM, Rocha JB, Souza DO (2004) Guanine derivatives modulate L-glutamate uptake into rat brain synaptic vesicles. Neurochem Int 44(6):423–431

    CAS  Article  PubMed  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 

  • Verty ANA, McFarlane JR, McGregor IS, Mallet PE (2004) Evidence for an interaction between CB1 cannabinoid and melanocortin MCR-4 receptors in regulating food intake. Endocrinol 145(7):3224–3231

    CAS  Article  Google Scholar 

  • Vicente-Sánchez A, Sánchez-Blázquez P, Rodríguez-Muñoz M, Garzón J (2013) HINT1 protein cooperates with cannabinoid 1 receptor to negatively regulate glutamate NMDA receptor activity. Mol Brain 6:42. doi:10.1186/1756-6606-6-42

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiley JL, Marusich JA, Zhang Y, Fulp A, Maitra R, Thomas BF, Mahadevan A (2012) Structural analogs of pyrazole and sulfonamide cannabinoids: effects on acute food intake in mice. Eur J Pharmacol 695:62–70

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Article  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

    CAS  Article  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

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by a grant from the Research Council of the Faculty of Veterinary Medicine, University of Tehran, Iran.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Morteza Zendehdel.

Ethics declarations

Conflict of interest

Authors declare that they have no conflict of interest.

Informed Consent

This manuscript does not contain any studies with human subjects performed by any of the authors.

Human and Animal Rights

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Keyshams, N., Zendehdel, M., Babapour, V. et al. Cannabinoid–glutamate interactions in the regulation of food intake in neonatal layer- type chicks: role of glutamate NMDA and AMPA receptors. Vet Res Commun 40, 63–71 (2016). https://doi.org/10.1007/s11259-016-9655-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11259-016-9655-8

Keywords

  • Cannabinoidergic
  • Glutamatergic system
  • Food intake
  • Chicken