Skip to main content

Advertisement

Log in

Intracerebroventricular Injection of the Glutamatergic Receptors Antagonist Affects N/OFQ-Induced Hyperphagia in Neonatal Broilers: Role of NMDA and AMPA Receptors

  • Published:
International Journal of Peptide Research and Therapeutics Aims and scope Submit manuscript

Abstract

This study was designed to determine possible interaction of the central nociceptin/orphanin FQ (N/OFQ) and glutamatergic system on feeding behavior in neonatal broilers chicken. In experiment 1, 3-h food deprived (FD3) chicks received intracerebroventricular (ICV) injection of (i) control solution, (ii) N/OFQ (16 nmol), (iii) MK-801 (NMDA [N-methyl-d-aspartate-type glutamate] receptor antagonist, 15 nmol) and (iv) N/OFQ + MK-801. Experiments 2–7 were similar to experiment 1, except chicken ICV injected with CNQX (AMPA [α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid] receptor antagonist, 390 nmol), UBP-302 (kainate receptor antagonist, 390 nmol), AIDA (mGluR1 antagonist, 2 nmol), LY341495 (mGluR2 antagonist, 150 nmol), UBP1112 (mGluR3 antagonist, 2 nmol) and Glutamate (300 nmol) instead of MK-801. Then the cumulative food intake measured until 120 min post injection. According to the results, ICV injection of N/OFQ significantly increased food intake (P < 0.05). Co-administration of the N/OFQ + MK-801 significantly amplified N/OFQ-induced hyperphagia in neonatal broilers (P < 0.05). Injection of the N/OFQ + CNQX significantly increased hyperphagic effect of the CNQX in neonatal meat-type chicken (P < 0.05). Co-injection of the N/OFQ + glutamate significantly decreased N/OFQ-induced hyperphagia in neonatal meat type chicken (P < 0.05). These results suggested interconnection between central N/OFQ and glutamatergic systems on feeding behavior mediates via NMDA and AMPA receptors in neonatal broilers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Diagram 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abbasnejad M, Jonaidi H, Pourrahimi AM (2005) Feeding and locomotion responses to centrally injected nociceptine/orphanin FQ in chicks. Physiol Behav 85:383–386

    Article  CAS  PubMed  Google Scholar 

  • Alt C, Lam JS, Harrison MT, Kershaw KM, Samuelsson S, Toll L, D’Andrea A (2012) Nociceptin/orphanin FQ inhibition with SB612111 ameliorates dextran sodium sulfate-induced colitis. Eur J Pharmacol 683:285–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andero R, Brothers SP, Jovanovic T, Chen YT, Salah-Uddin H, Cameron M et al (2013) Amygdala-dependent fear is regulated by Oprl1 in mice and humans with PTSD. Sci Transl Med 5:173–188

    Article  CAS  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 

  • Bayrakdar ET, Bojnik E, Armagan G, Kanit L, Benyhe S, Borsodi A, Yalcin A (2013) Kainic acid-induced seizure activity alters the mRNA expression and G-protein activation of the opioid/nociceptin receptors in the rat brain cortex. Epilepsy Res 105:13–19

    Article  CAS  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 

  • Bregola G, Candeletti S, Romualdi P, Simonato M (1999) Limbic seizures increase pronociceptin mRNA levels in the thalamic reticular nucleus. Neuroreport 10:541–546

    Article  CAS  PubMed  Google Scholar 

  • Bungo T, Shiraishi J, Yanagita K, Ohta Y, Fujita M (2009) Effect of Nociceptin/Orphanin FQ on feeding behavior and hypothalamic neuropeptide expression in layer-type chicks. Gen Comp Endocrinol 163:47–51

    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 

  • Farhang B, Pietruszewski L, Lutfy K, Wagner EJ (2010) The role of the nop receptor in regulating food intake, meal pattern, and the excitability of proopiomelanocortin neurons. Neuropharmacology 59(3):190–200

    Article  CAS  PubMed  PubMed Central  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 

  • Goeldner C, Reiss D, Wichmann J, Meziane H, Kieffer BL, Ouagazzal AM (2008) Nociceptin receptor impairs recognition memory via interaction with NMDA receptor-dependent mitogen-activated protein kinase/extracellular signal-regulated kinase signaling in the hippocampus. J Neurosci 28:2190–2198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goeldner C, Reiss D, Wichmann J, Kieffer BL, Ouagazzal AM (2009) Activation of nociceptin opioid peptide (NOP) receptor impairs contextual fear learning in mice through glutamatergic mechanisms. Neurobiol Learn Mem 91(4):393–401

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Hettes SR, Gonzaga WJ, 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 

  • Kallupi M, Varodayan FP, Oleata CS, Correia D, Luu G, Roberto M (2014) Nociceptin/orphanin FQ decreases glutamate transmission and blocks ethanol-induced effects in the central amygdala of naive and ethanol-dependent rats. Neuropsychopharmacology 39:1081–1092

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Marti M, Guerrini R, Beani L, Bianchi C, Morari M (2002) Nociceptin/orphanin FQ receptors modulate glutamate extracellular levels in the substantia nigra pars reticulata. a microdialysis study in the awake freely moving rat. Neuroscience 112(1):153–160

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Meyer LC, Paisley CE, Mohamed E, Bigbee JW, Kordula T, Richard H, Lutfy K, Sato-Bigbee C (2017) Novel role of the nociceptin system as a regulator of glutamate transporter expression in developing astrocytes. Glia 65:2003–2023

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicholson JR, Akil H, Watson SJ (2002) Orphanin FQ-induced hyperphagia is mediated by corticosterone and central glucocorticoid receptors. Neuroscience 115:637–643

    Article  CAS  PubMed  Google Scholar 

  • Novoseletsky N, Nussinovitch A, Friedman-Einat M (2011) Attenuation of food intake in chicks by an inverse agonist of cannabinoid receptor 1 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 

  • Olszewski PK, Grace MK, Sanders JB, Billington CJ, Levine AS (2002) Effect of Nociceptin/orphanin FQ on food intake in rats that differ in diet preference. Pharmacol Biochem Behav 73(3):529–535

    Article  CAS  PubMed  Google Scholar 

  • Olszewski PK, Grace MK, Shirazi Fard S, Greve`s ML, Klockars A, Massi M, Schiöth HB, Levine AS (2010) Central nociceptin/orphanin FQ system elevates food consumption by both increasing energy intake and reducing aversive responsiveness. Am J Physiol Regul Integr Comp Physiol 299:R655–R663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Reinscheid RK, Nothacker HP, Bourson A, Ardati A, Henningsen RA, Bunzow JR, Grandy DK, Langen H, Monsma FJ Jr, Civelli O (1995) Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor. Science 270(5237):792–794

    Article  CAS  PubMed  Google Scholar 

  • Roozendaal B, Lengvilas R, McGaugh JL, Civelli O, Reinscheid RK (2007) Orphanin FQ/nociceptin interacts with the basolateral amygdala noradrenergic system in memory consolidation. Learn Mem 14:29–35

    Article  CAS  PubMed  PubMed Central  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 

  • 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 

  • Stratford TR, Holahan MR, Kelley AE (1997) Injections of nociceptin into nucleus accumbens shell or ventromedial hypothalamic nucleus increase food intake. Neuroreport 8(2):423–426

    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 

  • Tajalli S, Jonaidi H, Abbasnejad M, Denbow DM (2006) Interaction between nociceptin/orphanin FQ (N/OFQ) and GABA in response to feeding. Physiol Behav 89:410–413

    Article  CAS  PubMed  Google Scholar 

  • Tallent MK (2008) Presynaptic inhibition of glutamate release by neuropeptides: use-dependent synaptic modification. Results Probl Cell Differ 44:177–200

    Article  CAS  PubMed  Google Scholar 

  • Toll L, Bruchas MR, Calo’ G, Cox BM, Zaveri NT (2016) Nociceptin/orphanin FQ receptor structure, signaling, ligands, functions, and interactions with opioid systems. Pharmacol Rev 68:419–457

    Article  PubMed  PubMed Central  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 

  • Werthwein S, Bauer U, Nakazi M, Kathmann M, Schlicker E (1999) Further characterization of the ORL1 receptor-mediated inhibition of noradrenaline release in the mouse brain in vitro. Br J Pharmacol 127:300–308

    Article  CAS  PubMed  PubMed Central  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, 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, Hamidi F, Hassanpour S (2013a) The effect of histaminergic system on Nociceptin/orphanin FQ induced food intake in chicken. Int J Pept Res Ther 21:179–186

    Article  CAS  Google Scholar 

  • Zendehdel M, Mokhtarpouriani K, Babapour V, Baghbanzadeh A, Pourrahimi M, Hassanpour S (2013b) The effect of serotonergic system on nociceptin/orphanin FQ induced food intake in chicken. J Physiol Sci 63:271–277

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the central laboratory (Dr. Rastegar Lab.) of the Faculty of Veterinary Medicine, University of Tehran for cooperation. This research is conducted as a part of the PhD thesis of the first author.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Morteza Zendehdel or Negar Panahi.

Ethics declarations

Conflict of interest

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abolghasempour, S., Zendehdel, M., Panahi, N. et al. Intracerebroventricular Injection of the Glutamatergic Receptors Antagonist Affects N/OFQ-Induced Hyperphagia in Neonatal Broilers: Role of NMDA and AMPA Receptors. Int J Pept Res Ther 25, 835–843 (2019). https://doi.org/10.1007/s10989-018-9733-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10989-018-9733-6

Keywords

Navigation