Opioid System and Leucine Interaction in the Regulation of Feed Intake in Broiler Chickens

Document Type : Original Article

Authors

1 Department of Clinical Sciences, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran

2 Department of Veterinary Laboratory Sciences, Faculty of Veterinary Sciences, Ilam University, Ilam, Iran

3 Department of Basic Sciences, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran

4 Department of Physiology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

Abstract

The opioidergic system plays a critical role in feed intake, among other physiological functions. This study investigated the potential effects of the opioidergic system, leucine and its interaction with the central regulation of feed intake in broilers. 108 one-day-old Ross 308 broiler chickens in six groups, each with three replicates (n=6) have been used. A guiding cannula was implanted into the right lateral cerebral ventricle. Seven days later, leucine (2 µg), morphine (250 pmol), naloxone (5 µg), morphine + leucine combination (250 pmol +2 µg), naloxone + leucine combination (5 µg + 2 µg), and normal saline were injected intra-cerebro-ventricularly (ICV) (injection volume = 10 μl, n = 6, each with three duplicates). The cumulative feed intake was measured at 30, 60, 90, 120, 180, and 240minutes post injection. Naloxone increased feed intake, whereas both leucine and morphine significantly reduced it (p<0.05). ICV injection of morphine increased the inhibitory effect of leucine on feed intake (p<0.05). Additionally, within the first 60 min post injection, the combination of leucine and naloxone increased feed intake (p>0.05), whereas naloxone mitigated the inhibitory effect of leucine during the same period (p>0.05). The feed intake remained significantly decreased up to 240 minutes following the ICV injection of the combination of leucine and naloxone (p<0.05). Leucine appears to decrease feed intake through mechanisms involving glutamate and neuropeptide Y.

Keywords


  1. Kuenzel WJ, Beck MM, Teruyama R. Neural sites and pathways regulating food intake in birds: a comparative analysis to mammalian systems. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology.  1999; 283(4‐5): 348-364.
  2. Hamidi F. Role of the Hypothalamic Arcuate Nucleus in Regulation of Food Intake. Journal of Neyshabur University of Medical Sciences. 2017; 5: 52 – 65.
  3. TavárezM A and los Santos FS. Impact of genetics and breeding on broiler production performance: a look into the past, present, and future of the industry. Animal Frontiers. 2016; 6: 37–41.
  4. Erwan E, Alimon AR, Sazili AQ, Yaakub H. Effect of varying levels of leucine and energy on performance and carcass characteristics of broiler chickens. International Journal of Poultry Science 2009; 7 (7): 696-699.
  5. Asuku AO, Ayinla MT, Ajibare AJ. Central Nervous System Regulation of Eating and Brain Functions. In Nutrition and Psychiatric Disorders: An Evidence-Based Approach to Understanding the Diet-Brain Connection. Springer. 2024; 69-87.
  6. Moe RO, Nordgreen J, Janczak AM, Spruijt BM, Bakken M. Effects of signalled reward type, food status and a μ-opioid receptor antagonist on cue-induced anticipatory behaviour in laying hens (Gallus domesticus). Applied Animal Behaviour Science. 2013; 148(1-2): 46-53.
  7. Gosnell BA, Levine AS, Morley JE. The stimulation of food intake by selective agonists of mu, kappa and delta opioid receptors. Life sciences. 1986; 38(12): 1081-1088.
  8. Cline MA, Denbow M, Gilbert E, Dridi S. Food intake regulation. In Sturkie's Avian Physiology. 2022; 687-713.
  9. Zendehdel M, Hassanpour Sh. Central regulation of food intake in mammals and birds: areview. Neurotransmitter 2014; 1: 251.
  10. Wu Y, He H, Cheng Z, Bai Y, Ma X. The Role of Neuropeptide Y and Peptide YY in the Development of Obesity via Gut-brain Axis. Curr Protein Pept Sci. 2019; 20(7): 750-758.
  11. Mercer Rebecca E, Melissa Chee, William F Colmers. The role of NPY in hypothalamic mediated food intake." Frontiers in neuroendocrinology. 2011; 32 (4): 398-415.
  12. Chang Y, Cai H, Liu G, Chang W, Zheng A, Zhang Sh, Liao R, Liu W, Li Y, Tian J.Effects of dietary leucine supplementation on the gene expression of mammalian target of rapamycin signaling pathway and intestinal development of broilers. Animal Nutrition, 2015; 1 (4): 313-319
  13. Swatson HK, Gous R, Iji PA, Zarrinkalam R. Effect of dietary protein level, amino acid balance, and feeding level on broiler chickens' growth, gastrointestinal tract, and mucosal structure of the small intestine. Animal Research. 2002; 51(6): 501-515.
  14. Peter J Garlick. The Role of Leucine in the Regulation of Protein Metabolism. The Journal of Nutrition. 2005; 135 (6): 1553-1556
  15. Chen K, Zhang Z, Li J, Xie S, Shi LJ, He YH, Liang XF, Zhu QS, He S. Different regulation of branched-chain amino acid on food intake by TOR signaling in Chinese perch (Siniperca chuatsi). Aquaculture. 2021; 530: 735-792.
  16. LiF, Yin Y,  Tan B, Kong X, Wu G. Leucine nutrition in animals and humans: mTOR signaling and beyond. Amino Acids. 2011; 41: 1185-1193.
  17. Pedroso J, Thais T, Zampieri J, Donato J. Reviewing the effects of L-leucine supplementation in the regulation of food intake, energy balance, and glucose homeostasis. Nutrients. 2015; 7 (5): 3914-3937.
  18. Pastor A, Wecke C, Liebert F. Assessing the age-dependent optimal dietary branched-chain amino acid ratio in growing chicken by application of a nonlinear modeling procedure. Poultry science. 2013; 92 (12): 3184-3195.
  19. Suryawan A, Asumthia JRenan OFiona WHanh NTeresa D. Leucine stimulates protein synthesis in the skeletal muscle of neonatal pigs by enhancing mTORC1 activation. American Journal of Physiology-Endocrinology and Metabolism. 2008; 295: 868-875.
  20. Plumstead Peter W. Response of young broilers to graded levels of dietary protein and amino acids. 2005.
  21. Scanes CG, Pierzchala-Koziec K. Perspectives on endogenous opioids in birds. Frontiers in physiology. 2018; 9: 1842.
  22. Bodnar Richard J. Recent advances in the understanding of the effects of opioid agents on feeding and appetite. Expert opinion on investigational drugs. 1998; 7 (4): 485-497.
  23. Sanger DJ, McCarthy P. Increased food and water intake produced in rats by opiate receptor agonists. Psychopharmacology. 1981; 74(3): 217-220.
  24. Arva Sh, Zendehdel M, Ebrahim Nezhad Y, Ghiasi Ghalehkandi J, Aghdam Shahryar H. Role of opioid receptors on food choice and macronutrient selection in meat-type chick. International Journal of Peptide Research and Therapeutics. 2016; 22: 219-228.
  25. Bodnar RJ. Opioid receptor subtype antagonists and ingestion. Drug receptor subtypes and ingestive behavior. 1996.
  26. Jafari-Anari M, Zendehdel M, Gilanpour H, Asghari A, Babapour V. Central opioidergic system interplay with histamine on food intake in neonatal chicks: role of µ-opioid and H1/H3 receptors. Brazilian Journal of Poultry Science. 2018; 20: 595-604.
  27. Selleck A, Brian B. Feeding-modulatory effects of mu-opioids in the medial prefrontal cortex: a review of recent findings and comparison to opioid actions in the nucleus accumbens. Psychopharmacology. 2017; 234: 1439-1449.
  28. Mills Richard H, Richard S, Paul E. Estrogen-induced μ-opioid receptor internalization in the medial preoptic nucleus is mediated via neuropeptide Y-Y1 receptor activation in the arcuate nucleus of female rats. Journal of Neuroscience. 2004; 24 (4): 947-955.
  29. Alimohammadi S, Zendehdel M, Babapour V. Modulation of opioid-induced feeding behavior by endogenous nitric oxide in neonatal layer-type chicks. Veterinary research communications. 2015; 39: 105-113.
  30. Murugesan S, Nidamanuri A. Role of leptin and ghrelin in the regulation of physiological functions of chicken. World's Poultry Science Journal. 2022; 78 (4): 1021-1036.
  31. Wang S, KhondoweP, Chen S, YuJ, Shu G, Xiaotong P, Gao Q, Xi, L, Zhang Y,  Jiang Q. Effects of Bioactive amino acids leucine, glutamate, arginine and tryptophan on feed intake and mRNA expression of relative neuropeptides in broiler chicks. Journal of Animal Science and Biotechnology. 2012; 3: 1-8.
  32. Hamidi B, Zendehdel M, Vazir B, Asghari A. The effect of the central administration of the Neuropeptide VF on feed intake and its possible interactions with glutamate and opioid systems in broiler chicken. International Journal of Peptide Research and Therapeutics. 2022; 28 (3): 101.
  33. Huang J., et al. Leucine and its Role in Opioid-Mediated Appetite Regulation. Animal Nutrition. 2020; 6(2): 162-169.
  34. Kong X., et al. Interactions Between Leucine and Opioidergic Pathways in Feeding Behavior of Broilers. Poultry Science. 2021; 100(6): 1001-1011.
  35. Denbow DM, Mccormack JF. Central versus peripheral opioid regulation of ingestive behavior in the domestic fowl. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology. 1990; 96 (1): 211-216.
  36. Wang HY, Friedman E, Olmstead MC, Burns LH. Ultra-low-dose naloxone suppresses opioid tolerance, dependence, and associated changes in mu opioid receptor–G protein coupling and Gβγ signaling. Neuroscience. 2005; 135: 247-261.
  37. McCormack, James F, Denbow DM. The effects of opioid antagonists on ingestive behavior in the domestic fowl. Pharmacology Biochemistry and Behavior. 1987; 27 (1): 25-33.
  38. Denbow DM, Cherry JA, Siegel PV, Van Krey HP. Eating, drinking, and temperature response of chicks to brain catecholamine injections. Physiology & Behavior. 1981; 27 (2): 265-269.
  39. Rahmani B, Ghashghae E, Zendehdel M, Khodadadi M. The crosstalk between brain mediators regulating food intake behavior in birds: a review. International Journal of Peptide Research and Therapeutics. 2021; 27: 2349-2370.
  40. Richards MP. Genetic regulation of feed intake and energy balance in poultry. Poultry science. 2003; 82 (6): 907-916.