The role of cyclooxygenase inhibitors in lipopolysaccharide-induced hypophagia in chicken

https://doi.org/10.17221/8403-CJASCitation:Zendehdel M., Baghbanzadeh A., Yeganeh B., Hassanpour S. (2015): The role of cyclooxygenase inhibitors in lipopolysaccharide-induced hypophagia in chicken. Czech J. Anim. Sci., 60: 342-350.
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Previous studies showed that cyclooxygenase 1 (COX) enzyme has an important role in lipopolysaccharide (LPS)-induced hypophagia in mammals but the effect of COX on LPS-induced hypophagia has not been studied in avian species. The current study was designed to investigate the effects of Indomethacin, a non-selective cyclooxygenase inhibitor, Aspirin (irreversible cyclooxygenase inhibitor), Piroxicam (a selective COX-1 inhibitor), and Celecoxib (a selective COX-2 inhibitor) on LPS-induced hypophagia in 3-h food-deprived (FD3) cockerels. One hundred and sixty ROSS 308 chickens were randomly divided into 5 experiments and 4 treatment groups (8 replicates in each group of experiments). Guide cannula was surgically implanted into the lateral ventricle of chickens. In Experiment 1, birds received LPS (5, 10, and 20 ng) intracerebroventricularly (ICV). In Experiment 2, chickens were intraperitoneally (i.p.) injected with Indomethacin (5 mg/kg) prior to LPS injection (20 ng; ICV). In Experiment 3, birds were i.p. injected with Aspirin (50 mg/kg) followed by LPS injection (20 ng; ICV). In Experiment 4, chickens were given LPS (20 ng; ICV) after Piroxicam injection (10 mg/kg; i.p.). In Experiment 5, chickens were injected with Celecoxib (10 mg/kg; i.p.) prior to LPS injection (20 ng; ICV). Cumulative feed intake was determined until 8 h post-injection. According to the results, LPS significantly decreased feed intake at 4 and 8 h post injection in birds (P ≤ 0.05). Furthermore, LPS-induced hypophagia was attenuated by pre-injection with Indomethacin, Aspirin, and Celecoxib (P ≤ 0.05). However, Piroxicam had no effect on LPS-induced hypophagia (P ≥ 0.05). These results suggest that presumably COX-2 mediates LPS-induced hypophagia in broilers.
References:
Abe Michie, Oka Takakazu, Hori Tetsuro, Takahashi Shosuke (2001): Prostanoids in the preoptic hypothalamus mediate systemic lipopolysaccharide-induced hyperalgesia in rats. Brain Research, 916, 41-49  https://doi.org/10.1016/S0006-8993(01)02861-X
 
Abrehdari Zahra, Zendehdel Morteza, Safarpour Elham, Allahdini Parvaneh (2014): The effects of coadministration of ghrelin agonist (GHRP-2) and GH on TNF-α, IL-6, and iNOS genes expression induced by LPS in mouse liver. Comparative Clinical Pathology, 23, 835-840  https://doi.org/10.1007/s00580-013-1698-4
 
Choi S.-H., Langenbach R., Bosetti F. (2007): Genetic deletion or pharmacological inhibition of cyclooxygenase-1 attenuate lipopolysaccharide-induced inflammatory response and brain injury. The FASEB Journal, 22, 1491-1501  https://doi.org/10.1096/fj.07-9411com
 
Denbow D.M., Cherry J.A., Siegel P.B., Van Krey H.P. (1981): Eating, drinking and temperature response of chicks to brain catecholamine injections. Physiology & Behavior, 27, 265-269  https://doi.org/10.1016/0031-9384(81)90268-7
 
de Paiva Viviane N., Lima Samuel N.P., Fernandes Mateus M., Soncini Roseli, Andrade Carina A.F., Giusti-Paiva Alexandre (2010): Prostaglandins mediate depressive-like behaviour induced by endotoxin in mice. Behavioural Brain Research, 215, 146-151  https://doi.org/10.1016/j.bbr.2010.07.015
 
Dunn Adrian J., Swiergiel Artur H. (2000): The Role of Cyclooxygenases in Endotoxin- and Interleukin-1-Induced Hypophagia. Brain, Behavior, and Immunity, 14, 141-152  https://doi.org/10.1006/brbi.1999.0580
 
Hollis Jacob H., Lemus Moyra, Evetts Megan J., Oldfield Brian J. (2010): Central interleukin-10 attenuates lipopolysaccharide-induced changes in food intake, energy expenditure and hypothalamic Fos expression. Neuropharmacology, 58, 730-738  https://doi.org/10.1016/j.neuropharm.2009.12.016
 
Inui A (): Cytokines and sickness behavior: implications from knockout animal models. Trends in Immunology, 22, 469-473  https://doi.org/10.1016/S1471-4906(01)01981-0
 
Inui A. (2002): Cancer anorexia– cachexia syndrome: current issues in research and management. CA: A Cancer Journal for Clinicians, 5272–5291.
 
Iwasa Takeshi, Matsuzaki Toshiya, Kinouchi Riyo, Fujisawa Shinobu, Murakami Masahiro, Kiyokawa Machiko, Kuwahara Akira, Yasui Toshiyuki, Irahara Minoru (2010): Neonatal LPS injection alters the body weight regulation systems of rats under non-stress and immune stress conditions. International Journal of Developmental Neuroscience, 28, 119-124  https://doi.org/10.1016/j.ijdevneu.2009.08.015
 
Johnson R.W. (1997): Inhibition of growth by pro-inflammatory cytokines: an integrated view. Journal of Animal Science, 75, 1244–1255.
 
Johnson R.W (1998): Immune and endocrine regulation of food intake in sick animals. Domestic Animal Endocrinology, 15, 309-319  https://doi.org/10.1016/S0739-7240(98)00031-9
 
Johnson R.W., von Borell E. (1994): Lipopolysaccharide-induced sickness behavior in pigs is inhibited by pretreatment with Indomethacin. Journal of Animal Science, 72, 309–314.
 
Johnson R.W., Curtis S.E., Dantzer R., Kelley K.W. (1993): Central and peripheral prostaglandins are involved in sickness behavior in birds. Physiology & Behavior, 53, 127-131  https://doi.org/10.1016/0031-9384(93)90020-G
 
Konsman Jan Pieter, Parnet Patricia, Dantzer Robert (2002): Cytokine-induced sickness behaviour: mechanisms and implications. Trends in Neurosciences, 25, 154-159  https://doi.org/10.1016/S0166-2236(00)02088-9
 
Kovács Zsolt, Czurkó András, Kékesi Katalin A., Juhász Gábor (2011): Intracerebroventricularly administered lipopolysaccharide enhances spike–wave discharges in freely moving WAG/Rij rats. Brain Research Bulletin, 85, 410-416  https://doi.org/10.1016/j.brainresbull.2011.05.003
 
Langhans Wolfgang (2000): Anorexia of infection: current prospects. Nutrition, 16, 996-1005  https://doi.org/10.1016/S0899-9007(00)00421-4
 
Langhans Wolfgang, Harlacher Rahel, Scharrer Erwin (1989): Verapamil and indomethacin attenuate endotoxin-induced anorexia. Physiology & Behavior, 46, 535-539  https://doi.org/10.1016/0031-9384(89)90032-2
 
Li S, Ballou L.R, Morham S.G, Blatteis C.M (2001): Cyclooxygenase-2 mediates the febrile response of mice to interleukin-1β. Brain Research, 910, 163-173  https://doi.org/10.1016/S0006-8993(01)02707-X
 
Mantovani Giovanni, Macciò Antonio, Madeddu Clelia, Serpe Roberto, Antoni Giorgia, Massa Elena, Dessì Mariele, Panzone Filomena (2010): Phase II nonrandomized study of the efficacy and safety of COX-2 inhibitor celecoxib on patients with cancer cachexia. Journal of Molecular Medicine, 88, 85-92  https://doi.org/10.1007/s00109-009-0547-z
 
Mortezaei Sepideh Seyedali, Zendehdel Morteza, Babapour Vahab, Hasani Keyvan (2013): The role of glutamatergic and GABAergic systems on serotonin- induced feeding behavior in chicken. Veterinary Research Communications, 37, 303-310  https://doi.org/10.1007/s11259-013-9576-8
 
Nadjar Agnès, Sauvant Julie, Combe Chantal, Parnet Patricia, Konsman Jan Pieter (2010): Brain cyclooxygenase-2 mediates interleukin-1-induced cellular activation in preoptic and arcuate hypothalamus, but not sickness symptoms. Neurobiology of Disease, 39, 393-401  https://doi.org/10.1016/j.nbd.2010.05.005
 
Ohinata Kousaku, Takagi Kuniko, Biyajima Kyoko, Fujiwara Yoko, Fukumoto Shingo, Eguchi Naomi, Urade Yoshihiro, Asakawa Akihiro, Fujimiya Mineko, Inui Akio, Yoshikawa Masaaki (2008): Central prostaglandin D2 stimulates food intake via the neuropeptide Y system in mice. FEBS Letters, 582, 679-684  https://doi.org/10.1016/j.febslet.2008.01.050
 
Ohinata K., Takagi K., Biyajima K., Kaneko K., Miyamoto C, Asakawa A., Eguchi N., Urade Y., Inui A., Yoshikawa M. (2009a): Complement C5a stimulates food intake via a prostaglandin D2- and neuropeptide Y-dependent mechanism in mice. Prostaglandins and Other Lipid Mediators, 90, 81–84.
 
Ohinata K., Fujiwata Y., Shingo F., Masaru I., Masatsugu H., Yoshikawa M. (2009b): Orally administered novokinin, an angiotensin AT2 receptor agonist, suppresses food intake via prostaglandin E2-dependent mechanism in mice. Peptides, 30, 1105–1108.
 
. H.A. Olanrewaju, . J.P. Thaxton, . W.A. Dozier III, . J. Purswell, . W.B. Roush, . S.L. Branton (2006): A Review of Lighting Programs for Broiler Production. International Journal of Poultry Science, 5, 301-308  https://doi.org/10.3923/ijps.2006.301.308
 
Parsadaniantz S. Mélik, Lebeau A., Duval P., Grimaldi B., Terlain§ B., Kerdelhué B. (2000): Effects of the Inhibition of Cyclo-Oxygenase 1 or 2 or 5-Lipoxygenase on the Activation of the Hypothalamic-Pituitary-Adrenal Axis Induced by Interleukin-1β in the Male Rat. Journal of Neuroendocrinology, 12, 766-773  https://doi.org/10.1046/j.1365-2826.2000.00517.x
 
Plata-Salamán C R (2001): Cytokines and feeding. International Journal of Obesity, 25, S48-S52  https://doi.org/10.1038/sj.ijo.0801911
 
Scarlett Jarrad M., Jobst Erin E., Enriori Pablo J., Bowe Darren D., Batra Ayesha K., Grant Wilmon F., Cowley Michael A., Marks Daniel L. (2007): Regulation of Central Melanocortin Signaling by Interleukin-1β. Endocrinology, 148, 4217-4225  https://doi.org/10.1210/en.2007-0017
 
Scarlett Jarrad M., Zhu Xinxia, Enriori Pablo J., Bowe Darren D., Batra Ayesha K., Levasseur Peter R., Grant Wilmon F., Meguid Michael M., Cowley Michael A., Marks Daniel L. (2008): Regulation of Agouti-Related Protein Messenger Ribonucleic Acid Transcription and Peptide Secretion by Acute and Chronic Inflammation. Endocrinology, 149, 4837-4845  https://doi.org/10.1210/en.2007-1680
 
Sergeyev Valeriy, Broberger Christian, Hökfelt Tomas (2001): Effect of LPS administration on the expression of POMC, NPY, galanin, CART and MCH mRNAs in the rat hypothalamus. Molecular Brain Research, 90, 93-100  https://doi.org/10.1016/S0169-328X(01)00088-2
 
Singh A.K., Jiang Y. (2004): How does peripheral lipopolysaccharide induce gene expression in the brain of rats? Toxicology, 201, 197–207.
 
Swiergiel A. H. (): Distinct Roles for Cyclooxygenases 1 and 2 in Interleukin-1-Induced Behavioral Changes. Journal of Pharmacology and Experimental Therapeutics, 302, 1031-1036  https://doi.org/10.1124/jpet.102.036640
 
Thurmon J.C., Tranquilli W.J., Benson G.J. (1996): Lumb and Jones’ Veterinary Anesthesia. Williams and Wilkins, Baltimore, USA.
 
van Tienhoven A., Juh�sz L. P. (1962): The chicken telencephalon, diencephalon and mesencephalon in stereotaxic coordinates. The Journal of Comparative Neurology, 118, 185-197  https://doi.org/10.1002/cne.901180205
 
Volkoff Helene, Peter Richard Ector (2004): Effects of lipopolysaccharide treatment on feeding of goldfish: role of appetite-regulating peptides. Brain Research, 998, 139-147  https://doi.org/10.1016/j.brainres.2003.11.011
 
Volkoff H., Unniappan S., Kelly S.P. (2009): The endocrine regulation of food intake. Fish Neuroendocrinology, 28, 421–465.
 
von Meyenburg Claudia, Langhans Wolfgang, Hrupka Brian J (2003): Evidence that the anorexia induced by lipopolysaccharide is mediated by the 5-HT2C receptor. Pharmacology Biochemistry and Behavior, 74, 505-512  https://doi.org/10.1016/S0091-3057(02)01029-8
 
Walker Adam K, Budac David P, Bisulco Stephanie, Lee Anna W, Smith Robin A, Beenders Brent, Kelley Keith W, Dantzer Robert (): NMDA Receptor Blockade by Ketamine Abrogates Lipopolysaccharide-Induced Depressive-Like Behavior in C57BL/6J Mice. Neuropsychopharmacology, 38, 1609-1616  https://doi.org/10.1038/npp.2013.71
 
Zendehdel M., Mokhtarpouriani K., Hamidi F., Montazeri R. (2012a): Intracerebroventricular injection of ghrelin produces hypophagia through central serotonergic mechanisms in chicken. Veterinary Research Communications, 37, 37–41.
 
Zendehdel M., Taati M., Jonaidi H., Amini E. (2012b): The role of central 5- HT (2C) and NMDA receptors on LPS-induced feeding behavior in chickens. The Journal of Physiological Sciences, 62, 413–419.
 
Zendehdel M., Hamidi F., Babapour V., Mokhtarpouriani K., Mazaheri Nezhad Fard R. (2012c): The effect of melanocortin (Mc3 and Mc4) antagonists on serotonin-induced food and water intake of broiler cockerels. Journal of Veterinary Science, 13, 229–234.
 
Zendehdel M., Taati M., Jonaidi H., Amini E. (2012d): The role of central 5-HT2C and NMDA receptors on LPS-induced feeding behavior in chickens. The Journal of Physiological Sciences, 62, 413–419.
 
Zendehdel M., Hasani K., Babapour V., Mortezaei S.S., Khoshbakht Y., Hassanpour S. (2013a): Dopamine-induced hypophagia is mediated by D1 and 5HT-2c receptors in chicken. Veterinary Research Communications, 38, 11–19.
 
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. The Journal of Physiological Sciences, 63, 271–277.
 
Zendehdel Morteza, Hassanpour Shahin (2014): Ghrelin-induced hypophagia is mediated by the β2 adrenergic receptor in chicken. The Journal of Physiological Sciences, 64, 383-391  https://doi.org/10.1007/s12576-014-0330-y
 
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