The effect of L-tryptophan on the food intake, rectal temperature, and blood metabolic parameters of 7-day-old chicks during feeding, fasting, and acute heat stress

Document Type : Full paper (Original article)

Authors

1 Ph.D. Student in Physiology, Department of Basic Sciences, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

2 Department of Basic Sciences, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

3 Department of Biology, Faculty of Sciences, Shahid Bahonar University of Kerman, Kerman, Iran

4 Department of Clinical Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

10.22099/ijvr.2020.37266.5428

Abstract

Background: Exposure to a high ambient temperature (HT) can cause heat stress, which has a negative impact on physiological functions. L-tryptophan (L-Trp) as a precursor of serotonergic and kynurenine (Kyn) pathways, has a calmative effect during different stress statuses. Aims: This study was carried out to determine the influence of intraperitoneal injection of Trp on feeding behavior, rectal temperature, and some blood parameters in the heat stress condition. Methods: L-tryptophan (25 and 50 mg/kg body weight, BW) was administered intraperitoneally during either HT (39°C) or control temperature (CT; 31°C) for 5 h whilst fed or fasted in 7-day-old chicks. Results: L-tryptophan caused elevation in decreased food intake and significantly decreased rectal temperature during acute heat stress at the dose of 50 mg/kg BW. Rectal temperature reduced in the fasted state at the dose of 50 mg/kg BW, and at the dose of 25 mg/kg BW Trp in the fed state in comparison with the other experimental groups. Reduction of serum glucose, triglyceride, and corticosterone levels was seen during the fed state. L-tryptophan had a significant reducing effect on the serum corticosterone level in the fasted state in comparison with the fed state, and also revealed a significant decline at the dose of 25 mg/kg BW on the elevated serum corticosterone under heat stress. Conclusion: Administration of L-tryptophan leads to increase cumulative food intake and decrease rectal temperature during heat stress. Also, L-Trp causes to decline increased serum corticosterone level under heat stress and fasted state. These findings indicated the potential regulator role of Trp to modulate stress response in heat-exposed chicks.

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Ahmed, AA; Ma, W; Ni, Y; Wang, S and Zhao, R (2014a). Corticosterone in ovo modifies aggressive behaviors and reproductive performances through alterations of the hypothalamic-pituitary-gonadal axis in the chicken. Anim. Reprod. Sci., 146: 193-201.
Ahmed, AA; Ma, W; Ni, Y; Zhou, Q and Zhao, R (2014b). Embryonic exposure to corticosterone modifies aggressive behavior through alterations of the hypothalamic pituitary adrenal axis and the serotonergic system in the chicken. Horm. Behav., 65: 97-105.
Ashraf, S; Zaneb, H; Yousaf, M; Ijaz, A; Sohail, M; Muti, S; Usman, M; Ijaz, S and Rehman, H (2013). Effect of dietary supplementation of prebiotics and probiotics on intestinal microarchitecture in broilers reared under cyclic heat stress. J. Anim. Physiol. Anim. Nutr., 97: 68-73.
Bahry, MA; Chowdhury, VS; Yang, H; Tran, PV; Do, PH; Han, G; Ikeda, H; Cockrem, JF and Furuse, M (2017). Central administration of neuropeptide Y differentially regulates monoamines and corticosterone in heat-exposed fed and fasted chicks. Neuropeptides. 62: 93-100.
Bandeira, LG; Bortolot, BS; Cecatto, MJ; Monte-Alto-Costa, A and Romana-Souza, B (2015). Exogenous tryptophan promotes cutaneous wound healing of chronically stressed mice through inhibition of TNF-α and IDO activation. PLoS One. 10: e0128439.
Bitzer-Quintero, OK; Dávalos-Marín, AJ; Ortiz, GG; del Angel Meza, AR; Torres-Mendoza, BM; Robles, RG; Huerta, VC and Beas-Zárate, C (2010). Antioxidant activity of tryptophan in rats under experimental endotoxic shock. Biomed. Pharmacother., 64: 77-81.
Buyse, J; Geypens, B; Malheiros, RD; Moraes, VM; Swennen, Q and Decuypere, E (2004). Assessment of age-related glucose oxidation rates of broiler chickens by using stable isotopes. Life Sci., 75: 2245-2255.
Chi, TC; Ho, YJ; Chen, WP; Chi, TL; Lee, SS; Cheng, JT and Su, MJ (2007). Serotonin enhances beta-endorphin secretion to lower plasma glucose in streptozotocin-induced diabetic rats. Life Sci., 80: 1832-1838.
Chowdhury, VS; Han, G; Bahry, MA; Tran, PV; Do, PH; Yang, H and Furuse, M (2017). L-Citrulline acts as potential hypothermic agent to afford thermotolerance in chicks. J. Therm. Biol., 69: 163-170.
Chowdhury, VS; Tomonaga, S; Ikegami, T; Erwan, E; Ito, K; Cockrem, JF and Furuse, M (2014). Oxidative damage and brain concentrations of free amino acid in chicks exposed to high ambient temperature. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 169: 70-76.
Chowdhury, VS; Tomonaga, S; Nishimura, S; Tabata, S; Cockrem, JF; Tsutsui, K and Furuse, M (2012). Hypothalamic gonadotropin-inhibitory hormone precursor mRNA is increased during depressed food intake in heat-exposed chicks. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 162: 227-233.
Denbow, DM; Van Krey, H and Cherry, J (1982). Feeding and drinking response of young chicks to injections of serotonin into the lateral ventricle of the brain. Poult. Sci., 61: 150-155.
El-Merahbi, R; Loffler, M; Mayer, A and Sumara, G (2015). The roles of peripheral serotonin in metabolic homeostasis. FEBS Lett., 589: 1728-1734.
Erwan, E; Chowdhury, VS; Nagasawa, M; Goda, R; Otsuka, T; Yasuo, S and Furuse, M (2014). Oral administration of D-aspartate, but not L-aspartate, depresses rectal temperature and alters plasma metabolites in chicks. Life Sci., 109: 65-71.
Govaerts, T; Room, G; Buyse, J; Lippens, M; De Groote, G and Decuypere, E (2000). Early and temporary quantitative food restriction of broiler chickens. 2. Effects on allometric growth and growth hormone secretion. Br. Poult. Sci., 41: 355-362.
Han, G; Yang, H; Bungo, T; Ikeda, H; Wang, Y; Nguyen, LT; Eltahan, HM; Furuse, M and Chowdhury, VS (2018). In ovo L-leucine administration stimulates lipid metabolisms in heat-exposed male, but not female, chicks to afford thermotolerance. J. Therm. Biol., 71: 74-82.
Ito, K; Bahry, MA; Hui, Y; Furuse, M and Chowdhury, VS (2015). Acute heat stress up-regulates neuropeptide Y precursor mRNA expression and alters brain and plasma concentrations of free amino acids in chicks. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 187: 13-19.
Ito, K; Erwan, E; Nagasawa, M; Furuse, M and Chowdhury, VS (2014). Changes in free amino acid concentrations in the blood, brain and muscle of heat-exposed chicks. Br. Poult. Sci., 55: 644-652.
Kaps, M and Lamberson, WR (2017). Biostatistics for animal science. Cabi. PP: 365-383.
Khattak, F and Helmbrecht, A (2018). Effect of different levels of tryptophan on productive performance, egg quality, blood biochemistry, and caecal microbiota of hens housed in enriched colony cages under commercial stocking density. Poult. Sci., 98: 2094-2104.
Kujundžić, RN and Lowenthal, JW (2008). The role of tryptophan metabolism in iNOS transcription and nitric oxide production by chicken macrophage cells upon treatment with interferon gamma. Immunol. Lett., 115: 153-159.
Lacy, M; Van Krey, H; Skewes, P and Denbow, M (1986). Tryptophan’s influence on feeding and body temperature in the fowl. Poult. Sci., 65: 1193-1196.
Lin, H; Decuypere, E and Buyse, J (2004). Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 2. Short-term effect. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 139: 745-751.
Lin, H; Decuypere, E and Buyse, J (2006). Acute heat stress induces oxidative stress in broiler chickens. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 144: 11-17.
Liu, Y; Yuan, J; Zhang, L; Zhang, Y; Cai, S; Yu, J and Xia, Z (2015). Effects of tryptophan supplementation on growth performance, antioxidative activity, and meat quality of ducks under high stocking density. Poult. Sci., 94: 1894-1901.
Mardones, O; Devia, E; Labbé, B; Oyarzún, R; Vargas-Chacoff, L and Muñoz, J (2018). Effect of L-tryptophan and melatonin supplementation on the serotonin gastrointestinal content and digestive enzymatic activity for Salmo salar and Oncorhynchus kisutch. Aquaculture. 482: 203-210.
Mellor, AL and Munn, DH (1999). Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol. Today. 20: 469-473.
Moon, RJ and Berry, LJ (1968). Effect of tryptophan and selected analogues on body temperature of endotoxin-poisoned mice. J. Bacteriol., 95: 764-770.
Moraes, V; Malheiros, R; Bruggeman, V; Collin, A; Tona, K; Van As, P; Onagbesan, O; Buyse, J; Decuypere, E and Macari, M (2004). The effect of timing of thermal conditioning during incubation on embryo physiological parameters and its relationship to thermotolerance in adult broiler chickens. J. Therm. Biol., 29: 55-61.
Nakagawa, H; Matsumura, T; Suzuki, K; Ninomiya, C and Ishiwata, T (2016). Changes of brain monoamine levels and physiological indexes during heat acclimation in rats. J. Therm. Biol., 58: 15-22.
Nonogaki, K; Kaji, T and Murakami, M (2018). A tryptophan hydroxylase inhibitor decreases hepatic FGF21 expression and circulating FGF21 in mice fed a high-fat diet. Neuropsychiatry. 8: 372-377.
Oshima, S; Shiiya, S and Nakamura, Y (2019). Combined supplementation with glycine and tryptophan reduces purine-induced serum uric acid elevation by accelerating urinary uric acid excretion: A randomized, single-blind, placebo-controlled, crossover study. Nutrients. 11: 2562-2569.
Pan, L; Zhao, P; Ma, X; Shang, Q; Long, S; Wu, Y; Wang, W and Piao, X (2018). Forsythia suspensa extract protects broilers against breast muscle oxidative injury induced by corticosterone mimicked pre-slaughter acute stress. Poult. Sci., 97: 2095-2105.
Paredes, SD; Terron, M; Cubero, J; Valero, V; Barriga, C; Reiter, RJ and Rodriguez, AB (2007). Tryptophan increases nocturnal rest and affects melatonin and serotonin serum levels in old ringdove. Physiol. Behav., 90: 576-582.
Piestun, Y; Shinder, D; Ruzal, M; Halevy, O and Yahav, S (2008). The effect of thermal manipulations during the development of the thyroid and adrenal axes on in-hatch and post-hatch thermoregulation. J. Therm. Biol., 33: 413-418.
Sahin, K; Sahin, N and Kucuk, O (2003). Effects of chromium, and ascorbic acid supplementation on growth, carcass traits, serum metabolites, and antioxidant status of broiler chickens reared at a high ambient temperature (32 C). Nutr. Res., 23: 225-238.
Shan, A; Sterling, K; Pesti, G; Bakalli, R; Driver, J and Tejedor, A (2003). The influence of temperature on the threonine and tryptophan requirements of young broiler chicks. Poult. Sci., 82: 1154-1162.
Shea, MM; Douglass, LW and Mench, JA (1991). The interaction of dominance status and supplemental tryptophan on aggression in Gallus domesticus males. Pharmacol. Biochem. Behav., 38: 587-591.
Song, Z; Liu, L; Sheikhahmadi, A; Jiao, H and Lin, H (2012a). Effect of heat exposure on gene expression of feed intake regulatory peptides in laying hens. J. Biomed. Biotechnol., 48: 48-69.
Song, Z; Liu, L; Yue, Y; Jiao, H; Lin, H; Sheikhahmadi, A; Everaert, N; Decuypere, E and Buyse, J (2012b). Fasting
alters protein expression of AMP-activated protein kinase in the hypothalamus of broiler chicks (Gallus gallus domesticus). Gen. Comp. Endocrinol., 178: 546-555.
Sun, X; Zhang, H; Sheikhahmadi, A; Wang, Y; Jiao, H; Lin, H and Song, Z (2015). Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (Gallus gallus domesticus). Int. J. Biometeorol., 59: 127-135.
Tanke, MA; Alserda, E; Doornbos, B; van der Most, PJ; Goeman, K; Postema, F and Korf, J (2008). Low tryptophan diet increases stress-sensitivity, but does not affect habituation in rats. Neurochem. Int., 52: 272-281.
Tran, PV; Chowdhury, VS; Do, PH; Bahry, MA; Yang, H and Furuse, M (2016). L-Ornithine is a potential acute satiety signal in the brain of neonatal chicks. Physiol. Behav., 155: 141-148.
Wang, S; Ni, Y; Guo, F; Sun, Z; Ahmed, A and Zhao, R (2014). Differential expression of hypothalamic fear- and stress-related genes in broiler chickens showing short or long tonic immobility. Domest. Anim. Endocrinol., 47: 65-72.
Watanabe, H; Akasaka, D; Ogasawara, H; Sato, K; Miyake, M; Saito, K; Takahashi, Y; Kanaya, T; Takakura, I and Hondo, T (2010). Peripheral serotonin enhances lipid metabolism by accelerating bile acid turnover. Endocrinology. 151: 4776-4786.
Yoshida, J; Erwan, E; Chowdhury, VS; Ogino, Y; Shigemura, A; Denbow, DM and Furuse, M (2015). Comparison of centrally injected tryptophan-related substances inducing sedation in acute isolation stress-induced neonatal chicks. Pharmacol. Biochem. Behav., 129: 1-6.
Yoshida, J; Shigemura, A; Ogino, Y; Denbow, DM and Furuse, M (2013). Two receptors are involved in the central functions of kynurenic acid under an acute stress in neonatal chicks. Neuroscience. 248: 194-200.
Zhao, J; Jiao, H; Song, Z and Lin, H (2009). Effects of L-arginine supplementation on glucose and nitric oxide (NO) levels and activity of NO synthase in corticosterone-challenged broiler chickens (Gallus gallus). Comp. Biochem. Physiol. C Toxicol. Pharmacol., 150: 474-480.