Dietary supplementation with tryptophan increases the plasma concentrations of tryptophan, kynurenine, and melatonin in Yili mares
Wenjie Zhang A # , Guodong Zhao A # , Xiaobin Li A , Ming Han A , Shiqi Zhang A , Haifeng Deng B and Kailun Yang A # *A
B
Handling Editor: Chris Rogers
Abstract
Tryptophan (Trp) is the precursor of melatonin (MT) and the latter plays vital physiological roles in mares.
The purpose of this experiment was to investigate the effects of dietary Trp supplementation on the plasma Trp, kynurenine (Kyn), 5-hydroxytryptophan (5-HT), and melatonin (MT) concentrations in female Yili horses.
Twenty Yili mares aged 2 years with mean bodyweight (BW) of 263.5 ± 14.77 kg and of similar stature were selected and randomly allocated to the control (CON; basal diet), basal diet plus Trp at 20 mg/kg BW (TRP1), basal diet plus Trp at 40 mg/kg BW (TRP2), or basal diet plus Trp at 60 mg/kg BW (TRP3) group.
The plasma total Trp, Kyn, and MT concentrations in all Trp groups steadily increased, reached their peak values, and gradually decreased after Trp supplementation between 0 h and 12 h. However, the plasma 5-HT concentration displayed the opposite trend. Peak plasma total Trp and 5-HT concentrations were attained between 1 h and 3 h, while those of KYN and MT appeared between 4 h and 6 h after Trp supplementation. The plasma total Trp and Kyn concentrations were significantly higher in TRP2 and TRP3 than in CON between 1 h and 12 h (P < 0.05) after Trp supplementation. The plasma 5-HT concentration was significantly (P < 0.05) lower in TRP1 than in CON at 3 h, 4 h, 6 h, 9 h, and 12 h after Trp supplementation. The plasma MT concentrations in TRP1 and TRP2 were significantly (P < 0.05) higher than in CON at 3 h, 4 h, and 12 h, and at 0 h, 1 h, and 12 h after Trp supplementation (P < 0.05).
Dietary Trp supplementation can increase the plasma total Trp, Kyn, and MT concentrations in Yili mares and the optimal Trp dosage was 20 mg/kg BW.
The addition of Trp to a basal diet or feed may increase the plasma total Trp, Kyn, and MT concentrations in female horses.
Keywords: 5-hydroxytryptophan, growth performance, kynurenine, melatonin, plasma concentration, supplementation, tryptophan, Yili mares.
References
Akiyama T, Carstens IM, Carstens E (2010) Enhanced scratching evoked by PAR-2 agonist and 5-HT but not histamine in a mouse model of chronic dry skin itch. Pain 151(2), 378-383.
| Crossref | Google Scholar | PubMed |
Alberghina D, Giannetto C, Visser EK, Ellis AD (2010) Effect of diet on plasma tryptophan and serotonin in trained mares and geldings. Veterinary Record 166(5), 133-136.
| Crossref | Google Scholar | PubMed |
Apolônio LR, Donzele JL, Oliveira RFMd, Saraiva A, Silva FCdO, Ferreira AS, Lima AL, Kill JL (2011) Digestible tryptophan levels in diets for pigs weighing 15 to 30 kg. Revista Brasileira de Zootecnia 40(8), 1706-1711.
| Crossref | Google Scholar |
Backhaus C, Rahman H, Scheffler S, Laatsch H, Hardeland R (2008) NO scavenging by 3-hydroxyanthranilic acid and 3-hydroxykynurenine: N-nitrosation leads via oxadiazoles to o-quinone diazides. Nitric Oxide 19(3), 237-244.
| Crossref | Google Scholar | PubMed |
Backström T, Winberg S (2017) Serotonin coordinates responses to social stress – what we can learn from fish. Frontiers in Neuroscience 11, 595.
| Crossref | Google Scholar |
Badawy AA-B, Smith MJH (1972) Changes in liver tryptophan and tryptophan pyrrolase activity after administration of salicylate and tryptophan to the rat. Biochemical Pharmacology 21(1), 97-101.
| Crossref | Google Scholar | PubMed |
Bagshaw CS, Ralston SL, Fisher H (1994) Behavioral and physiological effect of orally administered tryptophan on horses subjected to acute isolation stress. Applied Animal Behaviour Science 40(1), 1-12.
| Crossref | Google Scholar |
Bai M, Liu H, Xu K, Oso AO, Wu X, Liu G, Tossou MCB, Al-Dhabi NA, Duraipandiyan V, Xi Q, Yin Y (2017) A review of the immunomodulatory role of dietary tryptophan in livestock and poultry. Amino Acids 49(1), 67-74.
| Crossref | Google Scholar | PubMed |
Birkl P, Kjaer JB, Szkotnicki W, Forsythe P, Harlander-Matauschek A (2017) Acute tryptophan depletion: the first method validation in an avian species (Gallus gallus domesticus). Poultry Science 96(9), 3021-3025.
| Crossref | Google Scholar | PubMed |
Bondarenko LA (2004) Role of methionine in nocturnal melatonin peak in the pineal gland. Bulletin of Experimental Biology and Medicine 137(5), 431-432.
| Crossref | Google Scholar | PubMed |
Bubenik GA, Pang SF, Hacker RR, Smith PS (1996) Melatonin concentrations in serum and tissues of porcine gastrointestinal tract and their relationship to the intake and passage of food. Journal of Pineal Research 21(4), 251-256.
| Crossref | Google Scholar | PubMed |
Cabañas R, López-Serrano MC, Carreira J, Ventas P, Polo F, Caballero MT, Contreras J, Barranco P, Moreno-Ancillo A (2000) Importance of albumin in cross-reactivity among cat, dog and horse allergens. Journal of Investigational Allergology & Clinical Immunology 10(2), 71-77.
| Google Scholar | PubMed |
Cervenka I, Agudelo LZ, Ruas JL (2017) Kynurenines: tryptophan’s metabolites in exercise, inflammation, and mental health. Science 357(6349), eaaf9794.
| Crossref | Google Scholar |
Chung TK, Gelberg HB, Dorner JL, Baker DH (1991) Safety of L-tryptophan for pigs. Journal of Animal Science 69(7), 2955-2960.
| Crossref | Google Scholar | PubMed |
Davis BP, Engle TE, Ransom JI, Grandin T (2017) Preliminary evaluation on the effectiveness of varying doses of supplemental tryptophan as a calmative in horses. Applied Animal Behaviour Science 188, 34-41.
| Crossref | Google Scholar |
Dolivo DM, Larson SA, Dominko T (2018) Tryptophan metabolites kynurenine and serotonin regulate fibroblast activation and fibrosis. Cellular and Molecular Life Sciences 75(20), 3663-3681.
| Crossref | Google Scholar | PubMed |
Eder K, Nonn H, Kluge H, Peganova S (2003) Tryptophan requirement of growing pigs at various body weights. Journal of Animal Physiology and Animal Nutrition 87(9-10), 336-346.
| Crossref | Google Scholar | PubMed |
Esteban S, Nicolaus C, Garmundi A, Rial RV, Rodríguez AB, Ortega E, Ibars CB (2004) Effect of orally administered l-tryptophan on serotonin, melatonin, and the innate immune response in the rat. Molecular and Cellular Biochemistry 267(1), 39-46.
| Crossref | Google Scholar |
Felsing DE, Anastasio NC, Miszkiel JM, Gilbertson SR, Allen JA, Cunningham KA (2018) Biophysical validation of serotonin 5-HT2A and 5-HT2C receptor interaction. PLoS ONE 13(8), e0203137.
| Crossref | Google Scholar | PubMed |
Fitzgerald BP, McManus CJ (2000) Photoperiodic versus metabolic signals as determinants of seasonal anestrus in the mare. Biology of Reproduction 63(1), 335-340.
| Crossref | Google Scholar | PubMed |
Gelpi M, Vestad B, Raju SC, Hansen SH, Høgh J, Midttun Ø, Ueland PM, Ueland T, Benfield T, Kofoed KF, Hov JR, Trøseid M, Nielsen SD (2022) Association of the kynurenine pathway of tryptophan metabolism with Human Immunodeficiency Virus-related gut microbiota alterations and visceral adipose tissue accumulation. The Journal of Infectious Diseases 225, 1948-1954.
| Crossref | Google Scholar | PubMed |
González Esquivel D, Ramírez-Ortega D, Pineda B, Castro N, Ríos C, Pérez de la Cruz V (2017) Kynurenine pathway metabolites and enzymes involved in redox reactions. Neuropharmacology 112, 331-345.
| Crossref | Google Scholar |
Goo D, Kim JH, Park GH, Delos Reyes JB, Kil DY (2019) Effect of stocking density and dietary tryptophan on growth performance and intestinal barrier function in broiler chickens. Poultry Science 98(10), 4504-4508.
| Crossref | Google Scholar | PubMed |
Guerin MV, Deed JR, Kennaway DJ, Matthews CD (1995) Plasma melatonin in the horse: measurements in natural photoperiod and in acutely extended darkness throughout the year. Journal of Pineal Research 19(1), 7-15.
| Crossref | Google Scholar | PubMed |
Hajak G, Huether G, Blanke J, Blömer M, Freyer C, Poeggeler B, Reimer A, Rodenbeck A, Schulz-Varszegi M, Rüther E (1991) The influence of intravenous L-tryptophan on plasma melatonin and sleep in men. Pharmacopsychiatry 24(01), 17-20.
| Crossref | Google Scholar |
Hankins J (2006) The role of albumin in fluid and electrolyte balance. Journal of Infusion Nursing 29(5), 260-265.
| Crossref | Google Scholar | PubMed |
Hardeland R (2012) Melatonin in aging and disease – multiple consequences of reduced secretion, options and limits of treatment. Aging and Disease 3(2), 194-225.
| Google Scholar | PubMed |
Haritou SJA, Zylstra R, Ralli C, Turner S, Tortonese DJ (2008) Seasonal changes in circadian peripheral plasma concentrations of melatonin, serotonin, dopamine and cortisol in aged horses with Cushing’s disease under natural photoperiod. Journal of Neuroendocrinology 20(8), 988-996.
| Crossref | Google Scholar | PubMed |
Herichová I, Zeman M, Veselovský J (1998) Effect of tryptophan administration of melatonin concentrations in the pineal gland, plasma and gastrointestinal tract of chickens. Acta Veterinaria Brno 67(2), 89-95.
| Crossref | Google Scholar |
Kapoor D, Jain R, Kaur I, Soni N (2014) Melatonin as a potent antioxidant – a review. Indian Journal of Dental Sciences 6, 102-106.
| Google Scholar |
Kwon WB, Soto JA, Stein HH (2022) Effects of dietary leucine and tryptophan on serotonin metabolism and growth performance of growing pigs. Journal of Animal Science 100(1), skab356.
| Crossref | Google Scholar |
Leathwood PD (1987) Tryptophan availability and serotonin synthesis. Proceedings of the Nutrition Society 46(1), 143-156.
| Crossref | Google Scholar |
Lindquist C, Bjørndal B, Lund A, Slettom G, Skorve J, Nygård O, Svardal A, Berge RK (2020) Increased fatty acid oxidation and mitochondrial proliferation in liver are associated with increased plasma kynurenine metabolites and nicotinamide levels in normolipidemic and carnitine-depleted rats. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 1865(2), 158543.
| Crossref | Google Scholar |
Liu X-H, Zhai X-Y (2021) Role of tryptophan metabolism in cancers and therapeutic implications. Biochimie 182, 131-139.
| Crossref | Google Scholar | PubMed |
Liu HN, Hu C-AA, Bai MM, Liu G, Tossou MCB, Xu K, Li FN, Liao P, Kong XF, Wu X, Yin YL (2017) Short-term supplementation of isocaloric meals with l-tryptophan affects pig growth. Amino Acids 49, 2009-2014.
| Crossref | Google Scholar |
Liu N, Ji Y, Yang Y, Jia H, Si X, Jiang D, Zhang Y, Dai Z, Wu Z (2021) Impact of dietary crude protein level on hepatic lipid metabolism in weaned female piglets. Animals 11(6), 1829.
| Crossref | Google Scholar | PubMed |
Liu S, Xu J-Z, Zhang W-G (2022) Advances and prospects in metabolic engineering of Escherichia coli for L-tryptophan production. World Journal of Microbiology and Biotechnology 38(2), 22.
| Crossref | Google Scholar |
Mándi Y, Vécsei L (2012) The kynurenine system and immunoregulation. Journal of Neural Transmission 119(2), 197-209.
| Crossref | Google Scholar | PubMed |
Marrero MG, Dado-Senn B, Field SL, da Silva DR, Skibiel AL, Laporta J (2019) Increasing serotonin bioavailability in preweaned dairy calves impacts hematology, growth, and behavior. Domestic Animal Endocrinology 69, 42-50.
| Crossref | Google Scholar | PubMed |
Matte JJ, LeFloc’h N, Primot Y, Lessard M (2011) Interaction between dietary tryptophan and pyridoxine on tryptophan metabolism, immune responses and growth performance in post-weaning pigs. Animal Feed Science and Technology 170(3-4), 256-264.
| Crossref | Google Scholar |
Minakata K, Fukushima K, Nakamura M, Iwahashi H (2011) Effect of some naturally occurring iron ion chelators on the formation of radicals in the reaction mixtures of rat liver microsomes with ADP, Fe3+ and NADPH. Journal of Clinical Biochemistry and Nutrition 49(3), 207-215.
| Crossref | Google Scholar | PubMed |
Møller SE (1981) Pharmacokinetics of tryptophan, renal handling of kynurenine and the effect of nicotinamide on its appearance in plasma and urine following L-tryptophan loading of healthy subjects. European Journal of Clinical Pharmacology 21(2), 137-142.
| Crossref | Google Scholar | PubMed |
Myint A-M, Kim Y-K (2014) Network beyond IDO in psychiatric disorders: revisiting neurodegeneration hypothesis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 48, 304-313.
| Crossref | Google Scholar |
Nishizuka Y, Hayaishi O (1963) Enzymic synthesis of niacin nucleotides from 3-hydroxyanthranilic acid in mammalian liver. Journal of Biological Chemistry 238(1), PC483-PC485.
| Crossref | Google Scholar |
Pevet P, Challet E (2011) Melatonin: both master clock output and internal time-giver in the circadian clocks network. Journal of Physiology-Paris 105(4-6), 170-182.
| Crossref | Google Scholar | PubMed |
Pláteník J, Stopka P, Vejražka M, Štípek S (2001) Quinolinic acid – iron(II) complexes: slow autoxidation, but enhanced hydroxyl radical production in the Fenton reaction. Free Radical Research 34(5), 445-459.
| Crossref | Google Scholar | PubMed |
Reiter RJ (1993) The melatonin rhythm: both a clock and a calendar. Experientia 49(8), 654-664.
| Crossref | Google Scholar | PubMed |
Sánchez S, Sánchez CL, Paredes SD, Rodriguez AB, Barriga C (2008) The effect of tryptophan administration on the circadian rhythms of melatonin in plasma and the pineal gland of rats. Journal of Applied Biomedicine 6(4), 177-186.
| Crossref | Google Scholar |
Sliwinski T, Rozej W, Morawiec-Bajda A, Morawiec Z, Reiter R, Blasiak J (2007) Protective action of melatonin against oxidative DNA damage – chemical inactivation versus base-excision repair. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 634(1-2), 220-227.
| Crossref | Google Scholar |
Soumeh EA, van Milgen J, Sloth NM, Corrent E, Poulsen HD, Nørgaard JV (2015) Requirement of standardized ileal digestible valine to lysine ratio for 8- to 14-kg pigs. Animal 9(8), 1312-1318.
| Crossref | Google Scholar | PubMed |
Spohn SN, Mawe GM (2017) Non-conventional features of peripheral serotonin signaling – the gut and beyond. Nature Reviews Gastroenterology & Hepatology 14(7), 412-420.
| Crossref | Google Scholar | PubMed |
Terhaar HM, Allbaugh RA, Mochel JP, Sebbag L (2021) Serum albumin and total protein concentration in the tear film of horses with healthy or diseased eyes. Veterinary Ophthalmology 24(1), 20-27.
| Crossref | Google Scholar | PubMed |
Valente EEL, Klotz JL, Ahn G, Harmon DL (2021) Pattern of postruminal administration of l-tryptophan affects blood serotonin in cattle. Domestic Animal Endocrinology 74, 106574.
| Crossref | Google Scholar | PubMed |
Voigt J-P, Schade R, Fink H, Hörtnagl H (2002) Role of 5-HT1A receptors in the control of food intake in obese Zucker rats of different ages. Pharmacology Biochemistry and Behavior 72(1-2), 403-409.
| Crossref | Google Scholar | PubMed |
Walsh HA, Daya S (1997) Inhibition of hepatic tryptophan-2,3-dioxygenase: superior potency of melatonin over serotonin. Journal of Pineal Research 23(1), 20-23.
| Crossref | Google Scholar | PubMed |
Zapata RC, Singh A, Pezeshki A, Nibber T, Chelikani PK (2017) Whey protein components –lactalbumin and lactoferrin – improve energy balance and metabolism. Scientific Reports 7(1), 9917.
| Crossref | Google Scholar |
Zhang X, He Y, Ding M (2009) Simultaneous determination of tryptophan and kynurenine in plasma samples of children patients with Kawasaki disease by high-performance liquid chromatography with programmed wavelength ultraviolet detection. Journal of Chromatography B 877(16-17), 1678-1682.
| Crossref | Google Scholar |
Zhao F, Ma C, Zhao G, Wang G, Li X, Yang K (2019) Rumen-protected 5-hydroxytryptophan improves sheep melatonin synthesis in the pineal gland and intestinal tract. Medical Science Monitor 25, 3605-3616.
| Crossref | Google Scholar | PubMed |