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Responses of growth performance and tryptophan metabolism to oxidative stress induced by diquat in weaned pigs

Published online by Cambridge University Press:  06 December 2011

M. Lv ,
B. Yu ,
X. B. Mao ,
P. Zheng ,
J. He  and
D. W. Chen
M. Lv
Affiliation:
Key Laboratory of Animal Disease-Resistance Nutrition, Institute of Animal Nutrition, Sichuan Agricultural University, Ministry of Education, Yaan, Sichuan 625014, P. R. China
B. Yu
Affiliation:
Key Laboratory of Animal Disease-Resistance Nutrition, Institute of Animal Nutrition, Sichuan Agricultural University, Ministry of Education, Yaan, Sichuan 625014, P. R. China
X. B. Mao
Affiliation:
Key Laboratory of Animal Disease-Resistance Nutrition, Institute of Animal Nutrition, Sichuan Agricultural University, Ministry of Education, Yaan, Sichuan 625014, P. R. China
P. Zheng
Affiliation:
Key Laboratory of Animal Disease-Resistance Nutrition, Institute of Animal Nutrition, Sichuan Agricultural University, Ministry of Education, Yaan, Sichuan 625014, P. R. China
J. He
Affiliation:
Key Laboratory of Animal Disease-Resistance Nutrition, Institute of Animal Nutrition, Sichuan Agricultural University, Ministry of Education, Yaan, Sichuan 625014, P. R. China
D. W. Chen*
Affiliation:
Key Laboratory of Animal Disease-Resistance Nutrition, Institute of Animal Nutrition, Sichuan Agricultural University, Ministry of Education, Yaan, Sichuan 625014, P. R. China
*
†E-mail: daiwenc@yahoo.com
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Abstract

During many pathological conditions, the tryptophan concentration in blood may be reduced. However, the effects of oxidative stress on tryptophan metabolism remain unknown. In this study, we investigated the effects of oxidative stress on growth performance and tryptophan metabolism in weaned pigs. A total of 24 weaned pigs were assigned to one of three treatments that included pigs fed ad libitum (control), pigs challenged with diquat at a dose of 10 mg/kg BW and fed ad libitum (oxidative stress) or pigs pair-fed to receive the same amount of feed as the diquat-challenged pigs. The trial lasted for 7 days. The growth performance and activities of antioxidant enzymes were declined in diquat-challenged pigs. The diquat challenge decreased the tryptophan concentration in serum and the 5-hydroxytryptamine concentration in the hypothalamus, and increased large neutral amino acids, kynurenine (Kyn) and malondialdehyde in serum. The 544-bp porcine partial mRNA sequence of the tryptophan 2,3-dioxygenase (TDO) gene was obtained according to the conserved region in the human gene sequence. In addition, the oxidative stress induced by the diquat challenge stimulated TDO-relative mRNA abundance in the liver and γ-glutamyl transpeptidase activity in intestinal mucosa, but did not affect the mRNA levels of Na+-neutral amino acid transporter B0. These results suggested that oxidative stress induced by diquat depressed growth performance and increased metabolism of tryptophan via Kyn pathway that upregulated TDO mRNA expression in weaned pigs.

Keywords

pigsoxidative stresstryptophan metabolismtryptophan 2,3-dioxygenase
Type
Full Paper
Information
animal , Volume 6 , Issue 6 , June 2012 , pp. 928 - 934
Copyright
Copyright © The Animal Consortium 2011

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References

Anthony, TG, Reiter, AK, Anthony, JC, Kimball, SR, Jefferson, LS 2001. Deficiency of dietary EAA preferentially inhibits mRNA translation of ribosomal proteins in liver of meal-fed rats. American Journal of Physiology – Endocrinology and Metabolism 281, E430–E439.CrossRefGoogle ScholarPubMed
Beckman, KB, Ames, BN 1998. The free radical theory of aging matures. Physiological Reviews 78, 547–581.CrossRefGoogle ScholarPubMed
Dairam, A, Antunes, E, Saravanan, K, Daya, S 2006. Non-steroidal anti-inflammatory agents, tolmetin and sulindac, inhibit liver tryptophan 2,3-dioxygenase activity and alter brain neurotransmitter levels. Life Sciences 79, 2269–2274.Google Scholar
Diksic, M, Young, SN 2001. Study of the brain serotonergic system with labeled alpha-methyl-l-tryptophan. Journal of Neurochemistry 78, 1185–1200.CrossRefGoogle ScholarPubMed
Fernstrom, JD 2005. Branched-chain amino acids and brain function. Journal of Nutrition 135, 1539S–1546S.CrossRefGoogle ScholarPubMed
Freedman, DX, Belendiuk, K, Belendiuk, GW, Crayton, JW 1981. Blood tryptophan metabolism in chronic schizophrenics. Archives of General Psychiatry 38, 655–659.Google Scholar
Fu, Y, Cheng, WH, Porres, JM, Ross, DA, Lei, XG 1999. Knockout of cellular glutathione peroxidase gene renders mice susceptible to diquat-induced oxidative stress. Free Radical Biology and Medicine 27, 605–611.CrossRefGoogle ScholarPubMed
Gallagher, EP, Buetler, TM, Stapleton, PL, Wang, C, Stahl, DL, Eaton, DL 1995. The effects of diquat and ciprofibrate on mRNA expression and catalytic activities of hepatic xenobiotic metabolizing and antioxidant enzymes in rat liver. Toxicology and Applied Pharmacology 134, 81–91.Google Scholar
Gutteridge, JM 1995. Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clinical Chemistry 41, 1819–1828.Google Scholar
Guzik, AC, Matthews, JO, Kerr, BJ, Bidner, TD, Southern, LL 2006. Dietary tryptophan effects on plasma and salivary cortisol and meat quality in pigs. Journal of Animal Science 84, 2251–2259.Google Scholar
Hawkins, RA, O'Kane, RL, Simpson, IA, Vina, JR 2006. Structure of the blood–brain barrier and its role in the transport of amino acids. Journal of Nutrition 136, 218S–226S.Google Scholar
Henry, Y, Seve, B, Colleaux, Y, Ganier, P, Saligaut, C, Jego, P 1992. Interactive effects of dietary levels of tryptophan and protein on voluntary feed intake and growth performance in pigs, in relation to plasma free amino acids and hypothalamic serotonin. Journal of Animal Science 70, 1873–1887.Google Scholar
Koopmans, SJ, Guzik, AC, van der Meulen, J, Dekker, R, Kogut, J, Kerr, BJ, Southern, LL 2006. Effects of supplemental l-tryptophan on serotonin, cortisol, intestinal integrity, and behavior in weanling piglets. Journal of Animal Science 84, 963–971.Google Scholar
Kumar, S 2004. Changes in rat brain regions serotoninergic system following acephate poisoning. Pesticide Biochemistry and Physiology 78, 140–150.Google Scholar
Lestaevel, P, Romero, E, Dhieux, B, Ben Soussan, H, Berradi, H, Dublineau, I, Voisin, P, Gourmelon, P 2009. Different pattern of brain pro-/anti-oxidant activity between depleted and enriched uranium in chronically exposed rats. Toxicology 258, 1–9.CrossRefGoogle ScholarPubMed
Lightfoot, T, Skibola, C, Smith, A, Forrest, M, Adamson, P, Morgan, G, Bracci, P, Roman, E, Smith, M, Holly, E 2006. Polymorphisms in the oxidative stress genes, superoxide dismutase, glutathione peroxidase and catalase and risk of non-Hodgkin's lymphoma. Haematologica 91, 1222–1227.Google ScholarPubMed
Makino, N, Mochizuki, Y, Bannai, S, Sugita, Y 1994. Kinetic studies on the removal of extracellular hydrogen peroxide by cultured fibroblasts. Journal of Biological Chemistry 269, 1020–1025.CrossRefGoogle ScholarPubMed
Mates, JM, Sanchez-Jimenez, F 1999. Antioxidant enzymes and their implications in pathophysiologic processes. Frontiers in Bioscience 4, D339–D345.CrossRefGoogle ScholarPubMed
Melchior, D, Le Floc'h, N, Seve, B 2003. Effects of chronic lung inflammation on tryptophan metabolism in piglets. Advances in Experimental Medicine and Biology 527, 359–362.CrossRefGoogle ScholarPubMed
National Research Council (NRC) 1998. Nutrient requirement of swine, 10th edition. National Academy Press, Washington, DC, USA.Google Scholar
Osburn, WO, Wakabayashi, N, Misra, V, Nilles, T, Biswal, S, Trush, MA, Kensler, TW 2006. Nrf2 regulates an adaptive response protecting against oxidative damage following diquat-mediated formation of superoxide anion. Archives of Biochemistry and Biophysics 454, 7–15.Google Scholar
Palacin, M, Estevez, R, Bertran, J, Zorzano, A 1998. Molecular biology of mammalian plasma membrane amino acid transporters. Physiological Reviews 78, 969–1054.Google Scholar
Pfaffl, MW 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.Google Scholar
Romeu, M, Mulero, M, Giralt, M, Folch, J, Nogues, MR, Torres, A, Fortuno, A, Sureda, FX, Cabre, M, Paternain, JL, Mallol, J 2002. Parameters related to oxygen free radicals in erythrocytes, plasma and epidermis of the hairless rat. Life Sciences 71, 1739–1749.CrossRefGoogle ScholarPubMed
Schallreuter, KU, Gibbons, NC, Zothner, C, Abou Elloof, MM, Wood, JM 2007. Hydrogen peroxide-mediated oxidative stress disrupts calcium binding on calmodulin: more evidence for oxidative stress in vitiligo. Biochemical and Biophysical Research Communications 360, 70–75.CrossRefGoogle ScholarPubMed
Slaughter, MR, Thakkar, H, O'Brien, PJ 2002. Effect of diquat on the antioxidant system and cell growth in human neuroblastoma cells. Toxicology and Applied Pharmacology 178, 63–70.Google Scholar
Slavic, M, Appiah, I, Nikolic-Kokic, A, Radojicic, R, Jones, DR, Spasic, MB, Milovanovic, S, Blagojevic, D 2006. The anti-oxidative defence system in the isolated rat uterus during spontaneous rhythmic activity. Acta Physiologica Hungarica 93, 335–339.Google Scholar
Vina, JR, Palacin, M, Puertes, IR, Hernandez, R, Vina, J 1989. Role of the gamma-glutamyl cycle in the regulation of amino acid translocation. American Journal of Physiology 257, E916–E922.Google Scholar
Wozniak, A, Drewa, G, Wozniak, B, Schachtschabel, DO 2004. Activity of antioxidant enzymes and concentration of lipid peroxidation products in selected tissues of mice of different ages, both healthy and melanoma-bearing. Zeitschrift für Gerontologie und Geriatrie 37, 184–189.Google Scholar
Yang, CB, Wang, ZR, Yin, YL, Yang, XJ, Pluske, JR, Fan, ZM 2006. The neutral amino acid transporter B0 gene is up-regulated in the jejunal villus cells compared to crypt cells measured by quantitative real-time RT-PCR in formula-fed neonatal pigs. FASEB Journal 20, A1044.Google Scholar
Yuan, SB, Chen, DW, Zhang, KY, Yu, B 2007. Effects of oxidative stress on growth performance, nutrient digestibilities and activities of antioxidative enzymes of weanling pigs. Asian-Australasian Journal of Animal Sciences 20, 1600–1605.Google Scholar
Zhang, H, Forman, HJ, Choi, J 2005. Gamma-glutamyl transpeptidase in glutathione biosynthesis. Methods in Enzymology 401, 468–483.CrossRefGoogle ScholarPubMed