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Dietary arginine supplementation enhances intestinal expression of SLC7A7 and SLC7A1 and ameliorates growth depression in mycotoxin-challenged pigs

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Abstract

This study tested the hypothesis that dietary l-arginine supplementation confers beneficial effects on growing pigs fed a mold-contaminated diet. The measured variables included: (1) the average daily weight gain and feed:gain ratio; (2) activities of total superoxide dismutase, glutathione peroxidase, diamine oxidase, as well as amino acid and d-lactate concentrations in serum; (3) intestinal morphology; (4) expression of the genes for SLC7A7 (amino acid transporter light chain, y+L system, family 7, member 7), SLC7A1 (cationic amino acid transporter, y+ system, family 7, member 1), SLC1A1 (neuronal/epithelial high affinity glutamate transporter, system XAG, member 1), SLC5A1 (sodium/glucose cotransporter, family 5, member 1) in the ileum and jejunum. Mycotoxins in feedstuffs resulted in an enlarged small intestine mass, oxidative injury in tissues, and reduced growth performance in pigs. Dietary arginine supplementation enhanced (P < 0.05) expression of jejunal SLC7A7 and ileal SLC7A1, in comparison with the control and mycotoxin groups. In addition, supplementing 1 % l-arginine to the mycotoxin-contaminated feed had the following beneficial effects (P < 0.05): (1) alleviating the imbalance of the antioxidant system in the body; (2) ameliorating intestinal abnormalities; and (3) attenuating whole-body growth depression, compared with the mycotoxin group without arginine treatment. Collectively, these results indicate that dietary supplementation with l-arginine exerts a protective role in pigs fed mold-contaminated foods. The findings may have important nutritional implications for humans and other mammals.

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References

  • Andretta I, Kipper M, Lehnen CR et al (2012) Meta-analytical study of productive and nutritional interactions of mycotoxins in growing pigs. Animal 6:1476–1482

    Article  PubMed  CAS  Google Scholar 

  • Anggard E (1994) Nitric oxide: mediator, murderer, and medicine. Lancet 343:1199–1206

    Article  PubMed  CAS  Google Scholar 

  • Applegate TJ, Schatzmayr G, Prickel K et al (2009) Effect of aflatoxin culture on intestinal function and nutrient loss in laying hens. Poult Sci 88:1235–1241

    Article  PubMed  CAS  Google Scholar 

  • Aravind KL, Patil VS, Devegowda G et al (2003) Efficacy of esterified glucomannan to counteract mycotoxicosis in naturally contaminated feed on performance and serum biochemical and hematological parameters in broilers. Poult Sci 82:571–576

    Article  PubMed  CAS  Google Scholar 

  • Awad WA, Bohm J, Razzazi-Fazeli E et al (2006) Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens. Poult Sci 85:974–979

    Article  PubMed  CAS  Google Scholar 

  • Binder EM (2007) Managing the risk of mycotoxins in modern feed production. Anim Feed Sci Technol 133:149–166

    Article  CAS  Google Scholar 

  • Binder EM, Tan LM, Chin LJ et al (2007) Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Anim Feed Sci Technol 137:265–282

    Article  CAS  Google Scholar 

  • Chaytor AC, Hansen JA, van Heugten E et al (2011) Occurrence and decontamination of mycotoxins in swine feed. Asian-Australas J Anim Sci 24:723–738

    Article  CAS  Google Scholar 

  • Dai ZL, Wu G, Zhu WY (2011) Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Front Biosci 16:1768–1786

    Article  CAS  Google Scholar 

  • Dai ZL, Li XL, Xi PB et al (2012a) Metabolism of select amino acids in bacteria from the pig small intestine. Amino Acids 42:1597–1608

    Article  PubMed  CAS  Google Scholar 

  • Dai ZL, Li XL, Xi PB et al (2012b) Regulatory role for l-arginine in the utilization of amino acids by pig small-intestinal bacteria. Amino Acids 43:233–244

    Article  PubMed  CAS  Google Scholar 

  • Dai ZL, Li XL, Xi PB et al (2013a) l-Glutamine regulates amino acid utilization by intestinal bacteria. Amino Acids 45:501–512

    Article  PubMed  CAS  Google Scholar 

  • Dai ZL, Wu ZL, Yang Y et al (2013b) Nitric oxide and energy metabolism in mammals. BioFactors 39:383–391

    Article  PubMed  CAS  Google Scholar 

  • Deng D, Yin YL, Chu WY et al (2009) Impaired translation initiation activation and reduced protein synthesis in weaned piglets fed a low-protein diet. J Nutr Biochem 20:544–552

    Article  PubMed  CAS  Google Scholar 

  • Dinu D, Bodea GO, Ceapa CD et al (2011) Adapted response of the antioxidant defense system to oxidative stress induced by deoxynivalenol in Hek-293 cells. Toxicon 57:1023–1032

    Article  PubMed  CAS  Google Scholar 

  • Fokunang CN, Tembe-Fokunang EA, Tomkins P et al (2006) Global impact of mycotoxins on human and animal health management. Outlook Agric 35:247–253

    Article  Google Scholar 

  • Fu WJ, Stromberg AJ, Viele K et al (2010) Statistics and bioinformatics in nutritional sciences: analysis of complex data in the era of systems biology. J Nutr Biochem 21:561–572

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Guan S, Gong M, Yin YL et al (2011) Occurrence of mycotoxins in feeds and feed ingredients in China. J Food Agric Environ 9:163–167

    Google Scholar 

  • He QH, Ren PP, Kong XF et al (2012) Comparison of serum metabolite compositions between obese and lean growing pigs using an NMR-based metabonomic approach. J Nutr Biochem 23:133–139

    Article  PubMed  CAS  Google Scholar 

  • He LQ, Yang HS, Li TJ et al (2013a) Effects of dietary l-lysine intake on the intestinal mucosa and expression of CAT genes in weaned piglets. Amino Acids 45:383–391

    Article  PubMed  CAS  Google Scholar 

  • He LQ, Yin YL, Li TJ et al (2013b) Use of the Ussing chamber technique to study nutrient transport by epithelial tissues. Front Biosci 18:1266–1274

    Article  CAS  Google Scholar 

  • Hou YQ, Wang L, Zhang W et al (2012) Protective effects of N-acetylcysteine on intestinal functions of piglets challenged with lipopolysaccharide. Amino Acids 43:1233–1242

    Article  PubMed  CAS  Google Scholar 

  • Hou YQ, Wang L, Yi D et al (2013) N-Acetylcysteine reduces inflammation in the small intestine by regulating redox, EGF and TLR4 signaling. Amino Acids 45:513–522

    Article  PubMed  CAS  Google Scholar 

  • Jiang SZ, Yang ZB, Yang WR et al (2011) Effects of purified zearalenone on growth performance, organ size, serum metabolites, and oxidative stress in postweaning gilts. J Anim Sci 89:3008–3015

    Article  PubMed  CAS  Google Scholar 

  • Jobgen W, Fu WJ, Gao H et al (2009) High fat feeding and dietary l-arginine supplementation differentially regulate gene expression in rat white adipose tissue. Amino Acids 37:187–198

    Article  PubMed  CAS  Google Scholar 

  • Kim SW, Wu G (2004) Dietary arginine supplementation enhances the growth of milk-fed young pigs. J Nutr 134:625–630

    PubMed  CAS  Google Scholar 

  • Kong X, Tan B, Yin Y et al (2012) l-arginine stimulates the mTOR signaling pathway and protein synthesis in porcine trophectoderm cells. J Nutr Biochem 23:1178–1183

    Article  PubMed  CAS  Google Scholar 

  • Koppelmann T, Pollak Y, Mogilner J et al (2012) Dietary l-arginine supplementation reduces methotrexate-induced intestinal mucosal injury in rat. BMC Gastroenterol 12:41

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lei J, Feng DY, Zhang YL et al (2012) Nutritional and regulatory role of branched-chain amino acids in lactation. Front Biosci 17:2725–2739

    Article  CAS  Google Scholar 

  • Li P, Yin YL, Li DF et al (2007) Amino acids and immune function. Br J Nutr 98:237–252

    Article  PubMed  CAS  Google Scholar 

  • Li XL, Rezaei R, Li P et al (2011) Composition of amino acids in feed ingredients for animal diets. Amino Acids 40:1159–1168

    Article  PubMed  CAS  Google Scholar 

  • Liu YL, Meng GQ, Wang HR et al (2011) Effect of three mycotoxin adsorbents on growth performance, nutrient retention and meat quality in broilers fed on mould-contaminated feed. Br Poult Sci 52:255–263

    Article  PubMed  CAS  Google Scholar 

  • Liu XD, Wu X, Yin YL et al (2012) Effects of dietary l-arginine or N-carbamylglutamate supplementation during late gestation of sows on the miR-15b/16, miR-221/222, VEGFA and eNOS expression in umbilical vein. Amino Acids 42:2111–2119

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Maresca M, Mahfoud R, Garmy N et al (2002) The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J Nutr 132:2723–2731

    PubMed  CAS  Google Scholar 

  • Mary VS, Theumer MG, Arias SL et al (2012) Reactive oxygen species sources and biomolecular oxidative damage induced by aflatoxin B1 and fumonisin B1 in rat spleen mononuclear cells. Toxicology 302:299–307

    Article  PubMed  CAS  Google Scholar 

  • Packer RA, Moore GE, Chang CY et al (2012) Serum d-lactate concentrations in cats with gastrointestinal disease. J Vet Intern Med 26:905–910

    Article  PubMed  CAS  Google Scholar 

  • Park BJ, Takatori K, Sugita-Konishi Y et al (2007) Degradation of mycotoxins using microwave-induced argon plasma at atmospheric pressure. Surf Coat Technol 201:5733–5737

    Article  CAS  Google Scholar 

  • Ren W, Luo W, Wu M et al (2011) Dietary l-glutamine supplementation improves pregnancy outcome in mice infected with type-2 porcine circovirus. Amino Acids 45:479–488

    Article  PubMed  CAS  Google Scholar 

  • Ren W, Yin YL, Liu G et al (2012) Effect of dietary arginine supplementation on reproductive performance of mice with porcine circovirus type 2 infection. Amino Acids 42:2089–2094

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rezaei R, Knabe DA, Wu G (2013a) Impact of aflatoxins on swine nutrition and possible measures of control and amelioration. Aflatoxin control: safeguarding animal feed with calcium smectite. In: Joe B. Dixon, Ana L. Barrientos Velázquez, Youjun Deng, (eds) American Society of Agronomy and Soil Science, Madison, pp 54–67. doi:10.2136/2013.aflatoxins.c6

  • Rezaei R, Knabe DA, Tekwe CD et al (2013b) Dietary supplementation with monosodium glutamate is safe and improves growth performance in postweaning pigs. Amino Acids 44:911–923

    Article  PubMed  CAS  Google Scholar 

  • Rhoads JM, Wu G (2009) Glutamine, arginine, and leucine signaling in the intestine. Amino Acids 37:111–122

    Article  CAS  Google Scholar 

  • Rhoads JM, Liu Y, Niu X et al (2008) Arginine stimulates cdx2-transformed intestinal epithelial cell migration via a mechanism requiring both nitric oxide and phosphorylation of p70 S6 kinase. J Nutr 138:1652–1657

    PubMed  CAS  Google Scholar 

  • Richard JL et al (2007) Some major mycotoxins and their mycotoxicoses—an overview. Int J Food Microbiol 119:3–10

    Article  PubMed  CAS  Google Scholar 

  • Ruan Z, Lv YF, Fu XF et al (2013) Metabolomic analysis of amino acid metabolism in colitic rats supplemented with lactosucrose. Amino Acids 45:877–887

    Article  PubMed  CAS  Google Scholar 

  • Stechmiller JK, Childress B, Cowan L et al (2005) Arginine supplementation and wound healing. Nutr Clin Pract 20:52–61

    Article  PubMed  Google Scholar 

  • Swamy HVLN, Smith TK, MacDonald EJ et al (2003) Effects of feeding a blend of grains naturally contaminated with Fusarium mycotoxins on growth and immunological measurements of starter pigs, and the efficacy of a polymeric glucomannan mycotoxin adsorbent. J Anim Sci 81:2792–2803

    PubMed  CAS  Google Scholar 

  • Tan BE, Yin YL, Liu ZQ et al (2009) Dietary l-arginine supplementation increases muscle gain and reduces body fat mass in growing-finishing pigs. Amino Acids 37:169–175

    Article  PubMed  CAS  Google Scholar 

  • Tan BE, Yin YL, Kong XF et al (2010) l-Arginine stimulates proliferation and prevents endotoxin-induced death of intestinal cells. Amino Acids 38:1227–1235

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tan B, Li X, Wu G et al (2012a) Dynamic changes in blood flow and oxygen consumption in the portal-drained viscera of growing pigs receiving acute administration of l-arginine. Amino Acids 43:2481–2489

    Article  PubMed  CAS  Google Scholar 

  • Tan BE, Li XG, Yin YL et al (2012b) Regulatory roles for l-arginine in reducing white adipose tissue. Front Biosci 17:2237–2246

    Article  CAS  Google Scholar 

  • Wang JJ, Chen LX, Li P et al (2008) Gene expression is altered in piglet small intestine by weaning and dietary glutamine supplementation. J Nutr 138:1025–1032

    Article  PubMed  CAS  Google Scholar 

  • Wang XQ, Ou DY, Yin JD et al (2009) Proteomic analysis reveals altered expression of proteins related to glutathione metabolism and apoptosis in the small intestine of zinc oxide-supplemented piglets. Amino Acids 37:209–218

    Article  PubMed  CAS  Google Scholar 

  • Wang WW, Wu ZL, Dai ZL et al (2013) Glycine metabolism in animals and humans: implications for nutrition and health. Amino Acids 45:463–477

    Article  PubMed  CAS  Google Scholar 

  • Wei JW, Carroll RJ, Harden KK et al (2012) Comparisons of treatment means when factors do not interact in two-factorial studies. Amino Acids 42:2031–2035

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17

    Article  PubMed  CAS  Google Scholar 

  • Wu G (2010a) Recent advances in swine amino acid nutrition. J Anim Sci Biotechnol 1:49–61

    Google Scholar 

  • Wu G (2010b) Functional amino acids in growth, reproduction and health. Adv Nutr 1:31–37

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wu G (2013a) Functional amino acids in nutrition and health. Amino Acids 45:407–411

    Article  PubMed  CAS  Google Scholar 

  • Wu G (2013b) Amino acids: biochemistry and nutrition. CRC Press, Boca Raton

    Book  Google Scholar 

  • Wu G, Knabe DA (1995) Arginine synthesis in enterocytes of neonatal pigs. Am J Physiol Regul Integr Comp Physiol 269:R621–R629

    CAS  Google Scholar 

  • Wu G, Morris SM Jr (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1–17

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wu G, Knabe DA, Flynn NE (1994) Synthesis of citrulline from glutamine in pig enterocytes. Biochem J 299:115–121

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wu G, Meier SA, Knabe DA (1996a) Dietary glutamine supplementation prevents jejunal atrophy in weaned pigs. J Nutr 126:2578–2584

    PubMed  CAS  Google Scholar 

  • Wu G, Knabe DA, Flynn NE et al (1996b) Arginine degradation in developing porcine enterocytes. Am J Physiol Gastrointest Liver Physiol 271:G913–G919

    CAS  Google Scholar 

  • Wu G, Collins JK, Perkins-Veazie P et al (2007a) Dietary supplementation with watermelon pomace juice enhances arginine availability and ameliorates the metabolic syndrome in Zucker diabetic fatty rats. J Nutr 137:2680–2685

    PubMed  CAS  Google Scholar 

  • Wu G, Bazer FW, Cudd TA et al (2007b) Pharmacokinetics and safety of arginine supplementation in animals. J Nutr 137:1673S–1680S

    PubMed  CAS  Google Scholar 

  • Wu G, Bazer FW, Davis TA et al (2009) Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37:153–168

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wu X, Ruan Z, Gao YL et al (2010) Dietary supplementation with l-arginine or N-carbamylglutamate enhances intestinal growth and heat shock protein-70 expression in weanling pigs fed a corn- and soybean meal-based diet. Amino Acids 39:831–839

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Bazer FW, Johnson GA et al (2011a) Important roles for l-glutamine in swine nutrition and production. J Anim Sci 89:2017–2030

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Bazer FW, Burghardt RC et al (2011b) Proline and hydroxyproline metabolism: implications for animal and human nutrition. Amino Acids 40:1053–1063

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wu X, Yin YL, Liu YQ et al (2012) Effect of dietary arginine and N-carbamoylglutamate supplementation on reproduction and gene expression of eNOS, VEGFA and PlGF1 in placenta in late pregnancy of sows. Anim Reprod Sci 132:187–192

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Wu ZL, Dai ZL et al (2013a) Dietary requirements of “nutritionally nonessential amino acids” by animals and humans. Amino Acids 44:1107–1113

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Bazer FW, Satterfield MC et al (2013b) Impacts of arginine nutrition on embryonic and fetal development in mammals. Amino Acids 45:241–256

    Article  PubMed  CAS  Google Scholar 

  • Yao K, Guan S, Li T et al (2011) Dietary l-arginine supplementation enhances intestinal development and expression of vascular endothelial growth factor in weanling piglets. Br J Nutr 105:703–709

    Article  PubMed  CAS  Google Scholar 

  • Yao K, Yin YL, Li XL et al (2012) Alpha-ketoglutarate inhibits glutamine degradation and enhances protein synthesis in intestinal porcine epithelial cells. Amino Acids 42:2491–2500

    Article  PubMed  CAS  Google Scholar 

  • Yin YL, Tan B et al (2010) Manipulation of dietary nitrogen, amino acids and phosphorus to reduce environmental impact of swine production and enhance animal health. J Food Agric Environ 8:447–462

    CAS  Google Scholar 

  • Yin J, Ren W, Liu G et al (2013a) Birth oxidative stress and the development of an antioxidant system in newborn piglets. Free Radic Res 47:1027–1035

    Article  PubMed  CAS  Google Scholar 

  • Yin J, Ren WK, Wu XS et al (2013b) Oxidative stress-mediated signaling pathways: a review. J Food Agric Environ 11:132–139

    Google Scholar 

  • Young JC, Blackwell BA, Apsimon JW et al (1986) Alkaline-degradation of the mycotoxin 4-deoxynivalenol. Tetrahedron Lett 27:1019–1022

    Article  CAS  Google Scholar 

  • Yunus AW, Ghareeb K, Abd-El-Fattah AA et al (2011) Gross intestinal adaptations in relation to broiler performance during chronic aflatoxin exposure. Poult Sci 90:1683–1689

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Yin YL, Shu XG et al (2013a) Oral administration of MSG increases expression of glutamate receptors and transporters in the gastrointestinal tract of young piglets. Amino Acids 45:1169–1177

    Article  PubMed  CAS  Google Scholar 

  • Zhang SH, Qiao SY, Ren M et al (2013b) Supplementation with branched-chain amino acids to a low-protein diet regulates intestinal expression of amino acid and peptide transporters in weanling pigs. Amino Acids 45:1191–1205

    Article  PubMed  CAS  Google Scholar 

  • Zhou XH, Wu X, Yin YL et al (2012) Preventive oral supplementation with glutamine and arginine has beneficial effects on the intestinal mucosa and inflammatory cytokines in endotoxemic rats. Amino Acids 43:813–821

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The present work was supported by Grants from the 973 National Key Basic Research of China (No. 2013CB127301), the National Natural Science Foundation of China (No. 31272463, 31072042, and 31272450), Hunan Provincial Natural Science Foundation of China (No. K1307007-21), and Texas AgriLife Research Hatch Project (H-8200).

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Authors and Affiliations

  1. Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central China, Ministry of Agriculture, Hunan Provincial Engineering Research Center of Healthy Livestock, Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, Hunan, China

    Jie Yin, Wenkai Ren, Jielin Duan, Li Wu, Shuai Chen, Tiejun Li, Yulong Yin & Guoyao Wu

  2. University of Chinese Academy of Sciences, Beijing, 100039, China

    Jie Yin, Wenkai Ren, Jielin Duan & Li Wu

  3. State Key Laboratory of Animal Nutrition, China Agricultural University, Beijing, 100193, China

    Guoyao Wu

  4. Department of Animal Science, Texas A&M University, College Station, TX, 77843, USA

    Guoyao Wu

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  1. Jie Yin
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  2. Wenkai Ren
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Correspondence to Tiejun Li.

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J. Yin and W. Ren contributed equally to the present study.

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Yin, J., Ren, W., Duan, J. et al. Dietary arginine supplementation enhances intestinal expression of SLC7A7 and SLC7A1 and ameliorates growth depression in mycotoxin-challenged pigs. Amino Acids 46, 883–892 (2014). https://doi.org/10.1007/s00726-013-1643-5

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