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Journal of Integrative Agriculture  2016, Vol. 15 Issue (11): 2578-2587    DOI: 10.1016/S2095-3119(16)61404-1
Animal Science · Veterinary Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Regulatory effects of dietary L-Arg supplementation on the innate immunity and antioxidant ability in broiler chickens
HU Ya-di, TAN Jian-zhuang, QI Ji, ZHANG Hong-fu
State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
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Abstract      Here, we investigated the effect of dietary arginine (Arg) supplementation on innate immunity and the antioxidant ability of broiler chickens. The experiment was designed as a single-factorial arrangement (n=8 cages/treatment, six birds/cage), and we used four dietary Arg concentrations (10.0, 15.0, 20.0 or 25.0 g kg–1). On day 21, the birds were killed to obtain spleen, cecal tonsil and liver samples to determine the gene expression and antioxidant characteristics. Increasing the Arg concentration linearly decreased (P<0.05) the mRNA expression of splenic interleukin-18 (IL-18) and tumor necrosis factor-α (TNF-α). Dietary Arg supplementation quadratically decreased (P<0.05) the expression of interleukin-1b (IL-1b) and interferon-γ (IFN-γ) mRNA in the spleen. Increasing Arg concentrations linearly and quadratically reduced the expression of IL-18 mRNA in the spleen. Meanwhile, increasing dietary Arg supplementation linearly and quadratically increased the lymphotactin mRNA (P<0.05) expression, and linearly increased the macrophage inflammatory protein-1β (MIP-1β) and toll-like receptor 15 (TLR15) mRNA expression in the cecal tonsils. Dietary Arg supplementation linearly (P<0.05) increased the glutathione peroxidase (GSH-Px), catalase (CAT), and lysozyme (LZM) activities in the liver. However, the malondialdehyde (MDA) activity in the liver was not influenced by the dietary Arg concentration (P>0.05). No significant (P>0.05) effect was found on the activity of superoxide dismutase (SOD) in the liver. Thus high levels of Arg supplementation (>20.0 g kg–1) may potentially suppress the innate immunity of broiler chickens, and dietary Arg supplementation enhances the antioxidant activity in broiler chickens.
Keywords:  arginine        innate immunity        antioxidant ability        broiler  
Received: 09 November 2015   Accepted:
Fund: 

This study was supported by the National Key Technology R&D Program of China (2012BAD39B01) and the Agricultural Science and Technology Innovation Program of CAAS (ASTIP-IAS07) in China.

Corresponding Authors:  ZHANG Hong-fu, Tel: +86-10-62818910, E-mail: zhanghf6565@vip.sina.com   
About author:  HU Ya-di, E-mail: huyadi529@163.com;

Cite this article: 

HU Ya-di, TAN Jian-zhuang, QI Ji, ZHANG Hong-fu. 2016. Regulatory effects of dietary L-Arg supplementation on the innate immunity and antioxidant ability in broiler chickens. Journal of Integrative Agriculture, 15(11): 2578-2587.

Abdukalykova S, Ruiz-Feria C A. 2006. Arginine and vitamin E improve the cellular and humoral immune response of broiler chickens. Poultry Science, 5, 121–127.

Abe T, Sugano E, Saigo Y, Tamai M. 2003. Interleukin-1β and barrier function of retinal pigment epithelial cells (ARPE-19): Aberrant expression of junctional complex molecules. Investigative Ophthalmology & Visual Science, 44, 4097–4104.

Alican I, Kubes P. 1996. A critical role for nitric oxide in intestinal barrier function and dysfunction. American Journal of Physiology (Gastrointestinal and Liver Physiology), 270, 225–237.

Arthur J R. 2001. The glutathione peroxidases. Cellular and Molecular Life Sciences, 57, 1825–1835.

Ashkenazi A, Dixit V M. 1998. Death receptors: Signaling and modulation. Science, 281, 1305–1308.

Baggiolini M, Walz A, Kunkel S L. 1989. Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. Journal of Clinical Investigation, 84, 1045–1049.

Boyd A C, Peroval M Y, Hammond J A, Prickett M D, Young J R, Smith A L. 2012. TLR15 is unique to avian and reptilian lineages and recognizes a yeast-derived agonist. Journal of Immunology, 189, 4930–4938.

Bronte V, Zanovello P. 2005. Regulation of immune responses by L-arginine metabolism. Nature Reviews Immunology, 5, 641–654.

Calkins C M, Bensard D D, Heimbach J K, Meng X, Shames B D, Pulido E J, McIntyre R C. 2001. L-Arginine attenuates lipopolysaccharide-induced lung chemokine production. American Journal of Physiology (Lung Cellular and Molecular Physiology), 280, 400–408.

Coburn L A, Gong X, Singh K, Asim M, Scull B P, Allaman M M, Williams C S, Rosen M J, Washington M K, Barry D P, Piazuelo M B, Casero R A, Chaturvedi R, Zhao Z, Wilson K T. 2012. L-Arginine supplementation improves responses to injury and inflammation in dextran sulfate sodium colitis. PLoS ONE, 7, e33546.

Daly J M, Reynolds J, Thom A, Kinsley L, Dietrick-Gallagher M, Shou J, Ruggieri B. 1988. Immune and metabolic effects of arginine in the surgical patient. Annals of Surgery, 208, 512–521.

Durbin J E, Hackenmiller R, Simon M C, Levy D E. 1996. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell, 83, 443–450.

Evoy D, Lieberman M D, Fahey T J, Daly J M. 1998. Immunonutrition: The role of arginine. Nutrition, 14, 611–617.

Fiolka M J, Zagaja M P, Hulas-Stasiak M, Wielbo J. 2012. Activity and immunodetection of lysozyme in earthworm Dendrobaena veneta (Annelida). Journal of Invertebrate Pathology, 109, 83–90.

Fukuoka S, Kawamura M, Komiya K, Tojo M, Hachiya H, Hasegawa K, Konno S. 2003. A novel non-phosgene polycarbonate production process using by-product CO2 as starting material. Green Chemistry, 5, 497–507.

Garcia-Castro I, Gaya L. 1984. Effect of endotoxin treatment and tumour induction on liver catalase activity in mice. Microbiology, 130, 119–122.

Gonzales R, Auclair C, Voisin E, Gautero H, Dhermy D, Boivin P. 1984. Superoxide dismutase, catalase, and glutathione peroxidase in red blood cells from patients with malignant diseases. Cancer Research, 44, 4137–4139.

Kidd M, Peebles E, Whitmarsh S, Yeatman J, Wideman R. 2001. Growth and immunity of broiler chicks as affected by dietary arginine. Poultry Science, 80, 1535–1542.

Klasing K C, Barnes D M. 1988. Decreased amino acid requirements of growing chicks due to immunologic. The Journal of Nutrition, 118, 1158–1164.

Koch A E, Polverini P J, Kunkel S L, Harlow L A, Di Pietro L A, Elner V M, Strieter R M. 1992. Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science, 258, 1798–1801.

Lefevre P, Witham J, Lacroix C E, Cockerill P N, Bonifer C. 2008. The LPS-induced transcriptional upregulation of the chicken lysozyme locus involves CTCF eviction and noncoding RNA transcription. Molecular Cell, 32, 129–139.

Li P, Yin Y L, Li D, Kim S W, Wu G. 2007. Amino acids and immune function. British Journal of Nutrition, 98, 237–252.

Lillard J W, Boyaka P N, Hedrick J A, Zlotnik A, McGhee J R. 1999. Lymphotactin acts as an innate mucosal adjuvant. The Journal of Immunology, 162, 1959–1965.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402–408.

Ma C S, Nichols K E, Tangye S G. 2007. Regulation of cellular and humoral immune responses by the SLAM and SAP families of molecules. Annual Review of Immunology, 25, 337–379.

Maurer M, Von Stebut E. 2004. Macrophage inflammatory protein-1. The International Journal of Biochemistry & Cell Biology, 36, 1882–1886.

Mera M A, White J M, Sheehan K C, Bach E A, Rodig S J, Dighe A S, Carver-Moore K. 1996. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell, 84, 431–442.

Munir K, Muneer M, Masaoud E, Tiwari A, Mahmud A, Chaudhry R, Rashid A. 2009. Dietary arginine stimulates humoral and cell-mediated immunity in chickens vaccinated and challenged against Hydropericardium syndrome virus. Poultry Science, 88, 1629–1638.

Nieves Jr C, Langkamp-Henken B. 2002. Arginine and immunity: A unique perspective. Biomedicine & Pharmacotherapy, 56, 471–482.

Nijsten M, Hack C, Helle M, Ten Duis H, Klasen H, Aarden L. 1991. Interleukin-6 and its relation to the humoral immune response and clinical parameters in burned patients. Surgery, 109, 761–767.

NRC (National Research Council). 1994. Nutrient Requirements of Poultry. 9th ed. National Academy Press, Washington, D.C.

Opal S M, De Palo V A. 2000. Anti-inflammatory cytokines. Chest Journal, 117, 1162–1172.

Popovic P J, Zeh H J, Ochoa J B. 2007. Arginine and immunity. The Journal of Nutrition, 137, 1681S–1686S.

Rhoads J, Chen W, Gookin J, Wu G, Fu Q, Blikslager A, Rippe R, Argenzio R, Cance W, Weaver E. 2004. Arginine stimulates intestinal cell migration through a focal adhesion kinase dependent mechanism. Gut, 53, 514–522.

Roach J C, Glusman G, Rowen L, Kaur A, Purcell M K, Smith K D, Hood L E, Aderem A. 2005. The evolution of vertebrate Toll-like receptors. Proceedings of the National Academy of Sciences of the United States of America, 102, 9577–9582.

Shang H F, Tsai H J, Chiu W C, Yeh S L. 2003. Effects of dietary arginine supplementation on antibody production and antioxidant enzyme activity in burned mice. Burns, 29, 43–48.

Stechmiller J K, Childress B, Cowan L. 2005. Arginine supplementation and wound healing. Nutrition in Clinical Practice, 20, 52–61.

Stechmiller J K, Childress B, Porter T. 2004. Arginine immunonutrition in critically Ill patients: A clinical dilemma. American Journal of Critical Care, 13, 17–23.

Swaggerty C, Genovese K, He H, Duke S, Pevzner I, Kogut M. 2011. Broiler breeders with an efficient innate immune response are more resistant to Eimeria tenella. Poultry Science, 90, 1014–1019.

Tan J, Applegate T J, Liu S, Guo Y, Eicher S D. 2014. Supplemental dietary L-arginine attenuates intestinal mucosal disruption during a coccidial vaccine challenge in broiler chickens. British Journal of Nutrition, 112, 1098–1109.

Tan J, Guo Y, Applegate J T, Du E, Zhao X. 2015. L-Arginine regulates immune functions in chickens immunized with intermediate strain of infectious bursal disease vaccine. The Journal of Poultry Science, 52, 101–108.

Tan J, Liu S, Guo Y, Applegate T J, Eicher S D. 2014. Dietary L-arginine supplementation attenuates lipopolysaccharide-induced inflammatory response in broiler chickens. British Journal of Nutrition, 111, 1394–1404.

Tsai H J, Shang H F, Yeh C L, Yeh S L. 2002. Effects of arginine supplementation on antioxidant enzyme activity and macrophage response in burned mice. Burns, 28, 258–263.

Vertuani S, Angusti A, Manfredini S. 2004. The antioxidants and pro-antioxidants network: An overview. Current Pharmaceutical Design, 10, 1677–1694.

Wang L, Du F, Wang X. 2008. TNF-alpha induces two distinct caspase-8 activation pathways. Cell, 133, 693–703.

Weydert C J, Cullen J J. 2010. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nature Protocols, 5, 51–66.

Withanage G S K, Wigley P, Kaiser P, Mastroeni P, Brooks H, Powers C, McConnell I. 2005. Cytokine and chemokine responses associated with clearance of a primary Salmonella enterica serovar typhimurium infection in the chicken and in protective immunity to rechallenge. Infection and Immunity, 73, 5173–5182.

Wu G, Bazer F W, Davis T A, Kim S W, Li P, Marc Rhoads J, Carey Satterfield M, Smith S B, Spencer T E, Yin Y. 2009. Arginine metabolism and nutrition in growth, health and disease. Amino Acids, 37, 153–168.

Wu G, Yuan C, Shen C, Tang J, Gong Y D, Li D, Sun F, Huang C, Han X. 2007. Immunological and biochemical parameters in carp (Cyprinus carpio) after Qompsell feed ingredients for long-term administration. Aquaculture Research, 38, 246–255.

Xie H, Rath N C, Huff G R, Balog J M. 2000. Effects of Salmonella typhimurium lipopolysaccharide on broiler chickens. Poultry Science, 79, 33–40.

Yeh C L, Pai M H, Li C C, Tsai Y L, Yeh S L. 2010. Effect of arginine on angiogenesis induced by human colon cancer: In vitro and in vivo studies. The Journal of Nutritional Biochemistry, 21, 538–543.

Yu B P, Chung H Y. 2006. Adaptive mechanisms to oxidative stress during aging. Mechanisms of Ageing and Development, 127, 436–443.
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