Skip to main content
    • Aa
    • Aa
  • Access
  • Cited by 11
  • Cited by
    This article has been cited by the following publications. This list is generated based on data provided by CrossRef.

    Bortoluzzi, C. Menten, J. F. M. Silveira, H. Melo, A. D. B. and Rostagno, M. H. 2016. Hops β-acids (Humulus lupulus) decrease intestinal gene expression of proinflammatory cytokines in anex-vivomodel. The Journal of Applied Poultry Research, Vol. 25, Issue. 2, p. 191.

    Du, Encun Wang, Weiwei Gan, Liping Li, Zhui Guo, Shuangshuang and Guo, Yuming 2016. Effects of thymol and carvacrol supplementation on intestinal integrity and immune responses of broiler chickens challenged with Clostridium perfringens. Journal of Animal Science and Biotechnology, Vol. 7, Issue. 1,

    Gessner, D. K. Ringseis, R. and Eder, K. 2016. Potential of plant polyphenols to combat oxidative stress and inflammatory processes in farm animals. Journal of Animal Physiology and Animal Nutrition,

    Gottardo, E. T. Prokoski, K. Horn, D. Viott, A. D. Santos, T. C. and Fernandes, J. I. M. 2016. Regeneration of the intestinal mucosa inEimeriaandE. Colichallenged broilers supplemented with amino acids. Poultry Science, Vol. 95, Issue. 5, p. 1056.

    Lieboldt, M. A. Frahm, J. Halle, I. Görs, S. Schrader, L. Weigend, S. Preisinger, R. Metges, C. C. Breves, G. and Dänicke, S. 2016. Metabolic and clinical response toEscherichia colilipopolysaccharide in layer pullets of different genetic backgrounds supplied with graded dietary L-arginine. Poultry Science, Vol. 95, Issue. 3, p. 595.

    Lieboldt, M.-A. Frahm, J. Halle, I. Schrader, L. Weigend, S. Preisinger, R. Breves, G. and Dänicke, S. 2016. Haematological and febrile response toEscherichia colilipopolysaccharide in 12-week-old cockerels of genetically diverse layer lines fed diets with increasing L-arginine levels. Journal of Animal Physiology and Animal Nutrition,

    Wiegertjes, Geert F. Wentzel, Annelieke S. Spaink, Herman P. Elks, Philip M. and Fink, Inge R. 2016. Polarization of immune responses in fish: The ‘macrophages first’ point of view. Molecular Immunology, Vol. 69, p. 146.

    Xia, Weiguang Fouad, Ahmed Mohamed Chen, Wei Ruan, Dong Wang, Shuang Fan, Qiuli Wang, Ying Cui, Yiyan and Zheng, Chuntian 2016. Estimation of dietary arginine requirements for Longyan laying ducks. Poultry Science, p. pew205.

    Lieboldt, Marc-Alexander Halle, Ingrid Frahm, Jana Schrader, Lars Weigend, Steffen Preisinger, Rudolf and Dänicke, Sven 2015. Effects of Long-term Graded L-arginine Supply on Growth Development, Egg Laying and Egg Quality in Four Genetically Diverse Purebred Layer Lines. The Journal of Poultry Science, Vol. 53, Issue. 1, p. 8.

    Tan, Jianzhuang Guo, Yuming J. Applegate, Todd. Du, Encun and Zhao, Xu 2015. L-Arginine Regulates Immune Functions in Chickens Immunized with Intermediate Strain of Infectious Bursal Disease Vaccine. The Journal of Poultry Science, Vol. 52, Issue. 2, p. 101.

    Tan, Jian-Zhuang Guo, Yu-Ming Applegate, Todd J Du, En-Cun and Zhao, Xu 2015. Dietary L-arginine modulates immunosuppression in broilers inoculated with an intermediate strain of infectious bursa disease virus. Journal of the Science of Food and Agriculture, Vol. 95, Issue. 1, p. 126.


Dietary l-arginine supplementation attenuates lipopolysaccharide-induced inflammatory response in broiler chickens

  • Jianzhuang Tan (a1) (a2), Shasha Liu (a1), Yuming Guo (a1), Todd J. Applegate (a2) and Susan D. Eicher (a3)
  • DOI:
  • Published online: 13 January 2014

In the present study, two experiments were conducted to investigate the effect of dietary l-arginine (Arg) supplementation on the inflammatory response and innate immunity of broiler chickens. Expt 1 was designed as a 2 × 3 factorial arrangement (n 8 cages/treatment; n 6 birds/cage) with three dietary Arg concentrations (1·05, 1·42 and 1·90 %) and two immune treatments (injection of lipopolysaccharide (LPS) or saline) given at an interval of 48 h between 14 and 21 d of age. In Expt 2, correlation between dietary Arg concentration (0·99, 1·39, 1·76, 2·13 or 2·53 %) and percentage of circulating B cells (percentage of circulating lymphocytes) was determined. In Expt 1, LPS injection decreased body-weight gain and feed intake and increased feed conversion ratio of the challenged broilers (14–21 d; P< 0·05). LPS injection suppressed (P< 0·05) the percentages of splenic CD11+ and B cells (percentages of splenic lymphocytes) and phagocytic activity of splenic heterophils and macrophages; Arg supplementation linearly decreased the percentages of CD11+, CD14+ and B cells in the spleen (P< 0·10). LPS injection increased (P< 0·05) the expression of IL-1β and IL-6 mRNA in the spleen and caecal tonsils. Arginine supplementation decreased (P< 0·05) the expression of IL-1β, Toll-like receptor 4 (TLR4) and PPAR-γ mRNA in the spleen and IL-1β, IL-10, TLR4 and NF-κB mRNA in the caecal tonsils. In Expt 2, increasing dietary Arg concentrations linearly and quadratically reduced the percentage of circulating B cells (P< 0·01). Collectively, Arg supplementation attenuated the overexpression of pro-inflammatory cytokines probably through the suppression of the TLR4 pathway and CD14+ cell percentage. Furthermore, excessive Arg supplementation (1·76 %) suppressed the percentages of circulating and splenic B cells.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Dietary l-arginine supplementation attenuates lipopolysaccharide-induced inflammatory response in broiler chickens
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Dietary l-arginine supplementation attenuates lipopolysaccharide-induced inflammatory response in broiler chickens
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Dietary l-arginine supplementation attenuates lipopolysaccharide-induced inflammatory response in broiler chickens
      Available formats
Corresponding author
*Corresponding authors: Yuming Guo, fax +86 10 6273 3900, email; T. J. Applegate, fax +1 765 494 9346, email
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

2V Bronte & P Zanovello (2005) Regulation of immune responses by l-arginine metabolism. Nat Rev Immunol 5, 641654.

3YC Luiking , M Poeze , G Ramsay , et al. (2009) Reduced citrulline production in sepsis is related to diminished de novo arginine and nitric oxide production. Am J Clin Nutr 89, 142152.

5HP Shi , DT Efron , D Most , et al. (2000) Supplemental dietary arginine enhances wound healing in normal but not inducible nitric oxide synthase knockout mice. Surgery 128, 374378.

6C Tayade , T Jaiswal , S Mishra , et al. (2006) l-Arginine stimulates immune response in chickens immunized with intermediate plus strain of infectious bursal disease vaccine. Vaccine 24, 552560.

8R Jahanian (2009) Immunological responses as affected by dietary protein and arginine concentrations in starting broiler chicks. Poult Sci 88, 18181824.

10K Munir , MA Muneer , E Masaoud , et al. (2009) Dietary arginine stimulates humoral and cell-mediated immunity in chickens vaccinated and challenged against hydropericardium syndrome virus. Poult Sci 88, 16291638.

11J Han , Y Liu , W Fan , et al. (2009) Dietary l-arginine supplementation alleviates immunosuppression induced by cyclophosphamide in weaned pigs. Amino Acids 37, 643651.

12LA Coburn , X Gong , K Singh , et al. (2012) l-Arginine supplementation improves responses to injury and inflammation in dextran sulfate sodium colitis. PLoS ONE 7, e33546.

13M Zhang , T Nii , N Isobe , et al. (2012) Expression of Toll-like receptors and effects of lipopolysaccharide on the expression of proinflammatory cytokines and chemokine in the testis and epididymis of roosters. Poult Sci 91, 19972003.

14AM Keestra & JPM Putten (2008) Unique properties of the chicken TLR4/MD-2 complex: selective lipopolysaccharide activation of the MyD88-dependent pathway. J Immunol 181, 43544362.

15PM Munyaka , G Tactacan , M Jing , et al. (2012) Immunomodulation in young laying hens by dietary folic acid and acute immune responses after challenge with Escherichia coli lipopolysaccharide. Poult Sci 91, 24542463.

16YC Lu , WC Yeh & PS Ohashi (2008) LPS/TLR4 signal transduction pathway. Cytokine 42, 145151.

17B Beutler (2000) TLR4: central component of the sole mammalian LPS sensor. Curr Opin Immunol 12, 2026.

19RG Baker , MS Hayden & S Ghosh (2011) NF-κB, inflammation, and metabolic disease. Cell Metab 13, 1122.

20B Tan , Y Yin , X Kong , et al. (2010) l-Arginine stimulates proliferation and prevents endotoxin-induced death of intestinal cells. Amino Acids 38, 12271235.

22IJ Park , SY Cha , M Kang , et al. (2013) Immunomodulatory effect of a proanthocyanidin-rich extract from Pinus radiata bark by dosing period in chickens. Poult Sci 92, 352357.

23FY Long , YM Guo , Z Wang , et al. (2011) Conjugated linoleic acids alleviate infectious bursal disease virus-induced immunosuppression in broiler chickens. Poult Sci 90, 19261933.

25N Dil & MA Qureshi (2002) Differential expression of inducible nitric oxide synthase is associated with differential Toll-like receptor 4 expression in chicken macrophages from different genetic backgrounds. Vet Immunol Immunop 84, 191207.

26D Simms , PE Cizdziel & P Chomczynski (1993) TRIzol: a new reagent for optimal single-step isolation of RNA. Focus 15, 532535.

27KJ Livak & TD Schmittgen (2001) Analysis of relative gene expression data using real-time quantitative PCR and the $$2^{ - \Delta \Delta C_{t}} $$ method. Methods 25, 402408.

29B Tan , XG Li , X Kong , et al. (2009) Dietary l-arginine supplementation enhances the immune status in early-weaned piglets. Amino Acids 37, 323331.

30M Cook (2010) A review of science leading to host-targeted antibody strategies for preventing growth depression due to microbial colonization. J Anim Sci 89, 19811990.

32Z Jiang , G Schatzmayr , M Mohnl , et al. (2010) Net effect of an acute phase response partial alleviation with probiotic supplementation. Poult Sci 89, 2833.

33V Bansal , KM Syres , V Makarenkova , et al. (2005) Interactions between fatty acids and arginine metabolism: implications for the design of immune-enhancing diets. JPEN 29, S75S80.

34JB Ochoa , V Makarenkova & V Bansal (2004) A rational use of immune enhancing diets: when should we use dietary arginine supplementation? Nutr Clin Pract 19, 216225.

35S Seifert , C Fritz , N Carlini , et al. (2011) Modulation of innate and adaptive immunity by the probiotic Bifidobacterium longum PCB133 in turkeys. Poult Sci 90, 22752280.

36P Chuammitri , SB Redmond , K Kimura , et al. (2011) Heterophil functional responses to dietary immunomodulators vary in genetically distinct chicken lines. Vet Immunol Immunop 142, 219227.

37B Harmon (1998) Avian heterophils in inflammation and disease resistance. Poult Sci 77, 972977.

38J Lee , R Austic , S Naqi , et al. (2002) Dietary arginine intake alters avian leukocyte population distribution during infectious bronchitis challenge. Poult Sci 81, 793798.

39M Ibuki , J Kovacs-Nolan , K Fukui , et al. (2011) β 1–4 Mannobiose enhances Salmonella-killing activity and activates innate immune responses in chicken macrophages. Vet Immunol Immunop 139, 289295.

40C Pohlenz , A Buentello , W Mwangi , et al. (2012) Arginine and glutamine supplementation to culture media improves the performance of various channel catfish immune cells. Fish Shellfish Immun 32, 762768.

41Y Gong , E Hart , A Shchurin , et al. (2008) Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest 118, 30123024.

42AH Zea , PC Rodriguez , KS Culotta , et al. (2004) l-Arginine modulates CD3ζ expression and T cell function in activated human T lymphocytes. Cell immunol 232, 2131.

43PC Rodriguez , CP Hernandez , K Morrow , et al. (2010) l-Arginine deprivation regulates cyclin d3 mRNA stability in human T cells by controlling HuR expression. J Immunol 185, 51985204.

44WJ Jonge , KL Kwikkers , AA Velde , et al. (2002) Arginine deficiency affects early B cell maturation and lymphoid organ development in transgenic mice. J Clin Invest 110, 15391548.

45R Chaturvedi , Y Cheng , M Asim , et al. (2004) Induction of polyamine oxidase 1 by Helicobacterpylori causes macrophage apoptosis by hydrogen peroxide release and mitochondrial membrane depolarization. J Biol Chem 279, 4016140173.

46K Klasing (2007) Nutrition and the immune system. Br Poult Sci 48, 525537.

47E Maroufyan , A Kasim , M Ebrahimi , et al. (2012) Dietary methionine and n-6/n-3 polyunsaturated fatty acid ratio reduce adverse effects of infectious bursal disease in broilers. Poult Sci 91, 21732182.

48MZ Wang , LY Ding , JF Wang , et al. (2011) Effects of n-6:n-3 polyunsaturated fatty acid ratio on heterophil:lymphocyte ratio and T lymphocyte subsets in the peripheral blood of the Yangzhou gosling. Poult Sci 90, 824829.

50SM Opal & VA DePalo (2000) Anti-inflammatory cytokines. Chest 117, 11621172.

51CA Dinarello (2000) Proinflammatory cytokines. Chest 118, 503508.

52J Bossche , WH Lamers , ES Koehler , et al. (2012) Pivotal advance: arginase-1-independent polyamine production stimulates the expression of IL-4-induced alternatively activated macrophage markers while inhibiting LPS-induced expression of inflammatory genes. J Leukocyte Biol 91, 685699.

53R Shanmugasundaram & RK Selvaraj (2012) In vivo lipopolysaccharide injection alters CD4+CD25+ cell properties in chickens. J Anim Sci 90, 24982504.

54LA Moraes , L Piqueras & D Bishop-Bailey (2006) Peroxisome proliferator-activated receptors and inflammation. Pharmacol Therapeut 110, 371385.

55HJ Zhang , YM Guo , Y Yang , et al. (2006) Dietary conjugated linoleic acid enhances spleen PPAR-γ mRNA expression in broiler chicks. Br Poult Sci 47, 726733.

56Z Wu , L Rothwell , T Hu , et al. (2009) Chicken CD14, unlike mammalian CD14, is transmembrane rather than GPI-anchored. Dev Comp Immunol 33, 97104.

57C Schutt (1999) CD14. Int J Biochem Cell B 31, 545549.

58M Kogut , H He & P Kaiser (2005) Lipopolysaccharide binding protein/CD14/TLR4-dependent recognition of Salmonella LPS induces the functional activation of chicken heterophils and up-regulation of pro-inflammatory cytokine and chemokine gene expression in these cells. Anim Biotechnol 16, 165181.

59R Brownlie & B Allan (2011) Avian Toll-like receptors. Cell Tissue Res 343, 121130.

60MA Panaro , A Cianciulli , N Gagliardi , et al. (2008) CD14 major role during lipopolysaccharide-induced inflammation in chick embryo cardiomyocytes. FEMS Immunol Med Microbiol 53, 3545.

61N Dil & MA Qureshi (2002) Involvement of lipopolysaccharide related receptors and nuclear factor κB in differential expression of inducible nitric oxide synthase in chicken macrophages from different genetic backgrounds. Vet Immunol Immunop 88, 149161.

62D Leturcq , A Moriarty , G Talbott , et al. (1996) Antibodies against CD14 protect primates from endotoxin-induced shock. J Clin Invest 98, 1533.

63MR Zoete , AM Keestra , P Roszczenko , et al. (2010) Activation of human and chicken Toll-like receptors by Campylobacter spp. Infect Immun 78, 12291238.

64LAJ O'Neill & AG Bowie (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7, 353364.

65AM Keestra , MR Zoete , LI Bouwman , et al. (2013) Unique features of chicken Toll-like receptors. Dev Comp Immunol 41, 316323.

66F Khajali , M Tahmasebi , H Hassanpour , et al. (2011) Effects of supplementation of canola meal-based diets with arginine on performance, plasma nitric oxide, and carcass characteristics of broiler chickens grown at high altitude. Poult Sci 90, 22872294.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *