Review

Relationship between Iron Homeostasis and Intestinal Immune Responses against Salmonella

  • BAI Shiping ,
  • ZHANG Keying ,
  • DING Xuemei ,
  • LUO Yuheng ,
  • BAI Jie
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  • Animal Nutrition Institute, Ministry of Education Key Laboratory of Animal Disease-Resistant Nutrition, Sichuan Agricultural University, Chengdu 611130, China

Received date: 2012-09-13

  Online published: 2013-02-28

Abstract

Salmonella enteritidis is reported to be the most common pathogen of animal salmonellosis, which is harmful to animal production and the safety of animal products. Salmonella organisms mainly infect animals by the oral route and lead to colonization of the gastrointestinal tract. Iron is an essential nutrient for intestinal Salmonella survival and reproduction. Overload iron increases the amount of Salmonella adhered to or invaded in the small intestine.Intestinal iron status severely affects the process of intestinal immune responses against Salmonella, and vice versa. Therefore, the relationship between iron hemeostasis and intestinal Salmonella infection was reviewed in this paper, in order to provide references for developing some nutritional stratagems to interrupt the process of Salmonella infection, and keep the safety of animal products.

Cite this article

BAI Shiping , ZHANG Keying , DING Xuemei , LUO Yuheng , BAI Jie . Relationship between Iron Homeostasis and Intestinal Immune Responses against Salmonella[J]. Chinese Journal of Animal Nutrition, 2013 , 25(3) : 464 -468 . DOI: 10.3969/j.issn.1006-267x.2013.03.003

References

[1] HENTZE M W,MUCHKENTHALER M U,ANDREWS N C.Balancing acts:molecular control of mammalian iron metabolism[J].Cell,2004,117(3):285-297.  
[2] ANDREW N C.Medical progress:disorders of iron metabolism[J].New England Journal of Medicine,1999,41(12):1986-1995.
[3] GRIFFITHS E.Iron in biological systems[M]//BULLEN J J,GRIFFITHS E.Iron and infection.Chichester:Wiley Press,1999:1-26.
[4] KORTMAN G A M,BOLEIJ A,SWINKELS D W,et al.Iron availability increases the pathogenic potential of Salmonella typhimurium and other enteric pathogens at the intestinal epithelial interface[J].PLoS One,2012,7(1):e29968.doi:10.1371/journal.pone.0029968.
[5] FOSTER S L,RICHARDSON S H,FAILLA M L.Elevated iron status increase bacterial invasion and surevival and alters cytokine/chemokine mRNA expression in Caco-2 human intestinal cells[J].The Journal of Nutrition,2001,131(5):1452-1458.
[6] WESSLING-RESNICK M.Iron homeostasis and the inflammatory response[J].Annual Review of Nutrition,2010,30(4):105-122.
[7] GUNSHIN H,MACKENZIE B,BERGER U V,et al.Cloning and characterization of a mammalian proton coupled metal-ion transporter[J].Nature,1997,388(6641):482-488.  
[8] CONRAD M E,UMBREIT J N.Iron absorption and transport-an update[J].American Journal of Haematology,2000,64(4):287-298.  
[9] VULPE C D,KUO Y,MURHY T L,et al.Hephaestin, a ceruloplasmi homologue implicated in intestinal iron transport,is defective in the sla mouse[J].Nature Genetics,1999,21(2):195-199.  
[10] DONOVAN A,BROWNLIE A,ZHOU Y,et al.Positional cloning of zebrafish ferroportin 1 identifies a conserved vertebrae iron exporter[J].Nature,2000,403(6771):776-781.  
[11] BAI S P,LU L,LUO X G,et al.Kinetic of manganese absorption in ligated small intestinal segments of broilers[J].Poultry Science,2008,87(12):2596-2604.[JP+1]  
[12] FRAZER D M,WILKINS S J,BECKER E M,et al.A rapid decrease in the expression of DMT1 and Dcytb but not Ireg 1 or hephaestin explains the mucosal block phenomena of iron absorption[J].Gut,2003,52(3):340-346.  
[13] HAN O,WESSLING-RESNICK M.Copper repletion enhances apical iron uptake and transepithelial iron transport by Caco-2 cells[J].American Journal of Physiology:Gastrointestinal and Liver Physiology,2002,282(3):G527-G533.[JP+1]
[14] SINGH B,ARORA S,AGRAWAL P,et al.Hepcidin:a novel peptide hormone regulating iron metabolism[J].Clinica Chimica Acta,2011,412(11/12):823-830.[JP+1]
[15] KAWABATA H,YANG R,IRAMA T,et al.Molecular cloning of transferrin receptor 2. A new member of the transferrin receptor-like family[J].Journal of Biological Chemistry,1999,274(30):20826-20832.  
[16] MASARATANA P,LAFTAH A H,LATUNDE-DADA G O,et al.Iron absorption in hepcidin1 knockout mice[J].British Journal of Nutrition,2011,105(11):1583-1591.  
[17] GEWIRTZ A T,MADARA J L.Periscope,up!Monitoring microbes in the intestine[J].Nature Immunology,2001,2(4):288-290.  
[18] VASQUEZ-TORRES A,FANG F C.Cellular routes of invasion by enteropathogens[J].Current Opinion in Microbiology,2000,3(1):54-59.  
[19] GUMBINER B.Structure,biochemistry,and assembly of epithelial tight junctions[J].American Journal of Physiology,1987,253(6 Pt 1):C749-C758.
[20] BURKEY T E,SKJOLAAS-WILSON K,MINTON J E.Expression of porcine toll-like receptors 2,4 and 9 in response to lipopolysaccharide and Salmonella enterica serovars Typhimurium and Choleraesuis[J].Veterinary Immunology and Immunopathology,2009,130(1/2):96-101.
[21] NEUTRA M R,MANTIS N J,KRAEHENBUHL J P.Collaboration of epithelial cells with organized mucosal lymphoid tissues[J].Nature Immunology,2001,2(11):1004-1009.  
[22] DIDIERLAURENT A,SIRAD J C,KRAEHENBUHL J P,et al.How the gut senses its content[J].Cell Microbiology,2002,4(2):61-72.  
[23] AKIRA S,TAKEDA K.Toll-like receptor signaling[J].Nature Reviews Immunology,2004,4(7):499-511.
[24] GHOSH S,MAY M J,KOPP E B.Nf-kappa B and Rel proteins:evolutionarily conserved mediateors of immune responses[J].Annual Review Immunology,1998,16:225-260.
[25] SKJOLAAS K A,BURKEY T E,DRITZ S S,et al.Effects of Salmonella enterica serovars Typhimurium and Choleraesusis on chemokine and cytokine expression in swine ileum and jejunal epithelial cells[J].Veterinary Immunology and Immunopathology,2006,111(3/4):119-209.
[26] MEANS T K,HAYASHI F,SMITH K D,et al.The toll-like recetpor 5 stimulus bacterial flagell in induces maturation and chemokine production in human dendritic cells[J].Journal of Immunology,2003,170(10):5165-5175.
[27] TAKEDA K,AKIRA S.Toll receptors and pathogen resistance[J].Cell Micobiology,2003,5(3):143-153.
[28] MAASER C,KAGOFF M F.Role of the intestinal epithelium in orchestrating innate and adaptive mucosal immunity[J].Gastroenterology,2002,40(7):525-529.  
[29] KIRBY A C,YIRLID U,WICK M J.The innate immune response differs in primary and secondary Salmonella infection[J].Journal of Immunology,2002,169(8):4450-4459.
[30] MILLAR A D,RAMPTON D S,BLAKE D R.Effects of iron and iron chelation in vitro on mucosal oxidant activity in ulcerative colitis[J].Alimentary Pharmacology & Therapeutics,2000,14(9):1163-1168.  
[31] BERGERON R J,WIEGAND J,WEIMAR W R,et al.Prevention of acetic acid-induced colitis by desferrithiocin analogs in a rat model[J].Digestive Diseases and Sciences,2003,48(2):399-407.  
[32] SERIL D N,LIAO J,HO K L,et al.Dietary iron supplementation enhances DSS-induced colitis and associated colorectal carcinoma development in mice[J].Digestive Diseases and Sciences,2002,47(6):1266-1278.  
[33] WILSON A,REYES E,OFMAN J.Prevalence and outcomes of anemia in inflammatory bowel disease:a systematic review of the literature[J].American Journal of Medicine,2004,116(Suppl.7A):44S-49S.
[34] BYRD T F,HORWITZ M A.Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular mulitplication of Legionella pneumophila by limiting the availability of iron[J].Journal of Clinical Investigation,1989,83(5):1457-1465.  
[35] YEH K Y,YEH M,GLASS J.Hepcidin regulation of ferroportin 1 expression in the liver and intestine of the rat[J].American Journal of Physiology-Gastrointestinal and Liver Physiology,2004,286(3):G385-G394.[JP+1]
[36] PEPPERCORN M A.Is there a role for antibiotics as primary therapy in Crohn’s ileitis?[J].Journal of Clinical Gastroenterology,1993,17(3):235-237.  
[37] NICOLAS G,BENNOUN M,DEVAUX I,et al.Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice[J].Proceedings of the National Academy of Sciences of the United States of America,2001,98(15):8780-8785.  
[38] BURPEE T,MITCHELL P,FISHMAN D,et al.Intestinal ferroportin expression in pediatric Crohn’s disease[J].Inflammatory Bowel Diseases,2011,17(2):524-531.  
[39] NEMETH F,RIVERA S,GABAYAN V,et al.IL-6 mediates hypoferremia of inflammation by inducting the synthersis of the iron regulatory hormone hepcidin[J].Journal of Clinical Investigation,2004,113(9):1271-1276.
[40] YANG F,LIU X B,QUINONES M,et al.Regulation of reticuloendothelial iron transporter MTP1 by inflammation[J].Journal of Biological Chemistry,2002,277:39786-39791.
[41] JOHNSON E E,SANDGREN A,CHERAYIL B J,et al.Role of ferroportin in macrophage-mediated immunity[J].Infection and Immunity,2010,78(12):5099-5106.  
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