2,809
Views
62
CrossRef citations to date
0
Altmetric
ORIGINAL ARTICLES

Zinc prevents Salmonella enterica serovar Typhimurium-induced loss of intestinal mucosal barrier function in broiler chickens

, , , , &
Pages 361-367 | Received 24 Feb 2012, Accepted 02 Apr 2012, Published online: 27 Jul 2012

References

  • Altaf , W. , Perveen , S. , Rehman , K.U. , Teichberg , S. , Vancurova , I. , Harper , R.G. and Wapnir , R.A. 2002 . Zinc supplementation in oral rehydration solutions: experimental assessment and mechanisms of action . Journal of the American College of Nutrition , 21 : 26 – 32 .
  • Ballard , S.T. , Hunter , J.H. and Taylor , A.E. 1995 . Regulation of tight-junction permeability during nutrient absorption across the intestinal epithelium . Annual Review of Nutrition , 15 : 35 – 55 .
  • Berkes , J. , Viswanathan , V.K. , Savkovic , S.D. and Hecht , G. 2003 . Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation . Gut , 52 : 439 – 451 .
  • Boyle , E.C. , Brown , N.F. and Finlay , B.B. 2006 . Salmonella enterica serovar Typhimurium effectors SopB, SopE, SopE2 and SipA disrupt tight junction structure and function . Cellular Microbiology , 8 : 1946 – 1957 .
  • Bucker , R. , Schumann , M. , Amasheh , S. and Schulzke , J.D. 2010 . Claudins in intestinal function and disease . Current Topics in Membranes , 65 : 195 – 227 .
  • Cario , E. , Jung , S. , d'Heureuse , J.H. , Schulte , C. , Sturm , A. , Wiedenmann , B. , Goebell , H. and Dignass , A.U. 2000 . Effects of exogenous zinc supplementation on intestinal epithelial repair in vitro . European Journal of Clinical Investigation , 30 : 419 – 428 .
  • China 2004 . Feeding Standard of Chicken . Ministry of Agriculture of the People's Republic of China .
  • Cho , C.H. 1989 . Current views of zinc as a gastrohepatic protective agent . Drug Development Research , 17 : 185 – 197 .
  • Clarke , J.M. , Pelton , N.C. , Bajka , B.H. , Howarth , G.S. , Read , L.C. and Butler , R.N. 2006 . Use of the C-13-sucrose breath test to assess chemotherapy-induced small intestinal mucositis in the rat . Cancer Biology & Therapy , 5 : 34 – 38 .
  • Desmidt , M. , Ducatelle , R. and Haesebrouck , F. 1998 . Immunohistochemical observations in the ceca of chickens infected with Salmonella enteritidis phage type four . Poultry Science , 77 : 73 – 74 .
  • Duff , M. and Ettarh , R.R. 2002 . Crypt cell production rate in the small intestine of the zinc-supplemented mouse . Cells Tissues Organs , 172 : 21 – 28 .
  • Fanning , A.S. , Jameson , B.J. , Jesaitis , L.A. and Anderson , J.M. 1998 . The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton . Journal of Biological Chemistry , 273 : 29745 – 29753 .
  • Fasina , Y.O. , Hoerr , F.J. , McKee , S.R. and Conner , D.E. 2010 . Influence of Salmonella enterica serovar Typhimurium infection on intestinal goblet cells and villous morphology in broiler chicks . Avian Diseases , 54 : 841 – 847 .
  • Fasina , Y.O. , Holt , P.S. , Moran , E.T. , Moore , R.W. , Conner , D.E. and McKee , S.R. 2008 . Intestinal cytokine response of commercial source broiler chicks to Salmonella typhimurium infection . Poultry Science , 87 : 1335 – 1346 .
  • Finamore , A. , Massimi , M. , Devirgiliis , L.C. and Mengheri , E. 2008 . Zinc deficiency induces membrane barrier damage and increases neutrophil transmigration in Caco-2 cells . Journal of Nutrition , 138 : 1664 – 1670 .
  • Gaudier , E. , Jarry , A. , Blottiere , H.M. , de Coppet , P. , Buisine , M.P. , Aubert , J.P. , Laboisse , C. , Cherbut , C. and Hoebler , C. 2004 . Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose . American Journal of Physiology-Gastrointestinal and Liver Physiology , 287 : G1168 – G1174 .
  • Gumbiner , B.M. 1993 . Breaking through the tight junction barrier . Journal of Cell Biology , 123 : 1631 – 1633 .
  • Hecht , G. 1999 . Innate mechanisms of epithelial host defense: spotlight on intestine . American Journal of Physiology-Cell Physiology , 277 : C351 – C358 .
  • Hegazy , S.M. and Adachi , Y. 2000 . Comparison of the effects of dietary selenium, zinc, and selenium and zinc supplementation on growth and immune response between chick groups that were inoculated with Salmonella and aflatoxin or Salmonella . Poultry Science , 79 : 331 – 335 .
  • Jepson , M.A. , Collaresbuzato , C.B. , Clark , M.A. , Hirst , B.H. and Simmons , N.L. 1995 . Rapid disruption of epithelial barrier function by Salmonella typhimurium is associated with structural modification of intercellular-junctions . Infection and Immunity , 63 : 356 – 359 .
  • Jepson , M.A. , Schlecht , H.B. and Collares-Buzato , C.B. 2000 . Localization of dysfunctional tight junctions in Salmonella enterica serovar Typhimurium-infected epithelial layers . Infection and Immunity , 68 : 7202 – 7208 .
  • Kaiser , P. , Rothwell , L. , Galyov , E.E. , Barrow , P.A. , Burnside , J. and Wigley , P. 2000 . Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum . Microbiology , 146 : 3217 – 3226 .
  • Koehler , H. , Sakaguchi , T. , Hurley , B.P. , Kase , B.J. , Reinecker , H.-C. and McCormick , B.A. 2007 . Salmonella enterica serovar Typhimurium regulates intercellular junction proteins and facilitates transepithelial neutrophil and bacterial passage . American Journal of Physiology-Gastrointestinal and Liver Physiology , 293 : G178 – G187 .
  • Kops , S.K. , Lowe , D.K. , Bement , W.M. and West , A.B. 1996 . Migration of Salmonella typhi through intestinal epithelial monolayers: an in vitro study . Microbiology and Immunology , 40 : 799 – 811 .
  • Kucharzik , T. , Walsh , S.V. , Chen , J. , Parkos , C.A. and Nusrat , A. 2001 . Neutrophil transmigration in inflammatory bowel disease is associated with differential expression of epithelial intercellular junction proteins . American Journal of Pathology , 159 : 2001 – 2009 .
  • Lamb-Rosteski , J.M. , Kalischuk , L.D. , Inglis , G.D. and Buret , A.G. 2008 . Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation . Infection and Immunity , 76 : 3390 – 3398 .
  • Lambert , J.C. , Zhou , Z.X. , Wang , L.P. , Song , Z.Y. , McClain , C.J. and Kang , Y.J. 2004 . Preservation of intestinal structural integrity by zinc is independent of metallothionein in alcohol-intoxicated mice . American Journal of Pathology , 164 : 1959 – 1966 .
  • Landau , D. 2006 . Epithelial paracellular proteins in health and disease . Current Opinion in Nephrology and Hypertension , 15 : 425 – 429 .
  • Liljebjelke , K.A. , Hofacre , C.L. , Liu , T.R. , White , D.G. , Ayers , S. , Young , S. and Maurer , J.J. 2005 . Vertical and horizontal transmission of Salmonella within integrated broiler production system . Foodborne Pathogens and Disease , 2 : 90 – 102 .
  • Loppnow , H. , Brade , L. , Brade , H. , Rietschel , E.T. , Kusumoto , S. , Shiba , T. and Flad , H.D. 1986 . Induction of human interleukin-1 by bacterial and synthetic lipid-A . European Journal of Immunology , 16 : 1263 – 1267 .
  • Nakamura , A. , Ota , Y. , Mizukami , A. , Ito , T. , Ngwai , Y.B. and Adachi , Y. 2002 . Evaluation of Aviguard, a commercial competitive exclusion product for efficacy and after-effect on the antibody response of chicks to salmonella . Poultry Science , 81 : 1653 – 1660 .
  • Opitz , B. , Hippenstiel , S. , Eitel , J. and Suttorp , N. 2007 . Extra- and intracellular innate immune recognition in endothelial cells . Thrombosis and Haemostasis , 98 : 319 – 326 .
  • Parlesak , A. , Schafer , C. , Schutz , T. , Bode , J.C. and Bode , C. 2000 . Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease . Journal of Hepatology , 32 : 742 – 747 .
  • Rabsch , W. , Tschape , H. and Baumler , A.J. 2001 . Non-typhoidal salmonellosis: emerging problems . Microbes and Infection , 3 : 237 – 247 .
  • Rapp , C. , Johnson , A.B. , Fakler , T.M. , Ward , T.L. and Quarks , C.L. 2004 . Effect of zinc source on intestinal lesions and performance of broilers exposed to coccidiosis . Zootecnica International , 2 : 40 – 43 .
  • Rodriguez , P. , Darmon , N. , Chappuis , P. , Candalh , C. , Blaton , M.A. , Bouchaud , C. and Heyman , M. 1996 . Intestinal paracellular permeability during malnutrition in guinea pigs: effect of high dietary zinc . Gut , 39 : 416 – 422 .
  • Roselli , M. , Finamore , A. , Garaguso , I. , Britti , M.S. and Mengheri , E. 2003 . Zinc oxide protects cultured enterocytes from the damage induced by Escherichia coli . Journal of Nutrition , 133 : 4077 – 4082 .
  • Roy , S.K. , Behrens , R.H. , Haider , R. , Akramuzzaman , S.M. , Mahalanabis , D. , Wahed , M.A. and Tomkins , A.M. 1992 . Impact of zinc supplementation on intestinal permeability in Banglandeshi children with acute diarrhea and persistent diarrhea syndrome . Journal of Pediatric Gastroenterology and Nutrition , 15 : 289 – 296 .
  • Semrad , C.E. 1999 . Zinc and intestinal function . Current Gastroenterology Reports , 1 : 398 – 403 .
  • Sousa , S. , Lecuit , M. and Cossart , P. 2005 . Microbial strategies to target, cross or disrupt epithelia . Current Opinion in Cell Biology , 17 : 489 – 498 .
  • Sturniolo , G.C. , Di Leo , V. , Ferronato , A. , D'Odorico , A. and D'Inca , R. 2001 . Zinc supplementation tightens “leaky gut” in Crohn's disease . Inflammatory Bowel Diseases , 7 : 94 – 98 .
  • Sturniolo , G.C. , Fries , W. , Mazzon , E. , Di Leo , V. , Barollo , M. and D'Inca , R. 2002 . Effect of zinc supplementation on intestinal permeability in experimental colitis . Journal of Laboratory and Clinical Medicine , 139 : 311 – 315 .
  • Suzuki , S. 1994 . Pathogenicity of Salmonella enteritidis in poultry . International Journal of Food Microbiology , 21 : 89 – 105 .
  • Tafazoli , F. , Magnusson , K.E. and Zheng , L.M. 2003 . Disruption of epithelial barrier integrity by Salmonella enterica serovar Typhimurium requires geranylgeranylated proteins . Infection and Immunity , 71 : 872 – 881 .
  • Theodoropoulos , G. and Carraway , K.L. 2007 . Molecular signaling in the regulation of mucins . Journal of Cellular Biochemistry , 102 : 1103 – 1116 .
  • Tran , C.D. , Howarth , G.S. , Coyle , P. , Philcox , J.C. , Rofe , A.M. and Butler , R.N. 2003 . Dietary supplementation with zinc and a growth factor extract derived from bovine cheese whey improves methotrexate-damaged rat intestine . American Journal of Clinical Nutrition , 77 : 1296 – 1303 .
  • Turnbull , P.C. and Snoeyenbos , G.H. 1974 . Experimental salmonellosis in the chicken. 1. Fate and host response in alimentary canal, liver, and spleen . Avian Diseases , 18 : 153 – 177 .
  • Turner , J.R. 2006 . Molecular basis of epithelial barrier regulation-From basic mechanisms to clinical application . American Journal of Pathology , 169 : 1901 – 1909 .
  • Vallee , B.L. and Falchuk , K.H. 1993 . The biochemical basis of zinc physiology . Physiological Reviews , 73 : 79 – 118 .
  • Van Klinken , B.J.-W. , Dekker , J. , Buller , H.A. and Einerhand , A.W.C. 1995 . Mucin gene structure and expression: protection vs. adhesion . American Journal of Physiology , 269 : G613 – G627 .
  • Van Leeuwen , P. , Mouwen , J. , Van der Klis , J.D. and Verstegen , M.W.A. 2004 . Morphology of the small intestinal mucosal surface of broilers in relation to age, diet formulation, small intestinal microflora and performance . British Poultry Science , 45 : 41 – 48 .
  • Vandeplas , S. , Dauphin , R.D. , Thiry , C. , Beckers , Y. , Welling , G.W. , Thonart , P. and Thewis , A. 2009 . Efficiency of a Lactobacillus plantarum-xylanase combination on growth performances, microflora populations, and nutrient digestibilities of broilers infected with Salmonella Typhimurium . Poultry Science , 88 : 1643 – 1654 .
  • Zhang , B. and Guo , Y. 2009 . Supplemental zinc reduced intestinal permeability by enhancing occludin and zonula occludens protein-1 (ZO-1) expression in weaning piglets . British Journal of Nutrition , 102 : 687 – 693 .
  • Zhang , S.P. , Kingsley , R.A. , Santos , R.L. , Andrews-Polymenis , H. , Raffatellu , M. , Figueiredo , J. , Nunes , J. , Tsolis , R.M. , Adams , L.G. and Baumler , A.J. 2003 . Molecular pathogenesis of Salmonella enterica serotype Typhimurium-induced diarrhea . Infection and Immunity , 71 : 1 – 12 .
  • Zhao , J. , Guo , Y.M. , Suo , X. and Yuan , J.M. 2006 . Effect of dietary zinc level on serum carotenoid levels, body and shank pigmentation of chickens after experimental infection with coccidia . Archives of Animal Nutrition , 60 : 218 – 228 .

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.