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

Avian Pathology

Volumn 41, Issue 4, 2012, Pages 361-367

  Zhang, Bingkun ^a   Shao, Yuxin ^a   Liu, Dan ^a   Yin, Peihui ^b   Guo, Yuming ^a   Yuan, Jianmin ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b Beijing Resource Feed Co Ltd   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 1; ENDOTOXIN; MESSENGER RNA; MUCIN 2; OCCLUDIN; SUCRASE; ZINC;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ANIMAL SALMONELLOSIS; ARTICLE; BIRD DISEASE; BLOOD; CHICKEN; DIET; DIET SUPPLEMENTATION; DRUG EFFECT; ENZYMOLOGY; GENETICS; ILEUM; INTESTINE MUCOSA; MALE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; RANDOMIZATION; SALMONELLA TYPHIMURIUM; WEIGHT GAIN;

ANIMAL FEED; ANIMALS; CHICKENS; CLAUDIN-1; DIET; DIETARY SUPPLEMENTS; ENDOTOXINS; ILEUM; INTESTINAL MUCOSA; MALE; MUCIN-2; OCCLUDIN; POULTRY DISEASES; RANDOM ALLOCATION; RNA, MESSENGER; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SUCRASE; WEIGHT GAIN; ZINC;

EID: 84867856476     PISSN: 03079457     EISSN: 14653338     Source Type: Journal    
DOI: 10.1080/03079457.2012.692155     Document Type: Article

References (55)

1. 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.
2. 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.
3. 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.
4. 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.
5. Bucker, R., Schumann, M., Amasheh, S. and Schulzke, J.D. 2010. Claudins in intestinal function and disease. Current Topics in Membranes, 65: 195-227.
6. 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.
7. China 2004. Feeding Standard of Chicken. Ministry of Agriculture of the People's Republic of China.
8. Cho, C.H. 1989. Current views of zinc as a gastrohepatic protective agent. Drug Development Research, 17: 185-197.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. Gumbiner, B.M. 1993. Breaking through the tight junction barrier. Journal of Cell Biology, 123: 1631-1633.
18. Hecht, G. 1999. Innate mechanisms of epithelial host defense: spotlight on intestine. American Journal of Physiology-Cell Physiology, 277: C351-C358.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. Landau, D. 2006. Epithelial paracellular proteins in health and disease. Current Opinion in Nephrology and Hypertension, 15: 425-429.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. Rabsch, W., Tschape, H. and Baumler, A.J. 2001. Non-typhoidal salmonellosis: emerging problems. Microbes and Infection, 3: 237-247.
35. 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.
36. 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.
37. 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.
38. 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.
39. Semrad, C.E. 1999. Zinc and intestinal function. Current Gastroenterology Reports, 1: 398-403.
40. Sousa, S., Lecuit, M. and Cossart, P. 2005. Microbial strategies to target, cross or disrupt epithelia. Current Opinion in Cell Biology, 17: 489-498.
41. 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.
42. 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.
43. Suzuki, S. 1994. Pathogenicity of Salmonella enteritidis in poultry. International Journal of Food Microbiology, 21: 89-105.
44. 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.
45. Theodoropoulos, G. and Carraway, K.L. 2007. Molecular signaling in the regulation of mucins. Journal of Cellular Biochemistry, 102: 1103-1116.
46. 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.
47. 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.
48. Turner, J.R. 2006. Molecular basis of epithelial barrier regulation-From basic mechanisms to clinical application. American Journal of Pathology, 169: 1901-1909.
49. Vallee, B.L. and Falchuk, K.H. 1993. The biochemical basis of zinc physiology. Physiological Reviews, 73: 79-118.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.