Basis and regulation of gut barrier function and epithelial cell protection: Applications to the weaned pig

Dynamics in Animal Nutrition

Volumn , Issue , 2010, Pages 31-51

  Lalles J P ^a  

^a CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882648672     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.3921/978-90-8686-706-6     Document Type: Chapter

References (84)

1. Al-Sadi, R., Boivin, M., Ma, T., 2009. Mechanism of cytokine modulation of epithelial tight junction barrier. Frontiers in Bioscience 14: 2765-2778.
2. Arvans, D.L., Vavricka, S.R., Ren, H., Musch, M.W., Kang, L., Rocha, F.G., Lucioni, A., Turner, J.R., Alverdy, J., Chang, E.B., 2005. Luminal bacterial flora determines physiological expression of intestinal epithelial cytoprotective heat shock proteins 25 and 72. American Journal of Physiology, Gastrointestinal and Liver Physiology 288: G696-G704.
3. Abreu, M.T., Fukata, M., Arditi, M., 2005. TLR signaling in the gut in health and disease. Journal of Immunology 174: 4453-4460.
4. Barreau, F., Cartier, C., Ferrier, L., Fioramonti, J., Bueno, L., 2004a. Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats. Gastroenterology 127: 524-534.
5. Barreau, F., Ferrier, L., Fioramonti, J., Bueno, L., 2004b. Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut 53: 501-506.
6. Barreau, F., de Lahitte, J.D., Ferrier, L., Frexinos, J., Bueno, L., Fioramonti, J., 2006. Neonatal maternal deprivation promotes Nippostrongylus brasiliensis infection in adult rats. Brain Behavour & Immunology 20:254-260.
7. Barreau, F., Cartier, C., Leveque, M., Ferrier, L., Moriez, R., Laroute, V., Rosztoczy, A., Fioramonti, J., Bueno, L., 2007. Pathways involved in gut mucosal barrier dysfunction induced in adult rats by maternal deprivation: corticotrophin-releasing factor and nerve growth factor interplay. Journal of Physiology 580: 347-356.
8. Barreau, F., Salvador-Cartier, C., Houdeau, E., Bueno, L., Fioramonti, J., 2008. Longterm alterations of colonic nerve-mast cell interactions induced by neonatal maternal deprivation in rats. Gut 57: 582-590.
9. Boudry, G., Péron V., Le Huërou-Luron I., Lallès J.P., Sève, B. 2004. Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. Journal of Nutrition 134: 2256-2262.
10. Boudry, G., Douard, V., Mourot, J., Lallès, J.P., Le Huërou-Luron, I., 2009. Linseed oil in the maternal diet during gestation and lactation modifies fatty acid composition, mucosal architecture, and mast cell regulation of the ileal barrier in piglets. Journal of Nutrition 139: 1110-1117.
11. Cario, E., 2005. Bacterial interactions with cells of the intestinal mucosa: TOLL-like receptors and NOD2. Gut 54: 1182-1193.
12. Cario, E., Gerken, G., Podolsky, D.K., 2007. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 132: 1359-1374.
13. Carlson, D., Poulsen, H.D., Sehested, J. 2004. Influence of weaning and effect of post weaning dietary zinc and copper on electrophysiological response to glucose, theophylline and 5-HT in piglet small intestinal mucosa. Comparative Biochemistry & Physiology A 137: 757-765.
14. Carlson, D., Sehested J., Poulsen, H.D., 2006. Zinc reduces the electrophysiological responses in vitro to basolateral receptor mediated secretagogues in piglet small intestinal epithelium. Comparative Biochemistry & Physiology A 144: 514-519.
15. Carlson, D., Sehested J., Feng, Z., Poulsen, H.D., 2008. Serosal zinc attenuate serotonin and vasoactive intestinal peptide induced secretion in piglet small intestinal epithelium in vitro. Comparative Biochemistry & Physiology A 149: 51-58.
16. Carlson, R.M., Vavricka, S.R., Eloranta, J.J., Musch, M.W., Arvans, D.L., Kles, K.A., Walsh-Reitz, M.M., Kullak-Ublick, G.A., Chang, E.B., 2007. fMLP induces Hsp27 expression, attenuates NF-kappaB activation, and confers intestinal epithelial cell protection. American Journal of Physiology, Gastrointestinal and Liver Physiology 292: G1070-G1078.
17. Collins, S.M., Bercik, P., 2009. The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 136: 2003-2014.
18. Dalle-Donne, I., Rossi, R., Milzani, A., Di Simplicio, P., Colombo, R., 2001. The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radical Biology & Medicine 31: 1624-1632.
19. David, J.C., Grongnet, J.F., Lallès, J.P. 2002. Weaning affects the expression of heat shock proteins in different regions of the gastrointestinal tract of piglets. Journal of Nutrition 132: 2551-2561.
20. Dokladny, K., Moseley, P.L., Ma T.Y., 2006. Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. American Journal of Physiology, Gastrointestinal and Liver Physiology 290: G204-G212.
21. Ehrenfried, J.A., Chen, J., Li, J., Evers, B.M., 1995. Glutamine-mediated regulation of heat shock protein expression in intestinal cells. Surgery 118: 352-357.
22. Eutamene, H., Lamine, F., Chabo, C., Theodorou, V., Rochat, F., Bergonzelli, G.E., Corthésy-Theulaz, I., Fioramonti, J., Bueno, L., 2007. Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats. Journal of Nutrition 137: 1901-1907.
23. Fak, F., Ahrne S., Linderoth A., Molin, G., Jeppsson, B., Weström, B., 2008a. Age-related effects of the probiotic bacterium Lactobacillus plantarum 299v on gastrointestinal function in suckling rats. Digestive Disease & Science 53: 664-671.
24. Fak, F., Ahrne S., Molin, G., Jeppsson, B., Weström, B., 2008b. Microbial manipulation of the rat dam changes bacterial colonization and alters properties of the gut in her offspring. American Journal of Physiology, Gastrointestinal and Liver Physiology 294: G148-G154.
25. Feng, Z., Carlson, D., Poulsen, H.D., 2006. Zinc attenuates forskolin-stimulated electrolyte secretion without involvement of the enteric nervous system in small intestinal epithelium from weaned piglets. Comparative Biochemistry & Physiology A 145: 328-333.
26. Finamore, A., Massimi, M., Conti Devirgiliis, L., Mengheri, E., 2008. Zinc deficiency induces membrane barrier damage and increases neutrophil transmigration in Caco-2 cells. Journal of Nutrition 138: 1664-1670.
27. Gabler, N.K., Spencer, J.D., Webel, D.M., Spurlock, M.E., 2007. In utero and postnatal exposure to long chain (n-3) PUFA enhances intestinal glucose absorption and energy stores in weanling pigs. Journal of Nutrition 137: 2351-2358.
28. Gabler, N.K., Radcliffe, J.S., Spencer, J.D., Webel, D.M., Spurlock, M.E., 2009. Feeding long-chain n-3 polyunsaturated fatty acids during gestation increases intestinal glucose absorption potentially via the acute activation of AMPK. Journal of Nutritional Biochemistry 20: 17-25.
29. Gallois, M., Rothkötter, H.J., Bailey, M., Stokes, C.R., Oswald, I.P., 2009. Natural alternatives to in-feed antibiotics in pig production: Can immunomodulators play a role? Animal 3:1644-1661.
30. García-Rodenas, C.L., Bergonzelli, G.E., Nutten, S., Schumann, A., Cherbut, C., Turini, M., Ornstein, K., Rochat, F., Corthésy-Theulaz, I., 2006. Nutritional approach to restore impaired intestinal barrier function and growth after neonatal stress in rats. Journal of Pediatrics, Gastroenterology & Nutrition 43: 16-24.
31. Gareau, M.G., Jury, J., Yang, P.C., MacQueen, G., Perdue, M.H., 2006. Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance. Pediatric Research 59: 83-88.
32. Gareau, M.G., Jury, J., MacQueen, G., Sherman, P.M., Perdue, M.H., 2007a. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 56: 1522-1528.
33. Gareau, M.G., Jury, J., Perdue, M.H., 2007b. Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability. American Journal of Physiology, Gastrointestinal and Liver Physiology 293: G198-G203.
34. Gareau, M.G., Silva, M.A., Perdue, M.H., 2008. Pathophysiological mechanisms of stressinduced intestinal damage. Current Molecular Medicine 8: 274-281.
35. Harhaj, N.S., Antonetti, D.A., 2004. Regulation of tight junctions and loss of barrier function in pathophysiology. International Journal of Biochemistry & Cell Biology 36: 1206-1237.
36. Hedemann, M.S., Jensen, B.B., Poulsen, H.D., 2006. Influence of dietary zinc and copper on digestive enzyme activity and intestinal morphology in weaned pigs. Journal of Animal Science 84: 3310-3320.
37. Kojima, K., Musch, M.W., Ren, H., Boone, D.L., Hendrickson, B.A., Ma, A., Chang, E.B., 2003. Enteric flora and lymphocyte-derived cytokines determine expression of heat shock proteins in mouse colonic epithelial cells. Gastroenterology 124: 1395-1407.
38. Kojima, K., Musch, M.W., Ropeleski, M.J., Boone, D.L., Ma, A., Chang, E.B., 2004. Escherichia coli LPS induces heat shock protein 25 in intestinal epithelial cells through MAP kinase activation. American Journal of Physiology, Gastrointestinal and Liver Physiology 286: G645-G652.
39. Konstantinov, S.R., Smidt, H., Akkermans, A.D., Casini, L., Trevisi, P., Mazzoni, M., De Filippi, S., Bosi, P., de Vos, W.M., 2008. Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets. FEMS Microbiology & Ecology; 66: 599-607.
40. Lallès, J.P., Boudry, G., Favier, C., Le Floc'h, N., Luron, I., Montagne, L., Oswald, I.P., Pié, S., Piel, C., Sève, B., 2004. Gut function and dysfunction in young pigs: physiology. Animal Research 53: 301-316.
41. Lallès, J.P., Bosi P., Smidt H., Stokes, C.R., 2007. Nutritional management of gut health in pigs around weaning. Proceedings of the Nutrition Society 66: 260-268.
42. Lallès J.P., Bosi P., Janczyk P., Koopmans S.J., Torrallardona D., 2009. Impact of bioactive substances on the gastrointestinal tract and performance of weaned piglets: a review. Animal 3: 1625-1643.
43. Lebeer, S., Vanderleyden, J., De Keersmaecker, S.C., 2008. Genes and molecules of lactobacilli supporting probiotic action. Microbiology & Molecular Biology Reviews 72: 728-764.
44. Ma, T.Y., Anderson, J.M., 2006. Tight junctions and intestinal barrier. In: Johnson, L.R., (ed.) Physiology of the gastrointestinal tract. Academic Press, New York, USA, Volume 1, pp. 1559-1594.
45. Malago, J.J., Koninkx, J.F., Van Dijk, J.E., 2002. The heat shock response and cytoprotection of the intestinal epithelium. Cell Stress Chaperones 7: 191-199.
46. McCracken, B.A., Spurlock, M.E., Roos, M.A., Zuckermann, F.A., Gaskins, H.R., 1999. Weaning anorexia may contribute to local inflammation in the piglet small intestine. Journal of Nutrition 129: 613-619.
47. McKay, D.M., Baird, A.W., 1999. Cytokine regulation of epithelial permeability and ion transport. Gut 44: 283-289.
48. Moeser, A.J., Klok, C.V., Ryan, K.A., Wooten, J.G., Little, D., Cook, V.L., Blikslager, A.T., 2007a. Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. American Journal of Physiology, Gastrointestinal and Liver Physiology 292: G173-G181.
49. Moeser, A.J., Ryan, K.A., Nighot, P.K., Blikslager, A.T., 2007b. Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs. American Journal of Physiology, Gastrointestinal and Liver Physiology 293: G413-G421.
50. Montagne, L., Boudry, G., Favier, C., Le Huërou-Luron, I., Lallès, J.P., Sève, B., 2007. Main intestinal markers associated with the changes in gut architecture and function in piglets after weaning. British Journal of Nutrition 97: 45-57.
51. Musch, M.W., Petrof, E.O., Kojima, K., Ren, H., McKay, D.M., Chang, E.B., 2004. Bacterial superantigen-treated intestinal epithelial cells upregulate heat shock proteins 25 and 72 and are resistant to oxidant cytotoxicity. Infection & Immunity 72: 3187-3194.
52. Nutten, S., Schumann, A., Donnicola, D., Mercenier, A., Rami, S., Garcia-Rodenas, C.L., 2007. Antibiotic administration early in life impairs specific humoral responses to an oral antigen and increases intestinal mast cell numbers and mediator concentrations. Clinical & Vaccine Immunology 14: 190-197.
53. Ohkawara, T., Takeda, H., Kato, K., Miyashita, K., Kato, M., Iwanaga, T., Asaka, M., 2005. Polaprezinc (N-(3-aminopropionyl)-L-histidinato zinc) ameliorates dextran sulfate sodium-induced colitis in mice. Scandinavian Journal of Gastroenterology 40: 1321-1327.
54. Ohkawara, T., Nishihira, J., Nagashima, R., Takeda, H., Asaka, M., 2006. Polaprezinc protects human colon cells from oxidative injury induced by hydrogen peroxide: relevant to cytoprotective heat shock proteins. World Journal of Gastroenterology 12: 6178-6181.
55. Ou, D., Li, D., Cao, Y., Li, X., Yin, J., Qiao, S., Wu, G., 2007. Dietary supplementation with zinc oxide decreases expression of the stem cell factor in the small intestine of weanling pigs. Journal of Nutritional Biochemistry 18: 820-826.
56. Ovelgonne, J.H., Koninkx, J.F., Pusztai, A., Bardocz, S., Kok, W., Ewen, S.W., Hendriks, H.G., Van Dijk, J.E., 2000. Decreased levels of heat shock proteins in gut epithelial cells after exposure to plant lectins. Gut 46: 679-687.
57. Otaka, M., Odashima, M., Watanabe, S., 2006. Role of heat shock proteins (molecular chaperones) in intestinal mucosal protection. Biochemical and Biophysical Research Communications 348: 1-5.
58. Palazzo, M., Gariboldi, S., Zanobbio, L., Selleri, S., Dusio, G.F., Mauro, V., Rossini, A., Balsari, A., Rumio, C., 2008. Sodium-dependent glucose transporter-1 as a novel immunological player in the intestinal mucosa. Journal of Immunology 181: 3126-3136. Erratum in: Journal of Immunology 181: 7428.
59. Panasenko, O.O., Kim, M.V., Marston, S.B., Gusev, N.B., 2003. Interaction of the small heat shock protein with molecular mass 25 kDa (hsp25) with actin. European Journal of Biochemistry 270: 892-901.
60. Pappenheimer, JR., 1988. Physiological regulation of epithelial junctions in intestinal epithelia. Acta Physiologica Scandinavica Supplement 571:43-51.
61. Petrof, E.O., Ciancio, M.J., Chang, E.B., 2004. Role and regulation of intestinal epithelial heat shock proteins in health and disease. Chinese Journal of Digestive Disease 5: 45-50.
62. Petrof, E.O., Musch, M.W., Ciancio, M., Sun, J., Hobert, M.E., Claud, E.C., Gewirtz, A., Chang, E.B., 2008. Flagellin is required for salmonella-induced expression of heat shock protein Hsp25 in intestinal epithelium. American Journal of Physiology, Gastrointestinal and Liver Physiology 294: G808-G818.
63. Phanvijhitsiri, K., Musch, M.W., Ropeleski, M.J., Chang, E.B., 2006. Heat induction of heat shock protein 25 requires cellular glutamine in intestinal epithelial cells. American Journal of Physiology, Cell Physiology 291: C290-C299.
64. Pié, S., Lallès, J.P., Blazy, F., Laffitte, J., Sève, B., Oswald, I.P., 2004. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. Journal of Nutrition 134: 641-647.
65. Pluske, J.R., Hampson, D.J., Williams, I.H., 1997. Factors influencing the structure and function of the small intestine in the weaned pig: A review. Livestock Production Science 51: 215-236.
66. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., Medzhitov, R., 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
67. Ren, H., Musch, M.W., Kojima, K., Boone, D., Ma, A., Chang, E.B., 2001. Short-chain fatty acids induce intestinal epithelial heat shock protein 25 expression in rats and IEC 18 cells. Gastroenterology 121: 631-639.
68. Ropeleski, M.J., Tang, J., Walsh-Reitz, M.M., Musch, M.W., Chang, E.B., 2003. Interleukin-11-induced heat shock protein 25 confers intestinal epithelial-specific cytoprotection from oxidant stress. Gastroenterology 124: 1358-1368.
69. Roselli, M., Finamore, A., Garaguso, I., Britti M.S.,, Mengheri, E., 2003. Zinc oxide protects cultured enterocytes from the damage induced by Escherichia coli. Journal of Nutrition 133: 4077-4082.
70. Roselli, M., Finamore, A., Britti, M.S., Konstantinov, S.R., Smidt, H., de Vos, W.M., Mengheri, E., 2007. The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. Journal of Nutrition 137: 2709-2716.
71. Schroeder, B., Duncker, S., Barth, S., Bauerfeind, R., Gruber, A.D., Deppenmeier, S., Breves, G., 2006. Preventive effects of the probiotic Escherichia coli strain Nissle 1917 on acute secretory diarrhea in a pig model of intestinal infection. Digestive Disease & Science 51: 724-731.
72. Schumann, A., Nutten, S., Donnicola, D., Comelli, E.M., Mansourian, R., Cherbut, C., Corthesy-Theulaz, I., Garcia-Rodenas, C., 2005. Neonatal antibiotic treatment alters gastrointestinal tract developmental gene expression and intestinal barrier transcriptome. Physiological Genomics, 23: 235-245.
73. Siggers, R.H., Siggers, J., Boye, M., Thymann, T., Mølbak, L., Leser, T., Jensen, B.B., Sangild, P.T., 2008. Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs. Journal of Nutrition 138: 1437-1444.
74. Singleton, K.D., Wischmeyer, P.E., 2006. Oral glutamine enhances heat shock protein expression and improves survival following hyperthermia. Shock 25: 295-299.
75. Soderholm, J.D., Yates, D.A., Gareau, M.G., Yang, P.C., MacQueen, G., Perdue, M.H., 2002. Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. American Journal of Physiology, Gastrointestinal and Liver Physiology 283: G1257-G1263.
76. Soderholm, J.D., Perdue M.H., 2006. Effect of stress on intestinal mucosal function. In: Johnson, L.R. (Ed.), Physiology of the gastrointestinal tract. Academic Press, New York, USA, Volume 1, pp. 763-780.
77. Spreeuwenberg, M.A., Verdonk, J.M., Gaskins, H.R., Verstegen, M.W., Wang, J., Chen, L., Li, P., Li, X., Zhou, H., 2001. Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning. Journal of Nutrition 131: 1520-1527.
78. Tao, Y., Drabik, K.A., Waypa, T.S., Musch, M.W., Alverdy, J.C., Schneewind, O., Chang, E.B., Petrof, E.O., 2006. Soluble factors from Lactobacillus GG activate MAPKs and induce cytoprotective heat shock proteins in intestinal epithelial cells. American Journal of Physiology, Gastrointestinal and Liver Physiology 290: C1018-C1830. Erratum in: American Journal of Physiology, Gastrointestinal and Liver Physiology 291: C194.
79. Van Beers-Schreurs, H.M., Nabuurs, M.J., Vellenga, L., Kalsbeek-Van der Valk, H.J., Wensing, T., Breukink, H.J., 1998. Weaning and the weanling diet influence the villous height and crypt depth in the small intestine of pigs and alter the concentrations of short-chain fatty acids in the large intestine and blood. Journal of Nutrition 128: 947-953.
80. Wischmeyer, P.E., Musch, M.W., Madonna, M.B., Thisted, R., Chang, E.B., 1997. Glutamine protects intestinal epithelial cells: role of inducible HSP70. American Journal of Physiology 272: G879-G884.
81. Yu, L.C., Flynn, A.N., Turner, J.R., Buret, A.G., 2005. SGLT-1-mediated glucose uptake protects intestinal epithelial cells against LPS-induced apoptosis and barrier defects: a novel cellular rescue mechanism? FASEB Journal 19: 1822-1835.
82. Yu, L.C., Huang, C.Y., Kuo, W.T., Sayer, H., Turner, J.R., Buret, A.G., 2008. SGLT-1-mediated glucose uptake protects human intestinal epithelial cells against Giardia duodenalis-induced apoptosis. International Journal of Parasitology 38: 923-934.
83. Zhang, B., 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.
84. Zyrek, A.A., Cichon, C., Helms, S., Enders, C., Sonnenborn, U., Schmidt, M.A., 2006. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiology 9: 804-816.