Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015, Article ID 304149, 11 pages
http://dx.doi.org/10.1155/2015/304149
Research Article

Enterococcus faecium NCIMB 10415 Modulates Epithelial Integrity, Heat Shock Protein, and Proinflammatory Cytokine Response in Intestinal Cells

1Institute of Veterinary Physiology, Department of Veterinary Medicine, Freie Universität Berlin, Oertzenweg 19b, 14163 Berlin, Germany
2Institute of Veterinary Biochemistry, Department of Veterinary Medicine, Freie Universität Berlin, Oertzenweg 19b, 14163 Berlin, Germany
3Institute of Food Hygiene, Department of Veterinary Medicine, Freie Universität Berlin, Königsweg 69, 14163 Berlin, Germany
4Institute of Microbiology and Epizootics, Department of Veterinary Medicine, Freie Universität Berlin, Robert-von-Ostertag-Straße 7-13, 14163 Berlin, Germany

Received 4 July 2014; Revised 25 September 2014; Accepted 26 September 2014

Academic Editor: Ishak O. Tekin

Copyright © 2015 Shanti Klingspor et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. Arvola, K. Laiho, S. Torkkeli et al., “Prophylactic Lactobacillus GG reduces antibiotic-associated diarrhea in children with respiratory infections: a randomized study,” Pediatrics, vol. 104, no. 5, article e64, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Guandalini, L. Pensabene, M. A. Zikri et al., “Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial,” Journal of Pediatric Gastroenterology and Nutrition, vol. 30, no. 1, pp. 54–60, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. C. M. Surawicz, L. V. McFarland, R. N. Greenberg et al., “The search for a better treatment for recurrent Clostridium difficile disease: use of high-dose vancomycin combined with Saccharomyces boulardii,” Clinical Infectious Diseases, vol. 31, no. 4, pp. 1012–1017, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Szajewska, M. Kotowska, J. Z. Mrukowicz, M. Armánska, and W. Mikolajczyk, “Efficacy of Lactobacillus GG in prevention of nosocomial diarrhea in infants,” The Journal of Pediatrics, vol. 138, no. 3, pp. 361–365, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. S. R. Konstantinov, H. Smidt, A. D. L. Akkermans et al., “Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets,” FEMS Microbiology Ecology, vol. 66, no. 3, pp. 599–607, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Agostoni, I. Axelsson, C. Braegger et al., “Probiotic bacteria in dietetic products for infants: a commentary by the ESPGHAN Committee on Nutrition,” The Journal of pediatric gastroenterology and nutrition, vol. 38, no. 4, pp. 365–374, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Alexopoulos, A. Karagiannidis, S. K. Kritas, C. Boscos, I. E. Georgoulakis, and S. C. Kyriakis, “Field evaluation of a bioregulator containing live Bacillus cereus spores on health status and performance of sows and their litters,” Journal of Veterinary Medicine Series A: Physiology Pathology Clinical Medicine, vol. 48, no. 3, pp. 137–145, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Breves, C. Walter, M. Burmester, and B. Schröder, “In vitro studies on the effects of Saccharomyces boulardii and Bacillus cereus var. toyoi on nutrient transport in pig jejunum,” Journal of Animal Physiology and Animal Nutrition, vol. 84, no. 1-2, pp. 9–20, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Kirchgessner, F. X. Roth, U. Eidelsburger, and B. Gedek, “The nutritive efficiency of Bacillus cereus as a probiotic in the raising of piglets. 1. Effect on the growth parameters and gastrointestinal environment,” Archiv für Tierernährung, vol. 44, no. 2, pp. 111–121, 1993. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Taras, W. Vahjen, M. Macha, and O. Simon, “Performance, diarrhea incidence, and occurrence of Escherichia coli virulence genes during long-term administration of a probiotic Enterococcus faecium strain to sows and piglets,” Journal of Animal Science, vol. 84, no. 3, pp. 608–617, 2006. View at Google Scholar · View at Scopus
  11. A. Zeyner and E. Boldt, “Effects of a probiotic Enterococcus faecium strain supplemented from birth to weaning on diarrhoea patterns and performance of piglets,” Journal of Animal Physiology and Animal Nutrition, vol. 90, no. 1-2, pp. 25–31, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Buydens and S. Debeuckelaere, “Efficacy of SF 68 in the treatment of acute diarrhea. A placebo-controlled trial,” Scandinavian Journal of Gastroenterology, vol. 31, no. 9, pp. 887–891, 1996. View at Publisher · View at Google Scholar · View at Scopus
  13. P. F. Wunderlich, L. Braun, L. Fumagalli et al., “Double-blind report on the efficacy of lactic acid-producing enterococcus SF68 in the prevention of antibiotic-associated diarrhoea and in the treatment of acute diarrhoea,” Journal of International Medical Research, vol. 17, no. 4, pp. 333–338, 1989. View at Google Scholar · View at Scopus
  14. A. Di Mauro, J. Neu, G. Riezzo et al., “Gastrointestinal function development and microbiota,” Italian Journal of Pediatrics, vol. 39, no. 1, article 15, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. P. M. Sherman, J. C. Ossa, and K. Johnson-Henry, “Unraveling mechanisms of action of probiotics,” Nutrition in Clinical Practice, vol. 24, no. 1, pp. 10–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Isolauri, M. Kaila, T. Arvola et al., “Diet during rotavirus enteritis affects jejunal permeability to macromolecules in suckling rats,” Pediatric Research, vol. 33, no. 6, pp. 548–553, 1993. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Khailova, S. K. Mount Patrick, K. M. Arganbright, M. D. Halpern, T. Kinouchi, and B. Dvorak, “Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 299, no. 5, pp. G1118–G1127, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Mangell, P. Nejdfors, M. Wang et al., “Lactobacillus plantarum 299v inhibits Escherichia coli-induced intestinal permeability,” Digestive Diseases and Sciences, vol. 47, no. 3, pp. 511–516, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. K. C. Johnson-Henry, K. A. Donato, G. Shen-Tu, M. Gordanpour, and P. M. Sherman, “Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7-induced changes in epithelial barrier function,” Infection and Immunity, vol. 76, no. 4, pp. 1340–1348, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. P. M. Sherman, K. C. Johnson-Henry, H. P. Yeung, P. S. C. Ngo, J. Goulet, and T. A. Tompkins, “Probiotics reduce enterohemorrhagic Escherichia coli O157:H7- and enteropathogenic E. coli O127:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements,” Infection and Immunity, vol. 73, no. 8, pp. 5183–5188, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Bahrami, S. Macfarlane, and G. T. Macfarlane, “Induction of cytokine formation by human intestinal bacteria in gut epithelial cell lines,” Journal of Applied Microbiology, vol. 110, no. 1, pp. 353–363, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Perdigon, S. Alvarez, M. Rachid, G. Agüero, and N. Gobbato, “Immune system stimulation by probiotics,” Journal of Dairy Science, vol. 78, no. 7, pp. 1597–1606, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. E. Paszti-Gere, K. Szeker, E. Csibrik-Nemeth et al., “Metabolites of Lactobacillus plantarum 2142 prevent oxidative stress-induced overexpression of proinflammatory cytokines in IPEC-J2 cell line,” Inflammation, vol. 35, no. 4, pp. 1487–1499, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. D. L. Arvans, S. R. Vavricka, H. Ren et al., “Luminal bacterial flora determines physiological expression of intestinal epithelial cytoprotective heat shock proteins 25 and 72,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 288, no. 4, pp. G696–G704, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. S. R. Choi, S. A. Lee, Y. J. Kim, C. Y. Ok, H. J. Lee, and K. B. Hahm, “Role of heat shock proteins in gastric inflammation and ulcer healing.,” Journal of physiology and pharmacology: an official journal of the Polish Physiological Society, vol. 60, pp. 5–17, 2009. View at Google Scholar · View at Scopus
  26. M. J. Ropeleski, J. Tang, M. M. Walsh-Reitz, M. W. Musch, and E. B. Chang, “Interleukin-11-induced heat shock protein 25 confers intestinal epithelial-specific cytoprotection from oxidant stress,” Gastroenterology, vol. 124, no. 5, pp. 1358–1368, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Sepponen and A. R. Pösö, “The inducible form of heat shock protein 70 in the serum, colon and small intestine of the pig: comparison to conventional stress markers,” The Veterinary Journal, vol. 171, no. 3, pp. 519–524, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Youakim and M. Ahdieh, “Interferon-γ decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 276, no. 5, pp. G1279–G1288, 1999. View at Google Scholar · View at Scopus
  29. S. Klingspor, H. Martens, D. Çaushi, S. Twardziok, J. R. Aschenbach, and U. Lodemann, “Characterization of the effects of Enterococcus faecium on intestinal epithelial transport properties in piglets,” Journal of Animal Science, vol. 91, no. 4, pp. 1707–1718, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. P. Schierack, M. Nordhoff, M. Pollmann et al., “Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine,” Histochemistry and Cell Biology, vol. 125, no. 3, pp. 293–305, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Gabler, E. Ephraim, C. Holder, R. Einspanier, and M. Schmidt, “Higher mRNA expression of proinflammatory factors in immune cells of piglets in probiotic group after Salmonella infection,” in Book of Abstracts of the satellite meeting of the 2nd European Congress of Immunology Berlin, 2009, p. 40, 2009. View at Google Scholar
  32. U. Lodemann, R. Einspanier, F. Scharfen, H. Martens, and A. Bondzio, “Effects of zinc on epithelial barrier properties and viability in a human and a porcine intestinal cell culture model,” Toxicology in Vitro, vol. 27, no. 2, pp. 834–843, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Rhoads, W. Chen, P. Chu, H. M. Berschneider, R. A. Argenzio, and A. M. Paradiso, “L-Glutamine and L-asparagine stimulate Na+-H+ exchange in porcine jejunal enterocytes,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 266, no. 5, part 1, pp. G828–G838, 1994. View at Google Scholar · View at Scopus
  34. S. Hu, M. J. Ciancio, M. Lahav et al., “Translational inhibition of colonic epithelial heat shock proteins by IFN-gamma and TNF-alpha in intestinal inflammation,” Gastroenterology, vol. 133, no. 6, pp. 1893–1904, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Parlesak, D. Haller, S. Brinz, A. Baeuerlein, and C. Bode, “Modulation of cytokine release by differentiated CACO-2 cells in a compartmentalized coculture model with mononuclear leucocytes and nonpathogenic bacteria,” Scandinavian Journal of Immunology, vol. 60, no. 5, pp. 477–485, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Bernardini, A. Zannoni, M. E. Turba et al., “Effects of 50 Hz sinusoidal magnetic fields on Hsp27, Hsp70, Hsp90 expression in porcine aortic endothelial cells (PAEC),” Bioelectromagnetics, vol. 28, no. 3, pp. 231–237, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. T. G. Ramsay and T. J. Caperna, “Ontogeny of adipokine expression in neonatal pig adipose tissue,” Comparative Biochemistry and Physiology—Part A: Molecular & Integrative Physiology, vol. 152, no. 1, pp. 72–78, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Paszti-Gere, E. Csibrik-Nemeth, K. Szeker et al., “Lactobacillus plantarum 2142 prevents intestinal oxidative stress in optimized in vitro systems,” Acta Physiologica Hungarica, vol. 100, no. 1, pp. 89–98, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. C. C. Aperce, T. E. Burkey, B. KuKanich, B. A. Crozier-Dodson, S. S. Dritz, and J. E. Minton, “Interaction of Bacillus species and Salmonella enterica serovar Typhimurium in immune or inflammatory signaling from swine intestinal epithelial cells,” Journal of Animal Science, vol. 88, no. 5, pp. 1649–1656, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. C. M. Carey and M. Kostrzynska, “Lactic acid bacteria and bifidobacteria attenuate the proinflammatory response in intestinal epithelial cells induced by salmonella enterica serovar Typhimurium,” Canadian Journal of Microbiology, vol. 59, no. 1, pp. 9–17, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Madsen, A. Cornish, P. Soper et al., “Probiotic bacteria enhance murine and human intestinal epithelial barrier function,” Gastroenterology, vol. 121, no. 3, pp. 580–591, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. A. J. Brosnahan and D. R. Brown, “Porcine IPEC-J2 intestinal epithelial cells in microbiological investigations,” Veterinary Microbiology, vol. 156, no. 3-4, pp. 229–237, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. J.-M. Otte and D. K. Podolsky, “Functional modulation of enterocytes by gram-positive and gram-negative microorganisms,” American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 286, no. 4, pp. G613–G626, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. A. A. Zyrek, C. Cichon, S. Helms, C. Enders, U. Sonnenborn, and M. A. Schmidt, “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,” Cellular Microbiology, vol. 9, no. 3, pp. 804–816, 2007. View at Google Scholar
  45. J. B. Ewaschuk, H. Diaz, L. Meddings et al., “Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 295, no. 5, pp. G1025–G1034, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Resta-Lenert and K. E. Barrett, “Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive Escherichia coli (EIEC),” Gut, vol. 52, no. 7, pp. 988–997, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. P. López, I. González-Rodríguez, B. Sánchez et al., “Interaction of Bifidobacterium bifidum LMG13195 with HT29 Cells Influences regulatory-T-cell-associated chemokine receptor expression,” Applied and Environmental Microbiology, vol. 78, no. 8, pp. 2850–2857, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. M. M. Geens and T. A. Niewold, “Preliminary characterization of the transcriptional response of the porcine intestinal cell line IPEC-J2 to enterotoxigenic Escherichia coli, Escherichia coli, and E. coli lipopolysaccharide,” Comparative and Functional Genomics, vol. 2010, Article ID 469583, 11 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Roselli, M. S. Britti, I. Le Huërou-Luron, H. Marfaing, W. Y. Zhu, and E. Mengheri, “Effect of different plant extracts and natural substances (PENS) against membrane damage induced by enterotoxigenic Escherichia coli K88 in pig intestinal cells,” Toxicology in Vitro, vol. 21, no. 2, pp. 224–229, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. J. S. Ko, H. R. Yang, J. Y. Chang, and J. K. Seo, “Lactobacillus plantarum inhibits epithelial barrier dysfunction and interlukin-8 secretion induced by tumor necrosis factor-α,” World Journal of Gastroenterology, vol. 13, no. 13, pp. 1962–1965, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Roselli, A. Finamore, M. S. Britti et al., “The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage,” Journal of Nutrition, vol. 137, no. 12, pp. 2709–2716, 2007. View at Google Scholar · View at Scopus
  52. G. González-Ortiz, R. G. Hermes, R. Jiménez-Díaz, J. F. Pérez, and S. M. Martín-Orúe, “Screening of extracts from natural feed ingredients for their ability to reduce enterotoxigenic Escherichia coli (ETEC) K88 adhesion to porcine intestinal epithelial cell-line IPEC-J2,” Veterinary Microbiology, vol. 167, no. 3-4, pp. 494–499, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Lindquist and E. A. Craig, “The heat-shock proteins,” Annual Review of Genetics, vol. 22, pp. 631–677, 1988. View at Publisher · View at Google Scholar · View at Scopus
  54. H. M. Beere, “Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways,” The Journal of Clinical Investigation, vol. 115, no. 10, pp. 2633–2639, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. V. L. Gabai and M. Y. Sherman, “Invited review: Interplay between molecular chaperones and signaling pathways in survival of heat shock,” Journal of Applied Physiology, vol. 92, no. 4, pp. 1743–1748, 2002. View at Google Scholar · View at Scopus
  56. S. Hu, Y. Wang, L. Lichtenstein et al., “Regional differences in colonic mucosa-associated microbiota determine the physiological expression of host heat shock proteins,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 299, no. 6, pp. G1266–G1275, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Dokladny, P. L. Moseley, and T. Y. Ma, “Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 290, no. 2, pp. G204–G212, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. D. L. Arvans, S. R. Vavricka, H. Ren et al., “Luminal bacterial flora determines physiological expression of intestinal epithelial cytoprotective heat shock proteins 25 and 72,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 288, no. 4, pp. G696–G704, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. J. J. Malago, J. F. Koninkx, and J. E. van Dijk, “The heat shock response and cytoprotection of the intestinal epithelium,” Cell Stress and Chaperone, vol. 7, no. 2, pp. 191–199, 2002. View at Google Scholar
  60. J. F. J. G. Koninkx and J. J. Malago, “The protective potency of probiotic bacteria and their microbial products against enteric infections-review,” Folia Microbiologica, vol. 53, no. 3, pp. 189–194, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. J. J. Malago, P. C. Tooten, and J. F. Koninkx, “Anti-inflammatory properties of probiotic bacteria on Salmonella-induced IL-8 synthesis in enterocyte-like Caco-2 cells,” Beneficial microbes, vol. 1, no. 2, pp. 121–130, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. B. Siepert, N. Reinhardt, S. Kreuzer et al., “Enterococcus faecium NCIMB 10415 supplementation affects intestinal immune-associated gene expression in post-weaning piglets,” Veterinary Immunology and Immunopathology, vol. 157, no. 1-2, pp. 65–77, 2014. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Bruewer, A. Luegering, T. Kucharzik et al., “Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms,” The Journal of Immunology, vol. 171, no. 11, pp. 6164–6172, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Nusrat, J. R. Turner, and J. L. Madara, “Molecular physiology and pathophysiology of tight junctions. IV. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 279, no. 5, pp. G851–G857, 2000. View at Google Scholar · View at Scopus
  65. D. C. Chiossone, P. L. Simon, and P. L. Smith, “Interleukin-1: effects on rabbit ileal mucosal ion transport in vitro,” European Journal of Pharmacology, vol. 180, no. 2-3, pp. 217–228, 1990. View at Publisher · View at Google Scholar · View at Scopus
  66. J. Hardin, K. Kroeker, B. Chung, and D. G. Gall, “Effect of proinflammatory interleukins on jejunal nutrient transport,” Gut, vol. 47, no. 2, pp. 184–191, 2000. View at Publisher · View at Google Scholar · View at Scopus
  67. B. Sherry and A. Cerami, “Small cytokine super-family,” Current Opinion in Immunology, vol. 3, no. 1, pp. 56–60, 1991. View at Publisher · View at Google Scholar · View at Scopus
  68. S. E. Crowe, L. Alvarez, M. Dytoc et al., “Expression of interleukin 8 and CD54 by human gastric epithelium after Helicobacter pylori infection in vitro,” Gastroenterology, vol. 108, no. 1, pp. 65–74, 1995. View at Publisher · View at Google Scholar · View at Scopus
  69. D. I. Sonnier, S. R. Bailey, R. M. Schuster, A. B. Lentsch, and T. A. Pritts, “TNF-α induces vectorial secretion of IL-8 in Caco-2 cells,” Journal of Gastrointestinal Surgery, vol. 14, no. 10, pp. 1592–1599, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. J. Ewaschuk, R. Endersby, D. Thiel et al., “Probiotic bacteria prevent hepatic damage and maintain colonic barrier function in a mouse model of sepsis,” Hepatology, vol. 46, no. 3, pp. 841–850, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. K. A. Skjolaas, T. E. Burkey, S. S. Dritz, and J. E. Minton, “Effects of Salmonella enterica serovar Typhimurium, or serovar Choleraesuis, Lactobacillus reuteri and Bacillus licheniformis on chemokine and cytokine expression in the swine jejunal epithelial cell line, IPEC-J2,” Veterinary Immunology and Immunopathology, vol. 115, no. 3-4, pp. 299–308, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. D.-M. McCafferty and I. J. Zeitlin, “Short chain fatty acid-induced colitis in mice,” International Journal of Tissue Reactions, vol. 11, no. 4, pp. 165–168, 1989. View at Google Scholar · View at Scopus
  73. J. M. Harig, K. H. Soergel, R. A. Komorowski, and C. M. Wood, “Treatment of diversion colitis with short-chain-fatty acid irrigation,” The New England Journal of Medicine, vol. 320, no. 1, pp. 23–28, 1989. View at Publisher · View at Google Scholar · View at Scopus
  74. W. Scheppach, H. Sommer, T. Kirchner et al., “Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis,” Gastroenterology, vol. 103, no. 1, pp. 51–56, 1992. View at Google Scholar · View at Scopus