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BioMed Research International
Volume 2013 (2013), Article ID 909613, 15 pages
http://dx.doi.org/10.1155/2013/909613
Research Article

Inflammatory Bowel Disease Therapies and Gut Function in a Colitis Mouse Model

1School of Women’s and Children’s Health, University of New South Wales, Randwick, Sydney, NSW 2031, Australia
2School of Biotechnology and Biomolecular Sciences, University of New South Wales, Randwick, Sydney, NSW 2052, Australia
3Department of Gastroenterology, Sydney Children’s Hospital, Randwick, Sydney, NSW 2031, Australia
4Department of Pathology, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North 4442, New Zealand
5Paediatric Gastroenterology, Christchurch Hospital, Christchurch 8140, New Zealand
6Department of Paediatrics, University of Otago, Christchurch, Christchurch 8140, New Zealand

Received 30 April 2013; Revised 1 July 2013; Accepted 1 July 2013

Academic Editor: David Bernardo

Copyright © 2013 Lily Nahidi 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. C. Förster, “Tight junctions and the modulation of barrier function in disease,” Histochemistry and Cell Biology, vol. 130, no. 1, pp. 55–70, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Zeissig, N. Bürgel, D. Günzel et al., “Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease,” Gut, vol. 56, no. 1, pp. 61–72, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. B. K. Reuter and T. T. Pizarro, “Mechanisms of tight junction dysregulation in the SAMP1YitFc model of crohn's disease-like ileitis,” Annals of the New York Academy of Sciences, vol. 1165, pp. 301–307, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. N. S. H. de Jong, S. T. Leach, and A. S. Day, “Fecal S100A12: a novel noninvasive marker in children with Crohn's disease,” Inflammatory Bowel Diseases, vol. 12, no. 7, pp. 566–572, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. R. K. Linskens, X. W. Huijsdens, P. H. M. Savelkoul, C. M. J. E. Vandenbrouckc-Grauls, and S. G. M. Meuwissen, “The bacterial flora in inflammatory bowel disease: current insights in pathogenesis and the influence of antibiotics and probiotics,” Scandinavian Journal of Gastroenterology, vol. 36, Supplement, no. 234, pp. 29–40, 2001. View at Scopus
  6. C. Fiocchi, “Inflammatory bowel disease: etiology and pathogenesis,” Gastroenterology, vol. 115, no. 1, pp. 182–205, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. M. G. Laukoetter, P. Nava, and A. Nusrat, “Role of the intestinal barrier in inflammatory bowel disease,” World Journal of Gastroenterology, vol. 14, no. 3, pp. 401–407, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. J. G. Fox, Z. Ge, M. T. Whary, S. E. Erdman, and B. H. Horwitz, “Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer,” Mucosal Immunology, vol. 4, no. 1, pp. 22–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. K. L. Madsen, J. S. Doyle, L. D. Jewell, M. M. Tavernini, and R. N. Fedorak, “Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice,” Gastroenterology, vol. 116, no. 5, pp. 1107–1114, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. M. T. Whary, S. J. Danon, Y. Feng et al., “Rapid onset of ulcerative typhlocolitis in B6.129P2-IL10tm1Cgn (IL-10-/-) mice infected with Helicobacter trogontum is associated with decreased colonization by altered Schaedler's flora,” Infection and Immunity, vol. 74, no. 12, pp. 6615–6623, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. J. O. Lindsay and H. J. F. Hodgson, “Review article: the immunoregulatory cytokine interleukin-10: a therapy for Crohn's disease?” Alimentary Pharmacology and Therapeutics, vol. 15, no. 11, pp. 1709–1716, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. M. B. Ye, J. P. Bak, C. S. An et al., “Dietary β-glucan regulates the levels of inflammatory factors, inflammatory cytokines, and immunoglobulins in interleukin-10 knockout mice,” Journal of Medicinal Food, vol. 14, no. 5, pp. 468–474, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. E. N. Mendes, D. M. M. Queiroz, F. E. Dewhirst, B. J. Paster, S. B. Moura, and J. G. Fox, “Helicobacter trogontum sp. nov., isolated from the rat intestine,” International Journal of Systematic Bacteriology, vol. 46, no. 4, pp. 916–921, 1996. View at Scopus
  14. S. B. Moura, E. N. Mendes, D. M. M. Queiroz et al., “Microbiological and histological study of the gastrointestinal tract of germ-free mice infected with Helicobacter trogontum,” Research in Microbiology, vol. 150, no. 3, pp. 205–212, 1999. View at Scopus
  15. Z. Shen, Y. Feng, A. B. Rogers et al., “Cytolethal distending toxin promotes Helicobacter cinaedi-associated typhlocolitis in interleukin-10-deficient mice,” Infection and Immunity, vol. 77, no. 6, pp. 2508–2516, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. C. L. Franklin, P. L. Gorelick, L. K. Riley et al., “Helicobacter typhlonius sp. nov., a novel murine urease-negative Helicobacter species,” Journal of Clinical Microbiology, vol. 39, no. 11, pp. 3920–3926, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. N. O. Kaakoush, A. Sirianni, M. J. Raftery, et al., “The secretome of Helicobacter trogontum,” Helicobacter, vol. 18, no. 4, pp. 316–320, 2013.
  18. L. Zhang, A. Day, G. McKenzie, and H. Mitchell, “Nongastric Helicobacter species detected in the intestinal tract of children,” Journal of Clinical Microbiology, vol. 44, no. 6, pp. 2276–2279, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. S. M. Man, L. Zhang, A. S. Day, S. Leach, and H. Mitchell, “Detection of enterohepatic and gastric Helicobacter species in fecal specimens of children with crohn's disease,” Helicobacter, vol. 13, no. 4, pp. 234–238, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Miyauchi, H. Morita, J. Okuda, T. Sashihara, M. Shimizu, and S. Tanabe, “Cell wall fraction of Enterococcus hirae ameliorates TNF-α-induced barrier impairment in the human epithelial tight junction,” Letters in Applied Microbiology, vol. 46, no. 4, pp. 469–476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Kruidenier and H. W. Verspaget, “Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease: radicals or ridiculous?” Alimentary Pharmacology and Therapeutics, vol. 16, no. 12, pp. 1997–2015, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. A. S. Day, K. E. Whitten, and N. S. H. de Jong, “Nutrition and nutritional management of Crohn's disease in children and adolescents,” Current Nutrition and Food Science, vol. 2, no. 1, pp. 3–13, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Berni Canani, G. Terrin, O. Borrelli et al., “Short- and long-term therapeutic efficacy of nutritional therapy and corticosteroids in paediatric Crohn's disease,” Digestive and Liver Disease, vol. 38, no. 6, pp. 381–387, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Harris, E. R. Feller, and S. A. Shah, “Medical therapy of IBD in 2009,” Medicine and Health, Rhode Island, vol. 92, no. 3, pp. 78–81, 2009. View at Scopus
  25. G. Van Assche, S. Vermeire, and P. Rutgeerts, “Mucosal healing and anti TNFs in IBD,” Current Drug Targets, vol. 11, no. 2, pp. 227–233, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. P. Rutgeerts, S. Vermeire, and G. Van Assche, “Biological therapies for inflammatory bowel diseases,” Gastroenterology, vol. 136, no. 4, pp. 1182–1197, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Ferrante and G. Van Assche, “Medical therapy and mucosal healing,” Current Drug Targets, vol. 13, no. 10, pp. 1294–1299, 2012.
  28. A. S. Day, K. E. Whitten, M. Sidler, and D. A. Lemberg, “Systematic review: nutritional therapy in paediatric Crohn's disease,” Alimentary Pharmacology and Therapeutics, vol. 27, no. 4, pp. 293–307, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Papa, G. Mocci, F. Scaldaferri et al., “New therapeutic approach in inflammatory bowel disease,” European Review for Medical and Pharmacological Sciences, vol. 13, supplement 1, pp. 33–35, 2009. View at Scopus
  30. C. Thukral, W. J. Travassos, and M. A. Peppercorn, “The role of antibiotics in inflammatory bowel disease,” Current Treatment Options in Gastroenterology, vol. 8, no. 3, pp. 223–228, 2005. View at Scopus
  31. T. Ishikawa, S. Okamura, H. Oshimoto, R. Kobayashi, and M. Mori, “Metronidazole plus ciprofloxacin therapy for active Crohn's disease,” Internal Medicine, vol. 42, no. 4, pp. 318–321, 2003. View at Scopus
  32. K. L. Madsen, J. S. Doyle, M. M. Tavernini, L. D. Jewell, R. P. Rennie, and R. N. Fedorak, “Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice,” Gastroenterology, vol. 118, no. 6, pp. 1094–1105, 2000. View at Scopus
  33. S. Colpaert, Z. Liu, B. De Greef, P. Rutgeerts, J. L. Ceuppens, and K. Geboes, “Effects of anti-tumour necrosis factor, interleukin-10 and antibiotic therapy in the indometacin-induced bowel inflammation rat model,” Alimentary Pharmacology and Therapeutics, vol. 15, no. 11, pp. 1827–1836, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Sutherland, J. Singleton, J. Sessions et al., “Double blind, placebo controlled trial of metronidazole in Crohn's disease,” Gut, vol. 32, no. 9, pp. 1071–1075, 1991. View at Scopus
  35. J.-F. Colombel, M. Lémann, M. Cassagnou et al., “A controlled trial comparing ciprofloxacin with mesalazine for the treatment of active Crohn's disease,” The American Journal of Gastroenterology, vol. 94, no. 3, pp. 674–678, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Shen, J.-P. Achkar, B. A. Lashner et al., “A randomized clinical trial of ciprofloxacin and metronidazole to treat acute pouchitis,” Inflammatory Bowel Diseases, vol. 7, no. 4, pp. 301–305, 2001. View at Scopus
  37. Y.-X. Yang and G. R. Lichtenstein, “Corticosteroids in Crohn's disease,” The American Journal of Gastroenterology, vol. 97, no. 4, pp. 803–823, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. T. J. Creed and C. S. J. Probert, “Review article: steroid resistance in inflammatory bowel disease: mechanisms and therapeutic strategies,” Alimentary Pharmacology and Therapeutics, vol. 25, no. 2, pp. 111–122, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. O. Borrelli, L. Cordischi, M. Cirulli et al., “Polymeric diet alone versus corticosteroids in the treatment of active pediatric Crohn's disease: a randomized controlled open-label trial,” Clinical Gastroenterology and Hepatology, vol. 4, no. 6, pp. 744–753, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. R. M. Beattie, “Nutritional management of Crohn's disease in childhood,” Journal of the Royal Society of Medicine, vol. 91, no. 3, pp. 135–137, 1998. View at Scopus
  41. M. H. Alhagamhmad, A. S. Day, D. A. Lemberg, et al., “An update of the role of nutritional therapy in the management of Crohn's disease,” Journal of Gastroenterology, vol. 47, no. 8, pp. 872–882, 2012.
  42. N. S. H. de Jong, S. T. Leach, and A. S. Day, “Polymeric formula has direct anti-inflammatory effects on enterocytes in an in vitro model of intestinal inflammation,” Digestive Diseases and Sciences, vol. 52, no. 9, pp. 2029–2036, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. E. J. Breese, C. A. Michie, S. W. Nicholls et al., “Tumor necrosis factor α-producing cells in the intestinal mucosa of children with inflammatory bowel disease,” Gastroenterology, vol. 106, no. 6, pp. 1455–1466, 1994. View at Scopus
  44. J. M. E. Fell, M. Paintin, F. Arnaud-Battandieri et al., “Mucosal healing and a fall in mucosal pro-inflammatory cytokine mRNA induced by a specific oral polymeric diet in paediatric Crohn's disease,” Alimentary Pharmacology and Therapeutics, vol. 14, no. 3, pp. 281–289, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Nahidi, A. S. Day, D. A. Lemberg, and S. T. Leach, “Differential effects of nutritional and non-nutritional therapies on intestinal barrier function in an in vitro model,” Journal of Gastroenterology, vol. 47, no. 2, pp. 107–117, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Lewis, J. Caldwell, V. Phan et al., “Decreased epithelial barrier function evoked by exposure to metabolic stress and nonpathogenic E. coli is enhanced by TNF-α,” The American Journal of Physiology, vol. 294, no. 3, pp. G669–G678, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Santos, D. Yates, M. Guilarte, M. Vicario, C. Alonso, and M. H. Perdue, “Stress neuropeptides evoke epithelial responses via mast cell activation in the rat colon,” Psychoneuroendocrinology, vol. 33, no. 9, pp. 1248–1256, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. A. A. Teitelbaum, M. G. Gareau, J. Jury, C. Y. Ping, and M. H. Perdue, “Chronic peripheral administration of corticotropin-releasing factor causes colonic barrier dysfunction similar to psychological stress,” The American Journal of Physiology, vol. 295, no. 3, pp. G452–G459, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. A. J. Kiliaan, P. R. Saunders, P. B. Bijlsma et al., “Stress stimulates transepithelial macromolecular uptake in rat jejunum,” The American Journal of Physiology, vol. 275, no. 5, pp. G1037–G1044, 1998. View at Scopus
  50. F. Wang, W. V. Graham, Y. Wang, E. D. Witkowski, B. T. Schwarz, and J. R. Turner, “Interferon-γ and tumor necrosis factor-α synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression,” The American Journal of Pathology, vol. 166, no. 2, pp. 409–419, 2005. View at Scopus
  51. T. Y. Ma, M. A. Boivin, D. Ye, A. Pedram, and H. M. Said, “Mechanism of TNF-α modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression,” The American Journal of Physiology, vol. 288, no. 3, pp. G422–G430, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. D. R. Trune, R. J. Wobig, J. B. Kempton, and S. H. Hefeneider, “Steroid treatment in young MRL.MpJ-Fas(lpr) autoimmune mice prevents cochlear dysfunction,” Hearing Research, vol. 137, no. 1-2, pp. 167–173, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Cecilia Berin, P.-C. Yang, L. Ciok, S. Waserman, and M. H. Perdue, “Role for IL-4 in macromolecular transport across human intestinal epithelium,” The American Journal of Physiology, vol. 276, no. 5, pp. C1046–C1052, 1999. View at Scopus
  54. J. L. Johnson, H. Hong, J. Monfregola, and S. D. Catz, “Increased survival and reduced Neutrophil infiltration of the liver in rab27a- but not munc13-4-deficient mice in Lipopolysaccharide-induced systemic inflammation,” Infection and Immunity, vol. 79, no. 9, pp. 3607–3618, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. A.-K. Tide, T. Sjögren, M. Svensson et al., “2-Thioxanthines are mechanism-based inactivators of myeloperoxidase that block oxidative stress during inflammation,” Journal of Biological Chemistry, vol. 286, no. 43, pp. 37578–37589, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. X. Sun, H. Yang, K. Nose et al., “Decline in intestinal mucosal IL-10 expression and decreased intestinal barrier function in a mouse model of total parenteral nutrition,” The American Journal of Physiology, vol. 294, no. 1, pp. G139–G147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. A. A. A. Blanchard, P. H. Watson, R. P. C. Shiu et al., “Differential expression of claudin 1, 3, and 4 during normal mammary gland development in the mouse,” DNA and Cell Biology, vol. 25, no. 2, pp. 79–86, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. G. Zhi, J. W. Ryder, J. Huang et al., “Myosin light chain kinase and myosin phosphorylation effect frequency-dependent potentiation of skeletal muscle contraction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 48, pp. 17519–17524, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. M. J. Ruddy, F. Shen, J. B. Smith, A. Sharma, and S. L. Gaffen, “Interleukin-17 regulates expression of the CXC chemokine LIX/CXCL5 in osteoblasts: implications for inflammation and neutrophil recruitment,” Journal of Leukocyte Biology, vol. 76, no. 1, pp. 135–144, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. K. L. Brewer and T. A. Nolan, “Spinal and supraspinal changes in tumor necrosis factor-α expression following excitotoxic spinal cord injury,” Journal of Molecular Neuroscience, vol. 31, no. 1, pp. 13–21, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. P. Pulimeno, C. Bauer, J. Stutz, and S. Citi, “PLEKHA7 is an adherens junction protein with a tissue distribution and subcellular localization distinct from ZO-1 and E-Cadherin,” PLoS ONE, vol. 5, no. 8, Article ID e12207, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. K. L. Edelblum and J. R. Turner, “The tight junction in inflammatory disease: communication breakdown,” Current Opinion in Pharmacology, vol. 9, no. 6, pp. 715–720, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. P. Henderson, J. E. Van Limbergen, J. Schwarze, and D. C. Wilson, “Function of the intestinal epithelium and its dysregulation in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 17, no. 1, pp. 382–395, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. G. Roda, A. Sartini, E. Zambon et al., “Intestinal epithelial cells in inflammatory bowel diseases,” World Journal of Gastroenterology, vol. 16, no. 34, pp. 4264–4271, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. C. R. Weber and J. R. Turner, “Inflammatory bowel disease: is it really just another break in the wall?” Gut, vol. 56, no. 1, pp. 6–8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. P. R. Gibson, “Increased gut permeability in Crohn's disease: is TNF the link?” Gut, vol. 53, no. 12, pp. 1724–1725, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. H. S. Oz, M. Ray, T. S. Chen, and C. J. McClain, “Efficacy of a transforming growth factor β2 containing nutritional support formula in a murine model of inflammatory bowel disease,” Journal of the American College of Nutrition, vol. 23, no. 3, pp. 220–226, 2004. View at Scopus
  68. S. T. Leach, H. M. Mitchell, W. R. Eng, L. Zhang, and A. S. Day, “Sustained modulation of intestinal bacteria by exclusive enteral nutrition used to treat children with Crohn's disease,” Alimentary Pharmacology and Therapeutics, vol. 28, no. 6, pp. 724–733, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. E. Pryce-Millar, S. H. Murch, and R. B. Heusckel, “Enteral nutrition therapy in Crohn's disease changes the mucosal flora,” Journal of Pediatric Gastroenterology and Nutrition, vol. 39, no. 1, p. S289, 2004.
  70. P. Lionetti, M. Callegari, and M. Cavicchi, “Enteral nutrition-induced remission is associated with profound modification of the intestinal microflora in Crohn's disease,” Journal of Pediatric Gastroentersology and Nutrition, vol. 39, p. S106, 2004.
  71. 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 Scopus
  72. M. J. Medellin-Peña, H. Wang, R. Johnson, S. Anand, and M. W. Griffiths, “Probiotics affect virulence-related gene expression in Escherichia coli O157:H7,” Applied and Environmental Microbiology, vol. 73, no. 13, pp. 4259–4267, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. M. G. Gareau, J. Jury, G. MacQueen, P. M. Sherman, and M. H. Perdue, “Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation,” Gut, vol. 56, no. 11, pp. 1522–1528, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. L. de Ridder, E. H. H. M. Rings, G. M. Damen et al., “Infliximab dependency in pediatric Crohn's disease: long-term follow-up of an unselected cohort,” Inflammatory Bowel Diseases, vol. 14, no. 3, pp. 353–358, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. A. M. F. Yee and M. B. Pochapin, “Treatment of complicated sarcoidosis with infliximab anti-tumor necrosis factor-α therapy,” Annals of Internal Medicine, vol. 135, no. 1, pp. 27–31, 2001. View at Scopus