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Gastroenterology Research and Practice
Volume 2016, Article ID 4953120, 12 pages
http://dx.doi.org/10.1155/2016/4953120
Research Article

Treatment with a Monoclonal Anti-IL-12p40 Antibody Induces Substantial Gut Microbiota Changes in an Experimental Colitis Model

1Department of Food Science, Faculty of Science, University of Copenhagen, Rolighedsvej 26, 1958 Frederiksberg, Denmark
2Department of Veterinary Disease Biology, Faculty of Health and Medical Science, University of Copenhagen, Thorvaldsensvej 57, 1870 Frederiksberg, Denmark
3Department of Environmental Science, Aarhus University, Frederiksborgvej 399, 4000 Roskilde, Denmark
4Novo Nordisk Park, 2760 Maaloev, Denmark

Received 24 September 2015; Accepted 30 November 2015

Academic Editor: Jinsheng Yu

Copyright © 2016 Josué Castro-Mejía 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. R. B. Sartor, “Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis,” Nature Clinical Practice Gastroenterology & Hepatology, vol. 3, no. 7, pp. 390–407, 2006. View at Publisher · View at Google Scholar
  2. D. C. Baumgart and W. J. Sandborn, “Crohn's disease,” The Lancet, vol. 380, no. 9853, pp. 1590–1605, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. I. Ordás, L. Eckmann, M. Talamini, D. C. Baumgart, and W. J. Sandborn, “Ulcerative colitis,” The Lancet, vol. 380, no. 9853, pp. 1606–1619, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. E. V. Loftus Jr., “Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences,” Gastroenterology, vol. 126, no. 6, pp. 1504–1517, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Nell, S. Suerbaum, and C. Josenhans, “The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models,” Nature Reviews Microbiology, vol. 8, no. 8, pp. 564–577, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. A. A. te Velde, F. De Kort, E. Sterrenburg et al., “Comparative analysis of colonic gene expression of three experimental colitis models mimicking inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 13, no. 3, pp. 325–330, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Lindebo Holm, S. S. Poulsen, H. Markholst, and S. Reedtz-Runge, “Pharmacological evaluation of the scid t cell transfer model of colitis: as a model of Crohn's disease,” International Journal of Inflammation, vol. 2012, Article ID 412178, 11 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. M. M. Kosiewicz, C. C. Nast, A. Krishnan et al., “Th1-type responses mediate spontaneous ileitis in a novel murine model of Crohn's disease,” The Journal of Clinical Investigation, vol. 107, no. 6, pp. 695–702, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Kjellev, D. Lundsgaard, S. S. Poulsen, and H. Markholst, “Reconstitution of Scid mice with CD4+CD25 T cells leads to rapid colitis: an improved model for pharmacologic testing,” International Immunopharmacology, vol. 6, no. 8, pp. 1341–1354, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. K. R. B. Bastos, C. R. F. Marinho, R. Barboza, M. Russo, J. M. Álvarez, and M. R. D'Império Lima, “What kind of message does IL-12/IL-23 bring to macrophages and dendritic cells?” Microbes and Infection, vol. 6, no. 6, pp. 630–636, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Manetti, F. Gerosa, M. G. Giudizi et al., “Interleukin 12 induces stable priming for interferon γ (IFN-γ) production during differentiation of human T helper (Th) cells and transient IFN-γ production in established Th2 cell clones,” The Journal of Experimental Medicine, vol. 179, no. 4, pp. 1273–1283, 1994. View at Publisher · View at Google Scholar · View at Scopus
  12. S. H. Chan, M. Kobayashi, D. Santoli, B. Perussia, and G. Trinchier, “Mechanisms of IFN-gamma induction by natural killer cell stimulatory factor (NKSF/IL-12),” The Journal of Immunology, vol. 148, no. 1, pp. 92–98, 1992. View at Google Scholar
  13. W. J. Sandborn, B. G. Feagan, R. N. Fedorak et al., “A randomized trial of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with moderate-to-severe Crohn's disease,” Gastroenterology, vol. 135, no. 4, pp. 1130–1141, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. W. J. Sandborn, C. Gasink, L.-L. Gao et al., “Ustekinumab induction and maintenance therapy in refractory Crohn's disease,” The New England Journal of Medicine, vol. 367, no. 16, pp. 1519–1528, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Yen, J. Cheung, H. Scheerens et al., “IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6,” The Journal of Clinical Investigation, vol. 116, no. 5, pp. 1310–1316, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. P. J. Mannon, I. J. Fuss, L. Mayer et al., “Anti-interleukin-12 antibody for active Crohn's disease,” The New England Journal of Medicine, vol. 351, no. 20, pp. 2069–2079, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. I. J. Fuss, C. Becker, Z. Yang et al., “Both IL-12p70 and IL-23 are synthesized during active Crohn's disease and are down-regulated by treatment with anti-IL-12 p40 monoclonal antibody,” Inflammatory Bowel Diseases, vol. 12, no. 1, pp. 9–15, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Rajca, V. Grondin, E. Louis et al., “Alterations in the intestinal microbiome (Dysbiosis) as a predictor of relapse after infliximab withdrawal in Crohn's disease,” Inflammatory Bowel Diseases, vol. 20, no. 6, pp. 978–986, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. R. K. Sellon, S. Tonkonogy, M. Schultz et al., “Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice,” Infection and Immunity, vol. 66, no. 11, pp. 5224–5231, 1998. View at Google Scholar · View at Scopus
  20. 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
  21. N. A. Nagalingam, J. Y. Kao, and V. B. Young, “Microbial ecology of the murine gut associated with the development of dextran sodium sulfate-induced colitis,” Inflammatory Bowel Diseases, vol. 17, no. 4, pp. 917–926, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. S. M. Bloom, V. N. Bijanki, G. M. Nava et al., “Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease,” Cell Host and Microbe, vol. 9, no. 5, pp. 390–403, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. M. Heimesaat, A. Fischer, B. Siegmund et al., “Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via toll-like receptors 2 and 4,” PLoS ONE, vol. 2, no. 7, article e662, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Lupp, M. L. Robertson, M. E. Wickham et al., “Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae,” Cell Host and Microbe, vol. 2, no. 2, pp. 119–129, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Deplancke, K. Finster, W. V. Graham, C. T. Collier, J. E. Thurmond, and H. R. Gaskins, “Gastrointestinal and microbial responses to sulfate-supplemented drinking water in mice,” Experimental Biology and Medicine, vol. 228, no. 4, pp. 424–433, 2003. View at Google Scholar · View at Scopus
  26. S. J. Ott, M. Musfeldt, D. F. Wenderoth et al., “Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease,” Gut, vol. 53, no. 5, pp. 685–693, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Nicklas, P. Baneux, R. Boot et al., “Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units,” Laboratory Animals, vol. 36, no. 1, pp. 20–42, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. S. N. S. Murthy, H. S. Cooper, H. Shim, R. S. Shah, S. A. Ibrahim, and D. J. Sedergran, “Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin,” Digestive Diseases and Sciences, vol. 38, no. 9, pp. 1722–1734, 1993. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Becker, M. C. Fantini, and M. F. Neurath, “High resolution colonoscopy in live mice,” Nature Protocols, vol. 1, no. 6, pp. 2900–2904, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Becker, M. C. Fantini, S. Wirtz et al., “In vivo imaging of colitis and colon cancer development in mice using high resolution chromoendoscopy,” Gut, vol. 54, no. 7, pp. 950–954, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. B. Pyndt Jørgensen, J. T. Hansen, L. Krych et al., “A possible link between food and mood: dietary impact on gut microbiota and behavior in BALB/c mice,” PLoS ONE, vol. 9, no. 8, Article ID e103398, 2014. View at Publisher · View at Google Scholar
  32. R. C. Edgar, “UPARSE: highly accurate OTU sequences from microbial amplicon reads,” Nature Methods, vol. 10, no. 10, pp. 996–998, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. D. McDonald, M. N. Price, J. Goodrich et al., “An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea,” The ISME Journal, vol. 6, no. 3, pp. 610–618, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. J. G. Caporaso, J. Kuczynski, J. Stombaugh et al., “QIIME allows analysis of high-throughput community sequencing data,” Nature Methods, vol. 7, no. 5, pp. 335–336, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. C. H. F. Hansen, T. L. Holm, Ł. Krych et al., “Gut microbiota regulates NKG2D ligand expression on intestinal epithelial cells,” European Journal of Immunology, vol. 43, no. 2, pp. 447–457, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Melgar, L. Karlsson, E. Rehnström et al., “Validation of murine dextran sulfate sodium-induced colitis using four therapeutic agents for human inflammatory bowel disease,” International Immunopharmacology, vol. 8, no. 6, pp. 836–844, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Sokol, P. Seksik, J. P. Furet et al., “Low counts of faecalibacterium prausnitzii in colitis microbiota,” Inflammatory Bowel Diseases, vol. 15, no. 8, pp. 1183–1189, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Sokol, P. Seksik, L. Rigottier-Gois et al., “Specificities of the fecal microbiota in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 12, no. 2, pp. 106–111, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Atarashi, T. Tanoue, T. Shima et al., “Induction of colonic regulatory T cells by indigenous Clostridium species,” Science, vol. 331, no. 6015, pp. 337–341, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Atarashi, T. Tanoue, K. Oshima et al., “Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota,” Nature, vol. 500, no. 7461, pp. 232–236, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Bien, V. Palagani, and P. Bozko, “The intestinal microbiota dysbiosis and Clostridium difficile infection: is there a relationship with inflammatory bowel disease?” Therapeutic Advances in Gastroenterology, vol. 6, no. 1, pp. 53–68, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. H. C. Rath, K. H. Wilson, and R. B. Sartor, “Differential induction of colitis and gastritis in HLA-B27 transgenic rats selectively colonized with Bacteroides vulgatus or Escherichia coli,” Infection and Immunity, vol. 67, no. 6, pp. 2969–2974, 1999. View at Google Scholar · View at Scopus
  43. V. Nakano, D. A. Gomes, R. M. E. Arantes, J. R. Nicoli, and M. J. Avila-Campos, “Evaluation of the pathogenicity of the Bacteroides fragilis toxin gene subtypes in gnotobiotic mice,” Current Microbiology, vol. 53, no. 2, pp. 113–117, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. J. U. Scher, A. Sczesnak, R. S. Longman et al., “Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis,” eLife, vol. 2013, no. 2, Article ID e01202, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. B. M. Brinkman, A. Becker, R. B. Ayiseh et al., “Gut microbiota affects sensitivity to acute DSS-induced colitis independently of host genotype,” Inflammatory Bowel Diseases, vol. 19, no. 12, pp. 2560–2567, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. M. W. J. van Passel, R. Kant, E. G. Zoetendal et al., “The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes,” PLoS ONE, vol. 6, no. 3, Article ID e16876, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Derrien, M. C. Collado, K. Ben-Amor, S. Salminen, and W. M. De Vos, “The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract,” Applied and Environmental Microbiology, vol. 74, no. 5, pp. 1646–1648, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Sung Kang, M. Ban, E.-J. Choi et al., “Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis,” PLoS ONE, vol. 8, no. 10, Article ID e76520, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. C. W. Png, S. K. Lindén, K. S. Gilshenan et al., “Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria,” The American Journal of Gastroenterology, vol. 105, no. 11, pp. 2420–2428, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. B. P. Ganesh, R. Klopfleisch, G. Loh, and M. Blaut, “Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice,” PLoS ONE, vol. 8, no. 9, Article ID e74963, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. J. P. Zackular, N. T. Baxter, K. D. Iverson et al., “The gut microbiome modulates colon tumorigenesis,” mBio, vol. 4, no. 6, Article ID e00692, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Michail, M. Durbin, D. Turner et al., “Alterations in the gut microbiome of children with severe ulcerative colitis,” Inflammatory Bowel Diseases, vol. 18, no. 10, pp. 1799–1808, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. I. Mukhopadhya, R. Hansen, E. M. El-Omar, and G. L. Hold, “IBD—what role do Proteobacteria play?” Nature Reviews Gastroenterology and Hepatology, vol. 9, no. 4, pp. 219–230, 2012. View at Publisher · View at Google Scholar · View at Scopus