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Mediators of Inflammation
Volume 2016, Article ID 4281865, 12 pages
http://dx.doi.org/10.1155/2016/4281865
Research Article

TLR2-Dependent Signaling for IL-15 Production Is Essential for the Homeostasis of Intestinal Intraepithelial Lymphocytes

1Department of General Surgery of Xinqiao Hospital, The Third Military Medical University, Shapingba, Chongqing 400037, China
2Department of Thoracic Surgery of Xinqiao Hospital, The Third Military Medical University, Shapingba, Chongqing 400037, China

Received 17 March 2016; Revised 1 June 2016; Accepted 6 June 2016

Academic Editor: Víctor M. Baizabal-Aguirre

Copyright © 2016 Yuan Qiu 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. H. Cheroutre, F. Lambolez, and D. Mucida, “The light and dark sides of intestinal intraepithelial lymphocytes,” Nature Reviews Immunology, vol. 11, no. 7, pp. 445–456, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Peaudecerf, P. Ribeiro Dos Santos, A. Boudil, S. Ezine, N. Pardigon, and B. Rocha, “The role of the gut as a primary lymphoid organ: CD8αα intraepithelial T lymphocytes in euthymic mice derive from very immature CD44+ thymocyte precursors,” Mucosal Immunology, vol. 4, no. 1, pp. 93–101, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Yang, B. Madison, D. L. Gumucio, and D. H. Teitelbaum, “Specific overexpression of IL-7 in the intestinal mucosa: the role in intestinal intraepithelial lymphocyte development,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 294, no. 6, pp. G1421–G1430, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. L. J. Ma, L. F. Acero, T. Zal, and K. S. Schluns, “Trans-presentation of IL-15 by intestinal epithelial cells drives development of CD8αα IELs,” The Journal of Immunology, vol. 183, no. 2, pp. 1044–1054, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. M. K. Kennedy, M. Glaccum, S. N. Brown et al., “Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice,” The Journal of Experimental Medicine, vol. 191, no. 5, pp. 771–780, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Cario, “Toll-like receptors in inflammatory bowel diseases: a decade later,” Inflammatory Bowel Diseases, vol. 16, no. 9, pp. 1583–1597, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. M. T. Abreu, “Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function,” Nature Reviews Immunology, vol. 10, no. 2, pp. 131–143, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Frosali, D. Pagliari, G. Gambassi, R. Landolfi, F. Pandolfi, and R. Cianci, “How the intricate interaction among toll-like receptors, microbiota, and intestinal immunity can influence gastrointestinal pathology,” Journal of Immunology Research, vol. 2015, Article ID 489821, 12 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Schwandner, R. Dziarski, H. Wesche, M. Rothe, and C. J. Kirschning, “Peptidoglycan-and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2,” The Journal of Biological Chemistry, vol. 274, no. 25, pp. 17406–17409, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. N. W. J. Schröder, S. Morath, C. Alexander et al., “Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved,” The Journal of Biological Chemistry, vol. 278, no. 18, pp. 15587–15594, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. D. M. Underhill, A. Ozinsky, K. D. Smith, and A. Aderem, “Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 25, pp. 14459–14463, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Sandor, E. Latz, F. Re et al., “Importance of extra- and intracellular domains of TLR1 and TLR2 in NFκB signaling,” Journal of Cell Biology, vol. 162, no. 6, pp. 1099–1110, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Zheng, Z. Tan, T. Zhou et al., “The TLR2 is activated by sporozoites and suppresses intrahepatic rodent malaria parasite development,” Scientific Reports, vol. 5, Article ID 18239, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Bank, P. Skytt Andersen, J. Burisch et al., “Polymorphisms in the inflammatory pathway genes TLR2, TLR4, TLR9, LY96, NFKBIA, NFKB1, TNFA, TNFRSF1A, IL6R, IL10, IL23R, PTPN22, and PPARG are associated with susceptibility of inflammatory bowel disease in a Danish cohort,” PLoS ONE, vol. 9, no. 6, Article ID e98815, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Yang, X. Sun, E. Q. Haxhija, and D. H. Teitelbaum, “Intestinal epithelial cell-derived interleukin-7: a mechanism for the alteration of intraepithelial lymphocytes in a mouse model of total parenteral nutrition,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 292, no. 1, pp. G84–G91, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Qiu, Y. Ding, L. Zou et al., “Divergent roles of amino acid residues inside and outside the BB loop affect human toll-like receptor (TLR)2/2, TLR2/1 and TLR2/6 responsiveness,” PLoS ONE, vol. 8, no. 4, Article ID e61508, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Qiu, W. Wang, W. Xiao, and H. Yang, “Role of the intestinal cytokine microenvironment in shaping the intraepithelial lymphocyte repertoire,” Journal of Leukocyte Biology, vol. 97, no. 5, pp. 849–857, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. L. W. Peterson and D. Artis, “Intestinal epithelial cells: regulators of barrier function and immune homeostasis,” Nature Reviews Immunology, vol. 14, no. 3, pp. 141–153, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Cario, I. M. Rosenberg, S. L. Brandwein, P. L. Beck, H.-C. Reinecker, and D. K. Podolsky, “Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing toll-like receptors,” The Journal of Immunology, vol. 164, no. 2, pp. 966–972, 2000. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Palazzo, A. Balsari, A. Rossini et al., “Activation of enteroendocrine cells via TLRs induces hormone, chemokine, and defensin secretion,” The Journal of Immunology, vol. 178, no. 7, pp. 4296–4303, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Shin and A. Iwasaki, “Tissue-resident memory T cells,” Immunological Reviews, vol. 255, no. 1, pp. 165–181, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. Q. Yu, C. Tang, S. Xun, T. Yajima, K. Takeda, and Y. Yoshikai, “MyD88-dependent signaling for IL-15 production plays an important role in maintenance of CD8αα TCRαβ and TCRγδ intestinal intraepithelial lymphocytes,” Journal of Immunology, vol. 176, no. 10, pp. 6180–6185, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Kellermayer, S. E. Dowd, R. A. Harris et al., “Colonic mucosal DNA methylation, immune response, and microbiome patterns in Toll-like receptor 2-knockout mice,” The FASEB Journal, vol. 25, no. 5, pp. 1449–1460, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Qiu, K. Peng, M. Liu, W. Xiao, and H. Yang, “CD8αα TCRαβ intraepithelial lymphocytes in the mouse gut,” Digestive Diseases and Sciences, vol. 61, no. 6, pp. 1451–1460, 2016. View at Publisher · View at Google Scholar
  25. D. Isakov, A. Dzutsev, J. A. Berzofsky, and I. M. Belyakov, “Lack of IL-7 and IL-15 signaling affects interferon-γ production by, more than survival of, small intestinal intraepithelial memory CD8 + T cells,” European Journal of Immunology, vol. 41, no. 12, pp. 3513–3528, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. Y.-G. Lai, M.-S. Hou, Y.-W. Hsu et al., “IL-15 does not affect IEL development in the thymus but regulates homeostasis of putative precursors and mature CD8αα+ IELs in the intestine,” The Journal of Immunology, vol. 180, no. 6, pp. 3757–3765, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. Y.-G. Lai, M.-S. Hou, A. Lo et al., “IL-15 modulates the balance between Bcl-2 and Bim via a Jak3/1-PI3K-Akt-ERK pathway to promote CD8αα+ intestinal intraepithelial lymphocyte survival,” European Journal of Immunology, vol. 43, no. 9, pp. 2305–2316, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Inagaki-Ohara, H. Nishimura, A. Mitani, and Y. Yoshikai, “Interleukin-15 preferentially promotes the growth of intestinal intraepithelial lymphocytes bearing γδ T cell receptor in mice,” European Journal of Immunology, vol. 27, no. 11, pp. 2885–2891, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Montufar-Solis, T. Garza, and J. R. Klein, “T-cell activation in the intestinal mucosa,” Immunological Reviews, vol. 215, no. 1, pp. 189–201, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Fukatsu, “Impact of the feeding route on gut mucosal immunity,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 17, no. 2, pp. 164–170, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. A. S. Ismail, C. L. Behrendt, and L. V. Hooper, “Reciprocal interactions between commensal bacteria and γδ intraepithelial lymphocytes during mucosal injury,” Journal of Immunology, vol. 182, no. 5, pp. 3047–3054, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Washizu, H. Nishimura, N. Nakamura, Y. Nimura, and Y. Yoshikai, “The NF-κB binding site is essential for transcriptional activation of the IL-15 gene,” Immunogenetics, vol. 48, no. 1, pp. 1–7, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. Y.-Z. Zhang and Y.-Y. Li, “Inflammatory bowel disease: pathogenesis,” World Journal of Gastroenterology, vol. 20, no. 1, pp. 91–99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Cario, G. Gerken, and D. K. Podolsky, “Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function,” Gastroenterology, vol. 132, no. 4, pp. 1359–1374, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Ji, C. Xu, L. Sun et al., “Aryl hydrocarbon receptor activation down-regulates IL-7 and reduces inflammation in a mouse model of DSS-induced colitis,” Digestive Diseases and Sciences, vol. 60, no. 7, pp. 1958–1966, 2015. View at Publisher · View at Google Scholar · View at Scopus