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Mediators of Inflammation
Volume 2014, Article ID 235460, 7 pages
http://dx.doi.org/10.1155/2014/235460
Review Article

An Overview of the Role of Innate Lymphoid Cells in Gut Infections and Inflammation

Department of Systems Medicine, University of Rome “Tor Vergata”, 00133 Rome, Italy

Received 16 May 2014; Accepted 16 June 2014; Published 1 July 2014

Academic Editor: H. Barbaros Oral

Copyright © 2014 Silvia Sedda 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. A. Boltjes and F. van Wijk, “Human dendritic cell functional specialization in steady-state and inflammation,” Frontiers in Immunology, vol. 5, article 131, 2014. View at Publisher · View at Google Scholar
  2. G. Magombedze, “Cellular and population plasticity of helper CD4+ T cell responses,” Frontiers in Physiology, vol. 4, no. 206, pp. 1–9, 2013. View at Google Scholar
  3. H. Spits and T. Cupedo, “Innate lymphoid cells: emerging insights in development, lineage relationships, and function,” Annual Review of Immunology, vol. 30, pp. 647–675, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Spits, D. Artis, M. Colonna et al., “Innate lymphoid cells: a proposal for uniform nomenclature,” Nature Reviews Immunology, vol. 13, no. 2, pp. 145–149, 2013. View at Google Scholar
  5. K. Moro, T. Yamada, M. Tanabe et al., “Innate production of TH2 cytokines by adipose tissue-associated c-Kit+ Sca-1+ lymphoid cells,” Nature, vol. 463, no. 7280, pp. 540–544, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. Y. Yokota, A. Mansouri, S. Mori et al., “Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2,” Nature, vol. 397, no. 6721, pp. 702–706, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. S. M. Gordon, J. Chaix, L. J. Rupp et al., “The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation,” Immunity, vol. 36, no. 1, pp. 55–67, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. M. D. Boos, Y. Yokota, G. Eberl, and B. L. Kee, “Mature natural killer cell and lymphoid tissue—inducing cell development requires Id2-mediated suppression of E protein activity,” Journal of Experimental Medicine, vol. 204, no. 5, pp. 1119–1130, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. D. R. Neill, S. H. Wong, A. Bellosi et al., “Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity,” Nature, vol. 464, no. 7293, pp. 1367–1370, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. A. E. Price, H. Liang, B. M. Sullivan et al., “Systemically dispersed innate IL-13-expressing cells in type 2 immunity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 25, pp. 11489–11494, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. H. Liang, R. L. Reinhardt, J. K. Bando, B. M. Sullivan, I. Ho, and R. M. Locksley, “Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity,” Nature Immunology, vol. 13, no. 1, pp. 58–66, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. J. L. Barlow, A. Bellosi, C. S. Hardman et al., “Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity,” Journal of Allergy and Clinical Immunology, vol. 129, no. 1, pp. 191–198, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. K. R. Bartemes, K. Iijima, T. Kobayashi, G. M. Kephart, A. N. McKenzie, and H. Kita, “IL-33-responsive lineage -CD25 +CD44 hi lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs,” Journal of Immunology, vol. 188, no. 3, pp. 1503–1513, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Y. Kim, Y. Chang, S. Subramanian et al., “Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity,” Journal of Allergy and Clinical Immunology, vol. 129, no. 1, pp. 216–227, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Magri, M. Miyajima, S. Bascones et al., “Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells,” Nature Immunology, vol. 15, no. 4, pp. 354–364, 2014. View at Publisher · View at Google Scholar
  16. J. H. Bernink, C. P. Peters, M. Munneke et al., “Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues,” Nature Immunology, vol. 14, no. 3, pp. 221–229, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Fuchs, W. Vermi, J. S. Lee et al., “Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-γ-producing cells,” Immunity, vol. 38, no. 4, pp. 769–781, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. C. S. Klose, M. Flach, L. Möhle et al., “Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages,” Cell, vol. 157, no. 2, pp. 340–356, 2014. View at Publisher · View at Google Scholar
  19. M. G. Constantinides, B. D. McDonald, P. A. Verhoef, and A. Bendelac, “A committed precursor to innate lymphoid cells,” Nature, vol. 508, no. 7496, pp. 397–401, 2014. View at Publisher · View at Google Scholar
  20. S. A. Saenz, M. C. Siracusa, J. G. Perrigoue et al., “IL25 elicits a multipotent progenitor cell population that promotes TH2 cytokine responses,” Nature, vol. 464, no. 7293, pp. 1362–1366, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. L. A. Monticelli, G. F. Sonnenberg, M. C. Abt et al., “Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus,” Nature Immunology, vol. 12, no. 11, pp. 1045–1054, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. D. M. W. Zaiss, J. van Loosdregt, A. Gorlani et al., “Amphiregulin enhances regulatory T cell-suppressive function via the epidermal growth factor receptor,” Immunity, vol. 38, no. 2, pp. 275–284, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. S. H. Wong, J. A. Walker, H. E. Jolin et al., “Transcription factor RORα is critical for nuocyte development,” Nature Immunology, vol. 13, no. 3, pp. 229–236, 2012. View at Google Scholar
  24. T. Hoyler, C. S. N. Klose, A. Souabni et al., “The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells,” Immunity, vol. 37, no. 4, pp. 634–648, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Buonocore, P. P. Ahern, H. H. Uhlig et al., “Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology,” Nature, vol. 464, no. 7293, pp. 1371–1375, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. J. Chang, H. Y. Kim, L. A. Albacker et al., “Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity,” Nature Immunology, vol. 12, no. 7, pp. 631–638, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Geremia, C. V. Arancibia-Cárcamo, M. P. P. Fleming et al., “IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease,” The Journal of Experimental Medicine, vol. 208, no. 6, pp. 1127–1133, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Vivier, D. H. Raulet, A. Moretta et al., “Innate or adaptive immunity? The example of natural killer cells,” Science, vol. 331, no. 6013, pp. 44–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. G. F. Sonnenberg, M. G. Nair, T. J. Kirn, C. Zaph, L. A. Fouser, and D. Artis, “Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A,” Journal of Experimental Medicine, vol. 207, no. 6, pp. 1293–1305, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Taube, C. Tertilt, G. Gyülveszi et al., “IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease,” PLoS ONE, vol. 6, no. 7, Article ID e21799, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Zheng, P. A. Valdez, D. M. Danilenko et al., “Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens,” Nature Medicine, vol. 14, no. 3, pp. 282–289, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Cella, A. Fuchs, W. Vermi et al., “A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity,” Nature, vol. 457, no. 7230, pp. 722–725, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Sawa, M. Lochner, N. Satoh-Takayama et al., “RORγt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota,” Nature Immunology, vol. 12, no. 4, pp. 320–326, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Takayama, N. Kamada, H. Chinen et al., “Imbalance of NKp44+NKp46- and NKp44-NKp46+ natural killer cells in the intestinal mucosa of patients with Crohn's disease,” Gastroenterology, vol. 139, no. 3, pp. 882.e3–892.e3, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Coccia, O. J. Harrison, C. Schiering et al., “IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4+ Th17 cells,” The Journal of Experimental Medicine, vol. 209, no. 9, pp. 1595–1609, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Glatzer, M. Killig, J. Meisig et al., “RORγt+ innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44,” Immunity, vol. 38, no. 6, pp. 1223–1235, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Sciumé, K. Hirahara, H. Takahashi et al., “Distinct requirements for T-bet in gut innate lymphoid cells,” The Journal of Experimental Medicine, vol. 209, no. 13, pp. 2331–2338, 2012. View at Publisher · View at Google Scholar
  38. C. S. N. Klose, E. A. Kiss, V. Schwierzeck et al., “A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells,” Nature, vol. 494, no. 7436, pp. 261–265, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. C. V. Vonarbourg, A. Mortha, V. L. Bui et al., “Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt+ innate lymphocytes,” Immunity, vol. 33, no. 5, pp. 736–751, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Qiu and L. Zhou, “Aryl hydrocarbon receptor promotes RORγt+ group 3 ILCs and controls intestinal immunity and inflammation,” Seminars in Immunopathology, vol. 35, no. 6, pp. 657–670, 2013. View at Google Scholar
  41. J. Qiu, X. Guo, Z. Chen et al., “Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora,” Immunity, vol. 39, no. 2, pp. 386–399, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. E. A. Kiss, C. Vonarbourg, S. Kopfmann et al., “Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles,” Science, vol. 334, no. 6062, pp. 1561–1565, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Zelante, R. Iannitti, C. Cunha et al., “Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22,” Immunity, vol. 39, no. 2, pp. 372–385, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. N. K. Crellin, S. Trifari, C. D. Kaplan, N. Satoh-Takayama, J. P. di Santo, and H. Spits, “Regulation of cytokine secretion in human CD127+ LTi-like innate lymphoid cells by Toll-like receptor 2,” Immunity, vol. 33, no. 5, pp. 752–764, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. L. A. Mielke, J. R. Groom, L. C. Rankin et al., “TCF-1 controls ILC2 and NKp46+RORγt+ innate lymphocyte differentiation and protection in intestinal inflammation,” Journal of Immunology, vol. 191, no. 8, pp. 4383–4391, 2013. View at Publisher · View at Google Scholar
  46. G. F. Sonnenberg, L. A. Monticelli, T. Alenghat et al., “Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria,” Science, vol. 336, no. 6086, pp. 1321–1325, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Killig, T. Glatzer, and C. Romagnani, “Recognition strategies of group 3 innate lymphoid cells,” Frontiers in Immunology, vol. 5, p. 142, 2014. View at Google Scholar
  48. N. Satoh-Takayama, C. A. J. Vosshenrich, S. Lesjean-Pottier et al., “Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense,” Immunity, vol. 29, no. 6, pp. 958–970, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. A. de Luca, T. Zelante, C. D'Angelo et al., “IL-22 defines a novel immune pathway of antifungal resistance,” Mucosal Immunology, vol. 3, no. 4, pp. 361–373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. L. A. Zenewicz, G. D. Yancopoulos, D. M. Valenzuela, A. J. Murphy, S. Stevens, and R. A. Flavell, “Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease,” Immunity, vol. 29, no. 6, pp. 947–957, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Eken, A. K. Singh, P. M. Treuting, and M. Oukka, “IL-23R+ innate lymphoid cells induce colitis via interleukin-22-dependent mechanism,” Mucosal Immunology, vol. 7, pp. 143–154, 2014. View at Publisher · View at Google Scholar
  52. A. Fuchs and M. Colonna, “Innate lymphoid cells in homeostasis, infection, chronic inflammation and tumors of the gastrointestinal tract,” Current Opinion in Gastroenterology, vol. 29, no. 6, pp. 581–587, 2013. View at Publisher · View at Google Scholar
  53. W. S. Garrett, G. M. Lord, S. Punit et al., “Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system,” Cell, vol. 131, no. 1, pp. 33–45, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Powell, A. W. Walker, E. Stolarczyk et al., “The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells,” Immunity, vol. 37, no. 4, pp. 674–684, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Kirchberger, D. J. Royston, O. Boulard et al., “Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model,” Journal of Experimental Medicine, vol. 210, no. 5, pp. 917–931, 2013. View at Publisher · View at Google Scholar · View at Scopus