Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit

Nature

Volumn 529, Issue 7585, 2016, Pages 221-225

  Von Moltke, Jakob ^a   Ji, Ming ^a,b   Liang, Hong Erh ^a   Locksley, Richard M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHROMOGRANIN A; DOUBLECORTIN; DOUBLECORTIN LIKE KINASE 1; EPITHELIAL CELL ADHESION MOLECULE; INTERLEUKIN 13; INTERLEUKIN 25; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 5; MUCIN 2; PROSTAGLANDIN ENDOPEROXIDE SYNTHASE 1; PROSTAGLANDIN SYNTHASE; THYMIC STROMAL LYMPHOPOIETIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL M5; UNCLASSIFIED DRUG; INTERLEUKIN 17; PARASITE ANTIGEN;

ANNELID; CELLS AND CELL COMPONENTS; DIGESTIVE SYSTEM; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNITY; MUSCLE; PARASITE; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL HYPERPLASIA; CONTROLLED STUDY; CYTOKINE RELEASE; FLOW CYTOMETRY; GOBLET CELL; HELIGMOSOMOIDES POLYGYRUS; HELMINTHIASIS; HEMATOPOIETIC CELL; IMMUNOHISTOCHEMISTRY; INTESTINE CELL; LAMINA PROPRIA; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE CONTRACTION; TUFT CELL; ANIMAL; CELL PROLIFERATION; CYTOLOGY; FEMALE; HOMEOSTASIS; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE MUCOSA; LYMPHOCYTE; MALE; METABOLISM; MUCOSAL IMMUNITY; NIPPOSTRONGYLUS; SECRETION (PROCESS); SIGNAL TRANSDUCTION; SMALL INTESTINE; STEM CELL; STRONGYLE INFECTION; TH2 CELL;

MUS; VERMES;

ANIMALS; ANTIGENS, HELMINTH; CELL PROLIFERATION; FEMALE; GOBLET CELLS; HOMEOSTASIS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INTERLEUKIN-13; INTERLEUKIN-17; INTESTINAL MUCOSA; INTESTINE, SMALL; LYMPHOCYTES; MALE; MICE; NIPPOSTRONGYLUS; SIGNAL TRANSDUCTION; STEM CELLS; STRONGYLIDA INFECTIONS; TH2 CELLS;

EID: 84954286513     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16161     Document Type: Article

References (31)

1. Miller, H. R., Nawa, Y. Immune regulation of intestinal goblet cell differentiation. Specific induction of nonspecific protection against helminths Nouv. Rev. Fr. Hematol. 21, 31-45 (1979).
2. Castro, G. A., Badial-Aceves, F., Smith, J. W., Dudrick, S. J., Weisbrodt, N. W. Altered small bowel propulsion associated with parasitism. Gastroenterology 71, 620-625 (1976).
3. Grencis, R. K. Immunity to helminths: resistance, regulation, and susceptibility to gastrointestinal nematodes. Annu. Rev. Immunol. 33, 201-225 (2015).
4. Price, A. E. et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl Acad. Sci. USA 107, 11489-11494 (2010).
5. Neill, D. R. et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367-1370 (2010).
6. Fallon, P. G. et al. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J. Exp. Med. 203, 1105-1116 (2006).
7. Kang, Z. et al. Epithelial cell-specific Act1 adaptor mediates interleukin-25-dependent helminth expulsion through expansion of Linc-Kit+ innate cell population. Immunity 36, 821-833 (2012).
8. Zhao, A. et al. Critical role of IL-25 in nematode infection-induced alterations in intestinal function. J. Immunol. 185, 6921-6929 (2010).
9. Van Dyken, S. J. et al. Chitin activates parallel immune modules that direct distinct inflammatory responses via innate lymphoid type 2 and T cells. Immunity 40, 414-424 (2014).
10. Owyang, A. M. et al. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J. Exp. Med. 203, 843-849 (2006).
11. Angkasekwinai, P. et al. Interleukin 25 promotes the initiation of proallergic type 2 responses. J. Exp. Med. 204, 1509-1517 (2007).
12. Clevers, H. The intestinal crypt, a prototype stem cell compartment. Cell 154, 274-284 (2013).
13. Bjerknes, M. et al. Origin of the brush cell lineage in the mouse intestinal epithelium. Dev. Biol. 362, 194-218 (2012).
14. Gerbe, F., Legraverend, C., Jay, P. The intestinal epithelium tuft cells: specification and function. Cell. Mol. Life Sci. 69, 2907-2917 (2012).
15. Bezençon, C. et al. Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. J. Comp. Neurol. 509, 514-525 (2008).
16. McKenzie, G. J., Bancroft, A., Grencis, R. K., McKenzie, A. N. J. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr. Biol. 8, 339-342 (1998).
17. Fort, M. M. et al. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15, 985-995 (2001).
18. Hurst, S. D. et al. New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J. Immunol. 169, 443-453 (2002).
19. Liang, H.-E. et al. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nature Immunol. 13, 58-66 (2012).
20. Voehringer, D., Reese, T. A., Huang, X., Shinkai, K., Locksley, R. M. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic noneosinophil cells of the innate immune system. J. Exp. Med. 203, 1435-1446 (2006).
21. Oliphant, C. J. et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4+ T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 41, 283-295 (2014).
22. Munõz, J. et al. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent '+ 4' cell markers. EMBO J. 31, 3079-3091 (2012).
23. Reinecker, H. C., Podolsky, D. K. Human intestinal epithelial cells express functional cytokine receptors sharing the common gamma c chain of the interleukin 2 receptor. Proc. Natl Acad. Sci. USA 92, 8353-8357 (1995).
24. Nussbaum, J. C. et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502, 245-248 (2013).
25. Deckmann, K. et al. Bitter triggers acetylcholine release from polymodal urethral chemosensory cells and bladder reflexes. Proc. Natl Acad. Sci. USA 111, 8287-8292 (2014).
26. Krasteva, G. et al. Cholinergic chemosensory cells in the trachea regulate breathing. Proc. Natl Acad. Sci. USA 108, 9478-9483 (2011).
27. Saunders, C. J., Christensen, M., Finger, T. E., Tizzano, M. Cholinergic neurotransmission links solitary chemosensory cells to nasal inflammation. Proc. Natl Acad. Sci. USA 111, 6075-6080 (2014).
28. Lee, R. J. et al. Bitter and sweet taste receptors regulate human upper respiratory innate immunity. J. Clin. Invest. 124, 1393-1405 (2014).
29. Ballantyne, S. J. et al. Blocking IL-25 prevents airway hyperresponsiveness in allergic asthma. J. Allergy Clin. Immunol. 120, 1324-1331 (2007).
30. Han, H., Thelen, T. D., Comeau, M. R., Ziegler, S. F. Thymic stromal lymphopoietin-mediated epicutaneous inflammation promotes acute diarrhea and anaphylaxis. J. Clin. Invest. 124, 5442-5452 (2014).
31. Sato, T., Clevers, H. Primary mouse small intestinal epithelial cell cultures. Methods Mol. Biol. 945, 319-328 (2013).