Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration

Nature

Volumn 528, Issue 7583, 2015, Pages 560-564

  Lindemans, Caroline A ^a,b   Calafiore, Marco ^a   Mertelsmann, Anna M ^a   O'Connor, Margaret H ^a   Dudakov, Jarrod A ^a,c   Jenq, Robert R ^a,d   Velardi, Enrico ^a   Young, Lauren F ^a   Smith, Odette M ^a   Lawrence, Gillian ^a   Ivanov, Juliet A ^a   Fu, Ya Yuan ^a   Takashima, Shuichiro ^a   Hua, Guoqiang ^a   Martin, Maria L ^a   O'Rourke, Kevin P ^a   Lo, Yuan Hung ^e   Mokry, Michal ^b   Romera Hernandez, Monica ^f   Cupedo, Tom ^f   Dow, Lukas E ^d   Nieuwenhuis, Edward E ^b   Shroyer, Noah F ^e   Liu, Chen ^g   Kolesnick, Richard ^a   Van Den Brink, Marcel R M ^a   Hanash, Alan M ^a   more..

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c MONASH UNIVERSITY   (Australia)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f ERASMUS MEDICAL CENTER   (Netherlands)

^g UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DIPHTHERIA TOXIN; INTERLEUKIN 22; SLIT2 PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; WNT PROTEIN; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; STAT3 PROTEIN, HUMAN; STAT3 PROTEIN, MOUSE;

BIOLOGICAL DEVELOPMENT; BONE; CELLS AND CELL COMPONENTS; DIGESTIVE SYSTEM; IMMUNE SYSTEM; MORTALITY; PATHOLOGY; REGROWTH; RODENT;

ALLOGENIC BONE MARROW TRANSPLANTATION; APOPTOSIS; ARTICLE; CELL REGENERATION; EPITHELIAL REGENERATION; FLOW CYTOMETRY; GENE EXPRESSION; GRAFT VERSUS HOST REACTION; IMMUNOFLUORESCENCE TEST; INTESTINAL STEM CELL; INTESTINE EPITHELIUM CELL; INTESTINE INJURY; INTRACELLULAR SIGNALING; LAMINA PROPRIA; LYMPHOID CELL; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STEM CELL NICHE; ANIMAL; CYTOLOGY; CYTOPLASM; DEFICIENCY; EPITHELIUM CELL; FEMALE; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MOUSE; MUCOSAL IMMUNITY; PATHOLOGY; PHOSPHORYLATION; REGENERATION; SIGNAL TRANSDUCTION; SMALL INTESTINE; STEM CELL;

ANIMALS; EPITHELIAL CELLS; FEMALE; GRAFT VS HOST DISEASE; HUMANS; IMMUNITY, MUCOSAL; INTERLEUKINS; INTESTINAL MUCOSA; INTESTINE, SMALL; MICE; ORGANOIDS; PANETH CELLS; PHOSPHORYLATION; REGENERATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STEM CELL NICHE; STEM CELLS;

EID: 84951283991     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16460     Document Type: Article

References (40)

1. Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007 (2007).
2. Sato, T. et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418 (2011).
3. Sonnenberg, G. F. & Artis, D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nature Med. 21, 698-708 (2015).
4. Dudakov, J. A., Hanash, A. M. & van den Brink, M. R. Interleukin-22: immunobiology and pathology. Annu. Rev. Immunol. 33, 747-785 (2015).
5. + stem cells are indispensable for radiation-induced intestinal regeneration. Cell Stem Cell 14, 149-159 (2014).
6. Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nature Med. 14, 282-289 (2008).
7. Zenewicz, L. A. et al. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 27, 647-659 (2007).
8. Aujla, S. J. et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nature Med. 14, 275-281 (2008).
9. Dudakov, J. A. et al. Interleukin-22 drives endogenous thymic regeneration in mice. Science 336, 91-95 (2012).
10. Sato, T. et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009).
11. Zhou, W. J., Geng, Z. H., Spence, J. R. & Geng, J. G. Induction of intestinal stem cells by R-spondin 1 and Slit2 augments chemoradioprotection. Nature 501, 107-111 (2013).
12. Pickert, G. et al. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 206, 1465-1472 (2009).
13. Matthews, J. R., Sansom, O. J. & Clarke, A. R. Absolute requirement for STAT3 function in small-intestine crypt stem cell survival. Cell Death Differ. 18, 1934-1943 (2011).
14. Hernández, P. P. et al. Interferon-λ and interleukin 22 act synergistically for the induction of interferon-stimulated genes and control of rotavirus infection. Nature Immunol. 16, 698-707 (2015).
15. Schust, J., Sperl, B., Hollis, A., Mayer, T. U. & Berg, T. Stattic: a small-molecule inhibitor of STAT3 activation and dimerization. Chem. Biol. 13, 1235-1242 (2006).
16. Muñoz, J. et al. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent '+4' cell markers. EMBO J. 31, 3079-3091 (2012).
17. + secretory progenitor cells revert to stem cells upon crypt damage. Nature Cell Biol. 14, 1099-1104 (2012).
18. Eriguchi, Y. et al. Reciprocal expression of enteric antimicrobial proteins in intestinal graft-versus-host disease. Biol. Blood Marrow Transplant. 19, 1525-1529 (2013).
19. Hanash, A. M. et al. Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 37, 339-350 (2012).
20. Takashima, S. et al. The Wnt agonist R-spondin1 regulates systemic graft-versus-host disease by protecting intestinal stem cells. J. Exp. Med. 208, 285-294 (2011).
21. Jenq, R. R. et al. Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation. J. Exp. Med. 209, 903-911 (2012).
22. Eriguchi, Y. et al. Graft-versus-host disease disrupts intestinal microbial ecology by inhibiting Paneth cell production of α-defensins. Blood 120, 223-231 (2012).
23. Levine, J. E. et al. Low Paneth cell numbers at onset of gastrointestinal graft-versus-host disease identify patients at high risk for nonrelapse mortality. Blood 122, 1505-1509 (2013).
24. Kabiri, Z. et al. Stroma provides an intestinal stem cell niche in the absence of epithelial Wnts. Development 141, 2206-2215 (2014).
25. Tian, H. et al. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478, 255-259 (2011).
26. Durand, A. et al. Functional intestinal stem cells after Paneth cell ablation induced by the loss of transcription factor Math1 (Atoh1). Proc. Natl Acad. Sci. USA 109, 8965-8970 (2012).
27. Couturier, M. et al. IL-22 deficiency in donor T cells attenuates murine acute graft-versus-host disease mortality while sparing the graft-versus-leukemia effect. Leukemia 27, 1527-1537 (2013).
28. Zhao, K. et al. Interleukin-22 aggravates murine acute graft-versus-host disease by expanding effector T cell and reducing regulatory T cell. J. Interferon Cytokine Res. 34, 707-715 (2014).
29. Munneke, J. M. et al. Activated innate lymphoid cells are associated with a reduced susceptibility to graft-versus-host disease. Blood 124, 812-821 (2014).
30. Hill, G. R. & Ferrara, J. L. The primacy of the gastrointestinal tract as a target organ of acute graft-versus-host disease: rationale for the use of cytokine shields in allogeneic bone marrow transplantation. Blood 95, 2754-2759 (2000).
31. Ootani, A. et al. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nature Med. 15, 701-706 (2009).
32. Wang, F. et al. Isolation and characterization of intestinal stem cells based on surface marker combinations and colony-formation assay. Gastroenterology 145, 383-395 (2013).
33. Magness, S. T. et al. A multicenter study to standardize reporting and analyses of fluorescence-activated cell-sorted murine intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 305, G542-G551 (2013).
34. Spits, H. et al. Innate lymphoid cells - a proposal for uniform nomenclature. Nature Rev. Immunol. 13, 145-149 (2013).
35. Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nature Med. 14, 282-289 (2008).
36. Shroyer, N. F. et al. Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 132, 2478-2488 (2007).
37. Alpdogan, Ö. et al. IL-7 enhances peripheral T cell reconstitution after allogeneic hematopoietic stem cell transplantation. J. Clin. Invest. 112, 1095-1107 (2003).
38. Cooke, K. R. et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood 88, 3230-3239 (1996).
39. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).
40. Mootha, V. K. et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nature Genet. 34, 267-273 (2003).