IL-33 promotes recovery from acute colitis by inducing miR-320 to stimulate epithelial restitution and repair

Proceedings of the National Academy of Sciences of the United States of America

Volumn 115, Issue 40, 2018, Pages E9362-E9370

  Lopetuso, Loris R ^a,b,c   De Salvo, Carlo ^a   Pastorelli, Luca ^a,d,e   Rana, Nitish ^a   Senkfor, Henry N ^a   Petito, Valentina ^a,b,c   Di Martino, Luca ^a   Scaldaferri, Franco ^b,c   Gasbarrini, Antonio ^b,c   Cominelli, Fabio ^a   Abbott, Derek W ^a   Goodman, Wendy A ^a   Pizarro, Theresa T ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e IRCCS POLICLINICO SAN DONATO   (Italy)

Author keywords

DSS colitis; IBD; IL 33 ST2; Mir 320; Mucosal healing

Indexed keywords

INTERLEUKIN 1 RECEPTOR LIKE 1 PROTEIN; INTERLEUKIN 33; MESSENGER RNA; MICRORNA; MICRORNA 320; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 33; UNCLASSIFIED DRUG; DEXTRAN SULFATE; IL1RL1 PROTEIN, HUMAN; IL1RL1 PROTEIN, MOUSE; IL33 PROTEIN, HUMAN; IL33 PROTEIN, MOUSE; MIRN320 MICRORNA, HUMAN; MIRN320 MICRORNA, MOUSE;

ACUTE DISEASE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT GAIN; BODY WEIGHT LOSS; C57BL 6 MOUSE; CACO-2 CELL LINE; CELL PROLIFERATION; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CONVALESCENCE; CRYPT CELL; DEXTRAN SULFATE SODIUM-INDUCED COLITIS; DISEASE ACTIVITY; DISEASE EXACERBATION; DISEASE SEVERITY; EPITHELIZATION; GENE EXPRESSION REGULATION; GOBLET CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; LAMINA PROPRIA; MICROARRAY ANALYSIS; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE DISTRIBUTION; UPREGULATION; WOUND HEALING; ANIMAL; CHEMICALLY INDUCED; COLITIS; GENETICS; INFLAMMATORY BOWEL DISEASE; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; REGENERATION;

ACUTE DISEASE; ANIMALS; CACO-2 CELLS; COLITIS; DEXTRAN SULFATE; HUMANS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-1 RECEPTOR-LIKE 1 PROTEIN; INTERLEUKIN-33; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; MICRORNAS; REGENERATION;

EID: 85054376127     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1803613115     Document Type: Article

References (38)

1. Leoni G, Neumann PA, Sumagin R, Denning TL, Nusrat A (2015) Wound repair: Role of immune-epithelial interactions. Mucosal Immunol 8:959–968.
2. Cominelli F (2004) Cytokine-based therapies for Crohn’s disease–new paradigms. N Engl J Med 351:2045–2048.
3. Lopetuso LR, Chowdhry S, Pizarro TT (2013) Opposing functions of classic and novel IL-1 family members in gut health and disease. Front Immunol 4:181.
4. Schmitz J, et al. (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23:479–490.
5. Pastorelli L, et al. (2010) Epithelial-derived IL-33 and its receptor ST2 are dysregulated in ulcerative colitis and in experimental Th1/Th2 driven enteritis. Proc Natl Acad Sci USA 107:8017–8022.
6. Beltrán CJ, et al. (2010) Characterization of the novel ST2/IL-33 system in patients with inflammatory bowel disease. Inflamm Bowel Dis 16:1097–1107.
7. Kobori A, et al. (2010) Interleukin-33 expression is specifically enhanced in inflamed mucosa of ulcerative colitis. J Gastroenterol 45:999–1007.
8. Seidelin JB, et al. (2010) IL-33 is upregulated in colonocytes of ulcerative colitis. Immunol Lett 128:80–85.
9. Sponheim J, et al. (2010) Inflammatory bowel disease-associated interleukin-33 is preferentially expressed in ulceration-associated myofibroblasts. Am J Pathol 177: 2804–2815.
10. Carriere V, et al. (2007) IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc Natl Acad Sci USA 104:282–287.
11. Moussion C, Ortega N, Girard JP (2008) The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: A novel ‘alarmin’? PLoS One 3:e3331.
12. Chackerian AA, et al. (2007) IL-1 receptor accessory protein and ST2 comprise the IL-33 receptor complex. J Immunol 179:2551–2555.
13. Hayakawa H, Hayakawa M, Kume A, Tominaga S (2007) Soluble ST2 blocks interleukin-33 signaling in allergic airway inflammation. J Biol Chem 282:26369–26380.
14. + regulatory T-cell responses in mice. Mol Med 18:753–761.
15. Schiering C, et al. (2014) The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 513:564–568.
16. Min/+ mice. Sci Rep 7:5520.
17. Liew FY, Girard JP, Turnquist HR (2016) Interleukin-33 in health and disease. Nat Rev Immunol 16:676–689.
18. Okayasu I, et al. (1990) A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98:694–702.
19. Dieleman LA, et al. (1994) Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 107:1643–1652.
20. Cayrol C, Girard JP (2009) The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc Natl Acad Sci USA 106:9021–9026.
21. Groβ P, Doser K, Falk W, Obermeier F, Hofmann C (2012) IL-33 attenuates development and perpetuation of chronic intestinal inflammation. Inflamm Bowel Dis 18: 1900–1909.
22. Zhu J, et al. (2015) IL-33 alleviates DSS-induced chronic colitis in C57BL/6 mice colon lamina propria by suppressing Th17 cell response as well as Th1 cell response. Int Immunopharmacol 29:846–853.
23. Monticelli LA, et al. (2015) IL-33 promotes an innate immune pathway of intestinal tissue protection dependent on amphiregulin-EGFR interactions. Proc Natl Acad Sci USA 112:10762–10767.
24. Sedhom MA, et al. (2013) Neutralisation of the interleukin-33/ST2 pathway ameliorates experimental colitis through enhancement of mucosal healing in mice. Gut 62: 1714–1723.
25. Pizarro TT, et al. (2011) SAMP1/YitFc mouse strain: A spontaneous model of Crohn’s disease-like ileitis. Inflamm Bowel Dis 17:2566–2584.
26. De Salvo C, et al. (2016) IL-33 drives eosinophil infiltration and pathogenic type 2 helper T-cell immune responses leading to chronic experimental ileitis. Am J Pathol 186:885–898.
27. Medina-Contreras O, et al. (2016) Cutting edge: IL-36 receptor promotes resolution of intestinal damage. J Immunol 196:34–38.
28. Ngo VL, et al. (2018) A cytokine network involving IL-36γ, IL-23, and IL-22 promotes antimicrobial defense and recovery from intestinal Barrier damage. Proc Natl Acad Sci USA 115:E5076–E5085.
29. Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11:597–610.
30. Xiao L, et al. (2011) Regulation of cyclin-dependent kinase 4 translation through CUG-binding protein 1 and microRNA-222 by polyamines. Mol Biol Cell 22:3055–3069.
31. Xiao L, Wang JY (2014) RNA-binding proteins and microRNAs in gastrointestinal epithelial homeostasis and diseases. Curr Opin Pharmacol 19:46–53.
32. Fasseu M, et al. (2010) Identification of restricted subsets of mature microRNA abnormally expressed in inactive colonic mucosa of patients with inflammatory bowel disease. PLoS One 5:e13160.
33. Pierdomenico M, et al. (2016) NOD2 is regulated by Mir-320 in physiological conditions but this control is altered in inflamed tissues of patients with inflammatory bowel disease. Inflamm Bowel Dis 22:315–326.
34. Hugot JP, et al. (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease. Nature 411:599–603.
35. Ogura Y, et al. (2001) A frameshift mutation in NOD2 associated with susceptibility to Crohn’s disease. Nature 411:603–606.
36. Scaldaferri F, et al. (2007) Crucial role of the protein C pathway in governing micro-vascular inflammation in inflammatory bowel disease. J Clin Invest 117:1951–1960.
37. Kodani T, et al. (2013) Flexible colonoscopy in mice to evaluate the severity of colitis and colorectal tumors using a validated endoscopic scoring system. J Vis Exp 80:e50843.
38. Olson TS, et al. (2006) The primary defect in experimental ileitis originates from a nonhematopoietic source. J Exp Med 203:541–552.