Macrophage-derived IL-10 mediates mucosal repair by epithelial WISP-1 signaling

Journal of Clinical Investigation

Volumn 127, Issue 9, 2017, Pages 3510-3520

  Quiros, Miguel ^a   Nishio, Hikaru ^b   Neumann, Philipp A ^c   Siuda, Dorothee ^a   Brazil, Jennifer C ^a   Azcutia, Veronica ^a   Hilgarth, Roland ^a   O'Leary, Monique N ^a   Garcia Hernandez, Vicky ^a   Leoni, Giovanna ^d   Feng, Mingli ^a   Bernal, Gabriela ^a   Williams, Holly ^a   Dedhia, Priya H ^a   Gerner Smidt, Christian ^b   Spence, Jason ^a   Parkos, Charles A ^a   Denning, Timothy L ^e   Nusrat, Asma ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^e GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLYCOPROTEIN P 15095; INTERLEUKIN 10; UNCLASSIFIED DRUG; WNT1 INDUCIBLE SIGNALING PROTEIN 1; WNT1 PROTEIN; CCN PROTEIN; CD11 ANTIGEN; CREB1 PROTEIN, HUMAN; IL10 PROTEIN, HUMAN; ONCOPROTEIN; WISP1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL PROLIFERATION; COLON MUCOSA; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN SYNTHESIS; STOMACH MUCOSA INJURY; T LYMPHOCYTE; WOUND CLOSURE; WOUND HEALING; ANIMAL; C57BL MOUSE; COLON; CYTOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; INFLAMMATION; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD11; CCN INTERCELLULAR SIGNALING PROTEINS; CELL PROLIFERATION; COLON; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EPITHELIAL CELLS; GENE DELETION; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-10; INTESTINAL MUCOSA; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; WOUND HEALING;

EID: 85028945710     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI90229     Document Type: Article

References (51)

1. Wallace KL, Zheng LB, Kanazawa Y, Shih DQ. Immunopathology of inflammatory bowel disease. World J Gastroenterol. 2014;20(1):6-21.
2. Leoni G, Neumann PA, Sumagin R, Denning TL, Nusrat A. Wound repair: role of immune-epithelial interactions. Mucosal Immunol. 2015;8(5):959-968.
3. Kole A, Maloy KJ. Control of intestinal inflammation by interleukin-10. Curr Top Microbiol Immunol. 2014;380:19-38.
4. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75(2):263-274.
5. Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol. 2007;8(10):1086-1094.
6. Berschneider B, Konigshoff M. WNT1 inducible signaling pathway protein 1 (WISP1): a novel mediator linking development and disease. Int J Biochem Cell Biol. 2011;43(3):306-309.
7. Leoni G, et al. Annexin A1, formyl peptide receptor, and NOX1 orchestrate epithelial repair. J Clin Invest. 2013;123(1):443-454.
8. Leoni G, et al. Annexin A1-containing extracellular vesicles and polymeric nanoparticles promote epithelial wound repair. J Clin Invest. 2015;125(3):1215-1227.
9. Chassaing B, Srinivasan G, Delgado MA, Young AN, Gewirtz AT, Vijay-Kumar M. Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation. PLoS ONE. 2012;7(9):e44328.
10. Ranatunga DC, et al. A protective role for human IL-10-expressing CD4+ T cells in colitis. J Immunol. 2012;189(3):1243-1252.
11. Yanaba K, Yoshizaki A, Asano Y, Kadono T, Tedder TF, Sato S. IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol. 2011;178(2):735-743.
12. Xu L, Corcoran RB, Welsh JW, Pennica D, Levine AJ. WISP-1 is a Wnt-1-and beta-catenin-responsive oncogene. Genes Dev. 2000;14(5):585-595.
13. Capaldo CT, et al. IFN-γ and TNF-α-induced GBP-1 inhibits epithelial cell proliferation through suppression of β-catenin/TCF signaling. Mucosal Immunol. 2012;5(6):681-690.
14. Sansom OJ, et al. Myc deletion rescues Apc deficiency in the small intestine. Nature. 2007;446(7136):676-679.
15. Konigshoff M, et al. WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J Clin Invest. 2009;119(4):772-787.
16. Blander JM. Death in the intestinal epitheliumbasic biology and implications for inflammatory bowel disease. FEBS J. 2016;283(14):2720-2730.
17. Rivollier A, He J, Kole A, Valatas V, Kelsall BL. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J Exp Med. 2012;209(1):139-155.
18. Hayashi A, et al. A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host Microbe. 2013;13(6):711-722.
19. Ueda Y, et al. Commensal microbiota induce LPS hyporesponsiveness in colonic macrophages via the production of IL-10. Int Immunol. 2010;22(12):953-962.
20. Novak ML, Weinheimer-Haus EM, Koh TJ. Macrophage activation and skeletal muscle healing following traumatic injury. J Pathol. 2014;232(3):344-355.
21. Verma SK, et al. IL-10 Accelerates Re-Endothelialization and Inhibits Post-Injury Intimal Hyperplasia following Carotid Artery Denudation. PLoS ONE. 2016;11(1):e0147615.
22. Inoue G. Effect of interleukin-10 (IL-10) on experimental LPS-induced acute lung injury. J Infect Chemother. 2000;6(1):51-60.
23. Kominsky DJ, et al. IFN-γ-mediated induction of an apical IL-10 receptor on polarized intestinal epithelia. J Immunol. 2014;192(3):1267-1276.
24. King A, Balaji S, Le LD, Marsh E, Crombleholme TM, Keswani SG. Interleukin-10 regulates fetal extracellular matrix hyaluronan production. J Pediatr Surg. 2013;48(6):1211-1217.
25. Balaji S, et al. The role of interleukin-10 and hyaluronan in murine fetal fibroblast function in vitro: implications for recapitulating fetal regenerative wound healing. PLoS ONE. 2015;10(5):e0124302.
26. Autschbach F, et al. In situ expression of interleukin-10 in noninflamed human gut and in inflammatory bowel disease. Am J Pathol. 1998;153(1):121-130.
27. Jarry A, et al. Mucosal IL-10 and TGF-beta play crucial roles in preventing LPS-driven, IFN-gamma-mediated epithelial damage in human colon explants. J Clin Invest. 2008;118(3):1132-1142.
28. Kasten KR, Muenzer JT, Caldwell CC. Neutrophils are significant producers of IL-10 during sepsis. Biochem Biophys Res Commun. 2010;393(1):28-31.
29. Goto Y, et al. IL-10-producing CD4(+) T cells negatively regulate fucosylation of epithelial cells in the gut. Sci Rep. 2015;5:15918.
30. Leibovich SJ, Ross R. The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am J Pathol. 1975;78(1):71-100.
31. Hunt TK, Knighton DR, Thakral KK, Goodson WH, Andrews WS. Studies on inflammation and wound healing: angiogenesis and collagen synthesis stimulated in vivo by resident and activated wound macrophages. Surgery. 1984;96(1):48-54.
32. Mirza R, DiPietro LA, Koh TJ. Selective and specific macrophage ablation is detrimental to wound healing in mice. Am J Pathol. 2009;175(6):2454-2462.
33. Lucas T, et al. Differential roles of macrophages in diverse phases of skin repair. J Immunol. 2010;184(7):3964-3977.
34. Bain CC, et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol. 2014;15(10):929-937.
35. Itoh K, Hirohata S. The role of IL-10 in human B cell activation, proliferation, and differentiation. J Immunol. 1995;154(9):4341-4350.
36. Thompson-Snipes L, Dhar V, Bond MW, Mosmann TR, Moore KW, Rennick DM. Interleukin 10: a novel stimulatory factor for mast cells and their progenitors. J Exp Med. 1991;173(2):507-510.
37. Dosanjh A, Morris RE, Wan B. Bronchial epithelial cell-derived cytokine IL-10 and lung fibroblast proliferation. Transplant Proc. 2001;33(1-2):352-354.
38. Eming SA, et al. Accelerated wound closure in mice deficient for interleukin-10. Am J Pathol. 2007;170(1):188-202.
39. Shaywitz AJ, Greenberg ME. CREB: a stimulusinduced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem. 1999;68:821-861.
40. Wen AY, Sakamoto KM, Miller LS. The role of the transcription factor CREB in immune function. J Immunol. 2010;185(11):6413-6419.
41. Della Fazia MA, Servillo G, Sassone-Corsi P. Cyclic AMP signalling and cellular proliferation: regulation of CREB and CREM. FEBS Lett. 1997;410(1):22-24.
42. Dworkin S, et al. CREB activity modulates neural cell proliferation, midbrain-hindbrain organization and patterning in zebrafish. Dev Biol. 2007;307(1):127-141.
43. Bird AD, et al. cAMP response element binding protein is required for differentiation of respiratory epithelium during murine development. PLoS ONE. 2011;6(3):e17843.
44. Xu J, Tian J, Grumelli SM, Haley KJ, Shapiro SD. Stage-specific effects of cAMP signaling during distal lung epithelial development. J Biol Chem. 2006;281(50):38894-38904.
45. Gubbay O, Rae MT, McNeilly AS, Donadeu FX, Zeleznik AJ, Hillier SG. cAMP response element-binding (CREB) signalling and ovarian surface epithelial cell survival. J Endocrinol. 2006;191(1):275-285.
46. Fullerton JN, Gilroy DW. Resolution of inflammation: a new therapeutic frontier. Nat Rev Drug Discov. 2016;15(8):551-567.
47. Kucharzik T, Stoll R, Lugering N, Domschke W. Circulating antiinflammatory cytokine IL-10 in patients with inflammatory bowel disease (IBD). Clin Exp Immunol. 1995;100(3):452-456. 48. [No authors listed]. Seventh international workshop on the CCN family of genes. J Cell Commun Signal. 2014;8(1):77-92.
48. Loh YH, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet. 2006;38(4):431-440.
49. Li J, Li J, Chen B. Oct4 was a novel target of Wnt signaling pathway. Mol Cell Biochem. 2012;362(1-2):233-240.
50. Klee S, Lehmann M, Wagner DE, Baarsma HA, Konigshoff M. WISP1 mediates IL-6-dependent proliferation in primary human lung fibroblasts. Sci Rep. 2016;6:20547.
51. Roers A, et al. T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J Exp Med. 2004;200(10):1289-1297.