The bile acid receptor GPBAR1 regulates the M1/M2 phenotype of intestinal macrophages and activation of gpbar1 rescues mice from murine colitis

Journal of Immunology

Volumn 199, Issue 2, 2017, Pages 718-733

  Biagioli, Michele ^a   Carino, Adriana ^a   Cipriani, Sabrina ^a   Francisci, Daniela ^a   Marchianò, Silvia ^a   Scarpelli, Paolo ^a   Sorcini, Daniele ^a   Zampella, Angela ^b   Fiorucci, Stefano ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

6B ETHYL 3A,7B DIHYDROXY 5B CHOLAN 24 OL; ANTIINFLAMMATORY AGENT; CD11B ANTIGEN; CHEMOKINE RECEPTOR CCR7; DEXAMETHASONE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; 6-ETHYL-3,7-DIHYDROXYCHOLAN-24-OL; CCL2 PROTEIN, MOUSE; CHOLESTANOL; G PROTEIN COUPLED RECEPTOR; GPBAR1 PROTEIN, MOUSE; IL10 PROTEIN, MOUSE; INTERLEUKIN-6, MOUSE; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; OXAZOLONE; TRINITROBENZENESULFONIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE MARROW CELL; CCL2 GENE; CELL MIGRATION; COLITIS; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; ENTERITIS; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GPBAR1 GENE; IFN GAMMA GENE; IL 10 GENE; IL 1BETA GENE; IL 6 GENE; IN VITRO STUDY; INTESTINE MUCOSA; LAMINA PROPRIA; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MONOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; TNF ALPHA GENE; WASTING SYNDROME; AGONISTS; ANIMAL; CELL LINE; CELL MOTION; CHEMICALLY INDUCED; DEFICIENCY; DRUG EFFECTS; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MUCOSA; PROMOTER REGION; REGULATORY T LYMPHOCYTE;

ANIMALS; ANTIGENS, LY; CELL LINE; CELL MOVEMENT; CHEMOKINE CCL2; CHOLESTANOLS; COLITIS; GENE EXPRESSION REGULATION; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTESTINAL MUCOSA; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MUCOUS MEMBRANE; OXAZOLONE; PHENOTYPE; PROMOTER REGIONS, GENETIC; RECEPTORS, G-PROTEIN-COUPLED; T-LYMPHOCYTES, REGULATORY; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85023208268     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1700183     Document Type: Article

References (41)

1. de Souza, H. S., and C. Fiocchi. 2016. Immunopathogenesis of IBD: current state of the art. Nat. Rev. Gastroenterol. Hepatol. 13: 13-27.
2. Danese, S., and J. Panés. 2014. Development of drugs to target interactions between leukocytes and endothelial cells and treatment algorithms for inflammatory bowel diseases. Gastroenterology 147: 981-989.
3. Mosli, M. H., J. Rivera-Nieves, and B. G. Feagan. 2014. T-cell trafficking and anti-adhesion strategies in inflammatory bowel disease: current and future prospects. Drugs 74: 297-311.
4. Fiorucci, S., and E. Distrutti. 2015. Bile acid-activated receptors, intestinal microbiota, and the treatment of metabolic disorders. Trends Mol. Med. 21: 702-714.
5. Fiorucci, S., S. Cipriani, A. Mencarelli, B. Renga, E. Distrutti, and F. Baldelli. 2010. Counter-regulatory role of bile acid activated receptors in immunity and inflammation. Curr. Mol. Med. 10: 579-595.
6. Chiang, J. Y. L. 2013. Bile acid metabolism and signaling. Compr. Physiol. 3: 1191-1212.
7. Cipriani, S., A. Mencarelli, M. G. Chini, E. Distrutti, B. Renga, G. Bifulco, F. Baldelli, A. Donini, and S. Fiorucci. 2011. The bile acid receptor GPBAR-1 (TGR5) modulates integrity of intestinal barrier and immune response to experimental colitis. [Published erratum appears in 2013 PLoS One 8(1).] PLoS One 6: e25637.
8. Renga, B., A. Mencarelli, S. Cipriani, C. D'Amore, A. Carino, A. Bruno, D. Francisci, A. Zampella, E. Distrutti, and S. Fiorucci. 2013. The bile acid sensor FXR is required for immune-regulatory activities of TLR-9 in intestinal inflammation. PLoS One 8: e54472.
9. Fiorucci, S., A. Mencarelli, E. Distrutti, and A. Zampella. 2012. Farnesoid X receptor: from medicinal chemistry to clinical applications. Future Med. Chem. 4: 877-891.
10. Mencarelli, A., B. Renga, M. Migliorati, S. Cipriani, E. Distrutti, L. Santucci, and S. Fiorucci. 2009. The bile acid sensor farnesoid X receptor is a modulator of liver immunity in a rodent model of acute hepatitis. J. Immunol. 183: 6657-6666.
11. Vavassori, P., A. Mencarelli, B. Renga, E. Distrutti, and S. Fiorucci. 2009. The bile acid receptor FXR is a modulator of intestinal innate immunity. J. Immunol. 183: 6251-6261.
12. Maruyama, T., Y. Miyamoto, T. Nakamura, Y. Tamai, H. Okada, E. Sugiyama, T. Nakamura, H. Itadani, and K. Tanaka. 2002. Identification of membrane-type receptor for bile acids (M-BAR). Biochem. Biophys. Res. Commun. 298: 714-719.
13. Kawamata, Y., R. Fujii, M. Hosoya, M. Harada, H. Yoshida, M. Miwa, S. Fukusumi, Y. Habata, T. Itoh, Y. Shintani, et al. 2003. A G protein-coupled receptor responsive to bile acids. J. Biol. Chem. 278: 9435-9440.
14. Parker, H. E., K. Wallis, C. W. le Roux, K. Y. Wong, F. Reimann, and F. M. Gribble. 2012. Molecular mechanisms underlying bile acid-stimulated glucagon-like peptide-1 secretion. Br. J. Pharmacol. 165: 414-423.
15. Watanabe, M., S. M. Houten, C. Mataki, M. A. Christoffolete, B. W. Kim, H. Sato, N. Messaddeq, J. W. Harney, O. Ezaki, T. Kodama, et al. 2006. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439: 484-489.
16. Newton, K., and V. M. Dixit. 2012. Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol. 4: a006049.
17. Sheikh, S. Z., and S. E. Plevy. 2010. The role of the macrophage in sentinel responses in intestinal immunity. Curr. Opin. Gastroenterol. 26: 578-582.
18. Sun, M., C. He, Y. Cong, and Z. Liu. 2015. Regulatory immune cells in regulation of intestinal inflammatory response to microbiota. Mucosal Immunol. 8: 969-978.
19. Kuhl, A. A., U. Erben, L. I. Kredel, and B. Siegmund. 2015. Diversity of intestinal macrophages in inflammatory bowel diseases. Front. Immunol. 6: 613.
20. Festa, C., B. Renga, C. D'Amore, V. Sepe, C. Finamore, S. De Marino, A. Carino, S. Cipriani, M. C. Monti, A. Zampella, and S. Fiorucci. 2014. Exploitation of cholane scaffold for the discovery of potent and selective farnesoid X receptor (FXR) and G-protein coupled bile acid receptor 1 (GP-BAR1) ligands. J. Med. Chem. 57: 8477-8495.
21. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686.
22. Jablonski, K. A., S. A. Amici, L. M. Webb, Jde. D. Ruiz-Rosado, P. G. Popovich, S. Partida-Sanchez, and M. Guerau-de-Arellano. 2015. Novel markers to delineate murine M1 and M2 macrophages. PLoS One 10: e0145342.
23. Bain, C. C., and A. M. Mowat. 2014. The monocyte-macrophage axis in the intestine. Cell. Immunol. 291: 41-48.
24. Cerovic, V., C. C. Bain, A. M. Mowat, and S. W. Milling. 2014. Intestinal macrophages and dendritic cells: what's the difference? Trends Immunol. 35: 270-277.
25. Xuan, W., Q. Qu, B. Zheng, S. Xiong, and G. H. Fan. 2015. The chemotaxis of M1 and M2 macrophages is regulated by different chemokines. J. Leukoc. Biol. 97: 61-69.
26. Badylak, S. F., J. E. Valentin, A. K. Ravindra, G. P. McCabe, and A. M. Stewart-Akers. 2008. Macrophage phenotype as a determinant of biologic scaffold remodeling. Tissue Eng. Part A 14: 1835-1842.
27. Bain, C. C., and A. M. Mowat. 2014. Macrophages in intestinal homeostasis and inflammation. Immunol. Rev. 260:102-117.
28. Gordon, S., and P. R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5: 953-964.
29. Wang, X., Q. Ouyang, and W. J. Luo. 2004. Oxazolone-induced murine model of ulcerative colitis. Chin. J. Dig. Dis. 5: 165-168.
30. Heller, F., I. J. Fuss, E. E. Nieuwenhuis, R. S. Blumberg, and W. Strober. 2002. Oxazolone colitis, a Th2 colitis model resembling ulcerative colitis, is mediated by IL-13-producing NK-T cells. Immunity 17: 629-638.
31. Fiorucci, S., A. Mencarelli, G. Palladino, and S. Cipriani. 2009. Bile-acid-activated receptors: targeting TGR5 and farnesoid-X-receptor in lipid and glucose disorders. Trends Pharmacol. Sci. 30: 570-580.
32. Wang, Q., C. H. Fang, and P. O. Hasselgren. 2001. Intestinal permeability is reduced and IL-10 levels are increased in septic IL-6 knockout mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281: R1013-R1023.
33. Waldner, M. J., and M. F. Neurath. 2009. Chemically induced mouse models of colitis. Curr. Protoc. Pharmacol. Chapter 5: Unit 5.55.
34. Cox, D., M. Brennan, and N. Moran. 2010. Integrins as therapeutic targets: lessons and opportunities. Nat. Rev. Drug Discov. 9: 804-820.
35. Rivollier, A., J. He, A. Kole, V. Valatas, and B. L. Kelsall. 2012. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 209: 139-155.
36. Deshmane, S. L., S. Kremlev, S. Amini, and B. E. Sawaya. 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. J. Interferon Cytokine Res. 29: 313-326.
37. Mencarelli, A., S. Cipriani, D. Francisci, L. Santucci, F. Baldelli, E. Distrutti, and S. Fiorucci. 2016. Highly specific blockade of CCR5 inhibits leukocyte trafficking and reduces mucosal inflammation in murine colitis. Sci. Rep. 6: 30802.
38. Oppermann, M. 2004. Chemokine receptor CCR5: insights into structure, function, and regulation. Cell. Signal. 16: 1201-1210.
39. Mitroulis, I., V. I. Alexaki, I. Kourtzelis, A. Ziogas, G. Hajishengallis, and T. Chavakis. 2015. Leukocyte integrins: role in leukocyte recruitment and as therapeutic targets in inflammatory disease. Pharmacol. Ther. 147: 123-135.
40. Zimmerman, N. P., R. A. Vongsa, M. K. Wendt, and M. B. Dwinell. 2008. Chemokines and chemokine receptors in mucosal homeostasis at the intestinal epithelial barrier in inflammatory bowel disease. Inflamm. Bowel Dis. 14: 1000-1011.
41. Motomura, Y., W. I. Khan, R. T. El-Sharkawy, M. Verma-Gandhu, E. F. Verdu, J. Gauldie, and S. M. Collins. 2006. Induction of a fibrogenic response in mouse colon by overexpression of monocyte chemoattractant protein 1. Gut 55: 662-670.