Bile Acids Control Inflammation and Metabolic Disorder through Inhibition of NLRP3 Inflammasome

Immunity

Volumn 45, Issue 4, 2016, Pages 802-816

  Guo, Chuansheng ^a   Xie, Shujun ^a,b   Chi, Zhexu ^a   Zhang, Jinhua ^c   Liu, Yangyang ^a   Zhang, Li ^a   Zheng, Mingzhu ^a   Zhang, Xue ^a   Xia, Dajing ^b   Ke, Yuehai ^a   Lu, Linrong ^a   Wang, Di ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c ZHEJIANG PROVINCIAL PEOPLE'S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ALUMINUM POTASSIUM SULFATE; ALUMINUM SALT; BILE ACID; CASPASE 11; CRYOPYRIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; G PROTEIN COUPLED RECEPTOR; INFLAMMASOME; NLRP3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INFECTION CONTROL; INFLAMMATORY DISEASE; INSULIN RESISTANCE; LIPOPOLYSACCHARIDE-INDUCED SEPSIS; METABOLIC DISORDER; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PERITONITIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; CELL LINE; HEK293 CELL LINE; INFLAMMATION; MALE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; BILE ACIDS AND SALTS; CELL LINE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HEK293 CELLS; HUMANS; INFLAMMASOMES; INFLAMMATION; MALE; METABOLIC DISEASES; MICE; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PHOSPHORYLATION; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84994817318     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.09.008     Document Type: Article

References (50)

1. Broeders, E.P., Nascimento, E.B., Havekes, B., Brans, B., Roumans, K.H., Tailleux, A., Schaart, G., Kouach, M., Charton, J., Deprez, B., et al. The Bile Acid Chenodeoxycholic Acid Increases Human Brown Adipose Tissue Activity. Cell Metab. 22 (2015), 418–426.
2. Davis, B.K., Wen, H., Ting, J.P., The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29 (2011), 707–735.
3. de Aguiar Vallim, T.Q., Tarling, E.J., Edwards, P.A., Pleiotropic roles of bile acids in metabolism. Cell Metab. 17 (2013), 657–669.
4. Fiorucci, S., Distrutti, E., Bile Acid-Activated Receptors, Intestinal Microbiota, and the Treatment of Metabolic Disorders. Trends Mol. Med. 21 (2015), 702–714.
5. Gao, M., Karin, M., Regulating the regulators: control of protein ubiquitination and ubiquitin-like modifications by extracellular stimuli. Mol. Cell 19 (2005), 581–593.
6. Genet, C., Strehle, A., Schmidt, C., Boudjelal, G., Lobstein, A., Schoonjans, K., Souchet, M., Auwerx, J., Saladin, R., Wagner, A., Structure-activity relationship study of betulinic acid, a novel and selective TGR5 agonist, and its synthetic derivatives: potential impact in diabetes. J. Med. Chem. 53 (2010), 178–190.
7. Gloerich, M., Bos, J.L., Epac: defining a new mechanism for cAMP action. Annu. Rev. Pharmacol. Toxicol. 50 (2010), 355–375.
8. Guo, H., Callaway, J.B., Ting, J.P., Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 21 (2015), 677–687.
9. Hara, H., Tsuchiya, K., Kawamura, I., Fang, R., Hernandez-Cuellar, E., Shen, Y., Mizuguchi, J., Schweighoffer, E., Tybulewicz, V., Mitsuyama, M., Phosphorylation of the adaptor ASC acts as a molecular switch that controls the formation of speck-like aggregates and inflammasome activity. Nat. Immunol. 14 (2013), 1247–1255.
10. Haselow, K., Bode, J.G., Wammers, M., Ehlting, C., Keitel, V., Kleinebrecht, L., Schupp, A.K., Häussinger, D., Graf, D., Bile acids PKA-dependently induce a switch of the IL-10/IL-12 ratio and reduce proinflammatory capability of human macrophages. J. Leukoc. Biol. 94 (2013), 1253–1264.
11. Hov, J.R., Keitel, V., Laerdahl, J.K., Spomer, L., Ellinghaus, E., ElSharawy, A., Melum, E., Boberg, K.M., Manke, T., Balschun, T., et al., IBSEN Study Group. Mutational characterization of the bile acid receptor TGR5 in primary sclerosing cholangitis. PLoS ONE, 5, 2010, e12403.
12. Hunter, T., The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 28 (2007), 730–738.
13. Juliana, C., Fernandes-Alnemri, T., Kang, S., Farias, A., Qin, F., Alnemri, E.S., Non-transcriptional priming and deubiquitination regulate NLRP3 inflammasome activation. J. Biol. Chem. 287 (2012), 36617–36622.
14. Kawamata, Y., Fujii, R., Hosoya, M., Harada, M., Yoshida, H., Miwa, M., Fukusumi, S., Habata, Y., Itoh, T., Shintani, Y., et al. A G protein-coupled receptor responsive to bile acids. J. Biol. Chem. 278 (2003), 9435–9440.
15. Kayagaki, N., Warming, S., Lamkanfi, M., Vande Walle, L., Louie, S., Dong, J., Newton, K., Qu, Y., Liu, J., Heldens, S., et al. Non-canonical inflammasome activation targets caspase-11. Nature 479 (2011), 117–121.
16. Kayagaki, N., Wong, M.T., Stowe, I.B., Ramani, S.R., Gonzalez, L.C., Akashi-Takamura, S., Miyake, K., Zhang, J., Lee, W.P., Muszyński, A., et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341 (2013), 1246–1249.
17. Keitel, V., Donner, M., Winandy, S., Kubitz, R., Häussinger, D., Expression and function of the bile acid receptor TGR5 in Kupffer cells. Biochem. Biophys. Res. Commun. 372 (2008), 78–84.
18. Kosako, H., Yamaguchi, N., Aranami, C., Ushiyama, M., Kose, S., Imamoto, N., Taniguchi, H., Nishida, E., Hattori, S., Phosphoproteomics reveals new ERK MAP kinase targets and links ERK to nucleoporin-mediated nuclear transport. Nat. Struct. Mol. Biol. 16 (2009), 1026–1035.
19. Lamkanfi, M., Dixit, V.M., Mechanisms and functions of inflammasomes. Cell 157 (2014), 1013–1022.
20. Latz, E., Xiao, T.S., Stutz, A., Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13 (2013), 397–411.
21. Lee, G.S., Subramanian, N., Kim, A.I., Aksentijevich, I., Goldbach-Mansky, R., Sacks, D.B., Germain, R.N., Kastner, D.L., Chae, J.J., The calcium-sensing receptor regulates the NLRP3 inflammasome through Ca2+ and cAMP. Nature 492 (2012), 123–127.
22. Lu, A., Magupalli, V.G., Ruan, J., Yin, Q., Atianand, M.K., Vos, M.R., Schröder, G.F., Fitzgerald, K.A., Wu, H., Egelman, E.H., Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell 156 (2014), 1193–1206.
23. Martinon, F., Pétrilli, V., Mayor, A., Tardivel, A., Tschopp, J., Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440 (2006), 237–241.
24. Maruyama, T., Miyamoto, Y., Nakamura, T., Tamai, Y., Okada, H., Sugiyama, E., Nakamura, T., Itadani, H., Tanaka, K., Identification of membrane-type receptor for bile acids (M-BAR). Biochem. Biophys. Res. Commun. 298 (2002), 714–719.
25. ∗). Annu. Rev. Immunol. 27 (2009), 621–668.
26. Misawa, T., Takahama, M., Kozaki, T., Lee, H., Zou, J., Saitoh, T., Akira, S., Microtubule-driven spatial arrangement of mitochondria promotes activation of the NLRP3 inflammasome. Nat. Immunol. 14 (2013), 454–460.
27. Montminy, M., Transcriptional regulation by cyclic AMP. Annu. Rev. Biochem. 66 (1997), 807–822.
28. Pellicciari, R., Gioiello, A., Macchiarulo, A., Thomas, C., Rosatelli, E., Natalini, B., Sardella, R., Pruzanski, M., Roda, A., Pastorini, E., et al. Discovery of 6alpha-ethyl-23(S)-methylcholic acid (S-EMCA, INT-777) as a potent and selective agonist for the TGR5 receptor, a novel target for diabesity. J. Med. Chem. 52 (2009), 7958–7961.
29. Perino, A., Schoonjans, K., TGR5 and Immunometabolism: Insights from Physiology and Pharmacology. Trends Pharmacol. Sci. 36 (2015), 847–857.
30. Perino, A., Pols, T.W., Nomura, M., Stein, S., Pellicciari, R., Schoonjans, K., TGR5 reduces macrophage migration through mTOR-induced C/EBPβ differential translation. J. Clin. Invest. 124 (2014), 5424–5436.
31. Pols, T.W., Nomura, M., Harach, T., Lo Sasso, G., Oosterveer, M.H., Thomas, C., Rizzo, G., Gioiello, A., Adorini, L., Pellicciari, R., et al. TGR5 activation inhibits atherosclerosis by reducing macrophage inflammation and lipid loading. Cell Metab. 14 (2011), 747–757.
32. Pols, T.W., Noriega, L.G., Nomura, M., Auwerx, J., Schoonjans, K., The bile acid membrane receptor TGR5 as an emerging target in metabolism and inflammation. J. Hepatol. 54 (2011), 1263–1272.
33. Py, B.F., Kim, M.S., Vakifahmetoglu-Norberg, H., Yuan, J., Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol. Cell 49 (2013), 331–338.
34. Russell, D.W., Fifty years of advances in bile acid synthesis and metabolism. J. Lipid Res. 50:Suppl (2009), S120–S125.
35. Schaap, F.G., Trauner, M., Jansen, P.L., Bile acid receptors as targets for drug development. Nat. Rev. Gastroenterol. Hepatol. 11 (2014), 55–67.
36. Schroder, K., Zhou, R., Tschopp, J., The NLRP3 inflammasome: a sensor for metabolic danger?. Science 327 (2010), 296–300.
37. Sokolowska, M., Chen, L.Y., Liu, Y., Martinez-Anton, A., Qi, H.Y., Logun, C., Alsaaty, S., Park, Y.H., Kastner, D.L., Chae, J.J., Shelhamer, J.H., Prostaglandin E2 Inhibits NLRP3 Inflammasome Activation through EP4 Receptor and Intracellular Cyclic AMP in Human Macrophages. J. Immunol. 194 (2015), 5472–5487.
38. Songyang, Z., Blechner, S., Hoagland, N., Hoekstra, M.F., Piwnica-Worms, H., Cantley, L.C., Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4 (1994), 973–982.
39. Stienstra, R., van Diepen, J.A., Tack, C.J., Zaki, M.H., van de Veerdonk, F.L., Perera, D., Neale, G.A., Hooiveld, G.J., Hijmans, A., Vroegrijk, I., et al. Inflammasome is a central player in the induction of obesity and insulin resistance. Proc. Natl. Acad. Sci. USA 108 (2011), 15324–15329.
40. Strowig, T., Henao-Mejia, J., Elinav, E., Flavell, R., Inflammasomes in health and disease. Nature 481 (2012), 278–286.
41. Thomas, C., Pellicciari, R., Pruzanski, M., Auwerx, J., Schoonjans, K., Targeting bile-acid signalling for metabolic diseases. Nat. Rev. Drug Discov. 7 (2008), 678–693.
42. Thomas, C., Gioiello, A., Noriega, L., Strehle, A., Oury, J., Rizzo, G., Macchiarulo, A., Yamamoto, H., Mataki, C., Pruzanski, M., et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 10 (2009), 167–177.
43. Vandanmagsar, B., Youm, Y.H., Ravussin, A., Galgani, J.E., Stadler, K., Mynatt, R.L., Ravussin, E., Stephens, J.M., Dixit, V.D., The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17 (2011), 179–188.
44. Wang, Y.D., Chen, W.D., Yu, D., Forman, B.M., Huang, W., The G-protein-coupled bile acid receptor, Gpbar1 (TGR5), negatively regulates hepatic inflammatory response through antagonizing nuclear factor κ light-chain enhancer of activated B cells (NF-κB) in mice. Hepatology 54 (2011), 1421–1432.
45. Watanabe, M., Houten, S.M., Wang, L., Moschetta, A., Mangelsdorf, D.J., Heyman, R.A., Moore, D.D., Auwerx, J., Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J. Clin. Invest. 113 (2004), 1408–1418.
46. Watanabe, M., Houten, S.M., Mataki, C., Christoffolete, M.A., Kim, B.W., Sato, H., Messaddeq, N., Harney, J.W., Ezaki, O., Kodama, T., et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439 (2006), 484–489.
47. Wen, H., Gris, D., Lei, Y., Jha, S., Zhang, L., Huang, M.T., Brickey, W.J., Ting, J.P., Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 12 (2011), 408–415.
48. Yan, Y., Jiang, W., Liu, L., Wang, X., Ding, C., Tian, Z., Zhou, R., Dopamine controls systemic inflammation through inhibition of NLRP3 inflammasome. Cell 160 (2015), 62–73.
49. Yu, J.W., Wu, J., Zhang, Z., Datta, P., Ibrahimi, I., Taniguchi, S., Sagara, J., Fernandes-Alnemri, T., Alnemri, E.S., Cryopyrin and pyrin activate caspase-1, but not NF-kappaB, via ASC oligomerization. Cell Death Differ. 13 (2006), 236–249.
50. Zhou, R., Yazdi, A.S., Menu, P., Tschopp, J., A role for mitochondria in NLRP3 inflammasome activation. Nature 469 (2011), 221–225.