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Research Paper

Gut microbial bile acid metabolite skews macrophage polarization and contributes to high-fat diet-induced colonic inflammation

Lingyu Wanga Department of Pediatric Surgery, Xinhua Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China;b Department of Gastroenterology and Nutrition, Shanghai Institute for Pediatric Research, School of Medicine, Shanghai Jiaotong University, Shanghai, China;c Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, ChinaView further author information
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Zizhen Gonga Department of Pediatric Surgery, Xinhua Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China;b Department of Gastroenterology and Nutrition, Shanghai Institute for Pediatric Research, School of Medicine, Shanghai Jiaotong University, Shanghai, China;c Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, ChinaView further author information
,
Xiuyuan Zhangd State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences(Beijing), Beijing Institute of Lifeomics, Beijing, ChinaView further author information
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Fangxinxing Zhua Department of Pediatric Surgery, Xinhua Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China;b Department of Gastroenterology and Nutrition, Shanghai Institute for Pediatric Research, School of Medicine, Shanghai Jiaotong University, Shanghai, China;c Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, ChinaView further author information
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Yuchen Liud State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences(Beijing), Beijing Institute of Lifeomics, Beijing, ChinaView further author information
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Chaozhi Jind State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences(Beijing), Beijing Institute of Lifeomics, Beijing, ChinaView further author information
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Xixi Dua Department of Pediatric Surgery, Xinhua Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China;b Department of Gastroenterology and Nutrition, Shanghai Institute for Pediatric Research, School of Medicine, Shanghai Jiaotong University, Shanghai, China;c Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, ChinaView further author information
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Congfeng Xue Department of Cardiology, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, China;f Department of Immunology, Shanghai Institute of Immunology, Shanghai Jiaotong University School of Medicine, Shanghai, ChinaORCID Iconhttps://orcid.org/0000-0002-8009-4865View further author information
ORCID Icon,
Yingwei Chenb Department of Gastroenterology and Nutrition, Shanghai Institute for Pediatric Research, School of Medicine, Shanghai Jiaotong University, Shanghai, China;c Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, ChinaView further author information
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Wei Caia Department of Pediatric Surgery, Xinhua Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China;b Department of Gastroenterology and Nutrition, Shanghai Institute for Pediatric Research, School of Medicine, Shanghai Jiaotong University, Shanghai, China;c Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, ChinaCorrespondence[email protected]
View further author information
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Chunyan Tiand State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences(Beijing), Beijing Institute of Lifeomics, Beijing, ChinaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0003-1589-293XView further author information
ORCID Icon &
Jin Wua Department of Pediatric Surgery, Xinhua Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China;b Department of Gastroenterology and Nutrition, Shanghai Institute for Pediatric Research, School of Medicine, Shanghai Jiaotong University, Shanghai, China;c Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, ChinaCorrespondence[email protected]
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Article: 1819155 | Received 29 Nov 2019, Accepted 21 Aug 2020, Published online: 02 Oct 2020

References

  • Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: A systematic review of the literature. Am J Gastroenterol. 2011;106(4):563–573. doi:10.1038/ajg.2011.44. PMID: 21468064.
  • Duan Y, Zeng L, Zheng C, Song B, Li F, Kong X, Xu K. Inflammatory links between high fat diets and diseases. Front Immunol. 2018;9:2649. doi:10.3389/fimmu.2018.02649. PMID: 30483273.
  • Antonioli L, Caputi V, Fornai M, Pellegrini C, Gentile D, Giron MC, Orso G, Bernardini N, Segnani C, Ippolito C, et al. Interplay between colonic inflammation and tachykininergic pathways in the onset of colonic dysmotility in a mouse model of diet-induced obesity. Int J Obes (Lond). 2019;43(2):331–343. doi:10.1038/s41366-018-0166-2. PMID: 30082748.
  • Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142(1):46–54. e42;quiz e30. doi:10.1053/j.gastro.2011.10.001. PMID: 22001864.
  • Paik J, Fierce Y, Treuting PM, Brabb T, Maggio-Price L. High-fat diet-induced obesity exacerbates inflammatory bowel disease in genetically susceptible mdr1a-/- male mice. J Nutr. 2013;143:1240–1247. doi:10.3945/jn.113.174615. PMID: 23761644.
  • Maslowski KM, Mackay CR. Diet, gut microbiota and immune responses. Nat Immunol. 2011;12:5–9. doi:10.1038/ni0111-5. PMID: 21169997.
  • Bernstein H, Holubec H, Bernstein C, Ignatenko N, Gerner E, Dvorak K, Besselsen D, Ramsey L, Dall’Agnol M, Blohm-Mangone KA, et al. Unique dietary-related mouse model of colitis. Inflamm Bowel Dis. 2006;12:278–293. 10.1097/01.MIB.0000209789.14114.63. PMID: 16633050.
  • Richman E, Rhodes JM. Review article: evidence-based dietary advice for patients with inflammatory bowel disease. Aliment Pharmacol Ther PMID: 24102340. 2013;38:1156–1171. doi:10.1111/apt.12500.
  • Kawano Y, Nakae J, Watanabe N, Kikuchi T, Tateya S, Tamori Y, Kaneko M, Abe T, Onodera M, Itoh H. Colonic pro-inflammatory macrophages cause insulin resistance in an intestinal Ccl2/Ccr2-dependent manner. Cell Metab. 2016;24:295–310. doi:10.1016/j.cmet.2016.07.009. PMID: 27508875.
  • Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41(1):14–20. doi:10.1016/j.immuni.2014.06.008. PMID: 25035950.
  • Italiani P, Boraschi D. From monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation. Front Immunol. 2014;5:514. doi:10.3389/fimmu.2014.00514. PMID: 25368618.
  • Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11:723–737. doi:10.1038/nri3073. PMID: 21997792.
  • Zhu Y, Zhou J, Feng Y, Chen L, Zhang L, Yang F, Zha H, Wang X, Han X, Shu C, et al. Control of intestinal inflammation, colitis-associated tumorigenesis, and macrophage polarization by fibrinogen-like protein 2. Front Immunol. 2018;9:87. doi:10.3389/fimmu.2018.00087. PMID: 29441068
  • Lin Y, Yang X, Yue W, Xu X, Li B, Zou L, He R. Chemerin aggravates DSS-induced colitis by suppressing M2 macrophage polarization. Cell Mol Immunol. 2014;11(4):355–366. doi:10.1038/cmi.2014.15. PMID: 24727542.
  • Hunter MM, Wang A, Parhar KS, Johnston MJG, van Rooijen N, Beck PL, McKay DM. In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology. 2010;138(4):1395–1405. doi:10.1053/j.gastro.2009.12.041. PMID: 20044996.
  • Yang Y-F, Zhou Y-D, Hu J-C, Luo F-L, Xie Y, Shen Y-Y, Bian W-X, Yin Z-N, Li H-L, Zhang X-L. Ficolin-A/2, acting as a new regulator of macrophage polarization, mediates the inflammatory response in experimental mouse colitis. Immunology. 2017;151:433–450. doi:10.1111/imm.12741. PMID: 28380665.
  • Li C, Xu MM, Wang K, Adler AJ, Vella AT, Zhou B. Macrophage polarization and meta-inflammation. Transl Res. 2018;191:29–44. doi:10.1016/j.trsl.2017.10.004. PMID: 29154757.
  • Ler D, Schumann M, Batra A, Kredel L-I, Kühl AA, Erben U, May C, Schulzke J-D, Siegmund B. Monocyte and M1 macrophage-induced marrier defect contributes to chronic intestinal inflammation in IBD. Inflamm Bowel Dis. 2015;21:1297–1305. doi:10.1097/MIB.0000000000000384. PMID: 25901973.
  • Levy M, Thaiss CA, Elinav E. Metabolites: messengers between the microbiota and the immune system. Genes Dev. 2016;30(14):1589–1597. doi:10.1101/gad.284091.116. PMID: 27474437.
  • Shapiro H, Thaiss CA, Levy M, Elinav E. The cross talk between microbiota and the immune system: metabolites take center stage. Curr Opin Immunol. 2014;30:54–62. doi:10.1016/j.coi.2014.07.003. PMID: 25064714.
  • O’Hara AM, Shanahan F. Gut microbiota: mining for therapeutic potential. Clin Gastroenterol Hepatol. 2007;5(3):274–284. doi:10.1016/j.cgh.2006.12.009. PMID: 17368226.
  • Stenman LK, Holma R, Forsgård R, Gylling H, Korpela R. Higher fecal bile acid hydrophobicity is associated with exacerbation of dextran sodium sulfate colitis in mice. J Nutr. 2013;143(11):1691–1697. doi:10.3945/jn.113.180810. PMID: 24047703.
  • Payne CM, Weber C, Crowley-Skillicorn C, Dvorak K, Bernstein H, Bernstein C, Holubec H, Dvorakova B, Garewal H. Deoxycholate induces mitochondrial oxidative stress and activates NF-kappaB through multiple mechanisms in HCT-116 colon epithelial cells. Carcinogenesis. 2007;28(1):215–222. doi:10.1093/carcin/bgl139. PMID: 16887864.
  • Nagathihalli NS, Beesetty Y, Lee W, Washington MK, Chen X, Lockhart AC, Merchant NB. Novel mechanistic insights into ectodomain shedding of EGFR ligands amphiregulin and TGF-α: impact on gastrointestinal cancers driven by secondary bile acids. Cancer Res. 2014;74(7):2062–2072. doi:10.1158/0008-5472.CAN-13-2329. PMID: 24520077.
  • Ridlon JM, Kang D-J, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res. 2006;47(2):241–259. doi:10.1194/jlr.R500013-JLR200. PMID: 16299351.
  • Stenman LK, Holma R, Korpela R. High-fat-induced intestinal permeability dysfunction associated with altered fecal bile acids. World J Gastroenterol. 2012;18(9):923–929. doi:10.3748/wjg.v18.i9.923. PMID: 22408351.
  • Schaap FG, Trauner M, Jansen PLM. Bile acid receptors as targets for drug development. Nat Rev Gastroenterol Hepatol. 2014;11:55–67. doi:10.1038/nrgastro.2013.151. PMID: 23982684.
  • Zhou H, Hylemon PB. Bile acids are nutrient signaling hormones. Steroids. 2014;86:62–68. doi:10.1016/j.steroids.2014.04.016. PMID: 24819989.
  • Arbibe L, Mira JP, Teusch N, Kline L, Guha M, Mackman N, Godowski PJ, Ulevitch RJ, Knaus UG. Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway. Nat Immunol. 2000;1(6):533–540. doi:10.1038/82797. PMID: 11101877.
  • Cheng K, Raufman J-P. Bile acid-induced proliferation of a human colon cancer cell line is mediated by transactivation of epidermal growth factor receptors. Biochem Pharmacol. 2005;70:1035–1047. doi:10.1016/j.bcp.2005.07.023. PMID: 16139803.
  • Chun J, Prince A. Activation of C2+dependent signaling by TLR2+. J Immunol. 2006;177(2):1330–1337. doi:10.4049/jimmunol.177.2.1330. PMID: 16818794.
  • Kim HG, Kim JY, Gim MG, Lee JM, Chung DK. Mechanical stress induces tumor necrosis factor-{Alpha} production through Ca2+ release-dependent TLR2 signaling. Am J Physiol Cell Physiol. 2008;295(2):C432–9. doi:10.1152/ajpcell.00085. PMID: 18550705.
  • Jin XC, Morsy N, Shoeb F, Zavzavadjian J, Akbarali H. Coupling of M2 muscarinic receptor to L-type Ca channel via C-src kinase in rabbit colonic circular smooth muscle. Gastroenterology. 2002;123(3):827–834. doi:10.1053/gast.2002.35388. PMID: 12198709.
  • Chen ML, Takeda K, Sundrud MS. Emerging roles of bile acids in mucosal immunity and inflammation. Mucosal Immunol. 2019;12:851–861. doi:10.1038/s41385-019-0162-4. PMID: 30952999.
  • Hofmann AF, Hagey LR. Key discoveries in bile acid chemistry and biology and their clinical applications: history of the last eight decades. J Lipid Res. 2014;55:1553–1595. doi:10.1194/jlr.R049437. PMID: 24838141.
  • Pavlidis P, Powell N, Vincent RP, Ehrlich D, Bjarnason I, Hayee B. Systematic review: bile acids and intestinal inflammation-luminal aggressors or regulators of mucosal defence? Aliment Pharmacol Ther. 2015;42(7):802–817. doi:10.1111/apt.13333. PMID: 26223936.
  • Kadir SHSA, Miragoli M, Abu-Hayyeh S, Moshkov AV, Xie Q, Keitel V, VO N, Williamson C, Gorelik J. Bile acid-induced arrhythmia is mediated by muscarinic M2 receptors in neonatal rat cardiomyocytes. PLoS ONE. 2010;5(3):e9689. doi:10.1371/journal.pone.0009689. PMID: 20300620.
  • Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol. 2005;17(1):1–14. doi:10.1093/intimm/dxh186. PMID: 15585605.
  • Platt AM, Bain CC, Bordon Y, Sester DP, Mowat AM. An independent subset of TLR expressing CCR2-dependent macrophages promotes colonic inflammation. J Immunol. 2010;184(12):6843–6854. doi:10.4049/jimmunol.0903987. PMID: 20483766.
  • Yasuda H, Hirata S, Inoue K, Mashima H, Ohnishi H, Yoshiba M. Involvement of membrane-type bile acid receptor M-BAR/TGR5 in bile acid-induced activation of epidermal growth factor receptor and mitogen-activated protein kinases in gastric carcinoma cells. Biochem Biophys Res Commun. 2007;354(1):154–159. doi:10.1016/j.bbrc.2006.12.168. PMID: 17214962.
  • Zhao S, Gong Z, Zhou J, Tian C, Gao Y, Xu C, Chen Y, Cai W, Wu J. Deoxycholic acid triggers NLRP3 inflammasome activation and aggravates DSS-induced colitis in mice. Front Immunol. 2016;7:536. doi:10.3389/fimmu.2016.00536. PMID: 27965665.
  • Wang J, Li R, Peng Z, Hu B, Rao X, Li J. HMGB1 participates in LPS-induced acute lung injury by activating the AIM2 inflammasome in macrophages and inducing polarization of M1 macrophages via TLR2, TLR4, and RAGE/NF-κB signaling pathways. Int J Mol Med. 2020;45(1):61–80. doi:10.3892/ijmm.2019.4402. PMID: 31746367.
  • Awad F, Assrawi E, Jumeau C, Georgin-Lavialle S, Cobret L, Duquesnoy P, Piterboth W, Thomas L, Stankovic-Stojanovic K, Louvrier C, et al. Impact of human monocyte and macrophage polarization on NLR expression and NLRP3 inflammasome activation. PLoS One. 2017;12(4):e0175336. doi:10.1371/journal.pone.0175336. PMID: 28403163.
  • Edelstein A, Fink D, Musch M, Valuckaite V, Zaborina O, Grubjesic S, Firestone M, Matthews J, Alverdy J. Protective effects of nonionic triblock copolymers on bile acid-mediated epithelial barrier disruption. Shock. 2011;36(5):451–457. doi:10.1097/SHK.0b013e31822d8de1. PMID: 21937955.
  • Breuer NF, Rampton DS, Tammar A, Murphy GM, Dowling RH. Effect of colonic perfusion with sulfated and nonsulfated bile acids on mucosal structure and function in the rat. Gastroenterology. 1983;84(5):969–977. doi:10.1016/0016-5085(83)90199-3. PMID: 6299874.
  • Henrikson CK, Argenzio RA, Liacos JA, Khosla J. Morphologic and functional effects of bile salt on the porcine colon during injury and repair. Lab Invest. 1989;60(1):72–87. PMID: 2492061.
  • Sun Y, Fihn BM, Sjövall H, Jodal M. Enteric neurones modulate the colonic permeability response to luminal bile acids in rat colon in vivo. Gut. 2004;53(3):362–367. doi:10.1136/gut.2003.015867. PMID: 14960516.
  • Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, Taupin D, Thornton DJ, Png CW, Crockford TL, Cornall RJ, et al. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med. 2008;5(3):e54. doi:10.1371/journal.pmed.0050054. PMID: 18318598.
  • Zhang W-J, Wei H, Hagen T, Frei B. Alpha-lipoic acid attenuates LPS-induced inflammatory responses by activating the phosphoinositide 3-kinase/Akt signaling pathway. Proc Natl Acad Sci U S A. 2007;104:4077–4082. doi:10.1073/pnas.0700305104. PMID: 17360480.
  • Liu D, Chang C, Lu N, Wang X, Lu Q, Ren X, Ren P, Zhao D, Wang L, Zhu Y, et al. Comprehensive proteomics analysis reveals metabolic reprogramming of tumor-associated macrophages stimulated by the tumor microenvironment. J Proteome Res. 2017;16:288–297. doi:10.1021/acs.jproteome.6b00604. PMID: 27809537.

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