Inflammatory Milieu Related to Dysbiotic Gut Microbiota Promotes Tumorigenesis of Hepatocellular Carcinoma.
Journal
Journal of clinical gastroenterology
ISSN: 1539-2031
Titre abrégé: J Clin Gastroenterol
Pays: United States
ID NLM: 7910017
Informations de publication
Date de publication:
01 09 2023
01 09 2023
Historique:
medline:
16
8
2023
pubmed:
5
7
2023
entrez:
5
7
2023
Statut:
epublish
Résumé
Hepatocellular carcinoma (HCC) is an invasive primary liver cancer caused by multiple pathogenic factors and is a significant global health concern. With few effective therapeutic options, HCC is a heterogeneous carcinoma that typically arises in an inflammatory environment. Recent studies have suggested that dysbiotic gut microbiota is involved in hepatocarcinogenesis via multiple mechanisms. In this review, we discuss the effects of gut microbiota, microbial components, and microbiota-derived metabolites on the promotion and progression of HCC by feeding a persistent inflammatory milieu. In addition, we discuss the potential therapeutic modalities for HCC targeting the inflammatory status induced by gut microbiota. A better understanding of the correlation between the inflammatory milieu and gut microbiota in HCC may be beneficial for developing new therapeutic strategies and managing the disease.
Identifiants
pubmed: 37406184
doi: 10.1097/MCG.0000000000001883
pii: 00004836-202309000-00006
doi:
Types de publication
Review
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
782-788Informations de copyright
Copyright © 2023 Wolters Kluwer Health, Inc. All rights reserved.
Références
Yang JD, Hainaut P, Gores GJ, et al. A global view of hepatocellular carcinoma: trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol. 2019;16:589–604.
Ferlay J, Colombet M, Soerjomataram I, et al. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 2019;144:1941–1953.
European Association for the Study of the Liver. Electronic address: easloffice@easloffice.eu; European Association for the Study of the Liver. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol. 2018;69:182–236.
Kulik L, El-Serag HB. Epidemiology and management of hepatocellular carcinoma. Gastroenterology. 2019;156:477–491.
Caines A, Selim R, Salgia R. The changing global epidemiology of hepatocellular carcinoma. Clin Liver Dis. 2020;24:535–547.
Schneider KM, Mohs A, Gui W, et al. Imbalanced gut microbiota fuels hepatocellular carcinoma development by shaping the hepatic inflammatory microenvironment. Nat Commun. 2022;13:3964.
Behary J, Amorim N, Jiang XT, et al. Gut microbiota impact on the peripheral immune response in non-alcoholic fatty liver disease related hepatocellular carcinoma. Nat Commun. 2021;12:187.
Dong TS, Jacobs JP, Agopian V, et al. Duodenal microbiome and serum metabolites predict hepatocellular carcinoma in a multicenter cohort of patients with cirrhosis. Dig Dis Sci. 2022;67:3831–3841.
Ponziani FR, Zocco MA, Cerrito L, et al. Bacterial translocation in patients with liver cirrhosis: physiology, clinical consequences, and practical implications. Expert Rev Gastroenterol Hepatol. 2018;12:641–656.
Guo Y, Kitamoto S, Kamada N. Microbial adaptation to the healthy and inflamed gut environments. Gut Microbes. 2020;12:1857505.
Huang H, Ren Z, Gao X, et al. Integrated analysis of microbiome and host transcriptome reveals correlations between gut microbiota and clinical outcomes in HBV-related hepatocellular carcinoma. Genome Med. 2020;12:102.
Zhang W, Li J, Lu S, et al. Gut microbiota community characteristics and disease-related microorganism pattern in a population of healthy Chinese people. Sci Rep. 2019;9:1594.
Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013;13:800–812.
Jones RM, Neish AS. Gut microbiota in intestinal and liver disease. Annu Rev Pathol. 2021;16:251–275.
Deng T, Li J, He B, et al. Gut microbiome alteration as a diagnostic tool and associated with inflammatory response marker in primary liver cancer. Hepatol Int. 2022;16:99–111.
Tripathi A, Debelius J, Brenner DA, et al. The gut-liver axis and the intersection with the microbiome. Nat Rev Gastroenterol Hepatol. 2018;15:397–411.
Albillos A, de Gottardi A, Rescigno M. The gut-liver axis in liver disease: pathophysiological basis for therapy. J Hepatol. 2020;72:558–577.
Man SM. Inflammasomes in the gastrointestinal tract: infection, cancer and gut microbiota homeostasis. Nat Rev Gastroenterol Hepatol. 2018;15:721–737.
Bhatt AP, Redinbo MR, Bultman SJ. The role of the microbiome in cancer development and therapy. CA Cancer J Clin. 2017;67:326–344.
Thilakarathna WPDW, Rupasinghe HPV, Ridgway ND. Mechanisms by which probiotic bacteria attenuate the risk of hepatocellular carcinoma. Int J Mol Sci. 2021;22:2606.
Suk KT, Kim DJ. Gut microbiota: novel therapeutic target for nonalcoholic fatty liver disease. Expert Rev Gastroenterol Hepatol. 2019;13:193–204.
Martín-Mateos R, Albillos A. The role of the gut-liver axis in metabolic dysfunction-associated fatty liver disease. Front Immunol. 2021;12:660179.
Seki E, De Minicis S, Osterreicher CH, et al. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med. 2007;13:1324–1332.
Isayama F, Hines IN, Kremer M, et al. LPS signaling enhances hepatic fibrogenesis caused by experimental cholestasis in mice. Am J Physiol Gastrointest Liver Physiol. 2006;290:G1318–G1328.
Gäbele E, Mühlbauer M, Dorn C, et al. Role of TLR9 in hepatic stellate cells and experimental liver fibrosis. Biochem Biophys Res Commun. 2008;376:271–276.
Hartmann P, Haimerl M, Mazagova M, et al. Toll-like receptor 2-mediated intestinal injury and enteric tumor necrosis factor receptor I contribute to liver fibrosis in mice. Gastroenterology. 2012;143:1330–1340.
Seki E, Schnabl B. Role of innate immunity and the microbiota in liver fibrosis: crosstalk between the liver and gut. J Physiol. 2012;590:447–458.
Lebeaupin C, Proics E, de Bieville CH, et al. ER stress induces NLRP3 inflammasome activation and hepatocyte death. Cell Death Dis. 2015;6:e1879.
Yoshimoto S, Loo TM, Atarashi K, et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature. 2013;499:97–101.
Lee PC, Wu CJ, Hung YW, et al. Gut microbiota and metabolites associate with outcomes of immune checkpoint inhibitor-treated unresectable hepatocellular carcinoma. J Immunother Cancer. 2022;10:e004779.
Sehgal R, Bedi O, Trehanpati N. Role of microbiota in pathogenesis and management of viral hepatitis. Front Cell Infect Microbiol. 2020;10:341.
Larsen JM. The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology. 2017;151:363–374.
Farazi PA, DePinho RA. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer. 2006;6:674–687.
Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140:805–820.
Chen YH, Wu WK, Wu MS. Microbiota-associated therapy for non-alcoholic steatohepatitis-induced liver cancer: a review. Int J Mol Sci. 2020;21:5999.
Luu M, Pautz S, Kohl V, et al. The short-chain fatty acid pentanoate suppresses autoimmunity by modulating the metabolic-epigenetic crosstalk in lymphocytes. Nat Commun. 2019;10:760.
Canfora EE, Meex RCR, Venema K, et al. Gut microbial metabolites in obesity, NAFLD and T2DM. Nat Rev Endocrinol. 2019;15:261–273.
Bloom PP, Tapper EB, Young VB, et al. Microbiome therapeutics for hepatic encephalopathy. J Hepatol. 2021;75:1452–1464.
Yang W, Yu T, Huang X, et al. Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity. Nat Commun. 2020 Sep 8;11:4457.
Furusawa Y, Obata Y, Fukuda S, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446–450.
Fernandes AD, Reid JN, Macklaim JM, et al. Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome. 2014;2:15.
Sheng L, Jena PK, Hu Y, et al. Hepatic inflammation caused by dysregulated bile acid synthesis is reversible by butyrate supplementation. J Pathol. 2017;243:431–441.
Ren Z, Li A, Jiang J, et al. Gut microbiome analysis as a tool towards targeted non-invasive biomarkers for early hepatocellular carcinoma. Gut. 2019;68:1014–1023.
Belcheva A, Irrazabal T, Robertson SJ, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell. 2014;158:288–299.
Kaiko GE, Ryu SH, Koues OI, et al. The colonic crypt protects stem cells from microbiota-derived metabolites. Cell. 2016;165:1708–1720.
Kim MH, Kang SG, Park JH, et al. Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology. 2013;145:396–406.
Ponziani FR, Nicoletti A, Gasbarrini A, et al. Diagnostic and therapeutic potential of the gut microbiota in patients with early hepatocellular carcinoma. Ther Adv Med Oncol. 2019;11:1758835919848184.
Singh V, Yeoh BS, Chassaing B, et al. Dysregulated microbial fermentation of soluble fiber induces cholestatic liver cancer. Cell. 2018;175:679–694.
Gallage S, Kotsiliti E, Heikenwalder M. When soluble fibers meet hepatocellular carcinoma: the sark side of fermentation. Cell Metab. 2018;28:673–675.
Chiang JYL, Ferrell JM. Bile acid metabolism in liver pathobiology. Gene Expr. 2018;18:71–87.
Jia B, Jeon CO. Promotion and induction of liver cancer by gut microbiome-mediated modulation of bile acids. PLoS Pathog. 2019;15:e1007954.
Sydor S, Best J, Messerschmidt I, et al. Altered microbiota diversity and bile acid signaling in cirrhotic and noncirrhotic NASH-HCC. Clin Transl Gastroenterol. 2020;11:e00131.
Fouts DE, Torralba M, Nelson KE, et al. Bacterial translocation and changes in the intestinal microbiome in mouse models of liver disease. J Hepatol. 2012;56:1283–1292.
Schaap FG, Trauner M, Jansen PL. Bile acid receptors as targets for drug development. Nat Rev Gastroenterol Hepatol. 2014;11:55–67.
Zhang Y, Ge X, Heemstra LA, et al. Loss of FXR protects against diet-induced obesity and accelerates liver carcinogenesis in ob/ob mice. Mol Endocrinol. 2012;26:272–280.
Takahashi S, Tanaka N, Fukami T, et al. Role of farnesoid X receptor and bile acids in hepatic tumor development. Hepatol Commun. 2018;2:1567–1582.
Degirolamo C, Modica S, Vacca M, et al. Prevention of spontaneous hepatocarcinogenesis in farnesoid X receptor-null mice by intestinal-specific farnesoid X receptor reactivation. Hepatology. 2015;61:161–170.
Zarrinpar A, Loomba R. Review article: the emerging interplay among the gastrointestinal tract, bile acids and incretins in the pathogenesis of diabetes and non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2012;36:909–921.
Cui G, Martin RC, Jin H, et al. Up-regulation of FGF15/19 signaling promotes hepatocellular carcinoma in the background of fatty liver. J Exp Clin Cancer Res. 2018;37:136.
Han CY. Update on FXR biology: promising therapeutic target? Int J Mol Sci. 2018;19:2069.
Ma C, Han M, Heinrich B, et al. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science. 2018;360:eaan5931.
Demaria M, O’Leary MN, Chang J, et al. Cellular senescence promotes adverse effects of chemotherapy and cancer relapse. Cancer Discov. 2017;7:165–176.
Loo TM, Kamachi F, Watanabe Y, et al. Gut microbiota promotes obesity-associated liver cancer through PGE 2 -mediated suppression of antitumor immunity. Cancer Discov. 2017;7:522–538.
Hartmann P, Seebauer CT, Schnabl B. Alcoholic liver disease: the gut microbiome and liver cross talk. Alcohol Clin Exp Res. 2015;39:763–775.
Bayoumy AB, Mulder CJJ, Mol JJ, et al. Gut fermentation syndrome: a systematic review of case reports. United European Gastroenterol J. 2021;9:332–342.
Eslam M, Newsome PN, Sarin SK, et al. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol. 2020;73:202–209.
Younossi Z, Anstee QM, Marietti M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15:11–20.
Yuan J, Chen C, Cui J, et al. Fatty liver disease caused by high-alcohol-producing Klebsiella pneumoniae . Cell Metab. 2019;30:675–688.
Ghoshal UC, Goel A, Quigley EMM. Gut microbiota abnormalities, small intestinal bacterial overgrowth, and non-alcoholic fatty liver disease: an emerging paradigm. Indian J Gastroenterol. 2020;39:9–21.
Chen X, Zhang Z, Li H, et al. Endogenous ethanol produced by intestinal bacteria induces mitochondrial dysfunction in non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2020;35:2009–2019.
Banales JM, Iñarrairaegui M, Arbelaiz A, et al. Serum metabolites as diagnostic biomarkers for cholangiocarcinoma, hepatocellular carcinoma, and primary sclerosing cholangitis. Hepatology. 2019;70:547–562.
Temraz S, Nassar F, Kreidieh F, et al. Hepatocellular carcinoma immunotherapy and the potential influence of gut microbiome. Int J Mol Sci. 2021;22:7800.
Li J, Sung CY, Lee N, et al. Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice. Proc Natl Acad Sci USA. 2016;113:E1306–E1315.
Janssen AWF, Houben T, Katiraei S, et al. Modulation of the gut microbiota impacts nonalcoholic fatty liver disease: a potential role for bile acids. J Lipid Res. 2017;58:1399–1416.
Safari Z, Gérard P. The links between the gut microbiome and non-alcoholic fatty liver disease (NAFLD). Cell Mol Life Sci. 2019;76:1541–1558.
Gupta A, Khanna S. Fecal microbiota transplantation. JAMA. 2017;318:102.
Bibbò S, Ianiro G, Gasbarrini A, et al. Fecal microbiota transplantation: past, present and future perspectives. Minerva Gastroenterol Dietol. 2017;63:420–430.