Gut microbiota-derived indole compounds attenuate metabolic dysfunction-associated steatotic liver disease by improving fat metabolism and inflammation

References

• Friedman SL, Neuschwander-Tetri BA, Rinella M, Sanyal AJ. Mechanisms of NAFLD development and therapeutic strategies. Nat Med. 2018;24(7):908–22. doi:10.1038/s41591-018-0104-9.
   PubMed Web of Science ®Google Scholar
• Kawaguchi T, Tsutsumi T, Nakano D, Eslam M, George J, Torimura T. MAFLD enhances clinical practice for liver disease in the Asia-Pacific region. Clin Mol Hepatol. 2022;28(2):150–163. doi:10.3350/cmh.2021.0310.
   PubMed Web of Science ®Google Scholar
• Fukunaga S, Mukasa M, Nakano D, Tsutsumi T, Kawaguchi T. Changing from NAFLD to MASLD: similar cumulative incidence of reflux esophagitis between NAFLD and MASLD. Clin Mol Hepatol. 2024;30(1):121–123. doi:10.3350/cmh.2023.0437.
   PubMedGoogle Scholar
• Parry SA, Hodson L. Influence of dietary macronutrients on liver fat accumulation and metabolism. J Invest Med. 2017;65(8):1102–15. doi:10.1136/jim-2017-000524.
   PubMed Web of Science ®Google Scholar
• Blandino G, Inturri R, Lazzara F, Di Rosa M, Malaguarnera L. Impact of gut microbiota on diabetes mellitus. Diabetes Metab. 2016;42(5):303–15. doi:10.1016/j.diabet.2016.04.004.
   PubMed Web of Science ®Google Scholar
• Buzzetti E, Pinzani M, Tsochatzis EA. The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism. 2016;65(8):1038–48. doi:10.1016/j.metabol.2015.12.012.
   PubMed Web of Science ®Google Scholar
• Valdes AM, Walter J, Segal E, Spector TD. Role of the gut microbiota in nutrition and health. BMJ. 2018:361. doi:10.1136/bmj.k2179.
   Google Scholar
• Koning M, Herrema H, Nieuwdorp M, Meijnikman AS. Targeting nonalcoholic fatty liver disease via gut microbiome-centered therapies. Gut Microbes. 2023;15(1):2226922. doi:10.1080/19490976.2023.2226922.
   PubMed Web of Science ®Google Scholar
• Jennison E, Byrne CD. The role of the gut microbiome and diet in the pathogenesis of non-alcoholic fatty liver disease. Clin Mol Hepatol. 2021;27(1):22–43. doi:10.3350/cmh.2020.0129.
   PubMed Web of Science ®Google Scholar
• Lee NY, Yoon SJ, Han DH, Gupta H, Youn GS, Shin MJ, Ham YL, Kwak MJ, Kim BY, Yu JS. et al. Lactobacillus and pediococcus ameliorate progression of non-alcoholic fatty liver disease through modulation of the gut microbiome. Gut Microbes. 2020;11(4):882–99. doi:10.1080/19490976.2020.1712984.
   PubMed Web of Science ®Google Scholar
• Modoux M, Rolhion N, Mani S, Sokol H. Tryptophan metabolism as a pharmacological target. Trends Pharmacol Sci. 2021;42(1):60–73. doi:10.1016/j.tips.2020.11.006.
   PubMed Web of Science ®Google Scholar
• Gostner JM, Geisler S, Stonig M, Mair L, Sperner-Unterweger B, Fuchs D. Tryptophan metabolism and related pathways in psychoneuroimmunology: the impact of nutrition and lifestyle. Neuropsychobiology. 2020;79(1–2):89–99. doi:10.1159/000496293.
   PubMed Web of Science ®Google Scholar
• Yoon SJ, Yu JS, Min BH, Gupta H, Won SM, Park HJ, Han SH, Kim BY, Kim KH, Kim BK. et al. Bifidobacterium-derived short-chain fatty acids and indole compounds attenuate nonalcoholic fatty liver disease by modulating gut-liver axis. Front Microbiol. 2023;14:1129904. doi:10.3389/fmicb.2023.1129904.
   PubMed Web of Science ®Google Scholar
• Ji Y, Yin Y, Li Z, Zhang W. Gut microbiota-derived components and metabolites in the progression of non-alcoholic fatty liver disease (NAFLD). Nutrients. 2019;11(8):1712. doi:10.3390/nu11081712.
   PubMed Web of Science ®Google Scholar
• Krishnan S, Ding Y, Saedi N, Choi M, Sridharan GV, Sherr DH, Yarmush ML, Alaniz RC, Jayaraman A, Lee K. Gut microbiota-derived tryptophan metabolites modulate inflammatory response in hepatocytes and macrophages. Cell Rep. 2018;23(4):1099–111. doi:10.1016/j.celrep.2018.03.109.
   PubMed Web of Science ®Google Scholar
• Bansal T, Alaniz RC, Wood TK, Jayaraman A. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc Natl Acad Sci USA. 2010;107(1):228–233. doi:10.1073/pnas.0906112107.
   PubMed Web of Science ®Google Scholar
• Cusi K, Younossi Z, Roden M. From NAFLD to MASLD: promise and pitfalls of a new definitiondagger. Hepatology. 2023;19:10–97. doi:10.1016/j.jhep.2023.09.038.
   Google Scholar
• Kim GA, Moon JH, Kim W. Critical appraisal of metabolic dysfunction-associated steatotic liver disease: implication of janus-faced modernity. Clin Mol Hepatol. 2023;29(4):831–43. doi:10.3350/cmh.2023.0277.
   PubMedGoogle Scholar
• Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp‐Arida A. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41(6):1313–21. doi:10.1002/hep.20701.
   PubMed Web of Science ®Google Scholar
• Yu JS, Youn GS, Choi J, Kim CH, Kim BY, Yang SJ, Lee JH, Park TS, Kim BK, Kim YB. Lactobacillus lactis and pediococcus pentosaceus‐driven reprogramming of gut microbiome and metabolome ameliorates the progression of non‐alcoholic fatty liver disease. Clin Transl Med. 2021;11(12):e634. doi:10.1002/ctm2.634.
   PubMed Web of Science ®Google Scholar
• Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67(5):1613–7. doi:10.1099/ijsem.0.001755.
   PubMed Web of Science ®Google Scholar
• Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–1. doi:10.1093/bioinformatics/btq461.
   PubMed Web of Science ®Google Scholar
• Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host & Microbe. 2018;23(6):716–24. doi:10.1016/j.chom.2018.05.003.
   PubMed Web of Science ®Google Scholar
• Roh YS, Seki E. Chemokines and chemokine receptors in the development of NAFLD. Adv Exp Med Biol. 2018;1061:45–53. doi:10.1007/978-981-10-8684-7_4.
   PubMed Web of Science ®Google Scholar
• Koliada A, Syzenko G, Moseiko V, Budovska L, Puchkov K, Perederiy V, Gavalko Y, Dorofeyev A, Romanenko M, Tkach S. et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;17(1):120. doi:10.1186/s12866-017-1027-1.
   PubMed Web of Science ®Google Scholar
• Osawa Y, Kanamori H, Seki E, Hoshi M, Ohtaki H, Yasuda Y, Ito H, Suetsugu A, Nagaki M, Moriwaki H. L-tryptophan-mediated enhancement of susceptibility to nonalcoholic fatty liver disease is dependent on the mammalian target of rapamycin. J Biol Chem. 2011;286(40):34800–8. doi:10.1074/jbc.M111.235473.
   PubMed Web of Science ®Google Scholar
• Leung C, Rivera L, Furness JB, Angus PW. The role of the gut microbiota in NAFLD. Nat Rev Gastroenterol Hepatol. 2016;13(7):412–25. doi:10.1038/nrgastro.2016.85.
   PubMed Web of Science ®Google Scholar
• Sonnenburg JL, Bäckhed F. Diet–microbiota interactions as moderators of human metabolism. Nature. 2016;535(7610):56–64. doi:10.1038/nature18846.
   PubMed Web of Science ®Google Scholar
• Aron-Wisnewsky J, Warmbrunn MV, Nieuwdorp M, Clement K. Nonalcoholic fatty liver disease: modulating gut microbiota to improve severity? Gastroenterology. 2020;158(7):1881–98. doi:10.1053/j.gastro.2020.01.049.
   PubMed Web of Science ®Google Scholar
• Xue L, He J, Gao N, Lu X, Li M, Wu X, Liu Z, Jin Y, Liu J, Xu J. et al. Probiotics may delay the progression of nonalcoholic fatty liver disease by restoring the gut microbiota structure and improving intestinal endotoxemia. Sci Rep. 2017;7(1):45176. doi:10.1038/srep45176.
   PubMedGoogle Scholar
• Lamas B, Natividad JM, Sokol H. Aryl hydrocarbon receptor and intestinal immunity. Mucosal Immunol. 2018;11(4):1024–38. doi:10.1038/s41385-018-0019-2.
   PubMed Web of Science ®Google Scholar
• Qian M, Liu J, Zhao D, Cai P, Pan C, Jia W, Gao Y, Zhang Y, Zhang N, Zhang Y. Aryl hydrocarbon receptor deficiency in intestinal epithelial cells aggravates alcohol-related liver disease. Cell Mol Gastroenterol Hepatol. 2022;13(1):233–56. doi:10.1016/j.jcmgh.2021.08.014.
   PubMed Web of Science ®Google Scholar
• Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, Siuzdak G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci. 2009;106:3698–3703.
   PubMed Web of Science ®Google Scholar
• Reddy JK, Hashimoto T. P Eroxisomal β-oxidation and peroxisome proliferator–activated Receptor α: An Adaptive Metabolic System. Annu Rev Nutr. 2001;21(1):193. doi:10.1146/annurev.nutr.21.1.193.
   PubMedGoogle Scholar
• Rogue A, Lambert C, Jossé R, Antherieu S, Spire C, Claude N, Guillouzo A, Agoulnik I. Comparative gene expression profiles induced by PPARγ and PPARα/γ agonists in human hepatocytes. PloS ONE. 2011;6(4):e18816. doi:10.1371/journal.pone.0018816.
   PubMed Web of Science ®Google Scholar
• Hubbard TD, Murray IA, Perdew GH. Indole and tryptophan metabolism: endogenous and dietary routes to ah receptor activation. Drug Metab Dispos. 2015;43(10):1522–35. doi:10.1124/dmd.115.064246.
   PubMed Web of Science ®Google Scholar
• Imajo K, Fujita K, Yoneda M, Nozaki Y, Ogawa Y, Shinohara Y, Kato S, Mawatari H, Shibata W, Kitani H. Hyperresponsivity to low-dose endotoxin during progression to nonalcoholic steatohepatitis is regulated by leptin-mediated signaling. Cell Metab. 2012;16(1):44–54. doi:10.1016/j.cmet.2012.05.012.
   PubMed Web of Science ®Google Scholar
• Rao R. Endotoxemia and gut barrier dysfunction in alcoholic liver disease. Hepatol. 2009;50(2):638. doi:10.1002/hep.23009.
   PubMed Web of Science ®Google Scholar
• Li M, Sun X, Zhao J, Xia L, Li J, Xu M, Wang B, Guo H, Yu C, Gao Y. et al. CCL5 deficiency promotes liver repair by improving inflammation resolution and liver regeneration through M2 macrophage polarization. Cell Mol Immunol. 2020;17(7):753–64. doi:10.1038/s41423-019-0279-0.
   PubMed Web of Science ®Google Scholar
• Hwang D, Jang BC, Yu G, Boudreau M. Expression of mitogen-inducible cyclooxygenase induced by lipopolysaccharide: mediation through both mitogen-activated protein kinase and NF-kappaB signaling pathways in macrophages. Biochem Pharmacol. 1997;54(1):87–96. doi:10.1016/s0006-2952(97)00154-8.
   PubMed Web of Science ®Google Scholar
• Yeh ML, Yu ML. From nonalcoholic steatohepatitis, metabolic dysfunction-associated fatty liver disease, to steatotic liver disease: updates of nomenclature and impact on clinical trials. Clin Mol Hepatol. 2023;29(4):969–72. doi:10.3350/cmh.2023.0359.
   PubMedGoogle Scholar
• Chi Y, Wu Z, Du C, Zhang M, Wang X, Xie A, Wang P, Li R. Regulatory effects mediated by ulvan oligosaccharide and its zinc complex on lipid metabolism in high-fat diet-fed mice. Carbohydr Polym. 2023;300:120249. doi:10.1016/j.carbpol.2022.120249.
   PubMed Web of Science ®Google Scholar
• Safari Z, Gérard P. The links between the gut microbiome and non-alcoholic fatty liver disease (NAFLD). Cell Mol Life Sci. 2019;76(8):1541–58. doi:10.1007/s00018-019-03011-w.
   PubMed Web of Science ®Google Scholar
• Gupta H, Min B-H, Ganesan R, Gebru YA, Sharma SP, Park E, Won S-M, Jeong J-J, Lee S-B, Cha M-G. Gut microbiome in non-alcoholic fatty liver disease: from mechanisms to therapeutic role. Biomedicines. 2022;10(3):550. doi:10.3390/biomedicines10030550.
   PubMed Web of Science ®Google Scholar
• Dai X, Hou H, Zhang W, Liu T, Li Y, Wang S, Wang B, Cao H. Microbial metabolites: critical regulators in NAFLD. Front Microbiol. 2020;11:567654. doi:10.3389/fmicb.2020.567654.
   PubMed Web of Science ®Google Scholar
• Mar JS, Ota N, Pokorzynski ND, Peng Y, Jaochico A, Sangaraju D, Skippington E, Lekkerkerker AN, Rothenberg ME, Tan MW. et al. IL-22 alters gut microbiota composition and function to increase aryl hydrocarbon receptor activity in mice and humans. Microbiome. 2023;11(1):47. doi:10.1186/s40168-023-01486-1.
   PubMedGoogle Scholar
• Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F. et al. Diversity of bifidobacteria within the infant gut microbiota. PloS ONE. 2012;7(5):e36957. doi:10.1371/journal.pone.0036957.
   PubMed Web of Science ®Google Scholar
• da Silva JGV, Vieira AT, Sousa TJ, Viana MVC, Parise D, Sampaio B, da Silva AL, de Jesus LCL, de Castro Oliveira L, Aburjaile FF. Comparative genomics and in silico gene evaluation involved in the probiotic potential of Bifidobacterium longum 51A. Gene. 2021;795:145781. doi:10.1016/j.gene.2021.145781.
   PubMed Web of Science ®Google Scholar
• Sharma P, Bhardwaj P, Singh R. Administration of lactobacillus casei and bifidobacterium bifidum ameliorated hyperglycemia, dyslipidemia, and oxidative stress in diabetic rats. Int J Prev Med. 2016;7. doi:10.4103/2008-7802.188870.
   PubMedGoogle Scholar
• Agus A, Clément K, Sokol H. Gut microbiota-derived metabolites as central regulators in metabolic disorders. Gut. 2021;70(6):1174–82. doi:10.1136/gutjnl-2020-323071.
   PubMed Web of Science ®Google Scholar