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Research Paper

Resynchronized rhythmic oscillations of gut microbiota drive time-restricted feeding induced nonalcoholic steatohepatitis alleviation

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Article: 2221450 | Received 15 Jan 2023, Accepted 12 May 2023, Published online: 12 Jun 2023

References

  • Pan X, Mota S, Zhang B. Circadian clock regulation on lipid metabolism and metabolic diseases. Adv Exp Med Biol. 2020;1276:53–22. doi:10.1007/978-981-15-6082-8_5.
  • Masri S, Sassone-Corsi P. The emerging link between cancer, metabolism, and circadian rhythms. Nat Med. 2018;24(12):1795–1803. doi:10.1038/s41591-018-0271-8.
  • Chaix A, Lin T, Le HD, Chang MW, Panda S. Time-restricted feeding prevents obesity and metabolic syndrome in mice lacking a circadian clock. Cell Metabolism. 2019;29(2):303–19.e4. doi:10.1016/j.cmet.2018.08.004.
  • Pan X, Queiroz J, Hussain MM. Nonalcoholic fatty liver disease in CLOCK mutant mice. J Clin Invest. 2020;130:4282–4300. doi:10.1172/JCI132765.
  • Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science (New York, NY). 2005;308(5724):1043–1045. doi:10.1126/science.1108750.
  • Wang F, Zhang L, Zhang Y, Zhang B, He Y, Xie S, Li M, Miao X, Chan EYY, Tang JL, et al. Meta-analysis on night shift work and risk of metabolic syndrome. Obes Rev. 2014;15(9):709–720. doi:10.1111/obr.12194.
  • Wilkinson MJ, Manoogian ENC, Zadourian A, Lo H, Fakhouri S, Shoghi A, Wang X, Fleischer JG, Navlakha S, Panda S, et al. Ten-hour time-restricted eating reduces weight, blood pressure, and atherogenic lipids in patients with metabolic syndrome. Cell Metab. 2020;31(1):92–104.e5. doi:10.1016/j.cmet.2019.11.004.
  • Saran AR, Dave S, Zarrinpar A. Circadian rhythms in the pathogenesis and treatment of fatty liver disease. Gastroenterology. 2020;158(7):1948–66.e1. doi:10.1053/j.gastro.2020.01.050.
  • Boulangé CL, Neves AL, Chilloux J, Nicholson JK, Dumas ME. Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Med. 2016;8(1):42. doi:10.1186/s13073-016-0303-2.
  • Voigt RM, Forsyth CB, Green SJ, Engen PA, Keshavarzian A. Circadian rhythm and the gut microbiome. Int Rev Neurobiol. 2016;131:193–205.
  • Brooks JF 2nd, Behrendt CL, Ruhn KA, Lee S, Raj P, Takahashi JS, Hooper LV. The microbiota coordinates diurnal rhythms in innate immunity with the circadian clock. Cell. 2021;184:4154–67.e12. doi:10.1016/j.cell.2021.07.001.
  • Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, Abramson L, Katz M, Korem T, Zmora N, et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. 2014;159(3):514–529. doi:10.1016/j.cell.2014.09.048.
  • Heddes M, Altaha B, Niu Y, Reitmeier S, Kleigrewe K, Haller D, Kiessling S. The intestinal clock drives the microbiome to maintain gastrointestinal homeostasis. Nat Commun. 2022;13:6068. doi:10.1038/s41467-022-33609-x.
  • Fawad JA, Luzader DH, Hanson GF, Moutinho TJ Jr., McKinney CA, Mitchell PG, Brown-Steinke K, Kumar A, Park M, Lee S, et al. Histone deacetylase inhibition by gut microbe-generated short-chain fatty acids entrains intestinal epithelial circadian rhythms. Gastroenterology. 2022;163(5):1377–90.e11. doi:10.1053/j.gastro.2022.07.051.
  • Tahara Y, Yamazaki M, Sukigara H, Motohashi H, Sasaki H, Miyakawa H, Haraguchi A, Ikeda Y, Fukuda S, Shibata S, et al. Gut microbiota-derived short chain fatty acids induce circadian clock entrainment in mouse peripheral tissue. Sci Rep. 2018;8(1):1395. doi:10.1038/s41598-018-19836-7.
  • Segers A, Desmet L, Thijs T, Verbeke K, Tack J, Depoortere I. The circadian clock regulates the diurnal levels of microbial short-chain fatty acids and their rhythmic effects on colon contractility in mice. England: Acta physiologica Oxford; 2019 Vol. 225. p. e13193.
  • Zarrinpar A, Chaix A, Yooseph S, Panda S. Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab. 2014;20(6):1006–1017. doi:10.1016/j.cmet.2014.11.008.
  • Reitmeier S, Kiessling S, Clavel T, List M, Almeida EL, Ghosh TS, Neuhaus K, Grallert H, Linseisen J, Skurk T, et al. Arrhythmic gut microbiome signatures predict risk of type 2 diabetes. Cell Host & Microbe. 2020;28(2):258–72.e6. doi:10.1016/j.chom.2020.06.004.
  • Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, Pierre J, Heneghan A, Nadimpalli A, Hubert N, et al. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host & Microbe. 2015;17(5):681–689. doi:10.1016/j.chom.2015.03.006.
  • Jamshed H, Beyl RA, Della Manna DL, Yang ES, Ravussin E, Peterson CM. Early time-restricted feeding improves 24-hour glucose levels and affects markers of the circadian clock. Aging, And Autophagy In Humans Nutr. 2019;11:11. doi:10.3390/nu11061234.
  • Longo VD, Panda PS. Fasting, circadian rhythms, and time-restricted feeding in healthy lifespan. Cell Metab. 2016;23(6):1048–1059. doi:10.1016/j.cmet.2016.06.001.
  • Hatori M, Vollmers C, Zarrinpar A, DiTacchio L, Bushong EA, Gill S, Leblanc M, Chaix A, Joens M, Fitzpatrick JJ, et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metabolism. 2012;15(6):848–860. doi:10.1016/j.cmet.2012.04.019.
  • Kotarsky CJ, Johnson NR, Mahoney SJ, Mitchell SL, Schimek RL, Stastny SN, Hackney KJ. Time-restricted eating and concurrent exercise training reduces fat mass and increases lean mass in overweight and obese adults. Physiol Rep. 2021;9:e14868. doi:10.14814/phy2.14868.
  • Moro T, Tinsley G, Bianco A, Marcolin G, Pacelli QF, Battaglia G, Palma A, Gentil P, Neri M, Paoli A, et al. Effects of eight weeks of time-restricted feeding (16/8) on basal metabolism, maximal strength, body composition, inflammation, and cardiovascular risk factors in resistance-trained males. J Transl Med. 2016;14(1):290. doi:10.1186/s12967-016-1044-0.
  • Ye Y, Xu H, Xie Z, Wang L, Sun Y, Yang H, Hu D, Mao Y. Time-restricted feeding reduces the detrimental effects of a high-fat diet, possibly by modulating the circadian rhythm of hepatic lipid metabolism and gut microbiota. Front Nutrition. 2020;7:596285. doi:10.3389/fnut.2020.596285.
  • Adamovich Y, Rousso-Noori L, Zwighaft Z, Neufeld-Cohen A, Golik M, Kraut-Cohen J, Wang M, Han X, Asher G. Circadian clocks and feeding time regulate the oscillations and levels of hepatic triglycerides. Cell Metab. 2014;19:319–330. doi:10.1016/j.cmet.2013.12.016.
  • Thaiss CA, Levy M, Korem T, Dohnalová L, Shapiro H, Jaitin DA, David E, Winter DR, Gury-BenAri M, Tatirovsky E, et al. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell. 2016;167(6):1495–510.e12. doi:10.1016/j.cell.2016.11.003.
  • Schugar RC, Gliniak CM, Osborn LJ, Massey W, Sangwan N, Horak A, Banerjee R, Orabi D, Helsley RN, Brown AL, et al. Gut microbe-targeted choline trimethylamine lyase inhibition improves obesity via rewiring of host circadian rhythms. Elife. 2022;11:11. doi:10.7554/eLife.63998.
  • Scheer FA, Hilton MF, Mantzoros CS, Shea SA. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci U S A. 2009;106(11):4453–4458. doi:10.1073/pnas.0808180106.
  • Bass J, Takahashi JS. Circadian integration of metabolism and energetics. Science. 2010;330(6009):1349–1354. doi:10.1126/science.1195027.
  • Salgado-Delgado R, Angeles-Castellanos M, Saderi N, Buijs RM, Escobar C. Food intake during the normal activity phase prevents obesity and circadian desynchrony in a rat model of night work. Endocrinology. 2010;151(3):1019–1029. doi:10.1210/en.2009-0864.
  • Khalyfa A, Poroyko VA, Qiao Z, Gileles-Hillel A, Khalyfa AA, Akbarpour M, Almendros I, Farré R, Gozal D. Exosomes and metabolic function in mice exposed to alternating dark-light cycles mimicking night shift work schedules. Front Physiol. 2017;8:882. doi:10.3389/fphys.2017.00882.
  • Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong L-W, DiTacchio L, Atkins AR, Glass CK, et al. Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature. 2012;485(7396):123–127. doi:10.1038/nature11048.
  • Sutton EF, Beyl R, Early KS, Cefalu WT, Ravussin E, Peterson CM. Early time-restricted feeding improves insulin sensitivity, blood pressure, and oxidative stress even without weight loss in men with prediabetes. Cell Metab. 2018;27(6):1212–21.e3. doi:10.1016/j.cmet.2018.04.010.
  • Li C, Xing C, Zhang J, Zhao H, Shi W, He B. Eight-hour time-restricted feeding improves endocrine and metabolic profiles in women with anovulatory polycystic ovary syndrome. J Transl Med. 2021;19(1):148. doi:10.1186/s12967-021-02817-2.
  • Chung H, Chou W, Sears DD, Patterson RE, Webster NJ, Ellies LG. Time-restricted feeding improves insulin resistance and hepatic steatosis in a mouse model of postmenopausal obesity. Metabolism. 2016;65(12):1743–1754. doi:10.1016/j.metabol.2016.09.006.
  • Chaix A, Zarrinpar A, Miu P, Panda S. Time-restricted feeding is a preventative and therapeutic intervention against diverse nutritional challenges. Cell Metab. 2014;20(6):991–1005. doi:10.1016/j.cmet.2014.11.001.
  • Shu YY, Gao WK, Chu HK, Yang L, Pan XL, Ye J, Luo L. Attenuation by time-restricted feeding of high-fat and high-fructose diet-induced NASH in Mice is related to per2 and ferroptosis. Oxid Med Cell Longev. 2022;2022:1–20. doi:10.1155/2022/8063897.
  • Yamamuro D, Takahashi M, Nagashima S, Wakabayashi T, Yamazaki H, Takei A, Takei S, Sakai K, Ebihara K, Iwasaki Y, et al. Peripheral circadian rhythms in the liver and white adipose tissue of mice are attenuated by constant light and restored by time-restricted feeding. PLos One. 2020;15(6):e0234439. doi:10.1371/journal.pone.0234439.
  • Zhang X, Coker OO, Chu ES, Fu K, Lau HCH, Wang YX, Chan AWH, Wei H, Yang X, Sung JJY, et al. Dietary cholesterol drives fatty liver-associated liver cancer by modulating gut microbiota and metabolites. Gut. 2021;70(4):761–774. doi:10.1136/gutjnl-2019-319664.
  • Boursier J, Mueller O, Barret M, Machado M, Fizanne L, Araujo-Perez F, Guy CD, Seed PC, Rawls JF, David LA, et al. The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology. 2016;63(3):764–775. doi:10.1002/hep.28356.
  • Barrow F, Khan S, Fredrickson G, Wang H, Dietsche K, Parthiban P, Robert S, Kaiser T, Winer S, Herman A, et al. Microbiota-driven activation of intrahepatic B cells aggravates NASH through innate and adaptive signaling. Hepatology. 2021;74(2):704–722. doi:10.1002/hep.31755.
  • Murphy EF, Cotter PD, Healy S, Marques TM, O’Sullivan O, Fouhy F, Clarke SF, O’Toole PW, Quigley EM, Stanton C, et al. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut. 2010;59(12):1635–1642. doi:10.1136/gut.2010.215665.
  • Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341(6150):1241214. doi:10.1126/science.1241214.
  • 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):882–899. doi:10.1080/19490976.2020.1712984.
  • Xia J, Lv L, Liu B, Wang S, Zhang S, Wu Z, Yang L, Bian X, Wang Q, Wang K, et al. Akkermansia muciniphila ameliorates acetaminophen-induced liver injury by regulating gut microbial composition and metabolism. Microbiol Spectr. 2022;10(1):e0159621. doi:10.1128/spectrum.01596-21.
  • Hu W, Gao W, Liu Z, Fang Z, Wang H, Zhao J, Zhang H, Lu W, Chen W. Specific strains of faecalibacterium prausnitzii ameliorate nonalcoholic fatty liver disease in mice in association with gut microbiota regulation. Nutrients. 2022;14:14. doi:10.3390/nu14142945.
  • Wu G, Tang W, He Y, Hu J, Gong S, He Z, Wei G, Lv L, Jiang Y, Zhou H, et al. Light exposure influences the diurnal oscillation of gut microbiota in mice. Biochem Biophys Res Commun. 2018;501:16–23. doi:10.1016/j.bbrc.2018.04.095.
  • Segers A, Desmet L, Sun S, Verbeke K, Tack J, Depoortere I. Night-time feeding of Bmal1-/- mice restores SCFA rhythms and their effect on ghrelin. J Endocrinol. 2020;245:155–164. doi:10.1530/JOE-20-0011.
  • Wang L, Ren B, Hui Y, Chu C, Zhao Z, Zhang Y, Zhao B, Shi R, Ren J, Dai X, et al. Methionine restriction regulates cognitive function in high-fat diet-fed mice: roles of diurnal rhythms of SCFAs producing- and inflammation-related microbes. Mol Nutr Food Res. 2020;64(17):e2000190. doi:10.1002/mnfr.202000190.
  • Zhang X, Zou Q, Zhao B, Zhang J, Zhao W, Li Y, et al. Effects of alternate-day fasting, time-restricted fasting and intermittent energy restriction DSS-induced on colitis and behavioral disorders. Redox Biol. 2020;32:101535. doi:10.1016/j.redox.2020.101535.
  • Kuang Z, Wang Y, Li Y, Ye C, Ruhn KA, Behrendt CL, Olson EN, Hooper LV. The intestinal microbiota programs diurnal rhythms in host metabolism through histone deacetylase 3. Science. 2019;365:1428–1434. doi:10.1126/science.aaw3134.
  • Mayneris-Perxachs J, Cardellini M, Hoyles L, Latorre J, Davato F, Moreno-Navarrete JM, Arnoriaga-Rodríguez M, Serino M, Abbott J, Barton RH, et al. Iron status influences non-alcoholic fatty liver disease in obesity through the gut microbiome. Microbiome. 2021;9(1):104. doi:10.1186/s40168-021-01052-7.
  • Lundell LS, Parr EB, Devlin BL, Ingerslev LR, Altıntaş A, Sato S, Sassone-Corsi P, Barrès R, Zierath JR, Hawley JA, et al. Time-restricted feeding alters lipid and amino acid metabolite rhythmicity without perturbing clock gene expression. Nat Commun. 2020;11(1):4643. doi:10.1038/s41467-020-18412-w.
  • Koronowski KB, Greco CM, Huang H, Kim JK, Fribourgh JL, Crosby P, Mathur L, Ren X, Partch CL, Jang C, et al. Ketogenesis impact on liver metabolism revealed by proteomics of lysine β-hydroxybutyrylation. Cell Rep. 2021;36(5):109487. doi:10.1016/j.celrep.2021.109487.
  • Alexander RK, Liou YH, Knudsen NH, Starost KA, Xu C, Hyde AL, Liu S, Jacobi D, Liao N-S, Lee C-H, et al. Bmal1 integrates mitochondrial metabolism and macrophage activation. Elife. 2020;9. doi:10.7554/eLife.54090.
  • Chakraborty S, Mandal J, Cheng X, Galla S, Hindupur A, Saha P, Yeoh BS, Mell B, Yeo J-Y, Vijay-Kumar M, et al. Diurnal timing dependent alterations in gut microbial composition are synchronously linked to salt-sensitive hypertension and renal damage. Hypertension. 2020;76(1):59–72. doi:10.1161/HYPERTENSIONAHA.120.14830.
  • Gong S, Lan T, Zeng L, Luo H, Yang X, Li N, Chen X, Liu Z, Li R, Win S, et al. Gut microbiota mediates diurnal variation of acetaminophen induced acute liver injury in mice. J Hepatol. 2018;69(1):51–59. doi:10.1016/j.jhep.2018.02.024.
  • Chaix A, Deota S, Bhardwaj R, Lin T, Panda S. Sex- and age-dependent outcomes of 9-hour time-restricted feeding of a Western high-fat high-sucrose diet in C57BL/6J mice. Cell Rep. 2021;36(7):109543. doi:10.1016/j.celrep.2021.109543.
  • Hou T, Su W, Duncan MJ, Olga VA, Guo Z, Gong MC. Time-restricted feeding protects the blood pressure circadian rhythm in diabetic mice. Proc Natl Acad Sci U S A. 2021;118(25):118. doi:10.1073/pnas.2015873118.
  • Pan X, Taylor MJ, Cohen E, Hanna N, Circadian Clock MS. Time-restricted feeding and reproduction. Int J Mol Sci. 2020;21:21. doi:10.3390/ijms21030831.
  • Hosono T, Ono M, Daikoku T, Mieda M, Nomura S, Kagami K, Iizuka T, Nakata R, Fujiwara T, Fujiwara H, et al. Time-restricted feeding regulates circadian rhythm of murine uterine clock. Curr Dev Nutr. 2021;5:nzab064. doi:10.1093/cdn/nzab064.
  • Agus A, Clément K, Sokol H. Gut microbiota-derived metabolites as central regulators in metabolic disorders. Gut. 2021;70(6):1174–1182. doi:10.1136/gutjnl-2020-323071.
  • Dong F, Hao F, Murray IA, Smith PB, Koo I, Tindall AM, Kris-Etherton PM, Gowda K, Amin SG, Patterson AD, et al. Intestinal microbiota-derived tryptophan metabolites are predictive of Ah receptor activity. Gut Microbes. 2020;12(1):1–24. doi:10.1080/19490976.2020.1788899.
  • Mallmann NH, Lima ES, Lalwani P. Dysregulation of tryptophan catabolism in metabolic syndrome. Metab Syndr Relat Disord. 2018;16(3):135–142. doi:10.1089/met.2017.0097.
  • Ji Y, Yin Y, Sun L, Zhang W. The molecular and mechanistic insights based on gut–liver axis: nutritional target for Non-Alcoholic Fatty Liver DisEase (NAFLD) improvement. Int J Mol Sci. 2020;21:21. doi:10.3390/ijms21093066.
  • Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host & Microbe. 2018;23(6):716–724. doi:10.1016/j.chom.2018.05.003.
  • Ma L, Li H, Hu J, Zheng J, Zhou J, Botchlett R, Matthews D, Zeng T, Chen L, Xiao X, et al. Indole alleviates diet-induced hepatic steatosis and inflammation in a manner involving myeloid cell 6-phosphofructo-2-kinase/fructose-2,6-biphosphatase 3. Hepatology. 2020;72(4):1191–1203. doi:10.1002/hep.31115.
  • Ji Y, Gao Y, Chen H, Yin Y, Zhang W. Indole-3-acetic acid alleviates nonalcoholic fatty liver disease in mice via attenuation of hepatic lipogenesis, and oxidative and inflammatory stress. Nutrients. 2019;11(9):11. doi:10.3390/nu11092062.
  • Liu Z, Dai X, Zhang H, Shi R, Hui Y, Jin X, Zhang W, Wang L, Wang Q, Wang D, et al. Gut microbiota mediates intermittent-fasting alleviation of diabetes-induced cognitive impairment. Nat Commun. 2020;11(1):855. doi:10.1038/s41467-020-14676-4.