3,513
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

Fucose promotes intestinal stem cell-mediated intestinal epithelial development through promoting Akkermansia-related propanoate metabolism

, , , , , , & show all
Article: 2233149 | Received 29 Mar 2023, Accepted 30 Jun 2023, Published online: 10 Jul 2023

References

  • Gehart H, Clevers H. Tales from the crypt: new insights into intestinal stem cells. Nat Rev Gastroenterol Hepatol. 2019;16(1):19–19. doi:10.1038/s41575-018-0081-y.
  • Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell. 2013;154(2):274–284. doi:10.1016/j.cell.2013.07.004.
  • Barker N. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat Rev Mol Cell Biol. 2014;15(1):19–33. doi:10.1038/nrm3721.
  • van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol. 2009;71(1):241–260. doi:10.1146/annurev.physiol.010908.163145.
  • Goto Y, Uematsu S, Kiyono H. Epithelial glycosylation in gut homeostasis and inflammation. Nat Immunol. 2016;17(11):1244–1251. doi:10.1038/ni.3587.
  • Pickard JM, Chervonsky AV. Intestinal fucose as a mediator of host–microbe symbiosis. J Immunol. 2015;194(12):5588–5593. doi:10.4049/jimmunol.1500395.
  • Li Y, Jiang Y, Zhang L, Qian W, Hou X, Lin R. Exogenous l-fucose protects the intestinal mucosal barrier depending on upregulation of FUT2-mediated fucosylation of intestinal epithelial cells. The FASEB J. 2021;35(7):e21699. doi:10.1096/fj.202002446RRRR.
  • He R, Li Y, Han C, Lin R, Qian W, Hou X. L-Fucose ameliorates DSS-induced acute colitis via inhibiting macrophage M1 polarization and inhibiting NLRP3 inflammasome and NF-Kb activation. Int Immunopharmacol. 2019;73:379–388. doi:10.1016/j.intimp.2019.05.013.
  • Ke J, Li Y, Han C, He R, Lin R, Qian W, Hou X. Fucose ameliorate intestinal inflammation through modulating the crosstalk between bile acids and gut microbiota in a chronic colitis murine model. Inflamm Bowel Dis. 2020;26(6):863–873. doi:10.1093/ibd/izaa007.
  • Markandey M, Bajaj A, Ilott NE, Kedia S, Travis S, Powrie F, Ahuja V. Gut microbiota: sculptors of the intestinal stem cell niche in health and inflammatory bowel disease. Gut Microbes. 2021;13(1):1990827. doi:10.1080/19490976.2021.1990827.
  • Riehl TE, Alvarado D, Ee X, Zuckerman A, Foster L, Kapoor V, Thotala D, Ciorba MA, Stenson WF. Lactobacillus rhamnosus GG protects the intestinal epithelium from radiation injury through release of lipoteichoic acid, macrophage activation and the migration of mesenchymal stem cells. Gut. 2019;68(6):1003–1013. doi:10.1136/gutjnl-2018-316226.
  • Lee YS, Kim TY, Kim Y, Lee S-H, Kim S, Kang SW, Yang J-Y, Baek I-J, Sung YH, Park Y-Y, et al. Microbiota-derived lactate accelerates intestinal stem-cell-mediated epithelial development. Cell Host Microbe. 2018;24(6):833–846.e6. doi:10.1016/j.chom.2018.11.002.
  • Turroni F, Milani C, Duranti S, Mahony J, van Sinderen D, Ventura M. Glycan utilization and cross-feeding activities by bifidobacteria. Trends Microbiol. 2018;26(4):339–350. doi:10.1016/j.tim.2017.10.001.
  • Ottman N, Davids M, Suarez-Diez M, Boeren S, Schaap PJ, Martins dos Santos VAP, Smidt H, Belzer C, de Vos WM, et al. Genome-scale model and omics analysis of metabolic capacities of Akkermansia muciniphila reveal a preferential mucin-degrading lifestyle. Appl Environ Microbiol. 2017;83(18). doi:10.1128/AEM.01014-17.
  • Kim J, Cheong YE, Jung I, Kim K. Metabolomic and transcriptomic analyses of Escherichia coli for efficient fermentation of L-Fucose. Mar Drugs. 2019;17(2):17. doi:10.3390/md17020082.
  • Kim S, Shin YC, Kim TY, Kim Y, Lee Y-S, Lee S-H, Kim M-N, O E, Kim KS, Kweon M-N, et al. Mucin degrader Akkermansia muciniphila accelerates intestinal stem cell-mediated epithelial development. Gut Microbes. 2021;13(1):1–20. doi:10.1080/19490976.2021.1892441.
  • Gehart H, van Es JH, Hamer K, Beumer J, Kretzschmar K, Dekkers JF, Rios A, Clevers H. Identification of enteroendocrine regulators by real-time single-cell differentiation mapping. Cell. 2019;176(5):1158–1173.e16. doi:10.1016/j.cell.2018.12.029.
  • Kamioka M, Goto Y, Nakamura K, Yokoi Y, Sugimoto R, Ohira S, Kurashima Y, Umemoto S, Sato S, Kunisawa J, et al. Intestinal commensal microbiota and cytokines regulate Fut2 + Paneth cells for gut defense. Proc Natl Acad Sci USA. 2022;119(3):119. doi:10.1073/pnas.2115230119.
  • Tan C, Hong G, Wang Z, Duan C, Hou L, Wu J, Qian W, Han C, Hou X. Promoting effect of L-Fucose on the regeneration of intestinal stem cells through AHR/IL-22 pathway of intestinal lamina propria monocytes. Nutrients. 2022;14(22):14. doi:10.3390/nu14224789.
  • Borisova MA, Snytnikova OA, Litvinova EA, Achasova KM, Babochkina TI, Pindyurin AV, Tsentalovich YP, Kozhevnikova EN. Fucose ameliorates tryptophan metabolism and behavioral abnormalities in a mouse model of chronic colitis. Nutrients. 2020;12(2):12. doi:10.3390/nu12020445.
  • Kirmiz N, Galindo K, Cross KL, Luna E, Rhoades N, Podar M, Flores GE. Comparative genomics guides elucidation of vitamin B 12 biosynthesis in novel human-associated Akkermansia strains. Appl Environ Microbiol. 2020;86(3). doi:10.1128/AEM.02117-19.
  • Sivaprakasam S, Prasad PD, Singh N. Benefits of short-chain fatty acids and their receptors in inflammation and carcinogenesis. Pharmacology Therapeutics. 2016;164:144–151. doi:10.1016/j.pharmthera.2016.04.007.
  • Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, Harmsen HJ, Faber KN, Hermoso MA. Short Chain Fatty Acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10:277. doi:10.3389/fimmu.2019.00277.
  • Goto Y, Obata T, Kunisawa J, Sato S, Ivanov II, Lamichhane A, Takeyama N, Kamioka M, Sakamoto M, Matsuki T, et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science. 2014;345(6202):1254009. doi:10.1126/science.1254009.
  • Garber JM, Hennet T, Szymanski CM. Significance of fucose in intestinal health and disease. Mol Microbiol. 2021;115(6):1086–1093. doi:10.1111/mmi.14681.
  • Li M, Bai Y, Zhou J, Huang W, Yan J, Tao J, Fan Q, Liu Y, Mei D, Yan Q, et al. Core fucosylation of maternal milk N-Glycan Evokes B cell activation by selectively promoting the l-Fucose metabolism of gut bifidobacterium spp. and lactobacillus spp. mBio. 2019;10(2):10. doi:10.1128/mBio.00128-19.
  • Litvinova EA, Bets VD, Feofanova NA, Gvozdeva OV, Achasova KM, Alperina EL, Kozhevnikova EN. Dietary fucose affects macrophage polarization and reproductive performance in mice. Nutrients. 2021;13(3):855. doi:10.3390/nu13030855.
  • Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 2004;54(5):1469–1476. doi:10.1099/ijs.0.02873-0.
  • Zhai Q, Feng S, Arjan N, Chen W. A next generation probiotic, Akkermansia muciniphila. Crit Rev Food Sci Nutr. 2019;59(19):3227–3236. doi:10.1080/10408398.2018.1517725.
  • Ottman N, Geerlings SY, Aalvink S, de Vos WM, Belzer C. Action and function of Akkermansia muciniphila in microbiome ecology, health and disease. Best Pract Res Clin Gastroenterol. 2017;31(6):637–642. doi:10.1016/j.bpg.2017.10.001.
  • Wacklin P, Tuimala J, Nikkilä J, Tims S, Mäkivuokko H, Alakulppi N, Laine P, Rajilic-Stojanovic M, Paulin L, de Vos WM, et al. Faecal microbiota composition in adults is associated with the FUT2 gene determining the secretor status. PLoS One. 2014;9(4):e94863. doi:10.1371/journal.pone.0094863.
  • Wang JH, Bose S, Kim HG, Han K-S, Kim H. Fermented Rhizoma Atractylodis Macrocephalae alleviates high fat diet-induced obesity in association with regulation of intestinal permeability and microbiota in rats. Sci Rep. 2015;5(1):8391. doi:10.1038/srep08391.
  • Lukovac S, Belzer C, Pellis L, Keijser BJ, de Vos WM, Montijn RC, Roeselers G. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. mBio. 2014;5(4). doi:10.1128/mBio.01438-14.
  • Yao Y, Cai X, Fei W, Ye Y, Zhao M, Zheng C. The role of short-chain fatty acids in immunity, inflammation and metabolism. Crit Rev Food Sci Nutr. 2022;62(1):1–12. doi:10.1080/10408398.2020.1854675.
  • Willemsen LE, Koetsier MA, van Deventer SJ, Van Tol E.A. Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E(1) and E(2) production by intestinal myofibroblasts. Gut. 2003;52(10):1442–1447. doi:10.1136/gut.52.10.1442.
  • Xia Z, Han Y, Wang K, Guo S, Wu D, Huang X, Li Z, Zhu L. Oral administration of propionic acid during lactation enhances the colonic barrier function. Lipids Health Dis. 2017;16(1):62. doi:10.1186/s12944-017-0452-3.
  • Bilotta AJ, Ma C, Yang W, Yu Y, Yu Y, Zhao X, Zhou Z, Yao S, Dann SM, Cong Y, et al. Propionate enhances cell speed and persistence to promote intestinal epithelial turnover and repair. Cell Mol Gastroenterol Hepatol. 2021;11(4):1023–1044. doi:10.1016/j.jcmgh.2020.11.011.
  • Bajic D, Niemann A, Hillmer AK, Mejias-Luque R, Bluemel S, Docampo M, Funk MC, Tonin E, Boutros M, Schnabl B, et al. Gut microbiota-derived propionate regulates the expression of Reg3 mucosal lectins and ameliorates experimental colitis in mice. J Crohns Colitis. 2020;14(10):1462–1472. doi:10.1093/ecco-jcc/jjaa065.
  • Pinto D, Gregorieff A, Begthel H, Clevers H. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 2003;17(14):1709–1713. doi:10.1101/gad.267103.
  • Tang X, Wang W, Hong G, Duan C, Zhu S, Tian Y, Han C, Qian W, Lin R, Hou X, et al. Gut microbiota-mediated lysophosphatidylcholine generation promotes colitis in intestinal epithelium-specific Fut2 deficiency. J Biomed Sci. 2021;28(1):20. doi:10.1186/s12929-021-00711-z.
  • Wu H, Xie S, Miao J, Li Y, Wang Z, Wang M, Yu Q. Lactobacillus reuteri maintains intestinal epithelial regeneration and repairs damaged intestinal mucosa. Gut Microbes. 2020;11(4):997–1014. doi:10.1080/19490976.2020.1734423.
  • Yang L, Yang H, Chu Y, Song Y, Ding L, Zhu B, Zhai W, Wang X, Kuang Y, Ren F, et al. CREPT is required for murine stem cell maintenance during intestinal regeneration. Nat Commun. 2021;12(1):270. doi:10.1038/s41467-020-20636-9.