7,684
Views
17
CrossRef citations to date
0
Altmetric
Review

Mucins, gut microbiota, and postbiotics role in colorectal cancer

ORCID Icon, , , , , & ORCID Icon show all
Article: 1974795 | Received 09 Jun 2021, Accepted 24 Aug 2021, Published online: 29 Sep 2021

References

  • Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67(9):1716–17. doi:10.1136/gutjnl-2018-316723.
  • Cani PD, Van Hul M, Lefort C, Depommier C, Rastelli M, Everard A. Microbial regulation of organismal energy homeostasis. Nat Metab. 2019;1(1):34–46. doi:10.1038/s42255-018-0017-4.
  • Knight R, Callewaert C, Marotz C, Hyde ER, Debelius JW, McDonald D, Sogin ML. The microbiome and human biology. Annu Rev Genomics Hum Genet. 2017;18(1):65–86. doi:10.1146/annurev-genom-083115-022438.
  • Sender R, Fuchs S, Milo R. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell. 2016;164:337–340. doi:10.1016/j.cell.2016.01.013.
  • Johansson ME, Jakobsson HE, Holmen-Larsson J, Schutte A, Ermund A, Rodriguez-Pineiro AM, Arike L, Wising C, Svensson F, Bäckhed F, et al. Normalization of host intestinal mucus layers requires long-term microbial colonization. Cell Host Microbe. 2015;18:582–592. doi:10.1016/j.chom.2015.10.007.
  • Petersson J, Schreiber O, Hansson GC, Gendler SJ, Velcich A, Lundberg JO, Roos S, Holm L, Phillipson M. Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am J Physiol Gastrointest Liver Physiol. 2011;300:G327–33.
  • Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto J-M, Kennedy S, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541–546. doi:10.1038/nature12506.
  • Konig J, Wells J, Cani PD, Garcia-Rodenas CL, MacDonald T, Mercenier A, Whyte J, Troost F, Brummer R-J. Human intestinal barrier function in health and disease. Clin Transl Gastroenterol. 2016;7(10):e196. doi:10.1038/ctg.2016.54.
  • Wells JM, Brummer RJ, Derrien M, MacDonald TT, Troost F, Cani PD, Theodorou V, Dekker J, Méheust A, de Vos WM, et al. Homeostasis of the gut barrier and potential biomarkers. Am J Physiol Gastrointest Liver Physiol. 2017;312(3):G171–G93. doi:10.1152/ajpgi.00048.2015.
  • Tilg H, Adolph TE, Gerner RR, Moschen AR. The intestinal microbiota in colorectal cancer. Cancer Cell. 2018;33(6):954–964. doi:10.1016/j.ccell.2018.03.004.
  • Dai Z, Coker OO, Nakatsu G, Wu WKK, Zhao L, Chen Z, Chan FKL, Kristiansen K, Sung JJY, Wong SH, et al. Multi-cohort analysis of colorectal cancer metagenome identified altered bacteria across populations and universal bacterial markers. Microbiome. 2018;6(1):70. doi:10.1186/s40168-018-0451-2.
  • Wirbel J, Pyl PT, Kartal E, Zych K, Kashani A, Milanese A, Fleck JS, Voigt AY, Palleja A, Ponnudurai R, et al. Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nat Med. 2019;25:679–689. doi:10.1038/s41591-019-0406-6.
  • Pothuraju R, Sharma RK, Onteru SK, Singh S, Hussain SA. Hypoglycemic and hypolipidemic effects of aloe vera extract preparations: a review. Phytother Res. 2016;30(2):200–207. doi:10.1002/ptr.5532.
  • Morrison DJ, Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes. 2016;7(3):189–200. doi:10.1080/19490976.2015.1134082.
  • Earle KA, Billings G, Sigal M, Lichtman JS, Hansson GC, Elias JE, Amieva M, Huang K, Sonnenburg J. Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe. 2015;18(4):478–488. doi:10.1016/j.chom.2015.09.002.
  • Pothuraju R, Krishn SR, Gautam SK, Pai P, Ganguly K, Chaudhary S, Rachagani S, Kaur S, Batra SK. Mechanistic and functional shades of mucins and associated glycans in colon cancer. Cancers (Basel). 2020;12(3):649.
  • Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey Ca, Wolter M, Pudlo NA, Kitamoto S, Terrapon N, Muller A, et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. 2016;167(5):1339–53 e21. doi:10.1016/j.cell.2016.10.043.
  • Johansson ME, Sjovall H, Hansson GC. The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol. 2013;10(6):352–361. doi:10.1038/nrgastro.2013.35.
  • Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Büller HA, Dekker J, Van Seuningen I, Renes IB, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131(1):117–129. doi:10.1053/j.gastro.2006.04.020.
  • Birchenough G, Schroeder BO, Backhed F, Hansson GC. Dietary destabilisation of the balance between the microbiota and the colonic mucus barrier. Gut Microbes. 2019;10(2):246–250. doi:10.1080/19490976.2018.1513765.
  • Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2021. CA Cancer J Clin. 2021;71(1):7–33. doi:10.3322/caac.21654.
  • Islami F, Goding Sauer A, Miller KD, Siegel RL, Fedewa SA, Jacobs EJ, McCullough ML, Patel AV, Ma J, Soerjomataram I, et al. Proportion and number of cancer cases and deaths attributable to potentially modifiable risk factors in the United States. CA Cancer J Clin. 2018;68(1):31–54. doi:10.3322/caac.21440.
  • Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, Costea PI, Godneva A, Kalka IN, Bar N, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555(7695):210–215. doi:10.1038/nature25973.
  • Song M, Giovannucci E. Preventable incidence and mortality of carcinoma associated with lifestyle factors among white adults in the United States. JAMA Oncol. 2016;2(9):1154–1161. doi:10.1001/jamaoncol.2016.0843.
  • Song M, Chan AT. Environmental factors, gut microbiota, and colorectal cancer prevention. Clin Gastroenterol Hepatol. 2019;17(2):275–289. doi:10.1016/j.cgh.2018.07.012.
  • Cani PD, Jordan BF. Gut microbiota-mediated inflammation in obesity: a link with gastrointestinal cancer. Nat Rev Gastroenterol Hepatol. 2018;15(11):671–682. doi:10.1038/s41575-018-0025-6.
  • Kyriachenko Y, Falalyeyeva T, Korotkyi O, Molochek N, Kobyliak N. Crosstalk between gut microbiota and antidiabetic drug action. World J Diabetes. 2019;10(3):154–168. doi:10.4239/wjd.v10.i3.154.
  • Song M, Chan AT, Sun J. Influence of the gut microbiome, diet, and environment on risk of colorectal cancer. Gastroenterology. 2020;158(2):322–340. doi:10.1053/j.gastro.2019.06.048.
  • Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, Gaskins HR, O’Keefe SJ. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr. 2013;98(1):111–120. doi:10.3945/ajcn.112.056689.
  • Schroeder BO, Birchenough GMH, Stahlman M, Arike L, Johansson MEV, Hansson GC, Bäckhed F. Bifidobacteria or fiber protects against diet-induced microbiota-mediated colonic mucus deterioration. Cell Host Microbe. 2018;23(1):27–40 e7. doi:10.1016/j.chom.2017.11.004.
  • Tan J, Chen YX. Dietary and Lifestyle factors associated with colorectal cancer risk and interactions with microbiota: fiber, red or processed meat and alcoholic drinks. Gastrointest Tumors. 2016;3:17–24. doi:10.1159/000442831.
  • Song M, Garrett WS, Chan AT. Nutrients, foods, and colorectal cancer prevention. Gastroenterology. 2015;148:1244–60 e16.
  • Vieira AR, Abar L, Chan DSM, Vingeliene S, Polemiti E, Stevens C, Greenwood D, Norat T. Foods and beverages and colorectal cancer risk: a systematic review and meta-analysis of cohort studies, an update of the evidence of the WCRF-AICR Continuous Update Project. Ann Oncol. 2017;28:1788–1802. doi:10.1093/annonc/mdx171.
  • Donohoe DR, Holley D, Collins LB, Montgomery SA, Whitmore AC, Hillhouse A, Curry KP, Renner SW, Greenwalt A, Ryan EP. A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota- and butyrate-dependent manner. Cancer Discov. 2014;4:1387–1397. doi:10.1158/2159-8290.CD-14-0501.
  • Marchand LL. Combined influence of genetic and dietary factors on colorectal cancer incidence in Japanese Americans. J Natl Cancer Inst Monogr. 1999;101–105. doi:10.1093/oxfordjournals.jncimonographs.a024220.
  • Minchin RF, Reeves PT, Teitel CH, McManus ME, Mojarrabi B, Ilett KF, Kadlubar FF. N-and O-acetylation of aromatic and heterocyclic amine carcinogens by human monomorphic and polymorphic acetyltransferases expressed in COS-1 cells. Biochem Biophys Res Commun. 1992;185:839–844. doi:10.1016/0006-291X(92)91703-S.
  • O’Keefe SJ, Chung D, Mahmoud N, Sepulveda AR, Manafe M, Arch J, Adada H, van der Merwe T. Why do African Americans get more colon cancer than Native Africans? J Nutr. 2007;137:175S–82S. doi:10.1093/jn/137.1.175S.
  • O’Keefe SJ, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K, Posma JM, Kinross J, Wahl E, Ruder E, et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun. 2015;6(1):6342. doi:10.1038/ncomms7342.
  • Mehta RS, Nishihara R, Cao Y, Song M, Mima K, Qian ZR, Nowak JA, Kosumi K, Hamada T, Masugi Y, et al. Association of dietary patterns with risk of colorectal cancer subtypes classified by fusobacterium nucleatum in tumor tissue. JAMA Oncol. 2017;3(7):921–927. doi:10.1001/jamaoncol.2016.6374.
  • Mima K, Nishihara R, Qian ZR, Cao Y, Sukawa Y, Nowak JA, Yang J, Dou R, Masugi Y, Song M, et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut. 2016;65(12):1973–1980. doi:10.1136/gutjnl-2015-310101.
  • Dingeo G, Brito A, Samouda H, Iddir M, La Frano MR, Bohn T. Phytochemicals as modifiers of gut microbial communities. Food Funct. 2020;11:8444–8471. doi:10.1039/D0FO01483D.
  • Anhe FF, Roy D, Pilon G, Dudonne S, Matamoros S, Varin TV, Garofalo C, Moine Q, Desjardins Y, Levy E, et al. A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut. 2015;64(6):872–883. doi:10.1136/gutjnl-2014-307142.
  • Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110(22):9066–9071. doi:10.1073/pnas.1219451110.
  • Bassani B, Rossi T, De Stefano D, Pizzichini D, Corradino P, Macrì N, Noonan DM, Albini A, Bruno A. Potential chemopreventive activities of a polyphenol rich purified extract from olive mill wastewater on colon cancer cells. J Funct Foods. 2016;27:236–248.
  • Sun Y, Wu X, Cai X, Song M, Zheng J, Pan C, Qiu P, Zhang L, Zhou S, Tang Z, et al. Identification of pinostilbene as a major colonic metabolite of pterostilbene and its inhibitory effects on colon cancer cells. Mol Nutr Food Res. 2016;60(9):1924–1932. doi:10.1002/mnfr.201500989.
  • Paul S, DeCastro AJ, Lee HJ, Smolarek AK, So JY, Simi B, Wang CX, Zhou R, Rimando AM, Suh N, et al. Dietary intake of pterostilbene, a constituent of blueberries, inhibits the beta-catenin/p65 downstream signaling pathway and colon carcinogenesis in rats. Carcinogenesis. 2010;31:1272–1278. doi:10.1093/carcin/bgq004.
  • Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14(8):491–502. doi:10.1038/nrgastro.2017.75.
  • Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125:1401–1412. doi:10.1093/jn/125.6.1401.
  • Fong W, Li Q, Yu J. Gut microbiota modulation: a novel strategy for prevention and treatment of colorectal cancer. Oncogene. 2020;39:4925–4943. doi:10.1038/s41388-020-1341-1.
  • Markowiak-Kopec P, Slizewska K. The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome. Nutrients. 2020;12(4):1107.
  • Ratajczak W, Ryl A, Mizerski A, Walczakiewicz K, Sipak O, Laszczynska M. Immunomodulatory potential of gut microbiome-derived short-chain fatty acids (SCFAs). Acta Biochim Pol. 2019;66:1–12.
  • Keshteli AH, Madsen KL, Dieleman LA. Diet in the pathogenesis and management of ulcerative colitis; a review of randomized controlled dietary interventions. Nutrients. 2019;11(7):1498.
  • Davani-Davari D, Negahdaripour M, Karimzadeh I, Seifan M, Mohkam M, Masoumi SJ, Berenjian A, Ghasemi Y. Prebiotics: definition, types, sources, mechanisms, and clinical applications. Foods. 2019;8(3):92.
  • Lomax AR, Calder PC. Prebiotics, immune function, infection and inflammation: a review of the evidence. Br J Nutr. 2009;101:633–658. doi:10.1017/S0007114508055608.
  • Ohtsuka K, Tsuji K, Nakagawa Y, Ueda H, Ozawa O, Uchida T, Ichikawa T. Utilization and metabolism of [U-14C]4ʹ galactosyllactose (O-beta-D-galactopyranosyl-(1—-4)-O-beta-D-galactopyranosyl-(1—-4)- D-glucopyranose) in rats. J Nutr Sci Vitaminol (Tokyo). 1991;37:173–184. doi:10.3177/jnsv.37.173.
  • Figueroa-Lozano S, Ren C, Yin H, Pham H, van Leeuwen S, Dijkhuizen L, de Vos P. The impact of oligosaccharide content, glycosidic linkages and lactose content of galacto-oligosaccharides (GOS) on the expression of mucus-related genes in goblet cells. Food Funct. 2020;11:3506–3515. doi:10.1039/D0FO00064G.
  • Meslin JC, Andrieux C, Sakata T, Beaumatin P, Bensaada M, Popot F, O Szylit, Durand M. Effects of galacto-oligosaccharide and bacterial status on mucin distribution in mucosa and on large intestine fermentation in rats. Br J Nutr. 1993;69:903–912. doi:10.1079/BJN19930090.
  • Leforestier G, Blais A, Blachier F, Marsset-Baglieri A, Davila-Gay AM, Perrin E, Tomé D. Effects of galacto-oligosaccharide ingestion on the mucosa-associated mucins and sucrase activity in the small intestine of mice. Eur J Nutr. 2009;48:457–464. doi:10.1007/s00394-009-0036-8.
  • Fernandez J, Moreno FJ, Olano A, Clemente A, Villar CJ, Lombo F. A galacto-oligosaccharides preparation derived from lactulose protects against colorectal cancer development in an animal model. Front Microbiol. 2018;9:2004. doi:10.3389/fmicb.2018.02004.
  • Kaliannan K, Hamarneh SR, Economopoulos KP, Nasrin Alam S, Moaven O, Patel P, Malo NS, Ray M, Abtahi SM, Muhammad N, et al. Intestinal alkaline phosphatase prevents metabolic syndrome in mice. Proc Natl Acad Sci U S A. 2013;110(17):7003–7008. doi:10.1073/pnas.1220180110.
  • Okazaki Y, Katayama T. Consumption of non-digestible oligosaccharides elevates colonic alkaline phosphatase activity by up-regulating the expression of IAP-I, with increased mucins and microbial fermentation in rats fed a high-fat diet. Br J Nutr. 2019;121:146–154. doi:10.1017/S0007114518003082.
  • Tuohy KM, Kolida S, Lustenberger AM, Gibson GR. The prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides–a human volunteer study. Br J Nutr. 2001;86:341–348. doi:10.1079/BJN2001394.
  • Hsu CK, Liao JW, Chung YC, Hsieh CP, Chan YC. Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. J Nutr. 2004;134:1523–1528. doi:10.1093/jn/134.6.1523.
  • Pierre F, Perrin P, Champ M, Bornet F, Meflah K, Menanteau J. Short-chain fructo-oligosaccharides reduce the occurrence of colon tumors and develop gut-associated lymphoid tissue in min mice. Cancer Res. 1997;57:225–228.
  • Lima GC, Vieira VCC, Cazarin CBB, Ribeiro RDR, Junior SB, De Albuquerque CL, Vidal RO, Netto CC, Yamada ÁT, Augusto F, et al. Fructooligosaccharide intake promotes epigenetic changes in the intestinal mucosa in growing and ageing rats. Eur J Nutr. 2018;57(4):1499–1510. doi:10.1007/s00394-017-1435-x.
  • Bouhnik Y, Flourie B, Riottot M, Bisetti N, Gailing MF, Guibert A, Bornet F, Rambaud JC. Effects of fructo-oligosaccharides ingestion on fecal bifidobacteria and selected metabolic indexes of colon carcinogenesis in healthy humans. Nutr Cancer. 1996;26:21–29. doi:10.1080/01635589609514459.
  • Boutron-Ruault MC, Marteau P, Lavergne-Slove A, Myara A, Gerhardt MF, Franchisseur C, Bornet F. Effects of a 3-mo consumption of short-chain fructo-oligosaccharides on parameters of colorectal carcinogenesis in patients with or without small or large colorectal adenomas. Nutr Cancer. 2005;53:160–168. doi:10.1207/s15327914nc5302_5.
  • Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, et al. Expert consensus document. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506–514. doi:10.1038/nrgastro.2014.66.
  • Caballero-Franco C, Keller K, De Simone C, Chadee K. The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2007;292(1):G315–22. doi:10.1152/ajpgi.00265.2006.
  • Martin R, Chamignon C, Mhedbi-Hajri N, Chain F, Derrien M, Escribano-Vazquez U, Garault P, Cotillard A, Pham HP, Chervaux C, et al. The potential probiotic Lactobacillus rhamnosus CNCM I-3690 strain protects the intestinal barrier by stimulating both mucus production and cytoprotective response. Sci Rep. 2019;9(1):5398. doi:10.1038/s41598-019-41738-5.
  • Yang HS, Fu DZ, Kong XF, Wang WC, Yang XJ, Nyachoti CM, Yin YL. Dietary supplementation with N-carbamylglutamate increases the expression of intestinal amino acid transporters in weaned Huanjiang mini-pig piglets. J Anim Sci. 2013;91(6):2740–2748. doi:10.2527/jas.2012-5795.
  • Wang G, Huang S, Wang Y, Cai S, Yu H, Liu H, Zeng X, Zhang G, Qiao S. Bridging intestinal immunity and gut microbiota by metabolites. Cell Mol Life Sci. 2019;76(20):3917–3937. doi:10.1007/s00018-019-03190-6.
  • Zolkiewicz J, Marzec A, Ruszczynski M, Feleszko W. Postbiotics-a step beyond pre- and probiotics. Nutrients. 2020;12(8):2189.
  • Gaudier E, Jarry A, Blottiere HM, De Coppet P, Buisine MP, Aubert JP, Laboisse C, Cherbut C, Hoebler C. Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose. Am J Physiol Gastrointest Liver Physiol. 2004;287(6):G1168–74. doi:10.1152/ajpgi.00219.2004.
  • Burger-van Paassen N, Vincent A, Puiman PJ, van der Sluis M, Bouma J, Boehm G, van Goudoever J, Van seuningen I, Renes I. The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem J. 2009;420(2):211–219. doi:10.1042/BJ20082222.
  • Jung TH, Park JH, Jeon WM, Han KS. Butyrate modulates bacterial adherence on LS174T human colorectal cells by stimulating mucin secretion and MAPK signaling pathway. Nutr Res Pract. 2015;9:343–349. doi:10.4162/nrp.2015.9.4.343.
  • Jiminez JA, Uwiera TC, Abbott DW, Uwiera RRE, Inglis GD. Butyrate supplementation at high concentrations alters enteric bacterial communities and reduces intestinal inflammation in mice infected with citrobacter rodentium. mSphere. 2017;2(4):e00243-17.
  • Willemsen LE, Koetsier MA, Van Deventer SJ, van Tol EA. 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;52:1442–1447. doi:10.1136/gut.52.10.1442.
  • Bjarnason I, Hayllar J, MacPherson AJ, Russell AS. Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterology. 1993;104:1832–1847. doi:10.1016/0016-5085(93)90667-2.
  • Yamada T, Hino S, Iijima H, Genda T, Aoki R, Nagata R, Han K-H, Hirota M, Kinashi Y, Oguchi H, et al. Mucin O-glycans facilitate symbiosynthesis to maintain gut immune homeostasis. EBioMedicine. 2019;48:513–525. doi:10.1016/j.ebiom.2019.09.008.
  • Taleb S. Tryptophan dietary impacts gut barrier and metabolic diseases. Front Immunol. 2019;10:2113. doi:10.3389/fimmu.2019.02113.
  • Gheorghe CE, Martin JA, Manriquez FV, Dinan TG, Cryan JF, Clarke G. Focus on the essentials: tryptophan metabolism and the microbiome-gut-brain axis. Curr Opin Pharmacol. 2019;48:137–145. doi:10.1016/j.coph.2019.08.004.
  • Scott SA, Fu J, Chang PV. Microbial tryptophan metabolites regulate gut barrier function via the aryl hydrocarbon receptor. Proc Natl Acad Sci U S A. 2020;117(32):19376–19387. doi:10.1073/pnas.2000047117.
  • Lanis JM, Alexeev EE, Curtis VF, Kitzenberg DA, Kao DJ, Battista KD, Gerich ME, Glover LE, Kominsky DJ, Colgan SP, et al. Tryptophan metabolite activation of the aryl hydrocarbon receptor regulates IL-10 receptor expression on intestinal epithelia. Mucosal Immunol. 2017;10(5):1133–1144. doi:10.1038/mi.2016.133.
  • Venkatesh M, Mukherjee S, Wang H, Li H, Sun K, Benechet AP, Qiu Z, Maher L, Redinbo M, Phillips R, et al. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and toll-like receptor 4. Immunity. 2014;41(2):296–310. doi:10.1016/j.immuni.2014.06.014.
  • Li J, Zhang L, Wu T, Li Y, Zhou X, Ruan Z. Indole-3-propionic acid improved the intestinal barrier by enhancing epithelial barrier and mucus barrier. J Agric Food Chem. 2021;69(5):1487–1495. doi:10.1021/acs.jafc.0c05205.
  • Zhao ZH, Xin FZ, Xue Y, Hu Z, Han Y, Ma F, Zhou D, Liu XL, Cui A, Liu Z, et al. Indole-3-propionic acid inhibits gut dysbiosis and endotoxin leakage to attenuate steatohepatitis in rats. Exp Mol Med. 2019;51:1–14.
  • Wlodarska M, Luo C, Kolde R, d’Hennezel E, Annand JW, Heim CE, Krastel P, Schmitt EK, Omar AS, Creasey EA, et al. Indoleacrylic acid produced by commensal peptostreptococcus species suppresses inflammation. Cell Host Microbe. 2017;22(1):25–37 e6. doi:10.1016/j.chom.2017.06.007.
  • Shi J, Du P, Xie Q, Wang N, Li H, Smith EE, Li C, Liu F, Huo G, Li B, et al. Protective effects of tryptophan-catabolizing Lactobacillus plantarum KLDS 1.0386 against dextran sodium sulfate-induced colitis in mice. Food Funct. 2020;11(12):10736–10747. doi:10.1039/D0FO02622K.
  • Zihni C, Mills C, Matter K, Balda MS. Tight junctions: from simple barriers to multifunctional molecular gates. Nat Rev Mol Cell Biol. 2016;17:564–580. doi:10.1038/nrm.2016.80.
  • Yin J, Yang K, Zhou C, Xu P, Xiao W, Yang H. Aryl hydrocarbon receptor activation alleviates dextran sodium sulfate-induced colitis through enhancing the differentiation of goblet cells. Biochem Biophys Res Commun. 2019;514:180–186. doi:10.1016/j.bbrc.2019.04.136.
  • Sayin SI, Wahlstrom A, Felin J, Jantti S, Marschall HU, Bamberg K, Angelin B, Hyötyläinen T, Orešič M, Bäckhed F, et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 2013;17:225–235. doi:10.1016/j.cmet.2013.01.003.
  • Parseus A, Sommer N, Sommer F, Caesar R, Molinaro A, Stahlman M, Greiner TU, Perkins R, Bäckhed F. Microbiota-induced obesity requires farnesoid X receptor. Gut. 2017;66(3):429–437. doi:10.1136/gutjnl-2015-310283.
  • Floch MH, Binder HJ, Filburn B, Gershengoren W. The effect of bile acids on intestinal microflora. Am J Clin Nutr. 1972;25(12):1418–1426. doi:10.1093/ajcn/25.12.1418.
  • Pyo JS, Ko YS, Kang G, Kim DH, Kim WH, Lee BL, ohn JH. Bile acid induces MUC2 expression and inhibits tumor invasion in gastric carcinomas. J Cancer Res Clin Oncol. 2015;141:1181–1188. doi:10.1007/s00432-014-1890-1.
  • Lee HY, Crawley S, Hokari R, Kwon S, Kim YS. Bile acid regulates MUC2 transcription in colon cancer cells via positive EGFR/PKC/Ras/ERK/CREB, PI3K/Akt/IkappaB/NF-kappaB and p38/MSK1/CREB pathways and negative JNK/c-Jun/AP-1 pathway. Int J Oncol. 2010;36:941–953.
  • Cao H, Xu M, Dong W, Deng B, Wang S, Zhang Y, Wang S, Luo S, Wang W, Qi Y, et al. Secondary bile acid-induced dysbiosis promotes intestinal carcinogenesis. Int J Cancer. 2017;140(11):2545–2556. doi:10.1002/ijc.30643.
  • Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe. 2013;14:195–206. doi:10.1016/j.chom.2013.07.012.
  • Wang S, Dong W, Liu L, Xu M, Wang Y, Liu T, Zhang Y, Wang B, Cao H. Interplay between bile acids and the gut microbiota promotes intestinal carcinogenesis. Mol Carcinog. 2019;58(7):1155–1167. doi:10.1002/mc.22999.
  • Bakken JS, Borody T, Brandt LJ, Brill JV, Demarco DC, Franzos MA, Kelly C, Khoruts A, Louie T, Martinelli LP, et al. Treating clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol. 2011;9(12):1044–1049. doi:10.1016/j.cgh.2011.08.014.
  • Brandt LJ, Aroniadis OC. An overview of fecal microbiota transplantation: techniques, indications, and outcomes. Gastrointest Endosc. 2013;78(2):240–249. doi:10.1016/j.gie.2013.03.1329.
  • Choi HH, Cho YS. Fecal microbiota transplantation: current applications, effectiveness, and future perspectives. Clin Endosc. 2016;49:257–265. doi:10.5946/ce.2015.117.
  • Kelly CR, Khoruts A, Staley C, Sadowsky MJ, Abd M, Alani M, Bakow B, Curran P, McKenney J, Tisch A, et al. Effect of fecal microbiota transplantation on recurrence in multiply recurrent clostridium difficile infection: a randomized trial. Ann Intern Med. 2016;165:609–616. doi:10.7326/M16-0271.
  • Konturek PC, Koziel J, Dieterich W, Haziri D, Wirtz S, Glowczyk I, Konturek K, Neurath MF, Zopf Y. Successful therapy of clostridium difficile infection with fecal microbiota transplantation. J Physiol Pharmacol. 2016;67:859–866.
  • Kim KO, Schwartz MA, Lin OST, Chiorean MV, Gluck M. Reducing cost and complexity of fecal microbiota transplantation using universal donors for recurrent clostridium difficile Infection. Adv Ther. 2019;36(8):2052–2061. doi:10.1007/s12325-019-00974-x.
  • Wong SH, Zhao L, Zhang X, Nakatsu G, Han J, Xu W, Xiao X, Kwong TNY, Tsoi H, Wu WKK, et al. Gavage of fecal samples from patients with colorectal cancer promotes intestinal carcinogenesis in germ-free and conventional mice. Gastroenterology. 2017;153(6):1621–33 e6. doi:10.1053/j.gastro.2017.08.022.
  • Rosshart SP, Vassallo BG, Angeletti D, Hutchinson DS, Morgan AP, Takeda K, Hickman HD, McCulloch JA, Badger JH, Ajami NJ, et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell. 2017;171(5):1015–28 e13. doi:10.1016/j.cell.2017.09.016.
  • Cheng S, Ma X, Geng S, Jiang X, Li Y, Hu L, Li J, Wang Y, Han X. Fecal microbiota transplantation beneficially regulates intestinal mucosal autophagy and alleviates gut barrier injury. mSystems. 2018;3(5):e00137-18.
  • Li L, Li X, Zhong W, Yang M, Xu M, Sun Y, Ma J, Liu T, Song X, Dong W, et al. Corrigendum to ‘Gut microbiota from colorectal cancer patients enhances the progression of intestinal adenoma in Apc(min)(/+) mice’ [EBioMedicine 48 (2019) 301-315]. EBioMedicine. 2020;53:102680. doi:10.1016/j.ebiom.2020.102680.