Commensal bacteria-dependent indole production enhances epithelial barrier function in the colon
Open accessAbstract
Microbiota have been shown to have a great influence on functions of intestinal epithelial cells (ECs). The role of indole as a quorum-sensing (QS) molecule mediating intercellular signals in bacteria has been well appreciated. However, it remains unknown whether indole has beneficial effects on maintaining intestinal barriers in vivo. In this study, we analyzed the effect of indole on ECs using a germ free (GF) mouse model. GF mice showed decreased expression of junctional complex molecules in colonic ECs. The feces of specific pathogen-free (SPF) mice contained a high amount of indole; however the amount was significantly decreased in the feces of GF mice by 27-fold. Oral administration of indole-containing capsules resulted in increased expression of both tight junction (TJ)- and adherens junction (AJ)-associated molecules in colonic ECs in GF mice. In accordance with the increased expression of these junctional complex molecules, GF mice given indole-containing capsules showed higher resistance to dextran sodium sulfate (DSS)-induced colitis. A similar protective effect of indole on DSS-induced epithelial damage was also observed in mice bred in SPF conditions. These findings highlight the beneficial role of indole in establishing an epithelial barrier in vivo.
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Supplementation of indole capsules restored gut barrier integrity by elevating junctional protein expression in germ-free mice.
“Importantly, supplementation of indole capsules restored gut barrier integrity by elevating junctional protein expression in GF mice.90”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [90]
Indole levels in fecal samples of germ-free mice were 27-fold lower compared with conventionally raised mice.
“It was reported that indole levels in fecal samples of germ-free (GF) mice were 27-fold lower compared with conventionally raised mice.90”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [90]
Tight junction and adherens junction proteins (Cldn7, Ocln, ZO-1, E-cadherin 1) are significantly decreased in germ-free mice compared with conventionally raised mice.
“TJ and AJ proteins (Cldn7, Ocln, ZO-1, E-cadherin 1) are significantly decreased in GF mice compared with conventionally raised mice.90”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [90]
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Cites
Host-gut microbiota metabolic interactions
Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012) · Science · doi:10.1126/science.1223813 · Cited by 4,760 · see citing works
Functional interactions between the gut microbiota and host metabolism
Tremaroli, V., & Bäckhed, F. (2012) · Nature · doi:10.1038/nature11552 · Cited by 4,387 · see citing works
Intestinal mucosal barrier function in health and disease
Turner, J. R. (2009) · Nature reviews. Immunology · doi:10.1038/nri2653 · Cited by 3,952 · see citing works
Bifidobacteria can protect from enteropathogenic infection through production of acetate
Fukuda, S., Toh, H., Hase, K., Oshima, K., Nakanishi, Y., Yoshimura, K., Tobe, T., Clarke, J. M., Topping, D. L., Suzuki, T., et al. (2011) · Nature · doi:10.1038/nature09646 · Cited by 2,387 · see citing works
Immune adaptations that maintain homeostasis with the intestinal microbiota
Hooper, L. V., & Macpherson, A. J. (2010) · Nature reviews. Immunology · doi:10.1038/nri2710 · Cited by 1,455 · see citing works
Kim, M. H., Kang, S. G., Park, J. H., Yanagisawa, M., & Kim, C. H. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.04.056 · Cited by 1,127 · see citing works
Listening in on bacteria: acyl-homoserine lactone signalling
Fuqua, C., & Greenberg, E. P. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm907 · Cited by 1,081 · see citing works
Indole as an intercellular signal in microbial communities
Lee, J.-H., & Lee, J. (2010) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2009.00204.x · Cited by 1,059 · see citing works
Bacteria–host communication: the language of hormones
Sperandio, V., Torres, A. G., Jarvis, B., Nataro, J. P., & Kaper, J. B. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1537100100 · Cited by 902 · see citing works
Dextran Sodium Sulphate Colitis Mouse Model: Traps and Tricks
Perše, M., & Cerar, A. (2012) · BioMed Research International · doi:10.1155/2012/718617 · Cited by 886 · see citing works
Bansal, T., Alaniz, R. C., Wood, T. K., & Jayaraman, A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906112107 · Cited by 868 · see citing works
Inter-kingdom signalling: Communication between bacteria and their hosts
Hughes, D. T., & Sperandio, V. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1836 · Cited by 761 · see citing works
Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function
Cario, E., Gerken, G., & Podolsky, D. K. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.02.056 · Cited by 697 · see citing works
Tlaskalová-Hogenová, H., Štěpánková, R., Kozáková, H., Hudcovic, T., Vannucci, L., Tučková, L., Rossmann, P., Hrnčíř, T., Kverka, M., Zákostelská, Z., et al. (2011) · Cellular & Molecular Immunology · doi:10.1038/cmi.2010.67 · Cited by 693 · see citing works
Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells
Glass, C. K., & Saijo, K. (2010) · Nature Reviews Immunology · doi:10.1038/nri2748 · Cited by 619 · see citing works
Epithelial crosstalk at the microbiota–mucosal interface
Wells, J. M., Rossi, O., Meijerink, M., & van Baarlen, P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000092107 · Cited by 574 · see citing works
Fukata, M., Chen, A., Klepper, A. L., Krishnareddy, S., Vamadevan, A. S., Thomas, L. S., Xu, R., Inoue, H., Arditi, M., Dannenberg, A. J., et al. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.06.017 · Cited by 456 · see citing works
Blachier, F., Mariotti, F., Huneau, J. F., & Tomé, D. (2007) · Amino Acids · doi:10.1007/s00726-006-0477-9 · Cited by 452 · see citing works
Zyrek, A. A., Cichon, C., Helms, S., Enders, C., Sonnenborn, U., & Schmidt, M. A. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00836.x · Cited by 427 · see citing works
The mechanism of action of probiotics
Boirivant, M., & Strober, W. (2007) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e3282f0cffc · Cited by 379 · see citing works
Bacteria Penetrate the Inner Mucus Layer before Inflammation in the Dextran Sulfate Colitis Model
Johansson, M. E. V., Gustafsson, J. K., Sjöberg, K. E., Petersson, J., Holm, L., Sjövall, H., & Hansson, G. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012238 · Cited by 368 · see citing works
Tateda, K., Ishii, Y., Horikawa, M., Matsumoto, T., Miyairi, S., Pechère, J. C., Standiford, T. J., Ishiguro, M., & Yamaguchi, K. (2003) · Infection and Immunity · doi:10.1128/iai.71.10.5785-5793.2003 · Cited by 347 · see citing works
Resta‐Lenert, S. C., & Barrett, K. E. (2006) · Gastroenterology · doi:10.1053/j.gastro.2005.12.015 · Cited by 308 · see citing works
Indole and 7‐hydroxyindole diminish Pseudomonas aeruginosa virulence
Lee, J., Attila, C., Cirillo, S. L. G., Cirillo, J. D., & Wood, T. K. (2008) · Microbial Biotechnology · doi:10.1111/j.1751-7915.2008.00061.x · Cited by 244 · see citing works
Fujiya, M., Musch, M. W., Nakagawa, Y., Hu, S., Alverdy, J. C., Kohgo, Y., Schneewind, O., Jabrì, B., & Chang, E. B. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.05.004 · Cited by 239 · see citing works
Inflammation and Disruption of the Mucosal Architecture in Claudin-7–Deficient Mice
Ding, L., Lü, Z., Foreman, O., Tatum, R., Lu, Q., Renegar, R. H., Cao, J. P., & Chen, Y. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.10.025 · Cited by 219 · see citing works
Molecular Modulation of Intestinal Epithelial Barrier: Contribution of Microbiota
Sharma, R. R., Young, C., & Neu, J. (2010) · BioMed Research International · doi:10.1155/2010/305879 · Cited by 213 · see citing works
Lee, J., Bansal, T., Jayaraman, A., Bentley, W., & Wood, T. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00360-07 · Cited by 199 · see citing works
Identification and localization of soluble sulfotransferases in the human gastrointestinal tract
Teubner, W., Meinl, W., Florian, S., Kretzschmar, M., & Glatt, H. R. (2007) · Biochemical Journal · doi:10.1042/bj20061431 · Cited by 170 · see citing works
Dextran Sodium Sulfate-Induced Colitis in Germ-Free IQI/Jic Mice.
Kitajima, S., MORIMOTO, M., Sagara, E., SHIMIZU, C., & IKEDA, Y. (2001) · EXPERIMENTAL ANIMALS · doi:10.1538/expanim.50.387 · Cited by 168 · see citing works
Hepatic microsomal metabolism of indole to indoxyl, a precursor of indoxyl sulfate
Banoğlu, E., Jha, G. G., & King, R. J. (2001) · European Journal of Drug Metabolism and Pharmacokinetics · doi:10.1007/bf03226377 · Cited by 153 · see citing works
Li, N., & Neu, J. (2009) · Journal of Nutrition · doi:10.3945/jn.108.101485 · Cited by 121 · see citing works
Taki, K., Takayama, F., & Niwa, T. (2005) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2004.09.028 · Cited by 108 · see citing works
Sulfation of indoxyl by human and rat aryl (phenol) sulfotransferases to form indoxyl sulfate
Banoğlu, E., & King, R. S. (2002) · European Journal of Drug Metabolism and Pharmacokinetics · doi:10.1007/bf03190428 · Cited by 103 · see citing works
Chen, J., Xiao, L., Rao, J. N., Zou, T., Liu, L., Bellavance, E. C., Gorospe, M., & Wang, J. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-02-0175 · Cited by 80 · see citing works
SMITH, P. F., Siddharth, J., Pearson, R., Holway, N., Shaxted, M., Butler, M., Clark, N., Jamontt, J., Watson, R. P., Sanmugalingam, D., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030273 · Cited by 52 · see citing works
Occludin Is a Direct Target of Thyroid Transcription Factor-1 (TTF-1/NKX2–1)
Runkle, E. A., Rice, S. J., Qi, J., Masser, D. R., Antonetti, D. A., Winslow, M. M., & Mu, D. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.367987 · Cited by 49 · see citing works
Detection of possible AI-2-mediated quorum sensing system in commensal intestinal bacteria
Lukáš, F., GORENC, G., & Kopečný, J. (2008) · Folia Microbiologica · doi:10.1007/s12223-008-0030-1 · Cited by 44 · see citing works
Kohno, Y., Okamoto, T., Ishibe, T., Nagayama, S., Shima, Y., Nishijo, K., Shibata, K. R., Fukiage, K., Otsuka, S., Uejima, D., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m608389200 · Cited by 36 · see citing works
Induction of cyp2e-1 protein in mouse colon
Rosenberg, D. W., & Mankowski, D. C. (1994) · Carcinogenesis · doi:10.1093/carcin/15.1.73 · Cited by 32 · see citing works
Modulations of Food-derived Substances on Intestinal Permeability in Caco-2 Cell Monolayers
KONISHI, Y. (2003) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.67.2297 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Gut microbiota in human metabolic health and disease
Fan, Y., & Pedersen, O. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0433-9 · Cited by 4,724 · see citing works
Microbial tryptophan catabolites in health and disease
Roager, H. M., & Licht, T. R. (2018) · Nature Communications · doi:10.1038/s41467-018-05470-4 · Cited by 2,236 · see citing works
Impact of the Gut Microbiota on Intestinal Immunity Mediated by Tryptophan Metabolism
Gao, J., Xu, K., Liu, H., Liu, G., Bai, M., Peng, C., Li, T., & Yin, Y. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00013 · Cited by 1,313 · see citing works
Gut microbiota–generated metabolites in animal health and disease
Lee, W.-J., & Hase, K. (2014) · Nature Chemical Biology · doi:10.1038/nchembio.1535 · Cited by 756 · see citing works
Regulation of Intestinal Barrier Function by Microbial Metabolites
Ghosh, S., Whitley, C. S., Haribabu, B., & Jala, V. R. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.02.007 · Cited by 835 · see citing works
Interaction Between the Microbiota, Epithelia, and Immune Cells in the Intestine
Kayama, H., Okumura, R., & Takeda, K. (2020) · Annual Review of Immunology · doi:10.1146/annurev-immunol-070119-115104 · Cited by 765 · see citing works
Roles of intestinal epithelial cells in the maintenance of gut homeostasis
Okumura, R., & Takeda, K. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.20 · Cited by 712 · see citing works
Microbial tryptophan metabolites regulate gut barrier function via the aryl hydrocarbon receptor
Scott, S. A., Fu, J., & Chang, P. V. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2000047117 · Cited by 696 · see citing works
Role of intestinal microbiota and metabolites on gut homeostasis and human diseases
Lin, L., & Zhang, J. (2017) · BMC Immunology · doi:10.1186/s12865-016-0187-3 · Cited by 731 · see citing works
Alexeev, E. E., Lanis, J. M., Kao, D. J., Campbell, E. L., Kelly, C. J., Battista, K. D., Gerich, M. E., Jenkins, B. R., Walk, S. T., Kominsky, D. J., et al. (2018) · The American Journal of Pathology · doi:10.1016/j.ajpath.2018.01.011 · Cited by 532 · see citing works
Roles of indole as an interspecies and interkingdom signaling molecule
Lee, J.-H., Wood, T. K., & Lee, J. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.08.001 · Cited by 516 · see citing works
Effects of Psychological, Environmental and Physical Stressors on the Gut Microbiota
Karl, J. P., Hatch‐McChesney, A., Arcidiacono, S. M., Pearce, S., Pantoja-Feliciano, I. G., Doherty, L. A., & Soares, J. W. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02013 · Cited by 535 · see citing works
Zhang, L., & Davies, S. S. (2016) · Genome Medicine · doi:10.1186/s13073-016-0296-x · Cited by 499 · see citing works
Surface components and metabolites of probiotics for regulation of intestinal epithelial barrier
Liu, Q., Yu, Z., Tian, F., Zhao, J., Zhang, H., Zhai, Q., & Chen, W. (2020) · Microbial Cell Factories · doi:10.1186/s12934-020-1289-4 · Cited by 438 · see citing works
Precision Nutrition and the Microbiome, Part I: Current State of the Science
Mills, S., Stanton, C., Lane, J. A., Smith, G., & Ross, R. P. (2019) · Nutrients · doi:10.3390/nu11040923 · Cited by 406 · see citing works
Adaptation of the human aryl hydrocarbon receptor to sense microbiota-derived indoles
Hubbard, T. D., Murray, I. A., Bisson, W. H., Lahoti, T. S., Gowda, K., Amin, S. G., Patterson, A. D., & Perdew, G. H. (2015) · Scientific Reports · doi:10.1038/srep12689 · Cited by 377 · see citing works
Thomas, S., Izard, J., Walsh, E. K., Batich, K. A., Chongsathidkiet, P., Clarke, G. A., Sela, D. A., Muller, A. J., Mullin, J. M., Albert, K., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2929 · Cited by 369 · see citing works
Maintenance of intestinal homeostasis by mucosal barriers
Okumura, R., & Takeda, K. (2018) · Inflammation and Regeneration · doi:10.1186/s41232-018-0063-z · Cited by 368 · see citing works
Aburto, M. R., & Cryan, J. F. (2024) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-023-00890-0 · Cited by 391 · see citing works
Xu, X., Poulsen, K. L., Wu, L., Liu, S., Miyata, T., Song, Q., Wei, Q., Zhao, C., Lin, C., & Yang, J. B. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01119-3 · Cited by 370 · see citing works
Gut Microbiota Metabolites in NAFLD Pathogenesis and Therapeutic Implications
Chen, J., & Vitetta, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155214 · Cited by 357 · see citing works
Zhao, Z., Xin, F., Xue, Y., Hu, Z., Han, Y., Ma, F., Zhou, D., Liu, X., Cui, A., Liu, Z., et al. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0304-5 · Cited by 353 · see citing works
The impact of the microbiota-gut-brain axis on Alzheimer’s disease pathophysiology
Doifode, T., Giridharan, V. V., Generoso, J. S., Bhatti, G., Collodel, A., Schulz, P. E., Forlenza, O. V., & Barichello, T. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2020.105314 · Cited by 347 · see citing works
The Impact of CKD on Uremic Toxins and Gut Microbiota
Rysz, J., Franczyk, B., Ławiński, J., Olszewski, R., Ciałkowska-Rysz, A. D., & Gluba-Brzózka, A. (2021) · Toxins · doi:10.3390/toxins13040252 · Cited by 314 · see citing works
Modulation of a Circulating Uremic Solute via Rational Genetic Manipulation of the Gut Microbiota
Devlin, A. S., Marcobal, A. M., Dodd, D., Nayfach, S., Plummer, N. S., Meyer, T., Pollard, K. S., Sonnenburg, J. L., & Fischbach, M. A. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.10.021 · Cited by 300 · see citing works
Dual Role of Indoles Derived From Intestinal Microbiota on Human Health
Ye, X., Li, H., Anjum, K., Zhong, X., Miao, S., Zheng, G., Liu, W., & Li, L. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.903526 · Cited by 282 · see citing works
Beaumont, M., Portune, K. J., Steuer, N., Lan, A., Cerrudo, V., Audebert, M., Dumont, F., Mancano, G., Khodorova, N., Andriamihaja, M., et al. (2017) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.117.158816 · Cited by 250 · see citing works
Lactobacillus and intestinal diseases: Mechanisms of action and clinical applications
Huang, R., Wu, F. L., Zhou, Q., Wei, W., Juan, Y., Xiao, B., & Luo, Z. (2022) · Microbiological Research · doi:10.1016/j.micres.2022.127019 · Cited by 258 · see citing works
Prediction and quantification of bioactive microbiota metabolites in the mouse gut
Sridharan, G. V., Choi, K., Klemashevich, C. L., Wu, C., Prabakaran, D., Pan, L. B., Steinmeyer, S. H., Mueller, C., Yousofshahi, M., Alaniz, R. C., et al. (2014) · Nature Communications · doi:10.1038/ncomms6492 · Cited by 247 · see citing works
Rose, E. C., Odle, J., Blikslager, A. T., & Ziegler, A. L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136729 · Cited by 253 · see citing works
New Insights Into Gut-Bacteria-Derived Indole and Its Derivatives in Intestinal and Liver Diseases
Li, X., Zhang, B., Hu, Y., & Zhao, Y. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.769501 · Cited by 235 · see citing works
Multidrug Efflux Pumps at the Crossroad between Antibiotic Resistance and Bacterial Virulence
Alcalde‐Rico, M., Hernando‐Amado, S., Blanco, P., & Martínez, J. L. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01483 · Cited by 224 · see citing works
Hou, Y., Li, J., & Ying, S. (2023) · Metabolites · doi:10.3390/metabo13111166 · Cited by 225 · see citing works
Bosi, A., Banfi, D., Bistoletti, M., Giaroni, C., & Baj, A. (2020) · International Journal of Tryptophan Research · doi:10.1177/1178646920928984 · Cited by 221 · see citing works
Dietary effects of soybean products on gut microbiota and immunity of aquatic animals: A review
Zhou, Z., Ringø, E., Olsen, R. E., & Song, S. K. (2017) · Aquaculture Nutrition · doi:10.1111/anu.12532 · Cited by 216 · see citing works
Gryp, T., Paepe, K. D., Vanholder, R. C., Kerckhof, F., Biesen, W. V., de Wiele, T. V., Verbeke, F., Speeckaert, M. M., Joossens, M., Couttenye, M. M., et al. (2020) · Kidney International · doi:10.1016/j.kint.2020.01.028 · Cited by 212 · see citing works
Characterization of the 17 strains of regulatory T cell-inducing human-derived Clostridia
Narushima, S., Sugiura, Y., Oshima, K., Atarashi, K., Hattori, M., Suematsu, M., & Honda, K. (2014) · Gut Microbes · doi:10.4161/gmic.28572 · Cited by 210 · see citing works
Microbial-derived metabolites as a risk factor of age-related cognitive decline and dementia
Connell, E., Le Gall, G., Pontifex, M. G., Sami, S., Cryan, J. F., Clarke, G., Müller, M., & Vauzour, D. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00548-6 · Cited by 208 · see citing works
The gut microbiota metabolite indole alleviates liver inflammation in mice
Beaumont, M., Neyrinck, A. M., Olivares, M., Rodriguez, J., Nédélec, A., Roumain, M., Bindels, L. B., Cani, P. D., Evenepoel, P., Muccioli, G. G., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201800544 · Cited by 208 · see citing works
Indoles from commensal bacteria extend healthspan
Sonowal, R., Swimm, A., Sahoo, A., Luo, L., Matsunaga, Y., Wu, Z., Bhingarde, J. A., Ejzak, E. A., Ranawade, A., Qadota, H., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1706464114 · Cited by 197 · see citing works
Hendrikx, T., & Schnabl, B. (2019) · Journal of Internal Medicine · doi:10.1111/joim.12892 · Cited by 202 · see citing works
Zhang, Y., Chen, R., Zhang, D., Qi, S., & Liu, Y. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114295 · Cited by 209 · see citing works
Deciphering the Chemical Lexicon of Host–Gut Microbiota Interactions
Nicolas, G. R., & Chang, P. V. (2019) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2019.04.006 · Cited by 195 · see citing works
Gut microbiota bridges dietary nutrients and host immunity
Fan, L., Xia, Y., Wang, Y., Han, D., Liu, Y., Li, J., Fu, J., Wang, L., Gan, Z., Liu, B., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2346-1 · Cited by 197 · see citing works
The "Gut Feeling": Breaking Down the Role of Gut Microbiome in Multiple Sclerosis
Freedman, S. N., Shahi, S. K., & Mangalam, A. K. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0588-x · Cited by 168 · see citing works
Gilbert, M. S., Ijssennagger, N., Kies, A. K., & van Mil, S. W. C. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00319.2017 · Cited by 189 · see citing works
Espi, M., Koppe, L., Fouque, D. P., & Thaunat, O. (2020) · Toxins · doi:10.3390/toxins12050300 · Cited by 182 · see citing works
Swimm, A. I., Giver, C. R., DeFilipp, Z. M., Rangaraju, S., Sharma, A., Antonova, A. U., Sonowal, R., Capaldo, C., Powell, D. N., Qayed, M. D., et al. (2018) · Blood · doi:10.1182/blood-2018-03-838193 · Cited by 174 · see citing works
Zheng, Z., & Wang, B. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.775526 · Cited by 168 · see citing works
Cason, C. A., Dolan, K. T., Sharma, G., Tao, M., Kulkarni, R. N., Helenowski, I., Doane, B. M., Avram, M. J., McDermott, M. M., Chang, E. B., et al. (2017) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2017.09.029 · Cited by 165 · see citing works
Bacterial Quorum-Sensing Systems and Their Role in Intestinal Bacteria-Host Crosstalk
Wu, L., & Luo, Y. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.611413 · Cited by 163 · see citing works
Parasitic Protozoa and Interactions with the Host Intestinal Microbiota
Burgess, S. L., Gilchrist, C. A., Lynn, T. C., & Petri, W. A. (2017) · Infection and Immunity · doi:10.1128/iai.00101-17 · Cited by 156 · see citing works
Ala, M. (2021) · International Reviews of Immunology · doi:10.1080/08830185.2021.1954638 · Cited by 162 · see citing works
Tennoune, N., Andriamihaja, M., & Blachier, F. (2022) · Microorganisms · doi:10.3390/microorganisms10050930 · Cited by 159 · see citing works
Whitfield-Cargile, C., Cohen, N. D., Chapkin, R. S., Weeks, B. R., Davidson, L. A., Goldsby, J. S., Hunt, C. L., Steinmeyer, S. H., Menon, R., Suchodolski, J. S., et al. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1156827 · Cited by 146 · see citing works
He, M. R., Li, X., Poolsawat, L., Guo, Z., Yao, W., Zhang, C., & Leng, X. (2020) · Aquaculture Nutrition · doi:10.1111/anu.13064 · Cited by 145 · see citing works
Valenzano, M., Diguilio, K., Mercado, J. M., Teter, M., To, J., Ferraro, B., Mixson, B., Manley, I., Baker, V., Moore, B., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0133926 · Cited by 129 · see citing works
Microbial metabolites in health and disease: Navigating the unknown in search of function
Martinez, K., Leone, V., & Chang, E. B. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.r116.752899 · Cited by 132 · see citing works
Ding, Y., Yanagi, K., Cheng, C., Alaniz, R. C., Lee, K., & Jayaraman, A. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.01.029 · Cited by 122 · see citing works
Gut microbiota-motility interregulation: insights from in vivo, ex vivo and in silico studies
Waclawiková, B., Codutti, A., Alim, K., & Aidy, S. E. (2022) · Gut Microbes · doi:10.1080/19490976.2021.1997296 · Cited by 129 · see citing works
Blachier, F., Beaumont, M., Portune, K. J., Steuer, N., Lan, A., Audebert, M., Khodorova, N., Andriamihaja, M., Airinei, G., Benamouzig, R., et al. (2019) · Clinical Nutrition · doi:10.1016/j.clnu.2018.09.016 · Cited by 124 · see citing works
Vasquez, R., Oh, J. K., Song, J. H., & Kang, D. (2022) · Journal of Animal Science and Technology · doi:10.5187/jast.2022.e58 · Cited by 124 · see citing works
Microbiomes in respiratory health and disease: An Asia‐Pacific perspective
Chotirmall, S. H., Gellatly, S. L., Budden, K. F., Aogáin, M. M., Shukla, S. D., Wood, D., Hugenholtz, P., Pethe, K., & Hansbro, P. M. (2017) · Respirology · doi:10.1111/resp.12971 · Cited by 122 · see citing works
Dietary protein and the intestinal microbiota: An understudied relationship
Bartlett, A., & Kleiner, M. (2022) · iScience · doi:10.1016/j.isci.2022.105313 · Cited by 124 · see citing works
Gryp, T., Huys, G. R. B., Joossens, M., Biesen, W. V., Glorieux, G., & Vaneechoutte, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21061986 · Cited by 122 · see citing works
Volatiles in Inter-Specific Bacterial Interactions
Tyc, O., Zweers, H., de Boer, W., & Garbeva, P. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01412 · Cited by 115 · see citing works
Combatting bacterial persister cells
Wood, T. K. (2015) · Biotechnology and Bioengineering · doi:10.1002/bit.25721 · Cited by 114 · see citing works
Microbiota and cancer: host cellular mechanisms activated by gut microbial metabolites
Tsvetikova, S. A., & Koshel, E. I. (2020) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2020.151425 · Cited by 111 · see citing works
Greathouse, K. L., & Wyatt, M. (2021) · Nutrients · doi:10.3390/nu13041189 · Cited by 111 · see citing works
Diverse roles of microbial indole compounds in eukaryotic systems
Kumar, P., Lee, J., & Lee, J. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12765 · Cited by 112 · see citing works
Amino Acid Trp: The Far Out Impacts of Host and Commensal Tryptophan Metabolism
Grifka‐Walk, H. M., Jenkins, B. R., & Kominsky, D. J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.653208 · Cited by 112 · see citing works
Cukrowská, B., Sowińska, A., Bierła, J. B., Czarnowska, E., Rybak, A., & Grzybowska‐Chlebowczyk, U. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i42.7505 · Cited by 111 · see citing works
Interactions between Intestinal Microflora/Probiotics and the Immune System
Zhang, C., Wang, H., & Chen, T. (2019) · BioMed Research International · doi:10.1155/2019/6764919 · Cited by 103 · see citing works
Munawar, N., Ahsan, K., Muhammad, K., Ahmad, A., Anwar, M. A., Shah, I., Ameri, A. A., & Mughairbi, F. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147671 · Cited by 105 · see citing works
Mamic, P., Chaikijurajai, T., & Tang, W. H. W. (2020) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2020.12.001 · Cited by 99 · see citing works
Okumura, R., & Takeda, K. (2024) · Seminars in Immunopathology · doi:10.1007/s00281-024-01026-5 · Cited by 100 · see citing works
Amino Acids in Intestinal Physiology and Health
Beaumont, M., & Blachier, F. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-45328-2_1 · Cited by 98 · see citing works
Dietary and Microbial Determinants in Food Allergy
Victor, E. S., Crestani, E., & Chatila, T. A. (2020) · Immunity · doi:10.1016/j.immuni.2020.07.025 · Cited by 98 · see citing works
Liu, D., Zhang, S., Li, S., Zhang, Q., Cai, Y., Li, P., Li, H., Shen, B., Liao, Q., Hong, Y., et al. (2023) · BMC Biology · doi:10.1186/s12915-023-01578-2 · Cited by 97 · see citing works
Chen, M., Liu, Y., Xiong, S., Wu, M., Li, B., Ruan, Z., & Hu, X. (2019) · Food & Function · doi:10.1039/c9fo00123a · Cited by 95 · see citing works
Modulation of immunity by tryptophan microbial metabolites
Li, S. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1209613 · Cited by 101 · see citing works
Fungi as Part of the Microbiota and Interactions with Intestinal Bacteria
Kapitan, M., Niemiec, M. J., Steimle, A., Frick, J.-S., & Jacobsen, I. D. (2018) · Current topics in microbiology and immunology · doi:10.1007/82_2018_117 · Cited by 93 · see citing works
Díez-Sainz, E., Lorente‐Cebrián, S., Aranaz, P., Riezu‐Boj, J. I., Martínez, J. A., & Milagro, F. I. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.586564 · Cited by 92 · see citing works
Hu, J. P., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Microbiome · doi:10.1186/s40168-023-01551-9 · Cited by 92 · see citing works
Molecular Mechanisms of Microbiota-Mediated Pathology in Irritable Bowel Syndrome
Mishima, Y., & Ishihara, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228664 · Cited by 89 · see citing works
Persistent Persister Misperceptions
Kim, J., & Wood, T. K. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02134 · Cited by 84 · see citing works
Biochemical Features of Beneficial Microbes: Foundations for Therapeutic Microbiology
Engevik, M. A., & Versalovic, J. A. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.bad-0012-2016 · Cited by 85 · see citing works
Metabolic and functional interplay between gut microbiota and fat-soluble vitamins
Stacchiotti, V., Rezzi, S., Eggersdorfer, M. L., & Galli, F. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1793728 · Cited by 83 · see citing works
Targeting gut barrier dysfunction with phytotherapies: Effective strategy against chronic diseases
Dey, P. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105135 · Cited by 86 · see citing works
Current evidence linking diet to gut microbiota and brain development and function
Ceppa, F., Mancini, A., & Tuohy, K. M. (2018) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637486.2018.1462309 · Cited by 82 · see citing works
Vidal-Lletjós, S., Beaumont, M., Tomé, D., Benamouzig, R., Blachier, F., & Lan, A. (2017) · Nutrients · doi:10.3390/nu9030310 · Cited by 84 · see citing works
Darkoh, C., Plants-Paris, K., Bishoff, D. E., & DuPont, H. L. (2019) · mSystems · doi:10.1128/msystems.00346-18 · Cited by 81 · see citing works
Age-dependent remodeling of gut microbiome and host serum metabolome in mice
Wu, C., Muthyala, S. D. V., Klemashevich, C. L., Ufondu, A., Menon, R., Chen, Z., Devaraj, S., Jayaraman, A., & Sun, Y. (2021) · Aging · doi:10.18632/aging.202525 · Cited by 80 · see citing works
Fecal Indole as a Biomarker of Susceptibility to Cryptosporidium Infection
Chappell, C. L., Darkoh, C., Shimmin, L. C., Farhana, N., Kim, D.-K., Okhuysen, P. C., & Hixson, J. E. (2016) · Infection and Immunity · doi:10.1128/iai.00336-16 · Cited by 79 · see citing works
Shehata, A. M., Paswan, V. K., Attia, Y. A., Abdel‐Moneim, A. E., Abougabal, M. S., Sharaf, M., ElMazoudy, R. H., Alghafari, W. T., Osman, M. A., Farag, M. R., et al. (2021) · Animals · doi:10.3390/ani11123491 · Cited by 78 · see citing works
Microbial Tryptophan Metabolism Tunes Host Immunity, Metabolism, and Extraintestinal Disorders
Liu, M., Nieuwdorp, M., de Vos, W. M., & Rampanelli, E. (2022) · Metabolites · doi:10.3390/metabo12090834 · Cited by 83 · see citing works
Gut-microbiota derived bioactive metabolites and their functions in host physiology
Debnath, N., Kumar, R., Kumar, A., Mehta, P. K., & Yadav, A. K. (2021) · Biotechnology and Genetic Engineering Reviews · doi:10.1080/02648725.2021.1989847 · Cited by 77 · see citing works
The role of the microbiome in gastrointestinal inflammation
Sanders, D. J., Inniss, S., Sebepos‐Rogers, G., Rahman, F. Z., & Smith, A. M. (2021) · Bioscience Reports · doi:10.1042/bsr20203850 · Cited by 78 · see citing works
The tryptophan metabolic pathway of the microbiome and host cells in health and disease
Miyamoto, K., Sujino, T., & Kanai∥, T. (2024) · International Immunology · doi:10.1093/intimm/dxae035 · Cited by 81 · see citing works
- Authors
- Shimada, Y., Kinoshita, M., Harada, K., Mizutani, M., Masahata, K., Kayama, H., & Takeda, K.
- Affiliations
- Immunology Frontier Research Center, The University of Osaka (JP)
- Japan Science and Technology Agency (JP)
- The University of Osaka (JP)
- Morishita Jintan (Japan) (JP)
- Corresponding author
- Takeda, Kiyoshi
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-11-20
- Volume
- 8
- Issue
- 11
- Pages
- e80604
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3835565
- OpenAlex
- W2040501063
- Cited by
- 404
- References
- 41
- Citations by year
- 2026: 23 · 2025: 43 · 2024: 50 · 2023: 53 · 2022: 44 · 2021: 47 · 2020: 34 · 2019: 27 · 2018: 24 · 2017: 23 · 2016: 15 · 2015: 15 · 2014: 6
- FWCI
- 5.37
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- Ministry of Health, Labour and Welfare
- Japan Society for the Promotion of Science (24390120)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- indole, commensal bacteria, intestinal epithelial barrier, tight junctions, adherens junctions, quorum sensing, germ-free mice, DSS-induced colitis, colonic epithelial cells, gut microbiota, epithelial permeability
- MeSH terms
- Animals, Bacteria, Chromatography, High Pressure Liquid, Colon, Germ-Free Life, Indoles, Intestinal Mucosa, Mice, Tandem Mass Spectrometry, Real-Time Polymerase Chain Reaction
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