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Bile Acid Modifications at the Microbe-Host Interface: Potential for Nutraceutical and Pharmaceutical Interventions in Host Health
Open accessAbstract
Bile acids have emerged as important signaling molecules in the host, as they interact either locally or systemically with specific cellular receptors, in particular the farnesoid X receptor (FXR) and TGR5. These signaling functions influence systemic lipid and cholesterol metabolism, energy metabolism, immune homeostasis, and intestinal electrolyte balance. Through defined enzymatic activities, the gut microbiota can significantly modify the signaling properties of bile acids and therefore can have an impact upon host health. Alterations to the gut microbiota that influence bile acid metabolism are associated with metabolic disease, obesity, diarrhea, inflammatory bowel disease (IBD), Clostridium difficile infection, colorectal cancer, and hepatocellular carcinoma. Here, we examine the regulation of this gut-microbiota-liver axis in the context of bile acid metabolism and indicate how this pathway represents an important target for the development of new nutraceutical (diet and/or probiotics) and targeted pharmaceutical interventions.
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“Furthermore, Blautia and Bifidobacterium species are involved in the transformation of host bile.”
From Microbiota-related Changes in Bile Acid & Tryptophan Metabolism are Associated with Gastrointestinal Dysfunction in a Mouse Model of Autism (2017) · cites this paper as Joyce and Gahan, 2016
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In the citing paper
“The expansion of microbial BSH activity has increased the diversity of bile acids in the host (Joyce and Gahan, 2016).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Joyce and Gahan, 2016
Experimental — accuracy not yet measuredIn the citing paper
“Microbially derived secondary bile acids are hypothesized to be interkingdom signaling molecules due to their ability to influence the composition and function of the gut microbiota as well as host physiology (407, 408).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [408]
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“Bile that is not re-absorbed in terminal small intestine undergoes further transformation by the intestinal microbiota (Joyce and Gahan, 2016).”
From Microbiota-related Changes in Bile Acid & Tryptophan Metabolism are Associated with Gastrointestinal Dysfunction in a Mouse Model of Autism (2017) · cites this paper as Joyce and Gahan, 2016
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“Primary bile acids are synthesized in the liver, and subsequently combined to glycine or taurine to create conjugated primary bile acids (Joyce and Gahan, 2016).”
BackgroundFeng, X., Chen, M., Song, H., Ma, S., Ou, C., Li, Z., Hu, H., Yang, Y., Zhou, S., Pan, Y., et al. (2023) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.13254 · Cited by 68
Bile acids at the cross-roads of gut microbiome–host cardiometabolic interactions
Ryan, P. M., Stanton, C., & Caplice, N. M. (2017) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-017-0299-9 · Cited by 70
“The significance of bile acids, of intestinal and hepatic origin, as paracrine and endocrine signaling molecules with systemic reach has only recently been highlighted [17].”
BackgroundBourrie, B. C. T., Cotter, P. D., & Willing, B. P. (2018) · Journal of Functional Foods · doi:10.1016/j.jff.2018.04.039 · Cited by 64
Nithya, A., Misra, S., Panigrahi, C., Dalbhagat, C. G., & Mishra, H. N. (2023) · Food Chemistry Advances · doi:10.1016/j.focha.2023.100381 · Cited by 67
Xu, Y., Jing, H., Wang, J., Zhang, S., Chang, Q., Li, Z., Wu, X., & Zhang, Z. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.800604 · Cited by 65
“Decreased Diversity and Disturbed Composition of Gut Microbiota in Post-cholecystectomy Diarrhea Patients Due to anatomic and dynamic reasons, the unabsorbed bile acids have a great impact to the microbial community, so sequencing flowing bile acids to intestine needs to be emphasized (Joyce and Gahan, 2016).”
BackgroundMicrobiota-Mitochondria Inter-Talk: A Potential Therapeutic Strategy in Obesity and Type 2 Diabetes
Vezza, T., Abad‐Jiménez, Z., Martí‐Cabrera, M., Rocha, M., & Víctor, V. M. (2020) · Antioxidants · doi:10.3390/antiox9090848 · Cited by 61
The Gut Microbiota during a Behavioral Weight Loss Intervention
Stanislawski, M. A., Frank, D. N., Borengasser, S. J., Ostendorf, D. M., Ir, D., Jambal, P., Bing, K., Wayland, L. T., Siebert, J., Bessesen, D. H., et al. (2021) · Nutrients · doi:10.3390/nu13093248 · Cited by 62
“This suggests that the gut microbiota community structure may influence responsiveness to weight loss efforts, which is critical to understand more fully, as gut microbiota profiles are alterable through various means, such as probiotics/prebiotics [13], personalized dietary changes [86] or targeting gut microbiota pa…”
BackgroundPreventive and therapeutic aspects of fermented foods
Baruah, R., Ray, M., & Halami, P. M. (2022) · Journal of Applied Microbiology · doi:10.1111/jam.15444 · Cited by 60
“The therapeutic effect of microbial enzymes such as bile- salt hydrolase has been reported to influence systemic lipid and cholesterol metabolism, energy metabolism, immune homeostasis and intestinal electrolyte balance (Joyce & Gahan, 2016).”
BackgroundVincenzo, F. D., Puca, P., Lopetuso, L. R., Petito, V., Masi, L., Bartocci, B., Murgiano, M., Felice, M. D., Petronio, L., Gasbarrini, A., et al. (2022) · Nutrients · doi:10.3390/nu14132664 · Cited by 63
Production of New Microbially Conjugated Bile Acids by Human Gut Microbiota
García, C. J., Kosek, V., Beltrán, D., Tomás-Barberán, F. A., & Hajšlová, J. (2022) · Biomolecules · doi:10.3390/biom12050687 · Cited by 56
“Therefore, these signaling functions could affect the health of the host [6].”
BackgroundBile acids: Key players in inflammatory bowel diseases?
Kriaa, A., Mariaule, V., Jablaoui, A., Rhimi, S., Mkaouar, H., Hernandez, J., Korkmaz, B., Lesner, A., Maguin, E., Aghdassi, A., et al. (2022) · Cells · doi:10.3390/cells11050901 · Cited by 53
“Unabsorbed BAs (5%) that escape the enterohepatic circulation are further metabolized by the gut microbiota [18,21,22] (Figure 1).”
BackgroundSong, M., Zhang, F., Chen, L., Yang, Q., Su, H., Yang, X., He, H., Ling, M., Zheng, J., Duan, C., et al. (2021) · Animal nutrition · doi:10.1016/j.aninu.2020.07.011 · Cited by 53
Regulation of gut microbiota-bile acids axis by probiotics in inflammatory bowel disease
Li, L., Liu, T., Gu, Y., Wang, X., Xie, R., Sun, Y., Wang, B., & Cao, H. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.974305 · Cited by 52
“The synthesis andmetabolism of BAs are prominentlymodified by gut bacteriawithdiverse enzymes (22).”
BackgroundGut microbiota: a promising target against cardiometabolic diseases
Warmbrunn, M. V., Herrema, H., Aron‐Wisnewsky, J., Soeters, M. R., van Raalte, D. H., & Nieuwdorp, M. (2020) · Expert Review of Endocrinology & Metabolism · doi:10.1080/17446651.2020.1720511 · Cited by 49
Lu, Q., Chen, J., Jiang, L., Geng, T., Tian, S., Liao, Y., YANG, K. Y., Zheng, Y., He, M., Tang, H., et al. (2023) · American Journal of Clinical Nutrition · doi:10.1016/j.ajcnut.2023.08.023 · Cited by 47
Influence of nutrition therapy on the intestinal microbiome
Krezalek, M. A., Yeh, A., Alverdy, J. C., & Morowitz, M. J. (2016) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000348 · Cited by 47
Ursolic acid alleviates hypercholesterolemia and modulates the gut microbiota in hamsters
Hao, W., Kwek, E., He, Z., Zhu, H., Liu, J., Zhao, Y., Ma, K. Y., He, W., & Chen, Z. (2020) · Food & Function · doi:10.1039/d0fo00829j · Cited by 44
García-Gutiérrez, E., O’Mahony, A. K., dos Santos, R. S., Marroquí, L., & Cotter, P. D. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2401654 · Cited by 43
“139 Bile acid concentrations and profiles are considered influential in health and disease, with certain bile acids capable of activating host receptors and influencing glucose homeostasis, such as the farnesoid X receptor 140 and the G-protein-coupled receptor TGR5.”
BackgroundFunctional and Phylogenetic Diversity of BSH and PVA Enzymes
Daly, J. W., Keely, S. J., & Gahan, C. G. M. (2021) · Microorganisms · doi:10.3390/microorganisms9040732 · Cited by 40
Self-citationWei, D., Li, Y., Che, M., Li, C., Wu, Q., & Sun, C. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04412-0 · Cited by 41
High-cholesterol diet does not alter gut microbiota composition in mice
Dimova, L. G., Zlatkov, N., Verkade, H. J., Uhlin, B. E., & Tietge, U. J. F. (2017) · Nutrition & Metabolism · doi:10.1186/s12986-017-0170-x · Cited by 39
“In the large intestine unabsorbed bile acids are first deconjugated by the bacterial enzyme bile salt hydrolase; next they are dehydroxylated by bacteria to form the secondary bile acids [26].”
BackgroundJames, C. S., Fraser, K., Young, W., McNabb, W. C., & Roy, N. C. (2019) · Journal of Nutrition · doi:10.1093/jn/nxz302 · Cited by 41
“Five percent of BAs escape this process and undergo modification by microorganisms with the 7α-dehdroxylase enzyme, resulting in secondary BAs with altered structures that may interact differently with cellular receptors, potentially having impacts on the functionality of metabolites (13).”
BackgroundMicrobiota and metabolites in rheumatic diseases
Tong, Y., Marion, T. N., Schett, G. A., Luo, Y., & Liu, Y. (2020) · Autoimmunity Reviews · doi:10.1016/j.autrev.2020.102530 · Cited by 40
Emerging Role of Diet and Microbiota Interactions in Neuroinflammation
Janakiraman, M., & Krishnamoorthy, G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02067 · Cited by 39
Zhang, Y., Gu, Y., Jiang, J., Cui, X., Cheng, S., Liu, L., Huang, Z., Liao, R., Zhao, P., Yu, J.-Y., et al. (2022) · npj Science of Food · doi:10.1038/s41538-022-00156-0 · Cited by 40
Wang, A., Dongcheng, C., Zhang, H., Li, Q., Yan, Z., Qiu, Y., Xu, H., & Keji, C. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.02.018 · Cited by 37
James, S. C., Fraser, K., Young, W., Heenan, P. E., Gearry, R. B., Keenan, J. I., Talley, N. J., Joyce, S. A., McNabb, W. C., & Roy, N. C. (2021) · Metabolites · doi:10.3390/metabo11090612 · Cited by 38
“Primary bile acids are conjugated to either glycine or taurine and stored in the gallbladder [2,4].”
BackgroundInfluentialSelf-citationGhaffarzadegan, T., Marungruang, N., Fåk, F., & NYMAN, M. E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157427 · Cited by 36
“When a meal is consumed, BAs are secreted from hepatocytes and are absorbed in the duodenum by passive diffusion, or are actively transported from the terminal ileum to the liver via the portal vein to complete enterohepatic recirculation [1].”
BackgroundGut Microbiota Metabolites: Unveiling Their Role in Inflammatory Bowel Diseases and Fibrosis
Bernardi, F., D’Amico, F., Bencardino, S., Faggiani, I., Fanizza, J., Zilli, A., Parigi, T. L., Allocca, M., Danese, S., & Furfaro, F. (2024) · Pharmaceuticals · doi:10.3390/ph17030347 · Cited by 39
Gut–Brain Axis: Focus on Sex Differences in Neuroinflammation
Caldarelli, M., Rio, P., Marrone, A., Ocarino, F., Chiantore, M., Candelli, M., Gasbarrini, A., Gambassi, G., & Cianci, R. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105377 · Cited by 37
“TMAO (trimethylamine-N-oxide) and secondary bile acids, produced by microbiota, influence metabolism and neuroinflammation through Farsenoid X (FXR), Takeda G-protein-coupled receptor 5 (TGR5), and glucocorticoid receptor [34,35].”
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“Despite most BA are reabsorbed in the terminal ileum, the biotransformation of BA mainly occurs in the colon (44) and secondary BA will come into the blood stream via passive reabsorption and recycle in enterohepatic circulation.”
Gut microbiota–mitochondrial inter-talk in non-alcoholic fatty liver disease
Zhang, Q., Xing, W., Wang, Q., Tang, Z., Wang, Y., & Gao, W. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.934113 · Cited by 34
“FXR is a target of sirtuin-1 (SIRT1), an NADdependent protein deacetylase, that regulates the expression of FXR (82) to regulate carbohydrate response element binding protein (ChREBP), steroid response element binding protein1c (SREBP-1c), and PPAR-α to stimulate FA uptake and oxidation (83).”
BackgroundThe Crosstalk Between Gut Microbiota and Obesity and Related Metabolic Disorders
Xu, W., Nie, Y., Yang, Z., & Lü, N. (2016) · Future Microbiology · doi:10.2217/fmb-2015-0024 · Cited by 35
Elmi, A., Dorey, A., Watson, E., Jagatia, H., Inglis, N. F., Gundogdu, O., Bajaj‐Elliott, M., Wren, B. W., Smith, D. G., & Dorrell, N. (2017) · Cellular Microbiology · doi:10.1111/cmi.12814 · Cited by 34
Chemical Mechanisms of Colonization Resistance by the Gut Microbial Metabolome
Chang, P. V. (2020) · ACS Chemical Biology · doi:10.1021/acschembio.9b00813 · Cited by 38
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Activity-Based Protein Profiling—Enabling Multimodal Functional Studies of Microbial Communities
Whidbey, C., & Wright, A. (2018) · Current topics in microbiology and immunology · doi:10.1007/82_2018_128 · Cited by 29
“This can lead to altered receptor binding and thus signaling activity (Joyce and Gahan 2016).”
Background
Metadata
- Authors
- Joyce, S. A., & Gahan, C. G. M.
- Affiliations
- APC Microbiome Institute (IE)
- University College Cork (IE)
- Venue
- Annual Review of Food Science and Technology
- Publisher
- Annual Reviews
- Published
- 2016-02-28
- Volume
- 7
- Issue
- 1
- Pages
- 313-333
- ISSN
- 1941-1421 (ISSN-L)
- 1941-1413
- OpenAlex
- W2152714616
- Cited by
- 241
- References
- 135
- Citations by year
- 2026: 27 · 2025: 22 · 2024: 27 · 2023: 20 · 2022: 37 · 2021: 24 · 2020: 20 · 2019: 16 · 2018: 15 · 2017: 23 · 2016: 10
- FWCI
- 1.93
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annual Review of Food Science and Technology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Health Research Board
- Science Foundation Ireland (SFI/12/RC/, 12/RC/2273, 12/RC/, SFI/12/RC/2273.)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
- Keywords
- bile acids, gut microbiota, farnesoid X receptor, TGR5, bile acid metabolism, host-microbe interactions, probiotics, metabolic disorders, obesity, inflammatory bowel disease, Clostridium difficile infection, colorectal cancer, hepatocellular carcinoma, bile acid signaling
- MeSH terms
- Gastrointestinal Microbiome, Receptor, Farnesoid X-Activated, Aging, Bile Acids and Salts, Diet, Disease, Energy Metabolism, Health Status, Humans, Liver, Technology, Pharmaceutical, Signal Transduction, Weight Gain, Receptors, Cytoplasmic and Nuclear, Dietary Supplements, Probiotics
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