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Host-microbial interactions in the metabolism of therapeutic and diet-derived xenobiotics
Open accessAbstract
Our associated microbial communities play a critical role in human health and predisposition to disease, but the degree to which they also shape therapeutic interventions is not well understood. Here, we integrate results from classic and current studies of the direct and indirect impacts of the gut microbiome on the metabolism of therapeutic drugs and diet-derived bioactive compounds. We pay particular attention to microbial influences on host responses to xenobiotics, adding to the growing consensus that treatment outcomes reflect our intimate partnership with the microbial world, and providing an initial framework from which to consider a more comprehensive view of pharmacology and nutrition.
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“β-glucuronidases are another generalist enzyme family expressed by human-associated gut bacteria that influences the biological activity and toxicity of a wide range of drugs, dietary components, and endogenous metabolites47.”
From The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism (2016) · cites this paper as [47]
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“Many of these “diet-derived bioactive compounds” are metabolized by the gut microbiota (Fig. 4, Supplementary information S2 (table) and Supplementary information S3 (table)) and some are dependent on this transformation for activation and/or absorption47.”
From The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism (2016) · cites this paper as [47]
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Microbiome Metabolites and Thyroid Dysfunction
Bargiel, P., Szczuko, M., Stachowska, L., Prowans, P., Czapla, N., Markowska, M., Petriczko, J., Kledzik, J., Jędrzejczyk-Kledzik, A., Palma, J., et al. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10163609 · Cited by 74
“Helicobacter-bound Levodopa cannot cross the blood–brain barrier and therefore does not decarboxylate to dopamine in the central nervous system, which renders it ineffective [28].”
BackgroundInsights into human evolution from ancient and contemporary microbiome studies
Schnorr, S. L., Sankaranarayanan, K., Lewis, C. M., & Warinner, C. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.07.003 · Cited by 71
Microbial Determinants of Biochemical Individuality and Their Impact on Toxicology and Pharmacology
Patterson, A. D., & Turnbaugh, P. J. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.07.002 · Cited by 66
“…mediates the metabolic effects of drugs and environmental toxicants, as other recent reviews have provided a more in-depth view of the historic and current literature on drug and dietary bioactive metabolism (Carmody and Turnbaugh, 2014; Haiser and Turnbaugh, 2012, 2013; Sousa et al., 2008).”
Self-citationSources of Interindividual Variability
Thummel, K. E., & Lin, Y. S. (2014) · Methods in molecular biology · doi:10.1007/978-1-62703-758-7_17 · Cited by 65
The importance of the microbiome in pediatrics and pediatric infectious diseases
Gaufin, T., Tobin, N. H., & Aldrovandi, G. M. (2017) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000000576 · Cited by 63
The human microbiome and metabolomics: Current concepts and applications
Daliri, E. B., Wei, S., Oh, D., & Lee, B. H. (2016) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2016.1220913 · Cited by 66
“This was because the gut microbial azoreductases cleaved the N-N double bond of the prodrug to release active 5-aminosalicylic acid (Carmody and Turnbaugh, 2014).”
BackgroundShin, J., Kim, C.-S., Cha, J., Kim, S., Lee, S., Chae, S., Chun, W. Y., & Shin, D. (2021) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2021.108854 · Cited by 71
Wang, S., Ju, D., & Zeng, X. L. (2024) · Biomedicines · doi:10.3390/biomedicines12010194 · Cited by 63
Gut microbiome: An intermediary to neurotoxicity
Dempsey, J. L., Little, M., & Cui, J. Y. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.08.005 · Cited by 63
“The important role of gut microbiome in the biotransformation of various therapeutic drugs has been extensively reviewed (Bisanz et al., 2018; Carmody and Turnbaugh, 2014; Haiser and Turnbaugh, 2013; Spanogiannopoulos et al., 2016).”
BackgroundRelationship Between the Gut Microbiome and Systemic Chemotherapy
Ervin, S. M., Ramanan, S. V., & Bhatt, A. P. (2020) · Digestive Diseases and Sciences · doi:10.1007/s10620-020-06119-3 · Cited by 62
Gut Microbiota Modulates Interactions Between Polychlorinated Biphenyls and Bile Acid Homeostasis
Cheng, S. L., Li, X., Lehmler, H., Phillips, B., Shen, D. D., & Cui, J. Y. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy208 · Cited by 58
Gade, A., & Kumar, M. S. (2023) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-023-00981-1 · Cited by 71
“Inter-estingly, the characteristics of polyphenols are determined by bioactive metabolites formed by microorganisms during metabolism [19].”
BackgroundThe role of gut microbiota in the pharmacokinetics of antihypertensive drugs
Choi, M. S., Yu, J. S., Yoo, H. H., & Kim, D. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.01.019 · Cited by 57
Chemopreventive effect of natural dietary compounds on xenobiotic-induced toxicity
Wu, J.-C., Lai, C., Tsai, M.-L., Ho, C., Wang, Y., & Pan, M. (2016) · Journal of Food and Drug Analysis · doi:10.1016/j.jfda.2016.10.019 · Cited by 57
Annunziata, G., Sureda, A., Orhan, İ. E., Battino, M. A., Arnone, A., Jiménez‐García, M., Capó, X., Cabot, J., Sanadgol, N., Giampieri, F., et al. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.07.004 · Cited by 57
Circulating glucuronic acid predicts healthspan and longevity in humans and mice
Ho, A., Sinick, J., Esko, T., Fischer, K., Menni, C., Zierer, J., Matey-Hernandez, M. L., Fortney, K., & Morgen, E. K. (2019) · Aging · doi:10.18632/aging.102281 · Cited by 58
“This chemical modification increases solubility in bile, facilitates urinary excretion, and is a key step in the phase II metabolism of these compounds required for their effective clearance from the body [9].”
BackgroundToll-like receptors in the pathogenesis of chemotherapy-induced gastrointestinal toxicity
Cario, E. (2016) · Current Opinion in Supportive and Palliative Care · doi:10.1097/spc.0000000000000202 · Cited by 55
Lakshmanan, A. P., Murugesan, S., Khodor, S. A., & Terranegra, A. (2022) · Journal of Translational Medicine · doi:10.1186/s12967-022-03631-0 · Cited by 64
Kan, J., Wu, F., Wang, F., Zheng, J., Cheng, J., Li, Y., Yang, Y., & Du, J. C. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.960309 · Cited by 61
Rosa, G. L., Lonardo, M. S., Cacciapuoti, N., Muscariello, E., Guida, B., Faraonio, R., Santillo, M., & Damiano, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087247 · Cited by 56
“Their properties depend on bioactive metabolites, produced when they are metabolized by the microbiota [75].”
BackgroundWalsh, J., Olavarría‐Ramírez, L., Lach, G., Boehme, M., Dinan, T. G., Cryan, J. F., Griffin, B. T., Hyland, N. P., & Clarke, G. A. (2020) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00026.2020 · Cited by 55
Considerations and challenges for sex-aware drug repurposing
Fisher, J. L., Jones, E. F., Flanary, V. L., Williams, A. S., Wilk, E. J., & Lasseigne, B. N. (2022) · Biology of Sex Differences · doi:10.1186/s13293-022-00420-8 · Cited by 47
“Acetaminophen is an over-the-counter drug known to have different toxicity across individuals, which may be due to microbial metabolites that compete with acetaminophen for liver enzyme binding sites (67).”
BackgroundLin, H., Chen, C.-Y., Lin, T., Yeh, L.-F., Hsieh, W., Gao, S., Burnouf, P., Chen, B., Hsieh, T.-J., Dashnyam, P., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-01815-w · Cited by 49
Stanaway, I. B., Wallace, J. C., Shojaie, A., Griffith, W. C., Hong, S., Wilder, C. S., Green, F. H., Tsai, J. M., Knight, M., Workman, T. W., et al. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.02149-16 · Cited by 48
Zidi, O., Souai, N., Raies, H., Ayed, F. B., Mézlini, A., Mezrioui, S., Tranchida, F., Sabatier, J., Mosbah, A., Cherif, A., et al. (2021) · Molecules · doi:10.3390/molecules26082266 · Cited by 49
“Gut microorganisms also have the potential to decrease the absorption of certain drugs by physical binding and segregation [70].”
BackgroundMetabolic Enabling and Detoxification by Mammalian Gut Microbes
Dearing, M. D., & Weinstein, S. B. (2022) · Annual Review of Microbiology · doi:10.1146/annurev-micro-111121-085333 · Cited by 51
Paik, J., Pershutkina, O. V., Meeker, S. M., Yi, J., Dowling, S. C., Hsu, C. C., Hajjar, A. M., Maggio‐Price, L., & Beck, D. A. C. (2015) · Gut Microbes · doi:10.1080/19490976.2015.1064576 · Cited by 46
Challenges Associated with Route of Administration in Neonatal Drug Delivery
Linakis, M. W., Roberts, J. K., Lala, A., Spigarelli, M. G., Medlicott, N. J., Reith, D. M., Ward, R. M., & Sherwin, C. M. T. (2015) · Clinical Pharmacokinetics · doi:10.1007/s40262-015-0313-z · Cited by 47
Hoskinson, C., Zheng, K., Gabel, J., Kump, A., German, R., Podicheti, R., Marino, N., & Stiemsma, L. T. (2022) · mSystems · doi:10.1128/msystems.01489-21 · Cited by 42
“Degradation of carcinogenic xenobiotics into nontoxic bioproducts is shown to be protective against breast carcinogenesis (17).”
Investigation of Host–Gut Microbiota Modulation of Therapeutic Outcome
Yip, L. Y., & Chan, E. C. Y. (2015) · Drug Metabolism and Disposition · doi:10.1124/dmd.115.063750 · Cited by 41
Conducting metagenomic studies in microbiology and clinical research
Martin, T. C., Visconti, A., Spector, T. D., & Falchi, M. (2018) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-9209-9 · Cited by 40
Raval, U., Harary, J. M., Zeng, E., & Pasinetti, G. M. (2020) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2020.1775585 · Cited by 45
“neuromodulators such as choline, tryptophan, and short chain fatty acids (SCFAs) [16,17].”
BackgroundMicrobiota and Drug Response in Inflammatory Bowel Disease
Franzin, M., Stefančič, K., Lucafò, M., Decorti, G., & Stocco, G. (2021) · Pathogens · doi:10.3390/pathogens10020211 · Cited by 39
“The contribution of the GM on various drugs has been reviewed elsewhere and in depth [53,54].”
BackgroundThe TLC-Bioautography as a Tool for Rapid Enzyme Inhibitors detection - A Review
Legerská, B., Chmelová, D., Ondrejovič, M., & Miertuš, S. (2020) · Critical Reviews in Analytical Chemistry · doi:10.1080/10408347.2020.1797467 · Cited by 40
“This process causes irinotecaninduced severe diarrhea and serious intestinal injury.([159,160]) The selective GUS inhibitors alleviate the side effects.”
Background
Metadata
- Authors
- Carmody, R. N., & Turnbaugh, P. J.
- Corresponding author
- Turnbaugh, Peter J.
- Venue
- Journal of Clinical Investigation
- Published
- 2014-08-08
- Volume
- 124
- Issue
- 10
- Pages
- 4173-4181
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC4191041
- OpenAlex
- W1964115194
- Cited by
- 268
- References
- 91
- Citations by year
- 2026: 17 · 2025: 16 · 2024: 10 · 2023: 15 · 2022: 23 · 2021: 47 · 2020: 33 · 2019: 26 · 2018: 21 · 2017: 19 · 2016: 23 · 2015: 14 · 2014: 3
- FWCI
- 1.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Harvard University
- National Institutes of Health
- FAS Center for Systems Biology, Harvard University
- National Institute of General Medical Sciences (P50GM068763)
- National Institute of Diabetes and Digestive and Kidney Diseases (F32DK101154)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Pharmacogenetics and Drug Metabolism
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Keywords
- host-microbe interactions, gut microbiota, xenobiotic metabolism, drug metabolism, therapeutic drugs, personalized medicine
- MeSH terms
- Animals, Binding Sites, Diet, Humans, Intestines, Mice, Transgenic, Protein Binding, Xenobiotics, Gene Expression Regulation, Bacterial, Probiotics, Gastrointestinal Tract, Mice, Microbial Interactions, Microbiota
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