Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences

Blachier, F.; Mariotti, F.; Huneau, J. F.; Tomé, D.

doi:10.1007/s00726-006-0477-9

Cited by 452Gut microbiota and healthAnimal Nutrition and PhysiologyPolyamine Metabolism and Applications

Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences

Blachier, F., Mariotti, F., Huneau, J. F., Tomé, D.·2007·Amino Acids

DOI 10.1007/s00726-006-0477-9

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Abstract

Depending on the amount of alimentary proteins, between 6 and 18 g nitrogenous material per day enter the large intestine lumen through the ileocaecal junction. This material is used as substrates by the flora resulting eventually in the presence of a complex mixture of metabolites including ammonia, hydrogen sulfide, short and branched-chain fatty acids, amines; phenolic, indolic and N-nitroso compounds. The beneficial versus deleterious effects of these compounds on the colonic epithelium depend on parameters such as their luminal concentrations, the duration of the colonic stasis, the detoxication capacity of epithelial cells in response to increase of metabolite concentrations, the cellular metabolic utilization of these metabolites as well as their effects on colonocyte intermediary and oxidative metabolism. Furthermore, the effects of metabolites on electrolyte movements through the colonic epithelium must as well be taken into consideration for such an evaluation. The situation is further complicated by the fact that other non-nitrogenous compounds are believed to interfere with these various phenomenons. Finally, the pathological consequences of the presence of excessive concentrations of these compounds are related to the short- and, most important, long-term effects of these compounds on the rapid colonic epithelium renewing and homeostasis.

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Microbial-derived BCAAs include valerate, isobutyrate, and isovalerate, and these bacterial metabolites influence epithelial physiology and the mucosal immune system of the host.
“Microbial-derived BCAAs include valerate, isobutyrate, and isovalerate.Notably, these bacterial metabolites have been shown to influence epithelial physiology and the mucosal immune system of the host (Blachier et al., 2007;Schaible and Kaufmann, 2005).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Blachier et al., 2007
Most host-produced urea is hydrolyzed in the lumen of the large intestine into NH3 and nitrogen through bacterial urease activity.
“Most of host-produced urea is hydrolyzed in the lumen of the large intestine into NH3 and nitrogen through bacterial urease activity [131].”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [131]
NH3 can be used by bacteria for their own metabolism and protein synthesis.
“NH3 can be used by the bacteria for their own metabolism and protein synthesis [131].”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [131]
Specific branched-chain amino acids (valerate, isobutyrate, and isovalerate) influence epithelial and mucosal homeostasis.
“The GM produces higher proportions of specific BCAAs (valerate, isobutyrate, and isovalerate) relative to other amino acids, which have been shown to influence epithelial and mucosal homeostasis (332).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [332]
The gut microbiota produces higher proportions of specific branched-chain amino acids (valerate, isobutyrate, and isovalerate) relative to other amino acids.
“The GM produces higher proportions of specific BCAAs (valerate, isobutyrate, and isovalerate) relative to other amino acids, which have been shown to influence epithelial and mucosal homeostasis (332).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [332]

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The Microbiota-Gut-Brain Axis
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
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Short-chain fatty acids in control of body weight and insulin sensitivity
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Chemical transformation of xenobiotics by the human gut microbiota
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The role of microbial amino acid metabolism in host metabolism
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Dietary protein intake and human health
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Relevance of protein fermentation to gut health
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The Short-Chain Fatty Acid Acetate in Body Weight Control and Insulin Sensitivity
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Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes
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“Most of host-produced urea is hydrolyzed in the lumen of the large intestine into NH3 and nitrogen through bacterial urease activity [131].”
Background
The role of methionine on metabolism, oxidative stress, and diseases
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Intestinal luminal nitrogen metabolism: Role of the gut microbiota and consequences for the host
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Self-citation
Amino acid metabolism in intestinal bacteria: links between gut ecology and host health
Dai, Z. (2010) · Frontiers in bioscience · doi:10.2741/3820 · Cited by 563 · see citing works
Microbial Fermentation of Dietary Protein: An Important Factor in Diet–Microbe–Host Interaction
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Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health
Berding, K., Vlckova, K., Marx, W., Schellekens, H., Stanton, C., Clarke, G., Jacka, F., Dinan, T. G., & Cryan, J. F. (2021) · Advances in Nutrition · doi:10.1093/advances/nmaa181 · Cited by 451 · see citing works
Review article: insights into colonic protein fermentation, its modulation and potential health implications
Yao, C. K., Muir, J. G., & Gibson, P. R. (2016) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13456 · Cited by 441 · see citing works
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Commensal bacteria-dependent indole production enhances epithelial barrier function in the colon
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Differential 12 C-/ 13 C-Isotope Dansylation Labeling and Fast Liquid Chromatography/Mass Spectrometry for Absolute and Relative Quantification of the Metabolome
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Immune regulation by microbiome metabolites
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Gut Microbiota, Short-Chain Fatty Acids, and Herbal Medicines
Feng, W., Ao, H., & Peng, C. Y. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01354 · Cited by 368 · see citing works
Glutamine, arginine, and leucine signaling in the intestine
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Metabolomics of Fecal Extracts Detects Altered Metabolic Activity of Gut Microbiota in Ulcerative Colitis and Irritable Bowel Syndrome
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Towards microbial fermentation metabolites as markers for health benefits of prebiotics
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The Crosstalk between the Gut Microbiota and Mitochondria during Exercise
Clark, A. P., & Mach, N. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00319 · Cited by 338 · see citing works
Alteration of the fecal microbiota and serum metabolite profiles in dogs with idiopathic inflammatory bowel disease
Minamoto, Y., Otoni, C. C., Steelman, S. M., Büyükleblebici, O., Steiner, J. M., Jergens, A. E., & Suchodolski, J. S. (2015) · Gut Microbes · doi:10.1080/19490976.2014.997612 · Cited by 339 · see citing works
Metabolism and functions of l-glutamate in the epithelial cells of the small and large intestines
Blachier, F., Boutry, C., Bos, C., & Tomé, D. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27462s · Cited by 334 · see citing works
Self-citation
Comorbidity between major depressive disorder and physical diseases: a comprehensive review of epidemiology, mechanisms and management
Berk, M., Köhler‐Forsberg, O., Turner, M., Penninx, B. W. J. H., Wrobel, A., Firth, J., Loughman, A., Reavley, N. J., McGrath, J. J., Momen, N. C., et al. (2023) · World Psychiatry · doi:10.1002/wps.21110 · Cited by 336 · see citing works
An Overview on Fecal Branched Short-Chain Fatty Acids Along Human Life and as Related With Body Mass Index: Associated Dietary and Anthropometric Factors
Ríos-Covián, D., González, S., Nogacka, A. M., Arboleya, S., Salazar, N., Gueimonde, M., & Reyes-Gavilán, C. G. D. L. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00973 · Cited by 320 · see citing works
Dietary Amino Acids and the Gut‐Microbiome‐Immune Axis: Physiological Metabolism and Therapeutic Prospects
Ma, N., & Ma, X. (2018) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12401 · Cited by 278 · see citing works
Dietary fiber and protein fermentation in the intestine of swine and their interactive effects on gut health and on the environment: A review
Jha, R., & Berrocoso, J. D. (2015) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2015.12.002 · Cited by 272 · see citing works
Gut Microbial Activity, Implications for Health and Disease: The Potential Role of Metabolite Analysis
Nyangale, E. P., Mottram, D. S., & Gibson, G. R. (2012) · Journal of Proteome Research · doi:10.1021/pr300637d · Cited by 265 · see citing works
Metabolic and Microbial Modulation of the Large Intestine Ecosystem by Non-Absorbed Diet Phenolic Compounds: A Review
Mosele, J. I., Macià, A., & Motilva, M. (2015) · Molecules · doi:10.3390/molecules200917429 · Cited by 261 · see citing works
Quantity and source of dietary protein influence metabolite production by gut microbiota and rectal mucosa gene expression: A randomized, parallel, double-blind trial in overweight humans
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
Self-citation
Utilization of amino acids by bacteria from the pig small intestine
Dai, Z.-L., Zhang, J., Wu, G., & Zhu, W.-Y. (2010) · Amino Acids · doi:10.1007/s00726-010-0556-9 · Cited by 246 · see citing works
Metabolites of Dietary Protein and Peptides by Intestinal Microbes and their Impacts on Gut
Fan, P. F., Li, L., Rezaei, A., Eslamfam, S., Che, D., & Ma, X. (2015) · Current Protein and Peptide Science · doi:10.2174/1389203716666150630133657 · Cited by 235 · see citing works
Re-print of “Intestinal luminal nitrogen metabolism: Role of the gut microbiota and consequences for the host”
Davila, A.-M., Blachier, F., Gotteland, M., Andriamihaja, M., Benetti, P.-H., Sanz, Y., & Tomé, D. (2013) · Pharmacological Research · doi:10.1016/j.phrs.2013.01.003 · Cited by 231 · see citing works
Self-citation
Gut Microbiota Metabolism and Interaction with Food Components
Vernocchi, P., CHIERICO, F. D., & Putignani, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21103688 · Cited by 236 · see citing works
Amino acid metabolism in intestinal bacteria and its potential implications for mammalian reproduction
Dai, Z., Wu, Z., Hang, S., Zhu, W., & Wu, G. (2015) · Molecular Human Reproduction · doi:10.1093/molehr/gav003 · Cited by 228 · see citing works
Effect of Dietary Protein and Processing on Gut Microbiota—A Systematic Review
Wu, S., Bhat, Z., Gounder, R., Ahmed, I. A. M., Juhaimi, F. A., Ding, Y., & Bekhit, A. E. A. (2022) · Nutrients · doi:10.3390/nu14030453 · Cited by 230 · see citing works
Mitochondria and Sulfide: A Very Old Story of Poisoning, Feeding, and Signaling?
Bouillaud, F., & Blachier, F. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3678 · Cited by 211 · see citing works
Self-citation
Luminal sulfide and large intestine mucosa: friend or foe?
Blachier, F., Davila, A., Mimoun, S., Bénetti, P.-H., Atanasiu, C., Andriamihaja, M., Benamouzig, R., Bouillaud, F., & Tomé, D. (2009) · Amino Acids · doi:10.1007/s00726-009-0445-2 · Cited by 210 · see citing works
Self-citation
Polysaccharide of Hericium erinaceus attenuates colitis in C57BL/6 mice via regulation of oxidative stress, inflammation-related signaling pathways and modulating the composition of the gut microbiota
Ren, Y., Geng, Y., Du, Y. Z., Li, W., Lu, Z., Xu, H., Xu, G., Shi, J., & Xu, Z. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.03.005 · Cited by 207 · see citing works
Diet drives quick changes in the metabolic activity and composition of human gut microbiota in a validated in vitro gut model
Aguirre, M., Eck, A., Koenen, M. E., Savelkoul, P. H. M., Budding, A. E., & Venema, K. (2016) · Research in Microbiology · doi:10.1016/j.resmic.2015.09.006 · Cited by 204 · see citing works
Metabolite interactions between host and microbiota during health and disease: Which feeds the other?
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
Structural Differences among Alkali-Soluble Arabinoxylans from Maize (Zea mays), Rice (Oryza sativa), and Wheat (Triticum aestivum) Brans Influence Human Fecal Fermentation Profiles
Rose, D. J., Patterson, J. A., & Hamaker, B. R. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf9020416 · Cited by 198 · see citing works
Dietary supplementation with l-arginine or N-carbamylglutamate enhances intestinal growth and heat shock protein-70 expression in weanling pigs fed a corn- and soybean meal-based diet
Wu, X., Ruan, Z., Gao, Y., Yin, Y., Zhou, X., Wang, L., Geng, M., Hou, Y., & Wu, G. (2010) · Amino Acids · doi:10.1007/s00726-010-0538-y · Cited by 198 · see citing works
The impact of red and processed meat consumption on cancer and other health outcomes: Epidemiological evidences
Boada, L. D., Henríquez‐Hernández, L. A., & Luzardo, O. P. (2016) · Food and Chemical Toxicology · doi:10.1016/j.fct.2016.04.008 · Cited by 198 · see citing works
Rifaximin modulates the colonic microbiota of patients with Crohn's disease: an in vitro approach using a continuous culture colonic model system
Maccaferri, S., Vitali, B., Klinder, A., Kolida, S., Ndagijimana, M., Laghi, L., Calanni, F., Brigidi, P., Gibson, G. R., & Costabile, A. (2010) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkq345 · Cited by 186 · see citing works
l-Glutamine or l-alanyl-l-glutamine prevents oxidant- or endotoxin-induced death of neonatal enterocytes
Haynes, T. E., Li, P., Li, X., Shimotori, K., Sato, H., Flynn, N. E., Wang, J., Knabe, D. A., & Wu, G. (2009) · Amino Acids · doi:10.1007/s00726-009-0243-x · Cited by 183 · see citing works
Identification of the novel role of butyrate as AhR ligand in human intestinal epithelial cells
Marinelli, L., Martin‐Gallausiaux, C., Bourhis, J., Béguet-Crespel, F., Blottière, H. M., & Lapaque, N. (2019) · Scientific Reports · doi:10.1038/s41598-018-37019-2 · Cited by 190 · see citing works
Protein fermentation in the gut; implications for intestinal dysfunction in humans, pigs, and poultry
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
The impact of high dietary zinc oxide on the development of the intestinal microbiota in weaned piglets
Starke, I. C., Pieper, R., Neumann, K., Zentek, J., & Vahjen, W. (2013) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12233 · Cited by 179 · see citing works
Production of hydrogen sulfide by the intestinal microbiota and epithelial cells and consequences for the colonic and rectal mucosa
Blachier, F., Andriamihaja, M., Larraufie, P., Ahn, E., Lan, A., & Kim, E. (2020) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00261.2020 · Cited by 175 · see citing works
Self-citation
Role of gut microbiota in identification of novel TCM-derived active metabolites
Lin, T., Lu, C., Lai, W.-F., Wu, T., Lu, J., Chen, Y.-M., Tzeng, C., Liu, H., Wei, H., & Lai, H. (2020) · Protein & Cell · doi:10.1007/s13238-020-00784-w · Cited by 175 · see citing works
Gut Microbiota as the Link between Elevated BCAA Serum Levels and Insulin Resistance
Gojda, J., & Cahová, M. (2021) · Biomolecules · doi:10.3390/biom11101414 · Cited by 167 · see citing works
Dynamic digestion of tamarind seed polysaccharide: Indigestibility in gastrointestinal simulations and gut microbiota changes in vitro
Li, X., Guo, R. H., Wu, X., Liu, X., Ai, L., Sheng, Y., Song, Z., & Wu, Y. (2020) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2020.116194 · Cited by 168 · see citing works
The deleterious metabolic and genotoxic effects of the bacterial metabolite p-cresol on colonic epithelial cells
Andriamihaja, M., Lan, A., Beaumont, M., Audebert, M., Wong, X., Yamada, K., Yin, Y., Tomé, D., Carrasco‐Pozo, C., Gotteland, M., et al. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.04.004 · Cited by 162 · see citing works
Self-citation
Seaweed Components as Potential Modulators of the Gut Microbiota
Shannon, E., Conlon, M. A., & Hayes, M. (2021) · Marine Drugs · doi:10.3390/md19070358 · Cited by 164 · see citing works
Non-Digestible Food Ingredients, Colonic Microbiota and the Impact on Gut Health and Immunity: A Role for Metabolomics
Jacobs, D. M., Gaudier, E. A., van Duynhoven, J., & Vaughan, E. E. (2009) · Current Drug Metabolism · doi:10.2174/138920009787048383 · Cited by 162 · see citing works
Review of the association between meat consumption and risk of colorectal cancer
Kim, E., Coelho, D., & Blachier, F. (2013) · Nutrition Research · doi:10.1016/j.nutres.2013.07.018 · Cited by 155 · see citing works
Self-citation
Detrimental effects for colonocytes of an increased exposure to luminal hydrogen sulfide: The adaptive response
Beaumont, M., Andriamihaja, M., Lan, A., Khodorova, N., Audebert, M., Blouin, J., Grauso, M., Lancha, L., Bénetti, P.-H., Benamouzig, R., et al. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.01.028 · Cited by 155 · see citing works
Self-citation
Reduced Diversity and Imbalance of Fecal Microbiota in Patients with Ulcerative Colitis
Nemoto, H., Kataoka, K., Ishikawa, H., Ikata, K., Arimochi, H., Iwasaki, T., Ohnishi, Y., Kuwahara, T., & Yasutomo, K. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2236-y · Cited by 152 · see citing works
Composition of polyamines and amino acids in plant-source foods for human consumption
Hou, Y., He, W., Hu, S., & Wu, G. (2019) · Amino Acids · doi:10.1007/s00726-019-02751-0 · Cited by 151 · see citing works
Altered gut microbiota in Rett syndrome
Strati, F., Cavalieri, D., Albanese, D., Felice, C. D., Donati, C., Hayek, J., Jousson, O., Leoncini, S., Pindo, M., Renzi, D., et al. (2016) · Microbiome · doi:10.1186/s40168-016-0185-y · Cited by 148 · see citing works
Physiological Effects of Dietary Amino Acids on Gut Health and Functions of Swine
Yang, Z., & Liao, S. F. (2019) · Frontiers in Veterinary Science · doi:10.3389/fvets.2019.00169 · Cited by 145 · see citing works
Colon luminal content and epithelial cell morphology are markedly modified in rats fed with a high-protein diet
Andriamihaja, M., Davila, A., Eklou-Lawson, M., Petit, N., Delpal, S., Allek, F., Blais, A., Delteil, C., Tomé, D., & Blachier, F. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00149.2010 · Cited by 145 · see citing works
Self-citation
Dietary α-ketoglutarate supplementation ameliorates intestinal injury in lipopolysaccharide-challenged piglets
Hou, Y., Wang, L., Ding, B., Liu, Y., Zhu, H., Liu, J., YongTang, L., Wu, X., Yin, Y., & Wu, G. (2010) · Amino Acids · doi:10.1007/s00726-010-0473-y · Cited by 142 · see citing works
Bacteroides ovatus colonization influences the abundance of intestinal short chain fatty acids and neurotransmitters
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Authors: Blachier, F., Mariotti, F., Huneau, J. F., & Tomé, D.
Affiliations: Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
Physiologie de la Nutrition et du Comportement Alimentaire (FR)
ORCID: Blachier, F.
Mariotti, F.
Huneau, J. F.
Tomé, D.
Venue: Amino Acids
Publisher: Springer Science and Business Media LLC
Published: 2006-12-06
Volume: 33
Issue: 4
Pages: 547-562
ISSN: 0939-4451 (ISSN-L)
1438-2199
DOI: 10.1007/s00726-006-0477-9
OpenAlex: W1975034176
Semantic Scholar: 378e65004ac0b84d7d32fddc40404dfde955ba9e
Cited by: 452
References: 274
Citations by year: 2026: 19 · 2025: 25 · 2024: 43 · 2023: 35 · 2022: 41 · 2021: 34 · 2020: 32 · 2019: 36 · 2018: 36 · 2017: 21 · 2016: 18 · 2015: 27 · 2014: 11 · 2013: 12 · 2012: 17
FWCI: 0.48
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Amino Acids (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Polyamine Metabolism and Applications
Keywords: colonic epithelium, colonic microbiota, ammonia, hydrogen sulfide, short-chain fatty acids, branched-chain fatty acids, amines, phenolic compounds, N-nitroso compounds, colonic stasis, oxidative metabolism, electrolyte transport, colonic homeostasis, colon carcinogenesis
MeSH terms: Amino Acids, Ammonia, Animals, Bacteria, Colon, Colonic Diseases, Dietary Proteins, Digestion, Epithelial Cells, Fatty Acids, Humans, Hydrogen Sulfide, Intestinal Mucosa, Intestine, Large, Nitroso Compounds, Polyamines, Hydroxybenzoates

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Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences

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