Functional Characterization of Human Receptors for Short Chain Fatty Acids and Their Role in Polymorphonuclear Cell Activation
Open accessAbstract
Short chain fatty acids (SCFAs), including acetate, propionate, and butyrate, are produced at high concentration by bacteria in the gut and subsequently released in the bloodstream. Basal acetate concentrations in the blood (about 100 microm) can further increase to millimolar concentrations following alcohol intake. It was known previously that SCFAs can activate leukocytes, particularly neutrophils. In the present work, we have identified two previously orphan G protein-coupled receptors, GPR41 and GPR43, as receptors for SCFAs. Propionate was the most potent agonist for both GPR41 and GPR43. Acetate was more selective for GPR43, whereas butyrate and isobutyrate were more active on GPR41. The two receptors were coupled to inositol 1,4,5-trisphosphate formation, intracellular Ca2+ release, ERK1/2 activation, and inhibition of cAMP accumulation. They exhibited, however, a differential coupling to G proteins; GPR41 coupled exclusively though the Pertussis toxin-sensitive Gi/o family, whereas GPR43 displayed a dual coupling through Gi/o and Pertussis toxin-insensitive Gq protein families. The broad expression profile of GPR41 in a number of tissues does not allow us to infer clear hypotheses regarding its biological functions. In contrast, the highly selective expression of GPR43 in leukocytes, particularly polymorphonuclear cells, suggests a role in the recruitment of these cell populations toward sites of bacterial infection. The pharmacology of GPR43 matches indeed the effects of SCFAs on neutrophils, in terms of intracellular Ca2+ release and chemotaxis. Such a neutrophil-specific SCFA receptor is potentially involved in the development of a variety of diseases characterized by either excessive or inefficient neutrophil recruitment and activation, such as inflammatory bowel diseases or alcoholism-associated immune depression. GPR43 might therefore constitute a target allowing us to modulate immune responses in these pathological situations.
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Acetate, propionate, and butyrate can preferentially activate free fatty acid receptors (FFARs) to increase energy harvest and triglyceride storage in adipose tissue.
“Molecular data showed that acetate, propionate, and butyrate can preferentially activate a series of free fatty acid receptors (FFARs) to increase energy harvest and triglyceride storage in adipose tissue [34,35,36].”
From Preventive Effects and Mechanisms of Garlic on Dyslipidemia and Gut Microbiome Dysbiosis (2019) · cites this paper as [35]
SCFAs can activate several G-protein coupled receptors, of which free fatty acid receptor 2 (FFAR2) and 3 (FFAR3) are the most investigated.
“SCFAs can activate several G-protein coupled receptors (GPCR), of which free fatty acid receptor 2 (FFAR2, also referred to as GPR43) and 3 (FFAR3, also referred to as GPR41) are the most investigated (Brown et al., 2003;Le Poul et al., 2003;Nilsson et al., 2003).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Le Poul et al., 2003
SCFAs modulate immune cells, including regulation of neutrophil chemotaxis and inflammation, suppression of cytokine production from myeloid cells, and regulation of T regulatory, T helper 1, and T helper 17 cell differentiation.
“Further, SCFAs have been shown to modulate immune cells themselves (Correa-Oliveira et al., 2016;Kim et al., 2014).These include the regulation of neutrophils chemotaxis and inflammation (Le Poul et al., 2003;Vieira et al., 2017;Vinolo et al., 2011), the suppression of cytokine production from myeloid cells (Nastasi et al., 2015;Park et al., 2007) and by regulating T regulatory, T helper 1, and T”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Le Poul et al., 2003
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Frye, R. E., Rose, S., Chacko, J., Wynne, R., Bennuri, S. C., Slattery, J. C., Tippett, M., Delhey, L., Melnyk, S., Kahler, S. G., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.189 · Cited by 130 · see citing works
The Gut Microbiome as a Target for the Treatment of Type 2 Diabetes
Aydin, Ö., Nieuwdorp, M., & Gerdes, V. (2018) · Current Diabetes Reports · doi:10.1007/s11892-018-1020-6 · Cited by 124 · see citing works
Masse, K. E., & Lu, V. B. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1169624 · Cited by 120 · see citing works
“SCFAs activate several GPCRs including: the free fatty acid receptor 2 and 3 (FFA2 and FFA3) (80, 81), the olfactory receptor subfamily 51E1 and 51E2 (OR51E1 in human/Olfr558 in mouse; OR51E2 in human/Olfr78 in mouse) (82), and the hydroxycarboxylic acid receptor, HCAR2 (also known as the G-protein coupled receptor 10…”
BackgroundInfluentialDo SCFA have a role in appetite regulation?
Darzi, J., Frost, G. S., & Robertson, M. D. (2011) · Proceedings of the Nutrition Society · doi:10.1017/s0029665110004039 · Cited by 94 · see citing works
The Emerging Role of Polyphenols in the Management of Type 2 Diabetes
Wang, Y., Alkhalidy, H., & Liu, D. (2021) · Molecules · doi:10.3390/molecules26030703 · Cited by 88 · see citing works
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Preventive Effects and Mechanisms of Garlic on Dyslipidemia and Gut Microbiome Dysbiosis
Chen, K., Xie, K., Liu, Z., Nakasone, Y., Sakao, K., Hossain, M. A., & Hou, D.-X. (2019) · Nutrients · doi:10.3390/nu11061225 · Cited by 79 · see citing works
Microbiota-Derived Short-Chain Fatty Acids Promote LAMTOR2-Mediated Immune Responses in Macrophages
Wu, T., Li, H., Su, C., Xu, F., Yang, G., Sun, K., Xu, M., Lv, N., Meng, B., Liu, Y., et al. (2020) · mSystems · doi:10.1128/msystems.00587-20 · Cited by 78 · see citing works
The nutrient-sensing repertoires of mouse enterochromaffin cells differ between duodenum and colon
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Gut-microbiota derived bioactive metabolites and their functions in host physiology
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Uptake and Metabolism of the Short-Chain Fatty Acid Butyrate, a Critical Review of the Literature
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Incretin Hormones, Obesity and Gut Microbiota
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- Authors
- Le Poul, E., Loison, C., Struyf, S., Springael, J.-Y., Lannoy, V., Decobecq, M.-E., Brezillon, S., Dupriez, V., Vassart, G., Van Damme, J., Parmentier, M., & Detheux, M.
- Affiliations
- Euroscreen (Belgium) (BE)
- Rega Institute for Medical Research (BE)
- Université Libre de Bruxelles (BE)
- Corresponding author
- Parmentier, Marc
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2003-07
- Volume
- 278
- Issue
- 28
- Pages
- 25481-25489
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2162704444
- Cited by
- 1,651
- References
- 0
- Citations by year
- 2026: 75 · 2025: 90 · 2024: 122 · 2023: 117 · 2022: 137 · 2021: 129 · 2020: 110 · 2019: 96 · 2018: 100 · 2017: 82 · 2016: 90 · 2015: 87 · 2014: 71 · 2013: 62 · 2012: 59
- FWCI
- 5.76
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- short-chain fatty acids, GPR41, GPR43, G protein-coupled receptors, neutrophil activation, polymorphonuclear leukocytes, propionate, acetate, butyrate, isobutyrate, Gq coupling, inositol 1,4,5-trisphosphate, intracellular calcium release, ERK1/2 activation, cAMP inhibition, chemotaxis, inflammatory bowel disease, gut microbiota
- MeSH terms
- Acetates, Cyclic AMP, Aequorin, Amino Acid Sequence, Animals, Calcium, Chemotaxis, Dose-Response Relationship, Drug, Fatty Acids, Volatile, Cricetinae, Humans, Leukocytes, Molecular Sequence Data, Neutrophils, Phylogeny, Receptors, Cell Surface, Recombinant Proteins, Time Factors, Tissue Distribution, Transfection, Inositol 1,4,5-Trisphosphate, Guanosine 5'-O-(3-Thiotriphosphate), CHO Cells, Sequence Homology, Amino Acid, GTP-Binding Proteins, Mitogen-Activated Protein Kinase 1, Reverse Transcriptase Polymerase Chain Reaction, Mitogen-Activated Protein Kinases, MAP Kinase Signaling System, Pertussis Toxin, Receptors, G-Protein-Coupled, Mitogen-Activated Protein Kinase 3
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