Microbiota-Generated Metabolites Promote Metabolic Benefits via Gut-Brain Neural Circuits
Open accessAbstract
Soluble dietary fibers promote metabolic benefits on body weight and glucose control, but underlying mechanisms are poorly understood. Recent evidence indicates that intestinal gluconeogenesis (IGN) has beneficial effects on glucose and energy homeostasis. Here, we show that the short-chain fatty acids (SCFAs) propionate and butyrate, which are generated by fermentation of soluble fiber by the gut microbiota, activate IGN via complementary mechanisms. Butyrate activates IGN gene expression through a cAMP-dependent mechanism, while propionate, itself a substrate of IGN, activates IGN gene expression via a gut-brain neural circuit involving the fatty acid receptor FFAR3. The metabolic benefits on body weight and glucose control induced by SCFAs or dietary fiber in normal mice are absent in mice deficient for IGN, despite similar modifications in gut microbiota composition. Thus, the regulation of IGN is necessary for the metabolic benefits associated with SCFAs and soluble fiber.
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Mechanisms involved in the effects of SCFAs, mainly propionate and butyrate, in the brain responsible for controlling metabolic disorders include the activation of FFAR2 and FFAR3 receptors.
“Mechanisms involved in the effects of SCFAs, mainly propionate and butyrate, in the brain responsible for controlling metabolic disorders include the activation of FFAR2 and FFAR3 receptors (91).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [91]
FFAR3 receptor has been detected in the enteric neural plexus, the portal nerve, and autonomic and sensory ganglia.
“It is well established that SCFAs can activate the PNS, where FFAR3 receptor has been detected in the enteric neural plexus, the portal nerve and autonomic and sensory ganglia (De Vadder et al., 2014;Kaji et al., 2016;Nohr et al., 2015;Won et al., 2013).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as De Vadder et al., 2014
Short-chain fatty acids (SCFAs) can activate the peripheral nervous system (PNS).
“It is well established that SCFAs can activate the PNS, where FFAR3 receptor has been detected in the enteric neural plexus, the portal nerve and autonomic and sensory ganglia (De Vadder et al., 2014;Kaji et al., 2016;Nohr et al., 2015;Won et al., 2013).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as De Vadder et al., 2014
Activation of FFAR3 on the vagus nerve innervating the portal vein results in increased neuronal activity in the dorsal vagal complex, parabrachial nuclei, and hypothalamus.
“Particularly important for gut-brain axis signaling, activation of FFAR3 on the vagus nerve innervating the portal vein results in increased neuronal activity in the dorsal vagal complex, parabrachial nuclei and hypothalamus (De Vadder et al., 2014).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as De Vadder et al., 2014
SCFAs signal via the central nervous system and several G protein-coupled receptors to modulate energy homeostasis, lipid and carbohydrate metabolism, and suppression of inflammatory signals.
“SCFAs signal via the central nervous system and several G protein–coupled receptors (GPCRs) to modulate a range of physiological processes, including energy homeostasis, lipid and carbohydrate metabolism, and suppression of inflammatory signals (14, 15).”
From The gut microbiota at the intersection of diet and human health (2018) · cites this paper as [15]
Early experiments using germ-free or specific pathogen-free mice treated with antibiotics to reduce microbial diversity showed that several neurological problems occur in mice with reduced or lack of proper mature gut microbiota.
“Early experiments using germ-free (GF) or specific pathogen-free (SPF) mice treated with antibiotics, to reduce the microbial diversity within the intestine, showed that several neurological problems occur in mice with reduced or lack of proper mature gut microbiota (7, 10, 14, 15, 34, 80, 81).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [14]
Butyrate and propionate play a role in intestinal gluconeogenesis, which has beneficial effects on glucose and energy homeostasis.
“Butyrate and propionate have recently been demonstrated to play a role in intestinal gluconeogenesis, which has beneficial effects on glucose and energy homeostasis [20].”
From Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals (2016) · cites this paper as [20]
Gut microbiota produce many chemicals affecting brain function, such as serotonin, dopamine, r-aminobutyric acid, SCFAs, and p-cresol.
“For example, gut microbiota can regulate the hypothalamic-pituitary-adrenal (HPA) axis13, and produce many chemicals affecting brain function (e.g., serotonin, dopamine, r-aminobutyric acid, SCFAs, and p-cresol)14,15.”
From Altered composition and function of intestinal microbiota in autism spectrum disorders: A systematic review (2019) · cites this paper as [14]
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- Authors
- De Vadder, F., Kovatcheva-Datchary, P., Goncalves, D., Vinera, J., Zitoun, C., Duchampt, A., Bäckhed, F., & Mithieux, G.
- Affiliations
- Lyon 1 Université (FR)
- University of Copenhagen (DK)
- Corresponding author
- Mithieux, Gilles
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-01
- Volume
- 156
- Issue
- 1-2
- Pages
- 84-96
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2171016495
- Cited by
- 2,200
- References
- 58
- Citations by year
- 2026: 126 · 2025: 180 · 2024: 223 · 2023: 202 · 2022: 246 · 2021: 262 · 2020: 243 · 2019: 168 · 2018: 154 · 2017: 134 · 2016: 130 · 2015: 72 · 2014: 60
- FWCI
- 53.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-10-INBS-0007)
- Institut National de la Santé et de la Recherche Médicale
- Stiftelsen för Strategisk Forskning
- Knut och Alice Wallenbergs Stiftelse
- Vetenskapsrådet
- Göteborgs Universitet
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Keywords
- short-chain fatty acids, propionate, butyrate, intestinal gluconeogenesis, soluble dietary fiber, gut microbiota, FFAR3, cAMP signaling, glucose homeostasis, body weight regulation, energy homeostasis
- MeSH terms
- Animals, Brain, Dietary Fats, Dietary Fiber, Fatty Acids, Volatile, Gluconeogenesis, Glucose, Glucose-6-Phosphatase, Homeostasis, Insulin Resistance, Intestinal Mucosa, Intestines, Obesity, Oligosaccharides, Mice, Rats, Microbiota
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