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The Gut Microbiota Reduces Leptin Sensitivity and the Expression of the Obesity-Suppressing Neuropeptides Proglucagon (Gcg) and Brain-Derived Neurotrophic Factor (Bdnf) in the Central Nervous System
Abstract
The gut microbiota contributes to fat mass and the susceptibility to obesity. However, the underlying mechanisms are not completely understood. To investigate whether the gut microbiota affects hypothalamic and brainstem body fat-regulating circuits, we compared gene expression of food intake-regulating neuropeptides between germ-free and conventionally raised (CONV-R) mice. We found that CONV-R mice had decreased expression of the antiobesity neuropeptide glucagon-like peptide-1 (GLP-1) precursor proglucagon (Gcg) in the brainstem. Moreover, in both the hypothalamus and the brainstem, CONV-R mice had decreased expression of the antiobesity neuropeptide brain-derived neurotrophic factor (Bdnf). CONV-R mice had reduced expression of the pro-obesity peptides neuropeptide-Y (Npy) and agouti-related protein (Agrp), and increased expression of the antiobesity peptides proopiomelanocortin (Pomc) and cocaine- and amphetamine-regulated transcript (Cart) in the hypothalamus. The latter changes in neuropeptide expression could be secondary to elevated fat mass in CONV-R mice. Leptin treatment caused less weight reduction and less suppression of orexigenic Npy and Agrp expression in CONV-R mice compared with germ-free mice. The hypothalamic expression of leptin resistance-associated suppressor of cytokine signaling 3 (Socs-3) was increased in CONV-R mice. In conclusion, the gut microbiota reduces the expression of 2 genes coding for body fat-suppressing neuropeptides, Gcg and Bdnf, an alteration that may contribute to fat mass induction by the gut microbiota. Moreover, the presence of body fat-inducing gut microbiota is associated with hypothalamic signs of Socs-3-mediated leptin resistance, which may be linked to failed compensatory body fat reduction.
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“The gut microbiota have been shown to directly moderate brainstem and hypothalamic expression of BDNF, where conventionally raised mice differed significantly from GF mice (Schele et al., 2013).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Schele et al., 2013
In the citing paper
“several studies have demonstrated the significant role of gut microbiome in modulating leptin signaling and adiposity.”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [581]
In the citing paper
“In addition, Schéle et al. [116] found that administration of leptin reduced NPY expression in germ-free mice but not in conventionally raised mice, suggesting that the gut microbiota may decrease leptin sensitivity, effects that are dependent on vagal signaling [192].”
From Anxiety, depression, and the microbiome: A role for gut peptides (2018) · cites this paper as [116]
In the citing paper
“The expression of NPY in the hypothalamus (where NPY plays a major role in feeding behavior and stress response) is increased in adult, healthy, germ-free mice when compared with conventionally raised mice [116].”
From Anxiety, depression, and the microbiome: A role for gut peptides (2018) · cites this paper as [116]
In the citing paper
“Moreover, Schéle et al. [116] demonstrated the role of NPY in counteracting the increased plasma levels of corticosterone in germ-free rodents.”
From Anxiety, depression, and the microbiome: A role for gut peptides (2018) · cites this paper as [116]
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Metadata
- Authors
- Schéle, E., Grahnemo, L., Anesten, F., Hallén, A., Bäckhed, F., & Jansson, J.-O.
- Affiliations
- University of Gothenburg (SE)
- University of Copenhagen (DK)
- Corresponding author
- Jansson, John-Olov
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2013-10-01
- Volume
- 154
- Issue
- 10
- Pages
- 3643-3651
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W2013890677
- Cited by
- 209
- References
- 60
- Citations by year
- 2026: 7 · 2025: 15 · 2024: 19 · 2023: 19 · 2022: 18 · 2021: 24 · 2020: 11 · 2019: 19 · 2018: 15 · 2017: 13 · 2016: 20 · 2015: 16 · 2014: 12 · 2013: 1
- FWCI
- 8.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Vetenskapsrådet
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- gut microbiota, leptin resistance, proglucagon, brain-derived neurotrophic factor, obesity, hypothalamus, brainstem, neuropeptides, germ-free mice, SOCS3, neuropeptide Y, agouti-related protein, proopiomelanocortin, cocaine- and amphetamine-regulated transcript, food intake regulation, fat mass
- MeSH terms
- Suppressor of Cytokine Signaling 3 Protein, Cocaine- and Amphetamine-Regulated Transcript Protein, Animals, Brain Stem, Central Nervous System, Germ-Free Life, Hypothalamus, Injections, Intraperitoneal, Intestines, Male, Mice, Inbred C57BL, Nerve Tissue Proteins, Neurons, Neuropeptide Y, Pro-Opiomelanocortin, Recombinant Proteins, Down-Regulation, Brain-Derived Neurotrophic Factor, Leptin, Adiposity, Suppressor of Cytokine Signaling Proteins, Mice, Proglucagon, Agouti-Related Protein
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