Microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gut

Abstract The gut microbiome (GMB) regulates digestion, metabolism, immunity, and energy homeostasis. This study investigates how gut microbiota integrate the regulation in the neuroendocrine and enteroendocrine systems, with a focus on G protein‐coupled receptors (GPCRs) in the brain‐gut axis and se...

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Main Authors: Wynne Milhouse, Anna Clapp Organski, Xun Sun, Derek Ai, Baohua Zhou, Tzu‐Wen L. Cross, Hongxia Ren
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Physiological Reports
Subjects:
Online Access:https://doi.org/10.14814/phy2.70373
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author Wynne Milhouse
Anna Clapp Organski
Xun Sun
Derek Ai
Baohua Zhou
Tzu‐Wen L. Cross
Hongxia Ren
author_facet Wynne Milhouse
Anna Clapp Organski
Xun Sun
Derek Ai
Baohua Zhou
Tzu‐Wen L. Cross
Hongxia Ren
author_sort Wynne Milhouse
collection DOAJ
description Abstract The gut microbiome (GMB) regulates digestion, metabolism, immunity, and energy homeostasis. This study investigates how gut microbiota integrate the regulation in the neuroendocrine and enteroendocrine systems, with a focus on G protein‐coupled receptors (GPCRs) in the brain‐gut axis and sex differences. Germ‐free (GF) mice exhibited increased hypothalamic expression of the anorexigenic neuropeptide and decreased expression of the negative regulator of leptin signaling. GF males had significantly lower serum leptin levels compared to conventional (CON) males, highlighting a potential link between the microbiome and leptin resistance. In the gut, GF mice demonstrated heightened expression of anorexigenic gut hormones, including peptide YY (Pyy) and cholecystokinin (Cck), in addition to increased levels of G protein‐coupled receptors (GPCRs) involved in gut hormone secretion and nutrient metabolism, particularly in females. While carbohydrate metabolism genes were upregulated in CON mice, lipid metabolism genes were predominantly higher in GF mice. These findings suggest that the gut microbiota downregulates genes involved in appetite suppression, modulates GPCRs linked to gut hormone secretion, and contributes to leptin resistance, particularly in males. This research underscores the importance of the gut microbiome in host metabolism and reveals potential molecular targets for novel treatments of metabolic diseases.
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spelling doaj-art-4eb24fce5e5f4c4b9bea960e441cd7802025-08-20T04:27:55ZengWileyPhysiological Reports2051-817X2025-05-011310n/an/a10.14814/phy2.70373Microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gutWynne Milhouse0Anna Clapp Organski1Xun Sun2Derek Ai3Baohua Zhou4Tzu‐Wen L. Cross5Hongxia Ren6Department of Pediatrics Herman B. Wells Center for Pediatric Research, Indiana University School of Medicine Indianapolis Indiana USADepartment of Nutrition Science Purdue University West Lafayette Indiana USADepartment of Pediatrics Herman B. Wells Center for Pediatric Research, Indiana University School of Medicine Indianapolis Indiana USACenter for Diabetes and Metabolic Disease Indiana University School of Medicine Indianapolis Indiana USADepartment of Pediatrics Herman B. Wells Center for Pediatric Research, Indiana University School of Medicine Indianapolis Indiana USADepartment of Nutrition Science Purdue University West Lafayette Indiana USADepartment of Pediatrics Herman B. Wells Center for Pediatric Research, Indiana University School of Medicine Indianapolis Indiana USAAbstract The gut microbiome (GMB) regulates digestion, metabolism, immunity, and energy homeostasis. This study investigates how gut microbiota integrate the regulation in the neuroendocrine and enteroendocrine systems, with a focus on G protein‐coupled receptors (GPCRs) in the brain‐gut axis and sex differences. Germ‐free (GF) mice exhibited increased hypothalamic expression of the anorexigenic neuropeptide and decreased expression of the negative regulator of leptin signaling. GF males had significantly lower serum leptin levels compared to conventional (CON) males, highlighting a potential link between the microbiome and leptin resistance. In the gut, GF mice demonstrated heightened expression of anorexigenic gut hormones, including peptide YY (Pyy) and cholecystokinin (Cck), in addition to increased levels of G protein‐coupled receptors (GPCRs) involved in gut hormone secretion and nutrient metabolism, particularly in females. While carbohydrate metabolism genes were upregulated in CON mice, lipid metabolism genes were predominantly higher in GF mice. These findings suggest that the gut microbiota downregulates genes involved in appetite suppression, modulates GPCRs linked to gut hormone secretion, and contributes to leptin resistance, particularly in males. This research underscores the importance of the gut microbiome in host metabolism and reveals potential molecular targets for novel treatments of metabolic diseases.https://doi.org/10.14814/phy2.70373brain‐gut axisdiabetesendocrineGIGPCRintegrative
spellingShingle Wynne Milhouse
Anna Clapp Organski
Xun Sun
Derek Ai
Baohua Zhou
Tzu‐Wen L. Cross
Hongxia Ren
Microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gut
Physiological Reports
brain‐gut axis
diabetes
endocrine
GI
GPCR
integrative
title Microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gut
title_full Microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gut
title_fullStr Microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gut
title_full_unstemmed Microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gut
title_short Microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gut
title_sort microbiome affects mice metabolic homeostasis via differential regulation of gene expression in the brain and gut
topic brain‐gut axis
diabetes
endocrine
GI
GPCR
integrative
url https://doi.org/10.14814/phy2.70373
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