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Cited by 182Gut microbiota and healthRegulation of Appetite and ObesityGastrointestinal motility and disorders

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Increased Oral Detection, but Decreased Intestinal Signaling for Fats in Mice Lacking Gut Microbiota

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Duca, Frank A., Swartz, Timothy D., Sakar, Yassine, Covasa, Mihai·2012·PLoS ONE
DOI 10.1371/journal.pone.0039748PMC PMC3387243
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Abstract

Germ-free (GF) mice lacking intestinal microbiota are significantly leaner than normal (NORM) control mice despite consuming more calories. The contribution of microbiota on the recognition and intake of fats is not known. Thus, we investigated the preference for, and acceptance of, fat emulsions in GF and NORM mice, and associated changes in lingual and intestinal fatty acid receptors, intestinal peptide content, and plasma levels of gut peptides. GF and NORM C57Bl/6J mice were given 48-h two-bottle access to water and increasing concentrations of intralipid emulsions. Gene expression of the lingual fatty acid translocase CD36 and protein expression of intestinal satiety peptides and fatty-acid receptors from isolated intestinal epithelial cells were determined. Differences in intestinal enteroendocrine cells along the length of the GI tract were quantified. Circulating plasma satiety peptides reflecting adiposity and biochemical parameters of fat metabolism were also examined. GF mice had an increased preference and intake of intralipid relative to NORM mice. This was associated with increased lingual CD36 (P<0.05) and decreased intestinal expression of fatty acid receptors GPR40 (P<0.0001), GPR41 (P<0.0001), GPR43 (P<0.05), and GPR120 (P<0.0001) and satiety peptides CCK (P<0.0001), PYY (P<0.001), and GLP-1 (P<0.001). GF mice had fewer enteroendocrine cells in the ileum (P<0.05), and more in the colon (P<0.05), relative to NORM controls. Finally, GF mice had lower levels of circulating leptin and ghrelin (P<0.001), and altered plasma lipid metabolic markers indicative of energy deficits. Increased preference and caloric intake from fats in GF mice are associated with increased oral receptors for fats coupled with broad and marked decreases in expression of intestinal satiety peptides and fatty-acid receptors.

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Figure 1 Preference (A), raw intake (B), and calorie intake from intralipid emulsions (C) in GF and NORM C57B6/J mice during 48-h two-bottle intralipid vs. water tests. (A) GF mice preferred the lowest concentration (0.156% oil) of intralipid emulsion test more than NORM mice. (B) Intake of intralipid emulsions was similar at each concentration tested, but increased overall in GF mice relative to NORM controls. (C) GF mice consumed more energy from the highest concentration (1.25% oil) of intralipid emulsion tested. Data are expressed as means±SEM. *P<0.05 compared to NORM.
Figure 1 Preference (A), raw intake (B), and calorie intake from intralipid emulsions (C) in GF and NORM C57B6/J mice during 48-h two-bottle intralipid vs. water tests. (A) GF mice preferred the lowest concentration (0.156% oil) of intralipid emulsion test more than NORM mice. (B) Intake of intralipid emulsions was similar at each concentration tested, but increased overall in GF mice relative to NORM controls. (C) GF mice consumed more energy from the highest concentration (1.25% oil) of intralipid emulsion tested. Data are expressed as means±SEM. *P<0.05 compared to NORM.CC BY · PubMed Central
Figure 2 Gene expression of (A) lingual CD36, and protein expression of (B) intestinal CD36, and (C) intestinal FIAF. (A) GF mice exhibited 3-fold up-regulation of lingual CD36 mRNA in the posterior lingual epithelium relative to NORM mice during fasting. GF mice displayed a slight, but non-significant, increase in lingual CD36 expression following intralipid exposure. (B) Intestinal CD36 was significantly down-regulated in GF compared to NORM mice. (C) Intestinal FIAF expression was increased over 3-fold in GF relative to NORM mice Data are expressed as means±SEM. *P<0.05, **P<0.01, ***P<0.001, compared to NORM.
Figure 2 Gene expression of (A) lingual CD36, and protein expression of (B) intestinal CD36, and (C) intestinal FIAF. (A) GF mice exhibited 3-fold up-regulation of lingual CD36 mRNA in the posterior lingual epithelium relative to NORM mice during fasting. GF mice displayed a slight, but non-significant, increase in lingual CD36 expression following intralipid exposure. (B) Intestinal CD36 was significantly down-regulated in GF compared to NORM mice. (C) Intestinal FIAF expression was increased over 3-fold in GF relative to NORM mice Data are expressed as means±SEM. *P<0.05, **P<0.01, ***P<0.001, compared to NORM.CC BY · PubMed Central
Figure 3 Intestinal epithelial protein expression of fatty-acid responsive receptors in GF and NORM mice. GF mice displayed down-regulation of proximal intestinal GPR40, 41, 43, and 120 relative to NORM mice. Data are expressed as means±SEM. *P<0.05, ***P<0.001, compared to NORM mice.
Figure 3 Intestinal epithelial protein expression of fatty-acid responsive receptors in GF and NORM mice. GF mice displayed down-regulation of proximal intestinal GPR40, 41, 43, and 120 relative to NORM mice. Data are expressed as means±SEM. *P<0.05, ***P<0.001, compared to NORM mice.CC BY · PubMed Central
Figure 4 Intestinal epithelial protein expression of satiety peptide in GF and NORM mice. GF mice exhibited down-regulation of proximal intestinal CCK, GLP-1 and PYY relative to NORM mice. Data are expressed as means±SEM. **P<0.01, ***P<0.001, compared to NORM mice.
Figure 4 Intestinal epithelial protein expression of satiety peptide in GF and NORM mice. GF mice exhibited down-regulation of proximal intestinal CCK, GLP-1 and PYY relative to NORM mice. Data are expressed as means±SEM. **P<0.01, ***P<0.001, compared to NORM mice.CC BY · PubMed Central
Figure 5 (A) Cell counts of enteroendocrine cells expressing chromogrannin-A and (B) representative microphotographs of ileum and colon sections at 100× magnification. GF mice had significantly less enteroendocrine cells in the ileum, but more in the colon, compared to NORM controls. Data are expressed as means±SEM. *P<0.05, compared to NORM mice.
Figure 5 (A) Cell counts of enteroendocrine cells expressing chromogrannin-A and (B) representative microphotographs of ileum and colon sections at 100× magnification. GF mice had significantly less enteroendocrine cells in the ileum, but more in the colon, compared to NORM controls. Data are expressed as means±SEM. *P<0.05, compared to NORM mice.CC BY · PubMed Central
Figure 6 Plasma levels of (A) leptin, (B) ghrelin, and (C) PYY in GF and NORM mice following an overnight fast or re-feeding with 1-ml of 20% intralipid. (A) Plasma leptin was lower in GF mice relative to NORM controls. Re-feeding elevated plasma leptin in both groups. (B) GF mice displayed lower levels of plasma PYY compared to NORM mice while re-feeding increased plasma PYY in both groups. (C) GF mice exhibited lower circulating of ghrelin in both feeding conditions while re-feeding increased plasma ghrelin in NORM, but not GF mice. Data are expressed as means±SEM. **P<0.01 ***P<0.001, compared to NORM mice. ††P<0.01, ††† P<0.001, compared to fasting condition within group.
Figure 6 Plasma levels of (A) leptin, (B) ghrelin, and (C) PYY in GF and NORM mice following an overnight fast or re-feeding with 1-ml of 20% intralipid. (A) Plasma leptin was lower in GF mice relative to NORM controls. Re-feeding elevated plasma leptin in both groups. (B) GF mice displayed lower levels of plasma PYY compared to NORM mice while re-feeding increased plasma PYY in both groups. (C) GF mice exhibited lower circulating of ghrelin in both feeding conditions while re-feeding increased plasma ghrelin in NORM, but not GF mice. Data are expressed as means±SEM. **P<0.01 ***P<0.001, compared to NORM mice. ††P<0.01, ††† P<0.001, compared to fasting condition within group.CC BY · PubMed Central
Figure 7 Plasma levels of (A) glucose, (B) total triglycerides, (C) cholesterol, and (D) HDL in GF and NORM mice following an overnight fast or re-feeding with 1-ml of 20% intralipid. (A) Plasma glucose levels of GF mice were lower than NORM controls and re-feeding increased glucose levels in GF, but not NORM mice. (B) Plasma triglycerides were similar between both groups and feeding conditions. (C) Plasma total cholesterol was increased in GF mice relative to NORM controls and re-feeding increased cholesterol levels in both NORM and GF mice. (D) Total plasma HDL was increased in GF mice relative to NORM mice with re-feeding increasing total HDL in both groups. Data are expressed as means±SEM. **P<0.01 mice, ***P<0.001 compared to NORM. †P<0.05, †† P<0.01, compared to fasting condition within group.
Figure 7 Plasma levels of (A) glucose, (B) total triglycerides, (C) cholesterol, and (D) HDL in GF and NORM mice following an overnight fast or re-feeding with 1-ml of 20% intralipid. (A) Plasma glucose levels of GF mice were lower than NORM controls and re-feeding increased glucose levels in GF, but not NORM mice. (B) Plasma triglycerides were similar between both groups and feeding conditions. (C) Plasma total cholesterol was increased in GF mice relative to NORM controls and re-feeding increased cholesterol levels in both NORM and GF mice. (D) Total plasma HDL was increased in GF mice relative to NORM mice with re-feeding increasing total HDL in both groups. Data are expressed as means±SEM. **P<0.01 mice, ***P<0.001 compared to NORM. †P<0.05, †† P<0.01, compared to fasting condition within group.CC BY · PubMed Central

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  1. Y Demarne, 1972, Gastrointestinal flora and fat digestion in monogastrics., Ann Biol Anim Biochim Biophys, 12, 509

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Metadata

Authors
Duca, F. A., Swartz, T. D., Sakar, Y., & Covasa, M.
Affiliations
Microbiologie de l’alimentation au service de la santé (FR)
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2012-06-29
Volume
7
Issue
6
Pages
e39748
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0039748
PMC
PMC3387243
OpenAlex
W2061559910
Cited by
181
References
40
Citations by year
2026: 5 · 2025: 9 · 2024: 17 · 2023: 12 · 2022: 15 · 2021: 14 · 2020: 24 · 2019: 21 · 2018: 16 · 2017: 14 · 2016: 9 · 2015: 8 · 2014: 10 · 2013: 7
FWCI
3.22
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Institut National de la Recherche Agronomique
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords
gut microbiota, germ-free mice, dietary fat intake, fat preference, fatty acid receptor, CD36, GPR40, GPR41, GPR43, GPR120, satiety peptides, cholecystokinin, peptide YY, glucagon-like peptide-1, enteroendocrine cells, leptin, ghrelin, energy homeostasis, lipid emulsions
MeSH terms
Animals, Blood Glucose, Body Weight, Energy Intake, Cell Count, Emulsions, Gastrointestinal Hormones, Gene Expression Regulation, Germ-Free Life, Intestinal Mucosa, Intestines, Lipids, Male, Mice, Inbred C57BL, Mouth, Oils, Peptides, Signal Transduction, CD36 Antigens, Enteroendocrine Cells, Lipid Metabolism, Mice, Metagenome

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