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Research Article

Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals Lactobacillus paracasei and Escherichia coli

Asmaa Tazi, João Ricardo Araujo, Céline Mulet, Ellen T. Arena, Giulia Nigro, Thierry Pédron, Philippe J. Sansonetti
Jose A. Vazquez-Boland, Editor
Asmaa Tazi
aUnité de Pathogénie Microbienne Moléculaire, INSERM Unité 1202, Institut Pasteur, Paris, France
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João Ricardo Araujo
aUnité de Pathogénie Microbienne Moléculaire, INSERM Unité 1202, Institut Pasteur, Paris, France
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Céline Mulet
aUnité de Pathogénie Microbienne Moléculaire, INSERM Unité 1202, Institut Pasteur, Paris, France
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Ellen T. Arena
aUnité de Pathogénie Microbienne Moléculaire, INSERM Unité 1202, Institut Pasteur, Paris, France
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Giulia Nigro
aUnité de Pathogénie Microbienne Moléculaire, INSERM Unité 1202, Institut Pasteur, Paris, France
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Thierry Pédron
aUnité de Pathogénie Microbienne Moléculaire, INSERM Unité 1202, Institut Pasteur, Paris, France
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Philippe J. Sansonetti
aUnité de Pathogénie Microbienne Moléculaire, INSERM Unité 1202, Institut Pasteur, Paris, France
bCollège de France, Paris, France
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Jose A. Vazquez-Boland
University of Edinburgh
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DOI: 10.1128/mBio.01493-18
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ABSTRACT

The gut microbiota contributes to nutrients absorption and metabolism by enterocytes, but the molecular mechanisms involved remain poorly understood, and most conclusions are inferred from studies comparing germfree and conventional animals colonized with diverse bacterial species. We selected two model commensal microorganisms, Escherichia coli and Lactobacillus paracasei, to assess the role of the small-intestinal microbiota in modulating lipid absorption and metabolism by the epithelium. Using an integrated approach encompassing cellular and murine models and combining metabolic parameters measurement, lipid droplet imaging, and gene expression analysis, we demonstrated that under homeostatic conditions, L. paracasei promotes fat storage in enterocytes, whereas E. coli enhances lipid catabolism and reduces chylomicron circulating levels. The Akt/mammalian target of sirolimus (mTOR) pathway is inhibited by both bacterial species in vitro, indicating that several regulatory pathways are involved in the distinct intracellular lipid outcomes associated with each bacterial species. Moreover, soluble bacterial factors partially reproduce the effects observed with live microorganisms. However, reduction of chylomicron circulating levels in E. coli-colonized animals is lost under high-fat-diet conditions, whereas it is potentiated by L. paracasei colonization accompanied by resistance to hypercholesterolemia and excess body weight gain.

IMPORTANCE The specific contribution of each bacterial species within a complex microbiota to the regulation of host lipid metabolism remains largely unknown. Using two model commensal microorganisms, L. paracasei and E. coli, we demonstrated that both bacterial species impacted host lipid metabolism in a diet-dependent manner and, notably, that L. paracasei-colonized mice but not E. coli-colonized mice resisted high-fat-diet-induced body weight gain. In addition, we set up cellular models of fatty acid absorption and secretion by enterocytes cocultured with bacteria and showed that, in vitro, both L. paracasei and E. coli inhibited lipid secretion, through increased intracellular fat storage and enhanced lipid catabolism, respectively.

FOOTNOTES

    • Received 10 July 2018
    • Accepted 3 August 2018
    • Published 4 September 2018
  • Copyright © 2018 Tazi et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals Lactobacillus paracasei and Escherichia coli
Asmaa Tazi, João Ricardo Araujo, Céline Mulet, Ellen T. Arena, Giulia Nigro, Thierry Pédron, Philippe J. Sansonetti
mBio Sep 2018, 9 (5) e01493-18; DOI: 10.1128/mBio.01493-18

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Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals Lactobacillus paracasei and Escherichia coli
Asmaa Tazi, João Ricardo Araujo, Céline Mulet, Ellen T. Arena, Giulia Nigro, Thierry Pédron, Philippe J. Sansonetti
mBio Sep 2018, 9 (5) e01493-18; DOI: 10.1128/mBio.01493-18
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KEYWORDS

Escherichia coli
Lactobacillus
chylomicrons
high-fat diet
lipid metabolism
microbiota

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