Epithelial Cell Proliferation Arrest Induced by Lactate and Acetate from Lactobacillus casei and Bifidobacterium breve

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Abstract

In an attempt to identify and characterize how symbiotic bacteria of the gut microbiota affect the molecular and cellular mechanisms of epithelial homeostasis, intestinal epithelial cells were co-cultured with either Lactobacillus or Bifidobacterium as bona fide symbionts to examine potential gene modulations. In addition to genes involved in the innate immune response, genes encoding check-point molecules controlling the cell cycle were among the most modulated in the course of these interactions. In the m-ICcl2 murine cell line, genes encoding cyclin E1 and cyclin D1 were strongly down regulated by L. casei and B. breve respectively. Cell proliferation arrest was accordingly confirmed. Short chain fatty acids (SCFA) were the effectors of this modulation, alone or in conjunction with the acidic pH they generated. These results demonstrate that the production of SCFAs, a characteristic of these symbiotic microorganisms, is potentially an essential regulatory effector of epithelial proliferation in the gut.

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Most cited references 30

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Energy contributions of volatile fatty acids from the gastrointestinal tract in various species.

E BERGMAN (1990)

The VFA, also known as short-chain fatty acids, are produced in the gastrointestinal tract by microbial fermentation of carbohydrates and endogenous substrates, such as mucus. This can be of great advantage to the animal, since no digestive enzymes exist for breaking down cellulose or other complex carbohydrates. The VFA are produced in the largest amounts in herbivorous animal species and especially in the forestomach of ruminants. The VFA, however, also are produced in the lower digestive tract of humans and all animal species, and intestinal fermentation resembles that occurring in the rumen. The principal VFA in either the rumen or large intestine are acetate, propionate, and butyrate and are produced in a ratio varying from approximately 75:15:10 to 40:40:20. Absorption of VFA at their site of production is rapid, and large quantities are metabolized by the ruminal or large intestinal epithelium before reaching the portal blood. Most of the butyrate is converted to ketone bodies or CO2 by the epithelial cells, and nearly all of the remainder is removed by the liver. Propionate is similarly removed by the liver but is largely converted to glucose. Although species differences exist, acetate is used principally by peripheral tissues, especially fat and muscle. Considerable energy is obtained from VFA in herbivorous species, and far more research has been conducted on ruminants than on other species. Significant VFA, however, are now known to be produced in omnivorous species, such as pigs and humans. Current estimates are that VFA contribute approximately 70% to the caloric requirements of ruminants, such as sheep and cattle, approximately 10% for humans, and approximately 20-30% for several other omnivorous or herbivorous animals. The amount of fiber in the diet undoubtedly affects the amount of VFA produced, and thus the contribution of VFA to the energy needs of the body could become considerably greater as the dietary fiber increases. Pigs and some species of monkey most closely resemble humans, and current research should be directed toward examining the fermentation processes and VFA metabolism in those species. In addition to the energetic or nutritional contributions of VFA to the body, the VFA may indirectly influence cholesterol synthesis and even help regulate insulin or glucagon secretion. In addition, VFA production and absorption have a very significant effect on epithelial cell growth, blood flow, and the normal secretory and absorptive functions of the large intestine, cecum, and rumen. The absorption of VFA and sodium, for example, seem to be interdependent, and release of bicarbonate usually occurs during VFA absorption.(ABSTRACT TRUNCATED AT 400 WORDS)

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Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection.

Jason Wong, Linda C. Li (2001)

Recent advances in cDNA and oligonucleotide DNA arrays have made it possible to measure the abundance of mRNA transcripts for many genes simultaneously. The analysis of such experiments is nontrivial because of large data size and many levels of variation introduced at different stages of the experiments. The analysis is further complicated by the large differences that may exist among different probes used to interrogate the same gene. However, an attractive feature of high-density oligonucleotide arrays such as those produced by photolithography and inkjet technology is the standardization of chip manufacturing and hybridization process. As a result, probe-specific biases, although significant, are highly reproducible and predictable, and their adverse effect can be reduced by proper modeling and analysis methods. Here, we propose a statistical model for the probe-level data, and develop model-based estimates for gene expression indexes. We also present model-based methods for identifying and handling cross-hybridizing probes and contaminating array regions. Applications of these results will be presented elsewhere.

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Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon.

Markus Waldecker, Tanja Kautenburger, Heike Daumann … (2008)

Colorectal cancer is the most abundant cause of cancer mortality in the Western world. Nutrition and the microbial flora are considered to have a marked influence on the risk of colorectal cancer, the formation of butyrate and other short-chain fatty acids (SCFAs) possibly playing a major role as chemopreventive products of microbial fermentation in the colon. In this study, we investigated the effects of butyrate, other SCFAs, and of a number of phenolic SCFA and trans-cinnamic acid derivatives formed during the intestinal degradation of polyphenolic constituents of fruits and vegetables on global histone deacetylase (HDAC) activity in nuclear extracts from colon carcinoma cell cultures using tert-butoxycarbonyl-lysine (acetylated)-4-amino-7-methylcoumarin (Boc-Lys(Ac)-AMC) as substrate. Inhibition of HDAC activity, e.g., by butyrate, is related to a suppression of malignant transformation and a stimulation of apoptosis of precancerous colonic cells. In nuclear extracts from HT-29 human colon carcinoma cells, butyrate was found to be the most potent HDAC inhibitor (IC50=0.09 mM), while other SCFAs such as propionate were less potent. In the same assay, p-coumaric acid (IC50=0.19 mM), 3-(4-OH-phenyl)-propionate (IC50=0.62 mM) and caffeic acid (IC50=0.85 mM) were the most potent HDAC inhibitors among the polyphenol metabolites tested. Interestingly, butyrate was also the most potent HDAC inhibitor in a whole-cell HeLa Mad 38-based reporter gene assay, while all polyphenol metabolites and all other SCFAs tested were much less potent; some were completely inactive. The findings suggest that butyrate plays an outstanding role as endogenous HDAC inhibitor in the colon, and that other SCFAs and HDAC-inhibitory polyphenol metabolites present in the colon seem to play a much smaller role, probably because of their limited levels, their marked cytotoxicity and/or their limited intracellular availability.

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Author and article information

Contributors

Nicholas J. Mantis: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 30 April 2013

Volume: 8

Issue: 4

Electronic Location Identifier: e63053

Affiliations

[1 ]Unité de Pathogénie Microbienne Moléculaire, Institut Pasteur, Paris, France

[2 ]INSERM U 786, Institut Pasteur, Paris, France

[3 ]Chaire de Microbiologie et Maladies Infectieuses, Collège de France, Paris, France

[4 ]Genopole, Institut Pasteur, Paris, France

[5 ]Yakult Central Institute for Microbiological Research, Tokyo, Japan

Wadsworth Center, New York State Department of Health, United States of America

Author notes

* E-mail: philippe.sansonetti@ 123456pasteur.fr

Competing Interests: Takahiro Matsuki and Taeko Hara are employees of Yakult Central Institute for Microbiological Research. Danone Research provided a grant for this study. There are no patents, products in development or marketed products to declare. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials.

Conceived and designed the experiments: TM TP PJS. Performed the experiments: TM TP CM TH. Analyzed the data: TM TP BR PJS. Wrote the paper: TM TP PJS.

Article

Publisher ID: PONE-D-12-12578

DOI: 10.1371/journal.pone.0063053

PMC ID: 3639975

PubMed ID: 23646174

SO-VID: f3ed43bf-c3c1-49b5-8d6b-11baf58aa608

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This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 26 April 2012

Date accepted : 30 March 2013

Page count

Pages: 8

Funding

This work was supported by the European Research Council and from grants from Danone Research and Yakult Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Epithelial Cell Proliferation Arrest Induced by Lactate and Acetate from Lactobacillus casei and Bifidobacterium breve

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Abstract

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Gamma Delta T cells

Most cited references 30

Energy contributions of volatile fatty acids from the gastrointestinal tract in various species.

Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection.

Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon.

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