Determinants of human adipose tissue gene expression: impact of diet, sex, metabolic status, and cis genetic regulation
Weight control diets favorably affect parameters of the metabolic syndrome and delay the onset of diabetic complications. The adaptations occurring in adipose tissue (AT) are likely to have a profound impact on the whole body response as AT is a key target of dietary intervention. Identification of...
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creator | Viguerie, Nathalie Montastier, Emilie Maoret, Jean-José Roussel, Balbine Combes, Marion Valle, Carine Villa-Vialaneix, Nathalie Iacovoni, Jason S Martinez, J Alfredo Holst, Claus Astrup, Arne Vidal, Hubert Clément, Karine Hager, Jorg Saris, Wim H M Langin, Dominique |
description | Weight control diets favorably affect parameters of the metabolic syndrome and delay the onset of diabetic complications. The adaptations occurring in adipose tissue (AT) are likely to have a profound impact on the whole body response as AT is a key target of dietary intervention. Identification of environmental and individual factors controlling AT adaptation is therefore essential. Here, expression of 271 transcripts, selected for regulation according to obesity and weight changes, was determined in 515 individuals before, after 8-week low-calorie diet-induced weight loss, and after 26-week ad libitum weight maintenance diets. For 175 genes, opposite regulation was observed during calorie restriction and weight maintenance phases, independently of variations in body weight. Metabolism and immunity genes showed inverse profiles. During the dietary intervention, network-based analyses revealed strong interconnection between expression of genes involved in de novo lipogenesis and components of the metabolic syndrome. Sex had a marked influence on AT expression of 88 transcripts, which persisted during the entire dietary intervention and after control for fat mass. In women, the influence of body mass index on expression of a subset of genes persisted during the dietary intervention. Twenty-two genes revealed a metabolic syndrome signature common to men and women. Genetic control of AT gene expression by cis signals was observed for 46 genes. Dietary intervention, sex, and cis genetic variants independently controlled AT gene expression. These analyses help understanding the relative importance of environmental and individual factors that control the expression of human AT genes and therefore may foster strategies aimed at improving AT function in metabolic diseases. |
doi_str_mv | 10.1371/journal.pgen.1002959 |
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The adaptations occurring in adipose tissue (AT) are likely to have a profound impact on the whole body response as AT is a key target of dietary intervention. Identification of environmental and individual factors controlling AT adaptation is therefore essential. Here, expression of 271 transcripts, selected for regulation according to obesity and weight changes, was determined in 515 individuals before, after 8-week low-calorie diet-induced weight loss, and after 26-week ad libitum weight maintenance diets. For 175 genes, opposite regulation was observed during calorie restriction and weight maintenance phases, independently of variations in body weight. Metabolism and immunity genes showed inverse profiles. During the dietary intervention, network-based analyses revealed strong interconnection between expression of genes involved in de novo lipogenesis and components of the metabolic syndrome. Sex had a marked influence on AT expression of 88 transcripts, which persisted during the entire dietary intervention and after control for fat mass. In women, the influence of body mass index on expression of a subset of genes persisted during the dietary intervention. Twenty-two genes revealed a metabolic syndrome signature common to men and women. Genetic control of AT gene expression by cis signals was observed for 46 genes. Dietary intervention, sex, and cis genetic variants independently controlled AT gene expression. 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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: Viguerie N, Montastier E, Maoret J-J, Roussel B, Combes M, et al. (2012) Determinants of Human Adipose Tissue Gene Expression: Impact of Diet, Sex, Metabolic Status, and Cis Genetic Regulation. 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The adaptations occurring in adipose tissue (AT) are likely to have a profound impact on the whole body response as AT is a key target of dietary intervention. Identification of environmental and individual factors controlling AT adaptation is therefore essential. Here, expression of 271 transcripts, selected for regulation according to obesity and weight changes, was determined in 515 individuals before, after 8-week low-calorie diet-induced weight loss, and after 26-week ad libitum weight maintenance diets. For 175 genes, opposite regulation was observed during calorie restriction and weight maintenance phases, independently of variations in body weight. Metabolism and immunity genes showed inverse profiles. During the dietary intervention, network-based analyses revealed strong interconnection between expression of genes involved in de novo lipogenesis and components of the metabolic syndrome. 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genetics</subject><subject>Metabolic Syndrome - metabolism</subject><subject>Metabolism</subject><subject>Obesity - genetics</subject><subject>Obesity - metabolism</subject><subject>Physiological aspects</subject><subject>Santé publique et épidémiologie</subject><subject>Sex Factors</subject><subject>Weight control</subject><subject>Weight Loss</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVk11r2zAUhs3YWLtu_2BshsFYIcn0YdnSLgah-2ggrLCvWyHLx4mKbXmW3GX_fnLjlrj0YkMXEkfP-x7pSCeKnmO0wDTDby9t3zWqWrQbaBYYISKYeBAdY8boPEtQ8vBgfRQ9ce4SIcq4yB5HR4QiwmmaHke_P4CHrjaNaryLbRlv-1o1sSpMax3E3jjXQxxSQAy7tgPnjG3exaZulfYDXxjws9jBbhbX4FVuK6Nj55Xv3SxWTRFr4671PsQ72PSV8sHiafSoVJWDZ-N8Ev349PH72fl8ffF5dbZczzUnqZ_rnHIGPC2ZTnWqeC5ypjkFYDlCWmBdaFJkpIQyVyrlqCxyHACugVBBEkVPopd737ayTo41cxJTTBkRVKBArPZEYdWlbDtTq-6PtMrI64DtNlJ14fAVSIw5QSjnWZKUSQZIFBxKzbICFxnOFA9e78dsfV5DoaHxnaomptOdxmzlxl5JmjAhKAsGp3uD7R3Z-XIthxhCGcs4za5wYN-MyTr7qwfnZW2chqpSDdg-3BFxkiBBWBrQV3fQ-ysxUhsVLmua0oYz6sFULiliWGBBSKAW91BhFFAbbRsoTYhPBKcTQWA87PxG9c7J1bev_8F--Xf24ueUfX3AbkFVfuts1Q9f0U3BZA_qzjrXQXn7ChjJoe9uKieHvpNj3wXZi8OHvxXdNBr9C9TxJ20</recordid><startdate>20120901</startdate><enddate>20120901</enddate><creator>Viguerie, Nathalie</creator><creator>Montastier, Emilie</creator><creator>Maoret, Jean-José</creator><creator>Roussel, Balbine</creator><creator>Combes, Marion</creator><creator>Valle, Carine</creator><creator>Villa-Vialaneix, Nathalie</creator><creator>Iacovoni, Jason S</creator><creator>Martinez, J Alfredo</creator><creator>Holst, Claus</creator><creator>Astrup, Arne</creator><creator>Vidal, Hubert</creator><creator>Clément, Karine</creator><creator>Hager, Jorg</creator><creator>Saris, Wim H M</creator><creator>Langin, Dominique</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-1730-9915</orcidid><orcidid>https://orcid.org/0000-0002-2489-3355</orcidid><orcidid>https://orcid.org/0000-0003-1156-0639</orcidid><orcidid>https://orcid.org/0000-0003-4619-6785</orcidid><orcidid>https://orcid.org/0000-0003-0985-0047</orcidid><orcidid>https://orcid.org/0000-0002-9467-0317</orcidid><orcidid>https://orcid.org/0000-0002-2669-7825</orcidid><orcidid>https://orcid.org/0000-0001-8968-8996</orcidid></search><sort><creationdate>20120901</creationdate><title>Determinants of human adipose tissue gene expression: impact of diet, sex, metabolic status, and cis genetic regulation</title><author>Viguerie, Nathalie ; Montastier, Emilie ; Maoret, Jean-José ; Roussel, Balbine ; Combes, Marion ; Valle, Carine ; Villa-Vialaneix, Nathalie ; Iacovoni, Jason S ; Martinez, J Alfredo ; Holst, Claus ; Astrup, Arne ; Vidal, Hubert ; Clément, Karine ; Hager, Jorg ; Saris, Wim H M ; Langin, Dominique</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c826t-cb385e86f5c6c6a8b9b5c83ee5b00c91cdc2d72fefbaa680fdb15c88ce23924a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Adipose Tissue - 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The adaptations occurring in adipose tissue (AT) are likely to have a profound impact on the whole body response as AT is a key target of dietary intervention. Identification of environmental and individual factors controlling AT adaptation is therefore essential. Here, expression of 271 transcripts, selected for regulation according to obesity and weight changes, was determined in 515 individuals before, after 8-week low-calorie diet-induced weight loss, and after 26-week ad libitum weight maintenance diets. For 175 genes, opposite regulation was observed during calorie restriction and weight maintenance phases, independently of variations in body weight. Metabolism and immunity genes showed inverse profiles. During the dietary intervention, network-based analyses revealed strong interconnection between expression of genes involved in de novo lipogenesis and components of the metabolic syndrome. Sex had a marked influence on AT expression of 88 transcripts, which persisted during the entire dietary intervention and after control for fat mass. In women, the influence of body mass index on expression of a subset of genes persisted during the dietary intervention. Twenty-two genes revealed a metabolic syndrome signature common to men and women. Genetic control of AT gene expression by cis signals was observed for 46 genes. Dietary intervention, sex, and cis genetic variants independently controlled AT gene expression. 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recordid | cdi_plos_journals_1313529390 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central |
subjects | Adipose Tissue - metabolism Adipose tissues Biology Body fat Body Mass Index Caloric Restriction Diet Endocrinology and metabolism Energy Intake - genetics Female Gene expression Gene Expression Regulation - genetics Genetic aspects Genetic regulation Genetics Health aspects Human genetics Human health and pathology Humans Life Sciences Lipogenesis - genetics Male Medicine Metabolic disorders Metabolic Syndrome - genetics Metabolic Syndrome - metabolism Metabolism Obesity - genetics Obesity - metabolism Physiological aspects Santé publique et épidémiologie Sex Factors Weight control Weight Loss |
title | Determinants of human adipose tissue gene expression: impact of diet, sex, metabolic status, and cis genetic regulation |
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