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FGF21 and its underlying adipose tissue-liver axis inform cardiometabolic burden and improvement in obesity after metabolic surgery
This research investigates the determinants of circulating FGF21 levels in a cohort reflecting metabolic disease progression, examining the associations of circulating FGF21 with morphology and function of adipose tissue (AT), and with metabolic adjustments following metabolic surgery. We measured s...
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| Published in: | EBioMedicine 2024-12, Vol.110, p.105458, Article 105458 |
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| creator | Patt, Marie Karkossa, Isabel Krieg, Laura Massier, Lucas Makki, Kassem Tabei, Shirin Karlas, Thomas Dietrich, Arne Gericke, Martin Stumvoll, Michael Blüher, Matthias von Bergen, Martin Schubert, Kristin Kovacs, Peter Chakaroun, Rima M. |
| description | This research investigates the determinants of circulating FGF21 levels in a cohort reflecting metabolic disease progression, examining the associations of circulating FGF21 with morphology and function of adipose tissue (AT), and with metabolic adjustments following metabolic surgery.
We measured serum FGF21 in 678 individuals cross-sectionally and in 189 undergoing metabolic surgery longitudinally. Relationships between FGF21 levels, AT histology, transcriptomes and proteomes, cardiometabolic risk factors, and post-surgery metabolic adjustments were assessed using univariate and multivariate analyses, causal mediation analysis, and network integration of AT transcriptomes and proteomes.
FGF21 levels were linked to central adiposity, subclinical inflammation, insulin resistance, and cardiometabolic risk, and were driven by circulating leptin and liver enzymes. Higher FGF21 were linked with AT dysfunction reflected in fibro-inflammatory and lipid dysmetabolism pathways. Specifically, visceral AT inflammation was tied to both FGF21 elevation and liver dysfunction. Post-surgery, FGF21 peaked transitorily at three months. Mediation analysis highlighted an underlying increased AT catabolic state with elevated free fatty acids (FFA), contributing to higher liver stress and FGF21 levels (total effect of free fatty acids on FGF21 levels: 0.38, p |
| doi_str_mv | 10.1016/j.ebiom.2024.105458 |
| format | article |
| fullrecord | <record><control><sourceid>proquest_swepu</sourceid><recordid>TN_cdi_swepub_primary_oai_gup_ub_gu_se_344722</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S2352396424004948</els_id><sourcerecordid>3134065983</sourcerecordid><originalsourceid>FETCH-LOGICAL-c322t-f45b8a63019b1485323bc84b51432b6d44204638a2d31e898985d014dd7e430b3</originalsourceid><addsrcrecordid>eNp9kUtv1DAUha0K1FalvwAJeckmUz9TZ8ECVUxBqsSmXVt2fDPyKImDHwOz7h_HJaVlhbywdfSdc20fhN5TsqGEtlf7DVgfpg0jTFRFCqlO0DnjkjW8a8Wbf85n6DKlPSGESlFFdYrOqkwUkd05etzebhnFZnbY54TL7CCORz_vsHF-CQlw9ikVaEZ_gIjNL5-wn4cQJ9yb6OoVIBsbRt9jW6KDeY2alhgOMMGcK42DheTzEZsh14xXRypxB_H4Dr0dzJjg8nm_QA_bL_c3X5u777ffbj7fNT1nLDeDkFaZlhPaWSqU5IzbXgkrqeDMtk4IRkTLlWGOU1BdXdIRKpy7BsGJ5ReoWXPTT1iK1Uv0k4lHHYzXu7LoKu2KTqC5ENeMVf7jytfH_CiQsp586mEczQyhJM0pF6SVneIV5Svax5BShOElnBL9VJje6z-F6afC9FpYdX14HlDsBO7F87eeCnxaAajfcvAQdeo9zD04H6HP2gX_3wG_AQ-GqN4</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3134065983</pqid></control><display><type>article</type><title>FGF21 and its underlying adipose tissue-liver axis inform cardiometabolic burden and improvement in obesity after metabolic surgery</title><source>ScienceDirect Additional Titles</source><source>PubMed Central</source><creator>Patt, Marie ; Karkossa, Isabel ; Krieg, Laura ; Massier, Lucas ; Makki, Kassem ; Tabei, Shirin ; Karlas, Thomas ; Dietrich, Arne ; Gericke, Martin ; Stumvoll, Michael ; Blüher, Matthias ; von Bergen, Martin ; Schubert, Kristin ; Kovacs, Peter ; Chakaroun, Rima M.</creator><creatorcontrib>Patt, Marie ; Karkossa, Isabel ; Krieg, Laura ; Massier, Lucas ; Makki, Kassem ; Tabei, Shirin ; Karlas, Thomas ; Dietrich, Arne ; Gericke, Martin ; Stumvoll, Michael ; Blüher, Matthias ; von Bergen, Martin ; Schubert, Kristin ; Kovacs, Peter ; Chakaroun, Rima M.</creatorcontrib><description>This research investigates the determinants of circulating FGF21 levels in a cohort reflecting metabolic disease progression, examining the associations of circulating FGF21 with morphology and function of adipose tissue (AT), and with metabolic adjustments following metabolic surgery.
We measured serum FGF21 in 678 individuals cross-sectionally and in 189 undergoing metabolic surgery longitudinally. Relationships between FGF21 levels, AT histology, transcriptomes and proteomes, cardiometabolic risk factors, and post-surgery metabolic adjustments were assessed using univariate and multivariate analyses, causal mediation analysis, and network integration of AT transcriptomes and proteomes.
FGF21 levels were linked to central adiposity, subclinical inflammation, insulin resistance, and cardiometabolic risk, and were driven by circulating leptin and liver enzymes. Higher FGF21 were linked with AT dysfunction reflected in fibro-inflammatory and lipid dysmetabolism pathways. Specifically, visceral AT inflammation was tied to both FGF21 elevation and liver dysfunction. Post-surgery, FGF21 peaked transitorily at three months. Mediation analysis highlighted an underlying increased AT catabolic state with elevated free fatty acids (FFA), contributing to higher liver stress and FGF21 levels (total effect of free fatty acids on FGF21 levels: 0.38, p < 0.01; proportion mediation via liver 32%, p < 0.01). In line with this, histological AT fibrosis linked with less pronounced FGF21 responses and reduced fat loss post-surgery (FFA and visceral AT fibrosis: rho = −0.31, p = 0.030; FFA and fat-mass loss: rho = 0.17, p = 0.020).
FGF21 reflects the liver's disproportionate metabolic stress response in both central adiposity and after metabolic surgery, with its dynamics reflecting an AT-liver crosstalk.
This work was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) through CRC 1052, project number 209933838, CRC1382 and a Walther-Benjamin Fellowship and by a junior research grant by the Medical Faculty, University of Leipzig, and by the Federal Ministry of Education and Research (BMBF), Germany, FKZ: 01EO1501. Part of this work was supported by the European Union’s Seventh Framework Program for research, technological development and demonstration under grant agreement HEALTH-F4-2012-305312 and by the CRC1382 and the Novo Nordisk Foundation and by the Deutsche Forschungsgemeinschaft (DFG, German Research foundation) project number 530364326.</description><identifier>ISSN: 2352-3964</identifier><identifier>EISSN: 2352-3964</identifier><identifier>DOI: 10.1016/j.ebiom.2024.105458</identifier><identifier>PMID: 39608059</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Adipose tissue ; Adipose Tissue - metabolism ; Adult ; Allmänmedicin ; Biomarkers ; Cardiometabolic Risk Factors ; Cross-Sectional Studies ; Female ; FGF21 ; Fibroblast Growth Factors - blood ; Fibroblast Growth Factors - metabolism ; General Medicine ; Humans ; Insulin resistance ; Inter-organ crosstalk ; Liver - metabolism ; Liver - pathology ; Liver - surgery ; Male ; Metabolic disease ; Metabolic surgery ; Middle Aged ; Obesity ; Obesity - metabolism ; Obesity - surgery</subject><ispartof>EBioMedicine, 2024-12, Vol.110, p.105458, Article 105458</ispartof><rights>2024 The Author(s)</rights><rights>Copyright © 2024 The Author(s). Published by Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c322t-f45b8a63019b1485323bc84b51432b6d44204638a2d31e898985d014dd7e430b3</cites><orcidid>0000-0002-8109-8526 ; 0000-0001-9901-1815</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S2352396424004948$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3536,27901,27902,45756</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39608059$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://gup.ub.gu.se/publication/344722$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Patt, Marie</creatorcontrib><creatorcontrib>Karkossa, Isabel</creatorcontrib><creatorcontrib>Krieg, Laura</creatorcontrib><creatorcontrib>Massier, Lucas</creatorcontrib><creatorcontrib>Makki, Kassem</creatorcontrib><creatorcontrib>Tabei, Shirin</creatorcontrib><creatorcontrib>Karlas, Thomas</creatorcontrib><creatorcontrib>Dietrich, Arne</creatorcontrib><creatorcontrib>Gericke, Martin</creatorcontrib><creatorcontrib>Stumvoll, Michael</creatorcontrib><creatorcontrib>Blüher, Matthias</creatorcontrib><creatorcontrib>von Bergen, Martin</creatorcontrib><creatorcontrib>Schubert, Kristin</creatorcontrib><creatorcontrib>Kovacs, Peter</creatorcontrib><creatorcontrib>Chakaroun, Rima M.</creatorcontrib><title>FGF21 and its underlying adipose tissue-liver axis inform cardiometabolic burden and improvement in obesity after metabolic surgery</title><title>EBioMedicine</title><addtitle>EBioMedicine</addtitle><description>This research investigates the determinants of circulating FGF21 levels in a cohort reflecting metabolic disease progression, examining the associations of circulating FGF21 with morphology and function of adipose tissue (AT), and with metabolic adjustments following metabolic surgery.
We measured serum FGF21 in 678 individuals cross-sectionally and in 189 undergoing metabolic surgery longitudinally. Relationships between FGF21 levels, AT histology, transcriptomes and proteomes, cardiometabolic risk factors, and post-surgery metabolic adjustments were assessed using univariate and multivariate analyses, causal mediation analysis, and network integration of AT transcriptomes and proteomes.
FGF21 levels were linked to central adiposity, subclinical inflammation, insulin resistance, and cardiometabolic risk, and were driven by circulating leptin and liver enzymes. Higher FGF21 were linked with AT dysfunction reflected in fibro-inflammatory and lipid dysmetabolism pathways. Specifically, visceral AT inflammation was tied to both FGF21 elevation and liver dysfunction. Post-surgery, FGF21 peaked transitorily at three months. Mediation analysis highlighted an underlying increased AT catabolic state with elevated free fatty acids (FFA), contributing to higher liver stress and FGF21 levels (total effect of free fatty acids on FGF21 levels: 0.38, p < 0.01; proportion mediation via liver 32%, p < 0.01). In line with this, histological AT fibrosis linked with less pronounced FGF21 responses and reduced fat loss post-surgery (FFA and visceral AT fibrosis: rho = −0.31, p = 0.030; FFA and fat-mass loss: rho = 0.17, p = 0.020).
FGF21 reflects the liver's disproportionate metabolic stress response in both central adiposity and after metabolic surgery, with its dynamics reflecting an AT-liver crosstalk.
This work was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) through CRC 1052, project number 209933838, CRC1382 and a Walther-Benjamin Fellowship and by a junior research grant by the Medical Faculty, University of Leipzig, and by the Federal Ministry of Education and Research (BMBF), Germany, FKZ: 01EO1501. Part of this work was supported by the European Union’s Seventh Framework Program for research, technological development and demonstration under grant agreement HEALTH-F4-2012-305312 and by the CRC1382 and the Novo Nordisk Foundation and by the Deutsche Forschungsgemeinschaft (DFG, German Research foundation) project number 530364326.</description><subject>Adipose tissue</subject><subject>Adipose Tissue - metabolism</subject><subject>Adult</subject><subject>Allmänmedicin</subject><subject>Biomarkers</subject><subject>Cardiometabolic Risk Factors</subject><subject>Cross-Sectional Studies</subject><subject>Female</subject><subject>FGF21</subject><subject>Fibroblast Growth Factors - blood</subject><subject>Fibroblast Growth Factors - metabolism</subject><subject>General Medicine</subject><subject>Humans</subject><subject>Insulin resistance</subject><subject>Inter-organ crosstalk</subject><subject>Liver - metabolism</subject><subject>Liver - pathology</subject><subject>Liver - surgery</subject><subject>Male</subject><subject>Metabolic disease</subject><subject>Metabolic surgery</subject><subject>Middle Aged</subject><subject>Obesity</subject><subject>Obesity - metabolism</subject><subject>Obesity - surgery</subject><issn>2352-3964</issn><issn>2352-3964</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kUtv1DAUha0K1FalvwAJeckmUz9TZ8ECVUxBqsSmXVt2fDPyKImDHwOz7h_HJaVlhbywdfSdc20fhN5TsqGEtlf7DVgfpg0jTFRFCqlO0DnjkjW8a8Wbf85n6DKlPSGESlFFdYrOqkwUkd05etzebhnFZnbY54TL7CCORz_vsHF-CQlw9ikVaEZ_gIjNL5-wn4cQJ9yb6OoVIBsbRt9jW6KDeY2alhgOMMGcK42DheTzEZsh14xXRypxB_H4Dr0dzJjg8nm_QA_bL_c3X5u777ffbj7fNT1nLDeDkFaZlhPaWSqU5IzbXgkrqeDMtk4IRkTLlWGOU1BdXdIRKpy7BsGJ5ReoWXPTT1iK1Uv0k4lHHYzXu7LoKu2KTqC5ENeMVf7jytfH_CiQsp586mEczQyhJM0pF6SVneIV5Svax5BShOElnBL9VJje6z-F6afC9FpYdX14HlDsBO7F87eeCnxaAajfcvAQdeo9zD04H6HP2gX_3wG_AQ-GqN4</recordid><startdate>20241201</startdate><enddate>20241201</enddate><creator>Patt, Marie</creator><creator>Karkossa, Isabel</creator><creator>Krieg, Laura</creator><creator>Massier, Lucas</creator><creator>Makki, Kassem</creator><creator>Tabei, Shirin</creator><creator>Karlas, Thomas</creator><creator>Dietrich, Arne</creator><creator>Gericke, Martin</creator><creator>Stumvoll, Michael</creator><creator>Blüher, Matthias</creator><creator>von Bergen, Martin</creator><creator>Schubert, Kristin</creator><creator>Kovacs, Peter</creator><creator>Chakaroun, Rima M.</creator><general>Elsevier B.V</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>F1U</scope><orcidid>https://orcid.org/0000-0002-8109-8526</orcidid><orcidid>https://orcid.org/0000-0001-9901-1815</orcidid></search><sort><creationdate>20241201</creationdate><title>FGF21 and its underlying adipose tissue-liver axis inform cardiometabolic burden and improvement in obesity after metabolic surgery</title><author>Patt, Marie ; Karkossa, Isabel ; Krieg, Laura ; Massier, Lucas ; Makki, Kassem ; Tabei, Shirin ; Karlas, Thomas ; Dietrich, Arne ; Gericke, Martin ; Stumvoll, Michael ; Blüher, Matthias ; von Bergen, Martin ; Schubert, Kristin ; Kovacs, Peter ; Chakaroun, Rima M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c322t-f45b8a63019b1485323bc84b51432b6d44204638a2d31e898985d014dd7e430b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adipose tissue</topic><topic>Adipose Tissue - metabolism</topic><topic>Adult</topic><topic>Allmänmedicin</topic><topic>Biomarkers</topic><topic>Cardiometabolic Risk Factors</topic><topic>Cross-Sectional Studies</topic><topic>Female</topic><topic>FGF21</topic><topic>Fibroblast Growth Factors - blood</topic><topic>Fibroblast Growth Factors - metabolism</topic><topic>General Medicine</topic><topic>Humans</topic><topic>Insulin resistance</topic><topic>Inter-organ crosstalk</topic><topic>Liver - metabolism</topic><topic>Liver - pathology</topic><topic>Liver - surgery</topic><topic>Male</topic><topic>Metabolic disease</topic><topic>Metabolic surgery</topic><topic>Middle Aged</topic><topic>Obesity</topic><topic>Obesity - metabolism</topic><topic>Obesity - surgery</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Patt, Marie</creatorcontrib><creatorcontrib>Karkossa, Isabel</creatorcontrib><creatorcontrib>Krieg, Laura</creatorcontrib><creatorcontrib>Massier, Lucas</creatorcontrib><creatorcontrib>Makki, Kassem</creatorcontrib><creatorcontrib>Tabei, Shirin</creatorcontrib><creatorcontrib>Karlas, Thomas</creatorcontrib><creatorcontrib>Dietrich, Arne</creatorcontrib><creatorcontrib>Gericke, Martin</creatorcontrib><creatorcontrib>Stumvoll, Michael</creatorcontrib><creatorcontrib>Blüher, Matthias</creatorcontrib><creatorcontrib>von Bergen, Martin</creatorcontrib><creatorcontrib>Schubert, Kristin</creatorcontrib><creatorcontrib>Kovacs, Peter</creatorcontrib><creatorcontrib>Chakaroun, Rima M.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Göteborgs universitet</collection><jtitle>EBioMedicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Patt, Marie</au><au>Karkossa, Isabel</au><au>Krieg, Laura</au><au>Massier, Lucas</au><au>Makki, Kassem</au><au>Tabei, Shirin</au><au>Karlas, Thomas</au><au>Dietrich, Arne</au><au>Gericke, Martin</au><au>Stumvoll, Michael</au><au>Blüher, Matthias</au><au>von Bergen, Martin</au><au>Schubert, Kristin</au><au>Kovacs, Peter</au><au>Chakaroun, Rima M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>FGF21 and its underlying adipose tissue-liver axis inform cardiometabolic burden and improvement in obesity after metabolic surgery</atitle><jtitle>EBioMedicine</jtitle><addtitle>EBioMedicine</addtitle><date>2024-12-01</date><risdate>2024</risdate><volume>110</volume><spage>105458</spage><pages>105458-</pages><artnum>105458</artnum><issn>2352-3964</issn><eissn>2352-3964</eissn><abstract>This research investigates the determinants of circulating FGF21 levels in a cohort reflecting metabolic disease progression, examining the associations of circulating FGF21 with morphology and function of adipose tissue (AT), and with metabolic adjustments following metabolic surgery.
We measured serum FGF21 in 678 individuals cross-sectionally and in 189 undergoing metabolic surgery longitudinally. Relationships between FGF21 levels, AT histology, transcriptomes and proteomes, cardiometabolic risk factors, and post-surgery metabolic adjustments were assessed using univariate and multivariate analyses, causal mediation analysis, and network integration of AT transcriptomes and proteomes.
FGF21 levels were linked to central adiposity, subclinical inflammation, insulin resistance, and cardiometabolic risk, and were driven by circulating leptin and liver enzymes. Higher FGF21 were linked with AT dysfunction reflected in fibro-inflammatory and lipid dysmetabolism pathways. Specifically, visceral AT inflammation was tied to both FGF21 elevation and liver dysfunction. Post-surgery, FGF21 peaked transitorily at three months. Mediation analysis highlighted an underlying increased AT catabolic state with elevated free fatty acids (FFA), contributing to higher liver stress and FGF21 levels (total effect of free fatty acids on FGF21 levels: 0.38, p < 0.01; proportion mediation via liver 32%, p < 0.01). In line with this, histological AT fibrosis linked with less pronounced FGF21 responses and reduced fat loss post-surgery (FFA and visceral AT fibrosis: rho = −0.31, p = 0.030; FFA and fat-mass loss: rho = 0.17, p = 0.020).
FGF21 reflects the liver's disproportionate metabolic stress response in both central adiposity and after metabolic surgery, with its dynamics reflecting an AT-liver crosstalk.
This work was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) through CRC 1052, project number 209933838, CRC1382 and a Walther-Benjamin Fellowship and by a junior research grant by the Medical Faculty, University of Leipzig, and by the Federal Ministry of Education and Research (BMBF), Germany, FKZ: 01EO1501. Part of this work was supported by the European Union’s Seventh Framework Program for research, technological development and demonstration under grant agreement HEALTH-F4-2012-305312 and by the CRC1382 and the Novo Nordisk Foundation and by the Deutsche Forschungsgemeinschaft (DFG, German Research foundation) project number 530364326.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>39608059</pmid><doi>10.1016/j.ebiom.2024.105458</doi><orcidid>https://orcid.org/0000-0002-8109-8526</orcidid><orcidid>https://orcid.org/0000-0001-9901-1815</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adipose tissue Adipose Tissue - metabolism Adult Allmänmedicin Biomarkers Cardiometabolic Risk Factors Cross-Sectional Studies Female FGF21 Fibroblast Growth Factors - blood Fibroblast Growth Factors - metabolism General Medicine Humans Insulin resistance Inter-organ crosstalk Liver - metabolism Liver - pathology Liver - surgery Male Metabolic disease Metabolic surgery Middle Aged Obesity Obesity - metabolism Obesity - surgery |
| title | FGF21 and its underlying adipose tissue-liver axis inform cardiometabolic burden and improvement in obesity after metabolic surgery |
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