Changes in mechanical properties of adipose tissue after bariatric surgery driven by extracellular matrix remodelling and neovascularization are associated with metabolic improvements
Biomechanical properties of adipose tissue (AT) are closely involved in the development of obesity-associated comorbidities. Bariatric surgery (BS) constitutes the most effective option for a sustained weight loss in addition to improving obesity-associated metabolic diseases including type 2 diabet...
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creator | Unamuno, Xabier Gómez-Ambrosi, Javier Becerril, Sara Álvarez-Cienfuegos, Francisco Javier Ramírez, Beatriz Rodríguez, Amaia Ezquerro, Silvia Valentí, Víctor Moncada, Rafael Mentxaka, Amaia Llorente, Marcos Silva, Camilo Elizalde, María de los Reyes Catalán, Victoria Frühbeck, Gema |
description | Biomechanical properties of adipose tissue (AT) are closely involved in the development of obesity-associated comorbidities. Bariatric surgery (BS) constitutes the most effective option for a sustained weight loss in addition to improving obesity-associated metabolic diseases including type 2 diabetes (T2D). We aimed to determine the impact of weight loss achieved by BS and caloric restriction (CR) on the biomechanical properties of AT. BS but not CR changed the biomechanical properties of epididymal white AT (EWAT) from a diet-induced obesity rat model, which were associated with metabolic improvements. We found decreased gene expression levels of collagens and Lox together with increased elastin and Mmps mRNA levels in EWAT after BS, which were also associated with the biomechanical properties. Moreover, an increased blood vessel density was observed in EWAT after surgery, confirmed by an upregulation of Acta2 and Antxr1 gene expression levels, which was also correlated with the biomechanical properties. Visceral AT from patients with obesity showed increased stiffness after tensile tests compared to the EWAT from the animal model. This study uncovers new insights into EWAT adaptation after BS with decreased collagen crosslink and synthesis as well as an increased degradation together with enhanced blood vessel density providing, simultaneously, higher stiffness and more ductility.
Biomechanical properties of the adipose tissue (AT) are closely involved in the development of obesity-associated comorbidities. In this study, we show for the first time that biomechanical properties of AT determined by E, UTS and strain at UTS are decreased in obesity, being increased after bariatric surgery by the promotion of ECM remodelling and neovascularization. Moreover, these changes in biomechanical properties are associated with improvements in metabolic homeostasis. Consistently, a better characterization of the plasticity and biomechanical properties of the AT after bariatric surgery opens up a new field for the development of innovative strategies for the reduction of fibrosis and inflammation in AT as well as to better understand obesity and its associated comorbidities.
[Display omitted] |
doi_str_mv | 10.1016/j.actbio.2022.01.007 |
format | Article |
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Biomechanical properties of the adipose tissue (AT) are closely involved in the development of obesity-associated comorbidities. In this study, we show for the first time that biomechanical properties of AT determined by E, UTS and strain at UTS are decreased in obesity, being increased after bariatric surgery by the promotion of ECM remodelling and neovascularization. Moreover, these changes in biomechanical properties are associated with improvements in metabolic homeostasis. Consistently, a better characterization of the plasticity and biomechanical properties of the AT after bariatric surgery opens up a new field for the development of innovative strategies for the reduction of fibrosis and inflammation in AT as well as to better understand obesity and its associated comorbidities.
[Display omitted]</description><identifier>ISSN: 1742-7061</identifier><identifier>EISSN: 1878-7568</identifier><identifier>DOI: 10.1016/j.actbio.2022.01.007</identifier><identifier>PMID: 35007786</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Adipose tissue ; Adipose Tissue - metabolism ; Animal models ; Animals ; Bariatric Surgery ; Biomechanical properties ; Biomechanics ; Blood vessels ; Body fat ; Body weight loss ; Collagen ; Collagen - metabolism ; Cross-linking ; Density ; Diabetes mellitus (non-insulin dependent) ; Diabetes Mellitus, Type 2 - complications ; Diabetes Mellitus, Type 2 - metabolism ; Diabetes Mellitus, Type 2 - surgery ; Dietary restrictions ; Ductility ; Elastin ; Extracellular matrix ; Extracellular Matrix - metabolism ; Extracellular matrix remodelling ; Gastrointestinal surgery ; Gene expression ; Humans ; Liquid oxygen ; Mechanical properties ; Metabolic disorders ; Metabolism ; Microfilament Proteins - metabolism ; Obesity ; Obesity - surgery ; Rats ; Receptors, Cell Surface - metabolism ; Stiffness ; Surgery ; Tensile tests ; Vascularization ; Weight control ; Weight Loss</subject><ispartof>Acta biomaterialia, 2022-03, Vol.141, p.264-279</ispartof><rights>2022</rights><rights>Copyright © 2022. Published by Elsevier Ltd.</rights><rights>Copyright Elsevier BV Mar 15, 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c436t-44ff7bca20863bb72e3e2617f000e02b8719176552058fdd11fc99b1bae7d32b3</citedby><cites>FETCH-LOGICAL-c436t-44ff7bca20863bb72e3e2617f000e02b8719176552058fdd11fc99b1bae7d32b3</cites><orcidid>0000-0002-3441-1970 ; 0000-0002-6409-7513 ; 0000-0002-2180-461X ; 0000-0001-6536-1286 ; 0000-0003-4260-1325 ; 0000-0001-5601-1604 ; 0000-0001-7373-9912</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1742706122000071$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35007786$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Unamuno, Xabier</creatorcontrib><creatorcontrib>Gómez-Ambrosi, Javier</creatorcontrib><creatorcontrib>Becerril, Sara</creatorcontrib><creatorcontrib>Álvarez-Cienfuegos, Francisco Javier</creatorcontrib><creatorcontrib>Ramírez, Beatriz</creatorcontrib><creatorcontrib>Rodríguez, Amaia</creatorcontrib><creatorcontrib>Ezquerro, Silvia</creatorcontrib><creatorcontrib>Valentí, Víctor</creatorcontrib><creatorcontrib>Moncada, Rafael</creatorcontrib><creatorcontrib>Mentxaka, Amaia</creatorcontrib><creatorcontrib>Llorente, Marcos</creatorcontrib><creatorcontrib>Silva, Camilo</creatorcontrib><creatorcontrib>Elizalde, María de los Reyes</creatorcontrib><creatorcontrib>Catalán, Victoria</creatorcontrib><creatorcontrib>Frühbeck, Gema</creatorcontrib><title>Changes in mechanical properties of adipose tissue after bariatric surgery driven by extracellular matrix remodelling and neovascularization are associated with metabolic improvements</title><title>Acta biomaterialia</title><addtitle>Acta Biomater</addtitle><description>Biomechanical properties of adipose tissue (AT) are closely involved in the development of obesity-associated comorbidities. Bariatric surgery (BS) constitutes the most effective option for a sustained weight loss in addition to improving obesity-associated metabolic diseases including type 2 diabetes (T2D). We aimed to determine the impact of weight loss achieved by BS and caloric restriction (CR) on the biomechanical properties of AT. BS but not CR changed the biomechanical properties of epididymal white AT (EWAT) from a diet-induced obesity rat model, which were associated with metabolic improvements. We found decreased gene expression levels of collagens and Lox together with increased elastin and Mmps mRNA levels in EWAT after BS, which were also associated with the biomechanical properties. Moreover, an increased blood vessel density was observed in EWAT after surgery, confirmed by an upregulation of Acta2 and Antxr1 gene expression levels, which was also correlated with the biomechanical properties. Visceral AT from patients with obesity showed increased stiffness after tensile tests compared to the EWAT from the animal model. This study uncovers new insights into EWAT adaptation after BS with decreased collagen crosslink and synthesis as well as an increased degradation together with enhanced blood vessel density providing, simultaneously, higher stiffness and more ductility.
Biomechanical properties of the adipose tissue (AT) are closely involved in the development of obesity-associated comorbidities. In this study, we show for the first time that biomechanical properties of AT determined by E, UTS and strain at UTS are decreased in obesity, being increased after bariatric surgery by the promotion of ECM remodelling and neovascularization. Moreover, these changes in biomechanical properties are associated with improvements in metabolic homeostasis. Consistently, a better characterization of the plasticity and biomechanical properties of the AT after bariatric surgery opens up a new field for the development of innovative strategies for the reduction of fibrosis and inflammation in AT as well as to better understand obesity and its associated comorbidities.
[Display omitted]</description><subject>Adipose tissue</subject><subject>Adipose Tissue - metabolism</subject><subject>Animal models</subject><subject>Animals</subject><subject>Bariatric Surgery</subject><subject>Biomechanical properties</subject><subject>Biomechanics</subject><subject>Blood vessels</subject><subject>Body fat</subject><subject>Body weight loss</subject><subject>Collagen</subject><subject>Collagen - metabolism</subject><subject>Cross-linking</subject><subject>Density</subject><subject>Diabetes mellitus (non-insulin dependent)</subject><subject>Diabetes Mellitus, Type 2 - complications</subject><subject>Diabetes Mellitus, Type 2 - metabolism</subject><subject>Diabetes Mellitus, Type 2 - surgery</subject><subject>Dietary restrictions</subject><subject>Ductility</subject><subject>Elastin</subject><subject>Extracellular matrix</subject><subject>Extracellular Matrix - metabolism</subject><subject>Extracellular matrix remodelling</subject><subject>Gastrointestinal surgery</subject><subject>Gene expression</subject><subject>Humans</subject><subject>Liquid oxygen</subject><subject>Mechanical properties</subject><subject>Metabolic disorders</subject><subject>Metabolism</subject><subject>Microfilament Proteins - metabolism</subject><subject>Obesity</subject><subject>Obesity - surgery</subject><subject>Rats</subject><subject>Receptors, Cell Surface - metabolism</subject><subject>Stiffness</subject><subject>Surgery</subject><subject>Tensile tests</subject><subject>Vascularization</subject><subject>Weight control</subject><subject>Weight Loss</subject><issn>1742-7061</issn><issn>1878-7568</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kcuO1DAQRSMEYh7wBwhZYsMmwXYS271BQi1gkEZiA2vLj0qPW0nc2E7PND_G71FRDyxYsLJdPnXr2reqXjHaMMrEu31jXLEhNpxy3lDWUCqfVJdMSVXLXqinuJcdryUV7KK6ynlPaasYV8-ri7ZHWCpxWf3a3pl5B5mEmUzg8BCcGckhxQOkEvAiDsT4cIgZSAk5L0DMUCARa1IwJQVH8pJ2kE7Ep3CEmdgTgYeSjINxXEaTyLRiDyTBFD3WwrwjZvZkhng02a1I-GlKiDMxCdVzjg6VwZP7UO7QVTE2jjgnTGjrCBPMJb-ong1mzPDycb2uvn_6-G17U99-_fxl--G2dl0rSt11wyCtM5wq0VorObTABZMDpRQot0qyDZOi7znt1eA9Y4PbbCyzBqRvuW2vq7dnXRz9Y4Fc9BTy-jKD9pesUUxtqJKCIvrmH3QflzSjO6S6jspWyA6p7ky5FHNOMOhDCpNJJ82oXoPVe30OVq_Baso0ZoVtrx_FFzuB_9v0J0kE3p8BwN84Bkg6uwCzAx8SuKJ9DP-f8BuKc7tm</recordid><startdate>20220315</startdate><enddate>20220315</enddate><creator>Unamuno, Xabier</creator><creator>Gómez-Ambrosi, Javier</creator><creator>Becerril, Sara</creator><creator>Álvarez-Cienfuegos, Francisco Javier</creator><creator>Ramírez, Beatriz</creator><creator>Rodríguez, Amaia</creator><creator>Ezquerro, Silvia</creator><creator>Valentí, Víctor</creator><creator>Moncada, Rafael</creator><creator>Mentxaka, Amaia</creator><creator>Llorente, Marcos</creator><creator>Silva, Camilo</creator><creator>Elizalde, María de los Reyes</creator><creator>Catalán, Victoria</creator><creator>Frühbeck, Gema</creator><general>Elsevier Ltd</general><general>Elsevier BV</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>7QF</scope><scope>7QO</scope><scope>7QQ</scope><scope>7SC</scope><scope>7SE</scope><scope>7SP</scope><scope>7SR</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7U5</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>JG9</scope><scope>JQ2</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-3441-1970</orcidid><orcidid>https://orcid.org/0000-0002-6409-7513</orcidid><orcidid>https://orcid.org/0000-0002-2180-461X</orcidid><orcidid>https://orcid.org/0000-0001-6536-1286</orcidid><orcidid>https://orcid.org/0000-0003-4260-1325</orcidid><orcidid>https://orcid.org/0000-0001-5601-1604</orcidid><orcidid>https://orcid.org/0000-0001-7373-9912</orcidid></search><sort><creationdate>20220315</creationdate><title>Changes in mechanical properties of adipose tissue after bariatric surgery driven by extracellular matrix remodelling and neovascularization are associated with metabolic improvements</title><author>Unamuno, Xabier ; Gómez-Ambrosi, Javier ; Becerril, Sara ; Álvarez-Cienfuegos, Francisco Javier ; Ramírez, Beatriz ; Rodríguez, Amaia ; Ezquerro, Silvia ; Valentí, Víctor ; Moncada, Rafael ; Mentxaka, Amaia ; Llorente, Marcos ; Silva, Camilo ; Elizalde, María de los Reyes ; Catalán, Victoria ; Frühbeck, Gema</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c436t-44ff7bca20863bb72e3e2617f000e02b8719176552058fdd11fc99b1bae7d32b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adipose tissue</topic><topic>Adipose Tissue - metabolism</topic><topic>Animal models</topic><topic>Animals</topic><topic>Bariatric Surgery</topic><topic>Biomechanical properties</topic><topic>Biomechanics</topic><topic>Blood vessels</topic><topic>Body fat</topic><topic>Body weight loss</topic><topic>Collagen</topic><topic>Collagen - metabolism</topic><topic>Cross-linking</topic><topic>Density</topic><topic>Diabetes mellitus (non-insulin dependent)</topic><topic>Diabetes Mellitus, Type 2 - complications</topic><topic>Diabetes Mellitus, Type 2 - metabolism</topic><topic>Diabetes Mellitus, Type 2 - surgery</topic><topic>Dietary restrictions</topic><topic>Ductility</topic><topic>Elastin</topic><topic>Extracellular matrix</topic><topic>Extracellular Matrix - metabolism</topic><topic>Extracellular matrix remodelling</topic><topic>Gastrointestinal surgery</topic><topic>Gene expression</topic><topic>Humans</topic><topic>Liquid oxygen</topic><topic>Mechanical properties</topic><topic>Metabolic disorders</topic><topic>Metabolism</topic><topic>Microfilament Proteins - metabolism</topic><topic>Obesity</topic><topic>Obesity - surgery</topic><topic>Rats</topic><topic>Receptors, Cell Surface - metabolism</topic><topic>Stiffness</topic><topic>Surgery</topic><topic>Tensile tests</topic><topic>Vascularization</topic><topic>Weight control</topic><topic>Weight Loss</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Unamuno, Xabier</creatorcontrib><creatorcontrib>Gómez-Ambrosi, Javier</creatorcontrib><creatorcontrib>Becerril, Sara</creatorcontrib><creatorcontrib>Álvarez-Cienfuegos, Francisco Javier</creatorcontrib><creatorcontrib>Ramírez, Beatriz</creatorcontrib><creatorcontrib>Rodríguez, Amaia</creatorcontrib><creatorcontrib>Ezquerro, Silvia</creatorcontrib><creatorcontrib>Valentí, Víctor</creatorcontrib><creatorcontrib>Moncada, Rafael</creatorcontrib><creatorcontrib>Mentxaka, Amaia</creatorcontrib><creatorcontrib>Llorente, Marcos</creatorcontrib><creatorcontrib>Silva, Camilo</creatorcontrib><creatorcontrib>Elizalde, María de los Reyes</creatorcontrib><creatorcontrib>Catalán, Victoria</creatorcontrib><creatorcontrib>Frühbeck, Gema</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>Aluminium Industry Abstracts</collection><collection>Biotechnology Research Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Acta biomaterialia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Unamuno, Xabier</au><au>Gómez-Ambrosi, Javier</au><au>Becerril, Sara</au><au>Álvarez-Cienfuegos, Francisco Javier</au><au>Ramírez, Beatriz</au><au>Rodríguez, Amaia</au><au>Ezquerro, Silvia</au><au>Valentí, Víctor</au><au>Moncada, Rafael</au><au>Mentxaka, Amaia</au><au>Llorente, Marcos</au><au>Silva, Camilo</au><au>Elizalde, María de los Reyes</au><au>Catalán, Victoria</au><au>Frühbeck, Gema</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Changes in mechanical properties of adipose tissue after bariatric surgery driven by extracellular matrix remodelling and neovascularization are associated with metabolic improvements</atitle><jtitle>Acta biomaterialia</jtitle><addtitle>Acta Biomater</addtitle><date>2022-03-15</date><risdate>2022</risdate><volume>141</volume><spage>264</spage><epage>279</epage><pages>264-279</pages><issn>1742-7061</issn><eissn>1878-7568</eissn><abstract>Biomechanical properties of adipose tissue (AT) are closely involved in the development of obesity-associated comorbidities. Bariatric surgery (BS) constitutes the most effective option for a sustained weight loss in addition to improving obesity-associated metabolic diseases including type 2 diabetes (T2D). We aimed to determine the impact of weight loss achieved by BS and caloric restriction (CR) on the biomechanical properties of AT. BS but not CR changed the biomechanical properties of epididymal white AT (EWAT) from a diet-induced obesity rat model, which were associated with metabolic improvements. We found decreased gene expression levels of collagens and Lox together with increased elastin and Mmps mRNA levels in EWAT after BS, which were also associated with the biomechanical properties. Moreover, an increased blood vessel density was observed in EWAT after surgery, confirmed by an upregulation of Acta2 and Antxr1 gene expression levels, which was also correlated with the biomechanical properties. Visceral AT from patients with obesity showed increased stiffness after tensile tests compared to the EWAT from the animal model. This study uncovers new insights into EWAT adaptation after BS with decreased collagen crosslink and synthesis as well as an increased degradation together with enhanced blood vessel density providing, simultaneously, higher stiffness and more ductility.
Biomechanical properties of the adipose tissue (AT) are closely involved in the development of obesity-associated comorbidities. In this study, we show for the first time that biomechanical properties of AT determined by E, UTS and strain at UTS are decreased in obesity, being increased after bariatric surgery by the promotion of ECM remodelling and neovascularization. Moreover, these changes in biomechanical properties are associated with improvements in metabolic homeostasis. Consistently, a better characterization of the plasticity and biomechanical properties of the AT after bariatric surgery opens up a new field for the development of innovative strategies for the reduction of fibrosis and inflammation in AT as well as to better understand obesity and its associated comorbidities.
[Display omitted]</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>35007786</pmid><doi>10.1016/j.actbio.2022.01.007</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-3441-1970</orcidid><orcidid>https://orcid.org/0000-0002-6409-7513</orcidid><orcidid>https://orcid.org/0000-0002-2180-461X</orcidid><orcidid>https://orcid.org/0000-0001-6536-1286</orcidid><orcidid>https://orcid.org/0000-0003-4260-1325</orcidid><orcidid>https://orcid.org/0000-0001-5601-1604</orcidid><orcidid>https://orcid.org/0000-0001-7373-9912</orcidid><oa>free_for_read</oa></addata></record> |
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source | MEDLINE; Elsevier ScienceDirect Journals |
subjects | Adipose tissue Adipose Tissue - metabolism Animal models Animals Bariatric Surgery Biomechanical properties Biomechanics Blood vessels Body fat Body weight loss Collagen Collagen - metabolism Cross-linking Density Diabetes mellitus (non-insulin dependent) Diabetes Mellitus, Type 2 - complications Diabetes Mellitus, Type 2 - metabolism Diabetes Mellitus, Type 2 - surgery Dietary restrictions Ductility Elastin Extracellular matrix Extracellular Matrix - metabolism Extracellular matrix remodelling Gastrointestinal surgery Gene expression Humans Liquid oxygen Mechanical properties Metabolic disorders Metabolism Microfilament Proteins - metabolism Obesity Obesity - surgery Rats Receptors, Cell Surface - metabolism Stiffness Surgery Tensile tests Vascularization Weight control Weight Loss |
title | Changes in mechanical properties of adipose tissue after bariatric surgery driven by extracellular matrix remodelling and neovascularization are associated with metabolic improvements |
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