Testosterone is sequestered in dysfunctional adipose tissue, modifying androgen-responsive genes
Background/objective The recognized association between male hypogonadism and obesity has multifactorial implications on adipose tissue (AT) physiology. The fat solubility of testosterone (T) suggests a sequestration process in fat depots, leading to reduced circulating levels of T in obesity. Sever...
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| Veröffentlicht in: | International Journal of Obesity 2020-07, Vol.44 (7), p.1617-1625 |
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| container_title | International Journal of Obesity |
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| creator | Di Nisio, Andrea Sabovic, Iva De Toni, Luca Rocca, Maria Santa Dall’Acqua, Stefano Azzena, Bruno De Rocco Ponce, Maurizio Foresta, Carlo |
| description | Background/objective
The recognized association between male hypogonadism and obesity has multifactorial implications on adipose tissue (AT) physiology. The fat solubility of testosterone (T) suggests a sequestration process in fat depots, leading to reduced circulating levels of T in obesity. Several evidence suggest that steroids play a two-sided inhibitory role on adipogenesis by locally decreasing lipid accumulation and by stimulating lipolysis. The current study investigates T trafficking and activity in dysfunctional AT.
Subjects/methods
Samples of subcutaneous AT (SAT) were obtained from explants from lipoaspirate plastic surgery in six obese and six normal weight male patients. Experimental procedures on both SAT explants and insulin-resistant (IR) 3T3-L1 adipocytes were performed, including real-time PCR and mass-spectrometry quantification.
Results
A significant deregulation of gene responsiveness to androgens in IR cells and obese SAT was observed (all
p
|
| doi_str_mv | 10.1038/s41366-020-0568-9 |
| format | Article |
| fullrecord | <record><control><sourceid>gale_proqu</sourceid><recordid>TN_cdi_proquest_miscellaneous_2382674018</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A628215248</galeid><sourcerecordid>A628215248</sourcerecordid><originalsourceid>FETCH-LOGICAL-c498t-f9e28152d17f86b78a0ceb8b31b98801775ae2f53b368f706a8f774aa14b15613</originalsourceid><addsrcrecordid>eNp9kl1rFTEQhhdR7LH6A7yRBUG8cGu-k70spVWh4E29jtndyWnKbnLM7BbOvzfrqdaKSiBhkmdmeCdvVb2k5IQSbt6joFyphjDSEKlM0z6qNlRo1UjR6sfVhnCi1xd5VD1DvCGESEnY0-qIM0Y4pWRTfb0CnBPOkFOEOmCN8G2BNYahDrEe9uiX2M8hRTfWbgi7hFDPAXGBd_WUhuD3IW5rF4ecthCbDLhLEcMt1CUEfF498W5EeHF3HldfLs6vzj42l58_fDo7vWx60Zq58S0wQyUbqPZGddo40kNnOk671hhCtZYOmJe848p4TZQruxbOUdFRqSg_rt4e6u5y-qHATgF7GEcXIS1oGTdMaUGoKejrP9CbtOSir1BlepoLLeT_KWqMUYyze2rrRrAh-jRn16-t7alihhVJYu148heqrAGm0JfJ-1DuHyS8-S3hGtw4X2Mal_Uf8CFID2CfE2IGb3c5TC7vLSV2NYk9mMQWk9jVJLYtOa_ulC3dBMOvjJ-uKAA7AFie4hbyvfR_V_0OsMTEPg</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2418886232</pqid></control><display><type>article</type><title>Testosterone is sequestered in dysfunctional adipose tissue, modifying androgen-responsive genes</title><source>Nature</source><source>Alma/SFX Local Collection</source><creator>Di Nisio, Andrea ; Sabovic, Iva ; De Toni, Luca ; Rocca, Maria Santa ; Dall’Acqua, Stefano ; Azzena, Bruno ; De Rocco Ponce, Maurizio ; Foresta, Carlo</creator><creatorcontrib>Di Nisio, Andrea ; Sabovic, Iva ; De Toni, Luca ; Rocca, Maria Santa ; Dall’Acqua, Stefano ; Azzena, Bruno ; De Rocco Ponce, Maurizio ; Foresta, Carlo</creatorcontrib><description>Background/objective
The recognized association between male hypogonadism and obesity has multifactorial implications on adipose tissue (AT) physiology. The fat solubility of testosterone (T) suggests a sequestration process in fat depots, leading to reduced circulating levels of T in obesity. Several evidence suggest that steroids play a two-sided inhibitory role on adipogenesis by locally decreasing lipid accumulation and by stimulating lipolysis. The current study investigates T trafficking and activity in dysfunctional AT.
Subjects/methods
Samples of subcutaneous AT (SAT) were obtained from explants from lipoaspirate plastic surgery in six obese and six normal weight male patients. Experimental procedures on both SAT explants and insulin-resistant (IR) 3T3-L1 adipocytes were performed, including real-time PCR and mass-spectrometry quantification.
Results
A significant deregulation of gene responsiveness to androgens in IR cells and obese SAT was observed (all
p
< 0.05), together with reduced T release after adrenergic stimulation (−10% compared with −55% in lean SAT,
p
= 0.021). Higher concentrations of intracellular T and estradiol in obese SAT were also observed (2.4 vs. 1.3 ng/g,
p
= 0.013 and 0.075 vs. 0.22 ng/g,
p
= 0.004, respectively). Testosterone accumulation resulted in even lower expression in androgen-responsive genes involved in lipolytic and anti-adipogenic pathways from both in vitro and ex vivo experiments.
Conclusions
These results suggest an altered response of dysfunctional fat cells to testosterone stimulation, which normally favors lipolysis and induces an anti-adipogenic effect. The considerable reduction of lipolytic T release after adrenergic stimulation in obese SAT contributes to AT dysfunction, in a feedforward loop further reducing T levels in obese hypogonadal males.</description><identifier>ISSN: 0307-0565</identifier><identifier>EISSN: 1476-5497</identifier><identifier>DOI: 10.1038/s41366-020-0568-9</identifier><identifier>PMID: 32203110</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/106 ; 17β-Estradiol ; 38/39 ; 38/77 ; 38/90 ; 631/443/319/2723 ; 692/163/2743/393 ; 82/58 ; Accumulation ; Adipocytes ; Adipogenesis ; Adipose tissue ; Adipose tissues ; Androgens ; Body fat ; Deregulation ; Epidemiology ; Explants ; Gene expression ; Genes ; Health Promotion and Disease Prevention ; Hypogonadism ; Insulin ; Internal Medicine ; Lipids ; Lipolysis ; Medicine ; Medicine & Public Health ; Metabolic Diseases ; Obesity ; Physiological aspects ; Plastic surgery ; Public Health ; Sex hormones ; Spectrometry ; Steroid hormones ; Steroids ; Stimulation ; Surgery ; Surgery, Plastic ; Testosterone</subject><ispartof>International Journal of Obesity, 2020-07, Vol.44 (7), p.1617-1625</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2020</rights><rights>COPYRIGHT 2020 Nature Publishing Group</rights><rights>The Author(s), under exclusive licence to Springer Nature Limited 2020.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c498t-f9e28152d17f86b78a0ceb8b31b98801775ae2f53b368f706a8f774aa14b15613</citedby><cites>FETCH-LOGICAL-c498t-f9e28152d17f86b78a0ceb8b31b98801775ae2f53b368f706a8f774aa14b15613</cites><orcidid>0000-0002-6576-2183</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32203110$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Di Nisio, Andrea</creatorcontrib><creatorcontrib>Sabovic, Iva</creatorcontrib><creatorcontrib>De Toni, Luca</creatorcontrib><creatorcontrib>Rocca, Maria Santa</creatorcontrib><creatorcontrib>Dall’Acqua, Stefano</creatorcontrib><creatorcontrib>Azzena, Bruno</creatorcontrib><creatorcontrib>De Rocco Ponce, Maurizio</creatorcontrib><creatorcontrib>Foresta, Carlo</creatorcontrib><title>Testosterone is sequestered in dysfunctional adipose tissue, modifying androgen-responsive genes</title><title>International Journal of Obesity</title><addtitle>Int J Obes</addtitle><addtitle>Int J Obes (Lond)</addtitle><description>Background/objective
The recognized association between male hypogonadism and obesity has multifactorial implications on adipose tissue (AT) physiology. The fat solubility of testosterone (T) suggests a sequestration process in fat depots, leading to reduced circulating levels of T in obesity. Several evidence suggest that steroids play a two-sided inhibitory role on adipogenesis by locally decreasing lipid accumulation and by stimulating lipolysis. The current study investigates T trafficking and activity in dysfunctional AT.
Subjects/methods
Samples of subcutaneous AT (SAT) were obtained from explants from lipoaspirate plastic surgery in six obese and six normal weight male patients. Experimental procedures on both SAT explants and insulin-resistant (IR) 3T3-L1 adipocytes were performed, including real-time PCR and mass-spectrometry quantification.
Results
A significant deregulation of gene responsiveness to androgens in IR cells and obese SAT was observed (all
p
< 0.05), together with reduced T release after adrenergic stimulation (−10% compared with −55% in lean SAT,
p
= 0.021). Higher concentrations of intracellular T and estradiol in obese SAT were also observed (2.4 vs. 1.3 ng/g,
p
= 0.013 and 0.075 vs. 0.22 ng/g,
p
= 0.004, respectively). Testosterone accumulation resulted in even lower expression in androgen-responsive genes involved in lipolytic and anti-adipogenic pathways from both in vitro and ex vivo experiments.
Conclusions
These results suggest an altered response of dysfunctional fat cells to testosterone stimulation, which normally favors lipolysis and induces an anti-adipogenic effect. The considerable reduction of lipolytic T release after adrenergic stimulation in obese SAT contributes to AT dysfunction, in a feedforward loop further reducing T levels in obese hypogonadal males.</description><subject>13/106</subject><subject>17β-Estradiol</subject><subject>38/39</subject><subject>38/77</subject><subject>38/90</subject><subject>631/443/319/2723</subject><subject>692/163/2743/393</subject><subject>82/58</subject><subject>Accumulation</subject><subject>Adipocytes</subject><subject>Adipogenesis</subject><subject>Adipose tissue</subject><subject>Adipose tissues</subject><subject>Androgens</subject><subject>Body fat</subject><subject>Deregulation</subject><subject>Epidemiology</subject><subject>Explants</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Health Promotion and Disease Prevention</subject><subject>Hypogonadism</subject><subject>Insulin</subject><subject>Internal Medicine</subject><subject>Lipids</subject><subject>Lipolysis</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Metabolic Diseases</subject><subject>Obesity</subject><subject>Physiological aspects</subject><subject>Plastic surgery</subject><subject>Public Health</subject><subject>Sex hormones</subject><subject>Spectrometry</subject><subject>Steroid hormones</subject><subject>Steroids</subject><subject>Stimulation</subject><subject>Surgery</subject><subject>Surgery, Plastic</subject><subject>Testosterone</subject><issn>0307-0565</issn><issn>1476-5497</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kl1rFTEQhhdR7LH6A7yRBUG8cGu-k70spVWh4E29jtndyWnKbnLM7BbOvzfrqdaKSiBhkmdmeCdvVb2k5IQSbt6joFyphjDSEKlM0z6qNlRo1UjR6sfVhnCi1xd5VD1DvCGESEnY0-qIM0Y4pWRTfb0CnBPOkFOEOmCN8G2BNYahDrEe9uiX2M8hRTfWbgi7hFDPAXGBd_WUhuD3IW5rF4ecthCbDLhLEcMt1CUEfF498W5EeHF3HldfLs6vzj42l58_fDo7vWx60Zq58S0wQyUbqPZGddo40kNnOk671hhCtZYOmJe848p4TZQruxbOUdFRqSg_rt4e6u5y-qHATgF7GEcXIS1oGTdMaUGoKejrP9CbtOSir1BlepoLLeT_KWqMUYyze2rrRrAh-jRn16-t7alihhVJYu148heqrAGm0JfJ-1DuHyS8-S3hGtw4X2Mal_Uf8CFID2CfE2IGb3c5TC7vLSV2NYk9mMQWk9jVJLYtOa_ulC3dBMOvjJ-uKAA7AFie4hbyvfR_V_0OsMTEPg</recordid><startdate>20200701</startdate><enddate>20200701</enddate><creator>Di 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Group</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7T2</scope><scope>7TK</scope><scope>7TS</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8C1</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-6576-2183</orcidid></search><sort><creationdate>20200701</creationdate><title>Testosterone is sequestered in dysfunctional adipose tissue, modifying androgen-responsive genes</title><author>Di Nisio, Andrea ; Sabovic, Iva ; De Toni, Luca ; Rocca, Maria Santa ; Dall’Acqua, Stefano ; Azzena, Bruno ; De Rocco Ponce, Maurizio ; Foresta, Carlo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c498t-f9e28152d17f86b78a0ceb8b31b98801775ae2f53b368f706a8f774aa14b15613</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>13/106</topic><topic>17β-Estradiol</topic><topic>38/39</topic><topic>38/77</topic><topic>38/90</topic><topic>631/443/319/2723</topic><topic>692/163/2743/393</topic><topic>82/58</topic><topic>Accumulation</topic><topic>Adipocytes</topic><topic>Adipogenesis</topic><topic>Adipose tissue</topic><topic>Adipose tissues</topic><topic>Androgens</topic><topic>Body fat</topic><topic>Deregulation</topic><topic>Epidemiology</topic><topic>Explants</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Health Promotion and Disease Prevention</topic><topic>Hypogonadism</topic><topic>Insulin</topic><topic>Internal Medicine</topic><topic>Lipids</topic><topic>Lipolysis</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Metabolic Diseases</topic><topic>Obesity</topic><topic>Physiological aspects</topic><topic>Plastic surgery</topic><topic>Public Health</topic><topic>Sex hormones</topic><topic>Spectrometry</topic><topic>Steroid hormones</topic><topic>Steroids</topic><topic>Stimulation</topic><topic>Surgery</topic><topic>Surgery, Plastic</topic><topic>Testosterone</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Di Nisio, Andrea</creatorcontrib><creatorcontrib>Sabovic, Iva</creatorcontrib><creatorcontrib>De Toni, Luca</creatorcontrib><creatorcontrib>Rocca, Maria Santa</creatorcontrib><creatorcontrib>Dall’Acqua, Stefano</creatorcontrib><creatorcontrib>Azzena, Bruno</creatorcontrib><creatorcontrib>De Rocco Ponce, Maurizio</creatorcontrib><creatorcontrib>Foresta, Carlo</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health and Safety Science Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><jtitle>International Journal of Obesity</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Di Nisio, Andrea</au><au>Sabovic, Iva</au><au>De Toni, Luca</au><au>Rocca, Maria Santa</au><au>Dall’Acqua, Stefano</au><au>Azzena, Bruno</au><au>De Rocco Ponce, Maurizio</au><au>Foresta, Carlo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Testosterone is sequestered in dysfunctional adipose tissue, modifying androgen-responsive genes</atitle><jtitle>International Journal of Obesity</jtitle><stitle>Int J Obes</stitle><addtitle>Int J Obes (Lond)</addtitle><date>2020-07-01</date><risdate>2020</risdate><volume>44</volume><issue>7</issue><spage>1617</spage><epage>1625</epage><pages>1617-1625</pages><issn>0307-0565</issn><eissn>1476-5497</eissn><abstract>Background/objective
The recognized association between male hypogonadism and obesity has multifactorial implications on adipose tissue (AT) physiology. The fat solubility of testosterone (T) suggests a sequestration process in fat depots, leading to reduced circulating levels of T in obesity. Several evidence suggest that steroids play a two-sided inhibitory role on adipogenesis by locally decreasing lipid accumulation and by stimulating lipolysis. The current study investigates T trafficking and activity in dysfunctional AT.
Subjects/methods
Samples of subcutaneous AT (SAT) were obtained from explants from lipoaspirate plastic surgery in six obese and six normal weight male patients. Experimental procedures on both SAT explants and insulin-resistant (IR) 3T3-L1 adipocytes were performed, including real-time PCR and mass-spectrometry quantification.
Results
A significant deregulation of gene responsiveness to androgens in IR cells and obese SAT was observed (all
p
< 0.05), together with reduced T release after adrenergic stimulation (−10% compared with −55% in lean SAT,
p
= 0.021). Higher concentrations of intracellular T and estradiol in obese SAT were also observed (2.4 vs. 1.3 ng/g,
p
= 0.013 and 0.075 vs. 0.22 ng/g,
p
= 0.004, respectively). Testosterone accumulation resulted in even lower expression in androgen-responsive genes involved in lipolytic and anti-adipogenic pathways from both in vitro and ex vivo experiments.
Conclusions
These results suggest an altered response of dysfunctional fat cells to testosterone stimulation, which normally favors lipolysis and induces an anti-adipogenic effect. The considerable reduction of lipolytic T release after adrenergic stimulation in obese SAT contributes to AT dysfunction, in a feedforward loop further reducing T levels in obese hypogonadal males.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>32203110</pmid><doi>10.1038/s41366-020-0568-9</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-6576-2183</orcidid></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0307-0565 |
| ispartof | International Journal of Obesity, 2020-07, Vol.44 (7), p.1617-1625 |
| issn | 0307-0565 1476-5497 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_2382674018 |
| source | Nature; Alma/SFX Local Collection |
| subjects | 13/106 17β-Estradiol 38/39 38/77 38/90 631/443/319/2723 692/163/2743/393 82/58 Accumulation Adipocytes Adipogenesis Adipose tissue Adipose tissues Androgens Body fat Deregulation Epidemiology Explants Gene expression Genes Health Promotion and Disease Prevention Hypogonadism Insulin Internal Medicine Lipids Lipolysis Medicine Medicine & Public Health Metabolic Diseases Obesity Physiological aspects Plastic surgery Public Health Sex hormones Spectrometry Steroid hormones Steroids Stimulation Surgery Surgery, Plastic Testosterone |
| title | Testosterone is sequestered in dysfunctional adipose tissue, modifying androgen-responsive genes |
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