Thermogenic adipocyte-derived zinc promotes sympathetic innervation in male mice
Sympathetic neurons activate thermogenic adipocytes through release of catecholamine; however, the regulation of sympathetic innervation by thermogenic adipocytes is unclear. Here, we identify primary zinc ion (Zn) as a thermogenic adipocyte-secreted factor that promotes sympathetic innervation and...
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| Veröffentlicht in: | Nature metabolism 2023-03, Vol.5 (3), p.481-494 |
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| creator | Jiang, Junkun Zhou, Donglei Zhang, Anke Yu, Wenjing Du, Lei Yuan, Huiwen Zhang, Chuan Wang, Zelin Jia, Xuyang Zhang, Zhen-Ning Luan, Bing |
| description | Sympathetic neurons activate thermogenic adipocytes through release of catecholamine; however, the regulation of sympathetic innervation by thermogenic adipocytes is unclear. Here, we identify primary zinc ion (Zn) as a thermogenic adipocyte-secreted factor that promotes sympathetic innervation and thermogenesis in brown adipose tissue and subcutaneous white adipose tissue in male mice. Depleting thermogenic adipocytes or antagonizing β
3
-adrenergic receptor on adipocytes impairs sympathetic innervation. In obesity, inflammation-induced upregulation of Zn chaperone protein metallothionein-2 decreases Zn secretion from thermogenic adipocytes and leads to decreased energy expenditure. Furthermore, Zn supplementation ameliorates obesity by promoting sympathetic neuron-induced thermogenesis, while sympathetic denervation abrogates this antiobesity effect. Thus, we have identified a positive feedback mechanism for the reciprocal regulation of thermogenic adipocytes and sympathetic neurons. This mechanism is important for adaptive thermogenesis and could serve as a potential target for the treatment of obesity.
Sympathetic innervation of brown and white adipose tissue is shown to be promoted by zinc released from thermogenic adipocytes, revealing a positive feedback mechanism for regulation of thermogenesis and thereby energy expenditure. |
| doi_str_mv | 10.1038/s42255-023-00751-9 |
| format | Article |
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3
-adrenergic receptor on adipocytes impairs sympathetic innervation. In obesity, inflammation-induced upregulation of Zn chaperone protein metallothionein-2 decreases Zn secretion from thermogenic adipocytes and leads to decreased energy expenditure. Furthermore, Zn supplementation ameliorates obesity by promoting sympathetic neuron-induced thermogenesis, while sympathetic denervation abrogates this antiobesity effect. Thus, we have identified a positive feedback mechanism for the reciprocal regulation of thermogenic adipocytes and sympathetic neurons. This mechanism is important for adaptive thermogenesis and could serve as a potential target for the treatment of obesity.
Sympathetic innervation of brown and white adipose tissue is shown to be promoted by zinc released from thermogenic adipocytes, revealing a positive feedback mechanism for regulation of thermogenesis and thereby energy expenditure.</description><identifier>ISSN: 2522-5812</identifier><identifier>EISSN: 2522-5812</identifier><identifier>DOI: 10.1038/s42255-023-00751-9</identifier><identifier>PMID: 36879120</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13 ; 13/51 ; 14/19 ; 38/1 ; 38/35 ; 38/77 ; 38/90 ; 631/443/319/2723 ; 631/443/376 ; 631/80/86/2372 ; 64/60 ; 82 ; 96 ; 96/21 ; 96/63 ; Adipocytes - metabolism ; Adipose Tissue, Brown - metabolism ; Animals ; Biomedical and Life Sciences ; Life Sciences ; Male ; Mice ; Obesity - metabolism ; Thermogenesis ; Zinc - metabolism ; Zinc - pharmacology</subject><ispartof>Nature metabolism, 2023-03, Vol.5 (3), p.481-494</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to Springer Nature Limited.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c347t-ea1fd90bbb48256047db5ddbb7d2b28714fc8846a1a7b999a262d2f61eb51a2d3</citedby><cites>FETCH-LOGICAL-c347t-ea1fd90bbb48256047db5ddbb7d2b28714fc8846a1a7b999a262d2f61eb51a2d3</cites><orcidid>0000-0002-0409-2964</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s42255-023-00751-9$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s42255-023-00751-9$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27903,27904,41467,42536,51297</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36879120$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jiang, Junkun</creatorcontrib><creatorcontrib>Zhou, Donglei</creatorcontrib><creatorcontrib>Zhang, Anke</creatorcontrib><creatorcontrib>Yu, Wenjing</creatorcontrib><creatorcontrib>Du, Lei</creatorcontrib><creatorcontrib>Yuan, Huiwen</creatorcontrib><creatorcontrib>Zhang, Chuan</creatorcontrib><creatorcontrib>Wang, Zelin</creatorcontrib><creatorcontrib>Jia, Xuyang</creatorcontrib><creatorcontrib>Zhang, Zhen-Ning</creatorcontrib><creatorcontrib>Luan, Bing</creatorcontrib><title>Thermogenic adipocyte-derived zinc promotes sympathetic innervation in male mice</title><title>Nature metabolism</title><addtitle>Nat Metab</addtitle><addtitle>Nat Metab</addtitle><description>Sympathetic neurons activate thermogenic adipocytes through release of catecholamine; however, the regulation of sympathetic innervation by thermogenic adipocytes is unclear. Here, we identify primary zinc ion (Zn) as a thermogenic adipocyte-secreted factor that promotes sympathetic innervation and thermogenesis in brown adipose tissue and subcutaneous white adipose tissue in male mice. Depleting thermogenic adipocytes or antagonizing β
3
-adrenergic receptor on adipocytes impairs sympathetic innervation. In obesity, inflammation-induced upregulation of Zn chaperone protein metallothionein-2 decreases Zn secretion from thermogenic adipocytes and leads to decreased energy expenditure. Furthermore, Zn supplementation ameliorates obesity by promoting sympathetic neuron-induced thermogenesis, while sympathetic denervation abrogates this antiobesity effect. Thus, we have identified a positive feedback mechanism for the reciprocal regulation of thermogenic adipocytes and sympathetic neurons. This mechanism is important for adaptive thermogenesis and could serve as a potential target for the treatment of obesity.
Sympathetic innervation of brown and white adipose tissue is shown to be promoted by zinc released from thermogenic adipocytes, revealing a positive feedback mechanism for regulation of thermogenesis and thereby energy expenditure.</description><subject>13</subject><subject>13/51</subject><subject>14/19</subject><subject>38/1</subject><subject>38/35</subject><subject>38/77</subject><subject>38/90</subject><subject>631/443/319/2723</subject><subject>631/443/376</subject><subject>631/80/86/2372</subject><subject>64/60</subject><subject>82</subject><subject>96</subject><subject>96/21</subject><subject>96/63</subject><subject>Adipocytes - metabolism</subject><subject>Adipose Tissue, Brown - metabolism</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Mice</subject><subject>Obesity - metabolism</subject><subject>Thermogenesis</subject><subject>Zinc - metabolism</subject><subject>Zinc - pharmacology</subject><issn>2522-5812</issn><issn>2522-5812</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1PwzAMhiMEYtPYH-CAeuRSSNy0TY9o4kuaBIdxjpLG3TL1YyTtpPHrCXQgTpxsyY9f2Q8hl4zeMJqIW88B0jSmkMSU5imLixMyhRQgTgWD0z_9hMy931JKgTHOoDgnkyQTecGATsnraoOu6dbY2jJSxu668tBjbNDZPZrow7ZltHNd0_XoI39odqrfYB9Y27bo9qq3XRv6qFE1Ro0t8YKcVar2OD_WGXl7uF8tnuLly-Pz4m4ZlwnP-xgVq0xBtdZcQJpRnhudGqN1bkCDyBmvSiF4ppjKdVEUCjIwUGUMdcoUmGRGrsfccN37gL6XjfUl1rVqsRu8hFzwRHBKeUBhREvXee-wkjtnG-UOklH5JVOOMmWQKb9lyiIsXR3zB92g-V35UReAZAR8GLVrdHLbDa4NP_8X-wm40ICA</recordid><startdate>20230301</startdate><enddate>20230301</enddate><creator>Jiang, Junkun</creator><creator>Zhou, Donglei</creator><creator>Zhang, Anke</creator><creator>Yu, Wenjing</creator><creator>Du, Lei</creator><creator>Yuan, Huiwen</creator><creator>Zhang, Chuan</creator><creator>Wang, Zelin</creator><creator>Jia, Xuyang</creator><creator>Zhang, Zhen-Ning</creator><creator>Luan, Bing</creator><general>Nature Publishing Group UK</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>7X8</scope><orcidid>https://orcid.org/0000-0002-0409-2964</orcidid></search><sort><creationdate>20230301</creationdate><title>Thermogenic adipocyte-derived zinc promotes sympathetic innervation in male mice</title><author>Jiang, Junkun ; Zhou, Donglei ; Zhang, Anke ; Yu, Wenjing ; Du, Lei ; Yuan, Huiwen ; Zhang, Chuan ; Wang, Zelin ; Jia, Xuyang ; Zhang, Zhen-Ning ; Luan, Bing</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c347t-ea1fd90bbb48256047db5ddbb7d2b28714fc8846a1a7b999a262d2f61eb51a2d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>13</topic><topic>13/51</topic><topic>14/19</topic><topic>38/1</topic><topic>38/35</topic><topic>38/77</topic><topic>38/90</topic><topic>631/443/319/2723</topic><topic>631/443/376</topic><topic>631/80/86/2372</topic><topic>64/60</topic><topic>82</topic><topic>96</topic><topic>96/21</topic><topic>96/63</topic><topic>Adipocytes - metabolism</topic><topic>Adipose Tissue, Brown - metabolism</topic><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Mice</topic><topic>Obesity - metabolism</topic><topic>Thermogenesis</topic><topic>Zinc - metabolism</topic><topic>Zinc - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jiang, Junkun</creatorcontrib><creatorcontrib>Zhou, Donglei</creatorcontrib><creatorcontrib>Zhang, Anke</creatorcontrib><creatorcontrib>Yu, Wenjing</creatorcontrib><creatorcontrib>Du, Lei</creatorcontrib><creatorcontrib>Yuan, Huiwen</creatorcontrib><creatorcontrib>Zhang, Chuan</creatorcontrib><creatorcontrib>Wang, Zelin</creatorcontrib><creatorcontrib>Jia, Xuyang</creatorcontrib><creatorcontrib>Zhang, Zhen-Ning</creatorcontrib><creatorcontrib>Luan, Bing</creatorcontrib><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><jtitle>Nature metabolism</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jiang, Junkun</au><au>Zhou, Donglei</au><au>Zhang, Anke</au><au>Yu, Wenjing</au><au>Du, Lei</au><au>Yuan, Huiwen</au><au>Zhang, Chuan</au><au>Wang, Zelin</au><au>Jia, Xuyang</au><au>Zhang, Zhen-Ning</au><au>Luan, Bing</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Thermogenic adipocyte-derived zinc promotes sympathetic innervation in male mice</atitle><jtitle>Nature metabolism</jtitle><stitle>Nat Metab</stitle><addtitle>Nat Metab</addtitle><date>2023-03-01</date><risdate>2023</risdate><volume>5</volume><issue>3</issue><spage>481</spage><epage>494</epage><pages>481-494</pages><issn>2522-5812</issn><eissn>2522-5812</eissn><abstract>Sympathetic neurons activate thermogenic adipocytes through release of catecholamine; however, the regulation of sympathetic innervation by thermogenic adipocytes is unclear. Here, we identify primary zinc ion (Zn) as a thermogenic adipocyte-secreted factor that promotes sympathetic innervation and thermogenesis in brown adipose tissue and subcutaneous white adipose tissue in male mice. Depleting thermogenic adipocytes or antagonizing β
3
-adrenergic receptor on adipocytes impairs sympathetic innervation. In obesity, inflammation-induced upregulation of Zn chaperone protein metallothionein-2 decreases Zn secretion from thermogenic adipocytes and leads to decreased energy expenditure. Furthermore, Zn supplementation ameliorates obesity by promoting sympathetic neuron-induced thermogenesis, while sympathetic denervation abrogates this antiobesity effect. Thus, we have identified a positive feedback mechanism for the reciprocal regulation of thermogenic adipocytes and sympathetic neurons. This mechanism is important for adaptive thermogenesis and could serve as a potential target for the treatment of obesity.
Sympathetic innervation of brown and white adipose tissue is shown to be promoted by zinc released from thermogenic adipocytes, revealing a positive feedback mechanism for regulation of thermogenesis and thereby energy expenditure.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>36879120</pmid><doi>10.1038/s42255-023-00751-9</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-0409-2964</orcidid></addata></record> |
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| subjects | 13 13/51 14/19 38/1 38/35 38/77 38/90 631/443/319/2723 631/443/376 631/80/86/2372 64/60 82 96 96/21 96/63 Adipocytes - metabolism Adipose Tissue, Brown - metabolism Animals Biomedical and Life Sciences Life Sciences Male Mice Obesity - metabolism Thermogenesis Zinc - metabolism Zinc - pharmacology |
| title | Thermogenic adipocyte-derived zinc promotes sympathetic innervation in male mice |
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