Beneficial Metabolic Effects of TREM2 in Obesity Are Uncoupled From Its Expression on Macrophages
Obesity-induced white adipose tissue (WAT) hypertrophy is associated with elevated adipose tissue macrophage (ATM) content. Overexpression of the triggering receptor expressed on myeloid cells 2 (TREM2) reportedly increases adiposity, worsening health. Paradoxically, using insulin resistance, elevat...
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| Veröffentlicht in: | Diabetes (New York, N.Y.) N.Y.), 2021-09, Vol.70 (9), p.2042-2057 |
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| creator | Sharif, Omar Brunner, Julia Stefanie Korosec, Ana Martins, Rui Jais, Alexander Snijder, Berend Vogel, Andrea Caldera, Michael Hladik, Anastasiya Lakovits, Karin Saluzzo, Simona Boehm, Benedikta Gorki, Anna-Dorothea Mesteri, Ildiko Lindroos-Christensen, Josefine Tillmann, Katharina Stoiber, Dagmar Menche, Jörg Schabbauer, Gernot Bilban, Martin Superti-Furga, Giulio Esterbauer, Harald Knapp, Sylvia |
| description | Obesity-induced white adipose tissue (WAT) hypertrophy is associated with elevated adipose tissue macrophage (ATM) content. Overexpression of the triggering receptor expressed on myeloid cells 2 (TREM2) reportedly increases adiposity, worsening health. Paradoxically, using insulin resistance, elevated fat mass, and hypercholesterolemia as hallmarks of unhealthy obesity, a recent report demonstrated that ATM-expressed TREM2 promoted health. Here, we identified that in mice, TREM2 deficiency aggravated diet-induced insulin resistance and hepatic steatosis independently of fat and cholesterol levels. Metabolomics linked TREM2 deficiency with elevated obesity-instigated serum ceramides that correlated with impaired insulin sensitivity. Remarkably, while inhibiting ceramide synthesis exerted no influences on TREM2-dependent ATM remodeling, inflammation, or lipid load, it restored insulin tolerance, reversing adipose hypertrophy and secondary hepatic steatosis of TREM2-deficient animals. Bone marrow transplantation experiments revealed unremarkable influences of immune cell-expressed TREM2 on health, instead demonstrating that WAT-intrinsic mechanisms impinging on sphingolipid metabolism dominate in the systemic protective effects of TREM2 on metabolic health. |
| doi_str_mv | 10.2337/db20-0572 |
| format | Article |
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Overexpression of the triggering receptor expressed on myeloid cells 2 (TREM2) reportedly increases adiposity, worsening health. Paradoxically, using insulin resistance, elevated fat mass, and hypercholesterolemia as hallmarks of unhealthy obesity, a recent report demonstrated that ATM-expressed TREM2 promoted health. Here, we identified that in mice, TREM2 deficiency aggravated diet-induced insulin resistance and hepatic steatosis independently of fat and cholesterol levels. Metabolomics linked TREM2 deficiency with elevated obesity-instigated serum ceramides that correlated with impaired insulin sensitivity. Remarkably, while inhibiting ceramide synthesis exerted no influences on TREM2-dependent ATM remodeling, inflammation, or lipid load, it restored insulin tolerance, reversing adipose hypertrophy and secondary hepatic steatosis of TREM2-deficient animals. Bone marrow transplantation experiments revealed unremarkable influences of immune cell-expressed TREM2 on health, instead demonstrating that WAT-intrinsic mechanisms impinging on sphingolipid metabolism dominate in the systemic protective effects of TREM2 on metabolic health.</description><identifier>ISSN: 0012-1797</identifier><identifier>EISSN: 1939-327X</identifier><identifier>DOI: 10.2337/db20-0572</identifier><identifier>PMID: 33627323</identifier><language>eng</language><publisher>United States: American Diabetes Association</publisher><subject>Adipose tissue ; Adipose Tissue - metabolism ; Animals ; Body fat ; Bone marrow transplantation ; Ceramide ; Cholesterol ; Diet, High-Fat ; Fatty liver ; Hypercholesterolemia ; Hypertrophy ; Immunological tolerance ; Inflammation - metabolism ; Insulin ; Insulin resistance ; Insulin Resistance - physiology ; Lipid metabolism ; Lipid Metabolism - physiology ; Macrophages ; Macrophages - metabolism ; Membrane Glycoproteins - metabolism ; Metabolism ; Metabolomics ; Mice ; Myeloid cells ; Nutrient deficiency ; Obesity ; Obesity - metabolism ; Obesity Studies ; Receptors, Immunologic - metabolism ; Steatosis ; Up-Regulation</subject><ispartof>Diabetes (New York, N.Y.), 2021-09, Vol.70 (9), p.2042-2057</ispartof><rights>2021 by the American Diabetes Association.</rights><rights>Copyright American Diabetes Association Sep 1, 2021</rights><rights>2021 by the American Diabetes Association 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c469t-f0951e1725cefee77e0f36984c69e3b1feb4e24fe86149e82ec675f4ad2361f93</citedby><cites>FETCH-LOGICAL-c469t-f0951e1725cefee77e0f36984c69e3b1feb4e24fe86149e82ec675f4ad2361f93</cites><orcidid>0000-0001-7899-2343</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8576425/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8576425/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33627323$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sharif, Omar</creatorcontrib><creatorcontrib>Brunner, Julia Stefanie</creatorcontrib><creatorcontrib>Korosec, Ana</creatorcontrib><creatorcontrib>Martins, Rui</creatorcontrib><creatorcontrib>Jais, Alexander</creatorcontrib><creatorcontrib>Snijder, Berend</creatorcontrib><creatorcontrib>Vogel, Andrea</creatorcontrib><creatorcontrib>Caldera, Michael</creatorcontrib><creatorcontrib>Hladik, Anastasiya</creatorcontrib><creatorcontrib>Lakovits, Karin</creatorcontrib><creatorcontrib>Saluzzo, Simona</creatorcontrib><creatorcontrib>Boehm, Benedikta</creatorcontrib><creatorcontrib>Gorki, Anna-Dorothea</creatorcontrib><creatorcontrib>Mesteri, Ildiko</creatorcontrib><creatorcontrib>Lindroos-Christensen, Josefine</creatorcontrib><creatorcontrib>Tillmann, Katharina</creatorcontrib><creatorcontrib>Stoiber, Dagmar</creatorcontrib><creatorcontrib>Menche, Jörg</creatorcontrib><creatorcontrib>Schabbauer, Gernot</creatorcontrib><creatorcontrib>Bilban, Martin</creatorcontrib><creatorcontrib>Superti-Furga, Giulio</creatorcontrib><creatorcontrib>Esterbauer, Harald</creatorcontrib><creatorcontrib>Knapp, Sylvia</creatorcontrib><title>Beneficial Metabolic Effects of TREM2 in Obesity Are Uncoupled From Its Expression on Macrophages</title><title>Diabetes (New York, N.Y.)</title><addtitle>Diabetes</addtitle><description>Obesity-induced white adipose tissue (WAT) hypertrophy is associated with elevated adipose tissue macrophage (ATM) content. Overexpression of the triggering receptor expressed on myeloid cells 2 (TREM2) reportedly increases adiposity, worsening health. Paradoxically, using insulin resistance, elevated fat mass, and hypercholesterolemia as hallmarks of unhealthy obesity, a recent report demonstrated that ATM-expressed TREM2 promoted health. Here, we identified that in mice, TREM2 deficiency aggravated diet-induced insulin resistance and hepatic steatosis independently of fat and cholesterol levels. Metabolomics linked TREM2 deficiency with elevated obesity-instigated serum ceramides that correlated with impaired insulin sensitivity. Remarkably, while inhibiting ceramide synthesis exerted no influences on TREM2-dependent ATM remodeling, inflammation, or lipid load, it restored insulin tolerance, reversing adipose hypertrophy and secondary hepatic steatosis of TREM2-deficient animals. Bone marrow transplantation experiments revealed unremarkable influences of immune cell-expressed TREM2 on health, instead demonstrating that WAT-intrinsic mechanisms impinging on sphingolipid metabolism dominate in the systemic protective effects of TREM2 on metabolic health.</description><subject>Adipose tissue</subject><subject>Adipose Tissue - metabolism</subject><subject>Animals</subject><subject>Body fat</subject><subject>Bone marrow transplantation</subject><subject>Ceramide</subject><subject>Cholesterol</subject><subject>Diet, High-Fat</subject><subject>Fatty liver</subject><subject>Hypercholesterolemia</subject><subject>Hypertrophy</subject><subject>Immunological tolerance</subject><subject>Inflammation - metabolism</subject><subject>Insulin</subject><subject>Insulin resistance</subject><subject>Insulin Resistance - physiology</subject><subject>Lipid metabolism</subject><subject>Lipid Metabolism - physiology</subject><subject>Macrophages</subject><subject>Macrophages - metabolism</subject><subject>Membrane Glycoproteins - metabolism</subject><subject>Metabolism</subject><subject>Metabolomics</subject><subject>Mice</subject><subject>Myeloid cells</subject><subject>Nutrient deficiency</subject><subject>Obesity</subject><subject>Obesity - metabolism</subject><subject>Obesity Studies</subject><subject>Receptors, Immunologic - metabolism</subject><subject>Steatosis</subject><subject>Up-Regulation</subject><issn>0012-1797</issn><issn>1939-327X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkV9LHTEQxUNpqbfaB7-ABPqiD2vzPzcvgsq1FbwIRcG3kM2daGTvZk12Rb-9uWillhmYh_lxODMHoV1KDhnn-ueqZaQhUrNPaEYNNw1n-uYzmhFCWUO10VvoWyn3hBBV6yva4lwxzRmfIXcCPYToo-vwEkbXpi56vAgB_FhwCvjqz2LJcOzxZQsljs_4OAO-7n2ahg5W-CynNT6v6OJpyFBKTD2uvXQ-p-HO3ULZQV-C6wp8f5vb6PpscXX6u7m4_HV-enzReKHM2ARiJAWqmfQQALQGErgyc-GVAd7SAK0AJgLMFRUG5gy80jIIt2Jc0WD4Njp61R2mdg0rD_2YXWeHHNcuP9vkov246eOdvU2Pdi61EkxWgf03gZweJiijXcfioetcD2kqlgnDhVSC6Ir--A-9T1Pu63mWSa0lM5qoSh28UvUXpWQI72YosZvg7CY4uwmusnv_un8n_ybFXwAqeZNJ</recordid><startdate>20210901</startdate><enddate>20210901</enddate><creator>Sharif, Omar</creator><creator>Brunner, Julia Stefanie</creator><creator>Korosec, Ana</creator><creator>Martins, Rui</creator><creator>Jais, Alexander</creator><creator>Snijder, Berend</creator><creator>Vogel, Andrea</creator><creator>Caldera, Michael</creator><creator>Hladik, Anastasiya</creator><creator>Lakovits, Karin</creator><creator>Saluzzo, Simona</creator><creator>Boehm, Benedikta</creator><creator>Gorki, Anna-Dorothea</creator><creator>Mesteri, Ildiko</creator><creator>Lindroos-Christensen, Josefine</creator><creator>Tillmann, Katharina</creator><creator>Stoiber, Dagmar</creator><creator>Menche, Jörg</creator><creator>Schabbauer, Gernot</creator><creator>Bilban, Martin</creator><creator>Superti-Furga, Giulio</creator><creator>Esterbauer, Harald</creator><creator>Knapp, Sylvia</creator><general>American Diabetes Association</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>K9.</scope><scope>NAPCQ</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7899-2343</orcidid></search><sort><creationdate>20210901</creationdate><title>Beneficial Metabolic Effects of TREM2 in Obesity Are Uncoupled From Its Expression on Macrophages</title><author>Sharif, Omar ; Brunner, Julia Stefanie ; Korosec, Ana ; Martins, Rui ; Jais, Alexander ; Snijder, Berend ; Vogel, Andrea ; Caldera, Michael ; Hladik, Anastasiya ; Lakovits, Karin ; Saluzzo, Simona ; Boehm, Benedikta ; Gorki, Anna-Dorothea ; Mesteri, Ildiko ; Lindroos-Christensen, Josefine ; Tillmann, Katharina ; Stoiber, Dagmar ; Menche, Jörg ; Schabbauer, Gernot ; Bilban, Martin ; Superti-Furga, Giulio ; Esterbauer, Harald ; Knapp, Sylvia</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c469t-f0951e1725cefee77e0f36984c69e3b1feb4e24fe86149e82ec675f4ad2361f93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adipose tissue</topic><topic>Adipose Tissue - metabolism</topic><topic>Animals</topic><topic>Body fat</topic><topic>Bone marrow transplantation</topic><topic>Ceramide</topic><topic>Cholesterol</topic><topic>Diet, High-Fat</topic><topic>Fatty liver</topic><topic>Hypercholesterolemia</topic><topic>Hypertrophy</topic><topic>Immunological tolerance</topic><topic>Inflammation - metabolism</topic><topic>Insulin</topic><topic>Insulin resistance</topic><topic>Insulin Resistance - physiology</topic><topic>Lipid metabolism</topic><topic>Lipid Metabolism - physiology</topic><topic>Macrophages</topic><topic>Macrophages - metabolism</topic><topic>Membrane Glycoproteins - metabolism</topic><topic>Metabolism</topic><topic>Metabolomics</topic><topic>Mice</topic><topic>Myeloid cells</topic><topic>Nutrient deficiency</topic><topic>Obesity</topic><topic>Obesity - metabolism</topic><topic>Obesity Studies</topic><topic>Receptors, Immunologic - metabolism</topic><topic>Steatosis</topic><topic>Up-Regulation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sharif, Omar</creatorcontrib><creatorcontrib>Brunner, Julia Stefanie</creatorcontrib><creatorcontrib>Korosec, Ana</creatorcontrib><creatorcontrib>Martins, Rui</creatorcontrib><creatorcontrib>Jais, Alexander</creatorcontrib><creatorcontrib>Snijder, Berend</creatorcontrib><creatorcontrib>Vogel, Andrea</creatorcontrib><creatorcontrib>Caldera, Michael</creatorcontrib><creatorcontrib>Hladik, Anastasiya</creatorcontrib><creatorcontrib>Lakovits, Karin</creatorcontrib><creatorcontrib>Saluzzo, Simona</creatorcontrib><creatorcontrib>Boehm, Benedikta</creatorcontrib><creatorcontrib>Gorki, Anna-Dorothea</creatorcontrib><creatorcontrib>Mesteri, Ildiko</creatorcontrib><creatorcontrib>Lindroos-Christensen, Josefine</creatorcontrib><creatorcontrib>Tillmann, Katharina</creatorcontrib><creatorcontrib>Stoiber, Dagmar</creatorcontrib><creatorcontrib>Menche, Jörg</creatorcontrib><creatorcontrib>Schabbauer, Gernot</creatorcontrib><creatorcontrib>Bilban, Martin</creatorcontrib><creatorcontrib>Superti-Furga, Giulio</creatorcontrib><creatorcontrib>Esterbauer, Harald</creatorcontrib><creatorcontrib>Knapp, Sylvia</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Diabetes (New York, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sharif, Omar</au><au>Brunner, Julia Stefanie</au><au>Korosec, Ana</au><au>Martins, Rui</au><au>Jais, Alexander</au><au>Snijder, Berend</au><au>Vogel, Andrea</au><au>Caldera, Michael</au><au>Hladik, Anastasiya</au><au>Lakovits, Karin</au><au>Saluzzo, Simona</au><au>Boehm, Benedikta</au><au>Gorki, Anna-Dorothea</au><au>Mesteri, Ildiko</au><au>Lindroos-Christensen, Josefine</au><au>Tillmann, Katharina</au><au>Stoiber, Dagmar</au><au>Menche, Jörg</au><au>Schabbauer, Gernot</au><au>Bilban, Martin</au><au>Superti-Furga, Giulio</au><au>Esterbauer, Harald</au><au>Knapp, Sylvia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Beneficial Metabolic Effects of TREM2 in Obesity Are Uncoupled From Its Expression on Macrophages</atitle><jtitle>Diabetes (New York, N.Y.)</jtitle><addtitle>Diabetes</addtitle><date>2021-09-01</date><risdate>2021</risdate><volume>70</volume><issue>9</issue><spage>2042</spage><epage>2057</epage><pages>2042-2057</pages><issn>0012-1797</issn><eissn>1939-327X</eissn><abstract>Obesity-induced white adipose tissue (WAT) hypertrophy is associated with elevated adipose tissue macrophage (ATM) content. Overexpression of the triggering receptor expressed on myeloid cells 2 (TREM2) reportedly increases adiposity, worsening health. Paradoxically, using insulin resistance, elevated fat mass, and hypercholesterolemia as hallmarks of unhealthy obesity, a recent report demonstrated that ATM-expressed TREM2 promoted health. Here, we identified that in mice, TREM2 deficiency aggravated diet-induced insulin resistance and hepatic steatosis independently of fat and cholesterol levels. Metabolomics linked TREM2 deficiency with elevated obesity-instigated serum ceramides that correlated with impaired insulin sensitivity. Remarkably, while inhibiting ceramide synthesis exerted no influences on TREM2-dependent ATM remodeling, inflammation, or lipid load, it restored insulin tolerance, reversing adipose hypertrophy and secondary hepatic steatosis of TREM2-deficient animals. Bone marrow transplantation experiments revealed unremarkable influences of immune cell-expressed TREM2 on health, instead demonstrating that WAT-intrinsic mechanisms impinging on sphingolipid metabolism dominate in the systemic protective effects of TREM2 on metabolic health.</abstract><cop>United States</cop><pub>American Diabetes Association</pub><pmid>33627323</pmid><doi>10.2337/db20-0572</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-7899-2343</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Adipose tissue Adipose Tissue - metabolism Animals Body fat Bone marrow transplantation Ceramide Cholesterol Diet, High-Fat Fatty liver Hypercholesterolemia Hypertrophy Immunological tolerance Inflammation - metabolism Insulin Insulin resistance Insulin Resistance - physiology Lipid metabolism Lipid Metabolism - physiology Macrophages Macrophages - metabolism Membrane Glycoproteins - metabolism Metabolism Metabolomics Mice Myeloid cells Nutrient deficiency Obesity Obesity - metabolism Obesity Studies Receptors, Immunologic - metabolism Steatosis Up-Regulation |
| title | Beneficial Metabolic Effects of TREM2 in Obesity Are Uncoupled From Its Expression on Macrophages |
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