Membrane-Initiated Estrogen Receptor Signaling Mediates Metabolic Homeostasis via Central Activation of Protein Phosphatase 2A
Women gain weight and their diabetes risk increases as they transition through menopause; these changes can be partly reversed by hormone therapy. However, the underlying molecular mechanisms mediating these effects are unknown. A novel knock-in mouse line with the selective blockade of the membrane...
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| Veröffentlicht in: | Diabetes (New York, N.Y.) N.Y.), 2018-08, Vol.67 (8), p.1524-1537 |
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| creator | Ueda, Kazutaka Takimoto, Eiki Lu, Qing Liu, Pangyen Fukuma, Nobuaki Adachi, Yusuke Suzuki, Ryo Chou, Shengpu Baur, Wendy Aronovitz, Mark J Greenberg, Andrew S Komuro, Issei Karas, Richard H |
| description | Women gain weight and their diabetes risk increases as they transition through menopause; these changes can be partly reversed by hormone therapy. However, the underlying molecular mechanisms mediating these effects are unknown. A novel knock-in mouse line with the selective blockade of the membrane-initiated estrogen receptor (ER) pathway was used, and we found that the lack of this pathway precipitated excessive weight gain and glucose intolerance independent of food intake and that this was accompanied by impaired adaptive thermogenesis and reduced physical activity. Notably, the central activation of protein phosphatase (PP) 2A improved metabolic disorders induced by the lack of membrane-initiated ER signaling. Furthermore, the antiobesity effect of estrogen replacement in a murine menopause model was abolished by central PP2A inactivation. These findings define a critical role for membrane-initiated ER signaling in metabolic homeostasis via the central action of PP2A. |
| doi_str_mv | 10.2337/db17-1342 |
| format | Article |
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However, the underlying molecular mechanisms mediating these effects are unknown. A novel knock-in mouse line with the selective blockade of the membrane-initiated estrogen receptor (ER) pathway was used, and we found that the lack of this pathway precipitated excessive weight gain and glucose intolerance independent of food intake and that this was accompanied by impaired adaptive thermogenesis and reduced physical activity. Notably, the central activation of protein phosphatase (PP) 2A improved metabolic disorders induced by the lack of membrane-initiated ER signaling. Furthermore, the antiobesity effect of estrogen replacement in a murine menopause model was abolished by central PP2A inactivation. These findings define a critical role for membrane-initiated ER signaling in metabolic homeostasis via the central action of PP2A.</description><identifier>ISSN: 0012-1797</identifier><identifier>EISSN: 1939-327X</identifier><identifier>DOI: 10.2337/db17-1342</identifier><identifier>PMID: 29764860</identifier><language>eng</language><publisher>United States: American Diabetes Association</publisher><subject>3T3-L1 Cells ; Adipocytes - drug effects ; Adipocytes - metabolism ; Adipocytes - pathology ; Adiposity - drug effects ; Amino Acid Substitution ; Animals ; Body weight gain ; Cells, Cultured ; Diabetes ; Diabetes mellitus ; Diet, High-Fat - adverse effects ; Enzyme Activation - drug effects ; Estradiol - pharmacology ; Estradiol - therapeutic use ; Estrogen Receptor alpha - agonists ; Estrogen Receptor alpha - genetics ; Estrogen Receptor alpha - metabolism ; Estrogen receptors ; Estrogen Replacement Therapy ; Estrogens ; Female ; Food intake ; Food intolerance ; Gene Knock-In Techniques ; Glucose Intolerance - etiology ; Glucose Intolerance - metabolism ; Glucose Intolerance - pathology ; Glucose Intolerance - prevention & control ; Glucose tolerance ; Homeostasis ; Hormone replacement therapy ; Insulin Resistance ; Menopause ; Metabolic rate ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Molecular modelling ; Muscle, Smooth, Vascular - drug effects ; Muscle, Smooth, Vascular - metabolism ; Muscle, Smooth, Vascular - pathology ; Obesity - etiology ; Obesity - metabolism ; Obesity - pathology ; Obesity - prevention & control ; Obesity Studies ; Ovariectomy ; Phosphatase ; Phosphoprotein phosphatase ; Physical activity ; Point Mutation ; Protein phosphatase ; Protein Phosphatase 2 - chemistry ; Protein Phosphatase 2 - metabolism ; Proteins ; Signal transduction ; Signal Transduction - drug effects ; Thermogenesis</subject><ispartof>Diabetes (New York, N.Y.), 2018-08, Vol.67 (8), p.1524-1537</ispartof><rights>2018 by the American Diabetes Association.</rights><rights>Copyright American Diabetes Association Aug 1, 2018</rights><rights>2018 by the American Diabetes Association. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c469t-6324893848f001c81203cfc6e1485ce770bea7b18eeab9e9016b5c5839d0560c3</citedby><cites>FETCH-LOGICAL-c469t-6324893848f001c81203cfc6e1485ce770bea7b18eeab9e9016b5c5839d0560c3</cites><orcidid>0000-0001-5062-387X ; 0000-0002-0509-1840 ; 0000-0001-7799-091X</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/PMC6054435/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6054435/$$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/29764860$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ueda, Kazutaka</creatorcontrib><creatorcontrib>Takimoto, Eiki</creatorcontrib><creatorcontrib>Lu, Qing</creatorcontrib><creatorcontrib>Liu, Pangyen</creatorcontrib><creatorcontrib>Fukuma, Nobuaki</creatorcontrib><creatorcontrib>Adachi, Yusuke</creatorcontrib><creatorcontrib>Suzuki, Ryo</creatorcontrib><creatorcontrib>Chou, Shengpu</creatorcontrib><creatorcontrib>Baur, Wendy</creatorcontrib><creatorcontrib>Aronovitz, Mark J</creatorcontrib><creatorcontrib>Greenberg, Andrew S</creatorcontrib><creatorcontrib>Komuro, Issei</creatorcontrib><creatorcontrib>Karas, Richard H</creatorcontrib><title>Membrane-Initiated Estrogen Receptor Signaling Mediates Metabolic Homeostasis via Central Activation of Protein Phosphatase 2A</title><title>Diabetes (New York, N.Y.)</title><addtitle>Diabetes</addtitle><description>Women gain weight and their diabetes risk increases as they transition through menopause; these changes can be partly reversed by hormone therapy. However, the underlying molecular mechanisms mediating these effects are unknown. A novel knock-in mouse line with the selective blockade of the membrane-initiated estrogen receptor (ER) pathway was used, and we found that the lack of this pathway precipitated excessive weight gain and glucose intolerance independent of food intake and that this was accompanied by impaired adaptive thermogenesis and reduced physical activity. Notably, the central activation of protein phosphatase (PP) 2A improved metabolic disorders induced by the lack of membrane-initiated ER signaling. Furthermore, the antiobesity effect of estrogen replacement in a murine menopause model was abolished by central PP2A inactivation. These findings define a critical role for membrane-initiated ER signaling in metabolic homeostasis via the central action of PP2A.</description><subject>3T3-L1 Cells</subject><subject>Adipocytes - drug effects</subject><subject>Adipocytes - metabolism</subject><subject>Adipocytes - pathology</subject><subject>Adiposity - drug effects</subject><subject>Amino Acid Substitution</subject><subject>Animals</subject><subject>Body weight gain</subject><subject>Cells, Cultured</subject><subject>Diabetes</subject><subject>Diabetes mellitus</subject><subject>Diet, High-Fat - adverse effects</subject><subject>Enzyme Activation - drug effects</subject><subject>Estradiol - pharmacology</subject><subject>Estradiol - therapeutic use</subject><subject>Estrogen Receptor alpha - agonists</subject><subject>Estrogen Receptor alpha - genetics</subject><subject>Estrogen Receptor alpha - metabolism</subject><subject>Estrogen receptors</subject><subject>Estrogen Replacement Therapy</subject><subject>Estrogens</subject><subject>Female</subject><subject>Food intake</subject><subject>Food intolerance</subject><subject>Gene Knock-In Techniques</subject><subject>Glucose Intolerance - etiology</subject><subject>Glucose Intolerance - metabolism</subject><subject>Glucose Intolerance - pathology</subject><subject>Glucose Intolerance - prevention & control</subject><subject>Glucose tolerance</subject><subject>Homeostasis</subject><subject>Hormone replacement therapy</subject><subject>Insulin Resistance</subject><subject>Menopause</subject><subject>Metabolic rate</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Molecular modelling</subject><subject>Muscle, Smooth, Vascular - drug effects</subject><subject>Muscle, Smooth, Vascular - metabolism</subject><subject>Muscle, Smooth, Vascular - pathology</subject><subject>Obesity - etiology</subject><subject>Obesity - metabolism</subject><subject>Obesity - pathology</subject><subject>Obesity - prevention & control</subject><subject>Obesity Studies</subject><subject>Ovariectomy</subject><subject>Phosphatase</subject><subject>Phosphoprotein phosphatase</subject><subject>Physical activity</subject><subject>Point Mutation</subject><subject>Protein phosphatase</subject><subject>Protein Phosphatase 2 - chemistry</subject><subject>Protein Phosphatase 2 - metabolism</subject><subject>Proteins</subject><subject>Signal transduction</subject><subject>Signal Transduction - drug effects</subject><subject>Thermogenesis</subject><issn>0012-1797</issn><issn>1939-327X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkU1rGzEQhkVJaBy3h_6BIsgph230tdLqUjDGTQIOMWkCvQmtdtZWsCVXkg295Ld3jdPQoIME8_BqZh6EvlDyjXGurrqWqopywT6gEdVcV5ypXydoRAhlFVVanaHznJ8JIXI4H9EZ00qKRpIRermDTZtsgOo2-OJtgQ7PcklxCQE_gINtiQn_9Mtg1z4s8R10BygPj2LbuPYO38QNxFxs9hnvvcVTCCXZNZ644ve2-Bhw7PEixQI-4MUq5u3KDjhgNvmETnu7zvD59R6jpx-zx-lNNb-_vp1O5pUTUpdKciYazRvR9MNMrqGMcNc7CVQ0tQOlSAtWtbQBsK0GTahsa1c3XHeklsTxMfp-zN3u2g107tii2Sa_semPidab95XgV2YZ90aSWgheDwEXrwEp_t5BLuY57tKwlGwY0VxoxQYVY3R5pFyKOSfo336gxBxUmYMqc1A1sF__b-mN_OeG_wWBZZDM</recordid><startdate>20180801</startdate><enddate>20180801</enddate><creator>Ueda, Kazutaka</creator><creator>Takimoto, Eiki</creator><creator>Lu, Qing</creator><creator>Liu, Pangyen</creator><creator>Fukuma, Nobuaki</creator><creator>Adachi, Yusuke</creator><creator>Suzuki, Ryo</creator><creator>Chou, Shengpu</creator><creator>Baur, Wendy</creator><creator>Aronovitz, Mark J</creator><creator>Greenberg, Andrew S</creator><creator>Komuro, Issei</creator><creator>Karas, Richard H</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>5PM</scope><orcidid>https://orcid.org/0000-0001-5062-387X</orcidid><orcidid>https://orcid.org/0000-0002-0509-1840</orcidid><orcidid>https://orcid.org/0000-0001-7799-091X</orcidid></search><sort><creationdate>20180801</creationdate><title>Membrane-Initiated Estrogen Receptor Signaling Mediates Metabolic Homeostasis via Central Activation of Protein Phosphatase 2A</title><author>Ueda, Kazutaka ; Takimoto, Eiki ; Lu, Qing ; Liu, Pangyen ; Fukuma, Nobuaki ; Adachi, Yusuke ; Suzuki, Ryo ; Chou, Shengpu ; Baur, Wendy ; Aronovitz, Mark J ; Greenberg, Andrew S ; Komuro, Issei ; Karas, Richard H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c469t-6324893848f001c81203cfc6e1485ce770bea7b18eeab9e9016b5c5839d0560c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>3T3-L1 Cells</topic><topic>Adipocytes - drug effects</topic><topic>Adipocytes - metabolism</topic><topic>Adipocytes - pathology</topic><topic>Adiposity - drug effects</topic><topic>Amino Acid Substitution</topic><topic>Animals</topic><topic>Body weight gain</topic><topic>Cells, Cultured</topic><topic>Diabetes</topic><topic>Diabetes mellitus</topic><topic>Diet, High-Fat - adverse effects</topic><topic>Enzyme Activation - drug effects</topic><topic>Estradiol - pharmacology</topic><topic>Estradiol - therapeutic use</topic><topic>Estrogen Receptor alpha - agonists</topic><topic>Estrogen Receptor alpha - genetics</topic><topic>Estrogen Receptor alpha - metabolism</topic><topic>Estrogen receptors</topic><topic>Estrogen Replacement Therapy</topic><topic>Estrogens</topic><topic>Female</topic><topic>Food intake</topic><topic>Food intolerance</topic><topic>Gene Knock-In Techniques</topic><topic>Glucose Intolerance - etiology</topic><topic>Glucose Intolerance - metabolism</topic><topic>Glucose Intolerance - pathology</topic><topic>Glucose Intolerance - prevention & control</topic><topic>Glucose tolerance</topic><topic>Homeostasis</topic><topic>Hormone replacement therapy</topic><topic>Insulin Resistance</topic><topic>Menopause</topic><topic>Metabolic rate</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Transgenic</topic><topic>Molecular modelling</topic><topic>Muscle, Smooth, Vascular - drug effects</topic><topic>Muscle, Smooth, Vascular - metabolism</topic><topic>Muscle, Smooth, Vascular - pathology</topic><topic>Obesity - etiology</topic><topic>Obesity - metabolism</topic><topic>Obesity - pathology</topic><topic>Obesity - prevention & control</topic><topic>Obesity Studies</topic><topic>Ovariectomy</topic><topic>Phosphatase</topic><topic>Phosphoprotein phosphatase</topic><topic>Physical activity</topic><topic>Point Mutation</topic><topic>Protein phosphatase</topic><topic>Protein Phosphatase 2 - chemistry</topic><topic>Protein Phosphatase 2 - metabolism</topic><topic>Proteins</topic><topic>Signal transduction</topic><topic>Signal Transduction - drug effects</topic><topic>Thermogenesis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ueda, Kazutaka</creatorcontrib><creatorcontrib>Takimoto, Eiki</creatorcontrib><creatorcontrib>Lu, Qing</creatorcontrib><creatorcontrib>Liu, Pangyen</creatorcontrib><creatorcontrib>Fukuma, Nobuaki</creatorcontrib><creatorcontrib>Adachi, Yusuke</creatorcontrib><creatorcontrib>Suzuki, Ryo</creatorcontrib><creatorcontrib>Chou, Shengpu</creatorcontrib><creatorcontrib>Baur, Wendy</creatorcontrib><creatorcontrib>Aronovitz, Mark J</creatorcontrib><creatorcontrib>Greenberg, Andrew S</creatorcontrib><creatorcontrib>Komuro, Issei</creatorcontrib><creatorcontrib>Karas, Richard H</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>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>Ueda, Kazutaka</au><au>Takimoto, Eiki</au><au>Lu, Qing</au><au>Liu, Pangyen</au><au>Fukuma, Nobuaki</au><au>Adachi, Yusuke</au><au>Suzuki, Ryo</au><au>Chou, Shengpu</au><au>Baur, Wendy</au><au>Aronovitz, Mark J</au><au>Greenberg, Andrew S</au><au>Komuro, Issei</au><au>Karas, Richard H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Membrane-Initiated Estrogen Receptor Signaling Mediates Metabolic Homeostasis via Central Activation of Protein Phosphatase 2A</atitle><jtitle>Diabetes (New York, N.Y.)</jtitle><addtitle>Diabetes</addtitle><date>2018-08-01</date><risdate>2018</risdate><volume>67</volume><issue>8</issue><spage>1524</spage><epage>1537</epage><pages>1524-1537</pages><issn>0012-1797</issn><eissn>1939-327X</eissn><abstract>Women gain weight and their diabetes risk increases as they transition through menopause; these changes can be partly reversed by hormone therapy. However, the underlying molecular mechanisms mediating these effects are unknown. A novel knock-in mouse line with the selective blockade of the membrane-initiated estrogen receptor (ER) pathway was used, and we found that the lack of this pathway precipitated excessive weight gain and glucose intolerance independent of food intake and that this was accompanied by impaired adaptive thermogenesis and reduced physical activity. Notably, the central activation of protein phosphatase (PP) 2A improved metabolic disorders induced by the lack of membrane-initiated ER signaling. Furthermore, the antiobesity effect of estrogen replacement in a murine menopause model was abolished by central PP2A inactivation. These findings define a critical role for membrane-initiated ER signaling in metabolic homeostasis via the central action of PP2A.</abstract><cop>United States</cop><pub>American Diabetes Association</pub><pmid>29764860</pmid><doi>10.2337/db17-1342</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-5062-387X</orcidid><orcidid>https://orcid.org/0000-0002-0509-1840</orcidid><orcidid>https://orcid.org/0000-0001-7799-091X</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Diabetes (New York, N.Y.), 2018-08, Vol.67 (8), p.1524-1537 |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | 3T3-L1 Cells Adipocytes - drug effects Adipocytes - metabolism Adipocytes - pathology Adiposity - drug effects Amino Acid Substitution Animals Body weight gain Cells, Cultured Diabetes Diabetes mellitus Diet, High-Fat - adverse effects Enzyme Activation - drug effects Estradiol - pharmacology Estradiol - therapeutic use Estrogen Receptor alpha - agonists Estrogen Receptor alpha - genetics Estrogen Receptor alpha - metabolism Estrogen receptors Estrogen Replacement Therapy Estrogens Female Food intake Food intolerance Gene Knock-In Techniques Glucose Intolerance - etiology Glucose Intolerance - metabolism Glucose Intolerance - pathology Glucose Intolerance - prevention & control Glucose tolerance Homeostasis Hormone replacement therapy Insulin Resistance Menopause Metabolic rate Mice Mice, Inbred C57BL Mice, Transgenic Molecular modelling Muscle, Smooth, Vascular - drug effects Muscle, Smooth, Vascular - metabolism Muscle, Smooth, Vascular - pathology Obesity - etiology Obesity - metabolism Obesity - pathology Obesity - prevention & control Obesity Studies Ovariectomy Phosphatase Phosphoprotein phosphatase Physical activity Point Mutation Protein phosphatase Protein Phosphatase 2 - chemistry Protein Phosphatase 2 - metabolism Proteins Signal transduction Signal Transduction - drug effects Thermogenesis |
| title | Membrane-Initiated Estrogen Receptor Signaling Mediates Metabolic Homeostasis via Central Activation of Protein Phosphatase 2A |
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