Mitochondrial fission is required for thermogenesis in brown adipose tissue
Brown adipose tissue (BAT) thermogenesis is pivotal for maintaining body temperature and energy balance. Mitochondrial morphology is dynamically controlled by a balance between fusion and fission, which is crucial for cell differentiation, response to metabolic insults, and heat production. Dynamin-...
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| creator | Ibayashi, Yuta Hasuzawa, Nao Nomura, Seiji Kabashima, Masaharu Nagayama, Ayako Iwata, Shimpei Kitamura, Miyuki Ashida, Kenji Moriyama, Yoshinori Yamamoto, Ken Nomura, Masatoshi Wang, Lixiang |
| description | Brown adipose tissue (BAT) thermogenesis is pivotal for maintaining body temperature and energy balance. Mitochondrial morphology is dynamically controlled by a balance between fusion and fission, which is crucial for cell differentiation, response to metabolic insults, and heat production. Dynamin-related protein 1 (Drp1) is a key regulator of mitochondrial fission. This study investigates the role of Drp1 in BAT development and thermogenesis by generating Drp1-deficient mice. These mice were created by crossing Drp1 floxed mice with fatty acid-binding protein 4-Cre (aP2-Cre) transgenic mice, resulting in aP2-Cre+/-Drp1flox/flox (aP2-Drp1f/f) mice. The aP2-Drp1f/f mice exhibited severe BAT and brain hypoplasia, with the majority dying within 48 hours postnatally, highlighting Drp1's crucial role in neonatal survival. Impaired thermogenic responses were observed in aP2-Drp1f/f mice, characterized by significantly decreased expression of thermogenic and lipogenic genes in BAT. Ultrastructural analysis revealed disrupted mitochondrial morphology and reduced lipid droplet content in BAT. The few surviving adult aP2-Drp1f/f mice also showed impaired BAT and brain development, along with BAT thermogenesis dysfunction during cold exposure. Our findings underscore the essential role of Drp1-mediated mitochondrial fission in BAT thermogenesis and neonatal survival, providing insights into potential therapeutic approaches for metabolic disorders. |
| doi_str_mv | 10.1371/journal.pone.0312352 |
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Mitochondrial morphology is dynamically controlled by a balance between fusion and fission, which is crucial for cell differentiation, response to metabolic insults, and heat production. Dynamin-related protein 1 (Drp1) is a key regulator of mitochondrial fission. This study investigates the role of Drp1 in BAT development and thermogenesis by generating Drp1-deficient mice. These mice were created by crossing Drp1 floxed mice with fatty acid-binding protein 4-Cre (aP2-Cre) transgenic mice, resulting in aP2-Cre+/-Drp1flox/flox (aP2-Drp1f/f) mice. The aP2-Drp1f/f mice exhibited severe BAT and brain hypoplasia, with the majority dying within 48 hours postnatally, highlighting Drp1's crucial role in neonatal survival. Impaired thermogenic responses were observed in aP2-Drp1f/f mice, characterized by significantly decreased expression of thermogenic and lipogenic genes in BAT. Ultrastructural analysis revealed disrupted mitochondrial morphology and reduced lipid droplet content in BAT. The few surviving adult aP2-Drp1f/f mice also showed impaired BAT and brain development, along with BAT thermogenesis dysfunction during cold exposure. Our findings underscore the essential role of Drp1-mediated mitochondrial fission in BAT thermogenesis and neonatal survival, providing insights into potential therapeutic approaches for metabolic disorders.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0312352</identifier><identifier>PMID: 39652536</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adipocytes ; Adipose tissue ; Adipose tissue (brown) ; Adipose Tissue, Brown - metabolism ; Animals ; Antibodies ; Biology and Life Sciences ; Body fat ; Body temperature ; Brain ; Brain - metabolism ; Carbon dioxide ; Cell differentiation ; Cell fusion ; Cold ; Cold Temperature ; Differentiation (biology) ; Dynamin ; Dynamins - genetics ; Dynamins - metabolism ; Energy balance ; Engineering and Technology ; Fatty acid-binding protein ; Fission ; Flox ; Hypoplasia ; Kinases ; Laboratory animals ; Lipids ; Male ; Medicine and Health Sciences ; Metabolic disorders ; Metabolism ; Mice ; Mice, Transgenic ; Mitochondria ; Mitochondria - metabolism ; Mitochondrial Dynamics ; Morphology ; Neonates ; Postpartum period ; Proteins ; Software ; Survival ; Temperature requirements ; Thermogenesis ; Thermogenesis - genetics ; Transgenic mice</subject><ispartof>PloS one, 2024, Vol.19 (12), p.e0312352</ispartof><rights>Copyright: © 2024 Ibayashi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>2024 Ibayashi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 Ibayashi et al 2024 Ibayashi et al</rights><rights>2024 Ibayashi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0003-2087-4787</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/PMC11627380/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11627380/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,4024,23866,27923,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39652536$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ibayashi, Yuta</creatorcontrib><creatorcontrib>Hasuzawa, Nao</creatorcontrib><creatorcontrib>Nomura, Seiji</creatorcontrib><creatorcontrib>Kabashima, Masaharu</creatorcontrib><creatorcontrib>Nagayama, Ayako</creatorcontrib><creatorcontrib>Iwata, Shimpei</creatorcontrib><creatorcontrib>Kitamura, Miyuki</creatorcontrib><creatorcontrib>Ashida, Kenji</creatorcontrib><creatorcontrib>Moriyama, Yoshinori</creatorcontrib><creatorcontrib>Yamamoto, Ken</creatorcontrib><creatorcontrib>Nomura, Masatoshi</creatorcontrib><creatorcontrib>Wang, Lixiang</creatorcontrib><title>Mitochondrial fission is required for thermogenesis in brown adipose tissue</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Brown adipose tissue (BAT) thermogenesis is pivotal for maintaining body temperature and energy balance. Mitochondrial morphology is dynamically controlled by a balance between fusion and fission, which is crucial for cell differentiation, response to metabolic insults, and heat production. Dynamin-related protein 1 (Drp1) is a key regulator of mitochondrial fission. This study investigates the role of Drp1 in BAT development and thermogenesis by generating Drp1-deficient mice. These mice were created by crossing Drp1 floxed mice with fatty acid-binding protein 4-Cre (aP2-Cre) transgenic mice, resulting in aP2-Cre+/-Drp1flox/flox (aP2-Drp1f/f) mice. The aP2-Drp1f/f mice exhibited severe BAT and brain hypoplasia, with the majority dying within 48 hours postnatally, highlighting Drp1's crucial role in neonatal survival. Impaired thermogenic responses were observed in aP2-Drp1f/f mice, characterized by significantly decreased expression of thermogenic and lipogenic genes in BAT. Ultrastructural analysis revealed disrupted mitochondrial morphology and reduced lipid droplet content in BAT. The few surviving adult aP2-Drp1f/f mice also showed impaired BAT and brain development, along with BAT thermogenesis dysfunction during cold exposure. Our findings underscore the essential role of Drp1-mediated mitochondrial fission in BAT thermogenesis and neonatal survival, providing insights into potential therapeutic approaches for metabolic disorders.</description><subject>Adipocytes</subject><subject>Adipose tissue</subject><subject>Adipose tissue (brown)</subject><subject>Adipose Tissue, Brown - metabolism</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Biology and Life Sciences</subject><subject>Body fat</subject><subject>Body temperature</subject><subject>Brain</subject><subject>Brain - metabolism</subject><subject>Carbon dioxide</subject><subject>Cell differentiation</subject><subject>Cell fusion</subject><subject>Cold</subject><subject>Cold Temperature</subject><subject>Differentiation (biology)</subject><subject>Dynamin</subject><subject>Dynamins - genetics</subject><subject>Dynamins - metabolism</subject><subject>Energy balance</subject><subject>Engineering and Technology</subject><subject>Fatty acid-binding protein</subject><subject>Fission</subject><subject>Flox</subject><subject>Hypoplasia</subject><subject>Kinases</subject><subject>Laboratory animals</subject><subject>Lipids</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Metabolic disorders</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Mitochondria</subject><subject>Mitochondria - metabolism</subject><subject>Mitochondrial Dynamics</subject><subject>Morphology</subject><subject>Neonates</subject><subject>Postpartum period</subject><subject>Proteins</subject><subject>Software</subject><subject>Survival</subject><subject>Temperature requirements</subject><subject>Thermogenesis</subject><subject>Thermogenesis - genetics</subject><subject>Transgenic mice</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNptkctuFDEQRS0ESkLIH6CkJTZsZvCjXXavUBTxiAjKJqwtt12e8ajHntjdQfw9nWRACWJVluv63lMuQt4yumRCsQ-bPJVkh-UuJ1xSwbiQ_AU5Yp3gC-BUvHxyPiSva91QKoUGOCCHogPJpYAj8u17HLNb5-RLtEMTYq0xpybWpuDtFAv6JuTSjGss27zChHVuxdT0Jf9MjfVxlys24_xswjfkVbBDxZN9PSY_Pn-6ufi6uLr-cnlxfrXwXMEM1AM45IAiKEc1b4XnwTJ0uu2spEh7TikVEFznBZtRQStqGdCu771XVByTs0ff3ZCr2f9DNYK1XEqq23vF5aPCZ7sxuxK3tvwy2UbzcJHLytgyRjegkVpKzXRgjkE7x_aB2VY4pViwukU9e33cp039Fr3DNBY7PDN93klxbVb5zjAGXAl9T_N-71Dy7YR1NNtYHQ6DTZinB3AAqqBTs_TdP9L_j3f6FOkvy5-1it8ZmKVJ</recordid><startdate>2024</startdate><enddate>2024</enddate><creator>Ibayashi, Yuta</creator><creator>Hasuzawa, Nao</creator><creator>Nomura, Seiji</creator><creator>Kabashima, Masaharu</creator><creator>Nagayama, Ayako</creator><creator>Iwata, Shimpei</creator><creator>Kitamura, Miyuki</creator><creator>Ashida, Kenji</creator><creator>Moriyama, Yoshinori</creator><creator>Yamamoto, Ken</creator><creator>Nomura, Masatoshi</creator><creator>Wang, Lixiang</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-2087-4787</orcidid></search><sort><creationdate>2024</creationdate><title>Mitochondrial fission is required for thermogenesis in brown adipose tissue</title><author>Ibayashi, Yuta ; Hasuzawa, Nao ; Nomura, Seiji ; Kabashima, Masaharu ; Nagayama, Ayako ; Iwata, Shimpei ; Kitamura, Miyuki ; Ashida, Kenji ; Moriyama, Yoshinori ; Yamamoto, Ken ; Nomura, Masatoshi ; Wang, Lixiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-d2762-6b66ce26e3f7c08243d2fa1ec849a50e0b200036fc9d313966870a1609bbdd703</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adipocytes</topic><topic>Adipose tissue</topic><topic>Adipose tissue (brown)</topic><topic>Adipose Tissue, Brown - 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Mitochondrial morphology is dynamically controlled by a balance between fusion and fission, which is crucial for cell differentiation, response to metabolic insults, and heat production. Dynamin-related protein 1 (Drp1) is a key regulator of mitochondrial fission. This study investigates the role of Drp1 in BAT development and thermogenesis by generating Drp1-deficient mice. These mice were created by crossing Drp1 floxed mice with fatty acid-binding protein 4-Cre (aP2-Cre) transgenic mice, resulting in aP2-Cre+/-Drp1flox/flox (aP2-Drp1f/f) mice. The aP2-Drp1f/f mice exhibited severe BAT and brain hypoplasia, with the majority dying within 48 hours postnatally, highlighting Drp1's crucial role in neonatal survival. Impaired thermogenic responses were observed in aP2-Drp1f/f mice, characterized by significantly decreased expression of thermogenic and lipogenic genes in BAT. Ultrastructural analysis revealed disrupted mitochondrial morphology and reduced lipid droplet content in BAT. The few surviving adult aP2-Drp1f/f mice also showed impaired BAT and brain development, along with BAT thermogenesis dysfunction during cold exposure. Our findings underscore the essential role of Drp1-mediated mitochondrial fission in BAT thermogenesis and neonatal survival, providing insights into potential therapeutic approaches for metabolic disorders.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39652536</pmid><doi>10.1371/journal.pone.0312352</doi><orcidid>https://orcid.org/0000-0003-2087-4787</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adipocytes Adipose tissue Adipose tissue (brown) Adipose Tissue, Brown - metabolism Animals Antibodies Biology and Life Sciences Body fat Body temperature Brain Brain - metabolism Carbon dioxide Cell differentiation Cell fusion Cold Cold Temperature Differentiation (biology) Dynamin Dynamins - genetics Dynamins - metabolism Energy balance Engineering and Technology Fatty acid-binding protein Fission Flox Hypoplasia Kinases Laboratory animals Lipids Male Medicine and Health Sciences Metabolic disorders Metabolism Mice Mice, Transgenic Mitochondria Mitochondria - metabolism Mitochondrial Dynamics Morphology Neonates Postpartum period Proteins Software Survival Temperature requirements Thermogenesis Thermogenesis - genetics Transgenic mice |
| title | Mitochondrial fission is required for thermogenesis in brown adipose tissue |
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