Cardiolipin Synthesis in Brown and Beige Fat Mitochondria Is Essential for Systemic Energy Homeostasis
Activation of energy expenditure in thermogenic fat is a promising strategy to improve metabolic health, yet the dynamic processes that evoke this response are poorly understood. Here we show that synthesis of the mitochondrial phospholipid cardiolipin is indispensable for stimulating and sustaining...
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| Vydáno v: | Cell metabolism Ročník 28; číslo 1; s. 159 |
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| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
03.07.2018
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| ISSN: | 1932-7420, 1932-7420 |
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| Abstract | Activation of energy expenditure in thermogenic fat is a promising strategy to improve metabolic health, yet the dynamic processes that evoke this response are poorly understood. Here we show that synthesis of the mitochondrial phospholipid cardiolipin is indispensable for stimulating and sustaining thermogenic fat function. Cardiolipin biosynthesis is robustly induced in brown and beige adipose upon cold exposure. Mimicking this response through overexpression of cardiolipin synthase (Crls1) enhances energy consumption in mouse and human adipocytes. Crls1 deficiency in thermogenic adipocytes diminishes inducible mitochondrial uncoupling and elicits a nuclear transcriptional response through endoplasmic reticulum stress-mediated retrograde communication. Cardiolipin depletion in brown and beige fat abolishes adipose thermogenesis and glucose uptake, which renders animals insulin resistant. We further identify a rare human CRLS1 variant associated with insulin resistance and show that adipose CRLS1 levels positively correlate with insulin sensitivity. Thus, adipose cardiolipin has a powerful impact on organismal energy homeostasis through thermogenic fat bioenergetics. |
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| AbstractList | Activation of energy expenditure in thermogenic fat is a promising strategy to improve metabolic health, yet the dynamic processes that evoke this response are poorly understood. Here we show that synthesis of the mitochondrial phospholipid cardiolipin is indispensable for stimulating and sustaining thermogenic fat function. Cardiolipin biosynthesis is robustly induced in brown and beige adipose upon cold exposure. Mimicking this response through overexpression of cardiolipin synthase (Crls1) enhances energy consumption in mouse and human adipocytes. Crls1 deficiency in thermogenic adipocytes diminishes inducible mitochondrial uncoupling and elicits a nuclear transcriptional response through endoplasmic reticulum stress-mediated retrograde communication. Cardiolipin depletion in brown and beige fat abolishes adipose thermogenesis and glucose uptake, which renders animals insulin resistant. We further identify a rare human CRLS1 variant associated with insulin resistance and show that adipose CRLS1 levels positively correlate with insulin sensitivity. Thus, adipose cardiolipin has a powerful impact on organismal energy homeostasis through thermogenic fat bioenergetics.Activation of energy expenditure in thermogenic fat is a promising strategy to improve metabolic health, yet the dynamic processes that evoke this response are poorly understood. Here we show that synthesis of the mitochondrial phospholipid cardiolipin is indispensable for stimulating and sustaining thermogenic fat function. Cardiolipin biosynthesis is robustly induced in brown and beige adipose upon cold exposure. Mimicking this response through overexpression of cardiolipin synthase (Crls1) enhances energy consumption in mouse and human adipocytes. Crls1 deficiency in thermogenic adipocytes diminishes inducible mitochondrial uncoupling and elicits a nuclear transcriptional response through endoplasmic reticulum stress-mediated retrograde communication. Cardiolipin depletion in brown and beige fat abolishes adipose thermogenesis and glucose uptake, which renders animals insulin resistant. We further identify a rare human CRLS1 variant associated with insulin resistance and show that adipose CRLS1 levels positively correlate with insulin sensitivity. Thus, adipose cardiolipin has a powerful impact on organismal energy homeostasis through thermogenic fat bioenergetics. Activation of energy expenditure in thermogenic fat is a promising strategy to improve metabolic health, yet the dynamic processes that evoke this response are poorly understood. Here we show that synthesis of the mitochondrial phospholipid cardiolipin is indispensable for stimulating and sustaining thermogenic fat function. Cardiolipin biosynthesis is robustly induced in brown and beige adipose upon cold exposure. Mimicking this response through overexpression of cardiolipin synthase (Crls1) enhances energy consumption in mouse and human adipocytes. Crls1 deficiency in thermogenic adipocytes diminishes inducible mitochondrial uncoupling and elicits a nuclear transcriptional response through endoplasmic reticulum stress-mediated retrograde communication. Cardiolipin depletion in brown and beige fat abolishes adipose thermogenesis and glucose uptake, which renders animals insulin resistant. We further identify a rare human CRLS1 variant associated with insulin resistance and show that adipose CRLS1 levels positively correlate with insulin sensitivity. Thus, adipose cardiolipin has a powerful impact on organismal energy homeostasis through thermogenic fat bioenergetics. |
| Author | Lundh, Morten Stohlmann, Katharina Grarup, Niels Lynes, Matthew D Havelund, Jesper F Jespersen, Naja Z Neess, Ditte Wang, Jianing Jørgensen, Marit E Pedersen, Oluf Jedrychowski, Mark P Moreno-Torres, Marta Linneberg, Allan Peics, Julia Pedersen, Bente Klarlund Gerhart-Hines, Zachary Jastroch, Martin Kjær, Andreas Emanuelli, Brice Ma, Tao Plucinska, Kaja Larsen, Michael Gillum, Matthew P Kramar, Barbara Mandrup, Susanne Shamsi, Farnaz Nielsen, Carsten H Tseng, Yu-Hua Færgeman, Nils J Brandslund, Ivan Sustarsic, Elahu G Gygi, Steven P Forss, Isabel Hansen, Torben Hansen, Jakob B Keipert, Susanne Kiebish, Michael A Karavaeva, Iuliia Grevengoed, Trisha J Qvortrup, Klaus Nielsen, Søren Han, Xianlin Christensen, Cramer Scheele, Camilla |
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Department of Biomedical Sciences, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 6 givenname: Jesper F surname: Havelund fullname: Havelund, Jesper F organization: Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense 5230, Denmark – sequence: 7 givenname: Carsten H surname: Nielsen fullname: Nielsen, Carsten H organization: Department of Biomedical Sciences, University of Copenhagen, Copenhagen 2200, Denmark; Department of Clinical Physiology, Nuclear Medicine & PET and Cluster for Molecular Imaging, Rigshospitalet, Copenhagen 2200, Denmark – sequence: 8 givenname: Mark P surname: Jedrychowski fullname: Jedrychowski, Mark P organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 9 givenname: Marta surname: Moreno-Torres fullname: Moreno-Torres, Marta organization: Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense 5230, Denmark – sequence: 10 givenname: Morten surname: Lundh fullname: Lundh, Morten organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 11 givenname: Kaja surname: Plucinska fullname: Plucinska, Kaja organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 12 givenname: Naja Z surname: Jespersen fullname: Jespersen, Naja Z organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark; Centre of Inflammation and Metabolism and Centre for Physical Activity Research, Rigshospitalet, University Hospital of Copenhagen, Copenhagen 2200, Denmark – sequence: 13 givenname: Trisha J surname: Grevengoed fullname: Grevengoed, Trisha J organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 14 givenname: Barbara surname: Kramar fullname: Kramar, Barbara organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 15 givenname: Julia surname: Peics fullname: Peics, Julia organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark; Department of Biomedical Sciences, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 16 givenname: Jakob B surname: Hansen fullname: Hansen, Jakob B organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark; Department of Biomedical Sciences, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 17 givenname: Farnaz surname: Shamsi fullname: Shamsi, Farnaz organization: Section on Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 18 givenname: Isabel surname: Forss fullname: Forss, Isabel organization: Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense 5230, Denmark – sequence: 19 givenname: Ditte surname: Neess fullname: Neess, Ditte organization: Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense 5230, Denmark – sequence: 20 givenname: Susanne surname: Keipert fullname: Keipert, Susanne organization: Helmholtz Diabetes Center and German Diabetes Center (DZD), Helmholtz Zentrum München, Neuherberg 85764, Germany – sequence: 21 givenname: Jianing surname: Wang fullname: Wang, Jianing organization: Barshop Institute for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA – sequence: 22 givenname: Katharina surname: Stohlmann fullname: Stohlmann, Katharina organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 23 givenname: Ivan surname: Brandslund fullname: Brandslund, Ivan organization: Lillebaelt Hospital, Vejle 7100, Denmark; Institute of Regional Health Research, University of Southern Denmark, Odense 5230, Denmark – sequence: 24 givenname: Cramer surname: Christensen fullname: Christensen, Cramer organization: Lillebaelt Hospital, Vejle 7100, Denmark – sequence: 25 givenname: Marit E surname: Jørgensen fullname: Jørgensen, Marit E organization: Steno Diabetes Center, Gentofte 2820, Denmark; National Institute of Public Health, Southern Denmark University, Copenhagen 1353, Denmark – sequence: 26 givenname: Allan surname: Linneberg fullname: Linneberg, Allan organization: Research Center for Prevention and Health, Glostrup 2600, Denmark; Center for Clinical Research and Prevention, Bispebjerg and Frederiksberg Hospital, Copenhagen, Denmark; Department of Clinical Medicine, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 27 givenname: Oluf surname: Pedersen fullname: Pedersen, Oluf organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 28 givenname: Michael A surname: Kiebish fullname: Kiebish, Michael A organization: BERG Health, Framingham, MA 01701, USA – sequence: 29 givenname: Klaus surname: Qvortrup fullname: Qvortrup, Klaus organization: Department of Biomedical Sciences, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 30 givenname: Xianlin surname: Han fullname: Han, Xianlin organization: Barshop Institute for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA – sequence: 31 givenname: Bente Klarlund surname: Pedersen fullname: Pedersen, Bente Klarlund organization: Centre of Inflammation and Metabolism and Centre for Physical Activity Research, Rigshospitalet, University Hospital of Copenhagen, Copenhagen 2200, Denmark – sequence: 32 givenname: Martin surname: Jastroch fullname: Jastroch, Martin organization: Helmholtz Diabetes Center and German Diabetes Center (DZD), Helmholtz Zentrum München, Neuherberg 85764, Germany – sequence: 33 givenname: Susanne surname: Mandrup fullname: Mandrup, Susanne organization: Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense 5230, Denmark – sequence: 34 givenname: Andreas surname: Kjær fullname: Kjær, Andreas organization: Department of Biomedical Sciences, University of Copenhagen, Copenhagen 2200, Denmark; Department of Clinical Physiology, Nuclear Medicine & PET and Cluster for Molecular Imaging, Rigshospitalet, Copenhagen 2200, Denmark – sequence: 35 givenname: Steven P surname: Gygi fullname: Gygi, Steven P organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 36 givenname: Torben surname: Hansen fullname: Hansen, Torben organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 37 givenname: Matthew P surname: Gillum fullname: Gillum, Matthew P organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 38 givenname: Niels surname: Grarup fullname: Grarup, Niels organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 39 givenname: Brice surname: Emanuelli fullname: Emanuelli, Brice organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 40 givenname: Søren surname: Nielsen fullname: Nielsen, Søren organization: Centre of Inflammation and Metabolism and Centre for Physical Activity Research, Rigshospitalet, University Hospital of Copenhagen, Copenhagen 2200, Denmark – sequence: 41 givenname: Camilla surname: Scheele fullname: Scheele, Camilla organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark; Centre of Inflammation and Metabolism and Centre for Physical Activity Research, Rigshospitalet, University Hospital of Copenhagen, Copenhagen 2200, Denmark – sequence: 42 givenname: Yu-Hua surname: Tseng fullname: Tseng, Yu-Hua organization: Section on Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, MA 02215, USA – sequence: 43 givenname: Nils J surname: Færgeman fullname: Færgeman, Nils J organization: Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense 5230, Denmark – sequence: 44 givenname: Zachary surname: Gerhart-Hines fullname: Gerhart-Hines, Zachary email: zpg@sund.ku.dk organization: Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen 2200, Denmark; Department of Biomedical Sciences, University of Copenhagen, Copenhagen 2200, Denmark. Electronic address: zpg@sund.ku.dk |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29861389$$D View this record in MEDLINE/PubMed |
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| Keywords | beige adipose thermogenesis brown adipose mitochondria lipid metabolism CHOP-10 phospholipids CRLS1 cardiolipin insulin resistance |
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| SubjectTerms | Adipocytes - metabolism Adipose Tissue, Beige - metabolism Adipose Tissue, Brown - metabolism Animals Cardiolipins - biosynthesis Cells, Cultured Energy Metabolism Humans Membrane Proteins - genetics Membrane Proteins - metabolism Mice Mice, Inbred C57BL Mitochondria - metabolism Thermogenesis Transferases (Other Substituted Phosphate Groups) - genetics Transferases (Other Substituted Phosphate Groups) - metabolism |
| Title | Cardiolipin Synthesis in Brown and Beige Fat Mitochondria Is Essential for Systemic Energy Homeostasis |
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