Mitochondrial phosphatidylethanolamine modulates UCP1 to promote brown adipose thermogenesis.

Mice Animals Uncoupling Protein 1 / metabolism Phosphatidylethanolamines / metabolism Protons Mitochondria / metabolism Thermogenesis Obesity / metabolism Adenosine Triphosphate / metabolism Mice, Knockout

Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
24 02 2023
Historique:
entrez: 24 2 2023
pubmed: 25 2 2023
medline: 3 3 2023
Statut: ppublish

Résumé

Thermogenesis by uncoupling protein 1 (UCP1) is one of the primary mechanisms by which brown adipose tissue (BAT) increases energy expenditure. UCP1 resides in the inner mitochondrial membrane (IMM), where it dissipates membrane potential independent of adenosine triphosphate (ATP) synthase. Here, we provide evidence that phosphatidylethanolamine (PE) modulates UCP1-dependent proton conductance across the IMM to modulate thermogenesis. Mitochondrial lipidomic analyses revealed PE as a signature molecule whose abundance bidirectionally responds to changes in thermogenic burden. Reduction in mitochondrial PE by deletion of phosphatidylserine decarboxylase (PSD) made mice cold intolerant and insensitive to β3 adrenergic receptor agonist-induced increase in whole-body oxygen consumption. High-resolution respirometry and fluorometry of BAT mitochondria showed that loss of mitochondrial PE specifically lowers UCP1-dependent respiration without compromising electron transfer efficiency or ATP synthesis. These findings were confirmed by a reduction in UCP1 proton current in PE-deficient mitoplasts. Thus, PE performs a previously unknown role as a temperature-responsive rheostat that regulates UCP1-dependent thermogenesis.

Identifiants

DOI: 10.1126/sciadv.ade7864 PMID: 36827367 PMC: PMC9956115
pubmed: 36827367
doi: 10.1126/sciadv.ade7864
pmc: PMC9956115
doi:

Substances chimiques

Uncoupling Protein 1 0
Phosphatidylethanolamines 0
Protons 0
Adenosine Triphosphate 8L70Q75FXE
Ucp1 protein, mouse 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

eade7864

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK115867
Pays : United States
Organisme : NIDDK NIH HHS
ID : F31 DK130555
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM131854
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM144613
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL141353
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK127979
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL165797
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK107397
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK132239
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK118333
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK091317
Pays : United States

Références

World J Gastroenterol. 2014 Oct 21;20(39):14205-18
pubmed: 25339807
Am J Physiol. 1991 Oct;261(4 Pt 1):G608-20
pubmed: 1928348
J Neurol Sci. 1983 Dec;62(1-3):327-55
pubmed: 6142097
Cell. 2014 Jul 3;158(1):69-83
pubmed: 24995979
Mol Metab. 2022 Jan;55:101405
pubmed: 34844020
NCHS Data Brief. 2020 Jun;(369):1-8
pubmed: 32600518
Cell. 2012 Oct 12;151(2):400-13
pubmed: 23063128
Metabolism. 1984 Sep;33(9):853-7
pubmed: 6472117
Am J Physiol Cell Physiol. 2016 Aug 1;311(2):C239-45
pubmed: 27335172
Cell Rep. 2018 Jul 17;24(3):781-790
pubmed: 30021173
Prim Care. 2009 Jun;36(2):271-85
pubmed: 19501243
Am J Physiol. 1996 May;270(5 Pt 1):E768-75
pubmed: 8967464
Biochim Biophys Acta. 2009 Oct;1788(10):2048-58
pubmed: 19539604
Front Physiol. 2013 Apr 17;4:74
pubmed: 23616771
Curr Opin Cell Biol. 2020 Apr;63:162-173
pubmed: 32106003
Acta Physiol (Oxf). 2016 Aug;217(4):311-24
pubmed: 27064138
Cells. 2019 Apr 16;8(4):
pubmed: 30995798
J Lipid Res. 2008 May;49(5):1137-46
pubmed: 18281723
J Biol Chem. 1998 Jan 2;273(1):215-21
pubmed: 9417067
Life Sci Alliance. 2019 Mar 11;2(2):
pubmed: 30858161
Cell Metab. 2018 Apr 3;27(4):869-885.e6
pubmed: 29617645
Nat Med. 2017 Dec;23(12):1454-1465
pubmed: 29131158
Trends Endocrinol Metab. 2016 Aug;27(8):553-562
pubmed: 27370525
Biophys J. 2003 May;84(5):3436-56
pubmed: 12719270
J Biol Chem. 2009 Feb 20;284(8):5352-61
pubmed: 19049983
Sci Rep. 2017 Nov 22;7(1):16082
pubmed: 29167565
J Cardiovasc Pharmacol. 2017 Feb;69(2):71-78
pubmed: 28170359
Cell Metab. 2018 Jul 03;28(1):159-174.e11
pubmed: 29861389
Curr Opin Clin Nutr Metab Care. 2012 Mar;15(2):122-6
pubmed: 22248591
Chem Phys Lipids. 2014 Apr;179:75-81
pubmed: 24189589
Diabetologia. 2021 Jul;64(7):1642-1659
pubmed: 33770195
Biochim Biophys Acta Biomembr. 2017 Sep;1859(9 Pt B):1558-1572
pubmed: 28411170
Mol Metab. 2020 Jan;31:55-66
pubmed: 31918922
Proc Natl Acad Sci U S A. 2015 Jun 2;112(22):6973-8
pubmed: 26038550
Mech Ageing Dev. 2017 Mar;162:9-17
pubmed: 28213011
Nat Commun. 2022 May 19;13(1):2769
pubmed: 35589699
J Mol Cell Cardiol. 2009 Dec;47(6):819-27
pubmed: 19703463
Cells. 2019 Jul 16;8(7):
pubmed: 31315173
Cell Rep. 2015 Dec 1;13(9):2000-13
pubmed: 26628366
J Agric Food Chem. 2022 Mar 23;70(11):3529-3540
pubmed: 35212227
J Appl Physiol (1985). 2013 Feb 15;114(4):444-52
pubmed: 23221956
J Bioenerg Biomembr. 2014 Oct;46(5):447-57
pubmed: 24951897
Proc Natl Acad Sci U S A. 1975 Mar;72(3):883-7
pubmed: 1055387
J Exp Biol. 2018 Apr 11;221(Pt 7):
pubmed: 29643174
Cell Death Dis. 2020 Jan 23;11(1):51
pubmed: 31974344
Biochem Soc Trans. 2003 Dec;31(Pt 6):1120-4
pubmed: 14641008
FASEB J. 2013 May;27(5):2039-44
pubmed: 23322164
Nature. 2019 Jul;571(7766):515-520
pubmed: 31341297
Methods Enzymol. 1997;286:45-67
pubmed: 9309644
Nat Cell Biol. 2013 Jun;15(6):659-67
pubmed: 23624403
J Lipid Res. 2014 Nov;55(11):2276-86
pubmed: 25193997
Mol Metab. 2012 Nov 08;2(1):5-9
pubmed: 24024125
J Bioenerg Biomembr. 2016 Apr;48(2):99-112
pubmed: 25627476
J Biol Chem. 1995 May 12;270(19):11190-8
pubmed: 7744750
Biochim Biophys Acta. 2013 Mar;1831(3):543-54
pubmed: 22960354
Trends Biochem Sci. 2016 Mar;41(3):261-273
pubmed: 26857402
J Nutr Biochem. 2017 Jul;45:94-103
pubmed: 28437736
Diabetes. 2014 Aug;63(8):2620-30
pubmed: 24677714
Free Radic Biol Med. 2015 Dec;89:1067-76
pubmed: 26520807
J Biol Chem. 2013 Feb 8;288(6):4158-73
pubmed: 23250747
Nat Metab. 2021 Nov;3(11):1445-1465
pubmed: 34799702
Sci Adv. 2019 Sep 11;5(9):eaax8352
pubmed: 31535029
Nature. 2021 May;593(7860):580-585
pubmed: 33981039
Hum Mutat. 2019 Mar;40(3):299-309
pubmed: 30488656
Biochem J. 2011 Jul 15;437(2):215-22
pubmed: 21554250

Auteurs

Jordan M Johnson (JM)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Department of Nutrition and Integrative Physiology, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0002-2971-2322

Alek D Peterlin (AD)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Department of Nutrition and Integrative Physiology, University of Utah, Salt Lake City, UT, USA.
Utah Center for Clinical and Translational Research, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0002-2837-7446

Enrique Balderas (E)

Nora Eccles Harrison Cardiovascular Research and Training Institute, Division of Cardiovascular Medicine, Department of Internal Medicine, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0001-8780-9272

Elahu G Sustarsic (EG)

Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen, Denmark.
ORCID: 0000-0002-4792-4740

J Alan Maschek (JA)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Department of Nutrition and Integrative Physiology, University of Utah, Salt Lake City, UT, USA.
Metabolomics Core Research Facility, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0003-3217-2299

Marisa J Lang (MJ)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Department of Nutrition and Integrative Physiology, University of Utah, Salt Lake City, UT, USA.

Alejandro Jara-Ramos (A)

Nora Eccles Harrison Cardiovascular Research and Training Institute, Division of Cardiovascular Medicine, Department of Internal Medicine, University of Utah, Salt Lake City, UT, USA.

Vanja Panic (V)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Department of Biochemistry, University of Utah, Salt Lake City, UT, USA.

Jeffrey T Morgan (JT)

Department of Biochemistry, University of Utah, Salt Lake City, UT, USA.
Howard Hughes Medical Institute, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0002-3017-8665

Claudio J Villanueva (CJ)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Department of Biochemistry, University of Utah, Salt Lake City, UT, USA.
Department of Integrative Biology and Physiology, University of California Los Angeles, Los Angeles, CA, USA.

Alejandro Sanchez (A)

Division of Urology, Department of Surgery, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA.

Jared Rutter (J)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Department of Biochemistry, University of Utah, Salt Lake City, UT, USA.
Howard Hughes Medical Institute, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0002-2710-9765

Irfan J Lodhi (IJ)

Division of Endocrinology, Metabolism and Lipid Research, Washington University School of Medicine, St. Louis, MO, USA.
ORCID: 0000-0002-6246-9862

James E Cox (JE)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Metabolomics Core Research Facility, University of Utah, Salt Lake City, UT, USA.
Department of Biochemistry, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0002-5977-2350

Kelsey H Fisher-Wellman (KH)

East Carolina Diabetes and Obesity Institute, East Carolina University, Greenville, NC, USA.
ORCID: 0000-0002-0300-829X

Dipayan Chaudhuri (D)

Nora Eccles Harrison Cardiovascular Research and Training Institute, Division of Cardiovascular Medicine, Department of Internal Medicine, University of Utah, Salt Lake City, UT, USA.
Department of Biochemistry, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0003-0605-7334

Zachary Gerhart-Hines (Z)

Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen, Denmark.
ORCID: 0000-0003-2981-4991

Katsuhiko Funai (K)

Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT, USA.
Department of Nutrition and Integrative Physiology, University of Utah, Salt Lake City, UT, USA.
Molecular Medicine Program, University of Utah, Salt Lake City, UT, USA.
ORCID: 0000-0003-3802-4756

Articles similaires

Meal Timing and Anthropometric and Metabolic Outcomes: A Systematic Review and Meta-Analysis.

Hiu Yee Liu, Ashley A Eso, Nathan Cook et al.
1.00
Humans Meals Time Factors Female Adult

Evaluating the efficacy of telesurgery with dual console SSI Mantra Surgical Robotic System: experiment on animal model and clinical trials.

Sudhir Prem Srivastava, Vishwajyoti Pascual Srivastava, Avinesh Singh et al.
1.00
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell

FBXO22 inhibits colitis and colorectal carcinogenesis by regulating the degradation of the S2448-phosphorylated form of mTOR.

Minle Li, Xuan Chen, Pengfei Qu et al.
1.00
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH

Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › Eucaryotes › Animaux › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines mitochondriales › Protéines de transport de la membrane mitochondriale › Protéines de découplage mitochondrial › Protéine-1 de découplage › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › Lipides › Lipides membranaires › Phospholipides › Glycérophosphate › Acides phosphatidiques › Glycérophospholipides › Phosphatidyléthanolamine › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › Phénomènes physiques › Particules élémentaires › Nucléons › Protons › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › Cellules › Structures cellulaires › Fractions subcellulaires › Mitochondries › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › Phénomènes biologiques › Adaptation biologique › Adaptation physiologique › Régulation de la température corporelle › Thermogenèse › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › États, signes et symptômes pathologiques › Signes et symptômes › Obésité › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › Acides nucléiques, nucléotides et nucléosides › Nucléotides › Ribonucléotides › Nucléotides adényliques › Adénosine triphosphate › Mitochondrial phosphatidylethanolamine...
Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Souris transgéniques › Souris knockout › Mitochondrial phosphatidylethanolamine...