Adipocyte deletion of the oxygen-sensor PHD2 sustains elevated energy expenditure at thermoneutrality.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
29 Aug 2024
Historique:
received: 09 04 2022
accepted: 14 08 2024
medline: 1 9 2024
pubmed: 1 9 2024
entrez: 29 8 2024
Statut: epublish

Résumé

Enhancing thermogenic brown adipose tissue (BAT) function is a promising therapeutic strategy for metabolic disease. However, predominantly thermoneutral modern human living conditions deactivate BAT. We demonstrate that selective adipocyte deficiency of the oxygen-sensor HIF-prolyl hydroxylase (PHD2) gene overcomes BAT dormancy at thermoneutrality. Adipocyte-PHD2-deficient mice maintain higher energy expenditure having greater BAT thermogenic capacity. In human and murine adipocytes, a PHD inhibitor increases Ucp1 levels. In murine brown adipocytes, antagonising the major PHD2 target, hypoxia-inducible factor-(HIF)-2a abolishes Ucp1 that cannot be rescued by PHD inhibition. Mechanistically, PHD2 deficiency leads to HIF2 stabilisation and binding of HIF2 to the Ucp1 promoter, thus enhancing its expression in brown adipocytes. Serum proteomics analysis of 5457 participants in the deeply phenotyped Age, Gene and Environment Study reveal that serum PHD2 associates with increased risk of metabolic disease. Here we show that adipose-PHD2-inhibition is a therapeutic strategy for metabolic disease and identify serum PHD2 as a disease biomarker.

Identifiants

pubmed: 39209825
doi: 10.1038/s41467-024-51718-7
pii: 10.1038/s41467-024-51718-7
pmc: PMC11362468
doi:

Substances chimiques

Hypoxia-Inducible Factor-Proline Dioxygenases EC 1.14.11.29
Uncoupling Protein 1 0
Egln1 protein, mouse EC 1.14.11.29
EGLN1 protein, human EC 1.14.11.2
Ucp1 protein, mouse 0
endothelial PAS domain-containing protein 1 1B37H0967P
Basic Helix-Loop-Helix Transcription Factors 0
Oxygen S88TT14065
UCP1 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

7483

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom

Informations de copyright

© 2024. The Author(s).

Références

Nat Commun. 2015 Mar 10;6:6356
pubmed: 25754609
J Mol Med (Berl). 2020 May;98(5):719-731
pubmed: 32296880
Diabetes. 2013 Mar;62(3):864-74
pubmed: 23321074
J Biol Chem. 2004 Sep 24;279(39):40946-53
pubmed: 15258146
Drugs. 2019 Apr;79(5):563-572
pubmed: 30805897
Am J Physiol. 1986 Jun;250(6 Pt 1):C880-7
pubmed: 3717329
Nat Commun. 2022 Jan 25;13(1):480
pubmed: 35078996
Physiol Rep. 2016 May;4(10):
pubmed: 27230905
Cell Metab. 2015 Oct 6;22(4):546-59
pubmed: 26445512
J Am Soc Nephrol. 2020 Mar;31(3):560-577
pubmed: 31996409
Wellcome Open Res. 2019 Jan 29;4:17
pubmed: 30801039
Diabetes. 2014 Oct;63(10):3324-33
pubmed: 24789921
Nat Med. 2017 Dec;23(12):1454-1465
pubmed: 29131158
Adipocyte. 2016 Feb 18;5(2):119-29
pubmed: 27386156
Cell Metab. 2020 Aug 4;32(2):215-228.e7
pubmed: 32663458
Physiol Behav. 2017 Oct 1;179:55-66
pubmed: 28533176
Nat Commun. 2022 Jun 13;13(1):3401
pubmed: 35697682
J Biol Chem. 2000 Aug 18;275(33):25494-501
pubmed: 10829031
Mol Cell Endocrinol. 2021 Aug 1;533:111337
pubmed: 34062167
Science. 2001 Apr 20;292(5516):464-8
pubmed: 11292862
Cell Metab. 2019 Nov 5;30(5):937-951.e5
pubmed: 31668872
PLoS Biol. 2018 Jul 3;16(7):e2005970
pubmed: 29969450
J Innate Immun. 2022;14(1):4-30
pubmed: 33849008
Science. 2018 Aug 24;361(6404):769-773
pubmed: 30072576
Nat Commun. 2022 Jan 25;13(1):481
pubmed: 35079000
FEBS J. 2020 Aug;287(16):3370-3385
pubmed: 32301220
J Biol Chem. 2020 Feb 14;295(7):1926-1942
pubmed: 31914415
Am J Epidemiol. 2007 May 1;165(9):1076-87
pubmed: 17351290
Circulation. 2013 May 28;127(21):2078-87
pubmed: 23630130
Mol Cell Biol. 2009 Aug;29(16):4467-83
pubmed: 19546236
Genes Dev. 2012 Feb 1;26(3):259-70
pubmed: 22302938
Nat Med. 2011 Feb;17(2):200-5
pubmed: 21258337
N Engl J Med. 2019 Sep 12;381(11):1001-1010
pubmed: 31340089
Bioinformatics. 2016 Oct 15;32(20):3207-3209
pubmed: 27318201
Cell Metab. 2020 Aug 4;32(2):287-300.e7
pubmed: 32755608
Cell Metab. 2009 Jan 7;9(1):99-109
pubmed: 19117550
Cell Rep. 2020 Apr 14;31(2):107501
pubmed: 32294435
J Biol Chem. 2012 Feb 3;287(6):4188-97
pubmed: 22158867
Curr Obes Rep. 2017 Dec;6(4):389-396
pubmed: 29101739
J Exp Biol. 2011 Jan 15;214(Pt 2):242-53
pubmed: 21177944
Mol Metab. 2012 Nov 08;2(1):5-9
pubmed: 24024125
Cell Rep Med. 2021 Jul 07;2(7):100332
pubmed: 34337558
Science. 2001 Apr 20;292(5516):468-72
pubmed: 11292861
Front Endocrinol (Lausanne). 2021 Apr 13;12:652444
pubmed: 33927694
Mol Cell Biol. 2015 Nov 16;36(3):376-93
pubmed: 26572826
Chem Sci. 2017 Nov 1;8(11):7651-7668
pubmed: 29435217
Annu Rev Pharmacol Toxicol. 2019 Jan 6;59:379-403
pubmed: 30625281
Int J Obes (Lond). 2010 Dec;34 Suppl 2:S53-8
pubmed: 21151148
Adv Ther. 2018 Jan;35(1):5-11
pubmed: 29285707
Mol Metab. 2018 Jan;7:161-170
pubmed: 29122558
Drugs. 2020 Sep;80(14):1491-1497
pubmed: 32880805
Genes Dev. 2013 Feb 1;27(3):234-50
pubmed: 23388824
Cancer Res. 2016 Sep 15;76(18):5491-500
pubmed: 27635045
Cell Metab. 2011 Mar 2;13(3):249-59
pubmed: 21356515
J Clin Invest. 2020 Dec 1;130(12):6688-6699
pubmed: 33164985
Diabetes. 2015 Mar;64(3):733-45
pubmed: 25377876

Auteurs

Rongling Wang (R)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.

Mario Gomez Salazar (M)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.

Iris Pruñonosa Cervera (I)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.

Amanda Coutts (A)

Department of Biosciences, School of Science and Technology, Nottingham Trent University, Clifton, Nottingham, UK.

Karen French (K)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.

Marlene Magalhaes Pinto (MM)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.

Sabrina Gohlke (S)

Department of Adipocyte Development and Nutrition, German Institute of Human Nutrition, Potsdam-Rehbrücke, Nuthetal, Germany.

Ruben García-Martín (R)

Department of Immunology and Oncology, Centro Nacional de Biotecnología/CSIC (CNB-CSIC), Campus-UAM, Madrid, Spain.

Matthias Blüher (M)

Helmholtz Institute for Metabolic, Obesity and Vascular Research (HI-MAG) of the Helmholtz Zentrum München at the University of Leipzig and University Hospital Leipzig, Leipzig, Germany.

Christopher J Schofield (CJ)

Chemistry Research Laboratory, Department of Chemistry and the Ineos Oxford Institute for Antimicrobial Research University of Oxford, Oxford, UK.

Ioannis Kourtzelis (I)

Hull York Medical School, York Biomedical Research Institute, University of York, York, UK.

Roland H Stimson (RH)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.

Cécile Bénézech (C)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.

Mark Christian (M)

Department of Biosciences, School of Science and Technology, Nottingham Trent University, Clifton, Nottingham, UK.

Tim J Schulz (TJ)

Department of Adipocyte Development and Nutrition, German Institute of Human Nutrition, Potsdam-Rehbrücke, Nuthetal, Germany.
German Center for Diabetes Research (DZD), München-Neuherberg, Germany.

Elias F Gudmundsson (EF)

Icelandic Heart Association, Kopavogur, Iceland.

Lori L Jennings (LL)

Novartis Institutes for Biomedical Research, Cambridge, MA, USA.

Vilmundur G Gudnason (VG)

Icelandic Heart Association, Kopavogur, Iceland.
Faculty of Medicine, University of Iceland, Reykjavik, Iceland.

Triantafyllos Chavakis (T)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.
German Center for Diabetes Research (DZD), München-Neuherberg, Germany.
Institute for Clinical Chemistry and Laboratory Medicine, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.
Paul Langerhans Institute Dresden, Helmholtz Zentrum München, University Hospital and Faculty of Medicine Technische Universität Dresden, Dresden, Germany.

Nicholas M Morton (NM)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.
Department of Biosciences, School of Science and Technology, Nottingham Trent University, Clifton, Nottingham, UK.

Valur Emilsson (V)

Icelandic Heart Association, Kopavogur, Iceland.
Faculty of Medicine, University of Iceland, Reykjavik, Iceland.

Zoi Michailidou (Z)

Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK. zoi.michailidou@ntu.ac.uk.
Department of Biosciences, School of Science and Technology, Nottingham Trent University, Clifton, Nottingham, UK. zoi.michailidou@ntu.ac.uk.

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