Crosstalk between Drp1 phosphorylation sites during mitochondrial remodeling and their impact on metabolic adaptation.

Drp1 brown adipose tissue insulin resistance metabolic syndrome mitochondrial dynamics mitochondrial respiration phosphorylation thermoneutrality

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
24 08 2021
Historique:
received: 14 09 2020
revised: 07 06 2021
accepted: 29 07 2021
entrez: 25 8 2021
pubmed: 26 8 2021
medline: 12 2 2022
Statut: ppublish

Résumé

Mitochondria constantly undergo fusion and fission events, referred as mitochondrial dynamics, which determine mitochondrial architecture and bioenergetics. Cultured cell studies demonstrate that mitochondrial dynamics are acutely regulated by phosphorylation of the mitochondrial fission orchestrator dynamin-related protein 1 (Drp1) at S579 or S600. However, the physiological impact and crosstalk of these phosphorylation sites is poorly understood. Here, we describe the functional interrelation between S579 and S600 phosphorylation sites in vivo and their role on mitochondrial remodeling. Mice carrying a homozygous Drp1 S600A knockin (Drp1 KI) mutation display larger mitochondria and enhanced lipid oxidation and respiratory capacities, granting improved glucose tolerance and thermogenic response upon high-fat feeding. Housing mice at thermoneutrality blunts these differences, suggesting a role for the brown adipose tissue in the protection of Drp1 KI mice against metabolic damage. Overall, we demonstrate crosstalk between Drp1 phosphorylation sites and provide evidence that their modulation could be used in the treatment and prevention of metabolic diseases.

Identifiants

pubmed: 34433037
pii: S2211-1247(21)00999-2
doi: 10.1016/j.celrep.2021.109565
pmc: PMC8411118
pii:
doi:

Substances chimiques

Dnm1l protein, mouse EC 3.6.5.5
Dynamins EC 3.6.5.5

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

109565

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests M.V.-A., M.J., J.L.S.-G., A.C., A.V., L.D., A.N.G., and C.C. are employees of Nestlé Research Ltd., Société des Produits Nestlé SA. A.G.L. is co-founder and CSO of Eisbach Bio GmbH.

Références

Nat Commun. 2019 Jun 12;10(1):2576
pubmed: 31189900
Curr Protoc Mouse Biol. 2015 Jun 01;5(2):135-153
pubmed: 26069081
Biochim Biophys Acta. 2013 May;1833(5):1256-68
pubmed: 23434681
J Clin Invest. 2019 May 7;129(7):2807-2823
pubmed: 31063459
J Exp Biol. 2011 Jan 15;214(Pt 2):242-53
pubmed: 21177944
Front Physiol. 2013 Jun 04;4:128
pubmed: 23760815
J Proteome Res. 2021 May 7;20(5):2283-2290
pubmed: 33769819
Biochim Biophys Acta Mol Basis Dis. 2020 Mar 1;1866(3):165615
pubmed: 31759069
Physiol Rev. 2009 Jul;89(3):799-845
pubmed: 19584314
EMBO Rep. 2017 Jul;18(7):1123-1138
pubmed: 28539390
Proc Natl Acad Sci U S A. 2011 Jun 21;108(25):10190-5
pubmed: 21646527
EMBO Rep. 2019 Sep;20(9):e47928
pubmed: 31418169
Diabetologia. 2015 Oct;58(10):2371-80
pubmed: 26233250
J Clin Invest. 2019 Feb 1;129(2):694-711
pubmed: 30511960
EMBO J. 2017 Jun 1;36(11):1543-1558
pubmed: 28348166
J Biol Chem. 2011 Apr 1;286(13):11649-58
pubmed: 21292769
Mol Metab. 2014 Dec 18;4(2):118-31
pubmed: 25685699
Nat Cell Biol. 2011 May;13(5):589-98
pubmed: 21478857
Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15803-8
pubmed: 18838687
J Biol Chem. 2018 Jul 27;293(30):11809-11822
pubmed: 29853636
Ann N Y Acad Sci. 2010 Jul;1201:34-9
pubmed: 20649536
Mol Biol Cell. 2011 Jan 15;22(2):256-65
pubmed: 21119009
Cell Metab. 2013 Apr 2;17(4):491-506
pubmed: 23562075
Curr Protoc Mouse Biol. 2017 Mar 2;7(1):47-54
pubmed: 28252199
Am J Med Genet A. 2016 Aug;170(8):2002-11
pubmed: 27145208
J Neurosci. 2020 Apr 8;40(15):3119-3129
pubmed: 32144179
J Cell Biol. 2009 Sep 21;186(6):805-16
pubmed: 19752021
J Neurosci. 2018 Sep 19;38(38):8233-8242
pubmed: 30093535
EMBO Rep. 2007 Oct;8(10):939-44
pubmed: 17721437
Am J Physiol Regul Integr Comp Physiol. 2013 Mar 15;304(6):R393-406
pubmed: 23364527
J Biol Chem. 2007 Jul 27;282(30):21583-7
pubmed: 17553808
EMBO J. 2014 Mar 3;33(5):418-36
pubmed: 24431221
Nat Med. 2013 Jan;19(1):83-92
pubmed: 23202295
Cell Rep. 2019 Mar 12;26(11):2849-2858.e4
pubmed: 30865877
Nat Metab. 2019 Feb;1(2):189-200
pubmed: 31903450
Anal Chem. 2012 Jun 5;84(11):5035-9
pubmed: 22533540
Nat Cell Biol. 2009 Aug;11(8):958-66
pubmed: 19578372
Mol Cell. 2015 Feb 5;57(3):537-51
pubmed: 25658205
Acta Histochem. 2017 Apr;119(3):315-326
pubmed: 28314612
Cell Metab. 2012 Feb 8;15(2):186-200
pubmed: 22326220
J Biol Chem. 2016 Jan 1;291(1):493-507
pubmed: 26578513
Trends Endocrinol Metab. 2016 Feb;27(2):105-117
pubmed: 26754340
J Cell Biol. 2007 May 7;177(3):439-50
pubmed: 17470634
Mol Cell. 2015 Feb 5;57(3):521-36
pubmed: 25658204
Nat Protoc. 2006;1(6):2856-60
pubmed: 17406544
J Cell Biol. 2013 Jun 24;201(7):1037-51
pubmed: 23798729
J Appl Physiol (1985). 2013 Sep 1;115(5):765-70
pubmed: 23788579
J Biol Chem. 2007 Apr 13;282(15):11521-9
pubmed: 17301055
Diabetes. 2016 Dec;65(12):3552-3560
pubmed: 27613809
J Cell Biol. 2008 Aug 11;182(3):573-85
pubmed: 18695047
Oncol Rep. 2019 Jun;41(6):3292-3304
pubmed: 31002345
Int Rev Cell Mol Biol. 2018;340:129-167
pubmed: 30072090
J Cell Sci. 2019 May 31;132(11):
pubmed: 31076512
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
J Biol Chem. 2003 Mar 7;278(10):8597-605
pubmed: 12499366
J Biol Chem. 2003 May 9;278(19):17012-20
pubmed: 12618434
J Cell Sci. 2017 Sep 15;130(18):2953-2960
pubmed: 28842472
N Engl J Med. 2007 Apr 26;356(17):1736-41
pubmed: 17460227

Auteurs

Miriam Valera-Alberni (M)

Nestlé Institute of Health Sciences, Nestlé Research Ltd., Lausanne 1015, Switzerland; School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland.

Magali Joffraud (M)

Nestlé Institute of Health Sciences, Nestlé Research Ltd., Lausanne 1015, Switzerland.

Joan Miro-Blanch (J)

Universitat Rovira i Virgili, Department of Electronic Engineering & IISPV, 43003 Tarragona, Spain; CIBER de Diabetes y Enfermedates Metabólicas Asociadas (CIBERDEM), 28029 Madrid, Spain.

Jordi Capellades (J)

Universitat Rovira i Virgili, Department of Electronic Engineering & IISPV, 43003 Tarragona, Spain; CIBER de Diabetes y Enfermedates Metabólicas Asociadas (CIBERDEM), 28029 Madrid, Spain.

Alexandra Junza (A)

Universitat Rovira i Virgili, Department of Electronic Engineering & IISPV, 43003 Tarragona, Spain; CIBER de Diabetes y Enfermedates Metabólicas Asociadas (CIBERDEM), 28029 Madrid, Spain.

Loïc Dayon (L)

Nestlé Institute of Food Safety and Analytical Sciences, Nestlé Research Ltd., Lausanne 1015, Switzerland; Institut des Sciences et Ingénierie Chimiques, EPFL, Lausanne 1015, Switzerland.

Antonio Núñez Galindo (A)

Nestlé Institute of Food Safety and Analytical Sciences, Nestlé Research Ltd., Lausanne 1015, Switzerland.

Jose L Sanchez-Garcia (JL)

Nestlé Institute of Health Sciences, Nestlé Research Ltd., Lausanne 1015, Switzerland.

Armand Valsesia (A)

Nestlé Institute of Health Sciences, Nestlé Research Ltd., Lausanne 1015, Switzerland.

Angelique Cercillieux (A)

Nestlé Institute of Health Sciences, Nestlé Research Ltd., Lausanne 1015, Switzerland; School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland.

Flavia Söllner (F)

Biomedical Center, Department of Physiological Chemistry, Ludwig-Maximilians-Universität München, 82152 Planegg-Martinsried, Germany.

Andreas G Ladurner (AG)

Biomedical Center, Department of Physiological Chemistry, Ludwig-Maximilians-Universität München, 82152 Planegg-Martinsried, Germany.

Oscar Yanes (O)

Universitat Rovira i Virgili, Department of Electronic Engineering & IISPV, 43003 Tarragona, Spain; CIBER de Diabetes y Enfermedates Metabólicas Asociadas (CIBERDEM), 28029 Madrid, Spain.

Carles Cantó (C)

Nestlé Institute of Health Sciences, Nestlé Research Ltd., Lausanne 1015, Switzerland; School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland. Electronic address: carles.cantoalvarez@rd.nestle.com.

Articles similaires

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
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH