IF1 is a cold-regulated switch of ATP synthase hydrolytic activity to support thermogenesis in brown fat.
Adipocytes
Metabolism
Mitochondria
Thermogenesis
UCP1
Journal
The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664
Informations de publication
Date de publication:
16 Sep 2024
16 Sep 2024
Historique:
received:
30
04
2024
accepted:
16
08
2024
revised:
03
08
2024
medline:
17
9
2024
pubmed:
17
9
2024
entrez:
16
9
2024
Statut:
aheadofprint
Résumé
While mechanisms controlling uncoupling protein-1 (UCP1) in thermogenic adipocytes play a pivotal role in non-shivering thermogenesis, it remains unclear whether F
Identifiants
pubmed: 39284909
doi: 10.1038/s44318-024-00215-0
pii: 10.1038/s44318-024-00215-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)
ID : 2022/00358-1
Organisme : EC | European Research Council (ERC)
ID : 852742
Organisme : Deutsche Forschungsgemeinschaft (DFG)
ID : BA4925/2-1
Organisme : Deutsches Zentrum für Herz-Kreislaufforschung (DZHK)
ID : 81X3600212
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)
ID : 310287/2018-9
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)
ID : 88881.143924/2017-01
Informations de copyright
© 2024. The Author(s).
Références
Acin-Perez R, Beninca C, Fernandez L, Shu C, Baghdasarian S, Zanette V, Gerle C, Jiko C, Khairallah R, Khan S et al (2023) Inhibition of ATP synthase reverse activity restores energy homeostasis in mitochondrial pathologies. EMBO J 42:1–21
Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C et al (2011) Brown adipose tissue activity controls triglyceride clearance. Nat Med 17(2):200–206
pubmed: 21258337
doi: 10.1038/nm.2297
Benador IY, Veliova M, Mahdaviani K, Petcherski A, Wikstrom JD, Assali EA, Acín-Pérez R, Shum M, Oliveira MF, Cinti S et al (2018) Mitochondria bound to lipid droplets have unique bioenergetics, composition, and dynamics that support lipid droplet expansion. Cell Metab 27(4):869–885.e6
pubmed: 29617645
pmcid: 5969538
doi: 10.1016/j.cmet.2018.03.003
Brunetta HS, Petrick HL, Momken I, Handy RM, Pignanelli C, Nunes EA, Piquereau J, Mericskay M, Holloway GP (2022) Nitrate consumption preserves HFD-induced skeletal muscle mitochondrial ADP sensitivity and lysine acetylation: a potential role for SIRT1. Redox Biol 52(3):102307
pubmed: 35398714
pmcid: 9006675
doi: 10.1016/j.redox.2022.102307
Brunetta HS, Politis-Barber V, Petrick HL, Dennis KMJH, Kirsh AJ, Barbeau PA, Nunes EA, Holloway GP (2020) Nitrate attenuates high fat diet-induced glucose intolerance in association with reduced epididymal adipose tissue inflammation and mitochondrial reactive oxygen species emission. J Physiol 598(16):3357–3371
pubmed: 32449521
doi: 10.1113/JP279455
Cabezon E, Butler PJG, Runswick MJ, Walker JE (2000) Modulation of the oligomerization state of the bovine F
pubmed: 10831597
doi: 10.1074/jbc.M003859200
Cabezón E, Montgomery MG, Leslie AGW, Walker JE (2003) The structure of bovine F
pubmed: 12923572
doi: 10.1038/nsb966
Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84(1):277–359
pubmed: 14715917
doi: 10.1152/physrev.00015.2003
Carroll J, Watt IN, Wright CJ, Ding S, Fearnley IM, Walker JE (2024) The inhibitor protein IF1 from mammalian mitochondria inhibits ATP hydrolysis but not ATP synthesis by the ATP synthase complex. J Biol Chem 300(3):105690
pubmed: 38280428
pmcid: 10906535
doi: 10.1016/j.jbc.2024.105690
Chen WW, Mihaylova MM, Snitkin H, Stasinski I, Yucel B, Bayraktar EC, Carette JE, Clish CB, Brummelkamp TR, Sabatini DD (2014) Report inhibition of ATPIF1 ameliorates severe mitochondrial respiratory chain dysfunction in mammalian cells. Cell Rep 7:27–34
pubmed: 24685140
pmcid: 4040975
doi: 10.1016/j.celrep.2014.02.046
Chouchani ET, Kazak L, Spiegelman BM (2019) New advances in adaptive thermogenesis: UCP1 and beyond. Cell Metab 29(1):27–37
pubmed: 30503034
doi: 10.1016/j.cmet.2018.11.002
Collins S (2022) β-Adrenergic Receptors and Adipose Tissue Metabolism: Evolution of an Old Story. Annu Rev Physiol 84:1–16
Domínguez-Zorita S, Romero-Carramiñana I, Santa-Catterina F, Esparza-Moltó PB, Simó C, del-Arco A, Núñez de Arenas C, Saiz J, Barbas C et al (2023) IF1 ablation prevents ATP synthase oligomerization, enhances mitochondrial ATP turnover and promotes an adenosine-mediated pro-inflammatory phenotype. Cell Death Dis 14(7):413
pubmed: 37433784
pmcid: 10336053
doi: 10.1038/s41419-023-05957-z
Esparza-Moltó PB, Cristina M, Tapioles N, Cuezva JM (2017) Regulation of the H+-ATP synthase by IF
doi: 10.1007/s00018-017-2462-8
Fedorenko A, Lishko P, Kirichok Y (2012) Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151(1):400–413
pubmed: 23063128
pmcid: 3782081
doi: 10.1016/j.cell.2012.09.010
Formentini L, Ryan AJ, Gálvez-Santisteban M, Carter L, Taub P, Lapek JD, Gonzalez DJ, Villarreal F, Ciaraldi TP, Cuezva JM et al (2017) Mitochondrial H+-ATP synthase in human skeletal muscle: contribution to dyslipidaemia and insulin resistance. Diabetologia 60(10):2052–2065
pubmed: 28770317
pmcid: 6572787
doi: 10.1007/s00125-017-4379-z
Formentini L, Sánchez-Aragó M, Sánchez-Cenizo L, Cuezva JMC (2012) The mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response. Mol Cell 45(6):731–742
pubmed: 22342343
doi: 10.1016/j.molcel.2012.01.008
Forner F, Kumar C, Luber CA, Fromme T, Klingenspor M, Mann M (2009) Proteome differences between brown and white fat mitochondria reveal specialized metabolic functions. Cell Metab 10(4):324–335
pubmed: 19808025
doi: 10.1016/j.cmet.2009.08.014
Francisco A, Ronchi JA, Navarro CDC, Figueira TR, Castilho RF (2018) Nicotinamide nucleotide transhydrogenase is required for brain mitochondrial redox balance under hampered energy substrate metabolism and high-fat diet. J Neurochem 147(5):663–677
pubmed: 30281804
doi: 10.1111/jnc.14602
Fromme T, Kleigrewe K, Dunkel A, Retzler A, Li Y, Maurer S, Fischer N, Diezko R, Kanzleiter T, Hirschberg V et al (2018) Degradation of brown adipocyte purine nucleotides regulates uncoupling protein 1 activity. Mol Metab 8(12, 2017):77–85
pubmed: 29310935
doi: 10.1016/j.molmet.2017.12.010
García-Bermúdez J, Sánchez-Aragó M, Soldevilla B, del Arco A, Nuevo-Tapioles C, Cuezva JM (2015) PKA phosphorylates the ATPase inhibitory factor 1 and inactivates its capacity to bind and inhibit the mitochondrial H+-ATP synthase. Cell Rep 12(12):2143–2155
pubmed: 26387949
doi: 10.1016/j.celrep.2015.08.052
Gledhill JR, Montgomery MG, Leslie AGW, Walker JE (2007) How the regulatory protein, IF1, inhibits F1-ATPase from bovine mitochondria. Proc Natl Acad Sci USA 104(40):15671–15676
pubmed: 17895376
pmcid: 1994141
doi: 10.1073/pnas.0707326104
Hankir MK, Klingenspor M (2018) Brown adipocyte glucose metabolism: a heated subject. EMBO Rep 19(9):1–13
doi: 10.15252/embr.201846404
Kemp RG, Gunasekera D (2002) Evolution of the allosteric ligand sites of mammalian phosphofructo-1-kinase. Biochemistry 41(30):9426–9430
pubmed: 12135364
doi: 10.1021/bi020110d
Kobayashi R, Ueno H, Okazaki KI, Noji H (2023) Molecular mechanism on forcible ejection of ATPase inhibitory factor 1 from mitochondrial ATP synthase. Nat Commun 14(1):1682
pubmed: 37002198
pmcid: 10066207
doi: 10.1038/s41467-023-37182-9
Kotschi S, Jung A, Willemsen N, Ofoghi A, Proneth B, Conrad M, Bartelt A (2022) NFE2L1-mediated proteasome function protects from ferroptosis. Mol Metab 57:101436
pubmed: 34999280
pmcid: 8814388
doi: 10.1016/j.molmet.2022.101436
Li Y, Fromme T, Schweizer S, Schöttl T, Klingenspor M (2014) Taking control over intracellular fatty acid levels is essential for the analysis of thermogenic function in cultured primary brown and brite/beige adipocytes. EMBO Rep 15(10):1069–1076
pubmed: 25135951
pmcid: 4253847
doi: 10.15252/embr.201438775
Matthias A, Jacobsson A, Cannon B, Nedergaard J (1999) The bioenergetics of brown fat mitochondria from UCP1-ablated mice. UCP1 is not involved in fatty acid-induced de-energization (‘uncoupling’). J Biol Chem 274(40):28150–28160
pubmed: 10497167
doi: 10.1074/jbc.274.40.28150
Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148
pubmed: 13771349
doi: 10.1038/191144a0
Mookerjee SA, Gerencser AA, Nicholls DG, Brand MD (2017) Quantifying intracellular rates of glycolytic and oxidative ATP production and consumption using extracellular flux measurements. J Biol Chem 292(17):7189–7207
pubmed: 28270511
pmcid: 5409486
doi: 10.1074/jbc.M116.774471
Nedergaard J, Wang Y, Cannon B (2019) Cell proliferation and apoptosis inhibition: essential processes for recruitment of the full thermogenic capacity of brown adipose tissue. Biochim Biophys Acta - Mol Cell Biol Lipids 1864(1):51–58
pubmed: 29908367
doi: 10.1016/j.bbalip.2018.06.013
Nelson MAM, Mclaughlin KL, Hagen JT, Coalson HS, Schmidt C, Kassai M, Kew KA, Mcclung JM, Neufer PD et al (2021) Intrinsic OXPHOS limitations underlie cellular bioenergetics in leukemia. ELife 10:1–31
Nicholls DG (2021) Mitochondrial proton leaks and uncoupling proteins. Biochim Biophys Acta - Bioenerg 1862(7):148428
pubmed: 33798544
doi: 10.1016/j.bbabio.2021.148428
Nicholls DG (2023) Fifty years on: how we uncovered the unique bioenergetics of brown adipose tissue. Acta Physiol 237(4):e13938
doi: 10.1111/apha.13938
Park G, Haley JA, Le J, Jung SM, Fitzgibbons TP, Korobkina ED, Li H, Fluharty SM, Chen Q, Spinelli JB et al (2023) Quantitative analysis of metabolic fluxes in brown fat and skeletal muscle during thermogenesis. Nat Metab 5(7):1204–1220
pubmed: 37337122
pmcid: 10696589
doi: 10.1038/s42255-023-00825-8
Percie Du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, Browne WJ, Clark A, Cuthill IC, Dirnagl U et al (2020) The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. BMC Vet Res 16(1):1–12
Petrick HL, Brownell S, Vachon B, Brunetta HS, Handy RM, Van Loon LJC, Murrant CL, Holloway GP (2022) Dietary nitrate increases submaximal SERCA activity and ADP transfer to mitochondria in slow-twitch muscle of female mice. Am J Physiol - Endocrinol Metab 323(2):E171–E184
pubmed: 35732003
doi: 10.1152/ajpendo.00371.2021
Politis-Barber V, Petrick HL, Raajendiran A, Desormeaux GJ, Brunetta HS, Dos Reis LM, Mori MA, Wright DC, Watt MJ, Holloway GP (2022) Ckmt1 is dispensable for mitochondrial bioenergetics within white/beige adipose tissue. Function 3(5):1–16
doi: 10.1093/function/zqac037
Pullman ME, Monroy GC (1963) A naturally occurring inhibitor of mitochondrial adenosine. J Biol Chem 238(11):3762–3769
pubmed: 14109217
doi: 10.1016/S0021-9258(19)75338-1
Ruas JS, Siqueira-Santos ES, Rodrigues-Silva E, Castilho RF (2018) High glycolytic activity of tumor cells leads to underestimation of electron transport system capacity when mitochondrial ATP synthase is inhibited. Sci Rep 8(1):1–17
doi: 10.1038/s41598-018-35679-8
Sa L, Formentini L (2012) The Mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response. Mol Cell 1(45):731–742
Sánchez‐González C, Nuevo‐Tapioles C, Herrero-Martín JC, Pereira MP, Serrano SS, Molina A, Cuezva JM, Formentini L (2020) Dysfunctional oxidative phosphorylation shunts branched‐chain amino acid catabolism onto lipogenesis in skeletal muscle. EMBO J 39(14):e103812
pubmed: 32488939
pmcid: 7360968
doi: 10.15252/embj.2019103812
Schormann N, Hayden KL, Lee P, Banerjee S, Chattopadhyay D (2019) An overview of structure, function, and regulation of pyruvate kinases. Protein Sci 28(10):1771–1784
pubmed: 31342570
pmcid: 6739817
doi: 10.1002/pro.3691
Shahid M, Javed AA, Chandra D, Ramsey HE, Dilip S, Khan MF, Zhao L, Wu MX (2016) IEX-1 deficiency induces browning of white adipose tissue and resists diet-induced obesity. Sci Rep 3:1–14
Shen L, Zhi L, Hu W, Wu MX (2009) IEX-1 targets mitochondrial F
pubmed: 19096392
doi: 10.1038/cdd.2008.184
Sponton CH, de Lima-Junior JC, Leiria LO (2022) What puts the heat on thermogenic fat: metabolism of fuel substrates. Trends Endocrinol Metab 33(8):587–599
pubmed: 35697585
doi: 10.1016/j.tem.2022.05.003
Valdivieso-Rivera FB, Furino V de O, Sponton CH (2023) Investigation of beige fat biology and metabolism using the CRISPR SunTag-p65-HSF1 activation system. J Vis Exp 2023(191):1–15
Willemsen N, Arigoni I, Studencka-Turski M, Krüger E, Bartelt A (2022) Proteasome dysfunction disrupts adipogenesis and induces inflammation via ATF3. Mol Metab 62(May):101518
pubmed: 35636710
pmcid: 9194453
doi: 10.1016/j.molmet.2022.101518
Yamada EW, Huzel NJ, Bosf R, Kates A, Himms-Hagen J (1992) ATPase-inhibitor proteins of brown-adipose-tissue mitochondria from warm- and cold-acclimated rats. Biochem J 287:151–157
pubmed: 1417768
pmcid: 1133137
doi: 10.1042/bj2870151
Zhou B, Caudal A, Tang X, Chavez JD, McMillen TS, Keller A, Villet O, Zhao M, Liu Y, Ritterhoff J et al (2022) Upregulation of mitochondrial ATPase inhibitory factor 1 (ATPIF1) mediates increased glycolysis in mouse hearts. J Clin Investig 132(10):e155333
pubmed: 35575090
pmcid: 9106352
doi: 10.1172/JCI155333