{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T06:46:36Z","timestamp":1792651596455,"version":"4.5.0"},"reference-count":36,"publisher":"Elsevier BV","issue":"10","license":[{"start":{"date-parts":[[2022,6,1]],"date-time":"2022-06-01T00:00:00Z","timestamp":1654041600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2022,6,1]],"date-time":"2022-06-01T00:00:00Z","timestamp":1654041600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2022,5,13]],"date-time":"2022-05-13T00:00:00Z","timestamp":1652400000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000053","name":"National Eye Institute","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000053","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Cell Reports"],"published-print":{"date-parts":[[2022,6]]},"DOI":"10.1016\/j.celrep.2022.110917","type":"journal-article","created":{"date-parts":[[2022,6,7]],"date-time":"2022-06-07T10:57:35Z","timestamp":1654599455000},"page":"110917","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":37,"title":["Succinate metabolism in the retinal pigment epithelium uncouples respiration from ATP synthesis"],"prefix":"10.1016","volume":"39","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4481-1839","authenticated-orcid":false,"given":"Daniel T.","family":"Hass","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Celia M.","family":"Bisbach","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian M.","family":"Robbings","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin","family":"Sadilek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ian R.","family":"Sweet","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7754-0705","authenticated-orcid":false,"given":"James B.","family":"Hurley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.celrep.2022.110917_bib1","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1038\/s42255-019-0105-0","article-title":"Oxygen and mammalian cell culture: are we repeating the experiment of Dr. Ox?","volume":"1","author":"Ast","year":"2019","journal-title":"Nat. Metab."},{"key":"10.1016\/j.celrep.2022.110917_bib2","doi-asserted-by":"crossref","first-page":"107606","DOI":"10.1016\/j.celrep.2020.107606","article-title":"Succinate can shuttle reducing power from the hypoxic retina to the O2-rich pigment epithelium","volume":"31","author":"Bisbach","year":"2020","journal-title":"Cell Rep."},{"key":"10.1016\/j.celrep.2022.110917_bib3","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/nature13909","article-title":"Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS","volume":"515","author":"Chouchani","year":"2014","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2022.110917_bib4","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/S0006-3495(89)82782-1","article-title":"Adenosine triphosphate utilization rates and metabolic pool sizes in intact cells measured by transfer of 18O from water","volume":"55","author":"Dawis","year":"1989","journal-title":"Biophys. J."},{"key":"10.1016\/j.celrep.2022.110917_bib5","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1007\/978-1-4939-7831-1_3","article-title":"High-resolution FluoRespirometry and OXPHOS protocols for human cells, permeabilized fibers from small biopsies of muscle, and isolated mitochondria","volume":"1782","author":"Doerrier","year":"2018","journal-title":"Methods Mol. Biol."},{"key":"10.1016\/j.celrep.2022.110917_bib6","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/bs.mie.2015.04.002","article-title":"Probing metabolism in the intact retina using stable isotope tracers","volume":"561","author":"Du","year":"2015","journal-title":"Methods Enzymol."},{"key":"10.1016\/j.celrep.2022.110917_bib7","doi-asserted-by":"crossref","first-page":"47129","DOI":"10.1074\/jbc.M208262200","article-title":"Superoxide activates mitochondrial uncoupling protein 2 from the matrix side","volume":"277","author":"Echtay","year":"2002","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2022.110917_bib8","doi-asserted-by":"crossref","first-page":"12317","DOI":"10.1038\/ncomms12317","article-title":"Cell-permeable succinate prodrugs bypass mitochondrial complex I deficiency","volume":"7","author":"Ehinger","year":"2016","journal-title":"Nat. Commun."},{"key":"10.1016\/j.celrep.2022.110917_bib9","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/S0021-9258(18)57250-1","article-title":"The effect of succinate on respiration and certain metabolic processes of mammalian tissues at low oxygen tensions in\u00a0vitro","volume":"175","author":"Furchgott","year":"1948","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2022.110917_bib10","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1111\/bph.13738","article-title":"Identification and pharmacological characterization of succinate receptor agonists","volume":"174","author":"Geubelle","year":"2017","journal-title":"Br. J. Pharmacol."},{"key":"10.1016\/j.celrep.2022.110917_bib11","doi-asserted-by":"crossref","first-page":"101341","DOI":"10.1016\/j.redox.2019.101341","article-title":"The use of site-specific suppressors to measure the relative contributions of different mitochondrial sites to skeletal muscle superoxide and hydrogen peroxide production","volume":"28","author":"Goncalves","year":"2020","journal-title":"Redox Biol."},{"key":"10.1016\/j.celrep.2022.110917_bib12","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1038\/nature02488","article-title":"Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors","volume":"429","author":"He","year":"2004","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2022.110917_bib13","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/BF00423282","article-title":"Succinate accumulation in man during exercise","volume":"35","author":"Hochachka","year":"1976","journal-title":"Eur. J. Appl. Physiol. Occup. Physiol."},{"key":"10.1016\/j.celrep.2022.110917_bib14","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/0305-0491(75)90292-8","article-title":"Multiple end products of anaerobiosis in diving vertebrates","volume":"50","author":"Hochachka","year":"1975","journal-title":"Comp. Biochem. Physiol. B"},{"key":"10.1016\/j.celrep.2022.110917_bib15","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1016\/j.cmet.2019.06.002","article-title":"Metabolite exchange between mammalian organs quantified in pigs","volume":"30","author":"Jang","year":"2019","journal-title":"Cell Metabol."},{"key":"10.1016\/j.celrep.2022.110917_bib16","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1016\/0022-2828(79)90472-3","article-title":"Assessment of tissue and cell damage by succinate oxidation\u22171","volume":"11","author":"Jolly","year":"1979","journal-title":"J.\u00a0Mol. Cell. Cardiol."},{"key":"10.1016\/j.celrep.2022.110917_bib17","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1152\/physrev.00041.2017","article-title":"Defining physiological normoxia for improved translation of cell physiology to animal models and humans","volume":"99","author":"Keeley","year":"2019","journal-title":"Physiol. Rev."},{"key":"10.1016\/j.celrep.2022.110917_bib18","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.preteyeres.2017.01.003","article-title":"Retinal oxygen: from Animals to humans","volume":"58","author":"Linsenmeier","year":"2017","journal-title":"Prog. Retin. Eye Res."},{"key":"10.1016\/j.celrep.2022.110917_bib19","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1016\/0003-9861(89)90123-9","article-title":"Effect of esters of succinic acid and other citric acid cycle intermediates on insulin release and inositol phosphate formation by pancreatic islets","volume":"269","author":"MacDonald","year":"1989","journal-title":"Arch. Biochem. Biophys."},{"key":"10.1016\/j.celrep.2022.110917_bib20","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/0014-5793(75)80858-1","article-title":"On the oxidation of succinate by parenchymal cells isolated from rat liver","volume":"51","author":"Mapes","year":"1975","journal-title":"FEBS Lett."},{"key":"10.1016\/j.celrep.2022.110917_bib21","doi-asserted-by":"crossref","first-page":"1294","DOI":"10.1093\/bioinformatics\/bts127","article-title":"IsoCor: correcting MS data in isotope labeling experiments","volume":"28","author":"Millard","year":"2012","journal-title":"Bioinformatics"},{"key":"10.1016\/j.celrep.2022.110917_bib22","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1038\/s42255-021-00389-5","article-title":"UCP1 governs liver extracellular succinate and inflammatory pathogenesis","volume":"3","author":"Mills","year":"2021","journal-title":"Nature Metab."},{"key":"10.1016\/j.celrep.2022.110917_bib23","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1038\/s41586-018-0353-2","article-title":"Accumulation of succinate controls activation of adipose tissue thermogenesis","volume":"560","author":"Mills","year":"2018","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2022.110917_bib24","doi-asserted-by":"crossref","first-page":"2929","DOI":"10.1042\/BST20211032","article-title":"Controlled power: how biology manages succinate-driven energy release","volume":"49","author":"Mookerjee","year":"2021","journal-title":"Biochem. Soc. Trans."},{"key":"10.1016\/j.celrep.2022.110917_bib25","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1093\/toxsci\/kfv208","article-title":"Quantification of low-level drug effects using real-time, in\u00a0vitro measurement of oxygen consumption rate","volume":"148","author":"Neal","year":"2015","journal-title":"Toxicol. Sci."},{"key":"10.1016\/j.celrep.2022.110917_bib26","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1111\/j.1432-1033.1974.tb03899.x","article-title":"The influence of respiration and ATP hydrolysis on the proton-electrochemical gradient across the inner membrane of rat-liver mitochondria as determined by ion distribution","volume":"50","author":"Nicholls","year":"1974","journal-title":"Eur. J. Biochem."},{"key":"10.1016\/j.celrep.2022.110917_bib27","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1023\/A:1027376426860","article-title":"The non-ohmic proton leak - 25 Years on","volume":"17","author":"Nicholls","year":"1997","journal-title":"Biosci. Rep."},{"key":"10.1016\/j.celrep.2022.110917_bib28","doi-asserted-by":"crossref","first-page":"16274","DOI":"10.1016\/S0021-9258(18)41996-5","article-title":"The permeability transition in heart mitochondria is regulated synergistically by ADP and cyclosporin A","volume":"267","author":"Novgorodovsot","year":"1992","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2022.110917_bib29","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.cell.2020.08.039","article-title":"PH-gated succinate secretion regulates muscle remodeling in response to exercise","volume":"183","author":"Reddy","year":"2020","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2022.110917_bib30","doi-asserted-by":"crossref","first-page":"9869","DOI":"10.1074\/jbc.RA118.003647","article-title":"Control of mitochondrial superoxide production by reverse electron transport at complex I","volume":"293","author":"Robb","year":"2018","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2022.110917_bib31","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1126\/science.abi7495","article-title":"Fumarate is a terminal electron acceptor in the mammalian electron transport chain","volume":"374","author":"Spinelli","year":"2021","journal-title":"Science"},{"key":"10.1016\/j.celrep.2022.110917_bib32","doi-asserted-by":"crossref","first-page":"976","DOI":"10.1016\/j.bbrc.2003.12.182","article-title":"Systematic screening of potential \u03b2-cell imaging agents","volume":"314","author":"Sweet","year":"2004","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"10.1016\/j.celrep.2022.110917_bib33","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.freeradbiomed.2018.10.448","article-title":"Mitochondrial and cytosolic\u00a0sources of hydrogen peroxide in resting C2C12 myoblasts","volume":"130","author":"Wong","year":"2019","journal-title":"Free Radic. Biol. Med."},{"key":"10.1016\/j.celrep.2022.110917_bib34","doi-asserted-by":"crossref","first-page":"16804","DOI":"10.1074\/jbc.R117.789271","article-title":"Production of superoxide and hydrogen peroxide from specific mitochondrial sites under different bioenergetic conditions","volume":"292","author":"Wong","year":"2017","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2022.110917_bib35","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1006\/abio.2002.5698","article-title":"A convenient one-step extraction of cellular ATP using boiling water for the luciferin-luciferase assay of ATP","volume":"306","author":"Yang","year":"2002","journal-title":"Anal. Biochem."},{"key":"10.1016\/j.celrep.2022.110917_bib36","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1167\/iovs.05-1118","article-title":"Oxygen distribution in the mouse retina","volume":"47","author":"Yu","year":"2006","journal-title":"Investig. Ophthalmol. Vis. Sci."}],"container-title":["Cell Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2211124722006945?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2211124722006945?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,31]],"date-time":"2025-10-31T11:41:26Z","timestamp":1761910886000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2211124722006945"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6]]},"references-count":36,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2022,6]]}},"alternative-id":["S2211124722006945"],"URL":"https:\/\/doi.org\/10.1016\/j.celrep.2022.110917","relation":{},"ISSN":["2211-1247"],"issn-type":[{"value":"2211-1247","type":"print"}],"subject":[],"published":{"date-parts":[[2022,6]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Succinate metabolism in the retinal pigment epithelium uncouples respiration from ATP synthesis","name":"articletitle","label":"Article Title"},{"value":"Cell Reports","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.celrep.2022.110917","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2022 The Author(s).","name":"copyright","label":"Copyright"}],"article-number":"110917"}}