{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T05:29:14Z","timestamp":1792042154041,"version":"4.4.0"},"reference-count":48,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,3,14]],"date-time":"2026-03-14T00:00:00Z","timestamp":1773446400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,3,14]],"date-time":"2026-03-14T00:00:00Z","timestamp":1773446400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/100000968","name":"American Heart Association","doi-asserted-by":"publisher","award":["https:\/\/doi.org\/10.58275\/AHA.25POST1378853.pc.gr.227467"],"award-info":[{"award-number":["https:\/\/doi.org\/10.58275\/AHA.25POST1378853.pc.gr.227467"]}],"id":[{"id":"10.13039\/100000968","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000050","name":"National Heart, Lung, and Blood Institute","doi-asserted-by":"publisher","award":["HL168874"],"award-info":[{"award-number":["HL168874"]}],"id":[{"id":"10.13039\/100000050","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["physoc.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["The Journal of Physiology"],"abstract":"\n Abstract<\/jats:title>\n \n The energetic demands on ventricular myocytes imposed by the transport of ions and cross\u2010bridge cycling are well known, yet the spatiotemporal dynamics of ATP supply and demand remain poorly understood. Here, using confocal microscopy and genetically encoded fluorescent sensors targeted to mitochondria and cytosol, we visualized beat\u2010to\u2010beat ATP dynamics in ventricular myocytes from male and female mice. These probes showed fluctuations in mitochondrial ATP levels with each contraction, revealing two distinct, spatially localized waveforms \u2013 ATP \u2018gain\u2019 and ATP \u2018dip\u2019 \u2013 representing transient increases or decreases in matrix ATP levels, respectively. These waveforms were tightly phase\u2010locked to intracellular Ca\n 2+<\/jats:sup>\n transients and organized into energetic microdomains. Inhibition of the mitochondrial Ca\n 2+<\/jats:sup>\n uniporter or the adenine nucleotide translocase attenuated these ATP transients. Although female myocytes exhibited larger mitochondrial ATP transients than their male counterparts, their mitochondrial volume was lower. Female myocytes also exhibited tighter coupling between the sarcoplasmic reticulum and mitochondria and showed a higher density of mitofusin 2 and ATP synthase catalytic \u03b1\u2010subunit per unit volume, suggesting more efficient ATP production. Cytosolic ATP transients mirrored mitochondrial waveforms and domain structure in both male and female myocytes. During faster pacing, diastolic cytosolic ATP rose more rapidly in female myocytes, whereas beat\u2010locked ATP transients increased in both sexes but proportionally more in males than in females. These findings demonstrate that ATP is synthesized on a beat\u2010to\u2010beat basis in a modular, microdomain\u2010specific manner. We propose that male myocytes rely on greater mitochondrial mass for energetic scaling, whereas female cells employ architectural precision to optimize ATP delivery.\n \n \n image<\/jats:alt-text>\n <\/jats:graphic>\n <\/jats:boxed-text>\n <\/jats:p>\n <\/jats:sec>\n \n Key points<\/jats:title>\n \n \n \n It is known that each heartbeat requires precise ATP delivery to fuel ion transport and cross\u2010bridge cycling, but the timing and spatial organization of ATP production in heart cells has been unclear.<\/jats:p>\n <\/jats:list-item>\n \n Using advanced imaging and genetically encoded sensors, we visualized beat\u2010to\u2010beat ATP fluctuations in the mitochondria and cytosol of individual male and female mouse ventricular myocytes.<\/jats:p>\n <\/jats:list-item>\n \n \n Mitochondrial ATP levels rose or fell with each beat in spatially confined regions, forming ATP \u2018gain\u2019 or \u2018dip\u2019 microdomains that were synchronized with Ca\n 2+<\/jats:sup>\n transients.\n <\/jats:p>\n <\/jats:list-item>\n \n At higher firing rates, beat\u2010locked, diastolic ATP transients rose more quickly in female myocytes, but were larger in male myocytes, highlighting distinct sex\u2010specific strategies for matching energy supply to contractile demand.<\/jats:p>\n <\/jats:list-item>\n \n Ventricular myocytes \u2018live paycheck\u2010to\u2010paycheck\u2019, producing just enough ATP on demand to fuel each beat. Male and female myocytes adopt distinct strategies to meet this demand: male myocytes scale output through greater mitochondrial mass, while female myocytes achieve energetic precision via enhanced sarcoplasmic reticulum\u2013mitochondrial coupling.<\/jats:p>\n <\/jats:list-item>\n <\/jats:list>\n <\/jats:p>\n <\/jats:sec>","DOI":"10.1113\/jp289683","type":"journal-article","created":{"date-parts":[[2026,3,14]],"date-time":"2026-03-14T14:15:43Z","timestamp":1773497743000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Demonstration of beat\u2010to\u2010beat, on\u2010demand ATP synthesis in ventricular myocytes reveals sex\u2010specific mitochondrial and cytosolic dynamics"],"prefix":"10.1113","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6065-2903","authenticated-orcid":false,"given":"Paula","family":"Rhana","sequence":"first","affiliation":[{"name":"Department of Physiology and Membrane Biology, School of Medicine University of California Davis USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5370-1156","authenticated-orcid":false,"given":"Collin","family":"Matsumoto","sequence":"additional","affiliation":[{"name":"Department of Physiology and Membrane Biology, School of Medicine University of California Davis USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4297-8029","authenticated-orcid":false,"given":"L. Fernando","family":"Santana","sequence":"additional","affiliation":[{"name":"Department of Physiology and Membrane Biology, School of Medicine University of California Davis USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,3,14]]},"reference":[{"issue":"2","key":"e_1_2_6_2_1","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.yjmcc.2004.04.023","article-title":"Gender modulation of Ca2+ uptake in cardiac mitochondria","volume":"37","author":"Arieli Y.","year":"2004","journal-title":"Journal of Molecular and Cellular Cardiology"},{"issue":"3","key":"e_1_2_6_3_1","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1113\/jphysiol.1994.sp020036","article-title":"Processes that remove calcium from the cytoplasm during excitation\u2010contraction coupling in intact rat heart cells","volume":"474","author":"Balke C. 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