{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,16]],"date-time":"2026-03-16T13:14:23Z","timestamp":1773666863433,"version":"3.50.1"},"reference-count":61,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2022,6,28]],"date-time":"2022-06-28T00:00:00Z","timestamp":1656374400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002261","name":"Russian Foundation","doi-asserted-by":"publisher","award":["20-015-00029"],"award-info":[{"award-number":["20-015-00029"]}],"id":[{"id":"10.13039\/501100002261","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002261","name":"Russian Foundation","doi-asserted-by":"publisher","award":["075-01027-22-00"],"award-info":[{"award-number":["075-01027-22-00"]}],"id":[{"id":"10.13039\/501100002261","id-type":"DOI","asserted-by":"publisher"}]},{"name":"the Government of the RF","award":["20-015-00029"],"award-info":[{"award-number":["20-015-00029"]}]},{"name":"the Government of the RF","award":["075-01027-22-00"],"award-info":[{"award-number":["075-01027-22-00"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Membranes"],"abstract":"<jats:p>Mitochondria are capable of synchronized oscillations in many variables, but the underlying mechanisms are still unclear. In this study, we demonstrated that rat liver mitochondria, when exposed to a pulse of Sr2+ ions in the presence of valinomycin (a potassium ionophore) and cyclosporin A (a specific inhibitor of the permeability transition pore complex) under hypotonia, showed prolonged oscillations in K+ and Sr2+ fluxes, membrane potential, pH, matrix volume, rates of oxygen consumption and H2O2 formation. The dynamic changes in the rate of H2O2 production were in a reciprocal relationship with the respiration rate and in a direct relationship with the mitochondrial membrane potential and other indicators studied. The pre-incubation of mitochondria with Ca2+(Sr2+)-dependent phospholipase A2 inhibitors considerably suppressed the accumulation of free fatty acids, including palmitic and stearic acids, and all spontaneous Sr2+-induced cyclic changes. These data suggest that the mechanism of ion efflux from mitochondria is related to the opening of short-living pores, which can be caused by the formation of complexes between Sr2+(Ca2+) and endogenous long-chain saturated fatty acids (mainly, palmitic acid) that accumulate due to the activation of phospholipase A2 by the ions. A possible role for transient palmitate\/Ca2+(Sr2+)-induced pores in the maintenance of ion homeostasis and the prevention of calcium overload in mitochondria under pathophysiological conditions is discussed.<\/jats:p>","DOI":"10.3390\/membranes12070667","type":"journal-article","created":{"date-parts":[[2022,6,29]],"date-time":"2022-06-29T01:48:38Z","timestamp":1656467318000},"page":"667","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["The Short-Term Opening of Cyclosporin A-Independent Palmitate\/Sr2+-Induced Pore Can Underlie Ion Efflux in the Oscillatory Mode of Functioning of Rat Liver Mitochondria"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5707-6557","authenticated-orcid":false,"given":"Natalia V.","family":"Belosludtseva","sequence":"first","affiliation":[{"name":"Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, Institutskaya 3, 142290 Pushchino, Russia"},{"name":"Department of Biochemistry, Cell Biology and Microbiology, Mari State University, pl. Lenina 1, 424001 Yoshkar-Ola, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lyubov L.","family":"Pavlik","sequence":"additional","affiliation":[{"name":"Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, Institutskaya 3, 142290 Pushchino, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5392-7035","authenticated-orcid":false,"given":"Konstantin N.","family":"Belosludtsev","sequence":"additional","affiliation":[{"name":"Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, Institutskaya 3, 142290 Pushchino, Russia"},{"name":"Department of Biochemistry, Cell Biology and Microbiology, Mari State University, pl. Lenina 1, 424001 Yoshkar-Ola, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nils-Erik L.","family":"Saris","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Antimicrobials, Probiotics and Fermented Food, University of Helsinki, 00014 Helsinki, Finland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria I.","family":"Shigaeva","sequence":"additional","affiliation":[{"name":"Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, Institutskaya 3, 142290 Pushchino, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Galina D.","family":"Mironova","sequence":"additional","affiliation":[{"name":"Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, Institutskaya 3, 142290 Pushchino, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,6,28]]},"reference":[{"key":"ref_1","first-page":"a038802","article-title":"Cytoplasmic and mitochondrial calcium signaling: A two-way relationship","volume":"12","author":"Wacquier","year":"2020","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_2","first-page":"187","article-title":"A historical review of cellular calcium handling, with emphasis on mitochondria","volume":"70","author":"Saris","year":"2005","journal-title":"Biochemistry"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1038\/nrm3412","article-title":"Mitochondria as sensors and regulators of calcium signalling","volume":"13","author":"Rizzuto","year":"2012","journal-title":"Nat. Rev. Mol. Cell. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1007\/978-0-387-09794-7_8","article-title":"Mitochondrial oscillations in physiology and pathophysiology","volume":"641","author":"Aon","year":"2008","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"19316","DOI":"10.1038\/srep19316","article-title":"Interplay between intracellular Ca2+ oscillations and Ca2+-stimulated mitochondrial metabolism","volume":"6","author":"Wacquier","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1016\/0014-5793(76)80581-9","article-title":"Continuous Sr2+-induced oscillations of the ionic fluxes in mitochondria","volume":"66","author":"Gylkhandanyan","year":"1976","journal-title":"FEBS Lett."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/0005-2728(80)90034-1","article-title":"The stoichiometry of ion fluxes during Sr2+-induced oscillations in mitochondria","volume":"589","author":"Evtodienko","year":"1980","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_8","first-page":"612","article-title":"Excitability of inner mitochondrial membrane. II. Reversible Sr2+-induced Sr2+ release from mitochondria","volume":"8","author":"Holmuhamedov","year":"1991","journal-title":"Biol. Membr."},{"key":"ref_9","first-page":"944","article-title":"Characteristics of reversible and irreversible Ca2+-induced Ca2+ release from mitochondria in permeabilized Ehrlich ascites carcinoma cells","volume":"60","author":"Teplova","year":"1995","journal-title":"Biokhimiia"},{"key":"ref_10","first-page":"39","article-title":"Strontium excitability of the inner mitochondrial membrane: Regenerative strontium-induced strontium release","volume":"36","author":"Holmuhamedov","year":"1995","journal-title":"Biochem. Mol. Biol. Int."},{"key":"ref_11","first-page":"447","article-title":"Characteristics of Sr2+-induced permeability increase in the inner mitochondrial membrane","volume":"8","author":"Sidash","year":"1995","journal-title":"Membr. Cell Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1016\/j.bbamem.2014.10.027","article-title":"Involvement of palmitate\/Ca2+(Sr2+)-induced pore in the cycling of ions across the mitochondrial membrane","volume":"1848","author":"Mironova","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_13","unstructured":"Chance, B., Ghosh, A., and Pye, E. (1973). Biological and Biochemical Oscillators, Academic Press. [1st ed.]."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1152\/physrev.00041.2020","article-title":"Mitochondrial calcium exchange in physiology and disease","volume":"102","author":"Garbincius","year":"2022","journal-title":"Physiol. Rev."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1007\/s10863-016-9676-6","article-title":"Mitochondrial Ca2+ uptake pathways","volume":"49","author":"Elustondo","year":"2017","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_16","first-page":"593","article-title":"Mitochondrial Ca2+ transport: Mechanisms, molecular structures, and role in cells","volume":"84","author":"Belosludtsev","year":"2019","journal-title":"Biochemistry"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"101604","DOI":"10.1016\/j.jbc.2022.101604","article-title":"MCU (mitochondrial Ca2+ uniporter) makes the calcium go round","volume":"298","author":"Grant","year":"2022","journal-title":"J. Biol. Chem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"5054","DOI":"10.1523\/JNEUROSCI.21-14-05054.2001","article-title":"Spontaneous changes in mitochondrial membrane potential in cultured neurons","volume":"21","author":"Buckman","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3358","DOI":"10.1016\/S0006-3495(03)74755-9","article-title":"Spontaneous changes in mitochondrial membrane potential in single isolated brain mitochondria","volume":"85","author":"Vergun","year":"2003","journal-title":"Biophys. J."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"44735","DOI":"10.1074\/jbc.M302673200","article-title":"Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes","volume":"278","author":"Aon","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1007\/s10863-007-9079-9","article-title":"Mitochondrial Ca2+cycle mediated by the palmitate-activated cyclosporin A-insensitive pore","volume":"39","author":"Mironova","year":"2007","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1023\/B:JOBB.0000023620.42653.b7","article-title":"Formation of palmitic acid\/Ca2+complexes in the mitochondrial membrane: A possible role in the cyclosporin-insensitive permeability transition","volume":"36","author":"Mironova","year":"2004","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/S0005-2736(02)00666-1","article-title":"A permeability transition in liposomes induced by the formation of Ca2+\/palmitic acid complexes","volume":"1609","author":"Agafonov","year":"2003","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/s00232-007-9005-4","article-title":"Ca2+-induced phase separation in the membrane of palmitate-containing liposomes and its possible relation to membrane permeabilization","volume":"215","author":"Agafonov","year":"2007","journal-title":"J. Membr. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1023\/A:1010659323937","article-title":"Palmitic and stearic acids bind Ca2+ with high affinity and form nonspecific channels in black-lipid membranes. Possible relation to Ca2+-activated mitochondrial pores","volume":"33","author":"Mironova","year":"2001","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_26","first-page":"815","article-title":"Possible mechanism for formation and regulation of the palmitate-induced cyclosporin A-insensitive mitochondrial pore","volume":"70","author":"Belosludtsev","year":"2005","journal-title":"Biochemistry"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1007\/s10863-009-9230-x","article-title":"Physiological aspects of the mitochondrial cyclosporin A-insensitive palmitate\/Ca2+-induced pore: Tissue specificity, age profile and dependence on the animal\u2019s adaptation to hypoxia","volume":"41","author":"Belosludtsev","year":"2009","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1006\/abbi.2000.2195","article-title":"Free fatty acid effects on mitochondrial permeability: An overview","volume":"386","author":"Sultan","year":"2001","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1006\/abbi.2000.2194","article-title":"Palmitic acid opens a novel cyclosporin A-insensitive pore in the inner mitochondrial membrane","volume":"386","author":"Sultan","year":"2001","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Mironova, G.D., and Pavlov, E.V. (2021). Mitochondrial cyclosporine A-independent palmitate\/Ca2+-induced permeability transition pore (PA-mPT Pore) and its role in mitochondrial function and protection against calcium overload and glutamate toxicity. Cells, 10.","DOI":"10.3390\/cells10010125"},{"key":"ref_31","first-page":"319","article-title":"Lipid pores and stability of cell membranes","volume":"65","author":"Antonov","year":"1996","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0021-9258(19)52451-6","article-title":"Protein measurement with the Folin phenol reagent","volume":"193","author":"Lowry","year":"1951","journal-title":"J. Biol. Chem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3333","DOI":"10.1248\/cpb.37.3333","article-title":"Calculation of membrane potential in synaptosomes with use of a lipophilic cation (tetraphenylphosphonium)","volume":"37","author":"Aiuchi","year":"1989","journal-title":"Chem. Pharm. Bull."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1016\/j.bbamem.2018.06.012","article-title":"Effect of bedaquiline on the functions of rat liver mitochondria","volume":"1861","author":"Belosludtsev","year":"2019","journal-title":"Biochim. Biophys. Acta Biomembr."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/S0022-2275(20)38861-1","article-title":"Direct transesterification of all classes of lipids in a one-step reaction","volume":"27","author":"Lepage","year":"1986","journal-title":"J. Lipid Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1080\/15216540152845948","article-title":"The mitochondrial potassium cycle","volume":"52","author":"Garlid","year":"2001","journal-title":"IUBMB Life"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1038\/nature02246","article-title":"The mitochondrial calcium uniporter is a highly selective ion channel","volume":"427","author":"Kirichok","year":"2004","journal-title":"Nature"},{"key":"ref_38","first-page":"293","article-title":"Changes in the phospholipid content of intact mitochondria under mitochondrial swelling in hypotonic sucrose solutions","volume":"44","author":"Kargapolov","year":"1979","journal-title":"Biokhimiia"},{"key":"ref_39","first-page":"5","article-title":"Stimulation of phospholipase A2 activity in mitochondria by magnesium and polyamines","volume":"7","author":"Saris","year":"1994","journal-title":"Magnes. Res."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Murakami, M., Sato, H., and Taketomi, Y. (2020). Updating phospholipase A2 biology. Biomolecules, 10.","DOI":"10.3390\/biom10101457"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Kravenska, Y., Checchetto, V., and Szabo, I. (2021). Routes for potassium ions across mitochondrial membranes: A biophysical point of view with special focus on the ATP-sensitive K+ channel. Biomolecules, 11.","DOI":"10.3390\/biom11081172"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/0304-4157(95)00003-A","article-title":"The mitochondrial permeability transition","volume":"1241","author":"Zoratti","year":"1995","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_43","first-page":"45","article-title":"Mitochondrial lipid pore in the mechanism of glutamate-induced calcium disturbance of neurons","volume":"6","author":"Mironova","year":"2012","journal-title":"Biochem. Suppl. Ser. A Membr. Cell Biol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"16615","DOI":"10.1074\/jbc.M601770200","article-title":"Identification of the expressed form of human cytosolic phospholipase A2\u03b2(cPLA2\u03b2). cPLA2\u03b23 is a novel variant localized to mitochondria and early endosomes","volume":"281","author":"Ghosh","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.plipres.2010.12.001","article-title":"Recent progress in phospholipase A2 research: From cells to animals to humans","volume":"50","author":"Murakami","year":"2011","journal-title":"Prog. Lipid Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"14880","DOI":"10.1074\/jbc.M111.336776","article-title":"Activation of mitochondrial calcium-independent phospholipase A2\u03b3 (iPLA2\u03b3) by divalent cations mediating arachidonate release and production of downstream eicosanoids","volume":"287","author":"Moon","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1016\/j.plipres.2013.07.002","article-title":"Lipids of mitochondria","volume":"52","author":"Horvath","year":"2013","journal-title":"Prog. Lipid Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/S0014-5793(00)01376-4","article-title":"Long-chain fatty acid-promoted swelling of mitochondria: Further evidence for the protonophoric effect of fatty acids in the inner mitochondrial membrane","volume":"471","author":"Schonfeld","year":"2000","journal-title":"FEBS Lett."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1134\/S2517751621060111","article-title":"Biomimetic membranes with aqueous nanochannels. Phase transitions and oscillations","volume":"3","author":"Kocherginsky","year":"2021","journal-title":"Membr. Membr. Technol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1134\/S251775162106010X","article-title":"Biomimetic membranes without proteins but with aqueous nanochannels and facilitated transport","volume":"3","author":"Kocherginsky","year":"2021","journal-title":"Membr. Membr. Technol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/s00232-010-9302-1","article-title":"Palmitic acid induces the opening of a Ca2+-dependent pore in the plasma membrane of red blood cells: The possible role of the pore in erythrocyte lysis","volume":"237","author":"Belosludtsev","year":"2010","journal-title":"J. Membr. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1186\/s12958-020-00643-7","article-title":"Regulation of [Ca2+]i oscillations and mitochondrial activity by various calcium transporters in mouse oocytes","volume":"18","author":"Wang","year":"2020","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2060","DOI":"10.1529\/biophysj.104.041749","article-title":"A mitochondrial oscillator dependent on reactive oxygen species","volume":"87","author":"Cortassa","year":"2004","journal-title":"Biophys. J."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1038\/s41580-018-0052-8","article-title":"The machineries, regulation and cellular functions of mitochondrial calcium","volume":"19","author":"Giorgi","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.tips.2018.11.004","article-title":"Mitochondrial permeability transition: A molecular lesion with multiple drug targets","volume":"40","author":"Briston","year":"2019","journal-title":"Trends Pharmacol. Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2489","DOI":"10.1111\/brv.12764","article-title":"The mitochondrial permeability transition pore: An evolving concept critical for cell life and death","volume":"96","author":"Morciano","year":"2021","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0014-5793(97)01159-9","article-title":"High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria","volume":"416","author":"Korshunov","year":"1997","journal-title":"FEBS Lett."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"4","DOI":"10.32607\/actanaturae.11610","article-title":"Fifty years of research on protonophores: Mitochondrial uncoupling as a basis for therapeutic action","volume":"14","author":"Kotova","year":"2022","journal-title":"Acta Nat."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Demine, S., Renard, P., and Arnould, T. (2019). Mitochondrial uncoupling: A key controller of biological processes in physiology and diseases. Cells, 8.","DOI":"10.3390\/cells8080795"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/0005-2736(82)90371-6","article-title":"Involvement of periodic deacylation-acylation cycles of mitochondrial phospholipids during Sr2+-induced oscillatory ion transport in rat liver mitochondria","volume":"688","author":"Wiswedel","year":"1982","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1038\/s41467-017-02638-2","article-title":"Sequential forward and reverse transport of the Na+\/Ca2+ exchanger generates Ca2+ oscillations within mitochondria","volume":"9","author":"Samanta","year":"2018","journal-title":"Nat. Commun."}],"container-title":["Membranes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0375\/12\/7\/667\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:39:43Z","timestamp":1760139583000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0375\/12\/7\/667"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,28]]},"references-count":61,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["membranes12070667"],"URL":"https:\/\/doi.org\/10.3390\/membranes12070667","relation":{},"ISSN":["2077-0375"],"issn-type":[{"value":"2077-0375","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,28]]}}}