{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T19:29:46Z","timestamp":1790105386256,"version":"4.0.1"},"reference-count":210,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,9,23]],"date-time":"2024-09-23T00:00:00Z","timestamp":1727049600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell Dev. Biol."],"abstract":"<jats:p>It has long been thought that exocytosis was driven exclusively by well-studied fusion proteins. Some decades ago, the role of lipids became evident and escalated interest in the field. Our laboratory chose a particular cell to face this issue: the human sperm. What makes this cell special? Sperm, as terminal cells, are characterized by their scarcity of organelles and the complete absence of transcriptional and translational activities. They are specialized for a singular membrane fusion occurrence: the exocytosis of the acrosome. This unique trait makes them invaluable for the study of exocytosis in isolation. We will discuss the lipids\u2019 role in human sperm acrosome exocytosis from various perspectives, with a primary emphasis on our contributions to the field. Sperm cells have a unique lipid composition, very rare and not observed in many cell types, comprising a high content of plasmalogens, long-chain, and very-long-chain polyunsaturated fatty acids that are particular constituents of some sphingolipids. This review endeavors to unravel the impact of membrane lipid composition on the proper functioning of the exocytic pathway in human sperm and how this lipid dynamic influences its fertilizing capability. Evidence from our and other laboratories allowed unveiling the role and importance of multiple lipids that drive exocytosis. This review highlights the role of cholesterol, diacylglycerol, and particular phospholipids like phosphatidic acid, phosphatidylinositol 4,5-bisphosphate, and sphingolipids in driving sperm acrosome exocytosis. Furthermore, we provide a comprehensive overview of the factors and enzymes that regulate lipid turnover during the exocytic course. A more thorough grasp of the role played by lipids transferred from sperm can provide insights into certain causes of male infertility. It may lead to enhancements in diagnosing infertility and techniques like assisted reproductive technology (ART).<\/jats:p>","DOI":"10.3389\/fcell.2024.1457638","type":"journal-article","created":{"date-parts":[[2024,9,23]],"date-time":"2024-09-23T04:41:33Z","timestamp":1727066493000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":18,"title":["Lipid remodeling in acrosome exocytosis: unraveling key players in the human sperm"],"prefix":"10.3389","volume":"12","author":[{"given":"Laila","family":"Suhaiman","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvia A.","family":"Belmonte","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,9,23]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"109935","DOI":"10.1016\/j.celrep.2021.109935","article-title":"PMP2\/FABP8 induces PI(4,5)P(2)-dependent transbilayer reorganization of sphingomyelin in the plasma membrane","volume":"37","author":"Abe","year":"2021","journal-title":"Cell Rep."},{"key":"B2","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.1074\/jbc.272.2.1069","article-title":"Cell-permeable ceramides prevent the activation of phospholipase D by ADP-ribosylation factor and RhoA","volume":"272","author":"Abousalham","year":"1997","journal-title":"J. Biol. Chem."},{"key":"B3","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1186\/s12958-015-0032-1","article-title":"A unique view on male infertility around the globe","volume":"13","author":"Agarwal","year":"2015","journal-title":"Reprod. Biol. Endocrinol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1016\/j.chemphyslip.2018.12.008","article-title":"Mechanical properties of bilayers containing sperm sphingomyelins and ceramides with very long-chain polyunsaturated fatty acids","volume":"218","author":"Ahumada-Gutierrez","year":"2019","journal-title":"Chem. Phys. Lipids"},{"key":"B5","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1007\/978-3-7091-1368-4_3","article-title":"Sphingolipid metabolism and neutral sphingomyelinases","volume":"215","author":"Airola","year":"2013","journal-title":"Handb. Exp. Pharmacol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1093\/molehr\/gal119","article-title":"Analysis of lipid peroxidation in human spermatozoa using BODIPY C11","volume":"13","author":"Aitken","year":"2007","journal-title":"Mol. Hum. Reprod."},{"key":"B7","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1007\/978-94-007-0265-3_22","article-title":"Gating mechanisms of canonical transient receptor potential channel proteins: role of phosphoinositols and diacylglycerol","volume":"704","author":"Albert","year":"2011","journal-title":"Adv. Exp. Med. Biol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"125","DOI":"10.3389\/fendo.2013.00125","article-title":"Lipids in regulated exocytosis: what are they doing?","volume":"4","author":"Ammar","year":"2013","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"B9","doi-asserted-by":"publisher","first-page":"E1213","DOI":"10.1152\/ajpendo.00480.2012","article-title":"Ceramide 1-phosphate induces macrophage chemoattractant protein-1 release: involvement in ceramide 1-phosphate-stimulated cell migration","volume":"304","author":"Arana","year":"2013","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"B10","doi-asserted-by":"publisher","first-page":"e27362","DOI":"10.4161\/cib.27362","article-title":"Membrane rafts regulate phospholipase B activation in murine sperm","volume":"6","author":"Asano","year":"","journal-title":"Commun. Integr. Biol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"28104","DOI":"10.1074\/jbc.M113.450981","article-title":"Phospholipase B is activated in response to sterol removal and stimulates acrosome exocytosis in murine sperm","volume":"288","author":"Asano","year":"","journal-title":"J. Biol. Chem."},{"key":"B12","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1002\/jcp.21623","article-title":"Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts","volume":"218","author":"Asano","year":"2009","journal-title":"J. Cell Physiol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1038\/nm0203-149","article-title":"Thermotaxis of mammalian sperm cells: a potential navigation mechanism in the female genital tract","volume":"9","author":"Bahat","year":"2003","journal-title":"Nat. Med."},{"key":"B14","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1055\/s-0034-1375179","article-title":"Laboratory procedures for human in vitro fertilization","volume":"32","author":"Balaban","year":"2014","journal-title":"Semin. Reprod. Med."},{"key":"B15","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/j.jbior.2017.09.009","article-title":"Phosphatidic acid-producing enzymes regulating the synaptic vesicle cycle: role for PLD?","volume":"67","author":"Barber","year":"2018","journal-title":"Adv. Biol. Regul."},{"key":"B16","doi-asserted-by":"publisher","first-page":"S91","DOI":"10.1194\/jlr.R800080-JLR200","article-title":"Bioactive sphingolipids: metabolism and function","volume":"50","author":"Bartke","year":"2009","journal-title":"J. Lipid Res."},{"key":"B17","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/j.ydbio.2013.11.006","article-title":"Activation of Src and release of intracellular calcium by phosphatidic acid during Xenopus laevis fertilization","volume":"386","author":"Bates","year":"2014","journal-title":"Dev. Biol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"478","DOI":"10.1016\/j.yexcr.2012.01.002","article-title":"RIM, Munc13, and Rab3A interplay in acrosomal exocytosis","volume":"318","author":"Bello","year":"2012","journal-title":"Exp. Cell Res."},{"key":"B19","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1016\/j.ydbio.2005.07.001","article-title":"Cholesterol content regulates acrosomal exocytosis by enhancing Rab3A plasma membrane association","volume":"285","author":"Belmonte","year":"2005","journal-title":"Dev. Biol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1007\/978-3-319-30567-7_4","article-title":"The molecules of sperm exocytosis","volume":"220","author":"Belmonte","year":"2016","journal-title":"Adv. Anat. Embryol. Cell Biol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1007\/978-1-61779-800-9_9","article-title":"Optimized protocols to analyze sphingosine-1-phosphate signal transduction pathways during acrosomal exocytosis in human sperm","volume":"874","author":"Belmonte","year":"2012","journal-title":"Methods Mol. Biol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"1271","DOI":"10.1093\/biolre\/ioab035","article-title":"HDL mediates reverse cholesterol transport from ram spermatozoa and induces hyperactivated motility","volume":"104","author":"Bernecic","year":"2021","journal-title":"Biol. Reprod."},{"key":"B23","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1530\/REP-19-0430","article-title":"Synergism between albumin, bicarbonate and cAMP upregulation for cholesterol efflux from ram sperm","volume":"160","author":"Bernecic","year":"2020","journal-title":"Reproduction"},{"key":"B24","doi-asserted-by":"publisher","first-page":"dev176966","DOI":"10.1242\/dev.176966","article-title":"The molecular mechanisms mediating mammalian fertilization","volume":"146","author":"Bhakta","year":"2019","journal-title":"Development"},{"key":"B25","doi-asserted-by":"publisher","first-page":"1188","DOI":"10.1016\/j.theriogenology.2008.06.021","article-title":"Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: functional relationship with zona binding and the zona-induced acrosome reaction","volume":"70","author":"Boerke","year":"2008","journal-title":"Theriogenology"},{"key":"B26","doi-asserted-by":"publisher","first-page":"100783","DOI":"10.1016\/j.jbior.2020.100783","article-title":"Structure and regulation of human phospholipase D","volume":"79","author":"Bowling","year":"2021","journal-title":"Adv. Biol. Regul."},{"key":"B27","doi-asserted-by":"publisher","first-page":"192208","DOI":"10.1098\/rsos.192208","article-title":"Divalent cations bind to phosphoinositides to induce ion and isomer specific propensities for nano-cluster initiation in bilayer membranes","volume":"7","author":"Bradley","year":"2020","journal-title":"R. Soc. Open Sci."},{"key":"B28","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.bbrc.2004.04.006","article-title":"Spatio-temporal organization of Vam6P and SNAP on mouse spermatozoa and their involvement in sperm-zona pellucida interactions","volume":"318","author":"Brahmaraju","year":"2004","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B29","doi-asserted-by":"publisher","first-page":"24825","DOI":"10.1074\/jbc.M109.015362","article-title":"Epac activates the small G proteins Rap1 and Rab3A to achieve exocytosis","volume":"284","author":"Branham","year":"2009","journal-title":"J. Biol. Chem."},{"key":"B30","doi-asserted-by":"publisher","first-page":"8656","DOI":"10.1074\/jbc.M508854200","article-title":"Calcium-induced acrosomal exocytosis requires cAMP acting through a protein kinase A-independent, Epac-mediated pathway","volume":"281","author":"Branham","year":"2006","journal-title":"J. Biol. Chem."},{"key":"B31","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1016\/0092-8674(92)90189-j","article-title":"Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface","volume":"68","author":"Brown","year":"1992","journal-title":"Cell"},{"key":"B208","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1387\/ijdb.072532mb","article-title":"The role of the acrosomal matrix in fertilization","volume":"52","author":"Buffone","year":"2008","journal-title":"Int. J. Dev. Biol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1095\/biolreprod.114.117911","article-title":"Unresolved questions concerning mammalian sperm acrosomal exocytosis","volume":"90","author":"Buffone","year":"2014","journal-title":"Biol. Reprod."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1411","DOI":"10.3390\/cells12101411","article-title":"A plethora of functions condensed into tiny phospholipids: the story of PI4P and PI(4,5)P(2)","volume":"12","author":"Bura","year":"2023","journal-title":"Cells"},{"key":"B34","doi-asserted-by":"publisher","first-page":"E2057","DOI":"10.1073\/pnas.1121173109","article-title":"Rab27 and Rab3 sequentially regulate human sperm dense-core granule exocytosis","volume":"109","author":"Bustos","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B209","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1093\/jn\/137.3.545","article-title":"Lipid rafts--composition, characterization, and controversies","volume":"137","author":"Calder","year":"2007","journal-title":"J. Nutr."},{"key":"B35","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1016\/0002-9378(84)90466-6","article-title":"Human uterine fluid, examined in undiluted samples for osmolarity and the concentrations of inorganic ions, albumin, glucose, and urea","volume":"150","author":"Casslen","year":"1984","journal-title":"Am. J. Obstet. Gynecol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"5619","DOI":"10.1073\/pnas.091502398","article-title":"SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis","volume":"98","author":"Chamberlain","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B37","doi-asserted-by":"publisher","first-page":"1335","DOI":"10.1007\/s10571-010-9577-x","article-title":"Lipid dynamics in exocytosis","volume":"30","author":"Chasserot-Golaz","year":"2010","journal-title":"Cell Mol. Neurobiol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1186\/s12958-021-00792-3","article-title":"High-coverage targeted lipidomics revealed dramatic lipid compositional changes in asthenozoospermic spermatozoa and inverse correlation of ganglioside GM3 with sperm motility","volume":"19","author":"Chen","year":"2021","journal-title":"Reprod. Biol. Endocrinol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"1273878","DOI":"10.3389\/fendo.2023.1273878","article-title":"Lipidomics profiles of human spermatozoa: insights into capacitation and acrosome reaction using UPLC-MS-based approach","volume":"14","author":"Cheng","year":"2023","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"B40","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1016\/j.cell.2005.10.015","article-title":"Membrane hemifusion: crossing a chasm in two leaps","volume":"123","author":"Chernomordik","year":"2005","journal-title":"Cell"},{"key":"B41","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1038\/nsmb.1455","article-title":"Mechanics of membrane fusion","volume":"15","author":"Chernomordik","year":"2008","journal-title":"Nat. Struct. Mol. Biol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1016\/j.ydbio.2003.10.034","article-title":"Crosstalk between protein kinase A and C regulates phospholipase D and F-actin formation during sperm capacitation","volume":"267","author":"Cohen","year":"2004","journal-title":"Dev. Biol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1016\/j.devcel.2014.01.005","article-title":"Lipid modulation of calcium flux through CaV2.3 regulates acrosome exocytosis and fertilization","volume":"28","author":"Cohen","year":"2014","journal-title":"Dev. Cell"},{"key":"B44","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1007\/978-3-319-30567-7_6","article-title":"Lipid regulation of acrosome exocytosis","volume":"220","author":"Cohen","year":"2016","journal-title":"Adv. Anat. Embryol. Cell Biol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"2246","DOI":"10.1016\/j.bbamem.2007.06.011","article-title":"Membrane fluidity changes in goat sperm induced by cholesterol depletion using beta-cyclodextrin","volume":"1768","author":"Companyo","year":"2007","journal-title":"Biochim. Biophys. Acta"},{"key":"B46","doi-asserted-by":"publisher","first-page":"3814","DOI":"10.1073\/pnas.1117599109","article-title":"cAMP regulates DEP domain-mediated binding of the guanine nucleotide exchange factor Epac1 to phosphatidic acid at the plasma membrane","volume":"109","author":"Consonni","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B47","doi-asserted-by":"publisher","first-page":"1379","DOI":"10.1007\/s10815-019-01464-3","article-title":"Decreased very long chain polyunsaturated fatty acids in sperm correlates with sperm quantity and quality","volume":"36","author":"Craig","year":"2019","journal-title":"J. Assist. Reprod. Genet."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1129","DOI":"10.1095\/biolreprod63.4.1129","article-title":"Sphingomyelin modulates capacitation of human sperm in vitro","volume":"63","author":"Cross","year":"2000","journal-title":"Biol. Reprod."},{"key":"B49","doi-asserted-by":"publisher","first-page":"R27","DOI":"10.1530\/REP-13-0420","article-title":"New insights into epididymal function in relation to sperm maturation","volume":"147","author":"Dacheux","year":"2014","journal-title":"Reproduction"},{"key":"B50","doi-asserted-by":"publisher","first-page":"2406","DOI":"10.1016\/S0006-3495(03)74664-5","article-title":"Sphingomyelin\/phosphatidylcholine\/cholesterol phase diagram: boundaries and composition of lipid rafts","volume":"85","author":"de Almeida","year":"2003","journal-title":"Biophys. J."},{"key":"B51","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.plipres.2012.08.003","article-title":"Signal transduction pathways involving phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate: convergences and divergences among eukaryotic kingdoms","volume":"52","author":"Delage","year":"2013","journal-title":"Prog. Lipid Res."},{"key":"B52","doi-asserted-by":"publisher","first-page":"9254","DOI":"10.3390\/ijms24119254","article-title":"Membrane cholesterol inhibits progesterone-mediated sperm function through the possible involvement of ABHD2","volume":"24","author":"De Toni","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"B53","doi-asserted-by":"publisher","first-page":"3126","DOI":"10.3390\/ijms22063126","article-title":"Sperm cholesterol content modifies sperm function and TRPV1-mediated sperm migration","volume":"22","author":"De Toni","year":"2021","journal-title":"Int. J. Mol. Sci."},{"key":"B54","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1111\/j.1439-0272.1996.tb02753.x","article-title":"Acrosome content release in streptolysin O permeabilized mouse spermatozoa","volume":"28","author":"Diaz","year":"1996","journal-title":"Andrologia"},{"key":"B55","doi-asserted-by":"publisher","first-page":"297","DOI":"10.3390\/ijms25010297","article-title":"Lipidomic profile of human sperm membrane identifies a clustering of lipids associated with semen quality and function","volume":"25","author":"Di Nisio","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"1321","DOI":"10.1038\/s41589-020-00688-0","article-title":"Structural and functional consequences of reversible lipid asymmetry in living membranes","volume":"16","author":"Doktorova","year":"2020","journal-title":"Nat. Chem. Biol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1016\/j.aju.2017.12.004","article-title":"Lifestyle causes of male infertility","volume":"16","author":"Durairajanayagam","year":"2018","journal-title":"Arab. J. Urol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1002\/mrd.1080250213","article-title":"Bovine oviductal fluid components and their potential role in sperm cholesterol efflux","volume":"25","author":"Ehrenwald","year":"1990","journal-title":"Mol. Reprod. Dev."},{"key":"B59","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1111\/j.1439-0272.2007.00764.x","article-title":"Seminal plasma albumin: origin and relation to the male reproductive parameters","volume":"39","author":"Elzanaty","year":"2007","journal-title":"Andrologia"},{"key":"B60","doi-asserted-by":"publisher","first-page":"s57","DOI":"10.1038\/ncb-nm-fertilityS57","article-title":"The state of the union: the cell biology of fertilization","volume":"4","author":"Evans","year":"2002","journal-title":"Nat. Cell Biol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"3543","DOI":"10.1242\/jcs.114.19.3543","article-title":"Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane","volume":"114","author":"Flesch","year":"2001","journal-title":"J. Cell Sci."},{"key":"B62","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1016\/s0304-4157(00)00018-6","article-title":"Dynamics of the mammalian sperm plasma membrane in the process of fertilization","volume":"1469","author":"Flesch","year":"2000","journal-title":"Biochim. Biophys. Acta"},{"key":"B63","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1387\/ijdb.082696hf","article-title":"Regulating the acrosome reaction","volume":"52","author":"Florman","year":"2008","journal-title":"Int. J. Dev. Biol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1046\/j.1365-2605.2001.00309.x","article-title":"Membrane fluidity and lipid content of human spermatozoa selected by swim-up method","volume":"24","author":"Force","year":"2001","journal-title":"Int. J. Androl."},{"key":"B65","doi-asserted-by":"publisher","first-page":"1087","DOI":"10.1083\/jcb.200409068","article-title":"Interdependent assembly of specific regulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles","volume":"167","author":"Fratti","year":"2004","journal-title":"J. Cell Biol."},{"key":"B66","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.tips.2015.01.001","article-title":"The phospholipase D superfamily as therapeutic targets","volume":"36","author":"Frohman","year":"2015","journal-title":"Trends Pharmacol. Sci."},{"key":"B67","doi-asserted-by":"publisher","first-page":"18151","DOI":"10.1074\/jbc.M700709200","article-title":"Very long-chain polyunsaturated fatty acids are the major acyl groups of sphingomyelins and ceramides in the head of mammalian spermatozoa","volume":"282","author":"Furland","year":"","journal-title":"J. Biol. Chem."},{"key":"B68","doi-asserted-by":"publisher","first-page":"18141","DOI":"10.1074\/jbc.M700708200","article-title":"Ceramides and sphingomyelins with high proportions of very long-chain polyunsaturated fatty acids in mammalian germ cells","volume":"282","author":"Furland","year":"","journal-title":"J. Biol. Chem."},{"key":"B69","doi-asserted-by":"publisher","first-page":"935","DOI":"10.1242\/jcs.108.3.935","article-title":"Glycolipid migration from the apical to the equatorial subdomains of the sperm head plasma membrane precedes the acrosome reaction. Evidence for a primary capacitation event in boar spermatozoa","volume":"108","author":"Gadella","year":"1995","journal-title":"J. Cell Sci."},{"key":"B70","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1387\/ijdb.082583bg","article-title":"Sperm head membrane reorganisation during capacitation","volume":"52","author":"Gadella","year":"2008","journal-title":"Int. J. Dev. Biol."},{"key":"B71","doi-asserted-by":"publisher","first-page":"6805","DOI":"10.1007\/s12035-024-03991-2","article-title":"\u03b22-Adrenergic regulation of the neuromuscular transmission and its lipid-dependent switch","volume":"61","author":"Gafurova","year":"2024","journal-title":"Mol. Neurobiol."},{"key":"B72","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1016\/j.theriogenology.2004.11.021","article-title":"SNARE proteins and caveolin-1 in stallion spermatozoa: possible implications for fertility","volume":"64","author":"Gamboa","year":"2005","journal-title":"Theriogenology"},{"key":"B73","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1111\/andr.12468","article-title":"Impaired sperm function in infertile men relies on the membrane sterol pattern","volume":"6","author":"Garolla","year":"2018","journal-title":"Andrology"},{"key":"B74","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/978-1-4419-6741-1_1","article-title":"An overview of sphingolipid metabolism: from synthesis to breakdown","volume":"688","author":"Gault","year":"2010","journal-title":"Adv. Exp. Med. Biol."},{"key":"B75","doi-asserted-by":"publisher","first-page":"106884","DOI":"10.1016\/j.anireprosci.2021.106884","article-title":"\u201cFine feathers make fine birds\u201d - the mammalian sperm plasma membrane lipid composition and effects on assisted reproduction","volume":"246","author":"Gautier","year":"2022","journal-title":"Anim. Reprod. Sci."},{"key":"B76","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.plipres.2015.09.002","article-title":"Control of inflammatory responses by ceramide, sphingosine 1-phosphate and ceramide 1-phosphate","volume":"61","author":"Gomez-Munoz","year":"2016","journal-title":"Prog. Lipid Res."},{"key":"B77","doi-asserted-by":"publisher","first-page":"104918","DOI":"10.1016\/j.jbc.2023.104918","article-title":"Arachidonic acid reverses cholesterol and zinc inhibition of human voltage-gated proton channels","volume":"299","author":"Han","year":"2023","journal-title":"J. Biol. Chem."},{"key":"B78","doi-asserted-by":"publisher","first-page":"e2205420119","DOI":"10.1073\/pnas.2205420119","article-title":"Cholesterol inhibits human voltage-gated proton channel hHv1","volume":"119","author":"Han","year":"2022","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B79","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1038\/nrm2329","article-title":"Principles of bioactive lipid signalling: lessons from sphingolipids","volume":"9","author":"Hannun","year":"2008","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"B80","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1016\/j.theriogenology.2004.09.016","article-title":"Bicarbonate-induced membrane processing in sperm capacitation","volume":"63","author":"Harrison","year":"2005","journal-title":"Theriogenology"},{"key":"B81","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1038\/aja.2010.76","article-title":"Leukocytes and oxidative stress: dilemma for sperm function and male fertility","volume":"13","author":"Henkel","year":"2011","journal-title":"Asian J. Androl."},{"key":"B82","doi-asserted-by":"publisher","first-page":"844","DOI":"10.1016\/j.bbalip.2014.09.010","article-title":"Phosphoinositides regulate ion channels","volume":"1851","author":"Hille","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"B83","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1038\/nsmb.2570","article-title":"Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment","volume":"20","author":"Honigmann","year":"2013","journal-title":"Nat. Struct. Mol. Biol."},{"key":"B84","doi-asserted-by":"publisher","first-page":"117530","DOI":"10.1016\/j.cca.2023.117530","article-title":"Comprehensive metabolomics profiling of seminal plasma in asthenozoospermia caused by different etiologies","volume":"548","author":"Hou","year":"2023","journal-title":"Clin. Chim. Acta"},{"key":"B85","doi-asserted-by":"publisher","first-page":"e79433","DOI":"10.7554\/eLife.79433","article-title":"Phorbolester-activated Munc13-1 and ubMunc13-2 exert opposing effects on dense-core vesicle secretion","volume":"11","author":"Houy","year":"2022","journal-title":"Elife"},{"key":"B86","doi-asserted-by":"publisher","first-page":"15300","DOI":"10.1073\/pnas.261358698","article-title":"A role for phospholipase D1 in neurotransmitter release","volume":"98","author":"Humeau","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B87","doi-asserted-by":"publisher","first-page":"378","DOI":"10.1095\/biolreprod62.2.378","article-title":"Cholesterol efflux promotes acrosome reaction in goat spermatozoa","volume":"62","author":"Iborra","year":"2000","journal-title":"Biol. Reprod."},{"key":"B88","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1093\/molehr\/gar034","article-title":"Sperm flagella: comparative and phylogenetic perspectives of protein components","volume":"17","author":"Inaba","year":"2011","journal-title":"Mol. Hum. Reprod."},{"key":"B89","doi-asserted-by":"publisher","first-page":"14554","DOI":"10.1021\/ja507832e","article-title":"Lipid organization of the plasma membrane","volume":"136","author":"Ingolfsson","year":"2014","journal-title":"J. Am. Chem. Soc."},{"key":"B90","doi-asserted-by":"publisher","first-page":"2305","DOI":"10.1007\/s00018-005-5195-z","article-title":"Phospholipase D: a lipid centric review","volume":"62","author":"Jenkins","year":"2005","journal-title":"Cell Mol. Life Sci."},{"key":"B91","doi-asserted-by":"publisher","first-page":"1409","DOI":"10.1016\/j.celrep.2017.07.041","article-title":"Vesicle docking is a key target of local PI(4,5)P(2) metabolism in the secretory pathway of INS-1 cells","volume":"20","author":"Ji","year":"2017","journal-title":"Cell Rep."},{"key":"B92","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/j.prostaglandins.2011.01.001","article-title":"Ceramide induces serotonin release from RBL-2H3 mast cells through calcium mediated activation of phospholipase A2","volume":"94","author":"Ji","year":"2011","journal-title":"Prostagl. Other Lipid Mediat"},{"key":"B93","doi-asserted-by":"publisher","first-page":"53186","DOI":"10.1074\/jbc.M411363200","article-title":"Diacylglycerol and its formation by phospholipase C regulate Rab- and SNARE-dependent yeast vacuole fusion","volume":"279","author":"Jun","year":"2004","journal-title":"J. Biol. Chem."},{"key":"B94","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1038\/35074570","article-title":"Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3","volume":"3","author":"Jungnickel","year":"2001","journal-title":"Nat. Cell Biol."},{"key":"B95","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1016\/j.ydbio.2006.12.023","article-title":"Phosphoinositide-dependent pathways in mouse sperm are regulated by egg ZP3 and drive the acrosome reaction","volume":"304","author":"Jungnickel","year":"2007","journal-title":"Dev. Biol."},{"key":"B96","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1002\/j.1939-4640.2002.tb02232.x","article-title":"Zona pellucida and progesterone-induced Ca2+ signaling and acrosome reaction in human spermatozoa","volume":"23","author":"Kirkman-Brown","year":"2002","journal-title":"J. Androl."},{"key":"B97","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1016\/j.bbalip.2009.04.001","article-title":"Biophysics and function of phosphatidic acid: a molecular perspective","volume":"1791","author":"Kooijman","year":"2009","journal-title":"Biochim. Biophys. Acta"},{"key":"B98","doi-asserted-by":"publisher","first-page":"17007","DOI":"10.1021\/bi0518794","article-title":"What makes the bioactive lipids phosphatidic acid and lysophosphatidic acid so special?","volume":"44","author":"Kooijman","year":"","journal-title":"Biochemistry"},{"key":"B99","doi-asserted-by":"publisher","first-page":"2097","DOI":"10.1021\/bi0478502","article-title":"Spontaneous curvature of phosphatidic acid and lysophosphatidic acid","volume":"44","author":"Kooijman","year":"","journal-title":"Biochemistry"},{"key":"B100","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1091\/mbc.e07-02-0148","article-title":"SNARE-Catalyzed fusion events are regulated by Syntaxin1A-lipid interactions","volume":"19","author":"Lam","year":"2008","journal-title":"Mol. Biol. Cell"},{"key":"B101","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1113\/jphysiol.2007.134346","article-title":"SNARE proteins and \u2018membrane rafts","volume":"585","author":"Lang","year":"2007","journal-title":"J. Physiol."},{"key":"B210","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1042\/BST0370955","article-title":"Lipid rafts as functional heterogeneity in cell membranes","volume":"37","author":"Lingwood","year":"2009","journal-title":"Biochem Soc Trans."},{"key":"B102","doi-asserted-by":"publisher","first-page":"2202","DOI":"10.1093\/emboj\/20.9.2202","article-title":"SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis","volume":"20","author":"Lang","year":"2001","journal-title":"EMBO J."},{"key":"B103","doi-asserted-by":"publisher","first-page":"561","DOI":"10.4103\/1008-682X.153309","article-title":"New insights into the regulation of cholesterol efflux from the sperm membrane","volume":"17","author":"Leahy","year":"2015","journal-title":"Asian J. Androl."},{"key":"B104","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1038\/nature09767","article-title":"Progesterone activates the principal Ca2+ channel of human sperm","volume":"471","author":"Lishko","year":"2011","journal-title":"Nature"},{"key":"B105","doi-asserted-by":"publisher","first-page":"4121","DOI":"10.1096\/fj.06-7716com","article-title":"Membrane-permeant Rab3A triggers acrosomal exocytosis in living human sperm","volume":"21","author":"Lopez","year":"2007","journal-title":"FASEB J."},{"key":"B106","doi-asserted-by":"publisher","first-page":"1186","DOI":"10.1016\/j.bbalip.2012.05.001","article-title":"Diacylglycerol stimulates acrosomal exocytosis by feeding into a PKC- and PLD1-dependent positive loop that continuously supplies phosphatidylinositol 4,5-bisphosphate","volume":"1821","author":"Lopez","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"B107","doi-asserted-by":"publisher","first-page":"544","DOI":"10.1016\/j.bbamcr.2015.12.007","article-title":"The signaling module cAMP\/Epac\/Rap1\/PLC\u03b5\/IP3 mobilizes acrosomal calcium during sperm exocytosis","volume":"1863","author":"Lucchesi","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"B108","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1134\/s0006297908030073","article-title":"Lipid rafts association of synaptotagmin I on synaptic vesicles","volume":"73","author":"Lv","year":"2008","journal-title":"Biochem. (Mosc)"},{"key":"B109","doi-asserted-by":"publisher","first-page":"2363","DOI":"10.1182\/blood-2002-11-3341","article-title":"Ceramide inhibition of phospholipase D and its relationship to RhoA and ARF1 translocation in GTP gamma S-stimulated polymorphonuclear leukocytes","volume":"103","author":"Mansfield","year":"2004","journal-title":"Blood"},{"key":"B110","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1007\/978-94-007-3015-1_4","article-title":"Role of PI(4,5)P(2) in vesicle exocytosis and membrane fusion","volume":"59","author":"Martin","year":"2012","journal-title":"Subcell. Biochem."},{"key":"B111","doi-asserted-by":"publisher","first-page":"785","DOI":"10.1016\/j.bbalip.2014.09.017","article-title":"PI(4,5)P\u2082-binding effector proteins for vesicle exocytosis","volume":"1851","author":"Martin","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"B112","doi-asserted-by":"publisher","first-page":"jcs238816","DOI":"10.1242\/jcs.238816","article-title":"Capacitation-associated alkalization in human sperm is differentially controlled at the subcellular level","volume":"133","author":"Matamoros-Volante","year":"2020","journal-title":"J. Cell Sci."},{"key":"B113","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1038\/nature04398","article-title":"Plasma membrane phosphoinositide organization by protein electrostatics","volume":"438","author":"McLaughlin","year":"2005","journal-title":"Nature"},{"key":"B114","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1006\/dbio.2001.0316","article-title":"Synaptotagmin VI participates in the acrosome reaction of human spermatozoa","volume":"235","author":"Michaut","year":"2001","journal-title":"Dev. Biol."},{"key":"B115","doi-asserted-by":"publisher","first-page":"9996","DOI":"10.1073\/pnas.180206197","article-title":"Calcium-triggered acrosomal exocytosis in human spermatozoa requires the coordinated activation of Rab3A and N-ethylmaleimide-sensitive factor","volume":"97","author":"Michaut","year":"2000","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B116","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1126\/science.aad6887","article-title":"Unconventional endocannabinoid signaling governs sperm activation via the sex hormone progesterone","volume":"352","author":"Miller","year":"2016","journal-title":"Science"},{"key":"B117","doi-asserted-by":"publisher","first-page":"7868","DOI":"10.1074\/jbc.M116.716225","article-title":"Calcium promotes the formation of syntaxin 1 mesoscale domains through phosphatidylinositol 4,5-bisphosphate","volume":"291","author":"Milovanovic","year":"2016","journal-title":"J. Biol. Chem."},{"key":"B118","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1262\/jrd.50.667","article-title":"Ceramide enhances acrosomal exocytosis triggered by calcium and the calcium ionophore A23187 in boar spermatozoa","volume":"50","author":"Murase","year":"2004","journal-title":"J. Reprod. Dev."},{"key":"B119","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.1042\/bj3201017","article-title":"Progesterone and the zona pellucida activate different transducing pathways in the sequence of events leading to diacylglycerol generation during mouse sperm acrosomal exocytosis","volume":"320","author":"Murase","year":"1996","journal-title":"Biochem. J."},{"key":"B120","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1007\/BF02534053","article-title":"Lipid composition of the membrane released after an in vitro acrosome reaction of epididymal boar sperm","volume":"21","author":"Nikolopoulou","year":"","journal-title":"Lipids"},{"key":"B121","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/0003-9861(86)90698-3","article-title":"Modulation of the lipid composition of boar sperm plasma membranes during an acrosome reaction in vitro","volume":"250","author":"Nikolopoulou","year":"","journal-title":"Arch. Biochem. Biophys."},{"key":"B122","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.jri.2009.06.258","article-title":"The biological significance of detergent-resistant membranes in spermatozoa","volume":"83","author":"Nixon","year":"2009","journal-title":"J. Reprod. Immunol."},{"key":"B123","doi-asserted-by":"publisher","first-page":"2651","DOI":"10.1002\/jcp.22615","article-title":"Proteomic and functional analysis of human sperm detergent resistant membranes","volume":"226","author":"Nixon","year":"2011","journal-title":"J. Cell Physiol."},{"key":"B124","doi-asserted-by":"publisher","first-page":"102702","DOI":"10.1016\/j.jbc.2022.102702","article-title":"ABCA1 and cholesterol transfer protein Aster-A promote an asymmetric cholesterol distribution in the plasma membrane","volume":"298","author":"Ogasawara","year":"2022","journal-title":"J. Biol. Chem."},{"key":"B125","doi-asserted-by":"publisher","first-page":"3904","DOI":"10.1038\/s41598-018-22226-8","article-title":"A mathematical model of the phosphoinositide pathway","volume":"8","author":"Olivenca","year":"2018","journal-title":"Sci. Rep."},{"key":"B126","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1007\/s11745-011-3601-x","article-title":"Uneven distribution of ceramides, sphingomyelins and glycerophospholipids between heads and tails of rat spermatozoa","volume":"46","author":"Oresti","year":"2011","journal-title":"Lipids"},{"key":"B127","doi-asserted-by":"publisher","first-page":"16830","DOI":"10.1074\/jbc.RA117.001566","article-title":"CatSper channels are regulated by protein kinase A","volume":"293","author":"Orta","year":"2018","journal-title":"J. Biol. Chem."},{"key":"B128","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1093\/molehr\/2.12.921","article-title":"Protein kinase C activation during progesterone-stimulated acrosomal exocytosis in human spermatozoa","volume":"2","author":"O\u2019Toole","year":"","journal-title":"Mol. Hum. Reprod."},{"key":"B129","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1002\/(SICI)1098-2795(199610)45:2<204::AID-MRD13>3.0.CO;2-0","article-title":"Role for Ca2+ channels in the signal transduction pathway leading to acrosomal exocytosis in human spermatozoa","volume":"45","author":"O\u2019Toole","year":"","journal-title":"Mol. Reprod. Dev."},{"key":"B130","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1093\/molehr\/2.5.317","article-title":"A role for diacylglycerol in human sperm acrosomal exocytosis","volume":"2","author":"O\u2019Toole","year":"","journal-title":"Mol. Hum. Reprod."},{"key":"B131","doi-asserted-by":"publisher","first-page":"786","DOI":"10.1016\/j.cellsig.2013.01.009","article-title":"Ceramide 1-phosphate stimulates glucose uptake in macrophages","volume":"25","author":"Ouro","year":"2013","journal-title":"Cell Signal"},{"key":"B132","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1038\/nsmb.3097","article-title":"Synaptotagmin-1 binds to PIP(2)-containing membrane but not to SNAREs at physiological ionic strength","volume":"22","author":"Park","year":"2015","journal-title":"Nat. Struct. Mol. Biol."},{"key":"B133","doi-asserted-by":"publisher","first-page":"9823","DOI":"10.1074\/jbc.M114.629006","article-title":"ADP ribosylation factor 6 (ARF6) promotes acrosomal exocytosis by modulating lipid turnover and Rab3A activation","volume":"290","author":"Pelletan","year":"2015","journal-title":"J. Biol. Chem."},{"key":"B134","doi-asserted-by":"publisher","first-page":"4398","DOI":"10.1021\/acs.langmuir.7b04374","article-title":"Membrane restructuring events during the enzymatic generation of ceramides with very long-chain polyunsaturated fatty acids","volume":"34","author":"Penalva","year":"2018","journal-title":"Langmuir"},{"key":"B135","doi-asserted-by":"publisher","first-page":"2365","DOI":"10.1194\/jlr.M800159-JLR200","article-title":"Lipid levels in sperm, eggs, and during fertilization in Xenopus laevis","volume":"49","author":"Petcoff","year":"2008","journal-title":"J. Lipid Res."},{"key":"B136","doi-asserted-by":"publisher","first-page":"e62968","DOI":"10.1371\/journal.pone.0062968","article-title":"Ceramide synthases expression and role of ceramide synthase-2 in the lung: insight from human lung cells and mouse models","volume":"8","author":"Petrache","year":"2013","journal-title":"PLoS One"},{"key":"B137","doi-asserted-by":"publisher","first-page":"24966","DOI":"10.1074\/jbc.M111.237537","article-title":"Identification of a binding motif in the S5 helix that confers cholesterol sensitivity to the TRPV1 ion channel","volume":"286","author":"Picazo-Juarez","year":"2011","journal-title":"J. Biol. Chem."},{"key":"B138","doi-asserted-by":"publisher","first-page":"158630","DOI":"10.1016\/j.bbalip.2020.158630","article-title":"Novel signaling aspects of ceramide 1-phosphate","volume":"1865","author":"Presa","year":"2020","journal-title":"Biochim. Biophys. Acta Mol. Cell Biol. Lipids"},{"key":"B139","doi-asserted-by":"publisher","first-page":"1404","DOI":"10.1002\/jcp.25634","article-title":"Essential role of CFTR in PKA-dependent phosphorylation, alkalinization, and hyperpolarization during human sperm capacitation","volume":"232","author":"Puga Molina","year":"2017","journal-title":"J. Cell Physiol."},{"key":"B140","doi-asserted-by":"publisher","first-page":"2120","DOI":"10.1016\/S0006-3495(01)76185-1","article-title":"Cross-correlation analysis of inner-leaflet-anchored green fluorescent protein co-redistributed with IgE receptors and outer leaflet lipid raft components","volume":"80","author":"Pyenta","year":"2001","journal-title":"Biophys. J."},{"key":"B141","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.jbior.2016.09.004","article-title":"Phosphatidic acid and neurotransmission","volume":"63","author":"Raben","year":"2017","journal-title":"Adv. Biol. Regul."},{"key":"B142","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/s0092-8674(01)00635-3","article-title":"Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs","volume":"108","author":"Rhee","year":"2002","journal-title":"Cell"},{"key":"B143","doi-asserted-by":"publisher","first-page":"422","DOI":"10.1016\/j.ydbio.2005.07.007","article-title":"Protein kinase C-mediated phosphorylation of the two polybasic regions of synaptotagmin VI regulates their function in acrosomal exocytosis","volume":"285","author":"Roggero","year":"2005","journal-title":"Dev. Biol."},{"key":"B144","doi-asserted-by":"publisher","first-page":"89","DOI":"10.2741\/2050","article-title":"Sperm phospholipases and acrosomal exocytosis","volume":"12","author":"Roldan","year":"2007","journal-title":"Front. Biosci."},{"key":"B145","doi-asserted-by":"publisher","first-page":"1274","DOI":"10.1016\/j.fertnstert.2014.07.1248","article-title":"Acrosome reaction is impaired in spermatozoa of obese men: a preliminary study","volume":"102","author":"Samavat","year":"2014","journal-title":"Fertil. Steril."},{"key":"B146","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1098\/rstb.2003.1265","article-title":"Biosynthesis and degradation of mammalian glycosphingolipids","volume":"358","author":"Sandhoff","year":"2003","journal-title":"Philos. Trans. R. Soc. Lond B Biol. Sci."},{"key":"B147","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1186\/1477-7827-2-12","article-title":"Reactive oxygen species and sperm cells","volume":"2","author":"Sanocka","year":"2004","journal-title":"Reprod. Biol. Endocrinol."},{"key":"B148","doi-asserted-by":"publisher","first-page":"369","DOI":"10.3389\/fendo.2018.00369","article-title":"Cholesterol: a gatekeeper of male fertility?","volume":"9","author":"Sedes","year":"2018","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"B149","doi-asserted-by":"publisher","first-page":"636","DOI":"10.1002\/jcp.20504","article-title":"Segregation of micron-scale membrane sub-domains in live murine sperm","volume":"206","author":"Selvaraj","year":"2006","journal-title":"J. Cell Physiol."},{"key":"B150","doi-asserted-by":"publisher","first-page":"627","DOI":"10.3390\/ijms21020627","article-title":"Association of \u03b1\/\u03b2-Hydrolase D16B with bovine conception rate and sperm plasma membrane lipid composition","volume":"21","author":"Shan","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"B151","doi-asserted-by":"publisher","first-page":"8767","DOI":"10.3390\/ijms22168767","article-title":"Sperm lipid markers of male fertility in mammals","volume":"22","author":"Shan","year":"2021","journal-title":"Int. J. Mol. Sci."},{"key":"B152","doi-asserted-by":"publisher","first-page":"705","DOI":"10.3892\/mmr.2017.8000","article-title":"Characterization of cholesterol metabolism in Sertoli cells and spermatogenesis (Review)","volume":"17","author":"Shi","year":"2018","journal-title":"Mol. Med. Rep."},{"key":"B153","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1194\/jlr.M022715","article-title":"Ablation of ceramide synthase 2 strongly affects biophysical properties of membranes","volume":"53","author":"Silva","year":"2012","journal-title":"J. Lipid Res."},{"key":"B154","doi-asserted-by":"publisher","first-page":"6861","DOI":"10.3390\/ijms21186861","article-title":"Beyond lipid signaling: pleiotropic effects of diacylglycerol kinases in cellular signaling","volume":"21","author":"Sim","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"B155","doi-asserted-by":"publisher","first-page":"8322","DOI":"10.1021\/jp401414y","article-title":"Quantum and all-atom molecular dynamics simulations of protonation and divalent ion binding to phosphatidylinositol 4,5-bisphosphate (PIP2)","volume":"117","author":"Slochower","year":"2013","journal-title":"J. Phys. Chem. B"},{"key":"B156","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1093\/molehr\/gau110","article-title":"Kinetics of human sperm acrosomal exocytosis","volume":"21","author":"Sosa","year":"2015","journal-title":"Mol. Hum. Reprod."},{"key":"B157","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1095\/biolreprod.115.133231","article-title":"Acrosomal swelling is triggered by cAMP downstream of the opening of store-operated calcium channels during acrosomal exocytosis in human sperm","volume":"94","author":"Sosa","year":"2016","journal-title":"Biol. Reprod."},{"key":"B158","doi-asserted-by":"publisher","first-page":"864","DOI":"10.1093\/biolre\/ioad120","article-title":"Segmental differentiation of the murine epididymis: identification of segment-specific, GM1-enriched vesicles and regulation by luminal fluid factors\u2020","volume":"109","author":"Sosnicki","year":"2023","journal-title":"Biol. Reprod."},{"key":"B159","doi-asserted-by":"publisher","first-page":"1216","DOI":"10.1042\/bst0311216","article-title":"Exogenous and intracellularly generated sphingosine 1-phosphate can regulate cellular processes by divergent pathways","volume":"31","author":"Spiegel","year":"2003","journal-title":"Biochem. Soc. Trans."},{"key":"B160","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/0014-5793(92)81388-3","article-title":"A cell free system reveals that capacitation is a prerequisite for membrane fusion during the acrosome reaction","volume":"311","author":"Spungin","year":"1992","journal-title":"FEBS Lett."},{"key":"B161","doi-asserted-by":"publisher","first-page":"1218","DOI":"10.1016\/j.bbamcr.2009.04.006","article-title":"Ceramide synthase 1 is regulated by proteasomal mediated turnover","volume":"1793","author":"Sridevi","year":"2009","journal-title":"Biochim. Biophys. Acta"},{"key":"B162","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/j.ydbio.2015.02.020","article-title":"Phospholipase C and D regulation of Src, calcium release and membrane fusion during Xenopus laevis development","volume":"401","author":"Stith","year":"2015","journal-title":"Dev. Biol."},{"key":"B163","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1007\/978-3-319-30567-7_5","article-title":"Sperm capacitation and acrosome reaction in mammalian sperm","volume":"220","author":"Stival","year":"2016","journal-title":"Adv. Anat. Embryol. Cell Biol."},{"key":"B164","doi-asserted-by":"publisher","first-page":"370","DOI":"10.1016\/j.conb.2005.05.005","article-title":"Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate","volume":"15","author":"Suh","year":"2005","journal-title":"Curr. Opin. Neurobiol."},{"key":"B165","doi-asserted-by":"publisher","first-page":"3161","DOI":"10.1073\/pnas.1121434109","article-title":"Membrane-localized \u03b2-subunits alter the PIP2 regulation of high-voltage activated Ca2+ channels","volume":"109","author":"Suh","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B166","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1016\/j.neuron.2010.07.001","article-title":"Modulation of high-voltage activated Ca(2+) channels by membrane phosphatidylinositol 4,5-bisphosphate","volume":"67","author":"Suh","year":"2010","journal-title":"Neuron"},{"key":"B167","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1007\/978-1-0716-1044-2_10","article-title":"Different approaches to record human sperm exocytosis","volume":"2233","author":"Suhaiman","year":"2021","journal-title":"Methods Mol. Biol."},{"key":"B168","doi-asserted-by":"publisher","first-page":"16302","DOI":"10.1074\/jbc.M109.072439","article-title":"Sphingosine 1-phosphate and sphingosine kinase are involved in a novel signaling pathway leading to acrosomal exocytosis","volume":"285","author":"Suhaiman","year":"2010","journal-title":"J. Biol. Chem."},{"key":"B169","doi-asserted-by":"crossref","DOI":"10.1101\/2023.06.05.543781","volume-title":"Novel roles for diacylglycerol in synaptic vesicle priming and release revealed by complete reconstitution of core protein machinery","author":"Sundaram","year":"2023"},{"key":"B170","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1007\/s10735-008-9207-9","article-title":"Localization of EFA6A, a guanine nucleotide exchange factor for ARF6, in spermatogenic cells of testes of adult mice","volume":"40","author":"Suzuki","year":"2009","journal-title":"J. Mol. Histol."},{"key":"B171","doi-asserted-by":"publisher","first-page":"227","DOI":"10.5604\/12321966.1203881","article-title":"Infertility in the light of new scientific reports - focus on male factor","volume":"23","author":"Szkodziak","year":"2016","journal-title":"Ann. Agric. Environ. Med."},{"key":"B172","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1007\/s00221-007-1036-7","article-title":"Differential effects of ceramide species on exocytosis in rat PC12 cells","volume":"183","author":"Tang","year":"2007","journal-title":"Exp. Brain Res."},{"key":"B173","doi-asserted-by":"publisher","first-page":"108026","DOI":"10.1016\/j.celrep.2020.108026","article-title":"Mono- and poly-unsaturated phosphatidic acid regulate distinct steps of regulated exocytosis in neuroendocrine cells","volume":"32","author":"Tanguy","year":"2020","journal-title":"Cell Rep."},{"key":"B174","doi-asserted-by":"publisher","first-page":"100772","DOI":"10.1016\/j.jbior.2020.100772","article-title":"Phosphatidic acid: mono- and poly-unsaturated forms regulate distinct stages of neuroendocrine exocytosis","volume":"79","author":"Tanguy","year":"2021","journal-title":"Adv. Biol. Regul."},{"key":"B175","doi-asserted-by":"publisher","first-page":"100844","DOI":"10.1016\/j.jbior.2021.100844","article-title":"Phospholipase D1-generated phosphatidic acid modulates secretory granule trafficking from biogenesis to compensatory endocytosis in neuroendocrine cells","volume":"83","author":"Tanguy","year":"2022","journal-title":"Adv. Biol. Regul."},{"key":"B176","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.plipres.2018.08.002","article-title":"Properties, metabolism and roles of sulfogalactosylglycerolipid in male reproduction","volume":"72","author":"Tanphaichitr","year":"2018","journal-title":"Prog. Lipid Res."},{"key":"B177","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1111\/j.1439-0531.2012.02046.x","article-title":"The membrane of the mammalian spermatozoa: much more than an inert envelope","volume":"47","author":"Tapia","year":"2012","journal-title":"Reprod. Domest. Anim."},{"key":"B178","first-page":"275","article-title":"Molecular mechanisms of membrane fusion during acrosomal exocytosis","volume":"65","author":"Tomes","year":"2007","journal-title":"Soc. Reprod. Fertil. Suppl."},{"key":"B179","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1006\/dbio.2001.0475","article-title":"Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and Guinea pig spermatozoa","volume":"240","author":"Travis","year":"2001","journal-title":"Dev. Biol."},{"key":"B180","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1002\/jcp.20487","article-title":"Maitotoxin potently promotes Ca2+ influx in mouse spermatogenic cells and sperm, and induces the acrosome reaction","volume":"206","author":"Trevino","year":"2006","journal-title":"J. Cell Physiol."},{"key":"B181","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.ceca.2017.07.008","article-title":"Regulation of insulin exocytosis by calcium-dependent protein kinase C in beta cells","volume":"67","author":"Trexler","year":"2017","journal-title":"Cell Calcium"},{"key":"B182","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1080\/09687860701228692","article-title":"Syntaxin and VAMP association with lipid rafts depends on cholesterol depletion in capacitating sperm cells","volume":"24","author":"Tsai","year":"2007","journal-title":"Mol. Membr. Biol."},{"key":"B183","doi-asserted-by":"publisher","first-page":"121507","DOI":"10.1016\/j.lfs.2023.121507","article-title":"Sphingomyelinase modulates synaptic vesicle mobilization at the mice neuromuscular junctions","volume":"318","author":"Tsentsevitsky","year":"2023","journal-title":"Life Sci."},{"key":"B184","doi-asserted-by":"publisher","first-page":"5196","DOI":"10.3390\/molecules26175196","article-title":"The role of selected natural biomolecules in sperm production and functionality","volume":"26","author":"Tvrda","year":"2021","journal-title":"Molecules"},{"key":"B185","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1093\/humupd\/dmad006","article-title":"Contribution of semen to early embryo development: fertilization and beyond","volume":"29","author":"Vallet-Buisan","year":"2023","journal-title":"Hum. Reprod. Update"},{"key":"B186","doi-asserted-by":"publisher","first-page":"16447","DOI":"10.1074\/jbc.M112.343418","article-title":"Phosphatidylinositol 4,5-bisphosphate increases Ca2+ affinity of synaptotagmin-1 by 40-fold","volume":"287","author":"van den Bogaart","year":"2012","journal-title":"J. Biol. Chem."},{"key":"B187","doi-asserted-by":"publisher","first-page":"1148831","DOI":"10.3389\/fcell.2023.1148831","article-title":"The pair ceramide 1-phosphate\/ceramide kinase regulates intracellular calcium and progesterone-induced human sperm acrosomal exocytosis","volume":"11","author":"Vaquer","year":"2023","journal-title":"Front. Cell Dev. Biol."},{"key":"B188","doi-asserted-by":"publisher","first-page":"118704","DOI":"10.1016\/j.bbamcr.2020.118704","article-title":"Ceramide induces a multicomponent intracellular calcium increase triggering the acrosome secretion in human sperm","volume":"1867","author":"Vaquer","year":"2020","journal-title":"Biochim. Biophys. Acta Mol. Cell Res."},{"key":"B189","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1002\/(SICI)1098-2795(199709)48:1<95::AID-MRD12>3.0.CO;2-V","article-title":"Diacylglycerol species as messengers and substrates for phosphatidylcholine re-synthesis during Ca2+-dependent exocytosis in boar spermatozoa","volume":"48","author":"Vazquez","year":"1997","journal-title":"Mol. Reprod. Dev."},{"key":"B190","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1073\/pnas.0811895106","article-title":"Understanding the molecular basis of sperm capacitation through kinase design","volume":"106","author":"Visconti","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B191","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1042\/BST0380167","article-title":"Synthesis of fusogenic lipids through activation of phospholipase D1 by GTPases and the kinase RSK2 is required for calcium-regulated exocytosis in neuroendocrine cells","volume":"38","author":"Vitale","year":"2010","journal-title":"Biochem. Soc. Trans."},{"key":"B192","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1016\/j.jprot.2012.12.008","article-title":"In-depth proteomic analysis of the human sperm reveals complex protein compositions","volume":"79","author":"Wang","year":"2013","journal-title":"J. Proteomics"},{"key":"B193","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.chemphyslip.2014.01.001","article-title":"Counterion-mediated cluster formation by polyphosphoinositides","volume":"182","author":"Wang","year":"2014","journal-title":"Chem. Phys. Lipids"},{"key":"B194","doi-asserted-by":"publisher","DOI":"10.1016\/j.bpj.2024.01.012","article-title":"Syntaxin clusters and cholesterol affect the mobility of Syntaxin1a","author":"Weisgerber","year":"2024","journal-title":"Biophys. J."},{"key":"B195","doi-asserted-by":"publisher","first-page":"4910","DOI":"10.1091\/mbc.e09-04-0284","article-title":"Evidence that electrostatic interactions between vesicle-associated membrane protein 2 and acidic phospholipids may modulate the fusion of transport vesicles with the plasma membrane","volume":"20","author":"Williams","year":"2009","journal-title":"Mol. Biol. Cell"},{"key":"B196","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1016\/j.cellsig.2018.01.006","article-title":"Dopamine transporter trafficking is regulated by neutral sphingomyelinase 2\/ceramide kinase","volume":"44","author":"Won","year":"2018","journal-title":"Cell Signal"},{"key":"B197","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1016\/j.bbrc.2009.01.105","article-title":"Involvement of PKC alpha in PMA-induced facilitation of exocytosis and vesicle fusion in PC12 cells","volume":"380","author":"Xue","year":"2009","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B198","first-page":"189","article-title":"Mammalian fertilization","volume-title":"The physiology of reproduction","author":"Yanagimachi","year":"1994"},{"key":"B199","doi-asserted-by":"publisher","first-page":"528","DOI":"10.1111\/j.1365-2605.2009.00961.x","article-title":"Cholesterol and desmosterol in two sperm populations separated on Sil-Select gradient","volume":"33","author":"Zalata","year":"2010","journal-title":"Int. J. Androl."},{"key":"B200","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1093\/molehr\/4.2.111","article-title":"The fatty acid composition of phospholipids of spermatozoa from infertile patients","volume":"4","author":"Zalata","year":"","journal-title":"Mol. Hum. Reprod."},{"key":"B201","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1046\/j.1365-2605.1998.00112.x","article-title":"White blood cells cause oxidative damage to the fatty acid composition of phospholipids of human spermatozoa","volume":"21","author":"Zalata","year":"","journal-title":"Int. J. Androl."},{"key":"B202","doi-asserted-by":"publisher","first-page":"396","DOI":"10.1095\/biolreprod.109.076166","article-title":"Acrosomal swelling and membrane docking are required for hybrid vesicle formation during the human sperm acrosome reaction","volume":"81","author":"Zanetti","year":"2009","journal-title":"Biol. Reprod."},{"key":"B203","doi-asserted-by":"publisher","first-page":"1778","DOI":"10.1016\/j.biochi.2010.08.012","article-title":"Ceramides with 2-hydroxylated, very long-chain polyenoic fatty acids in rodents: from testis to fertilization-competent spermatozoa","volume":"92","author":"Zanetti","year":"","journal-title":"Biochimie"},{"key":"B204","doi-asserted-by":"publisher","first-page":"1886","DOI":"10.1016\/j.biochi.2010.08.015","article-title":"Differential involvement of rat sperm choline glycerophospholipids and sphingomyelin in capacitation and the acrosomal reaction","volume":"92","author":"Zanetti","year":"","journal-title":"Biochimie"},{"key":"B205","doi-asserted-by":"publisher","first-page":"21746","DOI":"10.1074\/jbc.M702968200","article-title":"Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage","volume":"282","author":"Zeniou-Meyer","year":"2007","journal-title":"J. Biol. Chem."},{"key":"B206","doi-asserted-by":"publisher","first-page":"3855","DOI":"10.1038\/s41467-021-24145-1","article-title":"Direct activation of the proton channel by albumin leads to human sperm capacitation and sustained release of inflammatory mediators by neutrophils","volume":"12","author":"Zhao","year":"2021","journal-title":"Nat. Commun."},{"key":"B207","doi-asserted-by":"publisher","first-page":"513","DOI":"10.4161\/cib.3.6.13137","article-title":"The \u201cacrosomal synapse\u201d: subcellular organization by lipid rafts and scaffolding proteins exhibits high similarities in neurons and mammalian spermatozoa","volume":"3","author":"Zitranski","year":"2010","journal-title":"Commun. Integr. Biol."}],"container-title":["Frontiers in Cell and Developmental Biology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2024.1457638\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,23]],"date-time":"2024-09-23T04:41:38Z","timestamp":1727066498000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2024.1457638\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,23]]},"references-count":210,"alternative-id":["10.3389\/fcell.2024.1457638"],"URL":"https:\/\/doi.org\/10.3389\/fcell.2024.1457638","relation":{},"ISSN":["2296-634X"],"issn-type":[{"value":"2296-634X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,23]]},"article-number":"1457638"}}