{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T10:19:29Z","timestamp":1791368369535,"version":"4.3.1"},"update-to":[{"DOI":"10.1371\/journal.ppat.1010438","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,4,5]],"date-time":"2022-04-05T00:00:00Z","timestamp":1649116800000}}],"reference-count":79,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2022,3,24]],"date-time":"2022-03-24T00:00:00Z","timestamp":1648080000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Swiss National Foundation","award":["FN3100A0-116722"],"award-info":[{"award-number":["FN3100A0-116722"]}]},{"name":"Scientific & Technological Cooperation Programme Switzerland-Rio de Janeiro","award":["IZRJZ3_164183"],"award-info":[{"award-number":["IZRJZ3_164183"]}]},{"name":"Swiss Government Excellence Scholarship"}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>\n                    Regulated microneme secretion governs motility, host cell invasion and egress in the obligate intracellular apicomplexans. Intracellular calcium oscillations and phospholipid dynamics critically regulate microneme exocytosis. Despite its importance for the lytic cycle of these parasites, molecular mechanistic details about exocytosis are still missing. Some members of the P4-ATPases act as flippases, changing the phospholipid distribution by translocation from the outer to the inner leaflet of the membrane. Here, the localization and function of the repertoire of P4-ATPases was investigated across the lytic cycle of\n                    <jats:italic>Toxoplasma gondii<\/jats:italic>\n                    . Of relevance, ATP2B and the non-catalytic subunit cell division control protein 50.4 (CDC50.4) form a stable heterocomplex at the parasite plasma membrane, essential for microneme exocytosis. This complex is responsible for flipping phosphatidylserine, which presumably acts as a lipid mediator for organelle fusion with the plasma membrane. Overall, this study points toward the importance of phosphatidylserine asymmetric distribution at the plasma membrane for microneme exocytosis.\n                  <\/jats:p>","DOI":"10.1371\/journal.ppat.1010438","type":"journal-article","created":{"date-parts":[[2022,3,24]],"date-time":"2022-03-24T17:59:14Z","timestamp":1648144754000},"page":"e1010438","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":31,"title":["Toxoplasma gondii phosphatidylserine flippase complex ATP2B-CDC50.4 critically participates in microneme exocytosis"],"prefix":"10.1371","volume":"18","author":[{"given":"Hugo","family":"Bisio","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7936-4442","authenticated-orcid":true,"given":"Aarti","family":"Krishnan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Baptiste","family":"Marq","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4156-2109","authenticated-orcid":true,"given":"Dominique","family":"Soldati-Favre","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,3,24]]},"reference":[{"issue":"9888","key":"ppat.1010438.ref001","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/S0140-6736(13)60844-2","article-title":"Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study.","volume":"382","author":"KL Kotloff","year":"2013","journal-title":"Lancet"},{"issue":"12","key":"ppat.1010438.ref002","doi-asserted-by":"crossref","first-page":"1415","DOI":"10.1017\/S0031182009990916","article-title":"Progress towards understanding the immunobiology of Theileria parasites","volume":"136","author":"WI Morrison","year":"2009","journal-title":"Parasitology"},{"issue":"30","key":"ppat.1010438.ref003","doi-asserted-by":"crossref","first-page":"5540","DOI":"10.1016\/j.vaccine.2006.12.030","article-title":"Challenges in the successful control of the avian coccidia","volume":"25","author":"MW Shirley","year":"2007","journal-title":"Vaccine"},{"key":"ppat.1010438.ref004","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1146\/annurev-micro-020518-120235","article-title":"Signaling Cascades Governing Entry into and Exit from Host Cells by Toxoplasma gondii","volume":"73","author":"H Bisio","year":"2019","journal-title":"Annu Rev Microbiol"},{"issue":"12","key":"ppat.1010438.ref005","doi-asserted-by":"crossref","DOI":"10.1098\/rsob.170213","article-title":"Cyclic nucleotide signalling in malaria parasites.","volume":"7","author":"DA Baker","year":"2017","journal-title":"Open Biol."},{"issue":"5","key":"ppat.1010438.ref006","doi-asserted-by":"crossref","first-page":"e1007670","DOI":"10.1371\/journal.ppat.1007670","article-title":"The triumvirate of signaling molecules controlling Toxoplasma microneme exocytosis: Cyclic GMP, calcium, and phosphatidic acid.","volume":"15","author":"HE Bullen","year":"2019","journal-title":"PLoS Pathog."},{"issue":"5","key":"ppat.1010438.ref007","doi-asserted-by":"crossref","first-page":"e13018","DOI":"10.1111\/cmi.13018","article-title":"Biogenesis and secretion of micronemes in Toxoplasma gondii","volume":"21","author":"DJ Dubois","year":"2019","journal-title":"Cell Microbiol"},{"issue":"3","key":"ppat.1010438.ref008","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1038\/s41564-018-0339-8","article-title":"Phosphatidic acid governs natural egress in Toxoplasma gondii via a guanylate cyclase receptor platform","volume":"4","author":"H Bisio","year":"2019","journal-title":"Nat Microbiol"},{"issue":"6","key":"ppat.1010438.ref009","doi-asserted-by":"crossref","first-page":"804","DOI":"10.1016\/j.chom.2018.10.015","article-title":"Essential cGMP Signaling in Toxoplasma Is Initiated by a Hybrid P-Type ATPase-Guanylate Cyclase","volume":"24","author":"KM Brown","year":"2018","journal-title":"Cell Host Microbe"},{"issue":"3","key":"ppat.1010438.ref010","doi-asserted-by":"crossref","DOI":"10.26508\/lsa.201900402","article-title":"An unusual and vital protein with guanylate cyclase and P4-ATPase domains in a pathogenic protist","volume":"2","author":"O Gunay-Esiyok","year":"2019","journal-title":"Life Sci Alliance"},{"issue":"22","key":"ppat.1010438.ref011","doi-asserted-by":"crossref","first-page":"8959","DOI":"10.1074\/jbc.RA118.005491","article-title":"An apically located hybrid guanylate cyclase-ATPase is critical for the initiation of Ca(2+) signaling and motility in Toxoplasma gondii.","volume":"294","author":"L Yang","year":"2019","journal-title":"J Biol Chem"},{"issue":"21","key":"ppat.1010438.ref012","doi-asserted-by":"crossref","first-page":"3250","DOI":"10.15252\/embj.201796794","article-title":"Crosstalk between PKA and PKG controls pH-dependent host cell egress of Toxoplasma gondii","volume":"36","author":"Y Jia","year":"2017","journal-title":"EMBO J"},{"issue":"9","key":"ppat.1010438.ref013","doi-asserted-by":"crossref","first-page":"e2005642","DOI":"10.1371\/journal.pbio.2005642","article-title":"Protein kinase A negatively regulates Ca2+ signalling in Toxoplasma gondii","volume":"16","author":"AD Uboldi","year":"2018","journal-title":"PLoS Biol"},{"issue":"3","key":"ppat.1010438.ref014","doi-asserted-by":"crossref","DOI":"10.1128\/mBio.00375-17","article-title":"Plasma Membrane Association by N-Acylation Governs PKG Function in Toxoplasma gondii.","volume":"8","author":"KM Brown","year":"2017","journal-title":"mBio"},{"issue":"3","key":"ppat.1010438.ref015","doi-asserted-by":"crossref","first-page":"e1001806","DOI":"10.1371\/journal.pbio.1001806","article-title":"Phosphoinositide metabolism links cGMP-dependent protein kinase G to essential Ca(2)(+) signals at key decision points in the life cycle of malaria parasites.","volume":"12","author":"M Brochet","year":"2014","journal-title":"PLoS Biol"},{"issue":"3","key":"ppat.1010438.ref016","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.ceca.2014.12.010","article-title":"The calcium signaling toolkit of the Apicomplexan parasites Toxoplasma gondii and Plasmodium spp","volume":"57","author":"S Lourido","year":"2015","journal-title":"Cell Calcium"},{"issue":"7296","key":"ppat.1010438.ref017","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1038\/nature09022","article-title":"Calcium-dependent protein kinase 1 is an essential regulator of exocytosis in Toxoplasma","volume":"465","author":"S Lourido","year":"2010","journal-title":"Nature"},{"issue":"24","key":"ppat.1010438.ref018","doi-asserted-by":"crossref","first-page":"4524","DOI":"10.1038\/emboj.2012.299","article-title":"Distinct signalling pathways control Toxoplasma egress and host-cell invasion","volume":"31","author":"S Lourido","year":"2012","journal-title":"EMBO J"},{"key":"ppat.1010438.ref019","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.42669","article-title":"Three F-actin assembly centers regulate organelle inheritance, cell-cell communication and motility in Toxoplasma gondii.","volume":"8","author":"N Tosetti","year":"2019","journal-title":"Elife"},{"issue":"11","key":"ppat.1010438.ref020","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1038\/nrmicro.2017.86","article-title":"Gliding motility powers invasion and egress in Apicomplexa","volume":"15","author":"K Frenal","year":"2017","journal-title":"Nat Rev Microbiol"},{"issue":"3","key":"ppat.1010438.ref021","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/j.chom.2016.02.006","article-title":"Phosphatidic Acid-Mediated Signaling Regulates Microneme Secretion in Toxoplasma","volume":"19","author":"HE Bullen","year":"2016","journal-title":"Cell Host Microbe"},{"key":"ppat.1010438.ref022","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1038\/s41420-019-0187-1","article-title":"Phosphatidic acid homeostasis regulated by a type-2 phosphatidic acid phosphatase represents a novel druggable target in malaria intervention","volume":"5","author":"R Kumar Sah","year":"2019","journal-title":"Cell Death Discov"},{"issue":"8","key":"ppat.1010438.ref023","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1016\/j.str.2018.05.001","article-title":"Structural Basis of Phosphatidic Acid Sensing by APH in Apicomplexan Parasites","volume":"26","author":"N Darvill","year":"2018","journal-title":"Structure"},{"issue":"6","key":"ppat.1010438.ref024","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1242\/jcs.114454","article-title":"Membrane curvature at a glance","volume":"128","author":"HT McMahon","year":"2015","journal-title":"J Cell Sci"},{"issue":"2","key":"ppat.1010438.ref025","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1074\/jbc.R600035200","article-title":"Phospholipid flippases.","volume":"282","author":"DL Daleke","year":"2007","journal-title":"J Biol Chem"},{"issue":"6","key":"ppat.1010438.ref026","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1080\/10409238.2016.1237934","article-title":"Decoding P4-ATPase substrate interactions","volume":"51","author":"BP Roland","year":"2016","journal-title":"Crit Rev Biochem Mol Biol"},{"issue":"6458","key":"ppat.1010438.ref027","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1126\/science.aay3353","article-title":"Cryo-EM structures capture the transport cycle of the P4-ATPase flippase","volume":"365","author":"M Hiraizumi","year":"2019","journal-title":"Science"},{"issue":"6","key":"ppat.1010438.ref028","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1016\/j.cell.2016.08.019","article-title":"A Genome-wide CRISPR Screen in Toxoplasma Identifies Essential Apicomplexan Genes","volume":"166","author":"SM Sidik","year":"2016","journal-title":"Cell"},{"key":"ppat.1010438.ref029","doi-asserted-by":"crossref","first-page":"10519","DOI":"10.1038\/ncomms10519","article-title":"Functional profiles of orphan membrane transporters in the life cycle of the malaria parasite.","volume":"7","author":"S Kenthirapalan","year":"2016","journal-title":"Nat Commun"},{"key":"ppat.1010438.ref030","doi-asserted-by":"crossref","first-page":"100315","DOI":"10.1016\/j.jbc.2021.100315","article-title":"Aminoglycerophospholipid flipping and P4-ATPases in Toxoplasma gondii","author":"K Chen","year":"2021","journal-title":"J Biol Chem"},{"issue":"12","key":"ppat.1010438.ref031","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a005637","article-title":"Synaptic vesicle exocytosis.","volume":"3","author":"TC Sudhof","year":"2011","journal-title":"Cold Spring Harb Perspect Biol"},{"issue":"3","key":"ppat.1010438.ref032","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1016\/j.cell.2011.09.046","article-title":"Doc2 is a Ca2+ sensor required for asynchronous neurotransmitter release","volume":"147","author":"J Yao","year":"2011","journal-title":"Cell"},{"key":"ppat.1010438.ref033","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.14211","article-title":"Synaptotagmin-1 C2B domain interacts simultaneously with SNAREs and membranes to promote membrane fusion.","volume":"5","author":"S Wang","year":"2016","journal-title":"Elife"},{"issue":"5","key":"ppat.1010438.ref034","doi-asserted-by":"crossref","DOI":"10.1128\/mBio.02092-20","article-title":"The ZIP Code of Vesicle Trafficking in Apicomplexa: SEC1\/Munc18 and SNARE Proteins.","volume":"11","author":"H Bisio","year":"2020","journal-title":"mBio"},{"issue":"6065","key":"ppat.1010438.ref035","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1126\/science.1210829","article-title":"A DOC2 protein identified by mutational profiling is essential for apicomplexan parasite exocytosis","volume":"335","author":"A Farrell","year":"2012","journal-title":"Science"},{"issue":"5","key":"ppat.1010438.ref036","doi-asserted-by":"crossref","first-page":"e12999","DOI":"10.1111\/cmi.12999","article-title":"Transmission of the malaria parasite requires ferlin for gamete egress from the red blood cell","volume":"21","author":"K Obrova","year":"2019","journal-title":"Cell Microbiol"},{"key":"ppat.1010438.ref037","article-title":"Toxoplasma ferlin1 is a versatile and dynamic mediator of microneme trafficking and secretion.","author":"DNA Tagoe","year":"2020","journal-title":"bioRxiv"},{"issue":"3","key":"ppat.1010438.ref038","doi-asserted-by":"crossref","first-page":"217","DOI":"10.3390\/life11030217","article-title":"Ferlins and TgDOC2 in Toxoplasma Microneme, Rhoptry and Dense Granule Secretion.","volume":"11","author":"DNA Tagoe","year":"2021","journal-title":"Life"},{"issue":"3","key":"ppat.1010438.ref039","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1111\/j.1365-2958.2009.06863.x","article-title":"Membrane transport proteins of the malaria parasite","volume":"74","author":"RE Martin","year":"2009","journal-title":"Mol Microbiol"},{"issue":"5","key":"ppat.1010438.ref040","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1111\/jeu.12626","article-title":"Tagging of Weakly Expressed Toxoplasma gondii Calcium-Related Genes with High-Affinity Tags","volume":"65","author":"MA Hortua Triana","year":"2018","journal-title":"J Eukaryot Microbiol"},{"issue":"48","key":"ppat.1010438.ref041","doi-asserted-by":"crossref","first-page":"33543","DOI":"10.1074\/jbc.M114.593012","article-title":"Phospholipid flippase activities and substrate specificities of human type IV P-type ATPases localized to the plasma membrane","volume":"289","author":"H Takatsu","year":"2014","journal-title":"J Biol Chem"},{"issue":"5860","key":"ppat.1010438.ref042","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1126\/science.1152066","article-title":"Membrane phosphatidylserine regulates surface charge and protein localization","volume":"319","author":"T Yeung","year":"2008","journal-title":"Science"},{"issue":"126","key":"ppat.1010438.ref043","article-title":"Distribution, dynamics and functional roles of phosphatidylserine within the cell","volume":"17","author":"JG Kay","year":"2019","journal-title":"Cell Commun Signal"},{"issue":"11","key":"ppat.1010438.ref044","doi-asserted-by":"crossref","first-page":"7230","DOI":"10.1074\/jbc.M705195200","article-title":"Crystal structure of lactadherin C2 domain at 1.7 A\u00b0 resolution with mutational and computational analyses of its membrane-binding motif","volume":"283","author":"C Shao","year":"2008","journal-title":"Journal of Biological Chemistry"},{"issue":"15","key":"ppat.1010438.ref045","doi-asserted-by":"crossref","first-page":"4629","DOI":"10.1021\/jp8001993","article-title":"Membrane potential and electrostatics of phospholipid bilayers with asymmetric transmembrane distribution of anionic lipids","volume":"112","author":"AA Gurtovenko","year":"2008","journal-title":"J Phys Chem B"},{"key":"ppat.1010438.ref046","article-title":"Phosphatidylserine is a critical modulator for Akt activation","volume":"25","author":"HY Kim","year":"2011","journal-title":"Faseb J"},{"key":"ppat.1010438.ref047","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.plipres.2014.06.002","article-title":"Phosphatidylserine in the brain: metabolism and function","volume":"56","author":"HY Kim","year":"2014","journal-title":"Prog Lipid Res"},{"key":"ppat.1010438.ref048","doi-asserted-by":"crossref","DOI":"10.3389\/fphys.2016.00275","article-title":"P4-ATPases as Phospholipid Flippases-Structure, Function, and Enigmas.","volume":"7","author":"JP Andersen","year":"2016","journal-title":"Front Physiol."},{"issue":"1","key":"ppat.1010438.ref049","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1080\/22221751.2020.1870413","article-title":"ATP2, The essential P4-ATPase of malaria parasites, catalyzes lipid-stimulated ATP hydrolysis in complex with a Cdc50 beta-subunit","volume":"10","author":"A Lamy","year":"2021","journal-title":"Emerg Microbes Infect"},{"key":"ppat.1010438.ref050","article-title":"The extracellular milieu of Toxoplasma\u2018s lytic cycle drives lab-adaptation and promotes changes in lipid metabolism primarily driven by transcriptional reprogramming","author":"VA Primo","year":"2021","journal-title":"bioRxiv"},{"issue":"17","key":"ppat.1010438.ref051","doi-asserted-by":"crossref","first-page":"7402","DOI":"10.1128\/MCB.24.17.7402-7418.2004","article-title":"Molecular interactions of yeast Neo1p, an essential member of the Drs2 family of aminophospholipid translocases, and its role in membrane trafficking within the endomembrane system","volume":"24","author":"S Wicky","year":"2004","journal-title":"Mol Cell Biol"},{"issue":"24","key":"ppat.1010438.ref052","doi-asserted-by":"crossref","first-page":"3883","DOI":"10.1091\/mbc.E16-08-0586","article-title":"The phospholipid flippase ATP9A is required for the recycling pathway from the endosomes to the plasma membrane","volume":"27","author":"Y Tanaka","year":"2016","journal-title":"Mol Biol Cell"},{"issue":"15","key":"ppat.1010438.ref053","doi-asserted-by":"crossref","first-page":"11235","DOI":"10.1074\/jbc.275.15.11235","article-title":"A guanylyl cyclase from Paramecium with 22 transmembrane spans. Expression of the catalytic domains and formation of chimeras with the catalytic domains of mammalian adenylyl cyclases","volume":"275","author":"JU Linder","year":"2000","journal-title":"J Biol Chem"},{"issue":"17","key":"ppat.1010438.ref054","doi-asserted-by":"crossref","first-page":"2763","DOI":"10.1016\/j.cub.2018.06.069","article-title":"ISP1-Anchored Polarization of GCbeta\/CDC50A Complex Initiates Malaria Ookinete Gliding Motility","volume":"28","author":"H Gao","year":"2018","journal-title":"Curr Biol"},{"issue":"1","key":"ppat.1010438.ref055","doi-asserted-by":"crossref","first-page":"1764","DOI":"10.1038\/s41467-020-15479-3","article-title":"An intracellular membrane protein GEP1 regulates xanthurenic acid induced gametogenesis of malaria parasites.","volume":"11","author":"Y Jiang","year":"2020","journal-title":"Nat Commun"},{"issue":"6388","key":"ppat.1010438.ref056","doi-asserted-by":"crossref","first-page":"eaap7847","DOI":"10.1126\/science.aap7847","article-title":"Uncovering the essential genes of the human malaria parasite Plasmodium falciparum by saturation mutagenesis","volume":"360","author":"M Zhang","year":"2018","journal-title":"Science"},{"issue":"38","key":"ppat.1010438.ref057","doi-asserted-by":"crossref","first-page":"23110","DOI":"10.1074\/jbc.M115.655027","article-title":"Characterization of P4 ATPase Phospholipid Translocases (Flippases) in Human and Rat Pancreatic Beta Cells: THEIR GENE SILENCING INHIBITS INSULIN SECRETION.","volume":"290","author":"IU Ansari","year":"2015","journal-title":"J Biol Chem"},{"issue":"8","key":"ppat.1010438.ref058","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1128\/EC.00054-15","article-title":"Lipid Biosynthetic Genes Affect Candida albicans Extracellular Vesicle Morphology, Cargo, and Immunostimulatory Properties","volume":"14","author":"JM Wolf","year":"2015","journal-title":"Eukaryot Cell"},{"issue":"11","key":"ppat.1010438.ref059","doi-asserted-by":"crossref","first-page":"e1002288","DOI":"10.1371\/journal.pbio.1002288","article-title":"Phosphatidylthreonine and Lipid-Mediated Control of Parasite Virulence","volume":"13","author":"RD Arroyo-Olarte","year":"2015","journal-title":"PLoS Biol"},{"issue":"25","key":"ppat.1010438.ref060","doi-asserted-by":"crossref","first-page":"4674","DOI":"10.1091\/mbc.E15-07-0487","article-title":"Phosphatidylserine translocation at the yeast trans-Golgi network regulates protein sorting into exocytic vesicles","volume":"26","author":"HM Hankins","year":"2015","journal-title":"Mol Biol Cell"},{"issue":"8387","key":"ppat.1010438.ref061","article-title":"Direct quantitative detection of Doc2b-induced hemifusion in optically trapped membranes.","volume":"6","author":"I Brouwer","year":"2015","journal-title":"Nat Commun."},{"issue":"2","key":"ppat.1010438.ref062","doi-asserted-by":"crossref","DOI":"10.1006\/bbrc.1995.1062","article-title":"Doc2: A Novel Brain Protein Having Two Repeated C2-like Domains.","volume":"206","author":"S Orita","year":"1995","journal-title":"Biochem and Biophysical Research Commun."},{"issue":"11","key":"ppat.1010438.ref063","article-title":"Phosphatidylserine Exposure by Toxoplasma gondii Is Fundamental to Balance the Immune Response Granting Survival of the Parasite and of the Host.","volume":"6","author":"TAT dos Santos","year":"2011","journal-title":"Plos One."},{"issue":"1","key":"ppat.1010438.ref064","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1111\/j.1574-6968.2006.00495.x","article-title":"Trypanosoma cruzi exposes phosphatidylserine as an evasion mechanism","volume":"266","author":"RA DaMatta","year":"2007","journal-title":"Fems Microbiol Lett"},{"issue":"1","key":"ppat.1010438.ref065","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0166-6851(03)00024-0","article-title":"Transbilayer translocation of membrane phosphatidylserine and its role in macrophage invasion in Leishmania promastigotes.","volume":"128","author":"A Tripathi","year":"2003","journal-title":"Mol Biochem Parasit"},{"issue":"27","key":"ppat.1010438.ref066","doi-asserted-by":"crossref","first-page":"22938","DOI":"10.1074\/jbc.M112.373639","article-title":"The obligate intracellular parasite Toxoplasma gondii secretes a soluble phosphatidylserine decarboxylase","volume":"287","author":"N Gupta","year":"2012","journal-title":"J Biol Chem"},{"issue":"5","key":"ppat.1010438.ref067","doi-asserted-by":"crossref","first-page":"215","DOI":"10.15698\/mic2016.05.500","article-title":"Optogenetic monitoring identifies phosphatidylthreonine-regulated calcium homeostasis in Toxoplasma gondii","volume":"3","author":"A Kuchipudi","year":"2016","journal-title":"Microb Cell"},{"issue":"5106","key":"ppat.1010438.ref068","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1126\/science.8469986","article-title":"Transient transfection and expression in the obligate intracellular parasite Toxoplasma gondii","volume":"260","author":"D Soldati","year":"1993","journal-title":"Science"},{"issue":"24","key":"ppat.1010438.ref069","doi-asserted-by":"crossref","first-page":"14010","DOI":"10.1074\/jbc.271.24.14010","article-title":"Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation","volume":"271","author":"RG Donald","year":"1996","journal-title":"J Biol Chem"},{"issue":"24","key":"ppat.1010438.ref070","doi-asserted-by":"crossref","first-page":"11703","DOI":"10.1073\/pnas.90.24.11703","article-title":"Stable molecular transformation of Toxoplasma gondii: a selectable dihydrofolate reductase-thymidylate synthase marker based on drug-resistance mutations in malaria","volume":"90","author":"RG Donald","year":"1993","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"5135","key":"ppat.1010438.ref071","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1126\/science.8235614","article-title":"Gene replacement in Toxoplasma gondii with chloramphenicol acetyltransferase as selectable marker","volume":"262","author":"K Kim","year":"1993","journal-title":"Science"},{"issue":"2","key":"ppat.1010438.ref072","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/0166-6851(96)02598-4","article-title":"A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei","volume":"77","author":"P Bastin","year":"1996","journal-title":"Mol Biochem Parasitol"},{"issue":"9","key":"ppat.1010438.ref073","doi-asserted-by":"crossref","first-page":"2149","DOI":"10.1093\/emboj\/21.9.2149","article-title":"Toxoplasma gondii myosin A and its light chain: a fast, single-headed, plus-end-directed motor","volume":"21","author":"A Herm-Gotz","year":"2002","journal-title":"EMBO J"},{"issue":"13","key":"ppat.1010438.ref074","doi-asserted-by":"crossref","first-page":"2409","DOI":"10.1242\/jcs.113.13.2409","article-title":"Toxoplasma gondii catalase: are there peroxisomes in Toxoplasma?","volume":"113","author":"M Ding","year":"2000","journal-title":"J Cell Sci"},{"issue":"7","key":"ppat.1010438.ref075","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis.","volume":"9","author":"J Schindelin","year":"2012","journal-title":"Nat Methods"},{"key":"ppat.1010438.ref076","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1186\/1471-2105-5-113","article-title":"MUSCLE: a multiple sequence alignment method with reduced time and space complexity","volume":"5","author":"RC Edgar","year":"2004","journal-title":"BMC Bioinformatics"},{"issue":"5","key":"ppat.1010438.ref077","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"RC Edgar","year":"2004","journal-title":"Nucleic Acids Res"},{"key":"ppat.1010438.ref078","doi-asserted-by":"crossref","first-page":"W465","DOI":"10.1093\/nar\/gkn180","article-title":"Phylogeny.fr: robust phylogenetic analysis for the non-specialist","volume":"36","author":"A Dereeper","year":"2008","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"ppat.1010438.ref079","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1038\/nmeth.3213","article-title":"The I-TASSER Suite: protein structure and function prediction.","volume":"12","author":"J Yang","year":"2015","journal-title":"Nat Methods."}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1010438","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,4,5]],"date-time":"2022-04-05T00:00:00Z","timestamp":1649116800000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1010438","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,5]],"date-time":"2022-04-05T13:56:16Z","timestamp":1649166976000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1010438"}},"subtitle":[],"editor":[{"given":"Michael J.","family":"Blackman","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,3,24]]},"references-count":79,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2022,3,24]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1010438","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.11.25.470034","asserted-by":"object"}]},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,24]]}}}