{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T05:15:29Z","timestamp":1790745329458,"version":"4.1.0"},"reference-count":128,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2021,1,25]],"date-time":"2021-01-25T00:00:00Z","timestamp":1611532800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01AI120607"],"award-info":[{"award-number":["R01AI120607"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>Eukaryotes critically rely on endocytosis of autologous and heterologous material to maintain homeostasis and to proliferate. Although mechanisms of endocytosis have been extensively identified in mammalian and plant systems along with model systems including budding yeast, relatively little is known about endocytosis in protozoan parasites including those belonging to the phylum Apicomplexa. Whereas it has been long established that the apicomplexan agents of malaria (Plasmodium spp.) internalize and degrade hemoglobin from infected red blood cells to acquire amino acids for growth, that the related and pervasive parasite Toxoplasma gondii has a functional and active endocytic system was only recently discovered. Here we discuss emerging and hypothesized mechanisms of endocytosis in Toxoplasma gondii with reference to model systems and malaria parasites. Establishing a framework for potential mechanisms of endocytosis in Toxoplasma gondii will help guide future research aimed at defining the molecular basis and biological relevance of endocytosis in this tractable and versatile parasite.<\/jats:p>","DOI":"10.3390\/life11020084","type":"journal-article","created":{"date-parts":[[2021,1,25]],"date-time":"2021-01-25T09:59:40Z","timestamp":1611568780000},"page":"84","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":24,"title":["Emerging Mechanisms of Endocytosis in Toxoplasma gondii"],"prefix":"10.3390","volume":"11","author":[{"given":"Olivia L.","family":"McGovern","sequence":"first","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan School of Medicine, Ann Arbor, MI 48109-5620, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yolanda","family":"Rivera-Cuevas","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan School of Medicine, Ann Arbor, MI 48109-5620, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6859-8895","authenticated-orcid":false,"given":"Vern B.","family":"Carruthers","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan School of Medicine, Ann Arbor, MI 48109-5620, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1038\/nrm3151","article-title":"Molecular Mechanism and Physiological Functions of Clathrin-mediated Endocytosis","volume":"12","author":"McMahon","year":"2011","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.1111\/j.1365-2958.2010.07165.x","article-title":"Characterization of a Novel Organelle in Toxoplasma Gondii with Similar Composition and Function to the Plant Vacuole","volume":"76","author":"Miranda","year":"2010","journal-title":"Mol. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1340","DOI":"10.1111\/j.1365-2958.2010.07181.x","article-title":"Cathepsin L Occupies a Vacuolar Compartment and Is a Protein Maturase within the Endo\/Exocytic System of Toxoplasma Gondii","volume":"76","author":"Parussini","year":"2010","journal-title":"Mol. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/j.chom.2012.03.006","article-title":"Toxoplasma Sortilin-like Receptor Regulates Protein Transport and Is Essential for Apical Secretory Organelle Biogenesis and Host Infection","volume":"11","author":"Sloves","year":"2012","journal-title":"Cell Host Microbe"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Kremer, K., Kamin, D., Rittweger, E., Wilkes, J., Flammer, H., Mahler, S., Heng, J., Tonkin, C.J., Langsley, G., and Hell, S.W. (2013). An Overexpression Screen of Toxoplasma Gondii Rab-GTPases Reveals Distinct Transport Routes to the Micronemes. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003213"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1111\/cmi.12426","article-title":"Toxoplasma Gondii Vps11, a Subunit of HOPS and CORVET Tethering Complexes, Is Essential for the Biogenesis of Secretory Organelles","volume":"17","author":"Pastore","year":"2015","journal-title":"Cell. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"11191","DOI":"10.1038\/ncomms11191","article-title":"Unconventional Endosome-like Compartment and Retromer Complex in Toxoplasma Gondii Govern Parasite Integrity and Host Infection","volume":"7","author":"Sangare","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Venugopal, K., Werkmeister, E., Barois, N., Saliou, J.M., Poncet, A., Huot, L., Sindikubwabo, F., Hakimi, M.A., Langsley, G., and Lafont, F. (2017). Dual Role of the Toxoplasma Gondii Clathrin Adaptor AP1 in the Sorting of Rhoptry and Microneme Proteins and in Parasite Division. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006331"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1007\/BF00933773","article-title":"Endocytosis at the Micropore of Toxoplasma Gondii","volume":"80","author":"Nichols","year":"1994","journal-title":"Parasitol. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1006\/expr.2001.4624","article-title":"Receptor-Mediated Endocytosis in an Apicomplexan Parasite (Toxoplasma Gondii)","volume":"98","author":"Lindh","year":"2001","journal-title":"Exp. Parasitol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e01188-14","DOI":"10.1128\/mBio.01188-14","article-title":"Toxoplasma Gondii Ingests and Digests Host Cytosolic Proteins","volume":"5","author":"Dou","year":"2014","journal-title":"mBio"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"4452","DOI":"10.4049\/jimmunol.159.9.4452","article-title":"Intracellular Fate of Vacuoles Containing Toxoplasma Gondii Is Determined at the Time of Formation and Depends on the Mechanism of Entry","volume":"159","author":"Mordue","year":"1997","journal-title":"J. Immunol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1783","DOI":"10.1084\/jem.190.12.1783","article-title":"Invasion by Toxoplasma Gondii Establishes a Moving Junction That Selectively Excludes Host Cell Plasma Membrane Proteins on the Basis of Their Membrane Anchoring","volume":"190","author":"Mordue","year":"1999","journal-title":"J. Exp. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1006\/expr.1999.4412","article-title":"Toxoplasma Gondii Resides in a Vacuole That Resists Fusion with Host Cell Endocytic and Exocytic Vesicular Trafficking Pathways","volume":"92","author":"Mordue","year":"1999","journal-title":"Exp. Parasitol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2063","DOI":"10.1084\/jem.20061318","article-title":"Vacuolar and Plasma Membrane Stripping and Autophagic Elimination of Toxoplasma Gondii in Primed Effector Macrophages","volume":"203","author":"Ling","year":"2006","journal-title":"J. Exp. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1128\/EC.00081-14","article-title":"Toxoplasma Gondii Development of Its Replicative Niche: In Its Host Cell and Beyond","volume":"13","author":"Blader","year":"2014","journal-title":"Eukaryotic Cell"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.exppara.2017.02.018","article-title":"Toxoplasma Growth in Vitro Is Dependent on Exogenous Tyrosine and Is Independent of AAH2 Even in Tyrosine-Limiting Conditions","volume":"176","author":"Marino","year":"2017","journal-title":"Exp. Parasitol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1749-6632.1994.tb44233.x","article-title":"Structure and Function of the Parasitophorous Vacuole Membrane Surrounding Toxoplasma Gondii","volume":"730","author":"Joiner","year":"1994","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1016\/j.chom.2015.04.003","article-title":"The Toxoplasma Dense Granule Proteins GRA17 and GRA23 Mediate the Movement of Small Molecules between the Host and the Parasitophorous Vacuole","volume":"17","author":"Gold","year":"2015","journal-title":"Cell Host Microbe"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.cell.2006.01.056","article-title":"Toxoplasma Gondii Sequesters Lysosomes from Mammalian Hosts in the Vacuolar Space","volume":"125","author":"Coppens","year":"2006","journal-title":"Cell"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1974","DOI":"10.1091\/mbc.e12-11-0827","article-title":"Toxoplasma Gondii Salvages Sphingolipids from the Host Golgi through the Rerouting of Selected Rab Vesicles to the Parasitophorous Vacuole","volume":"24","author":"Romano","year":"2013","journal-title":"Mol. Biol. Cell"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"4235","DOI":"10.1083\/jcb.201701108","article-title":"The Parasite Toxoplasma Sequesters Diverse Rab Host Vesicles within an Intravacuolar Network","volume":"216","author":"Romano","year":"2017","journal-title":"J. Cell Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1111\/tra.12556","article-title":"Intersection of Endocytic and Exocytic Systems in Toxoplasma Gondii","volume":"19","author":"McGovern","year":"2018","journal-title":"Traffic"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/j.pt.2020.03.010","article-title":"Endocytosis in Plasmodium and Toxoplasma Parasites","volume":"36","author":"Spielmann","year":"2020","journal-title":"Trends Parasitol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.tcb.2011.09.001","article-title":"Clathrin-Mediated Endocytosis in Budding Yeast","volume":"22","author":"Weinberg","year":"2012","journal-title":"Trends Cell Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1146\/annurev-arplant-043015-112242","article-title":"Endocytosis and Endosomal Trafficking in Plants","volume":"67","author":"Valencia","year":"2016","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1038\/nrm.2017.132","article-title":"Mechanisms of Clathrin-Mediated Endocytosis","volume":"19","author":"Kaksonen","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1146\/annurev-biochem-060910-094416","article-title":"Roles for Actin Assembly in Endocytosis","volume":"81","author":"Mooren","year":"2012","journal-title":"Annu. Rev. Biochem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1534\/genetics.112.145540","article-title":"Actin and Endocytosis in Budding Yeast","volume":"199","author":"Goode","year":"2015","journal-title":"Genetics"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/j.tcb.2006.08.004","article-title":"Bar Domain Proteins: A Role in Tubulation, Scission and Actin Assembly in Clathrin-Mediated Endocytosis","volume":"16","author":"Dawson","year":"2006","journal-title":"Trends Cell Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1038\/nrm3266","article-title":"Dynamin, a Membrane-Remodelling GTPase","volume":"13","author":"Ferguson","year":"2012","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"4991","DOI":"10.1093\/emboj\/cdg481","article-title":"Clathrin-Mediated Endocytosis Is Essential in Trypanosoma Brucei","volume":"22","author":"Allen","year":"2003","journal-title":"EMBO J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"894","DOI":"10.1111\/j.1600-0854.2009.00910.x","article-title":"The Single ENTH-Domain Protein of Trypanosomes; Endocytic Functions and Evolutionary Relationship with Epsin","volume":"10","author":"Dacks","year":"2009","journal-title":"Traffic"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"3502","DOI":"10.1105\/tpc.106.040923","article-title":"Somatic Cytokinesis and Pollen Maturation in Arabidopsis Depend on TPLATE, Which Has Domains Similar to Coat Proteins","volume":"18","author":"Damme","year":"2006","journal-title":"Plant Cell"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1016\/j.cell.2014.01.039","article-title":"The TPLATE Adaptor Complex Drives Clathrin-Mediated Endocytosis in Plants","volume":"156","author":"Gadeyne","year":"2014","journal-title":"Cell"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3897","DOI":"10.1093\/emboj\/18.14.3897","article-title":"Clathrin Functions in the Absence of Heterotetrameric Adaptors and AP180-Related Proteins in Yeast","volume":"18","author":"Huang","year":"1999","journal-title":"EMBO J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1016\/j.devcel.2009.08.006","article-title":"A Yeast Killer Toxin Screen Provides Insights into a\/b Toxin Entry, Trafficking, and Killing Mechanisms","volume":"17","author":"Carroll","year":"2009","journal-title":"Dev. Cell"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1083\/jcb.200305145","article-title":"Clathrin-Mediated Endocytosis in AP-2-Depleted Cells","volume":"162","author":"Motley","year":"2003","journal-title":"J. Cell Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3496","DOI":"10.1242\/jcs.070508","article-title":"A Role for the Dynamin-like Protein Vps1 during Endocytosis in Yeast","volume":"123","author":"Rooij","year":"2010","journal-title":"J. Cell Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3839","DOI":"10.1242\/jcs.01239","article-title":"The Yeast Dynamin-Related GTPase Vps1p Functions in the Organization of the Actin Cytoskeleton via Interaction with Sla1p","volume":"117","author":"Yu","year":"2004","journal-title":"J. Cell Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1016\/j.cub.2015.01.061","article-title":"A Dynamin-Actin Interaction Is Required for Vesicle Scission during Endocytosis in Yeast","volume":"25","author":"Palmer","year":"2015","journal-title":"Curr. Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"a016758","DOI":"10.1101\/cshperspect.a016758","article-title":"Clathrin-Independent Pathways of Endocytosis","volume":"6","author":"Mayor","year":"2014","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/j.tcb.2017.11.004","article-title":"Mechanisms of Carrier Formation during Clathrin-Independent Endocytosis","volume":"28","author":"Ferreira","year":"2018","journal-title":"Trends Cell Biol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1038\/nature14067","article-title":"Endophilin Marks and Controls a Clathrin-Independent Endocytic Pathway","volume":"517","author":"Boucrot","year":"2015","journal-title":"Nature"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1083\/jcb.200407078","article-title":"Ultrastructural Identification of Uncoated Caveolin-Independent Early Endocytic Vehicles","volume":"168","author":"Kirkham","year":"2005","journal-title":"J. Cell Boil."},{"key":"ref_46","first-page":"465","article-title":"Clathrin-Independent Carriers Form a High Capacity Endocytic Sorting System at the Leading Edge of Migrating Cells","volume":"168","author":"Howes","year":"2005","journal-title":"J. Cell Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1016\/j.cell.2007.05.018","article-title":"GEFs and GAPs: Critical Elements in the Control of Small G Proteins","volume":"129","author":"Bos","year":"2007","journal-title":"Cell"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1802","DOI":"10.1016\/j.cub.2008.10.044","article-title":"The GTPase-Activating Protein GRAF1 Regulates the CLIC\/GEEC Endocytic Pathway","volume":"18","author":"Lundmark","year":"2008","journal-title":"Curr. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.semcdb.2014.03.034","article-title":"Endosome Maturation, Transport and Functions","volume":"31","author":"Scott","year":"2014","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"3823","DOI":"10.1073\/pnas.1221785110","article-title":"The CORVET Complex Promotes Tethering and Fusion of Rab5\/Vps21-Positive Membranes","volume":"110","author":"Balderhaar","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1111\/tra.12232","article-title":"Mammalian CORVET Is Required for Fusion and Conversion of Distinct Early Endosome Subpopulations","volume":"15","author":"Perini","year":"2014","journal-title":"Traffic"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"30280","DOI":"10.1074\/jbc.M115.688440","article-title":"Characterization of the Mammalian CORVET and HOPS Complexes and Their Modular Restructuring for Endosome Specificity","volume":"290","author":"Kant","year":"2015","journal-title":"J. Biol. Chem."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1146\/annurev-biochem-052810-093700","article-title":"GTPase Networks in Membrane Traffic","volume":"81","author":"Novick","year":"2012","journal-title":"Annu. Rev. Biochem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1515\/hsz-2013-0258","article-title":"Endocytic Rabs in Membrane Trafficking and Signaling","volume":"395","author":"Numrich","year":"2014","journal-title":"Biol. Chem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2743","DOI":"10.1111\/febs.12151","article-title":"Tethering Complexes in the Endocytic Pathway: CORVET and HOPS","volume":"280","author":"Solinger","year":"2013","journal-title":"FEBS J."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1105\/tpc.105.037978","article-title":"Vacuolar H+-ATPase Activity Is Required for Endocytic and Secretory Trafficking in Arabidopsis","volume":"18","author":"Dettmer","year":"2006","journal-title":"Plant Cell"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1375","DOI":"10.1016\/j.cub.2014.05.004","article-title":"Plant Vacuolar Trafficking Occurs through Distinctly Regulated Pathways","volume":"24","author":"Ebine","year":"2014","journal-title":"Curr. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1016\/j.cub.2014.05.005","article-title":"Protein Delivery to Vacuole Requires SAND Protein-Dependent Rab GTPase Conversion for MVB-Vacuole Fusion","volume":"24","author":"Singh","year":"2014","journal-title":"Curr. Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"3463","DOI":"10.1105\/tpc.111.086918","article-title":"Multivesicular Bodies Mature from the Trans-Golgi Network\/Early Endosome in Arabidopsis","volume":"23","author":"Scheuring","year":"2011","journal-title":"Plant Cell"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Klinger, C.M., Klute, M.J., and Dacks, J.B. (2013). Comparative Genomic Analysis of Multi-Subunit Tethering Complexes Demonstrates an Ancient Pan-Eukaryotic Complement and Sculpting in Apicomplexa. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076278"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1091\/mbc.e02-08-0509","article-title":"The AtC-VPS Protein Complex Is Localized to the Tonoplast and the Prevacuolar Compartment in Arabidopsis","volume":"14","author":"Rojo","year":"2003","journal-title":"Mol. Biol. Cell"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.1083\/jcb.149.7.1335","article-title":"The Plant Vacuolar Sorting Receptor AtELP Is Involved in Transport of NH(2)-Terminal Propeptide-Containing Vacuolar Proteins in Arabidopsis Thaliana","volume":"149","author":"Ahmed","year":"2000","journal-title":"J. Cell Biol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"3006","DOI":"10.1105\/tpc.107.057711","article-title":"A SNARE Complex Unique to Seed Plants Is Required for Protein Storage Vacuole Biogenesis and Seed Development of Arabidopsis Thaliana","volume":"20","author":"Ebine","year":"2008","journal-title":"Plant Cell"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"6307","DOI":"10.1073\/pnas.1602757113","article-title":"AtVPS41-Mediated Endocytic Pathway Is Essential for Pollen Tube-Stigma Interaction in Arabidopsis","volume":"113","author":"Hao","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"E2457","DOI":"10.1073\/pnas.1717839115","article-title":"Distinct Sets of Tethering Complexes, SNARE Complexes, and Rab GTPases Mediate Membrane Fusion at the Vacuole in Arabidopsis","volume":"115","author":"Takemoto","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1083\/jcb.28.2.355","article-title":"The Feeding Mechanism of Avian Malarial Parasites","volume":"28","author":"Aikawa","year":"1966","journal-title":"J. Cell Biol."},{"key":"ref_67","first-page":"369","article-title":"Three-Dimensional Reconstruction of the Feeding Process of the Malaria Parasite","volume":"16","author":"Slomianny","year":"1990","journal-title":"Blood Cells"},{"key":"ref_68","first-page":"1686","article-title":"Dynamin like Protein 1 Participated in the Hemoglobin Uptake Pathway of Plasmodium Falciparum","volume":"122","author":"Zhou","year":"2009","journal-title":"Chin. Med. J."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1937","DOI":"10.1242\/jcs.023150","article-title":"A New Model for Hemoglobin Ingestion and Transport by the Human Malaria Parasite Plasmodium Falciparum","volume":"121","author":"Lazarus","year":"2008","journal-title":"J. Cell Sci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1128\/EC.00267-14","article-title":"Defining the Morphology and Mechanism of the Hemoglobin Transport Pathway in Plasmodium Falciparum Infected Erythrocytes","volume":"14","author":"Milani","year":"2015","journal-title":"Eukaryotic Cell"},{"key":"ref_71","first-page":"452","article-title":"Actin Is Required for Endocytic Trafficking in the Malaria Parasite Plasmodium Falciparum","volume":"10","author":"Smythe","year":"2007","journal-title":"Cell. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"8","DOI":"10.7554\/eLife.52355","article-title":"Single-Molecule Turnover Dynamics of Actin and Membrane Coat Proteins in Clathrin-Mediated Endocytosis","volume":"8","author":"Lacy","year":"2019","journal-title":"eLife"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"2463","DOI":"10.1073\/pnas.0711067105","article-title":"Four Distinct Pathways of Hemoglobin Uptake in the Malaria Parasite Plasmodium Falciparum","volume":"105","author":"Elliott","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1038\/nmeth.4223","article-title":"A Genetic System to Study Plasmodium Falciparum Protein Function","volume":"14","author":"Birnbaum","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.chom.2018.11.010","article-title":"PfVPS45 Is Required for Host Cell Cytosol Uptake by Malaria Blood Stage Parasites","volume":"25","author":"Jonscher","year":"2019","journal-title":"Cell Host Microbe"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2917","DOI":"10.1016\/j.celrep.2019.10.095","article-title":"Decreased K13 Abundance Reduces Hemoglobin Catabolism and Proteotoxic Stress, Underpinning Artemisinin Resistance","volume":"29","author":"Yang","year":"2019","journal-title":"Cell Rep."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1126\/science.aax4735","article-title":"A Kelch13-Defined Endocytosis Pathway Mediates Artemisinin Resistance in Malaria Parasites","volume":"367","author":"Birnbaum","year":"2020","journal-title":"Science"},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Nolan, S.J., Romano, J.D., and Coppens, I. (2017). Host Lipid Droplets: An Important Source of Lipids Salvaged by the Intracellular Parasite Toxoplasma Gondii. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006362"},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Gras, S., Jimenez-Ruiz, E., Klinger, C.M., Schneider, K., Klingl, A., Lemgruber, L., and Meissner, M. (2019). An Endocytic-Secretory Cycle Participates in Toxoplasma Gondii in Motility. PLoS Biol., 17.","DOI":"10.1371\/journal.pbio.3000060"},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Lige, B., Romano, J.D., Sampels, V., Sonda, S., Joiner, K.A., and Coppens, I. (2012). Introduction of Caveolae Structural Proteins into the Protozoan Toxoplasma Results in the Formation of Heterologous Caveolae but Not Caveolar Endocytosis. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0051773"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Pieperhoff, M.S., Schmitt, M., Ferguson, D.J., and Meissner, M. (2013). The Role of Clathrin in Post-Golgi Trafficking in Toxoplasma Gondii. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0077620"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1091\/mbc.e02-08-0458","article-title":"Actin Filament Polymerization Regulates Gliding Motility by Apicomplexan Parasites","volume":"14","author":"Wetzel","year":"2003","journal-title":"Mol. Biol. Cell"},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Bargieri, D., Lagal, V., Andenmatten, N., Tardieux, I., Meissner, M., and M\u00e9nard, R. (2014). Host Cell Invasion by Apicomplexan Parasites: The Junction Conundrum. PLoS Pathog., 10.","DOI":"10.1371\/journal.ppat.1004273"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.cub.2009.01.039","article-title":"A Dynamin Is Required for the Biogenesis of Secretory Organelles in Toxoplasma Gondii","volume":"19","author":"Breinich","year":"2009","journal-title":"Curr. Biol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.cub.2008.12.048","article-title":"A Novel Dynamin-Related Protein Has Been Recruited for Apicoplast Fission in Toxoplasma Gondii","volume":"19","author":"Reiff","year":"2009","journal-title":"Curr. Biol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1111\/mmi.14138","article-title":"TgDrpC, an Atypical Dynamin-Related Protein in Toxoplasma Gondii, Is Associated with Vesicular Transport Factors and Parasite Division","volume":"111","author":"Varberg","year":"2019","journal-title":"Mol. Microbiol."},{"key":"ref_87","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":"Sidik","year":"2016","journal-title":"Cell"},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Tomavo, S., Slomianny, C., Meissner, M., and Carruthers, V.B. (2013). Protein Trafficking through the Endosomal System Prepares Intracellular Parasites for a Home Invasion. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003629"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1128\/EC.05192-11","article-title":"Molecular Characterization of Toxoplasma Gondii Formin 3, an Actin Nucleator Dispensable for Tachyzoite Growth and Motility","volume":"11","author":"Daher","year":"2012","journal-title":"Eukaryotic Cell"},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Bisio, H., Chaabene, R.B., Sabitzki, R., Maco, B., Marq, J.B., Gilberger, T.-W., Spielmann, T., and Soldati-Favre, D. (2020). The ZIP Code of Vesicle Trafficking in Apicomplexa: SEC1\/Munc18 and SNARE Proteins. mBio, 11.","DOI":"10.1128\/mBio.02092-20"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1016\/j.cell.2017.04.031","article-title":"SnapShot: Macropinocytosis","volume":"169","author":"Marques","year":"2017","journal-title":"Cell"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1083\/jcb.201104045","article-title":"Existence of a Novel Clathrin-Independent Endocytic Pathway in Yeast That Depends on Rho1 and Formin","volume":"195","author":"Prosser","year":"2011","journal-title":"J. Cell Biol."},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Daher, W., Plattner, F., Carlier, M.F., and Soldati-Favre, D. (2010). Concerted Action of Two Formins in Gliding Motility and Host Cell Invasion by Toxoplasma Gondii. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1001132"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1038\/nature01020","article-title":"Curvature of Clathrin-Coated Pits Driven by Epsin","volume":"419","author":"Ford","year":"2002","journal-title":"Nature"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.cell.2012.01.047","article-title":"Membrane Fission Is Promoted by Insertion of Amphipathic Helices and Is Restricted by Crescent BAR Domains","volume":"149","author":"Boucrot","year":"2012","journal-title":"Cell"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"2397","DOI":"10.1091\/mbc.e02-01-0021","article-title":"Biogenesis of Nanotubular Network in Toxoplasma Parasitophorous Vacuole Induced by Parasite Proteins","volume":"13","author":"Mercier","year":"2002","journal-title":"Mol. Biol. Cell"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1669","DOI":"10.1242\/jcs.108.4.1669","article-title":"Regulated Secretion of Multi-Lamellar Vesicles Leads to Formation of a Tubulo-Vesicular Network in Host-Cell Vacuoles Occupied by Toxoplasma Gondii","volume":"108","author":"Sibley","year":"1995","journal-title":"J. Cell Sci."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/S0166-6851(99)00092-4","article-title":"Differential Membrane Targeting of the Secretory Proteins GRA4 and GRA6 within the Parasitophorous Vacuole Formed by Toxoplasma Gondii","volume":"102","author":"Labruyere","year":"1999","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1016\/j.ijpara.2007.10.010","article-title":"Functional Domains of the Toxoplasma GRA2 Protein in the Formation of the Membranous Nanotubular Network of the Parasitophorous Vacuole","volume":"38","author":"Travier","year":"2008","journal-title":"Int. J. Parasitol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"R116","DOI":"10.1016\/j.cub.2012.01.028","article-title":"The ESCRT Machinery","volume":"22","author":"Schmidt","year":"2012","journal-title":"Curr. Biol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.1038\/s41564-017-0018-1","article-title":"Efficient Invasion by Toxoplasma Depends on the Subversion of Host Protein Networks","volume":"2","author":"Guerin","year":"2017","journal-title":"Nat. Microbiol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"2163","DOI":"10.1242\/jcs.029884","article-title":"The ESCRT Machinery at a Glance","volume":"122","author":"Wollert","year":"2009","journal-title":"J. Cell Sci."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"912","DOI":"10.1038\/nrmicro1790","article-title":"Beyond Tsg101: The Role of Alix in \u201cESCRTing\u201d HIV-1","volume":"5","author":"Fujii","year":"2007","journal-title":"Nat. Rev. Genet."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1016\/j.chom.2013.08.012","article-title":"Virus Budding and the ESCRT Pathway","volume":"14","author":"Votteler","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1016\/j.devcel.2012.10.023","article-title":"ALIX Is a Lys63-Specific Polyubiquitin Binding Protein That Functions in Retrovirus Budding","volume":"23","author":"Dowlatshahi","year":"2012","journal-title":"Dev. Cell"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1972","DOI":"10.1111\/j.1600-0854.2008.00817.x","article-title":"Functional Replacement of a Retroviral Late Domain by Ubiquitin Fusion","volume":"9","author":"Joshi","year":"2008","journal-title":"Traffic"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"3546","DOI":"10.1128\/JVI.02045-10","article-title":"Multiple Interactions between the ESCRT Machinery and Arrestin-Related Proteins: Implications for PPXY-Dependent Budding","volume":"85","author":"Rauch","year":"2010","journal-title":"J. Virol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1111\/j.1462-5822.2005.00646.x","article-title":"The Rhoptry Neck Protein RON4 Re-Localizes at the Moving Junction during Toxoplasma Gondii Invasion","volume":"7","author":"Lebrun","year":"2005","journal-title":"Cell. Microbiol."},{"key":"ref_109","doi-asserted-by":"crossref","unstructured":"Besteiro, S., Michelin, A., Poncet, J., Dubremetz, J., and Lebrun, M. (2009). Export of a Toxoplasma Gondii Rhoptry Neck Protein Complex at the Host Cell Membrane to Form the Moving Junction during Invasion. PLoS Pathog., 5.","DOI":"10.1371\/journal.ppat.1000309"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"1703","DOI":"10.1126\/science.1085544","article-title":"The Deep Roots of Eukaryotes","volume":"300","author":"Baldauf","year":"2003","journal-title":"Science"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"38842","DOI":"10.1038\/srep38842","article-title":"A Critical Role for Toxoplasma Gondii Vacuolar Protein Sorting VPS9 in Secretory Organelle Biogenesis and Host Infection","volume":"6","author":"Sakura","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"4551","DOI":"10.1091\/mbc.e06-01-0064","article-title":"A Cleavable Propeptide Influences Toxoplasma Infection by Facilitating the Trafficking and Secretion of the TgMIC2-M2AP Invasion Complex","volume":"17","author":"Harper","year":"2006","journal-title":"Mol. Biol. Cell"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1083\/jcb.152.3.563","article-title":"Identification and Characterization of an Escorter for Two Secretory Adhesins in Toxoplasma Gondii","volume":"152","author":"Reiss","year":"2001","journal-title":"J. Cell Biol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1242\/jcs.115.3.563","article-title":"A Family of Transmembrane Microneme Proteins of Toxoplasma Gondii Contain EGF-like Domains and Function as Escorters","volume":"115","author":"Meissner","year":"2002","journal-title":"J. Cell Sci."},{"key":"ref_115","doi-asserted-by":"crossref","unstructured":"Huynh, M.H., and Carruthers, V.B. (2006). Toxoplasma MIC2 Is a Major Determinant of Invasion and Virulence. PLoS Pathog., 2.","DOI":"10.1371\/journal.ppat.0020084"},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.pbi.2017.08.005","article-title":"Vacuolar Trafficking and Biogenesis: A Maturation in the Field","volume":"40","author":"Brillada","year":"2017","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"16017","DOI":"10.1038\/nplants.2016.17","article-title":"Receptor-Mediated Sorting of Soluble Vacuolar Proteins Ends at the Trans-Golgi Network\/Early Endosome","volume":"2","author":"Kunzl","year":"2016","journal-title":"Nat. Plants"},{"key":"ref_118","doi-asserted-by":"crossref","unstructured":"Ezougou, C.N., Ben-Rached, F., Moss, D.K., Lin, J.W., Black, S., Knuepfer, E., Green, J.L., Khan, S.M., Mukhopadhyay, A., and Janse, C.J. (2014). Plasmodium Falciparum Rab5B Is an N-Terminally Myristoylated Rab GTPase That Is Targeted to the Parasite\u2019s Plasma and Food Vacuole Membranes. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0087695"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"23","DOI":"10.4161\/sgtp.18299","article-title":"Endosomal Trafficking Pathway Regulated by ARA6, a RAB5 GTPase Unique to Plants","volume":"3","author":"Ebine","year":"2012","journal-title":"Small GTPases"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"8840","DOI":"10.1073\/pnas.0601876103","article-title":"Plasmodium Falciparum Ensures Its Amino Acid Supply with Multiple Acquisition Pathways and Redundant Proteolytic Enzyme Systems","volume":"103","author":"Liu","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1016\/S0020-7519(02)00194-7","article-title":"Artemisinin: Mechanisms of Action, Resistance and Toxicity","volume":"32","author":"Meshnick","year":"2002","journal-title":"Int. J. Parasitol."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/0163-7258(93)90056-J","article-title":"Chloroquine: Mechanism of Drug Action and Resistance in Plasmodium Falciparum","volume":"57","author":"Slater","year":"1993","journal-title":"Pharmacol. Ther."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"5258","DOI":"10.1038\/s41467-020-18991-8","article-title":"Genome-Wide Screens Identify Toxoplasma Gondii Determinants of Parasite Fitness in IFN\u03b3-Activated Murine Macrophages","volume":"11","author":"Wang","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_124","first-page":"293225","article-title":"Acquisition of Host Cytosolic Protein by Toxoplasma Gondii Bradyzoites","volume":"2020","author":"Kannan","year":"2020","journal-title":"bioRxiv"},{"key":"ref_125","first-page":"1","article-title":"Toxoplasma Depends on Lysosomal Consumption of Autophagosomes for Persistent Infection","volume":"2","author":"Dou","year":"2017","journal-title":"Nat. Microbiol."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"57","DOI":"10.4269\/ajtmh.15-0007","article-title":"Antimalarial Drug Resistance: Literature Review and Activities and Findings of the ICEMR Network","volume":"93","author":"Cui","year":"2015","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/j.exppara.2009.02.003","article-title":"Minireview: Clinical Cryptosporidiosis","volume":"124","author":"Chalmers","year":"2010","journal-title":"Exp. Parasitol."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"29030","DOI":"10.1038\/srep29030","article-title":"Use of Fluorescent Nanoparticles to Investigate Nutrient Acquisition by Developing Eimeria Maxima Macrogametocytes","volume":"6","author":"Wallach","year":"2016","journal-title":"Sci. Rep."}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/11\/2\/84\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:14:54Z","timestamp":1760159694000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/11\/2\/84"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,25]]},"references-count":128,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["life11020084"],"URL":"https:\/\/doi.org\/10.3390\/life11020084","relation":{},"ISSN":["2075-1729"],"issn-type":[{"value":"2075-1729","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,25]]}}}