{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,6]],"date-time":"2026-05-06T16:25:29Z","timestamp":1778084729381,"version":"3.51.4"},"reference-count":113,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,8,31]],"date-time":"2021-08-31T00:00:00Z","timestamp":1630368000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>The Coccidia are a subclass of the Apicomplexa and include several genera of protozoan parasites that cause important diseases in humans and animals, with Toxoplasma gondii becoming the \u2018model organism\u2019 for research into the coccidian molecular and cellular processes. The amenability to the cultivation of T. gondii tachyzoites and the wide availability of molecular tools for this parasite have revealed many mechanisms related to their cellular trafficking and roles of parasite secretory organelles, which are critical in parasite-host interaction. Nevertheless, the extrapolation of the T. gondii mechanisms described in tachyzoites to other coccidian parasites should be done carefully. In this review, we considered published data from Eimeria parasites, a coccidian genus comprising thousands of species whose infections have important consequences in livestock and poultry. These studies suggest that the Coccidia possess both shared and diversified mechanisms of protein trafficking and secretion potentially linked to their lifecycles. Whereas trafficking and secretion appear to be well conversed prior to and during host-cell invasion, important differences emerge once endogenous development commences. Therefore, further studies to validate the mechanisms described in T. gondii tachyzoites should be performed across a broader range of coccidians (including T. gondii sporozoites). In addition, further genus-specific research regarding important disease-causing Coccidia is needed to unveil the individual molecular mechanisms of pathogenesis related to their specific lifecycles and hosts.<\/jats:p>","DOI":"10.3390\/life11090909","type":"journal-article","created":{"date-parts":[[2021,8,31]],"date-time":"2021-08-31T21:59:45Z","timestamp":1630447185000},"page":"909","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Do All Coccidia Follow the Same Trafficking Rules?"],"prefix":"10.3390","volume":"11","author":[{"given":"Virginia","family":"Marugan-Hernandez","sequence":"first","affiliation":[{"name":"The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms AL9 7TA, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gonzalo","family":"Sanchez-Arsuaga","sequence":"additional","affiliation":[{"name":"The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms AL9 7TA, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sue","family":"Vaughan","sequence":"additional","affiliation":[{"name":"Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford OX3 0BP, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alana","family":"Burrell","sequence":"additional","affiliation":[{"name":"Electron Microscopy Science Technology Platform, The Francis Crick Institute, London NW1 1AT, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fiona M.","family":"Tomley","sequence":"additional","affiliation":[{"name":"The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms AL9 7TA, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,8,31]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1467","DOI":"10.1242\/jcs.111.11.1467","article-title":"The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: An unusual compartment in infected cells","volume":"111","author":"Lingelbach","year":"1998","journal-title":"J. Cell Sci."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Sangar\u00e9, L.O., Alayi, T.D., Westermann, B., Hovasse, A., Sindikubwabo, F., Callebaut, I., Werkmeister, E., Lafont, F., Slomianny, C., and Hakimi, M.-A. (2016). Unconventional endosome-like compartment and retromer complex in Toxoplasma gondii govern parasite integrity and host infection. Nat. Commun., 7.","DOI":"10.1038\/ncomms11191"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"5343","DOI":"10.1074\/jbc.M208291200","article-title":"AP-1 in Toxoplasma gondii Mediates Biogenesis of the Rhoptry Secretory Organelle from a Post-Golgi Compartment","volume":"278","author":"Yang","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_4","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_5","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/S0020-7519(02)00021-8","article-title":"The conceptual basis for a new classification of the coccidia","volume":"32","author":"Tenter","year":"2002","journal-title":"Int. J. Parasitol."},{"key":"ref_6","first-page":"1","article-title":"Re-calculating the cost of coccidiosis in chickens","volume":"51","author":"Blake","year":"2020","journal-title":"Veter- Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1017\/S0031182019001562","article-title":"Life cycle stages, specific organelles and invasion mechanisms of Eimeria species","volume":"147","author":"Burrell","year":"2019","journal-title":"Parasitology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"698","DOI":"10.1128\/EC.00021-08","article-title":"MORN1 Has a Conserved Role in Asexual and Sexual Development across the Apicomplexa","volume":"7","author":"Ferguson","year":"2008","journal-title":"Eukaryot. Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3491","DOI":"10.1128\/IAI.00254-08","article-title":"Temporal and spatial distribution of Toxoplasma gondii differentiation into Bradyzoites and tissue cyst formation in vivo","volume":"76","author":"Marocco","year":"2008","journal-title":"Infect. Immun."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1761","DOI":"10.1128\/iai.62.5.1761-1767.1994","article-title":"Reduced replication of Toxoplasma gondii is necessary for induction of bradyzoite-specific antigens: A possible role for nitric oxide in triggering stage conversion","volume":"62","author":"Bohne","year":"1994","journal-title":"Infect. Immun."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Behnke, M.S., Zhang, T.P., Dubey, J.P., and Sibley, L.D. (2014). Toxoplasma gondii merozoite gene expression analysis with comparison to the life cycle discloses a unique expression state during enteric development. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-350"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Koreny, L., Zeeshan, M., Barylyuk, K., Tromer, E.C., van Hooff, J.J.E., Brady, D., Ke, H., Chelaghma, S., Ferguson, D.J.P., and Eme, L. (2021). Molecular characterization of the conoid complex in Toxoplasma reveals its conservation in all apicomplexans, including Plasmodium species. PLoS Biol., 19.","DOI":"10.1371\/journal.pbio.3001081"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"31","DOI":"10.2307\/3279101","article-title":"Ultrastructure of Cytoplasmic and Nuclear Changes in Eimeria tenella during First-Generation Schizogony in Cell Culture","volume":"61","author":"Pacheco","year":"1975","journal-title":"J. Parasitol."},{"key":"ref_14","first-page":"167","article-title":"Ultrastructural study of early stages of asexual multiplication and microgametogony of toxoplasma gondii in the small intestine of the cat","volume":"82","author":"Ferguson","year":"2009","journal-title":"Acta Pathol. Microbiol. Scand. Sect. B Microbiol. Immunol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1128\/CMR.11.2.267","article-title":"Structures of Toxoplasma gondii Tachyzoites, Bradyzoites, and Sporozoites and Biology and Development of Tissue Cysts","volume":"11","author":"Dubey","year":"1998","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_16","first-page":"285","article-title":"Transmission and scanning electron microscopy of host cell entry by Toxoplasma gondii","volume":"87","author":"Aikawa","year":"1977","journal-title":"Am. J. Pathol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/S0166-6851(00)00280-2","article-title":"Induction of secretion and surface capping of microneme proteins in Eimeria tenella","volume":"110","author":"Bumstead","year":"2000","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1111\/j.1462-5822.2011.01597.x","article-title":"The moving junction of apicomplexan parasites: A key structure for invasion","volume":"13","author":"Besteiro","year":"2011","journal-title":"Cell. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/0166-6851(87)90004-1","article-title":"Identification of immunodominant surface antigens of Eimeria acervulina sporozoites and merozoites","volume":"25","author":"Jenkins","year":"1987","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/0014-4894(92)90144-Y","article-title":"Toxoplasma gondii: The role of a 30-kDa surface protein in host cell invasion","volume":"74","author":"Grimwood","year":"1992","journal-title":"Exp. Parasitol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"8038","DOI":"10.4049\/jimmunol.174.12.8038","article-title":"Stage-specific expression of surface antigens by Toxoplasma gondii as a mechanism to facilitate parasite persistence","volume":"174","author":"Kim","year":"2005","journal-title":"J. Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.molbiopara.2004.01.013","article-title":"Eimeria tenella sporozoites and merozoites differentially express glycosylphosphatidylinositol-anchored variant surface proteins","volume":"135","author":"Tabares","year":"2004","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1676","DOI":"10.1101\/gr.168955.113","article-title":"Genomic analysis of the causative agents of coccidiosis in domestic chickens","volume":"24","author":"Reid","year":"2014","journal-title":"Genome Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1038\/s42003-021-01904-w","article-title":"The structure of a major surface antigen SAG19 from Eimeria tenella unifies the Eimeria SAG family","volume":"4","author":"Ramly","year":"2021","journal-title":"Commun. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"12063","DOI":"10.1074\/jbc.M109.054866","article-title":"Structural and functional characterization of SporoSAG: A SAG2-related surface antigen from Toxoplasma gondii","volume":"285","author":"Crawford","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1083\/jcb.141.6.1323","article-title":"The Protozoan Parasite Toxoplasma gondii Targets Proteins to Dense Granules and the Vacuolar Space Using Both Conserved and Unusual Mechanisms","volume":"141","author":"Karsten","year":"1998","journal-title":"J. Cell Biol."},{"key":"ref_27","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_28","first-page":"1","article-title":"Eimeria tenella protein trafficking: Differential regulation of secretion versus surface tethering during the life cycle","volume":"7","author":"Long","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"45341","DOI":"10.1074\/jbc.M106665200","article-title":"A Conserved Subtilisin-like Protein TgSUB1 in Microneme Organelles of Toxoplasma gondii","volume":"276","author":"Miller","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1007\/BF00930743","article-title":"Ultrastructural localization of basic proteins on the conoid, rhoptries and micronemes of Toxoplasma gondii","volume":"56","year":"1978","journal-title":"Z Parasitenkd."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1083\/jcb.200112086","article-title":"A novel polymer of tubulin forms the conoid of Toxoplasma gondii","volume":"156","author":"Hu","year":"2002","journal-title":"J. Cell Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1493","DOI":"10.1016\/S0020-7519(00)00116-8","article-title":"Mapping and expression of microneme genes in Eimeria tenella","volume":"30","author":"Ryan","year":"2000","journal-title":"Int. J. Parasitol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/S0166-6851(00)00179-1","article-title":"A microneme protein from Eimeria tenella with homology to the Apple domains of coagulation factor XI and plasma pre-kallikrein","volume":"107","author":"Brown","year":"2000","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1046\/j.1365-2958.2001.02513.x","article-title":"TgM2AP participates in Toxoplasma gondii invasion of host cells and is tightly associated with the adhesive protein TgMIC2","volume":"41","author":"Rabenau","year":"2001","journal-title":"Mol. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"16891","DOI":"10.1074\/jbc.M702407200","article-title":"The Microneme Proteins EtMIC4 and EtMIC5 of Eimeria tenella Form a Novel, Ultra-high Molecular Mass Protein Complex That Binds Target Host Cells","volume":"282","author":"Periz","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Lai, L., Bumstead, J., Liu, Y., Garnett, J., Campanero-Rhodes, M.A., Blake, D., Palma, A.D.S., Chai, W., Ferguson, D., and Simpson, P. (2011). The Role of Sialyl Glycan Recognition in Host Tissue Tropism of the Avian Parasite Eimeria tenella. PLoS Pathog., 7.","DOI":"10.1371\/journal.ppat.1002296"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Clough, B., Wright, J.D., Pereira, P.M., Hirst, E.M., Johnston, A.C., Henriques, R., and Frickel, E.M. (2016). K63-Linked Ubiquitination Targets Toxoplasma gondii for Endo-lysosomal Destruction in IFNgamma-Stimulated Human Cells. PLoS Pathog., 12.","DOI":"10.1371\/journal.ppat.1006027"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1038\/nature05395","article-title":"Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue","volume":"445","author":"Saeij","year":"2006","journal-title":"Nature"},{"key":"ref_39","first-page":"84","article-title":"Functional Characterization of Rhoptry Kinome in the Virulent Toxoplasma gondii RH Strain","volume":"8","author":"Wang","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/978-0-387-78267-6_2","article-title":"Microneme Proteins in Apicomplexans","volume":"47","author":"Carruthers","year":"2008","journal-title":"Mol. Mech. Parasite Invasion"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/j.ijpara.2012.10.024","article-title":"The rhoptry proteome of Eimeria tenella sporozoites","volume":"43","author":"Oakes","year":"2012","journal-title":"Int. J. Parasitol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"e13027","DOI":"10.1111\/cmi.13027","article-title":"Eimeria tenella ROP kinase EtROP1 induces G0\/G1 cell cycle arrest and inhibits host cell apoptosis","volume":"21","author":"Diallo","year":"2019","journal-title":"Cell. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Talevich, E., and Kannan, N. (2013). Structural and evolutionary adaptation of rhoptry kinases and pseudokinases, a family of coccidian virulence factors. BMC Evol. Biol., 13.","DOI":"10.1186\/1471-2148-13-117"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1242\/jcs.021089","article-title":"Organellar dynamics during the cell cycle of Toxoplasma gondii","volume":"121","author":"Nishi","year":"2008","journal-title":"J. Cell Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1111\/tra.12556","article-title":"Intersection of endocytic and exocytic systems inToxoplasma gondii","volume":"19","author":"McGovern","year":"2018","journal-title":"Traffic"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Dogga, S.K., Mukherjee, B., Jacot, D., Kockmann, T., Molino, L., Hammoudi, P.-M., Hartkoorn, R.C., Hehl, A.B., and Soldati-Favre, D. (2017). A druggable secretory protein maturase of Toxoplasma essential for invasion and egress. eLife, 6.","DOI":"10.7554\/eLife.27480"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1046\/j.1462-5822.2002.00178.x","article-title":"Toxoplasma gondii Rab5 enhances cholesterol acquisition from host cells","volume":"4","author":"Robibaro","year":"2002","journal-title":"Cell. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.ijpara.2013.10.003","article-title":"Evolutionary repurposing of endosomal systems for apical organelle biogenesis in Toxoplasma gondii","volume":"44","author":"Tomavo","year":"2014","journal-title":"Int. J. Parasitol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Venugopal, K., Chehade, S., Werkmeister, E., Barois, N., Periz, J., Lafont, F., Tardieux, I., Khalife, J., Langsley, G., and Meissner, M. (2020). Rab11A regulates dense granule transport and secretion during Toxoplasma gondii invasion of host cells and parasite replication. PLoS Pathog., 16.","DOI":"10.1371\/journal.ppat.1008106"},{"key":"ref_50","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_51","doi-asserted-by":"crossref","first-page":"2424","DOI":"10.1074\/jbc.274.4.2424","article-title":"Constitutive Calcium-independent Release of Toxoplasma gondii Dense Granules Occurs through the NSF\/SNAP\/SNARE\/Rab Machinery","volume":"274","author":"Chaturvedi","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Bisio, H., Ben Chaabene, R., 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_53","doi-asserted-by":"crossref","first-page":"1166","DOI":"10.1111\/tra.12102","article-title":"Toxoplasma gondiiSyntaxin 6 Is Required for Vesicular Transport Between Endosomal-Like Compartments and the Golgi Complex","volume":"14","author":"Jackson","year":"2013","journal-title":"Traffic"},{"key":"ref_54","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_55","doi-asserted-by":"crossref","unstructured":"Pieperhoff, M.S., Schmitt, M., Ferguson, D.J.P., 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_56","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_57","doi-asserted-by":"crossref","first-page":"4551","DOI":"10.1091\/mbc.e06-01-0064","article-title":"A Cleavable Propeptide InfluencesToxoplasmaInfection by Facilitating the Trafficking and Secretion of the TgMIC2\u2013M2AP Invasion Complex","volume":"17","author":"Harper","year":"2006","journal-title":"Mol. Biol. Cell"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1128\/EC.00413-07","article-title":"Molecular signals in the trafficking of Toxoplasma gondii protein MIC3 to the micronemes","volume":"7","author":"Papoin","year":"2008","journal-title":"Eukaryot. Cell"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"2174","DOI":"10.1128\/EC.00163-06","article-title":"Targeted Deletion of MIC5 Enhances Trimming Proteolysis of Toxoplasma Invasion Proteins","volume":"5","author":"Brydges","year":"2006","journal-title":"Eukaryot. Cell"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1016\/S0020-7519(01)00242-9","article-title":"The pro region of Toxoplasma ROP1 is a rhoptry-targeting signal","volume":"31","author":"Bradley","year":"2001","journal-title":"Int. J. Parasitol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1485","DOI":"10.1111\/j.1600-0854.2008.00774.x","article-title":"The Prodomain ofToxoplasma gondiiGPI-Anchored Subtilase TgSUB1 Mediates its Targeting to Micronemes","volume":"9","author":"Binder","year":"2008","journal-title":"Traffic"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"7332","DOI":"10.1128\/MCB.20.19.7332-7341.2000","article-title":"Two conserved amino acid motifs mediate protein targeting to the micronemes of the apicomplexan parasite Toxoplasma gondii","volume":"20","author":"Spaccapelo","year":"2000","journal-title":"Mol. Cell. Biol."},{"key":"ref_63","first-page":"449","article-title":"Targeting to rhoptry organelles of Toxoplasma gondii involves evolutionarily conserved mechanisms","volume":"2","author":"Hoppe","year":"2000","journal-title":"Nature"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/S0962-8924(96)10057-X","article-title":"Protein sorting by tyrosine-based signals: Adapting to the Ys and wherefores","volume":"7","author":"Marks","year":"1997","journal-title":"Trends Cell Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1111\/j.1600-0854.2011.01192.x","article-title":"Forward Targeting of Toxoplasma gondii Proproteins to the Micronemes Involves Conserved Aliphatic Amino Acids","volume":"12","author":"Gaji","year":"2011","journal-title":"Traffic"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1111\/j.1462-5822.2004.00403.x","article-title":"Trans-genera reconstitution and complementation of an adhesion complex in Toxoplasma gondii","volume":"6","author":"Huynh","year":"2004","journal-title":"Cell. Microbiol."},{"key":"ref_67","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_68","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.ijpara.2018.01.003","article-title":"Development of cross-protective Eimeria-vectored vaccines based on apical membrane antigens","volume":"48","author":"Kim","year":"2018","journal-title":"Int. J. Parasitol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"294","DOI":"10.3389\/fcimb.2020.00294","article-title":"Toxoplasma gondii Mechanisms of Entry Into Host Cells","volume":"10","author":"Portes","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_70","first-page":"420","article-title":"Dynamics and 3D organization of secretory organelles of Toxoplasma gondii","volume":"177","author":"Attias","year":"2011","journal-title":"J. Struct. Biol."},{"key":"ref_71","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":"Dubremetz","year":"2017","journal-title":"Nat. Rev. Genet."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"25870","DOI":"10.1074\/jbc.M202553200","article-title":"Toxoplasma gondii microneme secretion involves intracellular Ca(2+) release from inositol 1,4,5-triphosphate (IP(3))\/ryanodine-sensitive stores","volume":"277","author":"Lovett","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Bullen, H.E., Bisio, H., and Soldati-Favre, D. (2019). The triumvirate of signaling molecules controlling Toxoplasma microneme exocytosis: Cyclic GMP, calcium, and phosphatidic acid. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1007670"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"e13018","DOI":"10.1111\/cmi.13018","article-title":"Biogenesis and secretion of micronemes inToxoplasma gondii","volume":"21","author":"Dubois","year":"2019","journal-title":"Cell. Microbiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"102368","DOI":"10.1016\/j.parint.2021.102368","article-title":"Toxoplasma gondii manipulates host cell signaling pathways via its secreted effector molecules","volume":"83","author":"Ihara","year":"2021","journal-title":"Parasitol. Int."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1242\/jcs.022350","article-title":"Microneme protein 8\u2014A new essential invasion factor in Toxoplasma gondii","volume":"121","author":"Kessler","year":"2008","journal-title":"J. Cell Sci."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1038\/s41564-020-00854-z","article-title":"An Alveolata secretory machinery adapted to parasite host cell invasion","volume":"6","author":"Aquilini","year":"2021","journal-title":"Nat. Microbiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-019-11979-z","article-title":"A lipid-binding protein mediates rhoptry discharge and invasion in Plasmodium falciparum and Toxoplasma gondii parasites","volume":"10","author":"Suarez","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"e01510-18","DOI":"10.1128\/mBio.01510-18","article-title":"A Member of the Ferlin Calcium Sensor Family Is Essential for Toxoplasma gondii Rhoptry Secretion","volume":"9","author":"Coleman","year":"2018","journal-title":"mBio"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"3132","DOI":"10.1093\/emboj\/20.12.3132","article-title":"Toxoplasma evacuoles: A two-step process of secretion and fusion forms the parasitophorous vacuole","volume":"20","author":"Charron","year":"2001","journal-title":"EMBO J."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/S0022-5320(83)90067-9","article-title":"Secretion from the Rhoptries of Toxoplasma gondii during host-cell invasion","volume":"83","author":"Nichols","year":"1983","journal-title":"J. Ultrastruct. Res."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1016\/j.pt.2021.04.011","article-title":"Unraveling the Elusive Rhoptry Exocytic Mechanism of Apicomplexa","volume":"37","author":"Sparvoli","year":"2021","journal-title":"Trends Parasitol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.micron.2007.01.002","article-title":"Freeze-fracture study of the dynamics of Toxoplasma gondii parasitophorous vacuole development","volume":"39","author":"Lemgruber","year":"2008","journal-title":"Micron"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1016\/j.ijpara.2005.03.011","article-title":"Dense granules: Are they key organelles to help understand the parasitophorous vacuole of all Apicomplexa parasites?","volume":"35","author":"Mercier","year":"2005","journal-title":"Int. J. Parasitol."},{"key":"ref_85","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_86","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_87","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_88","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/j.chom.2013.03.002","article-title":"Host Cell Subversion by Toxoplasma GRA16, an Exported Dense Granule Protein that Targets the Host Cell Nucleus and Alters Gene Expression","volume":"13","author":"Bougdour","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_89","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_90","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1111\/j.1600-0854.2008.00713.x","article-title":"Protein Trafficking inside Toxoplasma gondii","volume":"9","author":"Sheiner","year":"2008","journal-title":"Traffic"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"588","DOI":"10.1007\/BF00933007","article-title":"Ultrastructural observations of development of Eimeria tenella in a novel established avian-derived cell line","volume":"80","author":"Danforth","year":"1994","journal-title":"Parasitol. Res."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"109480","DOI":"10.1016\/j.vetpar.2021.109480","article-title":"Full-length transcriptome sequence analysis of Eimeria necatrix unsporulated oocysts and sporozoites identifies genes involved in cellular invasion","volume":"296","author":"Gao","year":"2021","journal-title":"Veter- Parasitol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"4566","DOI":"10.1002\/pmic.200900305","article-title":"Proteomic comparison of four Eimeria tenella life-cycle stages: Unsporulated oocyst, sporulated oocyst, sporozoite and second-generation merozoite","volume":"9","author":"Lal","year":"2009","journal-title":"Proteomics"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"579833","DOI":"10.3389\/fcimb.2020.579833","article-title":"The Growth of Eimeria tenella: Characterization and Application of Quantitative Methods to Assess Sporozoite Invasion and Endogenous Development in Cell Culture","volume":"10","author":"Jeremiah","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41421-018-0023-4","article-title":"Lipid analysis of Eimeria sporozoites reveals exclusive phospholipids, a phylogenetic mosaic of endogenous synthesis, and a host-independent lifestyle","volume":"4","author":"Kong","year":"2018","journal-title":"Cell Discov."},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Hehl, A.B., Basso, W.U., Lippuner, C., Ramakrishnan, C., Okoniewski, M., Walker, A.R., Grigg, E.M., Smith, N.C., and Deplazes, P. (2015). Asexual expansion of Toxoplasma gondii merozoites is distinct from tachyzoites and entails expression of non-overlapping gene families to attach, invade, and replicate within feline enterocytes. BMC Genom., 16.","DOI":"10.1186\/s12864-015-1225-x"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1006\/expr.1998.4384","article-title":"The expression and distribution of dense granule proteins in the enteric (Coccidian) forms of Toxoplasma gondii in the small intestine of the cat","volume":"91","author":"Ferguson","year":"1999","journal-title":"Exp. Parasitol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1017\/S0031182099004692","article-title":"In vivo expression and distribution of dense granule protein 7 (GRA7) in the exoenteric (tachyzoite, bradyzoite) and enteric (coccidian) forms of Toxoplasma gondii","volume":"119","author":"Ferguson","year":"1999","journal-title":"Parasitology"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/j.ijpara.2017.04.001","article-title":"The merozoite-specific protein, TgGRA11B, identified as a component of the Toxoplasma gondii parasitophorous vacuole in a tachyzoite expression model","volume":"47","author":"Ramakrishnan","year":"2017","journal-title":"Int. J. Parasitol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"srep42746","DOI":"10.1038\/srep42746","article-title":"Mitochondrial behaviour throughout the lytic cycle of Toxoplasma gondii","volume":"7","author":"Ovciarikova","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"398","DOI":"10.2307\/3277421","article-title":"Morphological Changes in Eimeria bovis Sporozoites during Their First Day in Cultured Mammalian Cells","volume":"55","author":"Fayer","year":"1969","journal-title":"J. Parasitol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1111\/j.1550-7408.1969.tb02323.x","article-title":"Development of Eimeria auburnensis in Cell Cultures","volume":"16","author":"Clark","year":"1969","journal-title":"J. Protozool."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1111\/j.1550-7408.1970.tb05161.x","article-title":"Ultrastructural and Cytologic Studies of the Sporozoites of Four Eimeria Species","volume":"17","author":"Roberts","year":"1970","journal-title":"J. Protozool."},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Carmeille, R., Lomoriello, P.S., Devarakonda, P.M., Kellermeier, J.A., and Heaslip, A.T. (2021). Actin and an unconventional myosin motor, TgMyoF, control the organization and dynamics of the endomembrane network in Toxoplasma gondii. PLoS Pathog., 17.","DOI":"10.1371\/journal.ppat.1008787"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0014-4894(89)90002-7","article-title":"Eimeria tenella: Use of a monoclonal antibody in determining the intracellular fate of the refractile body organelles and the effect on in vitro development","volume":"68","author":"Danforth","year":"1989","journal-title":"Exp. Parasitol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.1016\/S0020-7519(00)00099-0","article-title":"Differential localisation of an Eimeria tenella aspartyl proteinase during the infection process","volume":"30","author":"Jean","year":"2000","journal-title":"Int. J. Parasitol."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"1107","DOI":"10.1645\/GE-1171R.1","article-title":"Characterization of the antigen so7 during development of eimeria tenella","volume":"93","author":"Fetterer","year":"2007","journal-title":"J. Parasitol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1399","DOI":"10.1016\/j.ijpara.2006.06.018","article-title":"Study of proteins associated with the Eimeria tenella refractile body by a proteomic approach","volume":"36","author":"Faigle","year":"2006","journal-title":"Int. J. Parasitol."},{"key":"ref_109","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_110","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-019-11855-w","article-title":"A CRISPR platform for targeted in vivo screens identifies Toxoplasma gondii virulence factors in mice","volume":"10","author":"Young","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S0031182000049775","article-title":"Eimeria tenella: Immunogenicity of the first generation of schizogony","volume":"93","author":"McDonald","year":"1986","journal-title":"Parasitology"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1111\/j.1365-3024.1988.tb00251.x","article-title":"Eimeria tenella: Immunological diversity between asexual generations","volume":"10","author":"McDonald","year":"1988","journal-title":"Parasite Immunol."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"4042","DOI":"10.1128\/iai.59.11.4042-4048.1991","article-title":"X-irradiation of Eimeria tenella oocysts provides direct evidence that sporozoite invasion and early schizont development induce a protective immune response(s)","volume":"59","author":"Jenkins","year":"1991","journal-title":"Infect. Immun."}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/11\/9\/909\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:53:35Z","timestamp":1760165615000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/11\/9\/909"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,31]]},"references-count":113,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["life11090909"],"URL":"https:\/\/doi.org\/10.3390\/life11090909","relation":{},"ISSN":["2075-1729"],"issn-type":[{"value":"2075-1729","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,31]]}}}