Expansion microscopy of apicomplexan parasites.
Cryptosporidium
Plasmodium
Toxoplasma
U-ExM
cytoskeleton
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
11 Aug 2023
11 Aug 2023
Historique:
revised:
15
07
2023
received:
24
06
2023
accepted:
20
07
2023
medline:
12
8
2023
pubmed:
12
8
2023
entrez:
12
8
2023
Statut:
aheadofprint
Résumé
Apicomplexan parasites comprise significant pathogens of humans, livestock and wildlife, but also represent a diverse group of eukaryotes with interesting and unique cell biology. The study of cell biology in apicomplexan parasites is complicated by their small size, and historically this has required the application of cutting-edge microscopy techniques to investigate fundamental processes like mitosis or cell division in these organisms. Recently, a technique called expansion microscopy has been developed, which rather than increasing instrument resolution like most imaging modalities, physically expands a biological sample. In only a few years since its development, a derivative of expansion microscopy known as ultrastructure-expansion microscopy (U-ExM) has been widely adopted and proven extremely useful for studying cell biology of Apicomplexa. Here, we review the insights into apicomplexan cell biology that have been enabled through the use of U-ExM, with a specific focus on Plasmodium, Toxoplasma and Cryptosporidium. Further, we summarize emerging expansion microscopy modifications and modalities and forecast how these may influence the field of parasite cell biology in future.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : American Heart Association
ID : 23POST1011626
Informations de copyright
© 2023 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.
Références
Alon, S., Goodwin, D.R., Sinha, A., Wassie, A.T., Chen, F., Daugharthy, E.R. et al. (2021) Expansion sequencing: spatially precise in situ transcriptomics in intact biological systems. Science, 371(6528), eaax2656.
Ambekar, S.V. (2022) Guardians of the Plasmodium nuclear galaxy: identification and characterization of Plasmodium berghei nuclear pore proteins PhD. Ames, IA: Iowa State University.
Amino, R., Thiberge, S., Martin, B., Celli, S., Shorte, S., Frischknecht, F. et al. (2006) Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nature Medicine, 12(2), 220-224.
Antunes, A.V., Shahinas, M., Swale, C., Farhat, D.C., Ramakrishnan, C., Bruley, C. et al. (2023) In vitro production of cat-restricted Toxoplasma pre-sexual stages by epigenetic reprogramming. bioRxiv. 2023.2001.2016.524187.
Araki, T., Kawai, S., Kakuta, S., Kobayashi, H., Umeki, Y., Saito-Nakano, Y. et al. (2020) Three-dimensional electron microscopy analysis reveals endopolygeny-like nuclear architecture segregation in Plasmodium oocyst development. Parasitology International, 76, 102034.
Atchou, K., Berger, B.M., Heussler, V. & Ochsenreiter, T. (2023) Pre-gelation staining expansion microscopy (PS-ExM) for visualization of the Plasmodium liver stage. bioRxiv. 2023.2005.2024.542037.
Bertiaux, E., Balestra, A.C., Bournonville, L., Louvel, V., Maco, B., Soldati-Favre, D. et al. (2021) Expansion microscopy provides new insights into the cytoskeleton of malaria parasites including the conservation of a conoid. PLoS Biology, 19(3), e3001020.
Brusini, L., Dos Santos Pacheco, N., Tromer, E.C., Soldati-Favre, D. & Brochet, M. (2022) Composition and organization of kinetochores show plasticity in apicomplexan chromosome segregation. Journal of Cell Biology, 221(9), e202111084.
Burki, F., Roger, A.J., Brown, M.W. & Simpson, A.G.B. (2020) The new tree of eukaryotes. Trends in Ecology & Evolution, 35(1), 43-55.
Calla, J., Mittal, N., LaMonte, G., Liffner, B., Godinez-Macias, K.P., Carolino, K. et al. (2023) Plasmodium exoerythrocytic parasites redirect trafficking of human proteins to the parasitophorous vacuole. bioRxiv. 2022.2011.2022.517223.
Campbell, B.C., Paez-Segala, M.G., Looger, L.L., Petsko, G.A. & Liu, C.F. (2022) Chemically stable fluorescent proteins for advanced microscopy. Nature Methods, 19(12), 1612-1621.
Carruthers, V. & Boothroyd, J.C. (2007) Pulling together: an integrated model of Toxoplasma cell invasion. Current Opinion in Microbiology, 10(1), 83-89.
Chang, T.-J.B., Hsu, J.C.-C. & Yang, T.T. (2023) Single-molecule localization microscopy reveals the ultrastructural constitution of distal appendages in expanded mammalian centrioles. Nature Communications, 14(1), 1688.
Chen, F., Tillberg, P.W. & Boyden, E.S. (2015) Expansion microscopy. Science, 347(6221), 543-548.
Chen, F., Wassie, A.T., Cote, A.J., Sinha, A., Alon, S., Asano, S. et al. (2016) Nanoscale imaging of RNA with expansion microscopy. Nature Methods, 13(8), 679-684.
Choudhary, H.H., Nava, M.G., Gartlan, B.E., Rose, S. & Vinayak, S. (2020) A conditional protein degradation system to study essential gene function in Cryptosporidium parvum. mBio, 11(4), e01231-20. Available from: https://doi.org/10.1128/mbio.01231-01220
Christoforou, A., Mulvey, C.M., Breckels, L.M., Geladaki, A., Hurrell, T., Hayward, P.C. et al. (2016) A draft map of the mouse pluripotent stem cell spatial proteome. Nature Communications, 7, 8992.
Considine, R.F., Dixon, D.R. & Drummond, C.J. (2000) Laterally-resolved force microscopy of biological microspheres oocysts of Cryptosporidium parvum. Langmuir, 16(3), 1323-1330.
Cowman, A.F., Berry, D. & Baum, J. (2012) The cellular and molecular basis for malaria parasite invasion of the human red blood cell. Journal of Cell Biology, 198(6), 961-971.
Cowman, A.F., Healer, J., Marapana, D. & Marsh, K. (2016) Malaria: biology and disease. Cell, 167(3), 610-624.
Cyrklaff, M., Frischknecht, F. & Kudryashev, M. (2017) Functional insights into pathogen biology from 3D electron microscopy. FEMS Microbiology Reviews, 41(6), 828-853.
Damstra, H.G.J., Mohar, B., Eddison, M., Akhmanova, A., Kapitein, L.C. & Tillberg, P.W. (2022) Visualizing cellular and tissue ultrastructure using ten-fold robust expansion microscopy (TREx). eLife, 11, e73775.
Dash, M., Sachdeva, S., Bansal, A. & Sinha, A. (2022) Gametogenesis in Plasmodium: delving deeper to connect the dots. Frontiers in Cellular and Infection Microbiology, 12.
Dave, N., LaFavers, K. & Arrizabalaga, G. (2022) The dually localized EF-hand domain-containing protein TgEFP1 regulates the lytic cycle of Toxoplasma gondii. Cells, 11(10), 1709.
Del Rosario, M., Periz, J., Pavlou, G., Lyth, O., Latorre-Barragan, F., Das, S. et al. (2019) Apicomplexan F-Actin is required for efficient nuclear entry during host cell invasion. EMBO Reports, 20(12), e48896.
Dos Santos Pacheco, N., Brusini, L., Haase, R., Tosetti, N., Maco, B., Brochet, M. et al. (2022) Conoid extrusion regulates glideosome assembly to control motility and invasion in Apicomplexa. Nature Microbiology, 7(11), 1777-1790.
Dos Santos Pacheco, N., Tosetti, N., Koreny, L., Waller, R.F. & Soldati-Favre, D. (2020) Evolution, composition, assembly, and function of the conoid in Apicomplexa. Trends in Parasitology, 36(8), 688-704.
Dvorin, J.D. & Goldberg, D.E. (2022) Plasmodium egress across the parasite life cycle. Annual Review of Microbiology, 76(1), 67-90.
Eappen, A.G., Li, T., Marquette, M., Chakravarty, S., Kc, N., Zanghi, G. et al. (2022) In vitro production of infectious Plasmodium falciparum sporozoites. Nature, 612(7940), 534-539.
Engelberg, K., Bechtel, T., Michaud, C., Weerapana, E. & Gubbels, M.-J. (2022) Proteomic characterization of the Toxoplasma gondii cytokinesis machinery portrays an expanded hierarchy of its assembly and function. Nature Communications, 13(1), 4644.
English, E.D., Guérin, A., Tandel, J. & Striepen, B. (2022) Live imaging of the Cryptosporidium parvum life cycle reveals direct development of male and female gametes from type I meronts. PLoS Biology, 20(4), e3001604.
Ferreira, J.L., Pražák, V., Vasishtan, D., Siggel, M., Hentzschel, F., Binder, A.M. et al. (2023) Variable microtubule architecture in the malaria parasite. Nature Communications, 14(1), 1216.
Frischknecht, F. & Matuschewski, K. (2017) Plasmodium sporozoite biology. Cold Spring Harbor Perspectives in Medicine, 7(5), a025478.
Gambarotto, D., Zwettler, F.U., Le Guennec, M., Schmidt-Cernohorska, M., Fortun, D., Borgers, S. et al. (2019) Imaging cellular ultrastructures using expansion microscopy (U-ExM). Nature Methods, 16(1), 71-74.
Gerald, N., Mahajan, B. & Kumar, S. (2011) Mitosis in the human malaria parasite Plasmodium falciparum. Eukaryotic Cell, 10(4), 474-482.
Ghosh, S. (2022) From coast to coast and beyond. Heidelberg, Germany: EMBLetc.
Gras, S., Jimenez-Ruiz, E., Klinger, C.M., Schneider, K., Klingl, A., Lemgruber, L. et al. (2019) An endocytic-secretory cycle participates in Toxoplasma gondii in motility. PLoS Biology, 17(6), e3000060.
Grassi, G.B. (1901) Studi di uno zoologo sulla malaria. Rome: R. Accademia dei Lincei.
Gubbels, M.-J., Coppens, I., Zarringhalam, K., Duraisingh, M.T. & Engelberg, K. (2021) The modular circuitry of apicomplexan cell division plasticity. Frontiers in Cellular and Infection Microbiology, 11.
Gubbels, M.J., Keroack, C.D., Dangoudoubiyam, S., Worliczek, H.L., Paul, A.S., Bauwens, C. et al. (2020) Fussing about fission: defining variety among mainstream and exotic apicomplexan cell division modes. Frontiers in Cellular and Infection Microbiology, 10, 269.
Guérin, A., Roy, N.H., Kugler, E.M., Berry, L., Burkhardt, J.K., Shin, J.-B. et al. (2021) Cryptosporidium rhoptry effector protein ROP1 injected during invasion targets the host cytoskeletal modulator LMO7. Cell Host & Microbe, 29(9), 1407-1420.e1405.
Guérin, A., Strelau, K.M., Barylyuk, K., Wallbank, B.A., Berry, L., Crook, O.M. et al. (2023) Cryptosporidium uses multiple distinct secretory organelles to interact with and modify its host cell. Cell Host & Microbe, 31, 650-664.e6.
Guérin, A. & Striepen, B. (2020) The biology of the intestinal intracellular parasite Cryptosporidium. Cell Host & Microbe, 28(4), 509-515.
Guttery, D.S., Roques, M., Holder, A.A. & Tewari, R. (2015) Commit and transmit: molecular players in Plasmodium sexual development and zygote differentiation. Trends in Parasitology, 31(12), 676-685.
Hanssen, E., Dekiwadia, C., Riglar, D.T., Rug, M., Lemgruber, L., Cowman, A.F. et al. (2013) Electron tomography of Plasmodium falciparum merozoites reveals core cellular events that underpin erythrocyte invasion. Cellular Microbiology, 15(9), 1457-1472.
Hanssen, E., Knoechel, C., Klonis, N., Abu-Bakar, N., Deed, S., LeGros, M. et al. (2011) Cryo transmission X-ray imaging of the malaria parasite, P. falciparum. Journal of Structural Biology, 173(1), 161-168.
Heo, I., Dutta, D., Schaefer, D.A., Iakobachvili, N., Artegiani, B., Sachs, N. et al. (2018) Modelling Cryptosporidium infection in human small intestinal and lung organoids. Nature Microbiology, 3(7), 814-823.
Hill, D. & Dubey, J.P. (2002) Toxoplasma gondii: transmission, diagnosis and prevention. Clinical Microbiology and Infection, 8(10), 634-640.
Jacobs, K., Charvat, R. & Arrizabalaga, G. (2020) Identification of Fis1 interactors in Toxoplasma gondii reveals a novel protein required for peripheral distribution of the mitochondrion. mBio, 11(1), e02732-19.
Jaskiewicz, J.J., Sandlin, R.D., Swei, A.A., Widmer, G., Toner, M. & Tzipori, S. (2018) Cryopreservation of infectious Cryptosporidium parvum oocysts. Nature Communications, 9(1), 2883.
John, A., Bader, S.M., Madiedo Soler, N., Wiradiputri, K., Tichkule, S., Smyth, S.T. et al. (2023) Conservation, abundance, glycosylation profile, and localization of the TSP protein family in Cryptosporidium parvum. Journal of Biological Chemistry, 299(3), 103006.
Josling, G.A. & Llinás, M. (2015) Sexual development in Plasmodium parasites: knowing when it's time to commit. Nature Reviews Microbiology, 13(9), 573-587.
Kafsack, B.F.C., Rovira-Graells, N., Clark, T.G., Bancells, C., Crowley, V.M., Campino, S.G. et al. (2014) A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature, 507(7491), 248-252.
Klimas, A., Gallagher, B.R., Wijesekara, P., Fekir, S., DiBernardo, E.F., Cheng, Z. et al. (2023) Magnify is a universal molecular anchoring strategy for expansion microscopy. Nature Biotechnology, 41(6), 858-869.
Laveran, A. (1881) Un nouveau parasite trouvé dans le sang des malades atteints de fièvre palustre: origine parasitaire des accidents de l'impaludisme. Paris: J.-B. Baillière.
Lentini, G., Ben Chaabene, R., Vadas, O., Ramakrishnan, C., Mukherjee, B., Mehta, V. et al. (2021) Structural insights into an atypical secretory pathway kinase crucial for Toxoplasma gondii invasion. Nature Communications, 12(1), 3788.
Li, J., Shami, G.J., Cho, E., Liu, B., Hanssen, E., Dixon, M.W.A. et al. (2022) Repurposing the mitotic machinery to drive cellular elongation and chromatin reorganisation in Plasmodium falciparum gametocytes. Nature Communications, 13(1), 5054.
Li, L., Sun, C., Sun, Y., Dong, Z., Wu, R., Sun, X. et al. (2022) Spatially resolved proteomics via tissue expansion. Nature Communications, 13(1), 7242.
Li, Z., Du, W., Yang, J., Lai, D.H., Lun, Z.R. & Guo, Q. (2023) Cryo-electron tomography of Toxoplasma gondii indicates that the conoid fiber may be derived from microtubules. Advanced Science, 10(14), e2206595.
Liffner, B. & Absalon, S. (2021) Expansion microscopy reveals Plasmodium falciparum blood-stage parasites undergo anaphase with a chromatin bridge in the absence of mini-chromosome maintenance complex binding protein. Microorganisms, 9(11), 2306.
Liffner, B., Balbin, J.M., Shami, G.J., Siddiqui, G., Strauss, J., Frölich, S. et al. (2022) Cell biological analysis reveals an essential role for Pfcerli2 in erythrocyte invasion by malaria parasites. Communications Biology, 5(1), 121.
Liffner, B., Cepeda Diaz, A.K., Blauwkamp, J., Anaguano, D., Frölich, S., Muralidharan, V. et al. (2023) Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy. eLife, 12, RP88088.
Loubens, M., Marinach, C., Paquereau, C.-E., Hamada, S., Hoareau-Coudert, B., Akbar, D. et al. (2023) The claudin-like apicomplexan microneme protein is required for gliding motility and infectivity of Plasmodium sporozoites. PLoS Pathogens, 19(3), e1011261.
Lourido, S. (2019) Toxoplasma gondii. Trends in Parasitology, 35(11), 944-945.
Louvel, V., Haase, R., Mercey, O., Laporte, M.H., Soldati-Favre, D., Hamel, V. et al. (2022) Nanoscopy of organelles and tissues with iterative ultrastructure expansion microscopy (iU-ExM). bioRxiv. 2022.2011.2014.516383.
Lyons, R.E., McLeod, R. & Roberts, C.W. (2002) Toxoplasma gondii tachyzoite-bradyzoite interconversion. Trends in Parasitology, 18(5), 198-201.
Maccallum, W.G. (1897) On the flagellated form of the malarial parasite. The Lancet, 150(3872), 1240-1241.
Mageswaran, S.K., Guérin, A., Theveny, L.M., Chen, W.D., Martinez, M., Lebrun, M. et al. (2021) In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems. Nature Communications, 12(1), 4983.
Martorelli Di Genova, B. & Knoll, L.J. (2020) Comparisons of the sexual cycles for the coccidian parasites Eimeria and Toxoplasma. Frontiers in Cellular and Infection Microbiology, 10, 604897.
Matsuoka, H., Yoshida, S., Hirai, M. & Ishii, A. (2002) A rodent malaria, Plasmodium berghei, is experimentally transmitted to mice by merely probing of infective mosquito, Anopheles stephensi. Parasitology International, 51(1), 17-23.
Matthews, H., Duffy, C.W. & Merrick, C.J. (2018) Checks and balances? DNA replication and the cell cycle in Plasmodium. Parasites & Vectors, 11(1), 216.
Matz, J.M. (2022) Plasmodium's bottomless pit: properties and functions of the malaria parasite's digestive vacuole. Trends in Parasitology, 38(7), 525-543.
Mehnert, A.-K., Simon, C.S. & Guizetti, J. (2019) Immunofluorescence staining protocol for STED nanoscopy of Plasmodium-infected red blood cells. Molecular and Biochemical Parasitology, 229, 47-52.
Millholland, M.G., Chandramohanadas, R., Pizzarro, A., Wehr, A., Shi, H., Darling, C. et al. (2011) The malaria parasite progressively dismantles the host erythrocyte cytoskeleton for efficient egress. Molecular & Cellular Proteomics, 10(12), M111.010678.
Montano, H., Anandkrishnan, R., Carruthers, V.B. & Gaji, R.Y. (2022) TgTKL4 is a novel kinase that plays an important role in Toxoplasma morphology and fitness. mSphere, 8, e00649-00622.
Morano, A.A., Rudlaff, R.M. & Dvorin, J.D. (2023) A PPP-type pseudophosphatase is required for the maintenance of basal complex integrity in Plasmodium falciparum. Nature Communications, 14(1), 3916.
Morrissette, N.S. & Sibley, L.D. (2002) Cytoskeleton of apicomplexan parasites. Microbiology and Molecular Biology Reviews, 66(1), 21-38.
M'Saad, O. & Bewersdorf, J. (2020) Light microscopy of proteins in their ultrastructural context. Nature Communications, 11(1), 3850.
Mueller, A.-K., Kohlhepp, F., Hammerschmidt, C. & Michel, K. (2010) Invasion of mosquito salivary glands by malaria parasites: prerequisites and defense strategies. International Journal for Parasitology, 40(11), 1229-1235.
Nanda, J.S. & Lorsch, J.R. (2014) Labeling a protein with fluorophores using NHS ester derivitization. Methods in Enzymology, 536, 87-94.
Neveu, G., Beri, D. & Kafsack, B.F.C. (2020) Metabolic regulation of sexual commitment in Plasmodium falciparum. Current Opinion in Microbiology, 58, 93-98.
Oliveira Souza, R.O., Jacobs, K.N., Back, P.S., Bradley, P.J. & Arrizabalaga, G. (2022) IMC10 and LMF1 mediate mitochondrial morphology through mitochondrion-pellicle contact sites in Toxoplasma gondii. Journal of Cell Science, 135(22), jcs260083.
Pacheco, N.D.S., Tosetti, N., Krishnan, A., Haase, R., Maco, B., Suarez, C. et al. (2021) Revisiting the role of Toxoplasma gondii ERK7 in the maintenance and stability of the apical complex. MBio, 12(5), e02057-02021.
Patterson, D.J. (1999) The diversity of eukaryotes. The American Naturalist, 154(S4), S96-s124.
Pavlou, G., Touquet, B., Vigetti, L., Renesto, P., Bougdour, A., Debarre, D. et al. (2020) Coupling polar adhesion with traction, spring, and torque forces allows high-speed helical migration of the protozoan parasite Toxoplasma. ACS Nano, 14(6), 7121-7139.
Prudêncio, M., Rodriguez, A. & Mota, M.M. (2006) The silent path to thousands of merozoites: the Plasmodium liver stage. Nature Reviews Microbiology, 4(11), 849-856.
Qian, P., Wang, X., Guan, C., Fang, X., Cai, M., Zhong, C.-Q. et al. (2022) Apical anchorage and stabilization of subpellicular microtubules by apical polar ring ensures Plasmodium ookinete infection in mosquito. Nature Communications, 13(1), 7465.
Qian, P., Wang, X., Zhong, C.-Q., Wang, J., Cai, M., Nguitragool, W. et al. (2022) Inner membrane complex proteomics reveals a palmitoylation regulation critical for intraerythrocytic development of malaria parasite. eLife, 11, e77447.
Rashpa, R. & Brochet, M. (2022) Expansion microscopy of Plasmodium gametocytes reveals the molecular architecture of a bipartite microtubule organisation centre coordinating mitosis with axoneme assembly. PLoS Pathogens, 18(1), e1010223.
Rashpa, R., Klages, N., Schvartz, D., Pasquarello, C. & Brochet, M. (2023) The Skp1-Cullin1-FBXO1 complex is a pleiotropic regulator required for the formation of gametes and motile forms in Plasmodium berghei. Nature Communications, 14(1), 1312.
Riglar, D.T., Richard, D., Wilson, D.W., Boyle, M.J., Dekiwadia, C., Turnbull, L. et al. (2011) Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host & Microbe, 9(1), 9-20.
Riglar, D.T., Rogers, K.L., Hanssen, E., Turnbull, L., Bullen, H.E., Charnaud, S.C. et al. (2013) Spatial association with PTEX complexes defines regions for effector export into Plasmodium falciparum-infected erythrocytes. Nature Communications, 4(1), 1415.
Roques, M., Bindschedler, A., Beyeler, R. & Heussler, V.T. (2023) Same, same but different: exploring Plasmodium cell division during liver stage development. PLoS Pathogens, 19(3), e1011210.
Ross, R. (1898) The role of the mosquito in the evolution of the malarial parasite. The Lancet, 152(3912), 488-490.
Rudlaff, R.M., Kraemer, S., Marshman, J. & Dvorin, J.D. (2020) Three-dimensional ultrastructure of Plasmodium falciparum throughout cytokinesis. PLoS Pathogens, 16(6), e1008587.
Rudlaff, R.M., Kraemer, S., Streva, V.A. & Dvorin, J.D. (2019) An essential contractile ring protein controls cell division in Plasmodium falciparum. Nature Communications, 10(1), 2181.
Sanchez, C.P., Karathanasis, C., Sanchez, R., Cyrklaff, M., Jäger, J., Buchholz, B. et al. (2019) Single-molecule imaging and quantification of the immune-variant adhesin VAR2CSA on knobs of Plasmodium falciparum-infected erythrocytes. Communications Biology, 2(1), 172.
Sateriale, A., Šlapeta, J., Baptista, R., Engiles, J.B., Gullicksrud, J.A., Herbert, G.T. et al. (2019) A genetically tractable, natural mouse model of cryptosporidiosis offers insights into host protective immunity. Cell Host & Microbe, 26(1), 135-146.e135.
Schaudinn, F. (1903) Studien über krankheitserregende Protozoen. II, Plasmodium vivax (Grassi & Feletti), der Erreger des Tertianfiebers beim Menschen/von Fritz Schaudinn. Berlin: Springer.
Schloetel, J.-G., Heine, J., Cowman, A.F. & Pasternak, M. (2019) Guided STED nanoscopy enables super-resolution imaging of blood stage malaria parasites. Scientific Reports, 9(1), 4674.
Segev-Zarko, L.-A., Dahlberg, P.D., Sun, S.Y., Pelt, D.M., Kim, C.Y., Egan, E.S. et al. (2022) Cryo-electron tomography with mixed-scale dense neural networks reveals key steps in deployment of Toxoplasma invasion machinery. PNAS Nexus, 1(4), pgac183.
Severo, V., Souza, R., Vitorino, F., Cunha, J., Ávila, A., Arrizabalaga, G. et al. (2022) Previously unidentified histone H1-like protein is involved in cell division and ribosome biosynthesis in Toxoplasma gondii. mSphere, 7(6), e0040322.
Shaib, A.H., Chouaib, A.A., Chowdhury, R., Mihaylov, D., Zhang, C., Imani, V. et al. (2023) Visualizing proteins by expansion microscopy. bioRxiv. 2022.2008.2003.502284.
Shortt, H.E., Fairley, N.H., Covell, G., Shute, P.G. & Garnham, P.C.C. (1949) The pre-erythrocytic stage of Plasmodium falciparum; a preliminary note. British Medical Journal, 2(4635), 1006-1008.
Shute, P.G. (1943) Successful transmission of human malaria with sporozoites which have not come into contact with the salivary glands of the insect host. Journal of Tropical Medicine and Hygiene, 46(5), 57-58.
Sibley, L.D. (2010) How apicomplexan parasites move in and out of cells. Current Opinion in Biotechnology, 21(5), 592-598.
Simon, C.S., Funaya, C., Bauer, J., Voβ, Y., Machado, M., Penning, A. et al. (2021) An extended DNA-free intranuclear compartment organizes centrosome microtubules in malaria parasites. Life Science Alliance, 4(11), e202101199.
Smith, T.G., Walliker, D. & Ranford-Cartwright, L.C. (2002) Sexual differentiation and sex determination in the Apicomplexa. Trends in Parasitology, 18(7), 315-323.
Sparvoli, D., Delabre, J., Penarete-Vargas, D.M., Kumar Mageswaran, S., Tsypin, L.M., Heckendorn, J. et al. (2022) An apical membrane complex for triggering rhoptry exocytosis and invasion in Toxoplasma. The EMBO Journal, 41(22), e111158.
Stelzer, E.H.K., Strobl, F., Chang, B.-J., Preusser, F., Preibisch, S., McDole, K. et al. (2021) Light sheet fluorescence microscopy. Nature Reviews Methods Primers, 1(1), 73.
Sun, S.Y., Segev-Zarko, L.-A., Chen, M., Pintilie, G.D., Schmid, M.F., Ludtke, S.J. et al. (2022) Cryo-ET of Toxoplasma parasites gives subnanometer insight into tubulin-based structures. Proceedings of the National Academy of Sciences, 119(6), e2111661119.
Tandel, J., English, E.D., Sateriale, A., Gullicksrud, J.A., Beiting, D.P., Sullivan, M.C. et al. (2019) Life cycle progression and sexual development of the apicomplexan parasite Cryptosporidium parvum. Nature Microbiology, 4(12), 2226-2236.
Tenter, A.M., Heckeroth, A.R. & Weiss, L.M. (2000) Toxoplasma gondii: from animals to humans. International Journal for Parasitology, 30(12), 1217-1258.
Tomasina, R., Gonzalez, F.C., Martins-Duarte, É.S., Bastin, P., Gissot, M. & Francia, M.E. (2022) Separate to operate: the centriole-free inner Core of the centrosome regulates the assembly of the intranuclear spindle in Toxoplasma gondii. mBio, 13(5), e01859-01822.
Tosetti, N., Dos Santos Pacheco, N., Bertiaux, E., Maco, B., Bournonville, L., Hamel, V. et al. (2020) Essential function of the alveolin network in the subpellicular microtubules and conoid assembly in Toxoplasma gondii. eLife, 9, e56635.
Truckenbrodt, S., Maidorn, M., Crzan, D., Wildhagen, H., Kabatas, S. & Rizzoli, S.O. (2018) X10 expansion microscopy enables 25-nm resolution on conventional microscopes. EMBO Reports, 19(9), e45836.
Vinayak, S., Pawlowic, M.C., Sateriale, A., Brooks, C.F., Studstill, C.J., Bar-Peled, Y. et al. (2015) Genetic modification of the diarrhoeal pathogen Cryptosporidium parvum. Nature, 523(7561), 477-480.
Vinetz, J.M. (2005) Plasmodium ookinete invasion of the mosquito midgut. In: Compans, R.W., Cooper, M.D., Honjo, T., Koprowski, H., Melchers, F., Oldstone, M.B.A. et al. (Eds.) Malaria: drugs, disease and post-genomic biology. Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 357-382.
Voß, Y., Klaus, S., Guizetti, J. & Ganter, M. (2023) Plasmodium schizogony, a chronology of the parasite's cell cycle in the blood stage. PLoS Pathogens, 19(3), e1011157.
Voß, Y., Klaus, S., Lichti, N.P., Ganter, M. & Guizetti, J. (2023) Malaria parasite centrins assemble by Ca2+-inducible condensation. bioRxiv. 2022.2007.2026.501452.
Wassie, A.T., Zhao, Y. & Boyden, E.S. (2019) Expansion microscopy: principles and uses in biological research. Nature Methods, 16(1), 33-41.
Wilke, G., Funkhouser-Jones, L.J., Wang, Y., Ravindran, S., Wang, Q., Beatty, W.L. et al. (2019) A stem-cell-derived platform enables complete Cryptosporidium development in vitro and genetic tractability. Cell Host & Microbe, 26(1), 123-134.e128.
Woglar, A., Pierron, M., Schneider, F.Z., Jha, K., Busso, C. & Gönczy, P. (2022) Molecular architecture of the C. elegans centriole. PLoS Biology, 20(9), e3001784.
Yang, C., Doud, E.H., Sampson, E. & Arrizabalaga, G. (2023) The protein phosphatase PPKL is a key regulator of daughter parasite development in Toxoplasma gondii. bioRxiv. 2023.2006.2013.544803.
Yang, S., Cai, M., Huang, J., Zhang, S., Mo, X., Jiang, K. et al. (2023) EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis. Nature Communications, 14(1), 2864.
Zeeshan, M., Rashpa, R., Ferguson, D.J.P., Abel, S., Chahine, Z., Brady, D. et al. (2022) Genome-wide functional analysis reveals key roles for kinesins in the mammalian and mosquito stages of the malaria parasite life cycle. PLoS Biology, 20(7), e3001704.
Zeeshan, M., Rea, E., Abel, S., Vukusic, K., Markus, R., Brady, D. et al. (2023) Plasmodium ARK2-EB1 axis drives the unconventional spindle dynamics, scaffold formation and chromosome segregation of sexual transmission stages. Research Square.
Zwettler, F.U., Reinhard, S., Gambarotto, D., Bell, T.D.M., Hamel, V., Guichard, P. et al. (2020) Molecular resolution imaging by post-labeling expansion single-molecule localization microscopy (ex-SMLM). Nature Communications, 11(1), 3388.