DOI: 10.1038/ncomms5098. Plasticity and redundancy among AMA–RON pairs ensure host cell entry of Toxoplasma parasites

Plasticity and redundancy among AMA–RON pairs ensure host cell entry of Toxoplasma parasites

10.1038/ncomms5098

Crossref journal-article

Springer Science and Business Media LLC

Nature Communications (297)

Bibliography

Lamarque, M. H., Roques, M., Kong-Hap, M., Tonkin, M. L., Rugarabamu, G., Marq, J.-B., Penarete-Vargas, D. M., Boulanger, M. J., Soldati-Favre, D., & Lebrun, M. (2014). Plasticity and redundancy among AMAâRON pairs ensure host cell entry of Toxoplasma parasites. Nature Communications, 5(1).

Authors 10

Mauld H. Lamarque (first)
Magali Roques (additional)
Marie Kong-Hap (additional)
Michelle L. Tonkin (additional)
George Rugarabamu (additional)
Jean-Baptiste Marq (additional)
Diana M. Penarete-Vargas (additional)
Martin J. Boulanger (additional)
Dominique Soldati-Favre (additional)
Maryse Lebrun (additional)

References 47 Referenced 150

Gaur, D. & Chitnis, C. E. Molecular interactions and signaling mechanisms during erythrocyte invasion by malaria parasites. Curr. Opin. Microbiol. 14, 422–428 (2011). (10.1016/j.mib.2011.07.018) / Curr. Opin. Microbiol. by D Gaur (2011)
Singh, S., Alam, M. M., Pal-Bhowmick, I., Brzostowski, J. A. & Chitnis, C. E. Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog. 6, e1000746 (2010). (10.1371/journal.ppat.1000746) / PLoS Pathog. by S Singh (2010)
Aikawa, M., Miller, L. H., Johnson, J. & Rabbege, J. Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J. Cell Biol. 77, 72–82 (1978). (10.1083/jcb.77.1.72) / J. Cell Biol. by M Aikawa (1978)
Sibley, L. D. How apicomplexan parasites move in and out of cells. Curr. Opin. Biotechnol. 21, 592–598 (2010). (10.1016/j.copbio.2010.05.009) / Curr. Opin. Biotechnol. by LD Sibley (2010)
Besteiro, S., Michelin, A., Poncet, J., Dubremetz, J. F. & Lebrun, M. Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLoS Pathog. 5, e1000309 (2009). (10.1371/journal.ppat.1000309) / PLoS Pathog. by S Besteiro (2009)
Lamarque, M. et al. The RON2-AMA1 interaction is a critical step in moving junction-dependent invasion by apicomplexan parasites. PLoS Pathog. 7, e1001276 (2011). (10.1371/journal.ppat.1001276) / PLoS Pathog. by M Lamarque (2011)
Bargieri, D., Lagal, V., Tardieux, I. & Menard, R. Host cell invasion by apicomplexans: what do we know? Trends. Parasitol. 28, 131–135 (2012). (10.1016/j.pt.2012.01.005) / Trends. Parasitol. by D Bargieri (2012)
Bargieri, D. Y. et al. Apical membrane antigen 1 mediates apicomplexan parasite attachment but is dispensable for host cell invasion. Nat. Commun. 4, 2552 (2013). (10.1038/ncomms3552) / Nat. Commun. by DY Bargieri (2013)
Giovannini, D. et al. Independent roles of apical membrane antigen 1 and rhoptry neck proteins during host cell invasion by apicomplexa. Cell Host Microbe 10, 591–602 (2011). (10.1016/j.chom.2011.10.012) / Cell Host Microbe by D Giovannini (2011)
Alexander, D. L., Mital, J., Ward, G. E., Bradley, P. & Boothroyd, J. C. Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathog. 1, e17 (2005). (10.1371/journal.ppat.0010017) / PLoS Pathog. by DL Alexander (2005)
Tyler, J. S. & Boothroyd, J. C. The C-terminus of Toxoplasma RON2 provides the crucial link between AMA1 and the host-associated invasion complex. PLoS Pathog. 7, e1001282 (2011). (10.1371/journal.ppat.1001282) / PLoS Pathog. by JS Tyler (2011)
Tonkin, M. L. et al. Host cell invasion by apicomplexan parasites: insights from the co-structure of AMA1 with a RON2 peptide. Science 333, 463–467 (2011). (10.1126/science.1204988) / Science by ML Tonkin (2011)
Vulliez-Le Normand, B. et al. Structural and functional insights into the malaria parasite moving junction complex. PLoS Pathog. 8, e1002755 (2012). (10.1371/journal.ppat.1002755) / PLoS Pathog. by B Vulliez-Le Normand (2012)
Srinivasan, P. et al. Disrupting malaria parasite AMA1-RON2 interaction with a small molecule prevents erythrocyte invasion. Nat. Commun. 4, 2261 (2013). (10.1038/ncomms3261) / Nat. Commun. by P Srinivasan (2013)
Collins, C. R., Withers-Martinez, C., Hackett, F. & Blackman, M. J. An inhibitory antibody blocks interactions between components of the malarial invasion machinery. PLoS Pathog. 5, e1000273 (2009). (10.1371/journal.ppat.1000273) / PLoS Pathog. by CR Collins (2009)
Richard, D. et al. Interaction between Plasmodium falciparum apical membrane antigen 1 and the rhoptry neck protein complex defines a key step in the erythrocyte invasion process of malaria parasites. J. Biol. Chem. 285, 14815–14822 (2010). (10.1074/jbc.M109.080770) / J. Biol. Chem. by D Richard (2010)
Srinivasan, P. et al. Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc. Natl Acad. Sci. USA 108, 13275–13280 (2011). (10.1073/pnas.1110303108) / Proc. Natl Acad. Sci. USA by P Srinivasan (2011)
Saeij, J. P. et al. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445, 324–327 (2007). (10.1038/nature05395) / Nature by JP Saeij (2007)
Mital, J., Meissner, M., Soldati, D. & Ward, G. E. Conditional expression of Toxoplasma gondii apical membrane antigen-1 (TgAMA1) demonstrates that TgAMA1 plays a critical role in host cell invasion. Mol. Biol. Cell. 16, 4341–4349 (2005). (10.1091/mbc.e05-04-0281) / Mol. Biol. Cell. by J Mital (2005)
Sheiner, L. et al. Toxoplasma gondii transmembrane microneme proteins and their modular design. Mol. Microbiol. 7, 912–929 (2010). (10.1111/j.1365-2958.2010.07255.x) / Mol. Microbiol. by L Sheiner (2010)
Treeck, M. et al. Functional analysis of the leading malaria vaccine candidate AMA-1 reveals an essential role for the cytoplasmic domain in the invasion process. PLoS Pathog. 5, e1000322 (2009). (10.1371/journal.ppat.1000322) / PLoS Pathog. by M Treeck (2009)
Dobrowolski, J. M. & Sibley, L. D. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84, 933–939 (1996). (10.1016/S0092-8674(00)81071-5) / Cell by JM Dobrowolski (1996)
Hakansson, S., Charron, A. J. & Sibley, L. D. Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole. Embo J. 20, 3132–3144 (2001). (10.1093/emboj/20.12.3132) / Embo J. by S Hakansson (2001)
Poukchanski, A. et al. Toxoplasma gondii sporozoites invade host cells using two novel paralogues of RON2 and AMA1. PLoS ONE 8, e70637 (2013). (10.1371/journal.pone.0070637) / PLoS ONE by A Poukchanski (2013)
Besteiro, S., Dubremetz, J. F. & Lebrun, M. The moving junction of apicomplexan parasites: a key structure for invasion. Cell. Microbiol. 13, 797–805 (2011). (10.1111/j.1462-5822.2011.01597.x) / Cell. Microbiol. by S Besteiro (2011)
Sheiner, L., Dowse, T. J. & Soldati-Favre, D. Identification of trafficking determinants for polytopic rhomboid proteases in Toxoplasma gondii. Traffic 9, 665–677 (2008). (10.1111/j.1600-0854.2008.00736.x) / Traffic by L Sheiner (2008)
Shen, B. & Sibley, L. D. Toxoplasma aldolase is required for metabolism but dispensable for host-cell invasion. Proc. Natl Acad. Sci. USA 111, 3567–3572 (2014). (10.1073/pnas.1315156111) / Proc. Natl Acad. Sci. USA by B Shen (2014)
Kariu, T., Yuda, M., Yano, K. & Chinzei, Y. MAEBL is essential for malarial sporozoite infection of the mosquito salivary gland. J. Exp. Med. 195, 1317–1323 (2002). (10.1084/jem.20011876) / J. Exp. Med. by T Kariu (2002)
Preiser, P. et al. Antibodies against MAEBL ligand domains M1 and M2 inhibit sporozoite development in vitro. Infect. Immun. 72, 3604–3608 (2004). (10.1128/IAI.72.6.3604-3608.2004) / Infect. Immun. by P Preiser (2004)
Beck, J. R., Chen, A. L., Kim, E. W. & Bradley, P. J. RON5 is critical for organization and function of the Toxoplasma moving junction complex. PLoS Pathog. 10, e1004025 (2014). (10.1371/journal.ppat.1004025) / PLoS Pathog. by JR Beck (2014)
Huynh, M. H. & Carruthers, V. B. Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot. Cell 8, 530–539 (2009). (10.1128/EC.00358-08) / Eukaryot. Cell by MH Huynh (2009)
Couvreur, G., Sadak, A., Fortier, B. & Dubremetz, J. F. Surface antigens of Toxoplasma gondii. Parasitology 97, (Pt 1): 1–10 (1988). (10.1017/S0031182000066695) / Parasitology by G Couvreur (1988)
Lebrun, M. et al. The rhoptry neck protein RON4 relocalizes at the moving junction during Toxoplasma gondii invasion. Cell. Microbiol. 7, 1823–1833 (2005). (10.1111/j.1462-5822.2005.00646.x) / Cell. Microbiol. by M Lebrun (2005)
Sadak, A., Taghy, Z., Fortier, B. & Dubremetz, J. F. Characterization of a family of rhoptry proteins of Toxoplasma gondii. Mol. Biochem. Parasitol. 29, 203–211 (1988). (10.1016/0166-6851(88)90075-8) / Mol. Biochem. Parasitol. by A Sadak (1988)
Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001). (10.1093/nar/29.9.e45) / Nucleic Acids Res. by MW Pfaffl (2001)
Kong-Hap, M. A. et al. Regulation of ATG8 membrane association by ATG4 in the parasitic protist Toxoplasma gondii. Autophagy 9, 1334–1348 (2013). (10.4161/auto.25189) / Autophagy by MA Kong-Hap (2013)
Sheiner, L. et al. A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor. PLoS Pathog. 7, e1002392 (2011). (10.1371/journal.ppat.1002392) / PLoS Pathog. by L Sheiner (2011)
Daher, W., Klages, N., Carlier, M. F. & Soldati-Favre, D. Molecular characterization of Toxoplasma gondii formin 3, an actin nucleator dispensable for tachyzoite growth and motility. Eukaryot. Cell 11, 343–352 (2012). (10.1128/EC.05192-11) / Eukaryot. Cell by W Daher (2012)
Zhang, Y. Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 69, (Suppl 8): 108–117 (2007). (10.1002/prot.21702) / Proteins by Y Zhang (2007)
Pettersen, E. F. et al. UCSF chimera--a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004). (10.1002/jcc.20084) / J. Comput. Chem. by EF Pettersen (2004)
Eswar, N. et al. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics Chapter 5, Unit 5 6 (2006). / Curr. Protoc. Bioinformatics by N Eswar (2006)
Kittichotirat, W., Guerquin, M., Bumgarner, R. E. & Samudrala, R. Protinfo PPC: a web server for atomic level prediction of protein complexes. Nucleic Acids Res. 37, W519–W525 (2009). (10.1093/nar/gkp306) / Nucleic Acids Res. by W Kittichotirat (2009)
London, N., Raveh, B., Cohen, E., Fathi, G. & Schueler-Furman, O. Rosetta FlexPepDock web server--high resolution modeling of peptide-protein interactions. Nucleic Acids Res. 39, W249–W253 (2011). (10.1093/nar/gkr431) / Nucleic Acids Res. by N London (2011)
Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797 (2007). (10.1016/j.jmb.2007.05.022) / J. Mol. Biol. by E Krissinel (2007)
Wallner, B. & Elofsson, A. Can correct protein models be identified? Protein. Sci. 12, 1073–1086 (2003). (10.1110/ps.0236803) / Protein. Sci. by B Wallner (2003)
Colovos, C. & Yeates, T. O. Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci. 2, 1511–1519 (1993). (10.1002/pro.5560020916) / Protein Sci. by C Colovos (1993)
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta. Crystallogr. D Biol. Crystallogr. 66, 12–21 (2010). (10.1107/S0907444909042073) / Acta. Crystallogr. D Biol. Crystallogr. by VB Chen (2010)

Dates

Type	When
Created	11 years, 2 months ago (June 17, 2014, 7:57 a.m.)
Deposited	1 year, 3 months ago (May 27, 2024, 3:58 p.m.)
Indexed	6 days, 4 hours ago (Aug. 27, 2025, 12:25 p.m.)
Issued	11 years, 2 months ago (June 17, 2014)
Published	11 years, 2 months ago (June 17, 2014)
Published Online	11 years, 2 months ago (June 17, 2014)

Funders 0

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BibTeX

@article{Lamarque_2014, title={Plasticity and redundancy among AMA–RON pairs ensure host cell entry of Toxoplasma parasites}, volume={5}, ISSN={2041-1723}, url={http://dx.doi.org/10.1038/ncomms5098}, DOI={10.1038/ncomms5098}, number={1}, journal={Nature Communications}, publisher={Springer Science and Business Media LLC}, author={Lamarque, Mauld H. and Roques, Magali and Kong-Hap, Marie and Tonkin, Michelle L. and Rugarabamu, George and Marq, Jean-Baptiste and Penarete-Vargas, Diana M. and Boulanger, Martin J. and Soldati-Favre, Dominique and Lebrun, Maryse}, year={2014}, month=jun }

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