Conservation of a Gliding Motility and Cell Invasion Machinery in Apicomplexan Parasites

doi:10.1083/jcb.147.5.937

This Article

	Full Text
	PDF (Full Text)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Kappe, S.
	Articles by Ménard, R.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Kappe, S.
	Articles by Ménard, R.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/1999/11/937/ $5.00
The Journal of Cell Biology, Volume 147, Number 5, November 29, 1999 937-944

Brief Report

Conservation of a Gliding Motility and Cell Invasion Machinery in Apicomplexan Parasites

Stefan Kappe^a, Thomas Bruderer^a, Soren Gantt^a, Hisashi Fujioka^c, Victor Nussenzweig^a, and Robert Ménard^a,b
^a Department of Pathology, Kaplan Cancer Center
^b Department of Medical and Molecular Parasitology, New York University School of Medicine, New York, New York 10016
^c Case Western Reserve University School of Medicine, Cleveland, Ohio 44106

Correspondence to: Robert Ménard, Department of Pathology, Division of Immunology, New York University School of Medicine, 550 First Avenue, New York, NY 10016. Tel:(212) 263-7870 Fax:(212) 263-8179 E-mail:menarr01{at}mcrcr6.med.nyu.edu.

Most Apicomplexan parasites, including the human pathogens Plasmodium,Toxoplasma, and Cryptosporidium, actively invade host cellsand display gliding motility, both actions powered by parasitemicrofilaments. In Plasmodium sporozoites, thrombospondin-relatedanonymous protein (TRAP), a member of a group of Apicomplexantransmembrane proteins that have common adhesion domains, isnecessary for gliding motility and infection of the vertebratehost. Here, we provide genetic evidence that TRAP is directlyinvolved in a capping process that drives both sporozoite glidingand cell invasion. We also demonstrate that TRAP-related proteinsin other Apicomplexa fulfill the same function and that theircytoplasmic tails interact with homologous partners in the respectiveparasite. Therefore, a mechanism of surface redistribution ofTRAP-related proteins driving gliding locomotion and cell invasionis conserved among Apicomplexan parasites.

Key Words: gliding motility, cell invasion, Apicomplexan parasites, thrombospondin-relatedanonymous protein, micronemal protein 2

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Mikolajczak, S. A., Silva-Rivera, H., Peng, X., Tarun, A. S., Camargo, N., Jacobs-Lorena, V., Daly, T. M., Bergman, L. W., de la Vega, P., Williams, J., Aly, A. S. I., Kappe, S. H. I. (2008). Distinct Malaria Parasite Sporozoites Reveal Transcriptional Changes That Cause Differential Tissue Infection Competence in the Mosquito Vector and Mammalian Host. Mol. Cell. Biol. 28: 6196-6207 [Abstract] [Full Text]
Heiss, K., Nie, H., Kumar, S., Daly, T. M., Bergman, L. W., Matuschewski, K. (2008). Functional Characterization of a Redundant Plasmodium TRAP Family Invasin, TRAP-Like Protein, by Aldolase Binding and a Genetic Complementation Test. Eukaryot Cell 7: 1062-1070 [Abstract] [Full Text]
Johnson, T. M., Rajfur, Z., Jacobson, K., Beckers, C. J. (2007). Immobilization of the Type XIV Myosin Complex in Toxoplasma gondii. Mol. Biol. Cell 18: 3039-3046 [Abstract] [Full Text]
Periz, J., Gill, A. C., Hunt, L., Brown, P., Tomley, F. M. (2007). The Microneme Proteins EtMIC4 and EtMIC5 of Eimeria tenella Form a Novel, Ultra-high Molecular Mass Protein Complex That Binds Target Host Cells. J. Biol. Chem. 282: 16891-16898 [Abstract] [Full Text]
Bosch, J., Buscaglia, C. A., Krumm, B., Ingason, B. P., Lucas, R., Roach, C., Cardozo, T., Nussenzweig, V., Hol, W. G. J. (2007). Aldolase provides an unusual binding site for thrombospondin-related anonymous protein in the invasion machinery of the malaria parasite. Proc. Natl. Acad. Sci. USA 104: 7015-7020 [Abstract] [Full Text]
Urban, S. (2006). Rhomboid proteins: conserved membrane proteases with divergent biological functions.. Genes Dev. 20: 3054-3068 [Abstract] [Full Text]
Starnes, G. L., Jewett, T. J., Carruthers, V. B., Sibley, L. D. (2006). Two Separate, Conserved Acidic Amino Acid Domains within the Toxoplasma gondii MIC2 Cytoplasmic Tail Are Required for Parasite Survival. J. Biol. Chem. 281: 30745-30754 [Abstract] [Full Text]
Garcia, J. E., Puentes, A., Patarroyo, M. E. (2006). Developmental Biology of Sporozoite-Host Interactions in Plasmodium falciparum Malaria: Implications for Vaccine Design. Clin. Microbiol. Rev. 19: 686-707 [Abstract] [Full Text]
Baum, J., Richard, D., Healer, J., Rug, M., Krnajski, Z., Gilberger, T.-W., Green, J. L., Holder, A. A., Cowman, A. F. (2006). A Conserved Molecular Motor Drives Cell Invasion and Gliding Motility across Malaria Life Cycle Stages and Other Apicomplexan Parasites. J. Biol. Chem. 281: 5197-5208 [Abstract] [Full Text]
Cerede, O., Dubremetz, J. F., Soete, M., Deslee, D., Vial, H., Bout, D., Lebrun, M. (2005). Synergistic role of micronemal proteins in Toxoplasma gondii virulence. JEM 201: 453-463 [Abstract] [Full Text]
Wetzel, D. M., Chen, L. A., Ruiz, F. A., Moreno, S. N. J., Sibley, L. D. (2004). Calcium-mediated protein secretion potentiates motility in Toxoplasma gondii. J. Cell Sci. 117: 5739-5748 [Abstract] [Full Text]
Gaskins, E., Gilk, S., DeVore, N., Mann, T., Ward, G., Beckers, C. (2004). Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. JCB 165: 383-393 [Abstract] [Full Text]
Sibley, L. D. (2004). Intracellular Parasite Invasion Strategies. Science 304: 248-253 [Abstract] [Full Text]
Jewett, T. J., Sibley, L. D. (2004). The Toxoplasma Proteins MIC2 and M2AP Form a Hexameric Complex Necessary for Intracellular Survival. J. Biol. Chem. 279: 9362-9369 [Abstract] [Full Text]
Silvie, O., Franetich, J.-F., Charrin, S., Mueller, M. S., Siau, A., Bodescot, M., Rubinstein, E., Hannoun, L., Charoenvit, Y., Kocken, C. H., Thomas, A. W., van Gemert, G.-J., Sauerwein, R. W., Blackman, M. J., Anders, R. F., Pluschke, G., Mazier, D. (2004). A Role for Apical Membrane Antigen 1 during Invasion of Hepatocytes by Plasmodium falciparum Sporozoites. J. Biol. Chem. 279: 9490-9496 [Abstract] [Full Text]
Okhuysen, P. C., Rogers, G. A., Crisanti, A., Spano, F., Huang, D. B., Chappell, C. L., Tzipori, S. (2004). Antibody Response of Healthy Adults to Recombinant Thrombospondin-Related Adhesive Protein of Cryptosporidium 1 after Experimental Exposure to Cryptosporidium Oocysts. CVI 11: 235-238 [Abstract] [Full Text]
Omer, F. M., de Souza, J. B., Corran, P. H., Sultan, A. A., Riley, E. M. (2003). Activation of Transforming Growth Factor {beta} by Malaria Parasite-derived Metalloproteinases and a Thrombospondin-like Molecule. JEM 198: 1817-1827 [Abstract] [Full Text]
Buscaglia, C. A., Coppens, I., Hol, W. G. J., Nussenzweig, V. (2003). Sites of Interaction between Aldolase and Thrombospondin-related Anonymous Protein in Plasmodium. Mol. Biol. Cell 14: 4947-4957 [Abstract] [Full Text]
Gilberger, T.-W., Thompson, J. K., Reed, M. B., Good, R. T., Cowman, A. F. (2003). The cytoplasmic domain of the Plasmodium falciparum ligand EBA-175 is essential for invasion but not protein trafficking. JCB 162: 317-327 [Abstract] [Full Text]
Delorme, V., Cayla, X., Faure, G., Garcia, A., Tardieux, I. (2003). Actin Dynamics Is Controlled by a Casein Kinase II and Phosphatase 2C Interplay on Toxoplasma gondii Toxofilin. Mol. Biol. Cell 14: 1900-1912 [Abstract] [Full Text]
Brossier, F., Jewett, T. J., Lovett, J. L., Sibley, L. D. (2003). C-terminal Processing of the Toxoplasma Protein MIC2 Is Essential for Invasion into Host Cells. J. Biol. Chem. 278: 6229-6234 [Abstract] [Full Text]
Bergman, L. W., Kaiser, K., Fujioka, H., Coppens, I., Daly, T. M., Fox, S., Matuschewski, K., Nussenzweig, V., Kappe, S. H. I. (2003). Myosin A tail domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. J. Cell Sci. 116: 39-49 [Abstract] [Full Text]
Deng, M., Templeton, T. J., London, N. R., Bauer, C., Schroeder, A. A., Abrahamsen, M. S. (2002). Cryptosporidium parvum Genes Containing Thrombospondin Type 1 Domains. Infect. Immun. 70: 6987-6995 [Abstract] [Full Text]
Kariu, T., Yuda, M., Yano, K., Chinzei, Y. (2002). MAEBL Is Essential for Malarial Sporozoite Infection of the Mosquito Salivary Gland. JEM 195: 1317-1323 [Abstract] [Full Text]
Joiner, K. A., Roos, D. S. (2002). Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. JCB 157: 557-563 [Abstract] [Full Text]
Morrissette, N. S., Sibley, L. D. (2002). Cytoskeleton of Apicomplexan Parasites. Microbiol. Mol. Biol. Rev. 66: 21-38 [Abstract] [Full Text]
Meissner, M., Reiss, M., Viebig, N., Carruthers, V. B., Toursel, C., Tomavo, S., Ajioka, J. W., Soldati, D. (2002). A family of transmembrane microneme proteins of Toxoplasma gondii contain EGF-like domains and function as escorters. J. Cell Sci. 115: 563-574 [Abstract] [Full Text]
Weatherall, D. J., Miller, L. H., Baruch, D. I., Marsh, K., Doumbo, O. K., Casals-Pascual, C., Roberts, D. J. (2002). Malaria and the Red Cell. ASH Education Book 2002: 35-57 [Abstract] [Full Text]
Kappe, S. H. I., Gardner, M. J., Brown, S. M., Ross, J., Matuschewski, K., Ribeiro, J. M., Adams, J. H., Quackenbush, J., Cho, J., Carucci, D. J., Hoffman, S. L., Nussenzweig, V. (2001). Exploring the transcriptome of the malaria sporozoite stage. Proc. Natl. Acad. Sci. USA 10.1073/pnas.171185198v1 [Abstract] [Full Text]
Reiss, M., Viebig, N., Brecht, S., Fourmaux, M.-N., Soete, M., Di Cristina, M., Dubremetz, J. F., Soldati, D. (2001). Identification and Characterization of an Escorter for Two Secretory Adhesins in Toxoplasma gondii. JCB 152: 563-578 [Abstract] [Full Text]
Di Cristina, M., Spaccapelo, R., Soldati, D., Bistoni, F., Crisanti, A. (2000). Two Conserved Amino Acid Motifs Mediate Protein Targeting to the Micronemes of the Apicomplexan Parasite Toxoplasma gondii. Mol. Cell. Biol. 20: 7332-7341 [Abstract] [Full Text]
Reed, M. B., Caruana, S. R., Batchelor, A. H., Thompson, J. K., Crabb, B. S., Cowman, A. F. (2000). Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proc. Natl. Acad. Sci. USA 97: 7509-7514 [Abstract] [Full Text]
Gantt, S., Persson, C., Rose, K., Birkett, A. J., Abagyan, R., Nussenzweig, V. (2000). Antibodies against Thrombospondin-Related Anonymous Protein Do Not Inhibit Plasmodium Sporozoite Infectivity In Vivo. Infect. Immun. 68: 3667-3673 [Abstract] [Full Text]
Hettmann, C., Herm, A., Geiter, A., Frank, B., Schwarz, E., Soldati, T., Soldati, D. (2000). A Dibasic Motif in the Tail of a Class XIV Apicomplexan Myosin Is an Essential Determinant of Plasma Membrane Localization. Mol. Biol. Cell 11: 1385-1400 [Abstract] [Full Text]
Brecht, S., Carruthers, V. B., Ferguson, D. J. P., Giddings, O. K., Wang, G., Jakle, U., Harper, J. M., Sibley, L. D., Soldati, D. (2001). The Toxoplasma Micronemal Protein MIC4 Is an Adhesin Composed of Six Conserved Apple Domains. J. Biol. Chem. 276: 4119-4127 [Abstract] [Full Text]
Howell, S. A., Withers-Martinez, C., Kocken, C. H. M., Thomas, A. W., Blackman, M. J. (2001). Proteolytic Processing and Primary Structure of Plasmodium falciparum Apical Membrane Antigen-1. J. Biol. Chem. 276: 31311-31320 [Abstract] [Full Text]
Kappe, S. H. I., Gardner, M. J., Brown, S. M., Ross, J., Matuschewski, K., Ribeiro, J. M., Adams, J. H., Quackenbush, J., Cho, J., Carucci, D. J., Hoffman, S. L., Nussenzweig, V. (2001). Exploring the transcriptome of the malaria sporozoite stage. Proc. Natl. Acad. Sci. USA 98: 9895-9900 [Abstract] [Full Text]