© The Rockefeller University Press,
0021-9525/1999//937 $5.00
The Journal of Cell Biology, Volume 147, Number 5,
, 1999 937-944
Conservation of a Gliding Motility and Cell Invasion Machinery in Apicomplexan Parasites
Stefan Kappea,
Thomas Bruderera,
Soren Gantta,
Hisashi Fujiokac,
Victor Nussenzweiga, and
Robert Ménarda,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
Department of Pathology, Division of Immunology, New York University School of Medicine, 550 First Avenue, New York, NY 10016.(212) 263-8179(212) 263-7870
menarr01{at}mcrcr6.med.nyu.edu
Most Apicomplexan parasites, including the human pathogens Plasmodium, Toxoplasma, and Cryptosporidium, actively invade host cells and display gliding motility, both actions powered by parasite microfilaments. In Plasmodium sporozoites, thrombospondin-related anonymous protein (TRAP), a member of a group of Apicomplexan transmembrane proteins that have common adhesion domains, is necessary for gliding motility and infection of the vertebrate host. Here, we provide genetic evidence that TRAP is directly involved in a capping process that drives both sporozoite gliding and cell invasion. We also demonstrate that TRAP-related proteins in other Apicomplexa fulfill the same function and that their cytoplasmic tails interact with homologous partners in the respective parasite. Therefore, a mechanism of surface redistribution of TRAP-related proteins driving gliding locomotion and cell invasion is conserved among Apicomplexan parasites.
Key Words: gliding motility cell invasion Apicomplexan parasites thrombospondin-related anonymous protein micronemal protein 2
© 1999 The Rockefeller University Press
Stefan Kappe and Thomas Bruderer contributed equally to this work and should be considered co-first authors.
Abbreviations used in this paper: EEF, exoerythrocytic forms; MIC2, micronemal protein 2; nt, nucleotide; TRAP, thrombospondin-related anonymous protein; TSR, thrombospondin type 1 repeat; WT, wild type.

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-
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-
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-
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