Gliding motility and cell invasion by Apicomplexa: insights from the Plasmodium sporozoite

Apicomplexa constitute one of the largest phyla of protozoa. Most Apicomplexa, including those pathogenic to humans, are obligate intracellular parasites. Their extracellular forms, which are highly polarized and elongated cells, share two unique abilities: they glide on solid substrates without changing their shape and reach an intracellular compartment without active participation from the host cell. There is now ample ultrastructural evidence that these processes result from the backward movement of extracellular interactions along the anteroposterior axis of the parasite. Recent work in several Apicomplexa, including genetic studies in the Plasmodium sporozoite, has provided molecular support for this ‘capping’ model. It appears that the same machinery drives both gliding motility and host cell invasion. The cytoplasmic motor, a transmembrane bridge and surface ligands essential for cell invasion are conserved among the main apicomplexan pathogens.

[1]  L. Sibley,et al.  Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii , 1999, Molecular microbiology.

[2]  J. Schwartzman,et al.  Characterization of myosin-A and myosin-C: two class XIV unconventional myosins from Toxoplasma gondii. , 1999, Cell motility and the cytoskeleton.

[3]  M. Götte,et al.  Functions of cell surface heparan sulfate proteoglycans. , 1999, Annual review of biochemistry.

[4]  A. Crisanti,et al.  Molecular cloning and expression analysis of a Cryptosporidium parvum gene encoding a new member of the thrombospondin family. , 1998, Molecular and biochemical parasitology.

[5]  S. Hoffman,et al.  Preventing sporozoite invasion of hepatocytes. , 1996 .

[6]  J. Vanderberg,et al.  Delayed migration of Plasmodium sporozoites from the mosquito bite site to the blood. , 1997, The American journal of tropical medicine and hygiene.

[7]  R. Wilson,et al.  Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: implications for red cell invasion. , 1998, Journal of cell science.

[8]  R. Entzeroth Invasion and early development of Sarcocystis muris (Apicomplexa, Sarcocystidae) in tissue cultures. , 1985, The Journal of protozoology.

[9]  O. Poupel,et al.  Toxoplasma gondii motility and host cell invasiveness are drastically impaired by jasplakinolide, a cyclic peptide stabilizing F-actin. , 1999, Microbes and infection.

[10]  P. Rieu,et al.  Identification of the complement iC3b binding site in the beta 2 integrin CR3 (CD11b/CD18). , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Y. Takada,et al.  Critical Threonine and Aspartic Acid Residues within the I Domains of β2 Integrins for Interactions with Intercellular Adhesion Molecule 1 (ICAM-1) and C3bi (*) , 1995, The Journal of Biological Chemistry.

[12]  S. Santoro,et al.  Binding of the alpha 2 integrin I domain to extracellular matrix ligands: structural and mechanistic differences between collagen and laminin binding. , 1998, Cell adhesion and communication.

[13]  H. Boleti,et al.  Toxofilin, a novel actin-binding protein from Toxoplasma gondii, sequesters actin monomers and caps actin filaments. , 2000, Molecular biology of the cell.

[14]  J. Jensen,et al.  Fine Structure of Penetration of Cultured Cells by Isospora canis Sporozoites , 1978 .

[15]  L. Sibley,et al.  Actin in the parasite Toxoplasma gondii is encoded by a single copy gene, ACT1 and exists primarily in a globular form. , 1997, Cell motility and the cytoskeleton.

[16]  A. Cevallos,et al.  Cryptosporidium: molecular basis of host-parasite interaction. , 1998, Advances in parasitology.

[17]  L. Sibley,et al.  Secretion of micronemal proteins is associated with toxoplasma invasion of host cells , 1999, Cellular microbiology.

[18]  A. Crisanti,et al.  Identification of heparin as a ligand for the A-domain of Plasmodium falciparum thrombospondin-related adhesion protein. , 1999, Molecular and biochemical parasitology.

[19]  R. Sinden,et al.  CTRP is essential for mosquito infection by malaria ookinetes , 1999, The EMBO journal.

[20]  D. Russell Host cell invasion by Apicomplexa: an expression of the parasite's contractile system? , 1983, Parasitology.

[21]  Richard W. Farndale,et al.  Structural Basis of Collagen Recognition by Integrin α2β1 , 2000, Cell.

[22]  L. Sibley,et al.  Toxoplasma Invasion of Mammalian Cells Is Powered by the Actin Cytoskeleton of the Parasite , 1996, Cell.

[23]  P. Sinnis The malaria sporozoite's journey into the liver. , 1996, Infectious agents and disease.

[24]  V. Nussenzweig,et al.  Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes , 1993, The Journal of experimental medicine.

[25]  M. Mossakowska,et al.  Actin-binding proteins of invasive malaria parasites and the regulation of actin polymerization by a complex of 32/34-kDa proteins associated with heat shock protein 70kDa. , 1998, Molecular and biochemical parasitology.

[26]  L. Sibley,et al.  Molecular characterization of a thrombospondin-related anonymous protein homologue in Neospora caninum. , 2000, Molecular and biochemical parasitology.

[27]  G. Torpier,et al.  Freeze fracture study of the pellicle of an eimerian sporozoite (Protozoa, Coccidia). , 1978, Journal of ultrastructure research.

[28]  E. Plow,et al.  Identification and Reconstruction of the Binding Site within αMβ2 for a Specific and High Affinity Ligand, NIF* , 1997, The Journal of Biological Chemistry.

[29]  L. Sibley,et al.  Cloning and characterization of actin depolymerizing factor from Toxoplasma gondii. , 1997, Molecular and biochemical parasitology.

[30]  M. Sheetz,et al.  Cell migration: regulation of force on extracellular-matrix-integrin complexes. , 1998, Trends in cell biology.

[31]  J. Remington,et al.  Effect of cytochalasin D on Toxoplasma gondii cell entry , 1978, Infection and immunity.

[32]  R. Ménard,et al.  Conservation of a Gliding Motility and Cell Invasion Machinery in Apicomplexan Parasites , 1999, The Journal of cell biology.

[33]  J. Schwartzman,et al.  A novel class of unconventional myosins from Toxoplasma gondii. , 1997, Journal of molecular biology.

[34]  L. Miller,et al.  Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation , 1979, The Journal of experimental medicine.

[35]  J. Spring,et al.  Drosophila syndecan: conservation of a cell-surface heparan sulfate proteoglycan. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Sinnis,et al.  Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum. , 1997, Molecular and biochemical parasitology.

[37]  Daniel Choquet,et al.  Ligand binding regulates the directed movement of β1 integrins on fibroblasts , 1996, Nature.

[38]  D. Soldati,et al.  Mix and match modules: structure and function of microneme proteins in apicomplexan parasites. , 2001, Trends in parasitology.

[39]  J. Vanderberg,et al.  The passage of Plasmodium berghei sporozoites through the salivary glands of Anopheles stephensi: an electron microscope study. , 1973, The Journal of parasitology.

[40]  V. Mermall,et al.  Unconventional myosins in cell movement, membrane traffic, and signal transduction. , 1998, Science.

[41]  M. Pangburn,et al.  Properdin binds to sulfatide [Gal(3-SO4)beta 1-1 Cer] and has a sequence homology with other proteins that bind sulfated glycoconjugates. , 1990, The Journal of biological chemistry.

[42]  A. Azad,et al.  Infectivity of Plasmodium bergheiSporozoites Delivered by Intravenous Inoculation versus Mosquito Bite: Implications for Sporozoite Vaccine Trials , 1999, Infection and Immunity.

[43]  Y. Takada,et al.  Identification of putative ligand binding sites within I domain of integrin α2β1 (VLA-2,CD49b/CD29). , 1996, The Journal of Biological Chemistry.

[44]  J. Jensen,et al.  Effects of antiphagocytic agents on penetration of Eimeria magna sporozoites into cultured cells. , 1976, The Journal of parasitology.

[45]  R. Abagyan,et al.  Antibodies against Thrombospondin-Related Anonymous Protein Do Not Inhibit Plasmodium Sporozoite Infectivity In Vivo , 2000, Infection and Immunity.

[46]  D. Lauffenburger,et al.  Cell Migration: A Physically Integrated Molecular Process , 1996, Cell.

[47]  D. Fidock,et al.  Developmental arrest of the human malaria parasite Plasmodium falciparum within the mosquito midgut via CTRP gene disruption , 2000, Molecular microbiology.

[48]  H. Bujard,et al.  Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. , 1993, The EMBO journal.

[49]  C. Sterling,et al.  Immunofluorescent microscopical visualization of trails left by gliding Cryptosporidium parvum sporozoites. , 1991, The Journal of parasitology.

[50]  V. Nussenzweig,et al.  Cell surface glycosaminoglycans are not obligatory for Plasmodium berghei sporozoite invasion in vitro. , 1996, Molecular and biochemical parasitology.

[51]  T. Mitchison,et al.  Actin-Based Cell Motility and Cell Locomotion , 1996, Cell.

[52]  T. Mitchison,et al.  Myosin is involved in postmitotic cell spreading , 1995, The Journal of cell biology.

[53]  R. Sinden,et al.  The role of the cytoskeleton in the motility of coccidian sporozoites. , 1981, Journal of cell science.

[54]  上田 武郎 Identification of the complement iC3b binding site in the β2 integrin CR3 (CD11b/CD18) , 1996 .

[55]  L. G. Tilney,et al.  Induction of an acrosomal process in Toxoplasma gondii: visualization of actin filaments in a protozoan parasite. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[56]  C. King Cell motility of sporozoan protozoa. , 1988, Parasitology today.

[57]  J. Dubremetz,et al.  Toxoplasma gondii: redistribution of monoclonal antibodies on tachyzoites during host cell invasion. , 1985, Experimental parasitology.

[58]  Gary G. Borisy,et al.  Analysis of the Actin–Myosin II System in Fish Epidermal Keratocytes: Mechanism of Cell Body Translocation , 1997, The Journal of cell biology.

[59]  M. J. Stewart,et al.  Malaria sporozoites release circumsporozoite protein from their apical end and translocate it along their surface. , 1991, The Journal of protozoology.

[60]  A. Krettli,et al.  Which Routes Do Plasmodium Sporozoites Use for Successful Infections of Vertebrates? , 2000, Infection and Immunity.

[61]  L. Miller,et al.  Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite , 1978, The Journal of cell biology.

[62]  J. Golenser,et al.  The dual role of macrophages in the sporozoite-induced malaria infection. A hypothesis. , 1980, International journal of nuclear medicine and biology.

[63]  E. Elson,et al.  Capping protein levels influence actin assembly and cell motility in dictyostelium , 1995, Cell.

[64]  E. Elson,et al.  A mechanical function of myosin II in cell motility. , 1995, Journal of cell science.

[65]  C A King,et al.  Cell surface interaction of the protozoan Gregarina with concanavalin A beads - implications for models of gregarine gliding. , 1981, Cell biology international reports.

[66]  M VALENTINCIC,et al.  [Toxoplasma gondii]. , 1953, Zdravstveni vestnik.

[67]  L. Smilenov,et al.  Focal adhesion motility revealed in stationary fibroblasts. , 1999, Science.

[68]  A. Horwitz,et al.  Dynamics of beta 1 integrin-mediated adhesive contacts in motile fibroblasts , 1992, The Journal of cell biology.

[69]  C. Newbold,et al.  A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite , 1988, Nature.

[70]  Timothy J. Mitchison,et al.  Identification of Novel Graded Polarity Actin Filament Bundles in Locomoting Heart Fibroblasts: Implications for the Generation of Motile Force , 1997, The Journal of cell biology.

[71]  B. Chait,et al.  Structural and functional properties of region II-plus of the malaria circumsporozoite protein , 1994, The Journal of experimental medicine.

[72]  L. Sibley,et al.  Invasion of Toxoplasma gondii occurs by active penetration of the host cell. , 1995, Journal of cell science.

[73]  V. Nussenzweig,et al.  The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of plasmodium falciparum sporozoites , 1992, Cell.

[74]  T. Mitchison,et al.  Moving and stationary actin filaments are involved in spreading of postmitotic PtK2 cells , 1993, The Journal of cell biology.

[75]  J. Zimmerberg,et al.  Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[76]  L. Sibley,et al.  Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. , 1997, European journal of cell biology.

[77]  L. Sibley,et al.  Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii , 1997, Molecular microbiology.

[78]  S. Hoffman,et al.  Characterization of Plasmodium falciparum sporozoite surface protein 2. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[79]  T. Sam-Yellowe Rhoptry organelles of the apicomplexa: Their role in host cell invasion and intracellular survival. , 1996, Parasitology today.

[80]  H. Sakaida,et al.  Targeted Disruption of the Plasmodium berghei Ctrp Gene Reveals Its Essential Role in Malaria Infection of the Vector Mosquito , 1999, The Journal of experimental medicine.

[81]  V. Nussenzweig,et al.  Circumsporozoite proteins of malaria parasites , 1985, Cell.

[82]  M. J. Stewart,et al.  Malaria sporozoites leave behind trails of circumsporozoite protein during gliding motility. , 1988, The Journal of protozoology.

[83]  D. Soldati,et al.  A dibasic motif in the tail of a class XIV apicomplexan myosin is an essential determinant of plasma membrane localization. , 2000, Molecular biology of the cell.

[84]  C. Speer,et al.  A Role for Host Phosphoinositide 3-Kinase and Cytoskeletal Remodeling during Cryptosporidium parvumInfection , 1999, Infection and Immunity.

[85]  S. Chew,et al.  Plasmodium sporozoite interactions with macrophages in vitro: a videomicroscopic analysis. , 1990, The Journal of protozoology.

[86]  J. Ajioka,et al.  Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. , 1997, Molecular and biochemical parasitology.

[87]  H. Mehlhorn,et al.  Comparative electron microscope study of pellicular structures in coccidia (Sarcocystis, Besnoitia and Eimeria). , 1977, International journal for parasitology.

[88]  A. König,et al.  Microneme secretion in Coccidia: confocal laser scanning and electron microscope study of Sarcocystis muris in cell culture. , 1992, European journal of cell biology.

[89]  L. Miller,et al.  The Journey of Malaria Sporozoites in the Mosquito Salivary Gland , 1994, The Journal of eukaryotic microbiology.

[90]  Andrea Crisanti,et al.  TRAP Is Necessary for Gliding Motility and Infectivity of Plasmodium Sporozoites , 1997, Cell.

[91]  M. Shaw,et al.  The same but different: the biology of Theileria sporozoite entry into bovine cells. , 1997, International journal for parasitology.