Actin depolymerizing factor controls actin turnover and gliding motility in Toxoplasma gondii

Molecular Biology of the Cell

Volumn 22, Issue 8, 2011, Pages 1290-1299

  Mehta, Simren ^a   Sibley, L David ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN DEPOLYMERIZING FACTOR; PROTOZOAL PROTEIN;

ACTIN FILAMENT; ARTICLE; CELL INVASION; CELL MOTILITY; CELL MOTION; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; HOST CELL; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN STRUCTURE; TACHYZOITE; TOXOPLASMA GONDII; TOXOPLASMOSIS; WESTERN BLOTTING;

ACTINS; CELL CULTURE TECHNIQUES; CELL MOVEMENT; CYTOSKELETON; DESTRIN; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; HOST-PARASITE INTERACTIONS; HUMANS; MALE; MICROFILAMENT PROTEINS; MICROFILAMENTS; MICROSCOPY, ELECTRON; POLYMERIZATION; PROTOZOAN PROTEINS; TOXOPLASMA;

TOXOPLASMA GONDII;

EID: 79954584860     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-12-0939     Document Type: Article

References (38)

1. Bamburg JR (1999). Proteins of the ADF/cofilin family: Essential regulators of actin dynamics. Annu Rev Cell Dev Biol 15, 185-230. (Pubitemid 32250375)
2. Baum J, Papenfuss AT, Baum B, Speed TP, Cowman AF (2006). Regulation of apicomplexan actin-based motility. Nat Rev Microbiol 4, 621-628. (Pubitemid 44317024)
3. Baum J, Tonkin CJ, Paul AS, Rug M, Smith BJ, Gould SB, Richard D, Pollard TD, Cowman AF (2008). A malaria parasite formin regulates actin polymerization and localizes to the parasite-erythrocyte moving junction during invasion. Cell Host Microbe 3, 188-198. (Pubitemid 351325762)
4. Bernstein BW, Bamburg JR (2010). ADF/cofilin: A functional node in cell biology. Trends Cell Biol 20, 187-195.
5. Buguliskis JS, Brossier F, Shuman J, Sibley LD (2010). Rhomboid 4 (ROM4) affects the processing of surface adhesins and facilitates host cell invasion by Toxoplasma gondii. PLoS Pathog 6, e1000858.
6. Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia GW, Hong Y, Chua NH, Pantaloni D (1997). Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: Implication in actin-based motility. J Cell Biol 136, 1307-1323.
7. Crews P, Manes LV, Boehler M (1986). Jasplakinolide, a cyclodepsipeptide from the marine sponge, Jaspis spp. Tetrahedron Lett 27, 2797-2800.
8. Daher W, Plattner F, Carlier MF, Soldati-Favre D (2010). Concerted action of two formins in gliding motility and host cell invasion by Toxoplasma gondii. PLoS Pathog 6.
9. Dobrowolski JM, Niesman IR, Sibley LD (1997). Actin in the parasite Toxoplasma gondii is encoded by a single copy gene, ACT1 and exists primarily in a globular form. Cell Motil Cytoskel 37, 253-262. (Pubitemid 27287685)
10. Dobrowolski JM, Sibley LD (1996). Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84, 933-939. (Pubitemid 26106862)
11. Doi Y, Shinzawa N, Fukumoto S, Okano H, Kanuka H (2010). ADF2 is required for transformation of the ookinete and sporozoite in malaria parasite development. Biochem Biophys Res Commun 397, 668-672.
12. Endo T, Sethi KK, Piekarski G (1982). Toxoplasma gondii: Calcium ionophore A23187-mediated exit of trophozoites from infected murine macrophages. Exp Parasitol 53, 179-188. (Pubitemid 12093281)
13. Håkansson S, Morisaki H, Heuser JE, Sibley LD (1999). Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion. Mol Biol Cell 10, 3539-3547. (Pubitemid 29534008)
14. Lourido S, Shuman J, Zhang C, Shokat KM, Hui R, Sibley LD (2010). Calcium-dependent protein kinase 1 is an essential regulator of exocytosis in Toxoplasma. Nature 465, 359-362.
15. McGough A, Pope B, Chiu W, Weeds A (1997). Cofilin changes the twist of F-actin: Implications for actin filament dynamics and cellular function. J Cell Biol 138, 771-781. (Pubitemid 27365041)
16. Mehta S, Sibley LD (2010). Toxoplasma gondii actin depolymerizing factor acts primarily to sequester G-actin. J Biol Chem 285, 6835-6847.
17. Meissner M, Schluter D, Soldati D (2002). Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298, 837-840. (Pubitemid 35231538)
18. Messina M, Niesman IR, Mercier C, Sibley LD (1995). Stable DNA transformation of Toxoplasma gondii using phleomycin selection. Gene 165, 213-217.
19. Miller LH, Aikawa M, Johnson JG, Shiroishi T (1979). Interaction between cytochalasin B-treated malarial parasites and erythrocytes. J Exp Med 149, 172-184. (Pubitemid 9081276)
20. Munter S, Sabass B, Selhuber-Unkel C, Kudryashev M, Hegge S, Engel U, Spatz JP, Matuschewski K, Schwarz US, Frischknecht F (2009). Plasmodium sporozoite motility is modulated by the turnover of discrete adhesion sites. Cell Host Microbe 6, 551-562.
21. Ono S (2007). Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics. Int Rev Cytol 258, 1-82. (Pubitemid 46330483)
22. Pinder JC, Fowler RE, Dluzewski AR, Bannister LH, Lavin FM, Mitchell GH, Wilson RJM, Gratzer WB (1998). Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum, implications for red cell invasion. J Cell Sci 111, 1831-1839. (Pubitemid 28370528)
23. Plattner F, Yarovinsky F, Romero S, Didry D, Carlier MF, Sher A, Soldati-Favre D (2008). Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 3, 77-87. (Pubitemid 351201784)
24. Poupel O, Tardieux I (1999). Toxoplasma gondii motility and host cell invasiveness are drastically impaired by jasplakinolide, a cyclic peptide stabilizing F-actin. Microb Infect 1, 653-662.
25. Rodrigues CO, Ruiz FA, Rohloff P, Scott DA, Moreno SNJ (2002). Characterization of isolated acidocalcisomes from Toxoplasma gondii tachyzoites reveals a novel pool of hydrolyzable polyphosphate. J Biol Chem 277, 48650-48656. (Pubitemid 35470828)
26. Roos DS, Donald RGK, Morrissette NS, Moulton AL (1994). Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 45, 28-61.
27. Sahoo N, Beatty WL, Heuser JE, Sept D, Sibley LD (2006). Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii. Mol Biol Cell 17, 895-906. (Pubitemid 43191122)
28. Schachtele C, Seifert R, Osswald H (1988). Stimulus-dependent inhibition of platelet aggregation by the protein kinase C inhibitors polymyxin B, H-7 and staurosporine. Biochem Biophys Res Commun 151, 542-547. (Pubitemid 18074189)
29. Schmitz S, Grainger M, Howell SA, Calder LJ, Gaeb M, Pinder JC, Holder AA, Veigel C (2005). Malaria parasite actin filaments are very short. J Mol Biol 349, 113-125. (Pubitemid 40616452)
30. Schüler H, Matuschewski K (2006). Regulation of apicomplexan microfilament dynamics by minimal set of actin-binding proteins. Traffic 7, 1433-1439. (Pubitemid 44524516)
31. Schuler H, Mueller AK, Matuschewski K (2005). A Plasmodium actin-depolymerizing factor that binds exclusively to actin monomers. Mol Biol Cell 16, 4013-4023. (Pubitemid 41262874)
32. Shaw MK, Tilney LG (1999). Induction of an acrosomal process in Toxoplasma gondii: Visualization of actin filaments in a protozoan parasite. Proc Natl Acad Sci USA 96, 9095-9099. (Pubitemid 29374713)
33. Sibley LD (2004). Invasion strategies of intracellular parasites. Science 304, 248-253.
34. Starnes GL, Jewett TJ, Carruthers VB, Sibley LD (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. (Pubitemid 44582130)
35. Wetzel DM, Chen LA, Ruiz FA, Moreno SNJ, Sibley LD (2004). Calcium-mediated protein secretion potentiates motility by Toxoplasma gondii. J Cell Sci 117, 5739-5748. (Pubitemid 40123941)
36. Wetzel DM, Håkansson S, Hu K, Roos DS, Sibley LD (2003). Actin filament polymerization regulates gliding motility by apicomplexan parasites. Mol Biol Cell 14, 396-406. (Pubitemid 36237004)
37. Wetzel DM, Schmidt J, Kuhlenschmidt M, Dubey JP, Sibley LD (2005). Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect Immun 73, 5379-5387. (Pubitemid 41192971)
38. Yamashiro S, Mohri K, Ono S (2005). The two Caenorhabditis elegans actin-depolymerizing factor/cofilin proteins differently enhance actin filament severing and depolymerization. Biochemistry 44, 14238-14247. (Pubitemid 41533048)