Targeted disruption of TgPhiL1 in toxoplasma gondii results in altered parasite morphology and fitness

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Barkhuff, Whittney Dotzler ^a   Gilk, Stacey D ^a   Whitmarsh, Ryan ^b   Tilley, Lucas D ^a   Hunter, Chris ^b   Ward, Gary E ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOTOSENSITIZED 5 IODONAPTHALINE 1 AZIDE I 125 LABELED PROTEIN 1; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APICOMPLEXA; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; FEMALE; GENE SILENCING; GENETIC COMPLEMENTATION; HOMOLOGOUS RECOMBINATION; INNER MEMBRANE COMPLEX; LIVER; MICROBIAL MORPHOLOGY; MOUSE; NONHUMAN; ORTHOLOGY; PARASITE LOAD; PARASITE VIRULENCE; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN DEFECT; PROTEIN FUNCTION; PROTEIN TARGETING; SPLEEN; TACHYZOITE; TOXOPLASMA GONDII; TOXOPLASMOSIS; WILD TYPE; ANIMAL; C57BL MOUSE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PARASITOLOGY; PATHOGENICITY; PROMOTER REGION; TOXOPLASMA; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING;

APICOMPLEXA; MUS; TOXOPLASMA GONDII;

ANIMALS; BLOTTING, WESTERN; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; PROMOTER REGIONS, GENETIC; PROTOZOAN PROTEINS; TOXOPLASMA; TOXOPLASMOSIS;

EID: 80052061997     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023977     Document Type: Article

References (42)

1. Mital J, Ward GE, (2007) Current and Emerging Approaches to Studying Invasion in Apicomplexan Parasites. Subcell Biochem 47: 1-32.
2. Kim K, Weiss LM, (2004) Toxoplasma gondii: the model apicomplexan. Int J Parasitol 34: 423-432.
3. Mann T, Beckers C, (2001) Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii. Mol Biochem Parasitol 115: 257-268.
4. Morrissette NS, Sibley LD, (2002) Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev 66: 21-38.
5. Dubremetz J-F, Torpier G, Maurois P, Prensier G, Sinden R, (1979) [Structure of the sporozoite pellicule of Plasmodium yoelii: a cryofracture study]. C. R. Acad Sci Paris 288: 623-626.
6. Dubremetz JF, Torpier G, (1978) Freeze fracture study of the pellicle of an eimerian sporozoite (Protozoa, Coccidia). J Ultrastruct Res 62: 94-109.
7. Gubbels MJ, Wieffer M, Striepen B, (2004) Fluorescent protein tagging in Toxoplasma gondii: identification of a novel inner membrane complex component conserved among Apicomplexa. Mol Biochem Parasitol 137: 99-110.
8. Anderson-White BR, Ivey FD, Cheng K, Szatanek T, Lorestani A, et al. (2010) A family of intermediate filament-like proteins is sequentially assembled into the cytoskeleton of Toxoplasma gondii. Cell Microbiol 13: 18-31.
9. Hu K, Roos DS, Murray JM, (2002) A novel polymer of tubulin forms the conoid of Toxoplasma gondii. J Cell Biol 156: 1039-1050.
10. Nichols BA, Chiappino ML, (1987) Cytoskeleton of Toxoplasma gondii. J Protozool 34: 217-226.
11. Santos JM, Lebrun M, Daher W, Soldati D, Dubremetz JF, (2009) Apicomplexan cytoskeleton and motors: key regulators in morphogenesis, cell division, transport and motility. Int J Parasitol 39: 153-162.
12. Mann T, Gaskins E, Beckers C, (2002) Proteolytic processing of TgIMC1 during maturation of the membrane skeleton of Toxoplasma gondii. J Biol Chem 277: 41240-41246.
13. Baum J, Richard D, Healer J, Rug M, Krnajski Z, et al. (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.
14. Gaskins E, Gilk S, DeVore N, Mann T, Ward G, et al. (2004) Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J Cell Biol 165: 383-393.
15. Keeley A, Soldati D, (2004) The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends Cell Biol 14: 528-532.
16. Frenal K, Polonais V, Marq JB, Stratmann R, Limenitakis J, et al. (2010) Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe 8: 343-357.
17. Bullen HE, Tonkin CJ, O'Donnell RA, Tham WH, Papenfuss AT, et al. (2009) A novel family of Apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. J Biol Chem 284: 25353-25363.
18. Gilk SD, Raviv Y, Hu K, Murray JM, Beckers CJ, et al. (2006) Identification of PhIL1, a novel cytoskeletal protein of the Toxoplasma gondii pellicle, through photosensitized labeling with 5-[125I]iodonaphthalene-1-azide. Eukaryot Cell 5: 1622-1634.
19. Wichroski MJ, Melton JA, Donahue CG, Tweten RK, Ward GE, (2002) Clostridium septicum alpha-toxin is active against the parasitic protozoan Toxoplasma gondii and targets members of the SAG family of glycosylphosphatidylinositol-anchored surface proteins. Infect Immun 70: 4353-4361.
20. Roos DS, Donald RG, Morrissette NS, Moulton AL, (1994) Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 45: 27-63.
21. Messina M, Niesman I, Mercier C, Sibley LD, (1995) Stable DNA transformation of Toxoplasma gondii using phleomycin selection. Gene 165: 213-217.
22. Hu K, Mann T, Striepen B, Beckers CJ, Roos DS, et al. (2002) Daughter cell assembly in the protozoan parasite Toxoplasma gondii. Mol Biol Cell 13: 593-606.
23. Ward GE, Carey KL, (1999) 96-Well plates providing high optical resolution for high-throughput, immunofluorescence-based screening of monoclonal antibodies against Toxoplasma gondii. J Immunol Methods 230: 11-18.
24. 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 Cytoskeleton 37: 253-262.
25. Beck JR, Rodriguez-Fernandez IA, Cruz de Leon J, Huynh MH, Carruthers VB, et al. (2010) A novel family of Toxoplasma IMC proteins displays a hierarchical organization and functions in coordinating parasite division. PLoS Pathog 6: e1001094.
26. Gubbels MJ, Vaishnava S, Boot N, Dubremetz JF, Striepen B, (2006) A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J Cell Sci 119: 2236-2245.
27. Millonig G, (1961) Advantages of a phosphate buffer for OsO4 solutions in fixation. J Appl Physics 32: 1637.
28. Grigg ME, Boothroyd JC, (2001) Rapid identification of virulent type I strains of the protozoan pathogen Toxoplasma gondii by PCR-restriction fragment length polymorphism analysis at the B1 gene. J Clin Microbiol 39: 398-400.
29. Mital J, Schwarz J, Taatjes DJ, Ward GE, (2006) Laser scanning cytometer-based assays for measuring host cell attachment and invasion by the human pathogen Toxoplasma gondii. Cytometry A 69: 13-19.
30. Mondragon R, Frixione E, (1996) Ca(2+)-dependence of conoid extrusion in Toxoplasma gondii tachyzoites. J Eukaryot Microbiol 43: 120-127.
31. Savage DF, Stroud RM, (2007) Structural basis of aquaporin inhibition by mercury. J Mol Biol 368: 607-617.
32. Miranda K, Pace DA, Cintron R, Rodrigues JC, Fang J, et al. (2010) Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole. Mol Microbiol 76: 1358-1375.
33. Frixione E, Mondragon R, Meza I, (1996) Kinematic analysis of Toxoplasma gondii motility. Cell Motil Cytoskeleton 34: 152-163.
34. Hakansson S, Morisaki H, Heuser J, 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.
35. Sibley LD, (2004) Intracellular parasite invasion strategies. Science 304: 248-253.
36. Khater EI, Sinden RE, Dessens JT, (2004) A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites. J Cell Biol 167: 425-432.
37. Tremp AZ, Khater EI, Dessens JT, (2008) IMC1b is a putative membrane skeleton protein involved in cell shape, mechanical strength, motility, and infectivity of malaria ookinetes. J Biol Chem 283: 27604-27611.
38. Brossier F, Starnes GL, Beatty WL, Sibley LD, (2008) Microneme rhomboid protease TgROM1 is required for efficient intracellular growth of Toxoplasma gondii. Eukaryot Cell 7: 664-674.
39. Turetzky JM, Chu DK, Hajagos BE, Bradley PJ, (2010) Processing and secretion of ROP13: A unique Toxoplasma effector protein. Int J Parasitol 40: 1037-1044.
40. Gilbert LA, Ravindran S, Turetzky JM, Boothroyd JC, Bradley PJ, (2007) Toxoplasma gondii targets a protein phosphatase 2C to the nuclei of infected host cells. Eukaryot Cell 6: 73-83.
41. Fox BA, Ristuccia JG, Gigley JP, Bzik DJ, (2009) Efficient gene replacements in Toxoplasma gondii strains deficient for nonhomologous end joining. Eukaryot Cell 8: 520-529.
42. Huynh MH, Carruthers VB, (2009) Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot Cell 8: 530-539.