Determination of protein subcellular localization in apicomplexan parasites

Trends in Parasitology

Volumn 28, Issue 12, 2012, Pages 546-554

  Woodcroft, Ben J ^a,b   McMillan, Paul J ^a,c   Dekiwadia, Chaitali ^a   Tilley, Leann ^a,c   Ralph, Stuart A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Antibody; Apicomplexa; Cell biology; GFP; Microscopy; Organelles; Plasmodium; Subcellular localization; Toxoplasma

Indexed keywords

APICOMPLEXAN PROTEIN; MICROORGANISM PROTEIN; UNCLASSIFIED DRUG;

ANTIBODY DETECTION; APICOMPLEXA; BIOINFORMATICS; GENETIC TRANSFECTION; HOST CELL; MICROSCOPY; PROTEIN LOCALIZATION; REVIEW; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; APICOMPLEXA; CELL BIOLOGY; CYTOLOGICAL TECHNIQUES; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; HUMANS; MICROSCOPY; PROTEIN TRANSPORT; PROTOZOAN PROTEINS;

ANIMALIA; APICOMPLEXA; PLASMODIUM (APICOMPLEXA); TOXOPLASMA; TOXOPLASMA GONDII;

EID: 84869160694     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2012.08.008     Document Type: Review

References (90)

1. World Health Organization (2011) World Malaria Report 2011, World Health Organization.
2. Murray C.J., et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012, 379:413-431.
3. Innes E.A. A brief history and overview of Toxoplasma gondii. Zoonoses Public Health 2010, 57:1-7.
4. Chalmers R.M., Giles M. Zoonotic cryptosporidiosis in the UK - challenges for control. J. Appl. Microbiol. 2010, 109:1487-1497.
5. Suarez C.E., Noh S. Emerging perspectives in the research of bovine babesiosis and anaplasmosis. Vet. Parasitol. 2011, 180:109-125.
6. McFadden G.I., et al. Plastid in human parasites. Nature 1996, 381:482.
7. Köhler S., et al. A plastid of probable green algal origin in apicomplexan parasites. Science 1997, 275:1485-1488.
8. Dubremetz J. L'ultrastructure du centriole et du centrocône chez la coccidie Eimeria necatrix. étude au cours de la schizogonie. J. Microsc. 1971, 12:453-458.
9. Ravindran S., Boothroyd J.C. Secretion of proteins into host cells by Apicomplexan parasites. Traffic 2008, 9:647-656.
10. Hu G., et al. Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nat. Biotechnol. 2010, 28:91-98.
11. Volz J., et al. Potential epigenetic regulatory proteins localise to distinct nuclear sub-compartments in Plasmodium falciparum. Int. J. Parasitol. 2010, 40:109-121.
12. Graewe S., et al. Hostile takeover by Plasmodium: reorganization of parasite and host cell membranes during liver stage egress. PLoS Pathog. 2011, 7:e1002224.
13. Pedroni M.J., et al. Babesia bovis: a bipartite signal directs the glutamyl-tRNA synthetase to the apicoplast. Exp. Parasitol. 2012, 131:261-266.
14. Donald R.G., Roos D.S. Stable molecular transformation of Toxoplasma gondii: a selectable dihydrofolate reductase-thymidylate synthase marker based on drug-resistance mutations in malaria. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:11703-11707.
15. Wu Y., et al. Transfection of Plasmodium falciparum within human red blood cells. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:973-977.
16. van Dijk M.R., et al. Stable transfection of malaria parasite blood stages. Science 1995, 268:1358-1362.
17. Beckers C.J., et al. The expression of Toxoplasma proteins in Neospora caninum and the identification of a gene encoding a novel rhoptry protein. Mol. Biochem. Parasitol. 1997, 89:209-223.
18. Gaji R.Y., et al. Molecular genetic transfection of the coccidian parasite Sarcocystis neurona. Mol. Biochem. Parasitol. 2006, 150:1-9.
19. Suarez C.E., McElwain T.F. Stable expression of a GFP-BSD fusion protein in Babesia bovis merozoites. Int. J. Parasitol. 2009, 39:289-297.
20. Yan W., et al. Stable transfection of Eimeria tenella: constitutive expression of the YFP-YFP molecule throughout the life cycle. Int. J. Parasitol. 2009, 39:109-117.
21. Li W., et al. Transient transfection of Cryptosporidium parvum using green fluorescent protein (GFP) as a marker. Mol. Biochem. Parasitol. 2009, 168:143-148.
22. Adamson R., et al. Transient transfection of Theileria annulata. Mol. Biochem. Parasitol. 2001, 114:53-61.
23. Pfahler J.M., et al. Transient transfection of Plasmodium vivax blood stage parasites. Mol. Biochem. Parasitol. 2006, 149:99-101.
24. Hasenkamp S., et al. Comparison of the absolute and relative efficiencies of electroporation-based transfection protocols for Plasmodium falciparum. Malar. J. 2012, 11:210.
25. Gardner M.J., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
26. Nkrumah L.J., et al. Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat. Methods 2006, 3:615-621.
27. Iwanaga S., et al. Centromere plasmid: a new genetic tool for the study of Plasmodium falciparum. PLoS ONE 2012, 7:e33326.
28. Caro F., et al. Plate-based transfection and culturing technique for genetic manipulation of Plasmodium falciparum. Malar. J. 2012, 11:22.
29. Hall N., et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 2005, 307:82-86.
30. Pfander C., et al. A scalable pipeline for highly effective genetic modification of a malaria parasite. Nat. Methods 2011, 8:1078-1082.
31. Kooij T.W., et al. Expansion of experimental genetics approaches for Plasmodium berghei with versatile transfection vectors. Mol. Biochem. Parasitol. 2012, 185:19-26.
32. Jambou R., et al. In vitro culture of Plasmodium berghei-ANKA maintains infectivity of mouse erythrocytes inducing cerebral malaria. Malar. J. 2011, 10:346.
33. Brooks C.F., et al. The toxoplasma apicoplast phosphate translocator links cytosolic and apicoplast metabolism and is essential for parasite survival. Cell Host Microbe 2010, 7:62-73.
34. Fox B.A., et al. Efficient gene replacements in Toxoplasma gondii strains deficient for nonhomologous end joining. Eukaryot. Cell 2009, 8:520-529.
35. Huynh M.H., Carruthers V.B. Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot. Cell 2009, 8:530-539.
36. Striepen B., et al. Expression, selection, and organellar targeting of the green fluorescent protein in Toxoplasma gondii. Mol. Biochem. Parasitol. 1998, 92:328-338.
37. Tilley L., et al. Illuminating Plasmodium falciparum-infected red blood cells. Trends Parasitol. 2007, 23:268-277.
38. Gruring C., et al. Development and host cell modifications of Plasmodium falciparum blood stages in four dimensions. Nat. Commun. 2011, 2:165.
39. Crivat G., et al. Tetracysteine-based fluorescent tags to study protein localization and trafficking in Plasmodium falciparum-infected erythrocytes. PLoS ONE 2011, 6:e22975.
40. van Dooren G.G., et al. Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:13574-13579.
41. Lodoen M.B., et al. A highly sensitive FRET-based approach reveals secretion of the actin-binding protein toxofilin during Toxoplasma gondii infection. Cell. Microbiol. 2010, 12:55-66.
42. Cruz L.N., et al. FRET peptides reveal differential proteolytic activation in intraerythrocytic stages of the malaria parasites Plasmodium berghei and Plasmodium yoelii. Int. J. Parasitol. 2011, 41:363-372.
43. Karsten V., et al. Targeting the secretory pathway of Toxoplasma gondii. Methods 1997, 13:103-111.
44. Harris P.K., et al. Molecular identification of a malaria merozoite surface sheddase. PLoS Pathog. 2005, 1:241-251.
45. Bradley P.J., et al. Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J. Biol. Chem. 2005, 280:34245-34258.
46. Bromley E., et al. Defining the protein repertoire of microneme secretory organelles in the apicomplexan parasite Eimeria tenella. Proteomics 2003, 3:1553-1561.
47. Vincensini L., et al. Proteomic analysis identifies novel proteins of the Maurer's clefts, a secretory compartment delivering Plasmodium falciparum proteins to the surface of its host cell. Mol. Cell. Proteomics 2005, 4:582-593.
48. Swedlow J.R., et al. Measuring tubulin content in Toxoplasma gondii: a comparison of laser-scanning confocal and wide-field fluorescence microscopy. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:2014-2019.
49. Wickham M.E., et al. Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J. 2001, 20:5636-5649.
50. Klonis N., et al. Fluorescence photobleaching analysis for the study of cellular dynamics. Eur. Biophys. J. 2002, 31:36-51.
51. Tawk L., et al. Phosphatidylinositol 3-monophosphate is involved in toxoplasma apicoplast biogenesis. PLoS Pathog. 2011, 7:e1001286.
52. Cervantes S., et al. High content live cell imaging for the discovery of new antimalarial marine natural products. BMC Infect. Dis. 2012, 12:1.
53. Sharling L., et al. A screening pipeline for antiparasitic agents targeting Cryptosporidium inosine monophosphate dehydrogenase. PLoS Negl. Trop. Dis. 2010, 4:e794.
54. Chen S.C., et al. Automated image analysis of protein localization in budding yeast. Bioinformatics 2007, 23:i66-i71.
55. Galbraith C.G., Galbraith J.A. Super-resolution microscopy at a glance. J. Cell Sci. 2011, 124:1607-1611.
56. Riglar D.T., et al. Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe 2011, 9:9-20.
57. Hanssen E., et al. Cellular architecture of Plasmodium falciparum-infected erythrocytes. Int. J. Parasitol. 2010, 40:1127-1135.
58. Yeoman J.A., et al. Tracking glideosome-associated protein-50 reveals the development and organization of the inner membrane complex of P. falciparum. Eukaryot. Cell 2011, 10:556-564.
59. Angrisano F., et al. Spatial localisation of actin filaments across developmental stages of the malaria parasite. PLoS ONE 2012, 7:e32188.
60. Aikawa M., Thompson P.E. Localization of acid phosphatase activity in Plasmodium berghei and P. gallinaceum: an electron microscopic observation. J. Parasitol. 1971, 57:603-610.
61. Aikawa M., et al. Caveola-vesicle complexes in the plasmalemma of erythrocytes infected by Plasmodium vivax and P. cynomolgi. Unique structures related to Schuffner's dots. Am. J. Pathol. 1975, 79:285-300.
62. Bannister L.H., Kent A.P. Immunoelectron microscopic localization of antigens in malaria parasites. Methods Mol. Biol. 1993, 21:415-429.
63. Hanssen E., et al. Electron tomography of the Maurer's cleft organelles of Plasmodium falciparum-infected erythrocytes reveals novel structural features. Mol. Microbiol. 2008, 67:703-718.
64. Tilley L., et al. The twists and turns of Maurer's cleft trafficking in P. falciparum-infected erythrocytes. Traffic 2008, 9:187-197.
65. Engelhardt P., et al. Whole-mount immunoelectron tomography of chromosomes and cells. Methods Mol. Biol. 2007, 369:387-405.
66. Nixon S.J., et al. A single method for cryofixation and correlative light, electron microscopy and tomography of zebrafish embryos. Traffic 2009, 10:131-136.
67. Delorme-Walker, V. et al. (2012) Toxofilin upregulates the host cortical actin cytoskeleton dynamics facilitating Toxoplasma invasion. J. Cell Sci., doi:10.1242/jcs.103648.
68. Tokumasu F., Dvorak J. Development and application of quantum dots for immunocytochemistry of human erythrocytes. J. Microsc. 2003, 211:256-261.
69. Ku M.J., et al. Quantum dots: a new tool for anti-malarial drug assays. Malar. J. 2011, 10:118.
70. Yang H., et al. A quick and parallel analytical method based on quantum dots labeling for ToRCH-related antibodies. Nanoscale Res. Lett. 2009, 4:1469-1474.
71. Williams G.J., et al. High-resolution X-ray imaging of Plasmodium falciparum-infected red blood cells. Cytometry A 2008, 73:949-957.
72. Hanssen E., et al. Cryo transmission X-ray imaging of the malaria parasite, P. falciparum. J. Struct. Biol. 2011, 173:161-168.
73. Kapishnikov S., et al. Aligned hemozoin crystals in curved clusters in malarial red blood cells revealed by nanoprobe X-ray Fe fluorescence and diffraction. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:11188-11193.
74. Foth B.J., et al. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 2003, 299:705-708.
75. Zuegge J., et al. Deciphering apicoplast targeting signals - feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene 2001, 280:19-26.
76. Cilingir G., et al. ApicoAP: the first computational model for identifying apicoplast-targeted proteins in multiple species of Apicomplexa. PLoS ONE 2012, 7:e36598.
77. Sheiner L., et al. A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor. PLoS Pathog. 2011, 7:e1002392.
78. Bender A., et al. Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum. Mol. Biochem. Parasitol. 2003, 132:59-66.
79. Chen Y.L., et al. Using increment of diversity to predict mitochondrial proteins of malaria parasite: integrating pseudo-amino acid composition and structural alphabet. Amino Acids 2012, 42:1309-1316.
80. Petersen T.N., et al. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786.
81. Sargeant T.J., et al. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol. 2006, 7:R12.
82. Verma R., et al. Identification of proteins secreted by malaria parasite into erythrocyte using SVM and PSSM profiles. BMC Bioinformatics 2008, 9:201.
83. Buchholz K.R., et al. Identification of tissue cyst wall components by transcriptome analysis of in vivo and in vitro Toxoplasma gondii bradyzoites. Eukaryot. Cell 2011, 10:1637-1647.
84. Young J.A., et al. The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol. Biochem. Parasitol. 2005, 143:67-79.
85. Brehelin L., et al. PlasmoDraft: a database of Plasmodium falciparum gene function predictions based on postgenomic data. BMC Bioinformatics 2008, 9:440.
86. Prat Y., et al. Recovering key biological constituents through sparse representation of gene expression. Bioinformatics 2011, 27:655-661.
87. Ashburner M., et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 2000, 25:25-29.
88. Gubbels M.J., et al. Fluorescent protein tagging in Toxoplasma gondii: identification of a novel inner membrane complex component conserved among Apicomplexa. Mol. Biochem. Parasitol. 2004, 137:99-110.
89. Shaner N.C., et al. A guide to choosing fluorescent proteins. Nat. Methods 2005, 2:905-909.
90. Sullivan W.J., et al. IMP dehydrogenase from the protozoan parasite Toxoplasma gondii. Antimicrob. Agents Chemother. 2005, 49:2172-2179.