The phosphoproteomes of plasmodium falciparum and toxoplasma gondii reveal unusual adaptations within and beyond the parasites' boundaries

Cell Host and Microbe

Volumn 10, Issue 4, 2011, Pages 410-419

  Treeck, Moritz ^a   Sanders, John L ^a   Elias, Joshua E ^a   Boothroyd, John C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME;

ARTICLE; LIQUID CHROMATOGRAPHY; NONHUMAN; PEPTIDE ANALYSIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SCHIZONT; TACHYZOITE; TANDEM MASS SPECTROMETRY; TOXOPLASMA GONDII;

ADAPTATION, BIOLOGICAL; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION REGULATION; MASS SPECTROMETRY; PHOSPHOPROTEINS; PHOSPHORYLATION; PLASMODIUM FALCIPARUM; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; SIGNAL TRANSDUCTION; TOXOPLASMA;

PLASMODIUM FALCIPARUM; TOXOPLASMA GONDII;

EID: 80054901700     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2011.09.004     Document Type: Article

References (54)

1. K. Abe, A. Aoyagi, and H. Saito Sustained phosphorylation of mitogen-activated protein kinase is required for basic fibroblast growth factor-mediated axonal branch formation in cultured rat hippocampal neurons Neurochem. Int. 38 2001 309 315 (Pubitemid 32012991)
2. S.A. Beausoleil, J. Villén, S.A. Gerber, J. Rush, and S.P. Gygi A probability-based approach for high-throughput protein phosphorylation analysis and site localization Nat. Biotechnol. 24 2006 1285 1292 (Pubitemid 44564776)
3. O. Billker, S. Lourido, and L.D. Sibley Calcium-dependent signaling and kinases in apicomplexan parasites Cell Host Microbe 5 2009 612 622
4. B. Bodenmiller, L.N. Mueller, M. Mueller, B. Domon, and R. Aebersold Reproducible isolation of distinct, overlapping segments of the phosphoproteome Nat. Methods 4 2007 231 237 (Pubitemid 46358873)
5. J.C. Boothroyd, and J.F. Dubremetz Kiss and spit: the dual roles of Toxoplasma rhoptries Nat. Rev. Microbiol. 6 2008 79 88 (Pubitemid 350286222)
6. K.L. Carey, A.M. Jongco, K. Kim, and G.E. Ward The Toxoplasma gondii rhoptry protein ROP4 is secreted into the parasitophorous vacuole and becomes phosphorylated in infected cells Eukaryot. Cell 3 2004 1320 1330 (Pubitemid 39385239)
7. A.F. Cowman, and B.S. Crabb Invasion of red blood cells by malaria parasites Cell 124 2006 755 766 (Pubitemid 43261450)
8. B.S. Crabb, T.F. de Koning-Ward, and P.R. Gilson Protein export in Plasmodium parasites: from the endoplasmic reticulum to the vacuolar export machine Int. J. Parasitol. 40 2010 509 513
9. A.K. Dunker, C.J. Brown, J.D. Lawson, L.M. Iakoucheva, and Z. Obradović Intrinsic disorder and protein function Biochemistry 41 2002 6573 6582 (Pubitemid 34547347)
10. J.D. Dunn, S. Ravindran, S.K. Kim, and J.C. Boothroyd The Toxoplasma gondii dense granule protein GRA7 is phosphorylated upon invasion and forms an unexpected association with the rhoptry proteins ROP2 and ROP4 Infect. Immun. 76 2008 5853 5861
11. J.D. Dvorin, D.C. Martyn, S.D. Patel, J.S. Grimley, C.R. Collins, C.S. Hopp, A.T. Bright, S. Westenberger, E. Winzeler, and M.J. Blackman A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes Science 328 2010 910 912
12. H. El Hajj, M. Lebrun, S.T. Arold, H. Vial, G. Labesse, and J.F. Dubremetz ROP18 is a rhoptry kinase controlling the intracellular proliferation of Toxoplasma gondii PLoS Pathog. 3 2007 e14
13. J.E. Elias, and S.P. Gygi Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 4 2007 207 214 (Pubitemid 46358868)
14. J.E. Elias, and S.P. Gygi Target-decoy search strategy for mass spectrometry-based proteomics Methods Mol. Biol. 604 2010 55 71
15. J.K. Eng, A.L. Mccormack, and J.R. Yates An Approach to Correlate Tandem Mass-Spectral Data of Peptides with Amino-Acid-Sequences in a Protein Database J. Am. Soc. Mass Spectrom. 5 1994 976 989
16. S.J. Fentress, M.S. Behnke, I.R. Dunay, M. Mashayekhi, L.M. Rommereim, B.A. Fox, D.J. Bzik, G.A. Taylor, B.E. Turk, and C.F. Lichti Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence Cell Host Microbe 8 2010 484 495
17. M.J. Gardner, N. Hall, E. Fung, O. White, M. Berriman, R.W. Hyman, J.M. Carlton, A. Pain, K.E. Nelson, and S. Bowman Genome sequence of the human malaria parasite Plasmodium falciparum Nature 419 2002 498 511
18. L.A. Gilbert, S. Ravindran, J.M. Turetzky, J.C. Boothroyd, and P.J. Bradley Toxoplasma gondii targets a protein phosphatase 2C to the nuclei of infected host cells Eukaryot. Cell 6 2007 73 83 (Pubitemid 46147654)
19. F. Gnad, F. Forner, D.F. Zielinska, E. Birney, J. Gunawardena, and M. Mann Evolutionary constraints of phosphorylation in eukaryotes, prokaryotes, and mitochondria Mol. Cell. Proteomics 9 2010 2642 2653
20. J.L. Green, R.R. Rees-Channer, S.A. Howell, S.R. Martin, E. Knuepfer, H.M. Taylor, M. Grainger, and A.A. Holder The motor complex of Plasmodium falciparum: phosphorylation by a calcium-dependent protein kinase J. Biol. Chem. 283 2008 30980 30989
21. S. Haase, and T.F. de Koning-Ward New insights into protein export in malaria parasites Cell. Microbiol. 12 2010 580 587
22. E.L. Huttlin, M.P. Jedrychowski, J.E. Elias, T. Goswami, R. Rad, S.A. Beausoleil, J. Villén, W. Haas, M.E. Sowa, and S.P. Gygi A tissue-specific atlas of mouse protein phosphorylation and expression Cell 143 2010 1174 1189
23. L.M. Iakoucheva, P. Radivojac, C.J. Brown, T.R. O'Connor, J.G. Sikes, Z. Obradovic, and A.K. Dunker The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Res. 32 2004 1037 1049 (Pubitemid 38854704)
24. J.L. Jiménez, B. Hegemann, J.R. Hutchins, J.M. Peters, and R. Durbin A systematic comparative and structural analysis of protein phosphorylation sites based on the mtcPTM database Genome Biol. 8 2007 R90
25. B.R. Joyce, S.F. Queener, R.C. Wek, and W.J. Sullivan Jr. Phosphorylation of eukaryotic initiation factor-2alpha promotes the extracellular survival of obligate intracellular parasite Toxoplasma gondii Proc. Natl. Acad. Sci. USA 107 2010 17200 17205
26. C. Jung, C.Y. Lee, and M.E. Grigg The SRS superfamily of Toxoplasma surface proteins Int. J. Parasitol. 34 2004 285 296 (Pubitemid 38299179)
27. K. Leykauf, M. Treeck, P.R. Gilson, T. Nebl, T. Braulke, A.F. Cowman, T.W. Gilberger, and B.S. Crabb Protein kinase a dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite PLoS Pathog. 6 2010 e1000941
28. W.A. Lim, and T. Pawson Phosphotyrosine signaling: evolving a new cellular communication system Cell 142 2010 661 667
29. S. Lourido, J. Shuman, C. Zhang, K.M. Shokat, R. Hui, and L.D. Sibley Calcium-dependent protein kinase 1 is an essential regulator of exocytosis in Toxoplasma Nature 465 2010 359 362
30. R.E. Lyons, R. McLeod, and C.W. Roberts Toxoplasma gondii tachyzoite-bradyzoite interconversion Trends Parasitol. 18 2002 198 201 (Pubitemid 34442589)
31. J. Mok, P.M. Kim, H.Y. Lam, S. Piccirillo, X. Zhou, G.R. Jeschke, D.L. Sheridan, S.A. Parker, V. Desai, and M. Jwa Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs Sci. Signal. 3 2010 ra12
32. R.W. Moon, C.J. Taylor, C. Bex, R. Schepers, D. Goulding, C.J. Janse, A.P. Waters, D.A. Baker, and O. Billker A cyclic GMP signalling module that regulates gliding motility in a malaria parasite PLoS Pathog. 5 2009 e1000599
33. D.G. Mordue, S. Hkansson, I. Niesman, and L.D. Sibley Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways Exp. Parasitol. 92 1999 87 99 (Pubitemid 29370067)
34. I.R. Nett, L. Davidson, D. Lamont, and M.A. Ferguson Identification and specific localization of tyrosine-phosphorylated proteins in Trypanosoma brucei Eukaryot. Cell 8 2009 617 626
35. I.R. Nett, D.M. Martin, D. Miranda-Saavedra, D. Lamont, J.D. Barber, A. Mehlert, and M.A. Ferguson The phosphoproteome of bloodstream form Trypanosoma brucei, causative agent of African sleeping sickness Mol. Cell. Proteomics 8 2009 1527 1538
36. M.C. Nunes, J.P. Goldring, C. Doerig, and A. Scherf A novel protein kinase family in Plasmodium falciparum is differentially transcribed and secreted to various cellular compartments of the host cell Mol. Microbiol. 63 2007 391 403 (Pubitemid 46058927)
37. J.V. Olsen, M. Vermeulen, A. Santamaria, C. Kumar, M.L. Miller, L.J. Jensen, F. Gnad, J. Cox, T.S. Jensen, and E.A. Nigg Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis Sci. Signal. 3 2010 ra3
38. Y.C. Ong, M.L. Reese, and J.C. Boothroyd Toxoplasma rhoptry protein 16 (ROP16) subverts host function by direct tyrosine phosphorylation of STAT6 J. Biol. Chem. 285 2010 28731 28740
39. L. Peixoto, F. Chen, O.S. Harb, P.H. Davis, D.P. Beiting, C.S. Brownback, D. Ouloguem, and D.S. Roos Integrative genomic approaches highlight a family of parasite-specific kinases that regulate host responses Cell Host Microbe 8 2010 208 218
40. M.L. Reese, and J.C. Boothroyd A helical membrane-binding domain targets the Toxoplasma ROP2 family to the parasitophorous vacuole Traffic 10 2009 1458 1470
41. J.P. Saeij, J.P. Boyle, S. Coller, S. Taylor, L.D. Sibley, E.T. Brooke-Powell, J.W. Ajioka, and J.C. Boothroyd Polymorphic secreted kinases are key virulence factors in toxoplasmosis Science 314 2006 1780 1783 (Pubitemid 44969090)
42. J.P. Saeij, S. Coller, J.P. Boyle, M.E. Jerome, M.W. White, and J.C. Boothroyd Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue Nature 445 2007 324 327 (Pubitemid 46122820)
43. D. Schwartz, and S.P. Gygi An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets Nat. Biotechnol. 23 2005 1391 1398 (Pubitemid 41679391)
44. T. Spielmann, and T.W. Gilberger Protein export in malaria parasites: do multiple export motifs add up to multiple export pathways? Trends Parasitol. 26 2010 6 10
45. T. Steinfeldt, S. Könen-Waisman, L. Tong, N. Pawlowski, T. Lamkemeyer, L.D. Sibley, J.P. Hunn, and J.C. Howard Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii PLoS Biol. 8 2010 e1000576
46. T. Sugi, K. Kato, K. Kobayashi, S. Watanabe, H. Kurokawa, H. Gong, K. Pandey, H. Takemae, and H. Akashi Use of the kinase inhibitor analog 1NM-PP1 reveals a role for Toxoplasma gondii CDPK1 in the invasion step Eukaryot. Cell 9 2010 667 670
47. C.S. Tan, B. Bodenmiller, A. Pasculescu, M. Jovanovic, M.O. Hengartner, C. Jørgensen, G.D. Bader, R. Aebersold, T. Pawson, and R. Linding Comparative analysis reveals conserved protein phosphorylation networks implicated in multiple diseases Sci. Signal. 2 2009 ra39
48. R. Tewari, U. Straschil, A. Bateman, U. Böhme, I. Cherevach, P. Gong, A. Pain, and O. Billker The systematic functional analysis of Plasmodium protein kinases identifies essential regulators of mosquito transmission Cell Host Microbe 8 2010 377 387
49. M. Treeck, S. Zacherl, S. Herrmann, A. Cabrera, M. Kono, N.S. Struck, K. Engelberg, S. Haase, F. Frischknecht, and K. Miura Functional analysis of the leading malaria vaccine candidate AMA-1 reveals an essential role for the cytoplasmic domain in the invasion process PLoS Pathog. 5 2009 e1000322
50. J. Villén, and S.P. Gygi The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry Nat. Protoc. 3 2008 1630 1638
51. P. Ward, L. Equinet, J. Packer, and C. Doerig Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote BMC Genomics 5 2004 79
52. J.M. Wilkes, and C. Doerig The protein-phosphatome of the human malaria parasite Plasmodium falciparum BMC Genomics 9 2008 412
53. M. Yamamoto, D.M. Standley, S. Takashima, H. Saiga, M. Okuyama, H. Kayama, E. Kubo, H. Ito, M. Takaura, and T. Matsuda A single polymorphic amino acid on Toxoplasma gondii kinase ROP16 determines the direct and strain-specific activation of Stat3 J. Exp. Med. 206 2009 2747 2760
54. M. Zhang, C. Fennell, L. Ranford-Cartwright, R. Sakthivel, P. Gueirard, S. Meister, A. Caspi, C. Doerig, R.S. Nussenzweig, and R. Tuteja The Plasmodium eukaryotic initiation factor-2alpha kinase IK2 controls the latency of sporozoites in the mosquito salivary glands J. Exp. Med. 207 2010 1465 1474