The plasmodium falciparum schizont phosphoproteome reveals extensive phosphatidylinositol and cAMP-protein kinase A signaling

Journal of Proteome Research

Volumn 11, Issue 11, 2012, Pages 5323-5337

  Lasonder, Edwin ^a   Green, Judith L ^b   Camarda, Grazia ^c   Talabani, Hana ^d   Holder, Anthony A ^b   Langsley, Gordon ^d   Alano, Pietro ^c  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d INSTITUT COCHIN   (France)

Author keywords

inositol PKA signalling pathways; malaria; phosphoproteome; schizonts

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; PHOSPHATIDYLINOSITOL;

ARTICLE; CELL INVASION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ERYTHROCYTE; MEROZOITE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SCHIZONT; SIGNAL TRANSDUCTION;

ANIMALS; CHROMATOGRAPHY, LIQUID; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; PHOSPHATIDYLINOSITOLS; PHOSPHOPROTEINS; PLASMODIUM FALCIPARUM; PROTEOME; PROTOZOAN PROTEINS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

PLASMODIUM FALCIPARUM;

EID: 84868332245     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300557m     Document Type: Article

References (59)

1. Gerald, N.; Mahajan, B.; Kumar, S. Mitosis in the human malaria parasite Plasmodium falciparum Eukaryotic Cell 2011, 10 (4) 474-82
2. Holder, A. A.; Mohd Ridzuan, M. A.; Green, J. L. Calcium dependent protein kinase 1 and calcium fluxes in the malaria parasite Microbes Infect. 2012, 14 (10) 825-30
3. Doerig, C.; Abdi, A.; Bland, N.; Eschenlauer, S.; Dorin-Semblat, D.; Fennell, C.; Halbert, J.; Holland, Z.; Nivez, M. P.; Semblat, J. P.; Sicard, A.; Reininger, L. Malaria: targeting parasite and host cell kinomes Biochim. Biophys. Acta 2010, 1804 (3) 604-12
4. Doerig, C.; Baker, D.; Billker, O.; Blackman, M. J.; Chitnis, C.; Dhar Kumar, S.; Heussler, V.; Holder, A. A.; Kocken, C.; Krishna, S.; Langsley, G.; Lasonder, E.; Menard, R.; Meissner, M.; Pradel, G.; Ranford-Cartwright, L.; Sharma, A.; Sharma, P.; Tardieux, T.; Tatu, U.; Alano, P. Signalling in malaria parasites. The MALSIG consortium Parasite 2009, 16 (3) 169-82
5. Koyama, F. C.; Chakrabarti, D.; Garcia, C. R. Molecular machinery of signal transduction and cell cycle regulation in Plasmodium Mol. Biochem. Parasitol. 2009, 165 (1) 1-7
6. Anamika; Srinivasan, N.; Krupa, A. A genomic perspective of protein kinases in Plasmodium falciparum Proteins 2005, 58 (1) 180-9
7. Ward, P.; Equinet, L.; Packer, J.; Doerig, C. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote BMC Genomics 2004, 5, 79
8. Solyakov, L.; Halbert, J.; Alam, M. M.; Semblat, J. P.; Dorin-Semblat, D.; Reininger, L.; Bottrill, A. R.; Mistry, S.; Abdi, A.; Fennell, C.; Holland, Z.; Demarta, C.; Bouza, Y.; Sicard, A.; Nivez, M. P.; Eschenlauer, S.; Lama, T.; Thomas, D. C.; Sharma, P.; Agarwal, S.; Kern, S.; Pradel, G.; Graciotti, M.; Tobin, A. B.; Doerig, C. Global kinomic and phospho-proteomic analyses of the human malaria parasite Plasmodium falciparum Nat. Commun. 2011, 2, 565
9. Leykauf, K.; Treeck, M.; Gilson, P. R.; Nebl, T.; Braulke, T.; Cowman, A. F.; Gilberger, T. W.; Crabb, B. S. Protein kinase a dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite PLoS Pathog. 2010, 6 (6) e1000941
10. Merckx, A.; Nivez, M. P.; Bouyer, G.; Alano, P.; Langsley, G.; Deitsch, K.; Thomas, S.; Doerig, C.; Egee, S. Plasmodium falciparum regulatory subunit of cAMP-dependent PKA and anion channel conductance PLoS Pathog. 2008, 4 (2) e19
11. Shewan, A.; Eastburn, D. J.; Mostov, K. Phosphoinositides in cell architecture Cold Spring Harbor Perspect. Biol. 2011, 3 (8) a004796
12. Janetopoulos, C.; Devreotes, P. Phosphoinositide signaling plays a key role in cytokinesis J. Cell Biol. 2006, 174 (4) 485-90
13. Di Paolo, G.; De Camilli, P. Phosphoinositides in cell regulation and membrane dynamics Nature 2006, 443 (7112) 651-7
14. Diella, F.; Cameron, S.; Gemund, C.; Linding, R.; Via, A.; Kuster, B.; Sicheritz-Ponten, T.; Blom, N.; Gibson, T. J. Phospho.ELM: a database of experimentally verified phosphorylation sites in eukaryotic proteins BMC Bioinf. 2004, 5, 79
15. Gnad, F.; Gunawardena, J.; Mann, M. PHOSIDA 2011: the posttranslational modification database Nucleic Acids Res. 2011, 39 (Database issue) D253-60
16. Pantaleo, A.; Ferru, E.; Carta, F.; Mannu, F.; Giribaldi, G.; Vono, R.; Lepedda, A. J.; Pippia, P.; Turrini, F. Analysis of changes in tyrosine and serine phosphorylation of red cell membrane proteins induced by P. falciparum growth Proteomics 2010, 10 (19) 3469-79
17. Wu, Y.; Nelson, M. M.; Quaile, A.; Xia, D.; Wastling, J. M.; Craig, A. Identification of phosphorylated proteins in erythrocytes infected by the human malaria parasite Plasmodium falciparum Malar. J. 2009, 8, 105
18. Walliker, D.; Quakyi, I. A.; Wellems, T. E.; McCutchan, T. F.; Szarfman, A.; London, W. T.; Corcoran, L. M.; Burkot, T. R.; Carter, R. Genetic analysis of the human malaria parasite Plasmodium falciparum Science 1987, 236 (4809) 1661-6
19. Olivieri, A.; Silvestrini, F.; Sanchez, M.; Alano, P. A 140-bp AT-rich sequence mediates positive and negative transcriptional control of a Plasmodium falciparum developmentally regulated promoter Int. J. Parasitol. 2008, 38 (3-4) 299-312
20. Lasonder, E.; Ishihama, Y.; Andersen, J. S.; Vermunt, A. M.; Pain, A.; Sauerwein, R. W.; Eling, W. M.; Hall, N.; Waters, A. P.; Stunnenberg, H. G.; Mann, M. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry Nature 2002, 419 (6906) 537-42
21. Rappsilber, J.; Ishihama, Y.; Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics Anal. Chem. 2003, 75 (3) 663-70
22. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis Nat. Methods 2009, 6 (5) 359-62
23. Wisniewski, J. R.; Nagaraj, N.; Zougman, A.; Gnad, F.; Mann, M. Brain phosphoproteome obtained by a FASP-based method reveals plasma membrane protein topology J. Proteome Res. 2010, 9 (6) 3280-9
24. Kyono, Y.; Sugiyama, N.; Imami, K.; Tomita, M.; Ishihama, Y. Successive and selective release of phosphorylated peptides captured by hydroxy acid-modified metal oxide chromatography J. Proteome Res. 2008, 7 (10) 4585-93
25. Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 2008, 26 (12) 1367-72
26. Renard, B. Y.; Kirchner, M.; Monigatti, F.; Ivanov, A. R.; Rappsilber, J.; Winter, D.; Steen, J. A.; Hamprecht, F. A.; Steen, H. When less can yield more-Computational preprocessing of MS/MS spectra for peptide identification Proteomics 2009, 9 (21) 4978-84
27. Zhou, Y.; Ramachandran, V.; Kumar, K. A.; Westenberger, S.; Refour, P.; Zhou, B.; Li, F.; Young, J. A.; Chen, K.; Plouffe, D.; Henson, K.; Nussenzweig, V.; Carlton, J.; Vinetz, J. M.; Duraisingh, M. T.; Winzeler, E. A. Evidence-based annotation of the malaria parasite's genome using comparative expression profiling PLoS One 2008, 3 (2) e1570
28. Bauer, S.; Grossmann, S.; Vingron, M.; Robinson, P. N. Ontologizer 2.0-a multifunctional tool for GO term enrichment analysis and data exploration Bioinformatics 2008, 24 (14) 1650-1
29. Huttlin, E. L.; Jedrychowski, M. P.; Elias, J. E.; Goswami, T.; Rad, R.; Beausoleil, S. A.; Villen, J.; Haas, W.; Sowa, M. E.; Gygi, S. P. A tissue-specific atlas of mouse protein phosphorylation and expression Cell 2010, 143 (7) 1174-89
30. Schwartz, D.; Gygi, S. P. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets Nat. Biotechnol. 2005, 23 (11) 1391-8
31. Szklarczyk, D.; Franceschini, A.; Kuhn, M.; Simonovic, M.; Roth, A.; Minguez, P.; Doerks, T.; Stark, M.; Muller, J.; Bork, P.; Jensen, L. J.; von Mering, C. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored Nucleic Acids Res. 2011, 39 (Database issue) D561-8
32. Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N. S.; Wang, J. T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: a software environment for integrated models of biomolecular interaction networks Genome Res. 2003, 13 (11) 2498-504
33. Bader, G. D.; Hogue, C. W. An automated method for finding molecular complexes in large protein interaction networks BMC Bioinf. 2003, 4, 2
34. Green, J. L.; Rees-Channer, R. R.; Howell, S. A.; Martin, S. R.; Knuepfer, E.; Taylor, H. M.; Grainger, M.; Holder, A. A. The motor complex of Plasmodium falciparum: phosphorylation by a calcium-dependent protein kinase J. Biol. Chem. 2008, 283 (45) 30980-9
35. Olsen, J. V.; Mann, M. Improved peptide identification in proteomics by two consecutive stages of mass spectrometric fragmentation Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (37) 13417-22
36. Rigbolt, K. T.; Prokhorova, T. A.; Akimov, V.; Henningsen, J.; Johansen, P. T.; Kratchmarova, I.; Kassem, M.; Mann, M.; Olsen, J. V.; Blagoev, B. System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation Sci. Signaling 2011, 4 (164) rs3
37. Thingholm, T. E.; Jensen, O. N.; Larsen, M. R. Enrichment and separation of mono- and multiply phosphorylated peptides using sequential elution from IMAC prior to mass spectrometric analysis Methods Mol. Biol. 2009, 527, 67-78 xi
38. Treeck, M.; Sanders, J. L.; Elias, J. E.; Boothroyd, J. C. The phosphoproteomes of Plasmodium falciparum and Toxoplasma gondii reveal unusual adaptations within and beyond the parasites' boundaries Cell Host Microbe 2011, 10 (4) 410-9
39. Maiorano, D.; Moreau, J.; Mechali, M. XCDT1 is required for the assembly of pre-replicative complexes in Xenopus laevis Nature 2000, 404 (6778) 622-5
40. Nishitani, H.; Lygerou, Z.; Nishimoto, T.; Nurse, P. The Cdt1 protein is required to license DNA for replication in fission yeast Nature 2000, 404 (6778) 625-8
41. Suganuma, T.; Workman, J. L. Signals and combinatorial functions of histone modifications Annu. Rev. Biochem. 2011, 80, 473-99
42. Campbell, T. L.; De Silva, E. K.; Olszewski, K. L.; Elemento, O.; Llinas, M. Identification and genome-wide prediction of DNA binding specificities for the ApiAP2 family of regulators from the malaria parasite PLoS Pathog. 2010, 6 (10) e1001165
43. Vaid, A.; Thomas, D. C.; Sharma, P. Role of Ca2+/calmodulin-PfPKB signaling pathway in erythrocyte invasion by Plasmodium falciparum J. Biol. Chem. 2008, 283 (9) 5589-97
44. Chaparro-Olaya, J.; Margos, G.; Coles, D. J.; Dluzewski, A. R.; Mitchell, G. H.; Wasserman, M. M.; Pinder, J. C. Plasmodium falciparum myosins: transcription and translation during asexual parasite development Cell Motil. Cytoskeleton 2005, 60 (4) 200-13
45. Pinder, J. C.; Fowler, R. E.; Dluzewski, A. R.; Bannister, L. H.; Lavin, F. M.; Mitchell, G. H.; Wilson, R. J.; Gratzer, W. B. Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: implications for red cell invasion J. Cell Sci. 1998, 111 (Pt 13) 1831-9
46. Singh, S.; Alam, M. M.; Pal-Bhowmick, I.; Brzostowski, J. A.; Chitnis, C. E. Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites PLoS Pathog. 2010, 6 (2) e1000746
47. Pantaleo, A.; Ferru, E.; Carta, F.; Valente, E.; Pippia, P.; Turrini, F. Effect of heterozygous beta thalassemia on the phosphorylative response to Plasmodium falciparum infection J. Proteomics 2012, 10.1016/j.jprot.2012.08.018
48. Brown, J. R.; Auger, K. R. Phylogenomics of phosphoinositide lipid kinases: perspectives on the evolution of second messenger signaling and drug discovery BMC Evol. Biol. 2011, 11, 4
49. Vaid, A.; Ranjan, R.; Smythe, W. A.; Hoppe, H. C.; Sharma, P. PfPI3K, a phosphatidylinositol-3 kinase from Plasmodium falciparum, is exported to the host erythrocyte and is involved in hemoglobin trafficking Blood 2010, 115 (12) 2500-7
50. Bhattacharjee, S.; Stahelin, R. V.; Speicher, K. D.; Speicher, D. W.; Haldar, K. Endoplasmic Reticulum PI(3)P lipid binding targets malaria proteins to the host cell Cell 2012, 148 (1-2) 201-12
51. Dvorin, J. D.; Martyn, D. C.; Patel, S. D.; Grimley, J. S.; Collins, C. R.; Hopp, C. S.; Bright, A. T.; Westenberger, S.; Winzeler, E.; Blackman, M. J.; Baker, D. A.; Wandless, T. J.; Duraisingh, M. T. A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes Science 2010, 328 (5980) 910-2
52. Taylor, H. M.; McRobert, L.; Grainger, M.; Sicard, A.; Dluzewski, A. R.; Hopp, C. S.; Holder, A. A.; Baker, D. A. The malaria parasite cyclic GMP-dependent protein kinase plays a central role in blood-stage schizogony Eukaryotic Cell 2010, 9 (1) 37-45
53. Giovannini, D.; Spath, S.; Lacroix, C.; Perazzi, A.; Bargieri, D.; Lagal, V.; Lebugle, C.; Combe, A.; Thiberge, S.; Baldacci, P.; Tardieux, I.; Menard, R. Independent roles of apical membrane antigen 1 and rhoptry neck proteins during host cell invasion by apicomplexa Cell Host Microbe 2011, 10 (6) 591-602
54. Lamarque, M.; Besteiro, S.; Papoin, J.; Roques, M.; Vulliez-Le Normand, B.; Morlon-Guyot, J.; Dubremetz, J. F.; Fauquenoy, S.; Tomavo, S.; Faber, B. W.; Kocken, C. H.; Thomas, A. W.; Boulanger, M. J.; Bentley, G. A.; Lebrun, M. The RON2-AMA1 interaction is a critical step in moving junction-dependent invasion by apicomplexan parasites PLoS Pathog. 2011, 7 (2) e1001276
55. Richard, D.; MacRaild, C. A.; Riglar, D. T.; Chan, J. A.; Foley, M.; Baum, J.; Ralph, S. A.; Norton, R. S.; Cowman, A. F. Interaction between Plasmodium falciparum apical membrane antigen 1 and the rhoptry neck protein complex defines a key step in the erythrocyte invasion process of malaria parasites J. Biol. Chem. 2010, 285 (19) 14815-22
56. Syin, C.; Parzy, D.; Traincard, F.; Boccaccio, I.; Joshi, M. B.; Lin, D. T.; Yang, X. M.; Assemat, K.; Doerig, C.; Langsley, G. The H89 cAMP-dependent protein kinase inhibitor blocks Plasmodium falciparum development in infected erythrocytes Eur. J. Biochem. 2001, 268 (18) 4842-9
57. Siden-Kiamos, I.; Pinder, J. C.; Louis, C. Involvement of actin and myosins in Plasmodium berghei ookinete motility Mol. Biochem. Parasitol. 2006, 150 (2) 308-17
58. Ono, T.; Cabrita-Santos, L.; Leitao, R.; Bettiol, E.; Purcell, L. A.; Diaz-Pulido, O.; Andrews, L. B.; Tadakuma, T.; Bhanot, P.; Mota, M. M.; Rodriguez, A. Adenylyl cyclase alpha and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection PLoS Pathog. 2008, 4 (2) e1000008
59. Bosch, J.; Turley, S.; Daly, T. M.; Bogh, S. M.; Villasmil, M. L.; Roach, C.; Zhou, N.; Morrisey, J. M.; Vaidya, A. B.; Bergman, L. W.; Hol, W. G. Structure of the MTIP-MyoA complex, a key component of the malaria parasite invasion motor Proc. Natl. Acad. Sci. U. S. A. 2006, 103 (13) 4852-7