Plasmodium falciparum Adhesins Play an Essential Role in Signalling and Activation of Invasion into Human Erythrocytes

PLoS Pathogens

Volumn 11, Issue 12, 2015, Pages

  Tham, Wai Hong ^a,b   Lim, Nicholas T Y ^a,b   Weiss, Greta E ^c   Lopaticki, Sash ^a,b   Ansell, Brendan R E ^a,b   Bird, Megan ^d   Lucet, Isabelle ^a,b,d   Dorin Semblat, Dominique ^e   Doerig, Christian ^d   Gilson, Paul R ^c,d   Crabb, Brendan S ^b,c,d   Cowman, Alan F ^a,b  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

^c BURNET INSTITUTE   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e hôpital Robert Debré et Institut national de la transfusion sanguine   (France)

Author keywords

[No Author keywords available]

Indexed keywords

APICAL MEMBRANE ANTIGEN 1; GLUTATHIONE TRANSFERASE; PHOSPHOTRANSFERASE; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL ACTIVATION; CELL SIGNALING ASSAY; ERYTHROCYTE; GENE MUTATION; GENE SEQUENCE; IMMUNOFLUORESCENCE; MEROZOITE; MOLECULAR CLONING; NONHUMAN; PARASITE GROWTH; PARASITE PHENOMENA AND FUNCTIONS; PLASMODIUM FALCIPARUM; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SCORING SYSTEM; HUMAN; MALARIA FALCIPARUM; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PHOSPHORYLATION;

AMINO ACID SEQUENCE; ERYTHROCYTES; HUMANS; MALARIA, FALCIPARUM; MEROZOITES; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS;

EID: 84953295638     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005343     Document Type: Article

References (38)

1. Tham W-H, Healer J, Cowman AF, Erythrocyte and reticulocyte binding-like proteins of Plasmodium falciparum. Trends Parasitol. 2012;28: 23–30. doi: 10.1016/j.pt.2011.10.002 22178537
2. Gilson PR, Crabb BS, Morphology and kinetics of the three distinct phases of red blood cell invasion by Plasmodium falciparum merozoites. Int J Parasitol. 2009;39: 91–96. doi: 10.1016/j.ijpara.2008.09.007 18952091
3. Cowman AF, Crabb BS, Invasion of red blood cells by malaria parasites. Cell. 2006;124: 755–766. 16497586
4. Riglar DT, Richard D, Wilson DW, Boyle MJ, Dekiwadia C, Turnbull L, et al. Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe. 2011;9: 9–20. doi: 10.1016/j.chom.2010.12.003 21238943
5. Adams JH, Blair PL, Kaneko O, Peterson DS, An expanding ebl family of Plasmodium falciparum. Trends Parasitol. 2001;17: 297–299. 11378038
6. Baum J, Maier AG, Good RT, Simpson KM, Cowman AF, Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog. 2005;1: e37. 16362075
7. Gao X, Gunalan K, Yap SSL, Preiser PR, Triggers of key calcium signals during erythrocyte invasion by Plasmodium falciparum. Nat Commun. 2013;4: 2862. doi: 10.1038/ncomms3862 24280897
8. Singh S, Alam MM, Pal-Bhowmick I, Brzostowski JA, Chitnis CE, Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog. 2010;6: e1000746. doi: 10.1371/journal.ppat.1000746 20140184
9. Leykauf K, Treeck M, Gilson PR, Nebl T, Braulke T, Cowman AF, et al. 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: e1000941. doi: 10.1371/journal.ppat.1000941 20532217
10. Treeck M, Zacherl S, Herrmann S, Cabrera A, Kono M, Struck NS, et al. Functional analysis of the leading malaria vaccine candidate AMA-1 reveals an essential role for the cytoplasmic domain in the invasion process. PLoS Pathog. 2009;5: e1000322. doi: 10.1371/journal.ppat.1000322 19283086
11. Tyler JS, Treeck M, Boothroyd JC, Focus on the ringleader: the role of AMA1 in apicomplexan invasion and replication. Trends Parasitol. 2011;27: 410–420. doi: 10.1016/j.pt.2011.04.002 21659001
12. Gilberger T-W, Thompson JK, Triglia T, Good RT, Duraisingh MT, Cowman AF, A novel erythrocyte binding antigen-175 paralogue from Plasmodium falciparum defines a new trypsin-resistant receptor on human erythrocytes. J Biol Chem. 2003;278: 14480–14486. 12556470
13. Dvorin JD, Bei AK, Coleman BI, Duraisingh MT, Functional diversification between two related Plasmodium falciparum merozoite invasion ligands is determined by changes in the cytoplasmic domain. Mol Microbiol. 2010;75: 990–1006. doi: 10.1111/j.1365-2958.2009.07040.x 20487292
14. Engelberg K, Paul AS, Prinz B, Kono M, Ching W, Heincke D, et al. Specific phosphorylation of the PfRh2b invasion ligand of Plasmodium falciparum. Biochem J. 2013;452: 457–466. doi: 10.1042/BJ20121694 23544851
15. Pal-Bhowmick I, Andersen J, Srinivasan P, Narum DL, Bosch J, Miller LH, Binding of aldolase and glyceraldehyde-3-phosphate dehydrogenase to the cytoplasmic tails of Plasmodium falciparum merozoite duffy binding-like and reticulocyte homology ligands. mBio. 2012;3.
16. Shen B, Sibley LD, Toxoplasma aldolase is required for metabolism but dispensable for host-cell invasion. Proc Natl Acad Sci U S A. 2014;111: 3567–3572. doi: 10.1073/pnas.1315156111 24550496
17. Blom N, Sicheritz-Pontén T, Gupta R, Gammeltoft S, Brunak S, Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics. 2004;4: 1633–1649. 15174133
18. Pagano MA, Andrzejewska M, Ruzzene M, Sarno S, Cesaro L, Bain J, et al. Optimization of protein kinase CK2 inhibitors derived from 4,5,6,7-tetrabromobenzimidazole. J Med Chem. 2004;47: 6239–6247. 15566294
19. Dvorin JD, Martyn DC, Patel SD, Grimley JS, Collins CR, Hopp CS, et al. A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes. Science. 2010;328: 910–912. doi: 10.1126/science.1188191 20466936
20. Gaur D, Singh S, Singh S, Jiang L, Diouf A, Miller LH, Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion. Proc Natl Acad Sci U S A. 2007;104: 17789–17794. 17971435
21. Reed MB, Caruana SR, Batchelor AH, Thompson JK, Crabb BS, Cowman AF, Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proc Natl Acad Sci U S A. 2000;97: 7509–7514. 10861015
22. Duraisingh MT, Triglia T, Ralph SA, Rayner JC, Barnwell JW, McFadden GI, et al. Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J. 2003;22: 1047–1057. 12606570
23. Stubbs J, Simpson KM, Triglia T, Plouffe D, Tonkin CJ, Duraisingh MT, et al. Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science. 2005;309: 1384–1387. 16123303
24. Jiang L, Gaur D, Mu J, Zhou H, Long CA, Miller LH, Evidence for erythrocyte-binding antigen 175 as a component of a ligand-blocking blood-stage malaria vaccine. Proc Natl Acad Sci U S A. 2011;108: 7553–7558. doi: 10.1073/pnas.1104050108 21502513
25. Tham W-H, Schmidt CQ, Hauhart RE, Guariento M, Tetteh-Quarcoo PB, Lopaticki S, et al. Plasmodium falciparum uses a key functional site in complement receptor type-1 for invasion of human erythrocytes. Blood. 2011;118: 1923–1933. doi: 10.1182/blood-2011-03-341305 21685372
26. Tham W-H, Wilson DW, Reiling L, Chen L, Beeson JG, Cowman AF, Antibodies to reticulocyte binding protein-like homologue 4 inhibit invasion of Plasmodium falciparum into human erythrocytes. Infect Immun. 2009;77: 2427–2435. doi: 10.1128/IAI.00048-09 19307208
27. Tham W-H, Wilson DW, Lopaticki S, Schmidt CQ, Tetteh-Quarcoo PB, Barlow PN, et al. Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand. Proc Natl Acad Sci U S A. 2010;107: 17327–17332. doi: 10.1073/pnas.1008151107 20855594
28. Weiss GE, Gilson PR, Taechalertpaisarn T, Tham W-H, de Jong NWM, Harvey KL, et al. Revealing the Sequence and Resulting Cellular Morphology of Receptor-Ligand Interactions during Plasmodium falciparum Invasion of Erythrocytes. PLoS Pathog. 2015;11: e1004670. doi: 10.1371/journal.ppat.1004670 25723550
29. Lopaticki S, Maier AG, Thompson J, Wilson DW, Tham W-H, Triglia T, et al. Reticulocyte and erythrocyte binding-like proteins function cooperatively in invasion of human erythrocytes by malaria parasites. Infect Immun. 2011;79: 1107–1117. doi: 10.1128/IAI.01021-10 21149582
30. 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. 15479470
31. Lasonder E, Treeck M, Alam M, Tobin AB, Insights into the Plasmodium falciparum schizont phospho-proteome. Microbes Infect Inst Pasteur. 2012;14: 811–819.
32. Vilk G, Weber JE, Turowec JP, Duncan JS, Wu C, Derksen DR, et al. Protein kinase CK2 catalyzes tyrosine phosphorylation in mammalian cells. Cell Signal. 2008;20: 1942–1951. doi: 10.1016/j.cellsig.2008.07.002 18662771
33. Wilson LK, Dhillon N, Thorner J, Martin GS, Casein kinase II catalyzes tyrosine phosphorylation of the yeast nucleolar immunophilin Fpr3. J Biol Chem. 1997;272: 12961–12967. 9148902
34. Marin O, Meggio F, Sarno S, Cesaro L, Pagano MA, Pinna LA, Tyrosine versus serine/threonine phosphorylation by protein kinase casein kinase-2. A study with peptide substrates derived from immunophilin Fpr3. J Biol Chem. 1999;274: 29260–29265. 10506183
35. Moore KL, Protein tyrosine sulfation: a critical posttranslation modification in plants and animals. Proc Natl Acad Sci U S A. 2009;106: 14741–14742. doi: 10.1073/pnas.0908376106 19717448
36. Triglia T, Tham W-H, Hodder A, Cowman AF, Reticulocyte binding protein homologues are key adhesins during erythrocyte invasion by Plasmodium falciparum. Cell Microbiol. 2009;11: 1671–1687. doi: 10.1111/j.1462-5822.2009.01358.x 19614665
37. Holland Z, Prudent R, Reiser J-B, Cochet C, Doerig C, Functional analysis of protein kinase CK2 of the human malaria parasite Plasmodium falciparum. Eukaryot Cell. 2009;8: 388–397. doi: 10.1128/EC.00334-08 19114502
38. Boyle MJ, Wilson DW, Richards JS, Riglar DT, Tetteh KKA, Conway DJ, et al. Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc Natl Acad Sci U S A. 2010;107: 14378–14383. doi: 10.1073/pnas.1009198107 20660744