A lysine-rich membrane-associated PHISTb protein involved in alteration of the cytoadhesive properties of Plasmodium falciparum-infected red blood cells

FASEB Journal

Volumn 28, Issue 7, 2014, Pages 3103-3113

  Proellocks, Nicholas I ^a   Herrmann, Susann ^a,b   Buckingham, Donna W ^a   Hanssen, Eric ^b   Hodges, Emma K ^a   Elsworth, Brendan ^a   Morahan, Belinda J ^a   Coppel, Ross L ^a   Cooke, Brian M ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cytoskeleton; Exported proteins; Malaria; Pathogenesis

Indexed keywords

CD36 ANTIGEN; ERYTHROCYTE MEMBRANE PROTEIN 1; LYSINE; PLASMODIUM HELICAL INTERSPERSED SUBTELOMERIC PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; ERYTHROCYTE; FLUORESCENCE MICROSCOPY; IMMUNOBLOTTING; IMMUNOELECTRON MICROSCOPY; INFECTED RED BLOOD CELL; MALARIA FALCIPARUM; NONHUMAN; PATHOPHYSIOLOGY; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SOUTHERN BLOTTING; TRANSMISSION ELECTRON MICROSCOPY; YOUNG MODULUS;

CYTOSKELETON; EXPORTED PROTEINS; MALARIA; PATHOGENESIS;

CELL ADHESION; CELL MEMBRANE; CYTOSKELETON; ENDOTHELIUM, VASCULAR; ERYTHROCYTES; HUMANS; LYSINE; MALARIA, FALCIPARUM; MEMBRANE PROTEINS; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAN PROTEINS;

EID: 84903716225     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-250399     Document Type: Article

References (52)

1. Sachs, J. (2002) A new global effort to control malaria. Science 298, 122-124
2. Snow, R., Guerra, C., Noor, A., Myint, H., and Hay, S. (2005) The global distribution of clinical episodes of Plasmodium falci-parum malaria. Nature 434, 214-217 (Pubitemid 40388051)
3. Waterkeyn, J. G., Wickham, M. E., Davern, K. M., Cooke, B. M., Coppel, R. L., Reeder, J. C., Culvenor, J. G., Waller, R. F., and Cowman, A. F. (2000) Targeted mutagenesis of Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) disrupts cytoadherence of malaria-infected red blood cells. EMBO J. 19, 2813-2823 (Pubitemid 30386754)
4. Haldar, K., Murphy, S. C., Milner, D. A., and Taylor, T. E. (2007) Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease. Annu. Rev. Pathol. 2, 217-249 (Pubitemid 46448065)
5. Cooke, B., Mohandas, N., and Coppel, R. (2004) Malaria and the red blood cell membrane. Semin. Hematol. 41, 173-188 (Pubitemid 38509641)
6. Cooke, B., Mohandas, N., and Coppel, R. (2001) The malaria-infected red blood cell: structural and functional changes. Adv. Parasitol. 50, 1-86 (Pubitemid 33086301)
7. Cooke, B. M., Mohandas, N., Cowman, A. F., and Coppel, R. L. (2005) Cellular adhesive phenomena in apicomplexan parasites of red blood cells. Vet. Parasitol. 132, 273-295 (Pubitemid 41224891)
8. Maier, A., Cooke, B., Cowman, A., and Tilley, L. (2009) Malaria parasite proteins that remodel the host erythrocyte. Nat. Rev. Microbiol. 7, 341-354
9. Hiller, N., Bhattacharjee, S., van Ooij, C., Liolios, K., Harrison, T., Lopez-Estrano, C., and Haldar, K. (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306, 1934-1937 (Pubitemid 39627857)
10. Marti, M., Good, R., Rug, M., Knuepfer, E., and Cowman, A. (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306, 1930-1933 (Pubitemid 39627856)
11. Grüring, C., Heiber, A., Kruse, F., Flemming, S., Franci, G., Colombo, S. F., Fasana, E., Schoeler, H., Borgese, N., Stunnen-berg, H. G., Przyborski, J. M., Gilberger, T.-W., and Spielmann, T. (2012) Uncovering common principles in protein export of malaria parasites. Cell Host Microbe 12, 717-729
12. Wickham, M., Rug, M., Ralph, S., Klonis, N., McFadden, G., Tilley, L., and Cowman, A. (2001) Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J. 20, 5636-5649 (Pubitemid 33010041)
13. Cooke, B. M., Buckingham, D. W., Glenister, F. K., Fernandez, K. M., Bannister, L. H., Marti, M., Mohandas, N., and Coppel, R. L. (2006) A Maurer's cleft-associated protein is essential for expression of the major malaria virulence antigen on the surface of infected red blood cells. J. Cell Biol. 172, 899-908
14. Grüing, C., Heiber, A., Kruse, F., Ungefehr, J., Gilberger, T., and Spielmann, T. (2011) Development and host cell modifications of Plasmodium falciparum blood stages in four dimensions. Nat. Commun. 2, 165
15. McMillan, P. J., Millet, C., Batinovic, S., Maiorca, M., Hanssen, E., Kenny, S., Muhle, R. A., Melcher, M., Fidock, D. A., Smith, J. D., Dixon, M. W. A., and Tilley, L. (2013) Spatial and temporal mapping of the PfEMP1 export pathway in Plasmodium falci-parum. Cell. Microbiol. 15, 1401-1418
16. Przyborski, J., Wickert, H., Krohne, G., and Lanzer, M. (2003) Maurer's clefts-a novel secretory organelle? Mol. Biochem. Parasitol. 132, 17-26 (Pubitemid 37239003)
17. Mundwiler-Pachlatko, E., and Beck, H.-P. (2013) Maurer's clefts, the enigma of Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 110, 1-8
18. Cooke, B., Lingelbach, K., Bannister, L., and Tilley, L. (2004) Protein trafficking in Plasmodium falciparum-infected red blood cells. Trends Parasitol. 20, 581-589 (Pubitemid 39446749)
19. Crabb, B. S., Cooke, B. M., Reeder, J. C., Waller, R. F., Caruana, S. R., Davern, K. M., Wickham, M. E., Brown, G. V., Coppel, R. L., and Cowman, A. F. (1997) Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89, 287-296 (Pubitemid 27199900)
20. Rug, M., Prescott, S. W., Fernandez, K. M., Cooke, B. M., and Cowman, A. F. (2006) The role of KAHRP domains in knob formation and cytoadherence of P. falciparum-infected human erythrocytes. Blood 108, 370-378 (Pubitemid 43990651)
21. Glenister, F. K., Coppel, R. L., Cowman, A. F., Mohandas, N., and Cooke, B. M. (2002) Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. Blood 99, 1060-1063 (Pubitemid 34525571)
22. Glenister, F. K., Fernandez, K. M., Kats, L. M., Hanssen, E., Mohandas, N., Coppel, R. L., and Cooke, B. M. (2009) Functional alteration of red blood cells by a megadalton protein of Plasmodium falciparum. Blood 113, 919-928
23. Nunes, M. C., Okada, M., Scheidig-Benatar, C., Cooke, B. M., and Scherf, A. (2010) Plasmodium falciparum FIKK kinase members target distinct components of the erythrocyte membrane. PLoS One 5, e11747
24. Kats, L.M., Fernandez, K.M., Glenister, F.K., Herrmann, S., Buckingham, D.W., Siddiqui, G., Sharma, L., Bamert, R., Lucet, I., Guillotte, M., Mercereau-Puijalon, O., and Cooke, B.M. (2014) An exported kinase (FIKK4.2) that mediates virulence-associated changes in Plasmodium falciparum-infected red blood cells. Int. J. Parasitol. doi: http://dx.doi.org/10.1016/j.ijpara.2014.01. 003
25. Sargeant, T., Marti, M., Caler, E., Carlton, J. M., Simpson, K. M., Speed, T., and Cowman, A. F. (2006) Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol. 7, R12
26. Ward, P., Equinet, L., Packer, J., and Doerig, C. (2004) Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5, 79
27. Akinyi, S., Hanssen, E., Meyer, E. V. S., Jiang, J., Korir, C. C., Singh, B., Lapp, S., Barnwell, J. W., Tilley, L., and Galinski, M. R. (2012) A 95 kDa protein of Plasmodium vivax and P. cynomolgi visualized by three-dimensional tomography in the caveola-vesicle complexes (Schüffner's dots) of infected erythrocytes is a member of the PHIST family. Mol. Microbiol. 84, 816-831
28. Maier, A. G., Rug, M., O'Neill, M. T., Brown, M., Chakravorty, S., Szestak, T., Chesson, J., Wu, Y., Hughes, K., Coppel, R. L., Newbold, C., Beeson, J. G., Craig, A., Crabb, B. S., and Cowman, A. F. (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134, 48-61 (Pubitemid 351905737)
29. Kilili, G. K., and LaCount, D. J. (2011) An erythrocyte cytoskel-eton-binding motif in exported Plasmodium falciparum proteins. Eukaryot. Cell 10, 1439-1447
30. Mayer, C., Slater, L., Erat, M. C., Konrat, R., and Vakonakis, I. (2012) Structural analysis of the Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) intracellular domain reveals a conserved interaction epitope. J. Biol. Chem. 287, 7182-7189
31. Parish, L. A., Mai, D. W., Jones, M. L., Kitson, E. L., and Rayner, J. C. (2013) A member of the Plasmodium falciparum PHIST family binds to the erythrocyte cytoskeleton component band 4.1. Malar. J. 12, 160
32. Cranmer, S. L., Magowan, C., Liang, J., Coppel, R. L., and Cooke, B. M. (1997) An alternative to serum for cultivation of Plasmodium falciparum in vitro. Trans. R. Soc. Trop. Med. Hyg. 91, 363-365 (Pubitemid 27261186)
33. Lambros, C., and Vanderberg, J. P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65, 418-420 (Pubitemid 10222999)
34. Dluzewski, A., Ling, I., Rangachari, K., Bates, P., and Wilson, R. (1984) A simple method for isolating viable mature parasites of Plasmodium falciparum from cultures. Trans. R. Soc. Trop. Med. Hyg. 78, 622-624 (Pubitemid 15062048)
35. Maier, A., Braks, J., Waters, A., and Cowman, A. (2006) Negative selection using yeast cytosine deaminase/uracil phosphoribosyl transferase in Plasmodium falciparum for targeted gene deletion by double crossover recombination. Mol. Biochem. Parasitol. 150, 118-121 (Pubitemid 44332581)
36. Boddey, J., Moritz, R., Simpson, R., and Cowman, A. (2009) Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10, 285-299
37. Ganesan, S. M., Morrisey, J. M., Ke, H., Painter, H. J., Laroiya, K., Phillips, M. A., Rathod, P. K., Mather, M. W., and Vaidya, A. B. (2011) Yeast dihydroorotate dehydrogenase as a new selectable marker for Plasmodium falciparum transfection. Mol. Biochem. Parasitol. 177, 29-34
38. Wu, Y., Sifri, C. D., Lei, H. H., Su, X. Z., and Wellems, T. E. (1995) Transfection of Plasmodium falciparum within human red blood cells. Proc. Natl. Acad. Sci. U.S.A. 92, 973-977
39. Slot, J. W., and Geuze, H. J. (2007) Cryosectioning and immu-nolabeling. Nat. Protoc. 2, 2480-2491
40. Waller, K. L., Stubberfield, L. M., Dubljevic, V., Nunomura, W., An, X., Mason, A. J., Mohandas, N., Cooke, B. M., and Coppel, R. L. (2007) Interactions of Plasmodium falciparum erythrocyte membrane protein 3 with the red blood cell membrane skeleton. Biochim. Biophys. Acta 1768, 2145-2156 (Pubitemid 47379605)
41. Cooke, B. M., Coppel, R. L., and Nash, G. B. (2002) Analysis of the adhesive properties of Plasmodium falciparum-infected red blood cells under conditions of flow. Methods Mol. Med. 72, 561-569
42. Cooke, B. M., Coppel, R. L., and Nash, G. B. (2002) Preparation of adhesive targets for flow-based cytoadhesion assays. Methods Mol. Med. 72, 571-579
43. Coppel, R. (1992) Repeat structures in a Plasmodium falciparum protein (MESA) that binds human erythrocyte protein 4.1. Mol. Biochem. Parasitol. 50, 335-347
44. Külzer, S., Rug, M., Brinkmann, K., Cannon, P., Cowman, A., Lingelbach, K., Blatch, G. L., Maier, A. G., and Przyborski, J. M. (2010) Parasite-encoded Hsp40 proteins define novel mobile structures in the cytosol of the P. falciparum-infected erythrocyte. Cell. Microbiol. 12, 1398-1420
45. Nilsson, S., Angeletti, D., Wahlgren, M., Chen, Q., and Moll, K. (2012) Plasmodium falciparum antigen 332 is a resident periph eral membrane protein of Maurer's clefts. PLoS One 7, e46980
46. Saridaki, T., Frohlich, K., Braun-Breton, C., and Lanzer, M. (2009) Export of PfSBP1 to the Plasmodium falciparum Maurer's clefts. Traffic 10, 137-152
47. Pallavi, R., Acharya, P., Chandran, S., Daily, J. P., and Tatu, U. (2010) Chaperone expression profiles correlate with distinct physiological states of Plasmodium falciparum in malaria patients. Malar. J. 9, 236
48. Oyelade, J., Ewejobi, I., Brors, B., Eils, R., and Adebiyi, E. (2011) Computational identification of signalling pathways in Plasmodium falciparum. Infect. Genet. Evol. 11, 755-764
49. Waller, K., Cooke, B., Nunomura, W., Mohandas, N., and Coppel, R. (1999) Mapping the binding domains involved in the interaction between the Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and the cytoadherence ligand P. falciparum erythrocyte membrane protein 1 (PfEMP1). J. Biol. Chem. 274, 23808-23813
50. Waller, K. L., Nunomura, W., Cooke, B. M., Mohandas, N., and Coppel, R. L. (2002) Mapping the domains of the cytoadher-ence ligand Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) that bind to the knob-associated histidine-rich protein (KAHRP). Mol. Biochem. Parasitol. 119, 125-129 (Pubitemid 34038033)
51. Pei, X., An, X., Guo, X., Tarnawski, M., Coppel, R., and Mohandas, N. (2005) Structural and functional studies of interaction between Plasmodium falciparum knob-associated his-tidine-rich protein (KAHRP) and erythrocyte spectrin. J. Biol. Chem. 280, 31166-31171 (Pubitemid 41291853)
52. Oh, S. S., Voigt, S., Fisher, D., Yi, S. J., LeRoy, P. J., Derick, L. H., Liu, S., and Chishti, A. H. (2000) Plasmodium falciparum eryth-rocyte membrane protein 1 is anchored to the actin-spectrin junction and knob-associated histidine-rich protein in the eryth-rocyte skeleton. Mol. Biochem. Parasitol. 108, 237-247 (Pubitemid 30317453)