Functional analysis of the exported type IV HSP40 protein PFGECO in plasmodium falciparum gametocytes

Eukaryotic Cell

Volumn 10, Issue 11, 2011, Pages 1492-1503

  Morahan, Belinda J ^a   Strobe, Carolyn ^b   Hasan, Uzma ^b   Czesny, Beata ^b   Mantel, Pierre Yves ^c   Marti, Matthias ^c   Eksi, Saliha ^b,d   Williamson, Kim C ^a,b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d RECEP TAYYIP ERDOGAN UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 40; PROTOZOAL PROTEIN;

ARTICLE; BIOSYNTHESIS; DNA MICROARRAY; ERYTHROCYTE; GENE; GENETICS; HEAT SHOCK RESPONSE; HUMAN; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ERYTHROCYTES; GENES, PROTOZOAN; HEAT-SHOCK RESPONSE; HSP40 HEAT-SHOCK PROTEINS; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

PLASMODIUM FALCIPARUM;

EID: 80055108114     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05155-11     Document Type: Article

References (94)

1. Aikawa, M., Y. Uni, A. T. Andrutis, and R. J. Howard. 1986. Membraneassociated electron-dense material of the asexual stages of Plasmodium falciparum: evidence for movement from the intracellular parasite to the erythrocyte membrane. Am. J. Trop. Med. Hyg. 35:30-36.
2. Anders, R. F., R. L. Coppel, G. V. Brown, and D. J. Kemp. 1988. Antigens with repeated amino acid sequences from the asexual blood stages of Plasmodium falciparum. Prog. Allergy 41:148-172.
3. Atkinson, C. T., and M. Aikawa. 1990. Ultrastructure of malaria-infected erythrocytes. Blood Cells 16:351-368.
4. Atkinson, C. T., et al. 1987. Ultrastructure of the erythrocytic stages of Plasmodium malariae. J. Protozool. 34:267-274.
5. Baldi, D. L., R. Good, M. T. Duraisingh, B. S. Crabb, and A. F. Cowman. 2002. Identification and disruption of the gene encoding the third member of the low-molecular-mass rhoptry complex in Plasmodium falciparum. Infect. Immun. 70:5236-5245.
6. Banumathy, G., V. Singh, and U. Tatu. 2002. Host chaperones are recruited in membrane-bound complexes by Plasmodium falciparum. J. Biol. Chem. 277:3902-3912.
7. Baruch, D. I., J. A. Gormely, C. Ma, R. J. Howard, and B. L. Pasloske. 1996. Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Proc. Natl. Acad. Sci. U. S. A. 93:3497-3502.
8. Bennett, B. J., N. Mohandas, and R. L. Coppel. 1997. Defining the minimal domain of the Plasmodium falciparum protein MESA involved in the interaction with the red cell membrane skeletal protein 4.1. J. Biol. Chem. 272:15299-15306.
9. Bhattacharjee, S., C. van Ooij, B. Balu, J. H. Adams, and K. Haldar. 2008. Maurer's clefts of Plasmodium falciparum are secretory organelles that concentrate virulence protein reporters for delivery to the host erythrocyte. Blood 111:2418-2426.
10. Bianco, A. E., et al. 1988. Patterns of antigen expression in asexual blood stages and gametocytes of Plasmodium falciparum. Am. J. Trop. Med. Hyg.38:258-267.
11. Black, C. G., et al. 2008. In vivo studies support the role of trafficking and cytoskeletal-binding motifs in the interaction of MESA with the membrane skeleton of Plasmodium falciparum-infected red blood cells. Mol. Biochem. Parasitol. 160:143-147.
12. Blisnick, T., et al. 2000. Pfsbp1, a Maurer's cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Mol. Biochem. Parasitol. 111:107-121.
13. Boddey, J. A., et al. 2010. An aspartyl protease directs malaria effector proteins to the host cell. Nature 463:627-631.
14. Boddey, J. A., R. L. Moritz, R. J. Simpson, and A. F. Cowman. 2009. Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10:285-299.
15. Bonilla, J. A., et al. 2007. Effects on growth, hemoglobin metabolism and paralogous gene expression resulting from disruption of genes encoding the digestive vacuole plasmepsins of Plasmodium falciparum. Int. J. Parasitol. 37:317-327.
16. Botha, M., E. R. Pesce, and G. L. Blatch. 2007. The Hsp40 proteins of Plasmodium falciparum and other apicomplexa: regulating chaperone power in the parasite and the host. Int. J. Biochem. Cell Biol. 39:1781-1803.
17. Bozdech, Z., et al. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1:E5.
18. Chang, H. H., et al. 2008. N-terminal processing of proteins exported by malaria parasites. Mol. Biochem. Parasitol. 160:107-115.
19. Cheetham, M. E., and A. J. Caplan. 1998. Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3:28-36.
20. Cheetham, M. E., A. P. Jackson, and B. H. Anderton. 1994. Regulation of 70-kDa heat-shock-protein ATPase activity and substrate binding by human DnaJ-like proteins, HSJ1a and HSJ1b. Eur. J. Biochem. 226:99-107.
21. Cooke, B. M., F. K. Glenister, N. Mohandas, and R. L. Coppel. 2002. Assignment of functional roles to parasite proteins in malaria-infected red blood cells by competitive flow-based adhesion assay. Br. J. Haematol. 117: 203-211.
22. Cooke, B. M., K. Lingelbach, L. H. Bannister, and L. Tilley. 2004. Protein trafficking in Plasmodium falciparum-infected red blood cells. Trends Parasitol. 20:581-589.
23. Coppel, R. L., S. Lustigman, L. Murray, and R. F. Anders. 1988. MESA is a Plasmodium falciparum phosphoprotein associated with the erythrocyte membrane skeleton. Mol. Biochem. Parasitol. 31:223-231.
24. Cowman, A. F., et al. 1984. The ring-infected erythrocyte surface antigen (RESA) polypeptide of Plasmodium falciparum contains two separate blocks of tandem repeats encoding antigenic epitopes that are naturally immunogenic in man. Mol. Biol. Med. 2:207-221.
25. Crabb, B. S., et al. 1997. Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89:287-296.
26. Crandall, I., and I. W. Sherman. 1994. Cytoadherence and the Plasmodium falciparum-infected erythrocyte. Methods Cell Biol. 45:193-210.
27. Culvenor, J. G., K. P. Day, and R. F. Anders. 1991. Plasmodium falciparum ring-infected erythrocyte surface antigen is released from merozoite dense granules after erythrocyte invasion. Infect. Immun. 59:1183-1187.
28. Da Silva, E., et al. 1994. The Plasmodium falciparum protein RESA interacts with the erythrocyte cytoskeleton and modifies erythrocyte thermal stability. Mol. Biochem. Parasitol. 66:59-69.
29. Day, K. P., R. E. Hayward, D. Smith, and J. G. Culvenor. 1998. CD36-dependent adhesion and knob expression of the transmission stages of Plasmodium falciparum is stage specific. Mol. Biochem. Parasitol. 93:167-177.
30. de Koning-Ward, T. F., et al. 2009. A newly discovered protein export machine in malaria parasites. Nature 459:945-949.
31. Eksi, S., et al. 2005. Identification of a subtelomeric gene family expressed during the asexual-sexual stage transition in Plasmodium falciparum. Mol. Biochem. Parasitol. 143:90-99.
32. Eksi, S., et al. 2002. Targeting and sequestration of truncated Pfs230 in an intraerythrocytic compartment during Plasmodium falciparum gametocytogenesis. Mol. Microbiol. 44:1507-1516.
33. Fidock, D. A., and T. E. Wellems. 1997. Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Proc. Natl. Acad. Sci. U. S. A. 94:10931-10936.
34. Fink, A. L. 1999. Chaperone-mediated protein folding. Physiol. Rev. 79:425-449.
35. Foley, M., L. Corcoran, L. Tilley, and R. Anders. 1994. Plasmodium falciparum: mapping the membrane-binding domain in the ring-infected erythrocyte surface antigen. Exp. Parasitol. 79:340-350.
36. Foley, M., L. Tilley, W. H. Sawyer, and R. F. Anders. 1991. The ring-infected erythrocyte surface antigen of Plasmodium falciparum associates with spectrin in the erythrocyte membrane. Mol. Biochem. Parasitol. 46:137-147.
37. Genevaux, P., A. Wawrzynow, M. Zylicz, C. Georgopoulos, and W. L. Kelley. 2001. DjlA is a third DnaK co-chaperone of Escherichia coli, and DjlAmediated induction of colanic acid capsule requires DjlA-DnaK interaction. J. Biol. Chem. 276:7906-7912.
38. Goldberg, D. E., and A. F. Cowman. 2010. Moving in and renovating: exporting proteins from Plasmodium into host erythrocytes. Nat. Rev. Microbiol. 8:617-621.
39. Haldar, K., and N. Mohandas. 2007. Erythrocyte remodeling by malaria parasites. Curr. Opin. Hematol. 14:203-209.
40. Hanssen, E., et al. 2008. Electron tomography of the Maurer's cleft organelles of Plasmodium falciparum-infected erythrocytes reveals novel structural features. Mol. Microbiol. 67:703-718.
41. Hawking, F., M. E. Wilson, and K. Gammage. 1971. Evidence for cyclic development and short-lived maturity in the gametocytes of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 65:549-559.
42. Hayward, R. E., B. Tiwari, K. P. Piper, D. I. Baruch, and K. P. Day. 1999. Virulence and transmission success of the malarial parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. U. S. A. 96:4563-4568.
43. Hennessy, F., M. E. Cheetham, H. W. Dirr, and G. L. Blatch. 2000. Analysis of the levels of conservation of the J domain among the various types of DnaJ-like proteins. Cell Stress Chaperones 5:347-358.
44. Hiller, N. L., et al. 2004. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306:1934-1937.
45. Horrocks, P., et al. 2005. PfEMP1 expression is reduced on the surface of knobless Plasmodium falciparum infected erythrocytes. J. Cell Sci. 118:2507-2518.
46. Hui, G. S., and W. A. Siddiqui. 1988. Characterization of a Plasmodium falciparum polypeptide associated with membrane vesicles in the infected erythrocytes. Mol. Biochem. Parasitol. 29:283-293.
47. Ifediba, T., and J. P. Vanderberg. 1981. Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature 294:364-366.
48. Klemba, M., and D. E. Goldberg. 2005. Characterization of plasmepsin V, a membrane-bound aspartic protease homolog in the endoplasmic reticulum of Plasmodium falciparum. Mol. Biochem. Parasitol. 143:183-191.
49. Knight, A., and R. E. Sinden. 1982. The purification of gametocytes of Plasmodium falciparum and P. yoelii nigeriensis by colloidal silica (Percoll) gradient centrifugation. Trans. R. Soc. Trop. Med. Hyg. 76:503-509.
50. Kongkasuriyachai, D., H. Fujioka, and N. Kumar. 2004. Functional analysis of Plasmodium falciparum parasitophorous vacuole membrane protein (Pfs16) during gametocytogenesis and gametogenesis by targeted gene disruption. Mol. Biochem. Parasitol. 133:275-285.
51. Kriek, N., et al. 2003. Characterization of the pathway for transport of the cytoadherence-mediating protein, PfEMP1, to the host cell surface in malaria parasite-infected erythrocytes. Mol. Microbiol. 50:1215-1227.
52. Lambros, C., and J. P. Vanderberg. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65:418-420.
53. Laufen, T., et al. 1999. Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc. Natl. Acad. Sci. U. S. A. 96:5452-5457.
54. Liberek, K., J. Marszalek, D. Ang, C. Georgopoulos, and M. Zylicz. 1991. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. U. S. A. 88:2874-2878.
55. Lingelbach, K., and J. M. Przyborski. 2006. The long and winding road: protein trafficking mechanisms in the Plasmodium falciparum infected erythrocyte. Mol. Biochem. Parasitol. 147:1-8.
56. Magowan, C., W. Wollish, L. Anderson, and J. Leech. 1988. Cytoadherence by Plasmodium falciparum-infected erythrocytes is correlated with the expression of a family of variable proteins on infected erythrocytes. J. Exp. Med. 168:1307-1320.
57. Maier, A. G., J. A. Braks, A. P. Waters, and A. F. Cowman. 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.
58. Maier, A. G., B. M. Cooke, A. F. Cowman, and L. Tilley. 2009. Malaria parasite proteins that remodel the host erythrocyte. Nat. Rev. Microbiol. 7:341-354.
59. Maier, A. G., et al. 2008. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134: 48-61.
60. Marti, M., J. Baum, M. Rug, L. Tilley, and A. F. Cowman. 2005. Signalmediated export of proteins from the malaria parasite to the host erythrocyte. J. Cell Biol. 171:587-592.
61. Marti, M., R. T. Good, M. Rug, E. Knuepfer, and A. F. Cowman. 2004. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306:1930-1933.
62. Mayer, M. P., T. Laufen, K. Paal, J. S. McCarty, and B. Bukau. 1999. Investigation of the interaction between DnaK and DnaJ by surface plasmon resonance spectroscopy. J. Mol. Biol. 289:1131-1144.
63. McRobert, L., et al. 2004. Distinct trafficking and localization of STEVOR proteins in three stages of the Plasmodium falciparum life cycle. Infect. Immun. 72:6597-6602.
64. Omara-Opyene, A. L., et al. 2004. Genetic disruption of the Plasmodium falciparum digestive vacuole plasmepsins demonstrates their functional redundancy. J. Biol. Chem. 279:54088-54096.
65. Osborne, A. R., et al. 2010. The host targeting motif in exported Plasmodium proteins is cleaved in the parasite endoplasmic reticulum. Mol. Biochem. Parasitol. 171:25-31.
66. Ponnudurai, T., A. H. Lensen, J. F. Meis, and J. H. Meuwissen. 1986. Synchronization of Plasmodium falciparum gametocytes using an automated suspension culture system. Parasitology 93(Pt 2):263-274.
67. Proellocks, N. I., et al. 2009. Characterisation of PfRON6, a Plasmodium falciparum rhoptry neck protein with a novel cysteine-rich domain. Int. J. Parasitol. 39:683-692.
68. Przyborski, J. M., and M. Lanzer. 2005. Protein transport and trafficking in Plasmodium falciparum-infected erythrocytes. Parasitology 130:373-388.
69. Ribaut, C., et al. 2008. Concentration and purification by magnetic separation of the erythrocytic stages of all human Plasmodium species. Malar. J. 7:45.
70. Riezman, H. 2004. Why do cells require heat shock proteins to survive heat stress? Cell Cycle 3:61-63.
71. Rogers, N. J., O. Daramola, G. A. Targett, and B. S. Hall. 1996. CD36 and intercellular adhesion molecule 1 mediate adhesion of developing Plasmodium falciparum gametocytes. Infect. Immun. 64:1480-1483.
72. Rogers, N. J., B. S. Hall, J. Obiero, G. A. Targett, and C. J. Sutherland. 2000. A model for sequestration of the transmission stages of Plasmodium falciparum: adhesion of gametocyte-infected erythrocytes to human bone marrow cells. Infect. Immun. 68:3455-3462.
73. Rogerson, S. J., S. C. Chaiyaroj, K. Ng, J. C. Reeder, and G. V. Brown. 1995. Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparuminfected erythrocytes. J. Exp. Med. 182:15-20.
74. Ruangjirachuporn, W., et al. 1991. Plasmodium falciparum: analysis of the interaction of antigen Pf155/RESA with the erythrocyte membrane. Exp. Parasitol. 73:62-72.
75. Russo, I., et al. 2010. Plasmepsin V licenses Plasmodium proteins for exort into the host erythrocyte. Nature 463:632-636.
76. Sargeant, T. J., et al. 2006. Lineage-specific expansion of proteins exported to rythrocytes in malaria parasites. Genome Biol. 7:R12.
77. Sharp, S., et al. 2006. Programmed transcription of the var gene family, but not of stevor, in Plasmodium falciparum gametocytes. Eukaryot. Cell 5:1206-1214.
78. Silva, M. D., et al. 2005. A role for the Plasmodium falciparum RESA protein in resistance against heat shock demonstrated using gene disruption. Mol. Microbiol. 56:990-1003.
79. Silvestrini, F., et al. 2010. Protein export marks the early phase of ametocytogenesis of the human malaria parasite Plasmodium falciparum. Mol. Cell Proteomics 9:1437-1448.
80. Smalley, M. E., S. Abdalla, and J. Brown. 1981. The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans. R. Soc. Trop. Med. Hyg. 75:103-105.
81. Spielmann, T., et al. 2006. A cluster of ring stage-specific genes linked to a locus implicated in cytoadherence in Plasmodium falciparum codes for PEXEL-negative and PEXEL-positive proteins exported into the host cell. Mol. Biol. Cell 17:3613-3624.
82. Taylor, D. W., et al. 1987. Localization of Plasmodium falciparum histidinerich protein 1 in the erythrocyte skeleton under knobs. Mol. Biochem. Parasitol. 25:165-174.
83. Taylor, H. M., M. Grainger, and A. A. Holder. 2002. Variation in the expression of a Plasmodium falciparum protein family implicated in erythrocyte invasion. Infect. Immun. 70:5779-5789.
84. Thomson, J. G., and A. Robertson. 1935. The structure and development of plasmodium falciparum gametocytes in the internal organs and peripheral circulation. Trans. R. Soc. Trop. Med. Hyg. 29:31-34.
85. Tilley, L., R. Sougrat, T. Lithgow, and E. Hanssen. 2008. The twists and turns of Maurer's cleft trafficking in P. falciparum-infected erythrocytes. Traffic 9:187-197.
86. Trager, W., and J. B. Jensen. 1997. Continuous culture of Plasmodium falciparum: its impact on malaria research. Int. J. Parasitol. 27:989-1006.
87. Tsai, J., and M. G. Douglas. 1996. A conserved HPD sequence of the J-domain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding. J. Biol. Chem. 271:9347-9354.
88. Udomsangpetch, R., M. Aikawa, K. Berzins, M. Wahlgren, and P. Perlmann. 1989. Cytoadherence of knobless Plasmodium falciparum-infected erythrocytes and its inhibition by a human monoclonal antibody. Nature 338:763-765.
89. Waller, K. L., et al. 2003. Mature parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum binds to the 30-kDa domain of protein 4.1 in malaria-infected red blood cells. Blood 102:1911-1914.
90. Walsh, P., D. Bursac, Y. C. Law, D. Cyr, and T. Lithgow. 2004. The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep. 5:567-571.
91. Wickert, H., W. Gottler, G. Krohne, and M. Lanzer. 2004. Maurer's cleft organization in the cytoplasm of plasmodium falciparum-infected erythrocytes: new insights from three-dimensional reconstruction of serial ultrathin sections. Eur. J. Cell Biol. 83:567-582.
92. Wickham, M. E., et al. 2001. Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J. 20:5636-5649.
93. Wittung-Stafshede, P., J. Guidry, B. E. Horne, and S. J. Landry. 2003. The J-domain of Hsp40 couples ATP hydrolysis to substrate capture in Hsp70. Biochemistry 42:4937-4944.
94. Young, J. A., et al. 2005. The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol. Biochem. Parasitol. 143:67-79.