Subcompartmentalisation of Proteins in the Rhoptries Correlates with Ordered Events of Erythrocyte Invasion by the Blood Stage Malaria Parasite

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Zuccala, Elizabeth S ^a,b   Gout, Alexander M ^a,b,e   Dekiwadia, Chaitali ^c   Marapana, Danushka S ^a   Angrisano, Fiona ^a,b   Turnbull, Lynne ^d   Riglar, David T ^a,b   Rogers, Kelly L ^a,b   Whitchurch, Cynthia B ^d   Ralph, Stuart A ^c   Speed, Terence P ^a,b   Baum, Jake ^a,b  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

APICAL SUSHI PROTEIN; CARRIER PROTEIN; INVASIN; PROTEIN PFF0645C; RHOPTRY NECK PROTEIN 2; UNCLASSIFIED DRUG;

ARTICLE; BLOOD PARASITE; CELL INVASION; COMPUTER MODEL; ERYTHROCYTE; HOST CELL; HOST PARASITE INTERACTION; MALARIA; MEROZOITE; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; SPECIES DIFFERENCE;

BLOTTING, WESTERN; ERYTHROCYTES; FLUORESCENT ANTIBODY TECHNIQUE; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA; MICROSCOPY, IMMUNOELECTRON; ORGANELLES; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS;

APICOMPLEXA; PLASMODIUM FALCIPARUM;

EID: 84866721049     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046160     Document Type: Article

References (79)

1. Putignani L, Menichella D, (2010) Global distribution, public health and clinical impact of the protozoan pathogen cryptosporidium. Interdiscip Perspect Infect Dis 2010.
2. Robert-Gangneux F, Darde ML, (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 25: 264-296.
3. Frenal K, Soldati-Favre D, (2009) Role of the parasite and host cytoskeleton in apicomplexa parasitism. Cell Host Microbe 5: 602-611.
4. Blackman MJ, Bannister LH, (2001) Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Mol Biochem Parasitol 117: 11-25.
5. Besteiro S, Dubremetz JF, Lebrun M, (2011) The moving junction of apicomplexan parasites: a key structure for invasion. Cell Microbiol 13: 797-805.
6. Schupp E, Michel R, Raether W, Niemeitz H, Uphoff M, (1978) [Invasion of erythrocytes by toxoplasma gondii (author's transl)]. Z Parasitenkd 55: 189-193.
7. Aikawa M, Miller LH, Johnson J, Rabbege J, (1978) Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J Cell Biol 77: 72-82.
8. Riglar DT, Richard D, Wilson DW, Boyle MJ, Dekiwadia C, et al. (2011) Super-Resolution Dissection of Coordinated Events during Malaria Parasite Invasion of the Human Erythrocyte. Cell Host Microbe 9: 9-20.
9. Torii M, Adams JH, Miller LH, Aikawa M, (1989) Release of merozoite dense granules during erythrocyte invasion by Plasmodium knowlesi. Infect Immun 57: 3230-3233.
10. Dobrowolski JM, Sibley LD, (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933-939.
11. Bannister LH, Butcher GA, Dennis ED, Mitchell GH, (1975) Structure and invasive behaviour of Plasmodium knowlesi merozoites in vitro. Parasitology 71: 483-491.
12. Boyle MJ, Wilson DW, Richards JS, Riglar DT, Tetteh KK, et al. (2010) Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc Natl Acad Sci USA 107: 14378-14383.
13. Charron AJ, Sibley LD, (2004) Molecular partitioning during host cell penetration by Toxoplasma gondii. Traffic 5: 855-867.
14. Suss-Toby E, Zimmerberg J, Ward GE, (1996) Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci U S A 93: 8413-8418.
15. Lingelbach K, Joiner KA, (1998) The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J Cell Sci 111: 1467-1475.
16. Elliott DA, Clark DP, (2000) Cryptosporidium parvum induces host cell actin accumulation at the host-parasite interface. Infect Immun 68: 2315-2322.
17. Elliott DA, Coleman DJ, Lane MA, May RC, Machesky LM, et al. (2001) Cryptosporidium parvum infection requires host cell actin polymerization. Infect Immun 69: 5940-5942.
18. Lumb R, Smith K, O'Donoghue PJ, Lanser JA, (1988) Ultrastructure of the attachment of Cryptosporidium sporozoites to tissue culture cells. Parasitol Res 74: 531-536.
19. Vetterling JM, Takeuchi A, Madden PA, (1971) Ultrastructure of Cryptosporidium wrairi from the guinea pig. J Protozool 18: 248-260.
20. Torii M, Nakamura K, Sieber KP, Miller LH, Aikawa M, (1992) Penetration of the mosquito (Aedes aegypti) midgut wall by the ookinetes of Plasmodium gallinaceum. J Protozool 39: 449-454.
21. Pizarro-Cerda J, Cossart P, (2006) Bacterial adhesion and entry into host cells. Cell 124: 715-727.
22. Baum J, Gilberger T-W, Frischknecht F, Meissner M, (2008) Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma. Trends Parasitol 24: 557-563.
23. Farrow RE, Green J, Katsimitsoulia Z, Taylor WR, Holder AA, et al. (2011) The mechanism of erythrocyte invasion by the malarial parasite, Plasmodium falciparum. Semin Cell Dev Biol 22: 953-960.
24. Alexander DL, Mital J, Ward GE, Bradley P, Boothroyd JC, (2005) Identification of the Moving Junction Complex of Toxoplasma gondii: A Collaboration between Distinct Secretory Organelles. PLoS Pathog 1: e17.
25. Besteiro S, Michelin A, Poncet J, Dubremetz JF, Lebrun M, (2009) Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLoS Pathog 5: e1000309.
26. Lebrun M, Michelin A, El Hajj H, Poncet J, Bradley PJ, et al. (2005) The rhoptry neck protein RON4 re-localizes at the moving junction during Toxoplasma gondii invasion. Cell Microbiol 7: 1823-1833.
27. Straub KW, Cheng SJ, Sohn CS, Bradley PJ, (2009) Novel components of the Apicomplexan moving junction reveal conserved and coccidia-restricted elements. Cell Microbiol 11: 590-603.
28. Giovannini D, Spath S, Lacroix C, Perazzi A, Bargieri D, et al. (2011) Independent roles of apical membrane antigen 1 and rhoptry neck proteins during host cell invasion by apicomplexa. Cell Host Microbe 10: 591-602.
29. Cao J, Kaneko O, Thongkukiatkul A, Tachibana M, Otsuki H, et al. (2009) Rhoptry neck protein RON2 forms a complex with microneme protein AMA1 in Plasmodium falciparum merozoites. Parasitol Int 58: 29-35.
30. Collins CR, Withers-Martinez C, Hackett F, Blackman MJ, (2009) An inhibitory antibody blocks interactions between components of the malarial invasion machinery. PLoS Pathog 5: e1000273.
31. Richard D, MacRaild CA, Riglar DT, Chan J-A, Foley M, et al. (2010) 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 285: 14815-14822.
32. Hossain ME, Dhawan S, Mohmmed A, (2011) The cysteine-rich regions of Plasmodium falciparum RON2 bind with host erythrocyte and AMA1 during merozoite invasion. Parasitol Res 110: 1711-1721.
33. Lamarque M, Besteiro S, Papoin J, Roques M, Vulliez-Le Normand B, et al. (2011) The RON2-AMA1 interaction is a critical step in moving junction-dependent invasion by apicomplexan parasites. PLoS Pathog 7: e1001276.
34. Tyler JS, Boothroyd JC, (2011) The C-terminus of Toxoplasma RON2 provides the crucial link between AMA1 and the host-associated invasion complex. PLoS Pathog 7: e1001282.
35. Tonkin ML, Roques M, Lamarque MH, Pugniere M, Douguet D, et al. (2011) Host cell invasion by apicomplexan parasites: insights from the co-structure of AMA1 with a RON2 peptide. Science 333: 463-467.
36. Narum DL, Nguyen V, Zhang Y, Glen J, Shimp RL, et al. (2008) Identification and characterization of the Plasmodium yoelii PyP140/RON4 protein, an orthologue of Toxoplasma gondii RON4, whose cysteine-rich domain does not protect against lethal parasite challenge infection. Infect Immun 76: 4876-4882.
37. Srinivasan P, Beatty WL, Diouf A, Herrera R, Ambroggio X, et al. (2011) Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc Natl Acad Sci U S A 108: 13275-13280.
38. Tufet-Bayona M, Janse CJ, Khan SM, Waters AP, Sinden RE, et al. (2009) Localisation and timing of expression of putative Plasmodium berghei rhoptry proteins in merozoites and sporozoites. Mol Biochem Parasitol 166: 22-31.
39. Kono M, Herrmann S, Loughran NB, Cabrera A, Engelberg K, et al. (2012) Evolution and Architecture of the Inner Membrane Complex in Asexual and Sexual Stages af the Malaria Parasite. Mol Biol Evol [Epub ahead of print].
40. Chen Z, Harb OS, Roos DS, (2008) In silico identification of specialized secretory-organelle proteins in apicomplexan parasites and in vivo validation in Toxoplasma gondii. PLoS One 3: e3611.
41. Hu G, Cabrera A, Kono M, Mok S, Chaal BK, et al. (2010) Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nature Biotechnology 28: 91-98.
42. Ito D, Han E-T, Takeo S, Thongkukiatkul A, Otsuki H, et al. (2011) Plasmodial ortholog of Toxoplasma gondii rhoptry neck protein 3 is localized to the rhoptry body. Parasitol Int 60: 132-138.
43. O'Keeffe AH, Green JL, Grainger M, Holder AA, (2005) A novel Sushi domain-containing protein of Plasmodium falciparum. Mol Biochem Parasitol 140: 61-68.
44. Srivastava A, Singh S, Dhawan S, Mahmood Alam M, Mohmmed A, et al. (2010) Localization of apical sushi protein in Plasmodium falciparum merozoites. Mol Biochem Parasitol 174: 66-69.
45. Bradley PJ, Ward C, Cheng SJ, Alexander DL, Coller S, et al. (2005) Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J Biol Chem 280: 34245-34258.
46. Desai SA, Krogstad DJ, McCleskey EW, (1993) A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362: 643-646.
47. Gilson PR, Nebl T, Vukcevic D, Moritz RL, Sargeant T, et al. (2006) Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics 5: 1286-1299.
48. Bannister LH, Hopkins JM, Fowler RE, Krishna S, Mitchell GH, (2000) A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitol Today 16: 427-433.
49. Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, et al. (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci U S A 95: 12352-12357.
50. Huynh MH, Carruthers VB, (2009) Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot Cell 8: 530-539.
51. Hu K, Mann T, Striepen B, Beckers CJ, Roos DS, et al. (2002) Daughter cell assembly in the protozoan parasite Toxoplasma gondii. Mol Biol Cell 13: 593-606.
52. Gaskins E, Gilk S, DeVore N, Mann T, Ward G, et al. (2004) Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J Cell Biol 165: 383-393.
53. Johnson TM, Rajfur Z, Jacobson K, Beckers CJ, (2007) Immobilization of the type XIV myosin complex in Toxoplasma gondii. Mol Biol Cell 18: 3039-3046.
54. Angrisano F, Riglar DT, Sturm A, Volz JC, Delves MJ, et al. (2012) Spatial localisation of actin filaments across developmental stages of the malaria parasite. PLoS One 7: e32188.
55. Schermelleh L, Carlton PM, Haase S, Shao L, Winoto L, et al. (2008) Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320: 1332-1336.
56. Gustafsson MG, Shao L, Carlton PM, Wang CJ, Golubovskaya IN, et al. (2008) Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J 94: 4957-4970.
57. Duraisingh MT, Triglia T, Ralph SA, Rayner JC, Barnwell JW, et al. (2003) Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. Embo J 22: 1047-1057.
58. Triglia T, Chen L, Lopaticki S, Dekiwadia C, Riglar DT, et al. (2011) Plasmodium falciparum merozoite invasion is inhibited by antibodies that target the PfRh2a and b binding domains. PLoS Pathog 7: e1002075.
59. Bushell GR, Ingram LT, Fardoulys CA, Cooper JA, (1988) An antigenic complex in the rhoptries of Plasmodium falciparum. Mol Biochem Parasitol 28: 105-112.
60. Richard D, Kats LM, Langer C, Black CG, Mitri K, et al. (2009) Identification of rhoptry trafficking determinants and evidence for a novel sorting mechanism in the malaria parasite Plasmodium falciparum. PLoS Pathog 5: e1000328.
61. Bannister LH, Mitchell GH, Butcher GA, Dennis ED, (1986) Lamellar membranes associated with rhoptries in erythrocytic merozoites of Plasmodium knowlesi: a clue to the mechanism of invasion. Parasitology 92: 291-303.
62. Carruthers VB, Sibley LD, (1997) Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73: 114-123.
63. Yeoh S, O'Donnell RA, Koussis K, Dluzewski AR, Ansell KH, et al. (2007) Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131: 1072-1083.
64. Dubremetz JF, (2007) Rhoptries are major players in Toxoplasma gondii invasion and host cell interaction. Cell Microbiol 9: 841-848.
65. Saffer LD, Mercereau-Puijalon O, Dubremetz JF, Schwartzman JD, (1992) Localization of a Toxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration. J Protozool 39: 526-530.
66. Boothroyd JC, Dubremetz J-F, (2008) Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat Rev Microbiol 6: 79-88.
67. Healer J, Crawford S, Ralph S, McFadden G, Cowman AF, (2002) Independent translocation of two micronemal proteins in developing Plasmodium falciparum merozoites. Infect Immun 70: 5751-5758.
68. Kawase O, Nishikawa Y, Bannai H, Igarashi M, Matsuo T, et al. (2010) Characterization of a novel thrombospondin-related protein in Toxoplasma gondii. Parasitol Int 59: 211-216.
69. Lopaticki S, Maier AG, Thompson J, Wilson DW, Tham WH, et al. (2011) Reticulocyte and erythrocyte binding-like proteins function cooperatively in invasion of human erythrocytes by malaria parasites. Infect Immun 79: 1107-1117.
70. Kirkitadze MD, Barlow PN, (2001) Structure and flexibility of the multiple domain proteins that regulate complement activation. Immunol Rev 180: 146-161.
71. Vernon LP, Evett GE, Zeikus RD, Gray WR, (1985) A toxic thionin from Pyrularia pubera: purification, properties, and amino acid sequence. Arch Biochem Biophys 238: 18-29.
72. Kaiser K, Camargo N, Coppens I, Morrisey JM, Vaidya AB, et al. (2004) A member of a conserved Plasmodium protein family with membrane-attack complex/perforin (MACPF)-like domains localizes to the micronemes of sporozoites. Mol Biochem Parasitol 133: 15-26.
73. Triglia T, Healer J, Caruana SR, Hodder AN, Anders RF, et al. (2000) Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol 38: 706-718.
74. Shaw MK, (2003) Cell invasion by Theileria sporozoites. Trends Parasitol 19: 2-6.
75. Gardner MJ, Bishop R, Shah T, de Villiers EP, Carlton JM, et al. (2005) Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309: 134-137.
76. Patra KP, Johnson JR, Cantin GT, Yates JR 3rd, Vinetz JM, (2008) Proteomic analysis of zygote and ookinete stages of the avian malaria parasite Plasmodium gallinaceum delineates the homologous proteomes of the lethal human malaria parasite Plasmodium falciparum. Proteomics 8: 2492-2499.
77. Lal K, Prieto JH, Bromley E, Sanderson SJ, Yates JR 3rd, et al. (2009) Characterisation of Plasmodium invasive organelles; an ookinete microneme proteome. Proteomics 9: 1142-1151.
78. Crabb BS, Rug M, Gilberger TW, Thompson JK, Triglia T, et al. (2004) Transfection of the human malaria parasite Plasmodium falciparum. Methods Mol Biol 270: 263-276.
79. Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, et al. (2004) Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 137: 13-21.