The Molecular Basis of Erythrocyte Invasion by Malaria Parasites

Cell Host and Microbe

Volumn 22, Issue 2, 2017, Pages 232-245

  Cowman, Alan F ^a,b   Tonkin, Christopher J ^a,b   Tham, Wai Hong ^a,b   Duraisingh, Manoj T ^c  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

erythrocyte; falciparum; invasion; malaria; merozoite; Plasmodium; vivax

Indexed keywords

MYOSIN ADENOSINE TRIPHOSPHATASE; ANTIBODY; PARASITE ANTIGEN;

CELL INVASION; ERYTHROCYTE; HOST; HUMAN; MEROZOITE; NONHUMAN; PLASMODIUM; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN POLYMORPHISM; REVIEW; SIGNAL TRANSDUCTION; TIGHT JUNCTION; TROPISM; VERTEBRATE; ANIMAL; BLOOD; HOST PARASITE INTERACTION; IMMUNOLOGY; MALARIA; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY;

ANIMALS; ANTIBODIES; ANTIGENS, PROTOZOAN; ERYTHROCYTES; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA; MEROZOITES; PLASMODIUM; SIGNAL TRANSDUCTION;

EID: 85030663407     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.07.003     Document Type: Review

References (116)

1. Ahmed, M.A., Cox-Singh, J., Plasmodium knowlesi—an emerging pathogen. ISBT Sci. Ser. 10:Suppl 1 (2015), 134–140.
2. Alam, M.M., Solyakov, L., Bottrill, A.R., Flueck, C., Siddiqui, F.A., Singh, S., Mistry, S., Viskaduraki, M., Lee, K., Hopp, C.S., et al. Phosphoproteomics reveals malaria parasite Protein Kinase G as a signalling hub regulating egress and invasion. Nat. Commun., 6, 2015, 7285.
3. Alexander, D.L., Mital, J., Ward, G.E., Bradley, P., Boothroyd, J.C., Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathog., 1, 2005, e17.
4. Assefa, S., Lim, C., Preston, M.D., Duffy, C.W., Nair, M.B., Adroub, S.A., Kadir, K.A., Goldberg, J.M., Neafsey, D.E., Divis, P., et al. Population genomic structure and adaptation in the zoonotic malaria parasite Plasmodium knowlesi. Proc. Natl. Acad. Sci. USA 112 (2015), 13027–13032.
5. Bargieri, D.Y., Andenmatten, N., Lagal, V., Thiberge, S., Whitelaw, J.A., Tardieux, I., Meissner, M., Menard, R., Apical membrane antigen 1 mediates apicomplexan parasite attachment but is dispensable for host cell invasion. Nat. Commun., 4, 2013, 2552.
6. Baum, J., Maier, A.G., Good, R.T., Simpson, K.M., Cowman, A.F., Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog., 1, 2005, e37.
7. Baum, J., Papenfuss, A.T., Baum, B., Speed, T.P., Cowman, A.F., Regulation of apicomplexan actin-based motility. Nat. Rev. Microbiol. 4 (2006), 621–628.
8. Baum, J., Richard, D., Healer, J., Rug, M., Krnajski, Z., Gilberger, T.W., Green, J.L., Holder, A.A., Cowman, A.F., A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites. J. Biol. Chem. 281 (2006), 5197–5208.
9. Baum, J., Tonkin, C.J., Paul, A.S., Rug, M., Smith, B.J., Gould, S.B., Richard, D., Pollard, T.D., Cowman, A.F., A malaria parasite formin regulates actin polymerization and localizes to the parasite-erythrocyte moving junction during invasion. Cell Host Microbe 3 (2008), 188–198.
10. Besteiro, S., Michelin, A., Poncet, J., Dubremetz, J.F., Lebrun, M., Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLoS Pathog., 5, 2009, e1000309.
11. Boddey, J.A., Cowman, A.F., Plasmodium nesting: remaking the erythrocyte from the inside out. Annu. Rev. Microbiol. 67 (2013), 243–269.
12. Bookwalter, C.S., Kelsen, A., Leung, J.M., Ward, G.E., Trybus, K.M., A Toxoplasma gondii class XIV myosin, expressed in Sf9 cells with a parasite co-chaperone, requires two light chains for fast motility. J. Biol. Chem. 289 (2014), 30832–30841.
13. Boyle, M.J., Reiling, L., Feng, G., Langer, C., Osier, F.H., Aspeling-Jones, H., Cheng, Y.S., Stubbs, J., Tetteh, K.K., Conway, D.J., et al. Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity 42 (2015), 580–590.
14. Bullen, H.E., Jia, Y., Yamaryo-Botte, Y., Bisio, H., Zhang, O., Jemelin, N.K., Marq, J.B., Carruthers, V., Botte, C.Y., Soldati-Favre, D., Phosphatidic acid-mediated signaling regulates microneme secretion in Toxoplasma. Cell Host Microbe 19 (2016), 349–360.
15. Camus, D., Hadley, T.J., A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 230 (1985), 553–556.
16. Chen, L., Lopaticki, S., Riglar, D.T., Dekiwadia, C., Uboldi, A.D., Tham, W.H., O'Neill, M.T., Richard, D., Baum, J., Ralph, S.A., et al. An EGF-like protein forms a complex with PfRh5 and is required for invasion of human erythrocytes by Plasmodium falciparum. PLoS Pathog., 7, 2011, e1002199.
17. Chen, L., Xu, Y., Healer, J., Thompson, J.K., Smith, B.J., Lawrence, M.C., Cowman, A.F., Crystal structure of PfRh5, an essential P. falciparum ligand for invasion of human erythrocytes. eLife, 3, 2014, 10.7554/eLife.04187.
18. Chen, L., Xu, Y., Wong, W., Thompson, J.K., Healer, J., Goddard-Borger, E., Lawrence, M.C., Cowman, A.F., Structural basis for inhibition of erythrocyte invasion by antibodies to Plasmodium falciparum protein CyRPA. Elife, 6, 2017, 10.7554/eLife.21347.
19. Chotivanich, K., Udomsangpetch, R., Simpson, J.A., Newton, P., Pukrittayakamee, S., Looareesuwan, S., White, N.J., Parasite multiplication potential and the severity of Falciparum malaria. J. Infect. Dis. 181 (2000), 1206–1209.
20. Cowman, A.F., Healer, J., Marapana, D., Marsh, K., Malaria: biology and disease. Cell 167 (2016), 610–624.
21. Cowper, B., Matthews, S., Tomley, F., The molecular basis for the distinct host and tissue tropisms of coccidian parasites. Mol. Biochem. Parasitol. 186 (2012), 1–10.
22. Crosnier, C., Bustamante, L.Y., Bartholdson, S.J., Bei, A.K., Theron, M., Uchikawa, M., Mboup, S., Ndir, O., Kwiatkowski, D.P., Duraisingh, M.T., et al. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480 (2011), 534–537.
23. Culleton, R.L., Mita, T., Ndounga, M., Unger, H., Cravo, P.V., Paganotti, G.M., Takahashi, N., Kaneko, A., Eto, H., Tinto, H., et al. Failure to detect Plasmodium vivax in West and Central Africa by PCR species typing. Malar. J., 7, 2008, 174.
24. Daher, W., Plattner, F., Carlier, M.F., Soldati-Favre, D., Concerted action of two formins in gliding motility and host cell invasion by Toxoplasma gondii. PLoS Pathog., 6, 2010, e1001132.
25. Dankwa, S., Lim, C., Bei, A.K., Jiang, R.H., Abshire, J.R., Patel, S.D., Goldberg, J.M., Moreno, Y., Kono, M., Niles, J.C., et al. Ancient human sialic acid variant restricts an emerging zoonotic malaria parasite. Nat. Commun., 7, 2016, 11187.
26. Das, S., Hertrich, N., Perrin, A.J., Withers-Martinez, C., Collins, C.R., Jones, M.L., Watermeyer, J.M., Fobes, E.T., Martin, S.R., Saibil, H.R., et al. Processing of Plasmodium falciparum merozoite surface protein MSP1 activates a spectrin-binding function enabling parasite egress from RBCs. Cell Host Microbe 18 (2015), 433–444.
27. Dasgupta, S., Auth, T., Gov, N.S., Satchwell, T.J., Hanssen, E., Zuccala, E.S., Riglar, D.T., Toye, A.M., Betz, T., Baum, J., et al. Membrane-wrapping contributions to malaria parasite invasion of the human erythrocyte. Biophys. J. 107 (2014), 43–54.
28. Dawn, A., Singh, S., More, K.R., Siddiqui, F.A., Pachikara, N., Ramdani, G., Langsley, G., Chitnis, C.E., The central role of cAMP in regulating Plasmodium falciparum merozoite invasion of human erythrocytes. PLoS Pathog., 10, 2014, e1004520.
29. Deans, A.M., Nery, S., Conway, D.J., Kai, O., Marsh, K., Rowe, J.A., Invasion pathways and malaria severity in Kenyan Plasmodium falciparum clinical isolates. Infect. Immun. 75 (2007), 3014–3020.
30. Douglas, A.D., Baldeviano, G.C., Lucas, C.M., Lugo-Roman, L.A., Crosnier, C., Bartholdson, S.J., Diouf, A., Miura, K., Lambert, L.E., Ventocilla, J.A., et al. A PfRH5-based vaccine is efficacious against Heterologous strain blood-stage Plasmodium falciparum infection in aotus monkeys. Cell Host Microbe 17 (2015), 130–139.
31. Douglas, A.D., Williams, A.R., Illingworth, J.J., Kamuyu, G., Biswas, S., Goodman, A.L., Wyllie, D.H., Crosnier, C., Miura, K., Wright, G.J., et al. The blood-stage malaria antigen PfRH5 is susceptible to vaccine-inducible cross-strain neutralizing antibody. Nat. Commun., 2, 2011, 601.
32. Douglas, A.D., Williams, A.R., Knuepfer, E., Illingworth, J.J., Furze, J.M., Crosnier, C., Choudhary, P., Bustamante, L.Y., Zakutansky, S.E., Awuah, D.K., et al. Neutralization of Plasmodium falciparum merozoites by antibodies against PfRH5. J. Immunol. 192 (2014), 245–258.
33. Dreyer, A.M., Matile, H., Papastogiannidis, P., Kamber, J., Favuzza, P., Voss, T.S., Wittlin, S., Pluschke, G., Passive immunoprotection of Plasmodium falciparum-infected mice designates the CyRPA as candidate malaria vaccine antigen. J. Immunol. 188 (2012), 6225–6237.
34. Duraisingh, M., Triglia, T., Ralph, S., Rayner, J., Barnwell, J., McFadden, G., Cowman, A., Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J. 22 (2003), 1047–1057.
35. Dvorak, J.A., Miller, L.H., Whitehouse, W.C., Shiroishi, T., Invasion of erythrocytes by malaria merozoites. Science 187 (1975), 748–750.
36. 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., et al. A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes. Science 328 (2010), 910–912.
37. Egan, E.S., Jiang, R.H., Moechtar, M.A., Barteneva, N.S., Weekes, M.P., Nobre, L.V., Gygi, S.P., Paulo, J.A., Frantzreb, C., Tani, Y., et al. Malaria. A forward genetic screen identifies erythrocyte CD55 as essential for Plasmodium falciparum invasion. Science 348 (2015), 711–714.
38. Elsworth, B., Sanders, P.R., Nebl, T., Batinovic, S., Kalanon, M., Nie, C.Q., Charnaud, S.C., Bullen, H.E., de Koning Ward, T.F., Tilley, L., et al. Proteomic analysis reveals novel proteins associated with the Plasmodium protein exporter PTEX and a loss of complex stability upon truncation of the core PTEX component, PTEX150. Cell Microbiol. 18 (2016), 1551–1569.
39. Engelberg, K., Paul, A.S., Prinz, B., Kono, M., Ching, W., Heincke, D., Dobner, T., Spielmann, T., Duraisingh, M.T., Gilberger, T.W., Specific phosphorylation of the PfRh2b invasion ligand of Plasmodium falciparum. Biochem. J. 452 (2013), 457–466.
40. Farrell, A., Thirugnanam, S., Lorestani, A., Dvorin, J.D., Eidell, K.P., Ferguson, D.J., Anderson-White, B.R., Duraisingh, M.T., Marth, G.T., Gubbels, M.J., A DOC2 protein identified by mutational profiling is essential for apicomplexan parasite exocytosis. Science 335 (2012), 218–221.
41. Favuzza, P., Guffart, E., Tamborrini, M., Scherer, B., Dreyer, A.M., Rufer, A.C., Erny, J., Hoernschemeyer, J., Thoma, R., Schmid, G., et al. Structure of the malaria vaccine candidate antigen CyRPA and its complex with a parasite invasion inhibitory antibody. Elife, 6, 2017, 10.7554/eLife.20383.
42. Frenal, K., Polonais, V., Marq, J.B., Stratmann, R., Limenitakis, J., Soldati-Favre, D., Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe 8 (2010), 343–357.
43. Galaway, F., Drought, L.G., Fala, M., Cross, N., Kemp, A.C., Rayner, J.C., Wright, G.J., P113 is a merozoite surface protein that binds the N terminus of Plasmodium falciparum RH5. Nat. Commun., 8, 2017, 14333.
44. Galinski, M.R., Medina, C.C., Ingravallo, P., Barnwell, J.W., A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell 69 (1992), 1213–1226.
45. Gao, X., Gunalan, K., Yap, S.S., Preiser, P.R., Triggers of key calcium signals during erythrocyte invasion by Plasmodium falciparum. Nat. Commun., 4, 2013, 2862.
46. Gaskins, E., Gilk, S., DeVore, N., Mann, T., Ward, G., Beckers, C., Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J. Cell Biol. 165 (2004), 383–393.
47. Gilberger, T., Thompson, J., Triglia, T., Good, R., Duraisingh, M., Cowman, A., A novel erythrocyte binding antigen-175 paralogue from Plasmodium falciparum defines a new trypsin-resistant receptor on human erythrocytes. J. Biol. Chem. 278 (2003), 14480–14486.
48. Gilson, P.R., Crabb, B.S., Morphology and kinetics of the three distinct phases of red blood cell invasion by Plasmodium falciparum merozoites. Int. J. Parasitol. 39 (2009), 91–96.
49. Green, J.L., Martin, S.R., Fielden, J., Ksagoni, A., Grainger, M., Yim Lim, B.Y., Molloy, J.E., Holder, A.A., The MTIP-myosin A complex in blood stage malaria parasites. J. Mol. Biol. 355 (2006), 933–941.
50. 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. 283 (2008), 30980–30989.
51. Gruszczyk, J., Lim, N.T., Arnott, A., He, W.Q., Nguitragool, W., Roobsoong, W., Mok, Y.F., Murphy, J.M., Smith, K.R., Lee, S., et al. Structurally conserved erythrocyte-binding domain in Plasmodium provides a versatile scaffold for alternate receptor engagement. Proc. Natl. Acad. Sci. USA 113 (2016), E191–E200.
52. Harding, C.R., Egarter, S., Gow, M., Jimenez-Ruiz, E., Ferguson, D.J., Meissner, M., Gliding associated proteins play essential roles during the formation of the inner membrane complex of Toxoplasma gondii. PLoS Pathog., 12, 2016, e1005403.
53. Haynes, J.D., Dalton, J.P., Klotz, F.W., McGinniss, M.H., Hadley, T.J., Hudson, D.E., Miller, L.H., Receptor-like specificity of a Plasmodium knowlesi malarial protein that binds to Duffy antigen ligands on erythrocytes. J. Exp. Med. 167 (1988), 1873–1881.
54. Hayton, K., Gaur, D., Liu, A., Takahashi, J., Henschen, B., Singh, S., Lambert, L., Furuya, T., Bouttenot, R., Doll, M., et al. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 4 (2008), 40–51.
55. Healer, J., Crawford, S., Ralph, S., McFadden, G., Cowman, A.F., Independent translocation of two micronemal proteins in developing Plasmodium falciparum merozoites. Infect. Immun. 70 (2002), 5751–5758.
56. Hester, J., Chan, E.R., Menard, D., Mercereau-Puijalon, O., Barnwell, J., Zimmerman, P.A., Serre, D., De novo assembly of a field isolate genome reveals novel Plasmodium vivax erythrocyte invasion genes. PLoS Negl. Trop. Dis., 7, 2013, e2569.
57. Holder, A.A., Mohd Ridzuan, M.A., Green, J.L., Calcium dependent protein kinase 1 and calcium fluxes in the malaria parasite. Microbes Infect. 14 (2012), 825–830.
58. Jacot, D., Tosetti, N., Pires, I., Stock, J., Graindorge, A., Hung, Y.F., Han, H., Tewari, R., Kursula, I., Soldati-Favre, D., An apicomplexan actin-binding protein serves as a connector and lipid sensor to coordinate motility and invasion. Cell Host Microbe 20 (2016), 731–743.
59. Jewett, T.J., Sibley, L.D., Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol. Cell 11 (2003), 885–894.
60. Kato, N., Sakata, T., Breton, G., Le Roch, K.G., Nagle, A., Andersen, C., Bursulaya, B., Henson, K., Johnson, J., Kumar, K.A., et al. Gene expression signatures and small-molecule compounds link a protein kinase to Plasmodium falciparum motility. Nat. Chem. Biol. 4 (2008), 347–356.
61. Kennedy, A.T., Schmidt, C.Q., Thompson, J.K., Weiss, G.E., Taechalertpaisarn, T., Gilson, P.R., Barlow, P.N., Crabb, B.S., Cowman, A.F., Tham, W.H., Recruitment of factor H as a novel complement evasion strategy for blood-stage Plasmodium falciparum infection. J. Immunol. 196 (2016), 1239–1248.
62. Koch, M., Wright, K.E., Otto, O., Herbig, M., Salinas, N.D., Tolia, N.H., Satchwell, T.J., Guck, J., Brooks, N.J., Baum, J., Plasmodium falciparum erythrocyte-binding antigen 175 triggers a biophysical change in the red blood cell that facilitates invasion. Proc. Natl. Acad. Sci. USA 114 (2017), 4225–4230.
63. Kremer, K., Kamin, D., Rittweger, E., Wilkes, J., Flammer, H., Mahler, S., Heng, J., Tonkin, C.J., Langsley, G., Hell, S.W., et al. An overexpression screen of Toxoplasma gondii Rab-GTPases reveals distinct transport routes to the micronemes. PLoS Pathog., 9, 2013, e1003213.
64. Krief, S., Escalante, A.A., Pacheco, M.A., Mugisha, L., Andre, C., Halbwax, M., Fischer, A., Krief, J.M., Kasenene, J.M., Crandfield, M., et al. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog., 6, 2010, e1000765.
65. Larremore, D.B., Sundararaman, S.A., Liu, W., Proto, W.R., Clauset, A., Loy, D.E., Speede, S., Plenderleith, L.J., Sharp, P.M., Hahn, B.H., et al. Ape parasite origins of human malaria virulence genes. Nat. Commun., 6, 2015, 8368.
66. Lasonder, E., Green, J.L., Camarda, G., Talabani, H., Holder, A.A., Langsley, G., Alano, P., The Plasmodium falciparum schizont phosphoproteome reveals extensive phosphatidylinositol and cAMP-protein kinase A signaling. J. Proteome Res. 11 (2012), 5323–5337.
67. Lew, V.L., Tiffert, T., Is invasion efficiency in malaria controlled by pre-invasion events?. Trends Parasitol. 23 (2007), 481–484.
68. 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., 6, 2010, e1000941.
69. Lim, C., Hansen, E., DeSimone, T.M., Moreno, Y., Junker, K., Bei, A., Brugnara, C., Buckee, C.O., Duraisingh, M.T., Expansion of host cellular niche can drive adaptation of a zoonotic malaria parasite to humans. Nat. Commun., 4, 2013, 1638.
70. Liu, W., Li, Y., Learn, G.H., Rudicell, R.S., Robertson, J.D., Keele, B.F., Ndjango, J.B., Sanz, C.M., Morgan, D.B., Locatelli, S., et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467 (2010), 420–425.
71. Lopaticki, S., Maier, A.G., Thompson, J., Wilson, D.W., Tham, W.H., Triglia, T., Gout, A., Speed, T.P., Beeson, J.G., Healer, J., et al. Reticulocyte and erythrocyte binding-like proteins function cooperatively in invasion of human erythrocytes by malaria parasites. Infect. Immun. 79 (2011), 1107–1117.
72. Lourido, S., Tang, K., Sibley, L.D., Distinct signalling pathways control Toxoplasma egress and host-cell invasion. EMBO J. 31 (2012), 4524–4534.
73. Maier, A., Duraisingh, M., Reeder, J., Patel, S., Kazura, J., Zimmerman, P., Cowman, A., Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat. Med. 9 (2003), 87–92.
74. Malaria Genomic Epidemiology Network, Band, G., Rockett, K.A., Spencer, C.C., Kwiatkowski, D.P., A novel locus of resistance to severe malaria in a region of ancient balancing selection. Nature 526 (2015), 253–257.
75. Mayer, D.C., Cofie, J., Jiang, L., Hartl, D.L., Tracy, E., Kabat, J., Mendoza, L.H., Miller, L.H., Glycophorin B is the erythrocyte receptor of Plasmodium falciparum erythrocyte-binding ligand, EBL-1. Proc. Natl. Acad. Sci. USA 106 (2009), 5348–5352.
76. Mayer, D.C., Jiang, L., Achur, R.N., Kakizaki, I., Gowda, D.C., Miller, L.H., The glycophorin C N-linked glycan is a critical component of the ligand for the Plasmodium falciparum erythrocyte receptor BAEBL. Proc. Natl. Acad. Sci. USA 103 (2006), 2358–2362.
77. Mehta, S., Sibley, L.D., Toxoplasma gondii actin depolymerizing factor acts primarily to sequester G-actin. J. Biol. Chem. 285 (2010), 6835–6847.
78. Mehta, S., Sibley, L.D., Actin depolymerizing factor controls actin turnover and gliding motility in Toxoplasma gondii. Mol. Biol. Cell 22 (2011), 1290–1299.
79. Meissner, M., Schluter, D., Soldati, D., Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298 (2002), 837–840.
80. Miller, L.H., Mason, S.J., Clyde, D.F., McGinniss, M.H., The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N. Engl. J. Med. 295 (1976), 302–304.
81. Moon, R.W., Hall, J., Rangkuti, F., Ho, Y.S., Almond, N., Mitchell, G.H., Pain, A., Holder, A.A., Blackman, M.J., Adaptation of the genetically tractable malaria pathogen Plasmodium knowlesi to continuous culture in human erythrocytes. Proc. Natl. Acad. Sci. USA 110 (2013), 531–536.
82. Moon, R.W., Sharaf, H., Hastings, C.H., Ho, Y.S., Nair, M.B., Rchiad, Z., Knuepfer, E., Ramaprasad, A., Mohring, F., Amir, A., et al. Normocyte-binding protein required for human erythrocyte invasion by the zoonotic malaria parasite Plasmodium knowlesi. Proc. Natl. Acad. Sci. USA 113 (2016), 7231–7236.
83. Naing, C., Whittaker, M.A., Nyunt Wai, V., Mak, J.W., Is Plasmodium vivax malaria a severe malaria?: a systematic review and meta-analysis. PLoS Negl. Trop. Dis., 8, 2014, e3071.
84. Ntumngia, F.B., Schloegel, J., McHenry, A.M., Barnes, S.J., George, M.T., Kennedy, S., Adams, J.H., Immunogenicity of single versus mixed allele vaccines of Plasmodium vivax Duffy binding protein region II. Vaccine 31 (2013), 4382–4388.
85. Olshina, M.A., Baumann, H., Willison, K.R., Baum, J., Plasmodium actin is incompletely folded by heterologous protein-folding machinery and likely requires the native Plasmodium chaperonin complex to enter a mature functional state. FASEB J. 30 (2016), 405–416.
86. Paul, A.S., Saha, S., Engelberg, K., Jiang, R.H., Coleman, B.I., Kosber, A.L., Chen, C.T., Ganter, M., Espy, N., Gilberger, T.W., et al. Parasite calcineurin regulates host cell recognition and attachment by apicomplexans. Cell Host Microbe 18 (2015), 49–60.
87. Plattner, F., Yarovinsky, F., Romero, S., Didry, D., Carlier, M.F., Sher, A., Soldati-Favre, D., Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 3 (2008), 77–87.
88. Prinz, B., Harvey, K.L., Wilcke, L., Ruch, U., Engelberg, K., Biller, L., Lucet, I., Erkelenz, S., Heincke, D., Spielmann, T., et al. Hierarchical phosphorylation of apical membrane antigen 1 is required for efficient red blood cell invasion by malaria parasites. Sci. Rep., 6, 2016, 34479.
89. Rayner, J.C., Vargas-Serrato, E., Huber, C.S., Galinski, M.R., Barnwell, J.W., A Plasmodium falciparum homologue of Plasmodium vivax reticulocyte binding protein (PvRBP1) defines a trypsin-resistant erythrocyte invasion pathway. J. Exp. Med. 194 (2001), 1571–1581.
90. Reddy, K.S., Amlabu, E., Pandey, A.K., Mitra, P., Chauhan, V.S., Gaur, D., Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion. Proc. Natl. Acad. Sci. USA, 2015, 10.1073/pnas.1415466112.
91. Riglar, D.T., Richard, D., Wilson, D.W., Boyle, M.J., Dekiwadia, C., Turnbull, L., Angrisano, F., Marapana, D.S., Rogers, K.L., Whitchurch, C.B., et al. Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe 9 (2011), 9–20.
92. Sanders, P.R., Gilson, P.R., Cantin, G.T., Greenbaum, D.C., Nebl, T., Carucci, D.J., McConville, M.J., Schofield, L., Hodder, A.N., Yates, J.R. 3rd, et al. Distinct protein classes including novel merozoite surface antigens in Raft-like membranes of Plasmodium falciparum. J. Biol. Chem. 280 (2005), 40169–40176.
93. Schmidt, C.Q., Kennedy, A.T., Tham, W.H., More than just immune evasion: hijacking complement by Plasmodium falciparum. Mol. Immunol. 67 (2015), 71–84.
94. Schuldt, K., Ehmen, C., Sievertsen, J., Evans, J., May, J., Ansong, D., Muntau, B., Ruge, G., Timmann, C., Agbenyega, T., et al. Lack of association of CD55 receptor genetic variants and severe malaria in Ghanaian children. G3 (Bethesda) 7 (2017), 859–864.
95. Sidik, S.M., Huet, D., Ganesan, S.M., Huynh, M.H., Wang, T., Nasamu, A.S., Thiru, P., Saeij, J.P., Carruthers, V.B., Niles, J.C., et al. A genome-wide CRISPR screen in toxoplasma identifies essential apicomplexan genes. Cell 166 (2016), 1423–1435.e12.
96. Singh, B., Kim Sung, L., Matusop, A., Radhakrishnan, A., Shamsul, S.S., Cox-Singh, J., Thomas, A., Conway, D.J., A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet 363 (2004), 1017–1024.
97. 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., 6, 2010, e1000746.
98. Sisquella, X., Nebl, T., Thompson, J.K., Whitehead, L., Malpede, B.M., Salinas, N.D., Rogers, K., Tolia, N.H., Fleig, A., O'Neill, J., et al. Plasmodium falciparum ligand binding to erythrocytes induce alterations in deformability essential for invasion. Elife, 6, 2017, 10.7554/eLife.21083.
99. Stubbs, J., Simpson, K., Triglia, T., Plouffe, D., Tonkin, C., Duraisingh, M., Maier, A., Winzeler, E., Cowman, A., Molecular mechanism for switching of P-falciparum invasion pathways into human erythrocytes. Science 309 (2005), 1384–1387.
100. 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. Eukaryot. Cell 9 (2010), 37–45.
101. Tham, W.-H., Wilson, D.W., Lopaticki, S., Schmidt, C.Q., Tetteh-Quarcoo, P.B., Barlow, P.N., Richard, D., Corbin, J.E., Beeson, J.G., Cowman, A.F., Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand. Proc. Natl. Acad. Sci. USA 107 (2010), 17327–17332.
102. Tham, W.H., Lim, N.T., Weiss, G.E., Lopaticki, S., Ansell, B.R., Bird, M., Lucet, I., Dorin-Semblat, D., Doerig, C., Gilson, P.R., et al. Plasmodium falciparum adhesins play an essential role in signalling and activation of invasion into human erythrocytes. PLoS Pathog., 11, 2015, e1005343.
103. Tolia, N.H., Enemark, E.J., Sim, B.K., Joshua-Tor, L., Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 122 (2005), 183–193.
104. Tonkin, M.L., Roques, M., Lamarque, M.H., Pugniere, M., Douguet, D., Crawford, J., Lebrun, M., Boulanger, M.J., Host cell invasion by apicomplexan parasites: insights from the co-structure of AMA1 with a RON2 peptide. Science 333 (2011), 463–467.
105. Triglia, T., Duraisingh, M., Good, R., Cowman, A., Reticulocyte-binding protein homologue 1 is required for sialic acid-dependent invasion into human erythrocytes by Plasmodium falciparum. Mol. Microbiol. 55 (2005), 162–174.
106. Vahokoski, J., Bhargav, S.P., Desfosses, A., Andreadaki, M., Kumpula, E.P., Martinez, S.M., Ignatev, A., Lepper, S., Frischknecht, F., Siden-Kiamos, I., et al. Structural differences explain diverse functions of Plasmodium actins. PLoS Pathog., 10, 2014, e1004091.
107. Varki, A., Gagneux, P., Human-specific evolution of sialic acid targets: explaining the malignant malaria mystery?. Proc. Natl. Acad. Sci. USA 106 (2009), 14739–14740.
108. Volz, J.C., Yap, A., Sisquella, X., Thompson, J.K., Lim, N.T., Whitehead, L.W., Chen, L., Lampe, M., Tham, W.H., Wilson, D., et al. Essential role of the PfRh5/PfRipr/CyRPA complex during Plasmodium falciparum invasion of erythrocytes. Cell Host Microbe 20 (2016), 60–71.
109. Wanaguru, M., Liu, W., Hahn, B.H., Rayner, J.C., Wright, G.J., RH5-Basigin interaction plays a major role in the host tropism of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 110 (2013), 20735–20740.
110. Weiss, G.E., Gilson, P.R., Taechalertpaisarn, T., Tham, W.H., de Jong, N.W., Harvey, K.L., Fowkes, F.J., Barlow, P.N., Rayner, J.C., Wright, G.J., et al. Revealing the sequence and resulting cellular morphology of receptor-ligand interactions during Plasmodium falciparum invasion of erythrocytes. PLoS Pathog., 11, 2015, e1004670.
111. WHO (2016). World malaria report. http://www.who.int/malaria/publications/world-malaria-report-2016/en/.
112. Williams, A.R., Douglas, A.D., Miura, K., Illingworth, J.J., Choudhary, P., Murungi, L.M., Furze, J.M., Diouf, A., Miotto, O., Crosnier, C., et al. Enhancing blockade of Plasmodium falciparum erythrocyte invasion: assessing combinations of antibodies against PfRH5 and other merozoite antigens. PLoS Pathog., 8, 2012, e1002991.
113. Williams, M.J., Alonso, H., Enciso, M., Egarter, S., Sheiner, L., Meissner, M., Striepen, B., Smith, B.J., Tonkin, C.J., Two essential light chains regulate the MyoA lever arm to promote Toxoplasma gliding motility. MBio, 6, 2015 e00845–15.
114. Wright, K.E., Hjerrild, K.A., Bartlett, J., Douglas, A.D., Jin, J., Brown, R.E., Illingworth, J.J., Ashfield, R., Clemmensen, S.B., de Jongh, W.A., et al. Structure of malaria invasion protein RH5 with erythrocyte basigin and blocking antibodies. Nature, 2014, 10.1038/nature13715.
115. Yeoh, S., O'Donnell, R.A., Koussis, K., Dluzewski, A.R., Ansell, K.H., Osborne, S.A., Hackett, F., Withers-Martinez, C., Mitchell, G.H., Bannister, L.H., et al. Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131 (2007), 1072–1083.
116. Zuccala, E.S., Baum, J., Cytoskeletal and membrane remodelling during malaria parasite invasion of the human erythrocyte. Br. J. Haematol. 154 (2011), 680–689.