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Abstract

Phylum Apicomplexa comprises a large group of obligate intracellular parasites of high medical and veterinary importance. These organisms succeed intracellularly by effecting remarkable changes in a broad range of diverse host cells. The transformation of the host erythrocyte is particularly striking in the case of the malaria parasite . exports hundreds of proteins that mediate a complex cellular renovation marked by changes in the permeability, rigidity, and cytoadherence properties of the host erythrocyte. The past decade has seen enormous progress in understanding the identity and function of these exported effectors, as well as the mechanisms by which they are trafficked into the host cell. Here we review these advances, place them in the context of host manipulation by related apicomplexans, and propose key directions for future research.

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2015-06-02
2024-04-20
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Literature Cited

  1. Levine ND. 1.  1988. Progress in taxonomy of the Apicomplexan protozoa. J. Protozool. 35:518–20 [Google Scholar]
  2. Hunter CA, Sibley LD. 2.  2012. Modulation of innate immunity by Toxoplasma gondii virulence effectors. Nat. Rev. Microbiol. 10:766–78 [Google Scholar]
  3. Dobbelaere DA, Küenzi P. 3.  2004. The strategies of the Theileria parasite: a new twist in host–pathogen interactions. Curr. Opin. Immunol. 16:524–30 [Google Scholar]
  4. Boddey JA, Hodder AN, Gunther S, Gilson PR, Patsiouras H. 4.  et al. 2010. An aspartyl protease directs malaria effector proteins to the host cell. Nature 463:627–31 [Google Scholar]
  5. Sleebs BE, Lopaticki S, Marapana DS, O'Neill MT, Rajasekaran P. 5.  et al. 2014. Inhibition of plasmepsin V activity demonstrates its essential role in protein export, PfEMP1 display, and survival of malaria parasites. PLOS Biol. 12:e1001897 [Google Scholar]
  6. Russo I, Babbitt S, Muralidharan V, Butler T, Oksman A, Goldberg DE. 6.  2010. Plasmepsin V licenses Plasmodium proteins for export into the host erythrocyte. Nature 463:632–36 [Google Scholar]
  7. Beck JR, Muralidharan V, Oksman A, Goldberg DE. 7.  2014. PTEX component HSP101 mediates export of diverse malaria effectors into host erythrocytes. Nature 511:592–95 [Google Scholar]
  8. Elsworth B, Matthews K, Nie CQ, Kalanon M, Charnaud SC. 8.  et al. 2014. PTEX is an essential nexus for protein export in malaria parasites. Nature 511:587–91 [Google Scholar]
  9. Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S. 9.  et al. 2008. Exported proteins required for virulence and rigidity of Plasmodium falciparum–infected human erythrocytes. Cell 134:48–61 [Google Scholar]
  10. Smith JD, Rowe JA, Higgins MK, Lavstsen T. 10.  2013. Malaria's deadly grip: cytoadhesion of Plasmodium falciparum–infected erythrocytes. Cell Microbiol. 15:1976–83 [Google Scholar]
  11. 11. World Health Organ. (WHO) 2014. World Malaria Report Geneva: WHO http://www.who.int/malaria/publications/world_malaria_report_2014/report/en/
  12. Maier AG, Cooke BM, Cowman AF, Tilley L. 12.  2009. Malaria parasite proteins that remodel the host erythrocyte. Nat. Rev. Microbiol. 7:341–54 [Google Scholar]
  13. Boddey JA, Cowman AF. 13.  2013. Plasmodium nesting: remaking the erythrocyte from the inside out. Annu. Rev. Microbiol. 67:243–69 [Google Scholar]
  14. Marti M, Spielmann T. 14.  2013. Protein export in malaria parasites: many membranes to cross. Curr. Opin. Microbiol. 16:445–51 [Google Scholar]
  15. Elsworth B, Crabb BS, Gilson PR. 15.  2014. Protein export in malaria parasites: an update. Cell Microbiol. 16:355–63 [Google Scholar]
  16. Prajapati SK, Culleton R, Singh OP. 16.  2014. Protein trafficking in Plasmodium falciparum–infected red cells and impact of the expansion of exported protein families. Parasitology 30:1–11 [Google Scholar]
  17. Ward GE, Miller LH, Dvorak JA. 17.  1993. The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes. J. Cell Sci. 106:237–48 [Google Scholar]
  18. Suss-Toby E, Zimmerberg J, Ward GE. 18.  1996. Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. PNAS 93:8413–18 [Google Scholar]
  19. Lingelbach K, Joiner KA. 19.  1998. The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J. Cell Sci. 111:1467–75 [Google Scholar]
  20. Marti M, Good RT, Rug M, Knuepfer E, Cowman AF. 20.  2004. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306:1930–33 [Google Scholar]
  21. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T. 21.  et al. 2004. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306:1934–37 [Google Scholar]
  22. Chang HH, Falick AM, Carlton PM, Sedat JW, DeRisi JL, Marletta MA. 22.  2008. N-Terminal processing of proteins exported by malaria parasites. Mol. Biochem. Parasitol. 160:107–15 [Google Scholar]
  23. Osborne AR, Speicher KD, Tamez PA, Bhattacharjee S, Speicher DW, Haldar K. 23.  2010. The host targeting motif in exported Plasmodium proteins is cleaved in the parasite endoplasmic reticulum. Mol. Biochem. Parasitol. 171:25–31 [Google Scholar]
  24. Boddey JA, Moritz RL, Simpson RJ, Cowman AF. 24.  2009. Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10:285–99 [Google Scholar]
  25. Tarr SJ, Cryar A, Thalassinos K, Haldar K, Osborne AR. 25.  2013. The C-terminal portion of the cleaved HT motif is necessary and sufficient to mediate export of proteins from the malaria parasite into its host cell. Mol. Microbiol. 87:835–50 [Google Scholar]
  26. Sargeant TJ, Marti M, Caler E, Carlton JM, Simpson K. 26.  et al. 2006. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol. 7:R12 [Google Scholar]
  27. Grüring C, Heiber A, Kruse F, Flemming S, Franci G. 27.  et al. 2012. Uncovering common principles in protein export of malaria parasites. Cell Host Microbe 12:717–29 [Google Scholar]
  28. Bhattacharjee S, Stahelin RV, Speicher KD, Speicher DW, Haldar K. 28.  2012. Endoplasmic reticulum PI(3)P lipid binding targets malaria proteins to the host cell. Cell 148:201–12 [Google Scholar]
  29. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E. 29.  et al. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284–95 [Google Scholar]
  30. Jiang RH, Stahelin RV, Bhattacharjee S, Haldar K. 30.  2013. Eukaryotic virulence determinants utilize phosphoinositides at the ER and host cell surface. Trends Microbiol. 21:145–56 [Google Scholar]
  31. Bhattacharjee S, Speicher KD, Stahelin RV, Speicher DW, Haldar K. 31.  2012. PI(3)P-independent and -dependent pathways function together in a vacuolar translocation sequence to target malarial proteins to the host erythrocyte. Mol. Biochem. Parasitol. 185:106–13 [Google Scholar]
  32. Heiber A, Kruse F, Pick C, Grüring C, Flemming S. 32.  et al. 2013. Identification of new PNEPs indicates a substantial non-PEXEL exportome and underpins common features in Plasmodium falciparum protein export. PLOS Pathog. 9:e1003546 [Google Scholar]
  33. Pasini EM, Braks JA, Fonager J, Klop O, Aime E. 33.  et al. 2013. Proteomic and genetic analyses demonstrate that Plasmodium berghei blood stages export a large and diverse repertoire of proteins. Mol. Cell Proteomics 12:426–48 [Google Scholar]
  34. Haase S, Herrmann S, Grüring C, Heiber A, Jansen PW. 34.  et al. 2009. Sequence requirements for the export of the Plasmodium falciparum Maurer's clefts protein REX2. Mol. Microbiol. 71:1003–17 [Google Scholar]
  35. Ansorge I, Benting J, Bhakdi S, Lingelbach K. 35.  1996. Protein sorting in Plasmodium falciparum–infected red blood cells permeabilized with the pore-forming protein streptolysin O. Biochem. J. 315:307–14 [Google Scholar]
  36. Gehde N, Hinrichs C, Montilla I, Charpian S, Lingelbach K, Przyborski JM. 36.  2009. Protein unfolding is an essential requirement for transport across the parasitophorous vacuolar membrane of Plasmodium falciparum. Mol. Microbiol. 71:613–28 [Google Scholar]
  37. de Koning–Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ. 37.  et al. 2009. A newly discovered protein export machine in malaria parasites. Nature 459:945–49 [Google Scholar]
  38. Bullen HE, Charnaud SC, Kalanon M, Riglar DT, Dekiwadia C. 38.  et al. 2012. Biosynthesis, localization, and macromolecular arrangement of the Plasmodium falciparum translocon of exported proteins (PTEX). J. Biol. Chem. 287:7871–84 [Google Scholar]
  39. Torii M, Adams JH, Miller LH, Aikawa M. 39.  1989. Release of merozoite dense granules during erythrocyte invasion by Plasmodium knowlesi. Infect. Immun. 57:3230–33 [Google Scholar]
  40. Riglar DT, Rogers KL, Hanssen E, Turnbull L, Bullen HE. 40.  et al. 2013. Spatial association with PTEX complexes defines regions for effector export into Plasmodium falciparum–infected erythrocytes. Nat. Commun. 4:1415 [Google Scholar]
  41. Hanson PI, Whiteheart SW. 41.  2005. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 6:519–29 [Google Scholar]
  42. White SR, Lauring B. 42.  2007. AAA+ ATPases: achieving diversity of function with conserved machinery. Traffic 8:1657–67 [Google Scholar]
  43. Sharma A, Sharma A, Dixit S, Sharma A. 43.  2011. Structural insights into thioredoxin-2: a component of malaria parasite protein secretion machinery. Sci. Rep. 1:179 [Google Scholar]
  44. Matthews K, Kalanon M, Chisholm SA, Sturm A, Goodman CD. 44.  et al. 2013. The Plasmodium translocon of exported proteins (PTEX) component thioredoxin-2 is important for maintaining normal blood-stage growth. Mol. Microbiol. 89:1167–86 [Google Scholar]
  45. Matz JM, Matuschewski K, Kooij TW. 45.  2013. Two putative protein export regulators promote Plasmodium blood stage development in vivo. Mol. Biochem. Parasitol. 191:44–52 [Google Scholar]
  46. Eifler N, Vetsch M, Gregorini M, Ringler P, Chami M. 46.  et al. 2006. Cytotoxin ClyA from Escherichia coli assembles to a 13-meric pore independent of its redox-state. EMBO J. 25:2652–61 [Google Scholar]
  47. Balsera M, Goetze TA, Kovács-Bogdán E, Schürmann P, Wagner R. 47.  et al. 2009. Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca2+ and a stromal regulatory disulfide bridge. J. Biol. Chem. 284:2603–16 [Google Scholar]
  48. Mata-Cabana A, Florencio FJ, Lindahl M. 48.  2007. Membrane proteins from the cyanobacterium Synechocystis sp. PCC 6803 interacting with thioredoxin. Proteomics 7:3953–63 [Google Scholar]
  49. Li HM, Chiu CC. 49.  2010. Protein transport into chloroplasts. Annu. Rev. Plant Biol. 61:157–80 [Google Scholar]
  50. Vembar SS, Brodsky JL. 50.  2008. One step at a time: endoplasmic reticulum–associated degradation. Nat. Rev. Mol. Cell Biol. 9:944–57 [Google Scholar]
  51. Bönemann G, Pietrosiuk A, Diemand A, Zentgraf H, Mogk A. 51.  2009. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 28:315–25 [Google Scholar]
  52. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. 52.  2012. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:182–86 [Google Scholar]
  53. Kapitein N, Bönemann G, Pietrosiuk A, Seyffer F, Hausser I. 53.  et al. 2013. ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol. Microbiol. 87:1013–28 [Google Scholar]
  54. Kube S, Kapitein N, Zimniak T, Herzog F, Mogk A, Wendler P. 54.  2014. Structure of the VipA/B type VI secretion complex suggests a contraction-state-specific recycling mechanism. Cell Rep. 8:20–30 [Google Scholar]
  55. Crabb BS, de Koning–Ward TF, Gilson PR. 55.  2010. Protein export in Plasmodium parasites: from the endoplasmic reticulum to the vacuolar export machine. Int. J. Parasitol. 40:509–13 [Google Scholar]
  56. Deponte M, Hoppe HC, Lee MC, Maier AG, Richard D. 56.  et al. 2012. Wherever I may roam: protein and membrane trafficking in P. falciparum–infected red blood cells. Mol. Biochem. Parasitol. 186:95–116 [Google Scholar]
  57. Adisa A, Rug M, Klonis N, Foley M, Cowman AF, Tilley L. 57.  2003. The signal sequence of exported protein 1 directs the green fluorescent protein to the parasitophorous vacuole of transfected malaria parasites. J. Biol. Chem. 278:6532–42 [Google Scholar]
  58. Pietrosiuk A, Lenherr ED, Falk S, Bönemann G, Kopp J. 58.  et al. 2011. Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion. J. Biol. Chem. 286:30010–21 [Google Scholar]
  59. Hanssen E, Carlton P, Deed S, Klonis N, Sedat J. 59.  et al. 2010. Whole cell imaging reveals novel modular features of the exomembrane system of the malaria parasite, Plasmodium falciparum. Int. J. Parasitol. 40:123–34 [Google Scholar]
  60. Aikawa M. 60.  1971. Parasitological review. Plasmodium: the fine structure of malarial parasites. Exp. Parasitol. 30:284–320 [Google Scholar]
  61. Lauer SA, Rathod PK, Ghori N, Haldar K. 61.  1997. A membrane network for nutrient import in red cells infected with the malaria parasite. Science 276:1122–25 [Google Scholar]
  62. Tilley L, Sougrat R, Lithgow T, Hanssen E. 62.  2008. The twists and turns of Maurer's cleft trafficking in P. falciparum–infected erythrocytes. Traffic 9:187–97 [Google Scholar]
  63. Mundwiler-Pachlatko E, Beck HP. 63.  2013. Maurer's clefts, the enigma of Plasmodium falciparum. PNAS 110:19987–94 [Google Scholar]
  64. Grüring C, Heiber A, Kruse F, Ungefehr J, Gilberger TW, Spielmann T. 64.  2011. Development and host cell modifications of Plasmodium falciparum blood stages in four dimensions. Nat. Commun. 2:165 [Google Scholar]
  65. McMillan PJ, Millet C, Batinovic S, Maiorca M, Hanssen E. 65.  et al. 2013. Spatial and temporal mapping of the PfEMP1 export pathway in Plasmodium falciparum. Cell Microbiol. 15:1401–18 [Google Scholar]
  66. Pachlatko E, Rusch S, Müller A, Hemphill A, Tilley L. 66.  et al. 2010. MAHRP2, an exported protein of Plasmodium falciparum, is an essential component of Maurer's cleft tethers. Mol. Microbiol. 77:1136–52 [Google Scholar]
  67. Spycher C, Rug M, Klonis N, Ferguson DJ, Cowman AF. 67.  et al. 2006. Genesis of and trafficking to the Maurer's clefts of Plasmodium falciparum–infected erythrocytes. Mol. Cell. Biol. 26:4074–85 [Google Scholar]
  68. Trelka DP, Schneider TG, Reeder JC, Taraschi TF. 68.  2000. Evidence for vesicle-mediated trafficking of parasite proteins to the host cell cytosol and erythrocyte surface membrane in Plasmodium falciparum infected erythrocytes. Mol. Biochem. Parasitol. 106:131–45 [Google Scholar]
  69. Hanssen E, Sougrat R, Frankland S, Deed S, Klonis N. 69.  et al. 2008. Electron tomography of the Maurer's cleft organelles of Plasmodium falciparum–infected erythrocytes reveals novel structural features. Mol. Microbiol. 67:703–18 [Google Scholar]
  70. Papakrivos J, Newbold CI, Lingelbach K. 70.  2005. A potential novel mechanism for the insertion of a membrane protein revealed by a biochemical analysis of the Plasmodium falciparum cytoadherence molecule PfEMP-1. Mol. Microbiol. 55:1272–84 [Google Scholar]
  71. Knuepfer E, Rug M, Klonis N, Tilley L, Cowman AF. 71.  2005. Trafficking of the major virulence factor to the surface of transfected P. falciparum–infected erythrocytes. Blood 105:4078–87 [Google Scholar]
  72. Külzer S, Charnaud S, Dagan T, Riedel J, Mandal P. 72.  et al. 2012. Plasmodium falciparum–encoded exported hsp70/hsp40 chaperone/co-chaperone complexes within the host erythrocyte. Cell Microbiol. 14:1784–95 [Google Scholar]
  73. Banumathy G, Singh V, Tatu U. 73.  2002. Host chaperones are recruited in membrane-bound complexes by Plasmodium falciparum. J. Biol. Chem. 277:3902–12 [Google Scholar]
  74. Külzer S, Rug M, Brinkmann K, Cannon P, Cowman A. 74.  et al. 2010. Parasite-encoded Hsp40 proteins define novel mobile structures in the cytosol of the P. falciparum–infected erythrocyte. Cell Microbiol. 12:1398–420 [Google Scholar]
  75. Kaneko O, Tsuboi T, Ling IT, Howell S, Shirano M. 75.  et al. 2001. The high molecular mass rhoptry protein, RhopH1, is encoded by members of the clag multigene family in Plasmodium falciparum and Plasmodium yoelii. Mol. Biochem. Parasitol. 118:223–31 [Google Scholar]
  76. Trenholme KR, Gardiner DL, Holt DC, Thomas EA, Cowman AF, Kemp DJ. 76.  2000. clag9: a cytoadherence gene in Plasmodium falciparum essential for binding of parasitized erythrocytes to CD36. PNAS 97:4029–33 [Google Scholar]
  77. Nguitragool W, Bokhari AA, Pillai AD, Rayavara K, Sharma P. 77.  et al. 2011. Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell 145:665–77 [Google Scholar]
  78. Kaneko O, Yim Lim BYS, Iriko H, Ling IT, Otsuki H. 78.  et al. 2005. Apical expression of three RhopH1/Clag proteins as components of the Plasmodium falciparum RhopH complex. Mol. Biochem. Parasitol. 143:20–28 [Google Scholar]
  79. Cowman AF, Berry D, Baum J. 79.  2012. The cellular and molecular basis for malaria parasite invasion of the human red blood cell. J. Cell Biol. 198:961–71 [Google Scholar]
  80. Shen B, Sibley LD. 80.  2012. The moving junction, a key portal to host cell invasion by apicomplexan parasites. Curr. Opin. Microbiol. 15:449–55 [Google Scholar]
  81. Cao J, Kaneko O, Thongkukiatkul A, Tachibana M, Otsuki H. 81.  et al. 2009. Rhoptry neck protein RON2 forms a complex with microneme protein AMA1 in Plasmodium falciparum merozoites. Parasitol. Int. 58:29–35 [Google Scholar]
  82. Anantharaman V, Iyer LM, Balaji S, Aravind L. 82.  2007. Adhesion molecules and other secreted host-interaction determinants in Apicomplexa: insights from comparative genomics. Int. Rev. Cytol. 262:1–74 [Google Scholar]
  83. Ling IT, Florens L, Dluzewski AR, Kaneko O, Grainger M. 83.  et al. 2004. The Plasmodium falciparum clag9 gene encodes a rhoptry protein that is transferred to the host erythrocyte upon invasion. Mol. Microbiol. 52:107–18 [Google Scholar]
  84. Vincensini L, Fall G, Berry L, Blisnick T, Braun Breton C. 84.  2008. The RhopH complex is transferred to the host cell cytoplasm following red blood cell invasion by Plasmodium falciparum. Mol. Biochem. Parasitol. 160:81–89 [Google Scholar]
  85. van Ooij C, Tamez P, Bhattacharjee S, Hiller NL, Harrison T. 85.  et al. 2008. The malaria secretome: from algorithms to essential function in blood stage infection. PLOS Pathog. 4:e1000084 [Google Scholar]
  86. Siau A, Huang X, Yam XY, Bob NS, Sun H. 86.  et al. 2014. Identification of a new export signal in Plasmodium yoelii: identification of a new exportome. Cell Microbiol. 16:673–86 [Google Scholar]
  87. Chua CL, Brown G, Hamilton JA, Rogerson S, Boeuf P. 87.  2013. Monocytes and macrophages in malaria: protection or pathology?. Trends Parasitol. 29:26–34 [Google Scholar]
  88. Scherf A, Lopez-Rubio JJ, Riviere L. 88.  2008. Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol. 62:445–70 [Google Scholar]
  89. Voss TS, Bozdech Z, Bartfai R. 89.  2014. Epigenetic memory takes center stage in the survival strategy of malaria parasites. Curr. Opin. Microbiol. 20C:88–95 [Google Scholar]
  90. Turner L, Lavstsen T, Berger SS, Wang CW, Petersen JE. 90.  et al. 2013. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498:502–5 [Google Scholar]
  91. Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L. 91.  et al. 2004. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 200:1197–203 [Google Scholar]
  92. Kats LM, Fernandez KM, Glenister FK, Herrmann S, Buckingham DW. 92.  et al. 2014. An exported kinase (FIKK4.2) that mediates virulence-associated changes in Plasmodium falciparum–infected red blood cells. Int. J. Parasitol. 44:319–28 [Google Scholar]
  93. Taylor DW, Parra M, Chapman GB, Stearns ME, Rener J. 93.  et al. 1987. Localization of Plasmodium falciparum histidine-rich protein 1 in the erythrocyte skeleton under knobs. Mol. Biochem. Parasitol. 25:165–74 [Google Scholar]
  94. Crabb BS, Cooke BM, Reeder JC, Waller RF, Caruana SR. 94.  et al. 1997. Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89:287–96 [Google Scholar]
  95. Mayer C, Slater L, Erat MC, Konrat R, Vakonakis I. 95.  2012. Structural analysis of the Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) intracellular domain reveals a conserved interaction epitope. J. Biol. Chem. 287:7182–89 [Google Scholar]
  96. Oberli A, Slater LM, Cutts E, Brand F, Mundwiler-Pachlatko E. 96.  et al. 2014. A Plasmodium falciparum PHIST protein binds the virulence factor PfEMP1 and comigrates to knobs on the host cell surface. FASEB J. 28:4420–33 [Google Scholar]
  97. Proellocks NI, Herrmann S, Buckingham DW, Hanssen E, Hodges EK. 97.  et al. 2014. A lysine-rich membrane-associated PHISTb protein involved in alteration of the cytoadhesive properties of Plasmodium falciparum–infected red blood cells. FASEB J. 28:3103–13 [Google Scholar]
  98. Waterkeyn JG, Wickham ME, Davern KM, Cooke BM, Coppel RL. 98.  et al. 2000. Targeted mutagenesis of Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) disrupts cytoadherence of malaria-infected red blood cells. EMBO J. 19:2813–23 [Google Scholar]
  99. Cooke BM, Buckingham DW, Glenister FK, Fernandez KM, Bannister LH. 99.  et al. 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 [Google Scholar]
  100. Glenister FK, Fernandez KM, Kats LM, Hanssen E, Mohandas N. 100.  et al. 2009. Functional alteration of red blood cells by a megadalton protein of Plasmodium falciparum. Blood 113:919–28 [Google Scholar]
  101. Rug M, Cyrklaff M, Mikkonen A, Lemgruber L, Külzer S. 101.  et al. 2014. Export of virulence proteins by malaria-infected erythrocytes involves remodeling of host actin cytoskeleton. Blood 124:3459–68 [Google Scholar]
  102. Lopes SC, Albrecht L, Carvalho BO, Siqueira AM, Thomson-Luque R. 102.  et al. 2014. Paucity of Plasmodium vivax mature schizonts in peripheral blood is associated with their increased cytoadhesive potential. J. Infect. Dis. 209:1403–7 [Google Scholar]
  103. Costa FT, Lopes SC, Ferrer M, Leite JA, Martin-Jaular L. 103.  et al. 2011. On cytoadhesion of Plasmodium vivax: raison d'être? Mem. Inst. Oswaldo Cruz 106:Suppl. 179–84 [Google Scholar]
  104. Kaul DK, Roth EF Jr, Nagel RL, Howard RJ, Handunnetti SM. 104.  1991. Rosetting of Plasmodium falciparum–infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 78:812–19 [Google Scholar]
  105. Niang M, Bei AK, Madnani KG, Pelly S, Dankwa S. 105.  et al. 2014. STEVOR is a Plasmodium falciparum erythrocyte binding protein that mediates merozoite invasion and rosetting. Cell Host Microbe 16:81–93 [Google Scholar]
  106. Cheng Q, Cloonan N, Fischer K, Thompson J, Waine G. 106.  et al. 1998. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol. Biochem. Parasitol. 97:161–76 [Google Scholar]
  107. Fernandez V, Hommel M, Chen Q, Hagblom P, Wahlgren M. 107.  1999. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum–infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. J. Exp. Med. 190:1393–404 [Google Scholar]
  108. Joannin N, Abhiman S, Sonnhammer EL, Wahlgren M. 108.  2008. Sub-grouping and sub-functionalization of the RIFIN multi-copy protein family. BMC Genomics 9:19 [Google Scholar]
  109. Kyes SA, Rowe JA, Kriek N, Newbold CI. 109.  1999. Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. PNAS 96:9333–38 [Google Scholar]
  110. Mphande FA, Ribacke U, Kaneko O, Kironde F, Winter G, Wahlgren M. 110.  2008. SURFIN4.1, a schizont-merozoite associated protein in the SURFIN family of Plasmodium falciparum. Malar. J. 7:116 [Google Scholar]
  111. Winter G, Kawai S, Haeggstrom M, Kaneko O, von Euler A. 111.  et al. 2005. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J. Exp. Med. 201:1853–63 [Google Scholar]
  112. Sam-Yellowe TY, Florens L, Johnson JR, Wang T, Drazba JA. 112.  et al. 2004. A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling. Genome Res. 14:1052–59 [Google Scholar]
  113. Chan JA, Fowkes FJ, Beeson JG. 113.  2014. Surface antigens of Plasmodium falciparum–infected erythrocytes as immune targets and malaria vaccine candidates. Cell Mol. Life Sci. 73:3633–57 [Google Scholar]
  114. Anong WA, Franco T, Chu H, Weis TL, Devlin EE. 114.  et al. 2009. Adducin forms a bridge between the erythrocyte membrane and its cytoskeleton and regulates membrane cohesion. Blood 114:1904–12 [Google Scholar]
  115. Salomao M, Zhang X, Yang Y, Lee S, Hartwig JH. 115.  et al. 2008. Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. PNAS 105:8026–31 [Google Scholar]
  116. Oh SS, Voigt S, Fisher D, Yi SJ, LeRoy PJ. 116.  et al. 2000. Plasmodium falciparum erythrocyte membrane protein 1 is anchored to the actin-spectrin junction and knob-associated histidine-rich protein in the erythrocyte skeleton. Mol. Biochem. Parasitol. 108:237–47 [Google Scholar]
  117. Pei X, An X, Guo X, Tarnawski M, Coppel R, Mohandas N. 117.  2005. Structural and functional studies of interaction between Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and erythrocyte spectrin. J. Biol. Chem. 280:31166–71 [Google Scholar]
  118. Weng H, Guo X, Papoin J, Wang J, Coppel R. 118.  et al. 2014. Interaction of Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) with erythrocyte ankyrin R is required for its attachment to the erythrocyte membrane. Biochim. Biophys. Acta 1838:185–92 [Google Scholar]
  119. Magowan C, Nunomura W, Waller KL, Yeung J, Liang J. 119.  et al. 2000. Plasmodium falciparum histidine-rich protein 1 associates with the Band 3 binding domain of ankyrin in the infected red cell membrane. Biochim. Biophys. Acta 1502:461–70 [Google Scholar]
  120. Parish LA, Mai DW, Jones ML, Kitson EL, Rayner JC. 120.  2013. A member of the Plasmodium falciparum PHIST family binds to the erythrocyte cytoskeleton component Band 4.1. Malar. J. 12:160 [Google Scholar]
  121. Chishti AH, Maalouf GJ, Marfatia S, Palek J, Wang W. 121.  et al. 1994. Phosphorylation of protein 4.1 in Plasmodium falciparum–infected human red blood cells. Blood 83:3339–45 [Google Scholar]
  122. Pei X, Guo X, Coppel R, Mohandas N, An X. 122.  2007. Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) destabilizes erythrocyte membrane skeleton. J. Biol. Chem. 282:26754–58 [Google Scholar]
  123. Baines AJ, Lu HC, Bennett PM. 123.  2014. The Protein 4.1 family: hub proteins in animals for organizing membrane proteins. Biochim. Biophys. Acta 1838:605–19 [Google Scholar]
  124. Pei X, Guo X, Coppel R, Bhattacharjee S, Haldar K. 124.  et al. 2007. The ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Blood 110:1036–42 [Google Scholar]
  125. Riglar DT, Richard D, Wilson DW, Boyle MJ, Dekiwadia C. 125.  et al. 2011. Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe 9:9–20 [Google Scholar]
  126. Brandt GS, Bailey S. 126.  2013. Dematin, a human erythrocyte cytoskeletal protein, is a substrate for a recombinant FIKK kinase from Plasmodium falciparum. Mol. Biochem. Parasitol. 191:20–23 [Google Scholar]
  127. Kirk K. 127.  2001. Membrane transport in the malaria-infected erythrocyte. Physiol. Rev. 81:495–537 [Google Scholar]
  128. Desai SA. 128.  2014. Why do malaria parasites increase host erythrocyte permeability?. Trends Parasitol. 30:151–59 [Google Scholar]
  129. Desai SA, Bezrukov SM, Zimmerberg J. 129.  2000. A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite. Nature 406:1001–5 [Google Scholar]
  130. Egee S, Lapaix F, Decherf G, Staines HM, Ellory JC. 130.  et al. 2002. A stretch-activated anion channel is up-regulated by the malaria parasite Plasmodium falciparum. J. Physiol. 542:795–801 [Google Scholar]
  131. Huber SM, Uhlemann AC, Gamper NL, Duranton C, Kremsner PG, Lang F. 131.  2002. Plasmodium falciparum activates endogenous Cl channels of human erythrocytes by membrane oxidation. EMBO J. 21:22–30 [Google Scholar]
  132. Huber SM, Duranton C, Henke G, Van De Sand C, Heussler V. 132.  et al. 2004. Plasmodium induces swelling-activated ClC-2 anion channels in the host erythrocyte. J. Biol. Chem. 279:41444–52 [Google Scholar]
  133. Verloo P, Kocken CH, Van der Wel A, Tilly BC, Hogema BM. 133.  et al. 2004. Plasmodium falciparum–activated chloride channels are defective in erythrocytes from cystic fibrosis patients. J. Biol. Chem. 279:10316–22 [Google Scholar]
  134. Bouyer G, Cueff A, Egee S, Kmiecik J, Maksimova Y. 134.  et al. 2011. Erythrocyte peripheral type benzodiazepine receptor/voltage-dependent anion channels are upregulated by Plasmodium falciparum. Blood 118:2305–12 [Google Scholar]
  135. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, Arbel N. 135.  2010. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol. Aspects Med. 31:227–85 [Google Scholar]
  136. Alkhalil A, Cohn JV, Wagner MA, Cabrera JS, Rajapandi T, Desai SA. 136.  2004. Plasmodium falciparum likely encodes the principal anion channel on infected human erythrocytes. Blood 104:4279–86 [Google Scholar]
  137. Alkhalil A, Pillai AD, Bokhari AA, Vaidya AB, Desai SA. 137.  2009. Complex inheritance of the plasmodial surface anion channel in a Plasmodium falciparum genetic cross. Mol. Microbiol. 72:459–69 [Google Scholar]
  138. Baumeister S, Winterberg M, Duranton C, Huber SM, Lang F. 138.  et al. 2006. Evidence for the involvement of Plasmodium falciparum proteins in the formation of new permeability pathways in the erythrocyte membrane. Mol. Microbiol. 60:493–504 [Google Scholar]
  139. Mitamura T, Hanada K, Ko-Mitamura EP, Nishijima M, Horii T. 139.  2000. Serum factors governing intraerythrocytic development and cell cycle progression of Plasmodium falciparum. Parasitol. Int. 49:219–29 [Google Scholar]
  140. Hsiao LL, Howard RJ, Aikawa M, Taraschi TF. 140.  1991. Modification of host cell membrane lipid composition by the intra-erythrocytic human malaria parasite Plasmodium falciparum. Biochem. J. 274:121–32 [Google Scholar]
  141. Tokumasu F, Crivat G, Ackerman H, Hwang J, Wellems TE. 141.  2014. Inward cholesterol gradient of the membrane system in P. falciparum–infected erythrocytes involves a dilution effect from parasite-produced lipids. Biol. Open 3:529–41 [Google Scholar]
  142. van Ooij C, Withers-Martinez C, Ringel A, Cockcroft S, Haldar K, Blackman MJ. 142.  2013. Identification of a Plasmodium falciparum phospholipid transfer protein. J. Biol. Chem. 288:31971–83 [Google Scholar]
  143. Iqbal J, Siddique A, Jameel M, Hira PR. 143.  2004. Persistent histidine-rich protein 2, parasite lactate dehydrogenase, and panmalarial antigen reactivity after clearance of Plasmodium falciparum monoinfection. J. Clin. Microbiol. 42:4237–41 [Google Scholar]
  144. Papalexis V, Siomos MA, Campanale N, Guo X, Kocak G. 144.  et al. 2001. Histidine-rich protein 2 of the malaria parasite, Plasmodium falciparum, is involved in detoxification of the by-products of haemoglobin degradation. Mol. Biochem. Parasitol. 115:77–86 [Google Scholar]
  145. Sullivan DJ Jr., Gluzman IY, Goldberg DE. 145.  1996. Plasmodium hemozoin formation mediated by histidine-rich proteins. Science 271:219–22 [Google Scholar]
  146. Ndonwi M, Burlingame OO, Miller AS, Tollefsen DM, Broze GJ Jr., Goldberg DE. 146.  2011. Inhibition of antithrombin by Plasmodium falciparum histidine-rich protein II. Blood 117:6347–54 [Google Scholar]
  147. Parra ME, Evans CB, Taylor DW. 147.  1991. Identification of Plasmodium falciparum histidine-rich protein 2 in the plasma of humans with malaria. J. Clin. Microbiol. 29:1629–34 [Google Scholar]
  148. Buffet PA, Safeukui I, Deplaine G, Brousse V, Prendki V. 148.  et al. 2011. The pathogenesis of Plasmodium falciparum malaria in humans: insights from splenic physiology. Blood 117:381–92 [Google Scholar]
  149. Schnitzer B, Sodeman T, Mead ML, Contacos PG. 149.  1972. Pitting function of the spleen in malaria: ultrastructural observations. Science 177:175–77 [Google Scholar]
  150. Chotivanich K, Udomsangpetch R, Dondorp A, Williams T, Angus B. 150.  et al. 2000. The mechanisms of parasite clearance after antimalarial treatment of Plasmodium falciparum malaria. J. Infect. Dis. 182:629–33 [Google Scholar]
  151. Anyona SB, Schrier SL, Gichuki CW, Waitumbi JN. 151.  2006. Pitting of malaria parasites and spherocyte formation. Malar. J. 5:64 [Google Scholar]
  152. Regev-Rudzki N, Wilson DW, Carvalho TG, Sisquella X, Coleman BM. 152.  et al. 2013. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 153:1120–33 [Google Scholar]
  153. Mantel PY, Hoang AN, Goldowitz I, Potashnikova D, Hamza B. 153.  et al. 2013. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe 13:521–34 [Google Scholar]
  154. Ponce da Motta L, Araújo da Costa M, Barreto Gouvea M, Saraiva Tibúrcio A, João Filho EC. 154.  et al. 2011. Postmalaria neurological syndrome: a case report. Rev. Soc. Bras. Med. Trop. 44:787–88 [Google Scholar]
  155. van der Wal G, Verhagen WI, Dofferhoff AS. 155.  2005. Neurological complications following Plasmodium falciparum infection. Neth. J. Med. 63:180–83 [Google Scholar]
  156. Ingmundson A, Alano P, Matuschewski K, Silvestrini F. 156.  2014. Feeling at home from arrival to departure: protein export and host cell remodelling during Plasmodium liver stage and gametocyte maturation. Cell Microbiol. 16:324–33 [Google Scholar]
  157. Singh AP, Buscaglia CA, Wang Q, Levay A, Nussenzweig DR. 157.  et al. 2007. Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 131:492–504 [Google Scholar]
  158. Tibúrcio M, Silvestrini F, Bertuccini L, Sander AF, Turner L. 158.  et al. 2013. Early gametocytes of the malaria parasite Plasmodium falciparum specifically remodel the adhesive properties of infected erythrocyte surface. Cell Microbiol. 15:647–59 [Google Scholar]
  159. Aingaran M, Zhang R, Law SK, Peng Z, Undisz A. 159.  et al. 2012. Host cell deformability is linked to transmission in the human malaria parasite Plasmodium falciparum. Cell Microbiol. 14:983–93 [Google Scholar]
  160. Taylor S, Barragan A, Su C, Fux B, Fentress SJ. 160.  et al. 2006. A secreted serine/threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314:1776–80 [Google Scholar]
  161. Saeij JP, Boyle JP, Coller S, Taylor S, Sibley LD. 161.  et al. 2006. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314:1780–83 [Google Scholar]
  162. Saeij JP, Coller S, Boyle JP, Jerome ME, White MW, Boothroyd JC. 162.  2007. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445:324–27 [Google Scholar]
  163. Reese ML, Zeiner GM, Saeij JP, Boothroyd JC, Boyle JP. 163.  2011. Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence. PNAS 108:9625–30 [Google Scholar]
  164. Behnke MS, Khan A, Wootton JC, Dubey JP, Tang K, Sibley LD. 164.  2011. Virulence differences in Toxoplasma mediated by amplification of a family of polymorphic pseudokinases. PNAS 108:9631–36 [Google Scholar]
  165. Counihan NA, Kalanon M, Coppel RL, de Koning–Ward TF. 165.  2013. Plasmodium rhoptry proteins: why order is important. Trends Parasitol. 29:228–36 [Google Scholar]
  166. Alaganan A, Fentress SJ, Tang K, Wang Q, Sibley LD. 166.  2014. Toxoplasma GRA7 effector increases turnover of immunity-related GTPases and contributes to acute virulence in the mouse. PNAS 111:1126–31 [Google Scholar]
  167. Pernas L, Adomako-Ankomah Y, Shastri AJ, Ewald SE, Treeck M. 167.  et al. 2014. Toxoplasma effector MAF1 mediates recruitment of host mitochondria and impacts the host response. PLOS Biol. 12:e1001845 [Google Scholar]
  168. Bougdour A, Tardieux I, Hakimi MA. 168.  2014. Toxoplasma exports dense granule proteins beyond the vacuole to the host cell nucleus and rewires the host genome expression. Cell Microbiol. 16:334–43 [Google Scholar]
  169. Rosowski EE, Lu D, Julien L, Rodda L, Gaiser RA. 169.  et al. 2011. Strain-specific activation of the NF-κB pathway by GRA15, a novel Toxoplasma gondii dense granule protein. J. Exp. Med. 208:195–212 [Google Scholar]
  170. Bougdour A, Durandau E, Brenier-Pinchart MP, Ortet P, Barakat M. 170.  et al. 2013. Host cell subversion by Toxoplasma GRA16, an exported dense granule protein that targets the host cell nucleus and alters gene expression. Cell Host Microbe 13:489–500 [Google Scholar]
  171. Braun L, Brenier-Pinchart MP, Yogavel M, Curt-Varesano A, Curt-Bertini RL. 171.  et al. 2013. A Toxoplasma dense granule protein, GRA24, modulates the early immune response to infection by promoting a direct and sustained host p38 MAPK activation. J. Exp. Med. 210:2071–86 [Google Scholar]
  172. Hsiao CH, Hiller NL, Haldar K, Knoll LJ. 172.  2013. A HT/PEXEL motif in Toxoplasma dense granule proteins is a signal for protein cleavage but not export into the host cell. Traffic 14:519–31 [Google Scholar]
  173. Shea M, Jakle U, Liu Q, Berry C, Joiner KA, Soldati-Favre D. 173.  2007. A family of aspartic proteases and a novel, dynamic and cell-cycle-dependent protease localization in the secretory pathway of Toxoplasma gondii. Traffic 8:1018–34 [Google Scholar]
  174. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP. 174.  et al. 2009. Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med. 361:455–67 [Google Scholar]
  175. Staines HM, Ellory JC, Chibale K. 175.  2005. The new permeability pathways: targets and selective routes for the development of new antimalarial agents. Comb. Chem. High Throughput Screen. 8:81–88 [Google Scholar]
  176. Pillai AD, Pain M, Solomon T, Bokhari AA, Desai SA. 176.  2010. A cell-based high-throughput screen validates the plasmodial surface anion channel as an antimalarial target. Mol. Pharmacol. 77:724–33 [Google Scholar]
  177. Kirk K, Horner HA, Elford BC, Ellory JC, Newbold CI. 177.  1994. Transport of diverse substrates into malaria-infected erythrocytes via a pathway showing functional characteristics of a chloride channel. J. Biol. Chem. 269:3339–47 [Google Scholar]
  178. Kirk K, Horner HA, Spillett DJ, Elford BC. 178.  1993. Glibenclamide and meglitinide block the transport of low molecular weight solutes into malaria-infected erythrocytes. FEBS Lett. 323:123–28 [Google Scholar]
  179. Kutner S, Breuer WV, Ginsburg H, Cabantchik ZI. 179.  1987. On the mode of action of phlorizin as an antimalarial agent in in vitro cultures of Plasmodium falciparum. Biochem. Pharmacol. 36:123–29 [Google Scholar]
  180. Kirk K, Horner HA. 180.  1995. In search of a selective inhibitor of the induced transport of small solutes in Plasmodium falciparum–infected erythrocytes: effects of arylaminobenzoates. Biochem. J. 311:761–68 [Google Scholar]
  181. Staines HM, Dee BC, O'Brien M, Lang HJ, Englert H. 181.  et al. 2004. Furosemide analogues as potent inhibitors of the new permeability pathways of Plasmodium falciparum–infected human erythrocytes. Mol. Biochem. Parasitol. 133:315–18 [Google Scholar]
  182. Staines HM, Rae C, Kirk K. 182.  2000. Increased permeability of the malaria-infected erythrocyte to organic cations. Biochim. Biophys. Acta 1463:88–98 [Google Scholar]
  183. Baumeister S, Endermann T, Charpian S, Nyalwidhe J, Duranton C. 183.  et al. 2003. A biotin derivative blocks parasite induced novel permeation pathways in Plasmodium falciparum–infected erythrocytes. Mol. Biochem. Parasitol. 132:35–45 [Google Scholar]
  184. Lisk G, Kang M, Cohn JV, Desai SA. 184.  2006. Specific inhibition of the plasmodial surface anion channel by dantrolene. Eukaryot. Cell 5:1882–93 [Google Scholar]
  185. Sisodia BS, Negi AS, Darokar MP, Dwivedi UN, Khanuja SP. 185.  2012. Antiplasmodial activity of steroidal chalcones: evaluation of their effect on hemozoin synthesis and the new permeation pathway of Plasmodium falciparum–infected erythrocyte membrane. Chem. Biol. Drug Des. 79:610–15 [Google Scholar]
  186. Go ML, Liu M, Wilairat P, Rosenthal PJ, Saliba KJ, Kirk K. 186.  2004. Antiplasmodial chalcones inhibit sorbitol-induced hemolysis of Plasmodium falciparum–infected erythrocytes. Antimicrob. Agents Chemother. 48:3241–45 [Google Scholar]
  187. Nguitragool W, Rayavara K, Desai SA. 187.  2014. Proteolysis at a specific extracellular residue implicates integral membrane CLAG3 in malaria parasite nutrient channels. PLOS ONE 9:e93759 [Google Scholar]
  188. Baumeister S, Wiesner J, Reichenberg A, Hintz M, Bietz S. 188.  et al. 2011. Fosmidomycin uptake into Plasmodium- and Babesia-infected erythrocytes is facilitated by parasite-induced new permeability pathways. PLOS ONE 6:e19334 [Google Scholar]
  189. Gero AM, Dunn CG, Brown DM, Pulenthiran K, Gorovits EL. 189.  et al. 2003. New malaria chemotherapy developed by utilization of a unique parasite transport system. Curr. Pharm. Des. 9:867–77 [Google Scholar]
  190. Hanssen E, Hawthorne P, Dixon MW, Trenholme KR, McMillan PJ. 190.  et al. 2008. Targeted mutagenesis of the ring-exported protein of Plasmodium falciparum disrupts the architecture of Maurer's cleft organelles. Mol. Microbiol. 69:938–53 [Google Scholar]
  191. Spycher C, Klonis N, Spielmann T, Kump E, Steiger S. 191.  et al. 2003. MAHRP-1, a novel Plasmodium falciparum histidine-rich protein, binds ferriprotoporphyrin IX and localizes to the Maurer's clefts. J. Biol. Chem. 278:35373–83 [Google Scholar]
  192. Dietz O, Rusch S, Brand F, Mundwiler-Pachlatko E, Gaida A. 192.  et al. 2014. Characterization of the small exported Plasmodium falciparum membrane protein SEMP1. PLOS ONE 9:e103272 [Google Scholar]
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