Publikationsserver der Universitätsbibliothek Marburg

Titel:Proteintransport zum Apicoplasten von Plasmodium falciparum - Hinweise für einen Golgi-abhängigen Transportweg
Autor:Heiny, Sabrina Rita
Weitere Beteiligte: Przyborski, Jude (PD Dr.)
Veröffentlicht:2013
URI:https://archiv.ub.uni-marburg.de/diss/z2014/0469
DOI: https://doi.org/10.17192/z2014.0469
URN: urn:nbn:de:hebis:04-z2014-04691
DDC: Biowissenschaften, Biologie
Titel (trans.):Protein trafficking to the apicoplast of Plasmodium falciparum - evidence for a golgi-dependent transport system
Publikationsdatum:2014-12-03
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
protein trafficking, Plasmodium falciparum, Brefeldin A, Apicoplast, Golgi

Zusammenfassung:
Wie die meisten apicomplexen Parasiten besitzt Plasmodium falciparum eine komplexe von vier Membranen umschlossene Plastide sekundär endosymbiotischen Ursprungs, die als Apicoplast bezeichnet wird. Obwohl nicht länger photosynthetisch aktiv, ist der Apicoplast ein Zentrum metabolischer Aktivität und gilt aufgrund seiner für den Parasiten essentiellen Stoffwechselwege als vielversprechende Angriffsfläche neuer anti-Malaria Medikamente. Die meisten Apicoplast Proteine sind jedoch Zellkern-kodiert und müssen daher post-translational in die Plastide importiert werden, was die Etablierung entsprechender Signale und Transportmechanismen voraussetzt. Die Signale, welche die zunächst co-translationale Insertion von Apicoplast Proteinen ins ER und den anschließenden Transport zur Plastide vermitteln, wurden wie die molekularen Komponenten, die an der Translokation über die drei inneren Membranen beteiligt sind, in den letzten Jahren eingehend untersucht. Weitestgehend unbekannt ist, wie Apicoplast Proteine zunächst vom ER zur äußeren Apicoplasten Membran gelangen. In der gegenwärtigen Literatur wir ein Modell favorisiert bei dem Apicoplast Proteine bereits im ER erkannt und in ein spezielles vesikuläres System sortiert werden, über das sie unter Ausschluss des Golgi-Apparates auf direktem Weg vom ER zur äußeren Apicoplasten Membran transportiert werden. Diese Arbeit liefert Hinweise, dass lösliche Apicoplast Proteine über eine Passage durch den Golgi-Apparat zum Apicoplasten transportiert werden. Anhand von ER retrieval Sequenzen, welche im Golgi erkannt werden, kann der Transport eines löslichen Apicoplast-gerichteten Reporterproteins nachhaltig beeinträchtigt werden. Desweiteren wird der Transport löslicher Apicoplast-gerichteter Reporterproteine unter Einfluss von Brefeldin A, einem bekannten Inhibitor des Golgi/ER vesikulären Systems, in einer P. falciparum Wildtyp Parasitenlinie weitestgehend inhibiert, während vor dem Hintergrund einer BFA-resistenten P. falciparum Zelllinie keine Beeinträchtigung des Transports zum Apicoplasten erfolgt. Entgegen der gegenwärtigen Literatur wird ein Modell vorgeschlagen, bei dem lösliche Apicoplast Proteine nach ihrer co-translationalen Insertion ins ER zunächst entlang des sekretorischen Weges transportiert werden. Im Golgi-Apparat werden sie dann, vermutlich von einem Golgi-residenten Transitpeptid Rezeptor, erkannt und über ein vesikuläres Transportsystem zur äußeren Apicoplasten Membran sortiert und transportiert.

Bibliographie / References

  1. Seeber, F., and D. Soldati-Favre, 2010, Metabolic pathways in the apicoplast of apicomplexa: Int Rev Cell Mol Biol, v. 281, p. 161-228.
  2. Adisa, A., S. Frankland, M. Rug, K. Jackson, A. G. Maier, P. Walsh, T. Lithgow, N. Klonis, P. R. Gilson, A. F. Cowman, and L. Tilley, 2007, Re-assessing the locations of components of the classical vesicle-mediated trafficking machinery in transfected Plasmodium falciparum: Int J Parasitol, v. 37, p. 1127-41.
  3. Pachlatko, E., S. Rusch, A. Müller, A. Hemphill, L. Tilley, E. Hanssen, and H. P. Beck, 2010, MAHRP2, an exported protein of Plasmodium falciparum, is an essential component of Maurer's cleft tethers: Mol Microbiol, v. 77, p. 1136-52.
  4. Hanssen, E., P. Carlton, S. Deed, N. Klonis, J. Sedat, J. DeRisi, and L. Tilley, 2010a, Whole cell imaging reveals novel modular features of the exomembrane system of the malaria parasite, Plasmodium falciparum: Int J Parasitol, v. 40, p. 123-34.
  5. Garcia-Bustos, J. F., and F. J. Gamo, 2013, Antimalarial drug resistance and early drug discovery: Curr Pharm Des, v. 19, p. 270-81.
  6. Kirk, K., H. M. Staines, R. E. Martin, and K. J. Saliba, 1999, Transport properties of the host cell membrane: Novartis Found Symp, v. 226, p. 55-66; discussion 66-73.
  7. Harb, O. S., B. Chatterjee, M. J. Fraunholz, M. J. Crawford, M. Nishi, and D. S. Roos, 2004, Multiple functionally redundant signals mediate targeting to the apicoplast in the apicomplexan parasite Toxoplasma gondii: Eukaryot Cell, v. 3, p. 663-74.
  8. Waller, R. F., and G. I. McFadden, 2005, The apicoplast: a review of the derived plastid of apicomplexan parasites: Curr Issues Mol Biol, v. 7, p. 57-79.
  9. Toso, M. A., and C. K. Omoto, 2007, Gregarina niphandrodes may lack both a plastid genome and organelle: J Eukaryot Microbiol, v. 54, p. 66-72.
  10. Strittmatter, P., J. Soll, and B. Bölter, 2010, The chloroplast protein import machinery: a review: Methods Mol Biol, v. 619, p. 307-21.
  11. Vacula, R., S. Sláviková, and S. D. Schwartzbach, 2007, Protein trafficking to the complex chloroplasts of Euglena: Methods Mol Biol, v. 390, p. 219-37.
  12. Gould, S. B., M. S. Sommer, K. Hadfi, S. Zauner, P. G. Kroth, and U. G. Maier, 2006, Protein targeting into the complex plastid of cryptophytes: J Mol Evol, v. 62, p. 674-81.
  13. Hayton, K., and X. Z. Su, 2008, Drug resistance and genetic mapping in Plasmodium falciparum: Curr Genet, v. 54, p. 223-39.
  14. Köhler, S., 2005, Multi-membrane-bound structures of Apicomplexa: I. the architecture of the Toxoplasma gondii apicoplast: Parasitol Res, v. 96, p. 258-72.
  15. Külzer, S., N. Gehde, and J. M. Przyborski, 2009, Return to sender: use of Plasmodium ER retrieval sequences to study protein transport in the infected erythrocyte and predict putative ER protein families: Parasitol Res, v. 104, p. 1535-41.
  16. Gruber, A., S. Vugrinec, F. Hempel, S. B. Gould, U. G. Maier, and P. G. Kroth, 2007, Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif: Plant Mol Biol, v. 64, p. 519-30.
  17. Kilejian, A., 1975, Circular mitochondrial DNA from the avian malarial parasite Plasmodium lophurae: Biochim Biophys Acta, v. 390, p. 276-84.
  18. Suplick, K., R. Akella, A. Saul, and A. B. Vaidya, 1988, Molecular cloning and partial sequence of a 5.8 kilobase pair repetitive DNA from Plasmodium falciparum: Mol Biochem Parasitol, v. 30, p. 289-90.
  19. Kumar, N., G. Koski, M. Harada, M. Aikawa, and H. Zheng, 1991, Induction and localization of Plasmodium falciparum stress proteins related to the heat shock protein 70 family: Mol Biochem Parasitol, v. 48, p. 47-58.
  20. Kreis, T. E., and R. Pepperkok, 1994, Coat proteins in intracellular membrane transport: Curr Opin Cell Biol, v. 6, p. 533-7.
  21. Nassoury, N., and D. Morse, 2005, Protein targeting to the chloroplasts of photosynthetic eukaryotes: getting there is half the fun: Biochim Biophys Acta, v. 1743, p. 5-19.
  22. Andrès, C., B. Agne, and F. Kessler, 2010, The TOC complex: preprotein gateway to the chloroplast: Biochim Biophys Acta, v. 1803, p. 715-23.
  23. Pasternak, N. D., and R. Dzikowski, 2009, PfEMP1: an antigen that plays a key role in the pathogenicity and immune evasion of the malaria parasite Plasmodium falciparum: Int J Biochem Cell Biol, v. 41, p. 1463-6.
  24. Archibald, J. M., 2009, The puzzle of plastid evolution: Curr Biol, v. 19, p. R81-8.
  25. McIntosh, M. T., D. A. Elliott, and K. A. Joiner, 2005, Plasmodium falciparum: discovery of peroxidase active organelles: Exp Parasitol, v. 111, p. 133-6.
  26. Nakhasi, and S. Kumar, 2006, Protein disulfide isomerase assisted protein folding in malaria parasites: Int J Parasitol, v. 36, p. 1037-48.
  27. Oborník, M., J. Janouskovec, T. Chrudimský, and J. Lukes, 2009, Evolution of the apicoplast and its hosts: from heterotrophy to autotrophy and back again: Int J Parasitol, v. 39, p. 1-12.
  28. Nagaraj, V. A., R. Arumugam, N. R. Chandra, D. Prasad, P. N. Rangarajan, and G. Padmanaban, 2009a, Localisation of Plasmodium falciparum uroporphyrinogen III decarboxylase of the heme- biosynthetic pathway in the apicoplast and characterisation of its catalytic properties: Int J Parasitol, v. 39, p. 559-68.
  29. Kumar, B., S. Chaubey, P. Shah, A. Tanveer, M. Charan, M. I. Siddiqi, and S. Habib, 2011, Interaction between sulphur mobilisation proteins SufB and SufC: evidence for an iron-sulphur cluster biogenesis pathway in the apicoplast of Plasmodium falciparum: Int J Parasitol, v. 41, p. 991- 9.
  30. Reichel, M. P., M. Alejandra Ayanegui-Alcérreca, L. F. Gondim, and J. T. Ellis, 2013, What is the global economic impact of Neospora caninum in cattle -the billion dollar question: Int J Parasitol, v. 43, p. 133-42.
  31. Tonkin, C. J., J. A. Pearce, G. I. McFadden, and A. F. Cowman, 2006a, Protein targeting to destinations of the secretory pathway in the malaria parasite Plasmodium falciparum: Curr Opin Microbiol, v. 9, p. 381-7.
  32. Lingelbach, K., and J. M. Przyborski, 2006, The long and winding road: protein trafficking mechanisms in the Plasmodium falciparum infected erythrocyte: Mol Biochem Parasitol, v. 147, p. 1-8.
  33. Hernández-Rivas, R., A. M. Herrera-Solorio, M. Sierra-Miranda, D. M. Delgadillo, and M. Vargas, 2013, Impact of chromosome ends on the biology and virulence of Plasmodium falciparum: Mol Biochem Parasitol, v. 187, p. 121-8.
  34. Scales, S. J., M. Gomez, and T. E. Kreis, 2000, Coat proteins regulating membrane traffic: Int Rev Cytol, v. 195, p. 67-144.
  35. Kamchonwongpaisan, S., E. Samoff, and S. R. Meshnick, 1997, Identification of hemoglobin degradation products in Plasmodium falciparum: Mol Biochem Parasitol, v. 86, p. 179-86.
  36. Wilson, C., R. Venditti, L. R. Rega, A. Colanzi, G. D'Angelo, and M. A. De Matteis, 2011, The Golgi apparatus: an organelle with multiple complex functions: Biochem J, v. 433, p. 1-9.
  37. Kriek, N., L. Tilley, P. Horrocks, R. Pinches, B. C. Elford, D. J. Ferguson, K. Lingelbach, and C. I. Newbold, 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, v. 50, p. 1215-27.
  38. Majoul, I., K. Sohn, F. T. Wieland, R. Pepperkok, M. Pizza, J. Hillemann, and H. D. Söling, 1998, KDEL receptor (Erd2p)-mediated retrograde transport of the cholera toxin A subunit from the Golgi involves COPI, p23, and the COOH terminus of Erd2p: J Cell Biol, v. 143, p. 601-12.
  39. Wellems, T. E., and C. V. Plowe, 2001, Chloroquine-resistant malaria: J Infect Dis, v. 184, p. 770-6.
  40. White, 2007, Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites: J Infect Dis, v. 195, p. 927-33.
  41. Huber, S. M., A. C. Uhlemann, N. L. Gamper, C. Duranton, P. G. Kremsner, and F. Lang, 2002, Plasmodium falciparum activates endogenous Cl(-) channels of human erythrocytes by membrane oxidation: EMBO J, v. 21, p. 22-30.
  42. Felsner, G., M. S. Sommer, N. Gruenheit, F. Hempel, D. Moog, S. Zauner, W. Martin, and U. G. Maier, 2011, ERAD components in organisms with complex red plastids suggest recruitment of a preexisting protein transport pathway for the periplastid membrane: Genome Biol Evol, v. 3, p. 140-50.
  43. Woehle, C., T. Dagan, W. F. Martin, and S. B. Gould, 2011, Red and problematic green phylogenetic signals among thousands of nuclear genes from the photosynthetic and apicomplexa-related Chromera velia: Genome Biol Evol, v. 3, p. 1220-30.
  44. Hoseki, J., R. Ushioda, and K. Nagata, 2010, Mechanism and components of endoplasmic reticulum- associated degradation: J Biochem, v. 147, p. 19-25.
  45. Hummel, E., A. Osterrieder, D. G. Robinson, and C. Hawes, 2010, Inhibition of Golgi function causes plastid starch accumulation: J Exp Bot, v. 61, p. 2603-14.
  46. Ralph, S. A., B. J. Foth, N. Hall, and G. I. McFadden, 2004a, Evolutionary pressures on apicoplast transit peptides: Mol Biol Evol, v. 21, p. 2183-94.
  47. Hempel, F., L. Bullmann, J. Lau, S. Zauner, and U. G. Maier, 2009, ERAD-derived preprotein transport across the second outermost plastid membrane of diatoms: Mol Biol Evol, v. 26, p. 1781-90.
  48. Tonkin, C. J., N. S. Struck, K. A. Mullin, L. M. Stimmler, and G. I. McFadden, 2006b, Evidence for Golgi- independent transport from the early secretory pathway to the plastid in malaria parasites: Mol Microbiol, v. 61, p. 614-30.
  49. Külzer, S., M. Rug, K. Brinkmann, P. Cannon, A. Cowman, K. Lingelbach, G. L. Blatch, A. G. Maier, and J. M. Przyborski, 2010, Parasite-encoded Hsp40 proteins define novel mobile structures in the cytosol of the P. falciparum-infected erythrocyte: Cell Microbiol, v. 12, p. 1398-420.
  50. Wallace, 1980, A newly revised classification of the protozoa: J Protozool, v. 27, p. 37-58.
  51. Gallagher, J. R., K. A. Matthews, and S. T. Prigge, 2011, Plasmodium falciparum apicoplast transit peptides are unstructured in vitro and during apicoplast import: Traffic, v. 12, p. 1124-38.
  52. Rosario, V., 1981, Cloning of naturally occurring mixed infections of malaria parasites: Science, v. 212, p. 1037-8.
  53. Kalanon, M., C. J. Tonkin, and G. I. McFadden, 2009, Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum: Eukaryot Cell, v. 8, p. 1146-54.
  54. Dancourt, J., and C. Barlowe, 2010, Protein sorting receptors in the early secretory pathway: Annu Rev Biochem, v. 79, p. 777-802.
  55. Gillingham, A. K., and S. Munro, 2007, The small G proteins of the Arf family and their regulators: Annu Rev Cell Dev Biol, v. 23, p. 579-611.
  56. Vaidya, A. B., and M. W. Mather, 2009, Mitochondrial evolution and functions in malaria parasites: Annu Rev Microbiol, v. 63, p. 249-67.
  57. Winterberg, M., E. Rajendran, S. Baumeister, S. Bietz, K. Kirk, and K. Lingelbach, 2012, Chemical activation of a high-affinity glutamate transporter in human erythrocytes and its implications for malaria-parasite-induced glutamate uptake: Blood, v. 119, p. 3604-12.
  58. Nassoury, N., M. Cappadocia, and D. Morse, 2003, Plastid ultrastructure defines the protein import pathway in dinoflagellates: J Cell Sci, v. 116, p. 2867-74.
  59. Struck, N. S., S. Herrmann, C. Langer, A. Krueger, B. J. Foth, K. Engelberg, A. L. Cabrera, S. Haase, M. Treeck, M. Marti, A. F. Cowman, T. Spielmann, and T. W. Gilberger, 2008a, Plasmodium falciparum possesses two GRASP proteins that are differentially targeted to the Golgi complex via a higher-and lower-eukaryote-like mechanism: J Cell Sci, v. 121, p. 2123-9.
  60. Sláviková, S., R. Vacula, Z. Fang, T. Ehara, T. Osafune, and S. D. Schwartzbach, 2005, Homologous and heterologous reconstitution of Golgi to chloroplast transport and protein import into the complex chloroplasts of Euglena: J Cell Sci, v. 118, p. 1651-61.
  61. Horrocks, P., R. A. Pinches, S. J. Chakravorty, J. Papakrivos, Z. Christodoulou, S. A. Kyes, B. C. Urban, D. J. Ferguson, and C. I. Newbold, 2005, PfEMP1 expression is reduced on the surface of knobless Plasmodium falciparum infected erythrocytes: J Cell Sci, v. 118, p. 2507-18.
  62. Struck, N. S., S. de Souza Dias, C. Langer, M. Marti, J. A. Pearce, A. F. Cowman, and T. W. Gilberger, 2005, Re-defining the Golgi complex in Plasmodium falciparum using the novel Golgi marker PfGRASP: J Cell Sci, v. 118, p. 5603-13. 112
  63. Abu Bakar, N., N. Klonis, E. Hanssen, C. Chan, and L. Tilley, 2010, Digestive-vacuole genesis and endocytic processes in the early intraerythrocytic stages of Plasmodium falciparum: J Cell Sci, v. 123, p. 441-50.
  64. Goodman, C. D., and G. I. McFadden, 2012, Targeting apicoplasts in malaria parasites: Expert Opin Ther Targets.
  65. Staines, H. M., J. C. Ellory, and K. Chibale, 2005, The new permeability pathways: targets and selective routes for the development of new antimalarial agents: Comb Chem High Throughput Screen, v. 8, p. 81-8.
  66. Saadatnia, G., and M. Golkar, 2012, A review on human toxoplasmosis: Scand J Infect Dis, v. 44, p. 805-14.
  67. Stork, S., D. Moog, J. M. Przyborski, I. Wilhelmi, S. Zauner, and U. G. Maier, 2012, Distribution of the SELMA translocon in secondary plastids of red algal origin and predicted uncoupling of ubiquitin-dependent translocation from degradation: Eukaryot Cell, v. 11, p. 1472-81.
  68. Wickham, M. E., M. Rug, S. A. Ralph, N. Klonis, G. I. McFadden, L. Tilley, and A. F. Cowman, 2001, Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes: EMBO J, v. 20, p. 5636-49.
  69. Przyborski, J. M., S. K. Miller, J. M. Pfahler, P. P. Henrich, P. Rohrbach, B. S. Crabb, and M. Lanzer, 2005, Trafficking of STEVOR to the Maurer's clefts in Plasmodium falciparum-infected erythrocytes: EMBO J, v. 24, p. 2306-17.
  70. Williamson, D. H., R. J. Wilson, P. A. Bates, S. McCready, F. Perler, and B. U. Qiang, 1985, Nuclear and mitochondrial DNA of the primate malarial parasite Plasmodium knowlesi: Mol Biochem Parasitol, v. 14, p. 199-209.
  71. McFadden, G. I., 2000, Mergers and acquisitions: malaria and the great chloroplast heist: Genome Biol, v. 1, p. REVIEWS1026.
  72. Mozley-Standridge, T. A. Nerad, C. A. Shearer, A. V. Smirnov, F. W. Spiegel, and M. F. Taylor, 2005, The new higher level classification of eukaryotes with emphasis on the taxonomy of protists: J Eukaryot Microbiol, v. 52, p. 399-451.
  73. Struck, N. S., S. Herrmann, I. Schmuck-Barkmann, S. de Souza Dias, S. Haase, A. L. Cabrera, M. Treeck, C. Bruns, C. Langer, A. F. Cowman, M. Marti, T. Spielmann, and T. W. Gilberger, 2008b, Spatial dissection of the cis-and trans-Golgi compartments in the malaria parasite Plasmodium falciparum: Mol Microbiol, v. 67, p. 1320-30.
  74. Tonkin, C. J., G. G. van Dooren, T. P. Spurck, N. S. Struck, R. T. Good, E. Handman, A. F. Cowman, and G. I. McFadden, 2004, Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method: Mol Biochem Parasitol, v. 137, p. 13-21.
  75. van Dooren, G. G., V. Su, M. C. D'Ombrain, and G. I. McFadden, 2002, Processing of an apicoplast leader sequence in Plasmodium falciparum and the identification of a putative leader cleavage enzyme: J Biol Chem, v. 277, p. 23612-9.
  76. Glaser, S., G. G. van Dooren, S. Agrawal, C. F. Brooks, G. I. McFadden, B. Striepen, and M. K. Higgins, 2012, Tic22 is an essential chaperone required for protein import into the apicoplast: J Biol Chem, v. 287, p. 39505-12.
  77. Hanssen, E., C. Dekiwadia, D. T. Riglar, M. Rug, L. Lemgruber, A. F. Cowman, M. Cyrklaff, M. Kudryashev, F. Frischknecht, J. Baum, and S. A. Ralph, 2013, Electron tomography of Plasmodium falciparum merozoites reveals core cellular events that underpin erythrocyte invasion: Cell Microbiol.
  78. Agrawal, S., G. G. van Dooren, W. L. Beatty, and B. Striepen, 2009, Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins: J Biol Chem, v. 284, p. 33683-91.
  79. Aikawa, M., P. K. Hepler, C. G. Huff, and H. Sprinz, 1966, The feeding mechanism of avian malarial parasites: J Cell Biol, v. 28, p. 355-73.
  80. Ward, G. E., L. H. Miller, and J. A. Dvorak, 1993, The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes: J Cell Sci, v. 106 ( Pt 1), p. 237-48.
  81. Kim, E., and L. E. Graham, 2008, EEF2 analysis challenges the monophyly of Archaeplastida and Chromalveolata: PLoS One, v. 3, p. e2621.
  82. Williamson, D. H., M. J. Gardner, P. Preiser, D. J. Moore, K. Rangachari, and R. J. Wilson, 1994, The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry: Mol Gen Genet, v. 243, p. 249-52.
  83. Markus, M. B., 2011, Malaria: origin of the term "hypnozoite": J Hist Biol, v. 44, p. 781-6.
  84. Green, B. R., 2011, After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c: Photosynth Res, v. 107, p. 103-15.
  85. Maher, S. P., B. Balu, D. A. Shoue, M. E. Weissenbach, and J. H. Adams, 2008, A highly sensitive, PCR- based method for the detection of Plasmodium falciparum clones in microtiter plates: Malar J, v. 7, p. 222.
  86. Rogerson, S. J., 2010, Malaria in pregnancy and the newborn: Adv Exp Med Biol, v. 659, p. 139-52.
  87. Rowe, J. A., A. Claessens, R. A. Corrigan, and M. Arman, 2009, Adhesion of Plasmodium falciparum- infected erythrocytes to human cells: molecular mechanisms and therapeutic implications: Expert Rev Mol Med, v. 11, p. e16.
  88. Lauer, S. A., P. K. Rathod, N. Ghori, and K. Haldar, 1997, A membrane network for nutrient import in red cells infected with the malaria parasite: Science, v. 276, p. 1122-5.
  89. Karnataki, A., A. E. Derocher, I. Coppens, J. E. Feagin, and M. Parsons, 2007b, A membrane protease is targeted to the relict plastid of toxoplasma via an internal signal sequence: Traffic, v. 8, p. 1543-53.
  90. Spork, S., J. A. Hiss, K. Mandel, M. Sommer, T. W. Kooij, T. Chu, G. Schneider, U. G. Maier, and J. M. Przyborski, 2009, An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum: Eukaryot Cell, v. 8, p. 1134-45.
  91. Carter, 2008, A photosynthetic alveolate closely related to apicomplexan parasites: Nature, v. 451, p. 959-63.
  92. Roos, 1997, A plastid of probable green algal origin in Apicomplexan parasites: Science, v. 275, p. 1485-9.
  93. Fichera, M. E., and D. S. Roos, 1997, A plastid organelle as a drug target in apicomplexan parasites: Nature, v. 390, p. 407-9.
  94. Striepen, 2011, A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor: PLoS Pathog, v. 7, p. e1002392.
  95. Schnittger, L., A. E. Rodriguez, M. Florin-Christensen, and D. A. Morrison, 2012, Babesia: a world emerging: Infect Genet Evol, v. 12, p. 1788-809.
  96. Mouray, E., M. Moutiez, S. Girault, C. Sergheraert, I. Florent, and P. Grellier, 2007, Biochemical properties and cellular localization of Plasmodium falciparum protein disulfide isomerase: Biochimie, v. 89, p. 337-46.
  97. Sharman, P. A., N. C. Smith, M. G. Wallach, and M. Katrib, 2010, Chasing the golden egg: vaccination against poultry coccidiosis: Parasite Immunol, v. 32, p. 590-8.
  98. Schmid, S. L., 1997, Clathrin-coated vesicle formation and protein sorting: an integrated process: Annu Rev Biochem, v. 66, p. 511-48.
  99. Waller, R. F., P. J. Keeling, G. G. van Dooren, and G. I. McFadden, 2003, Comment on "A green algal apicoplast ancestor": Science, v. 301, p. 49; author reply 49. 114
  100. McNew, J. A., F. Parlati, R. Fukuda, R. J. Johnston, K. Paz, F. Paumet, T. H. Söllner, and J. E. Rothman, 2000, Compartmental specificity of cellular membrane fusion encoded in SNARE proteins: Nature, v. 407, p. 153-9.
  101. Moore, P. W. Moore, and D. H. Williamson, 1996, Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum: J Mol Biol, v. 261, p. 155-72.
  102. Margos, G., L. H. Bannister, A. R. Dluzewski, J. Hopkins, I. T. Williams, and G. H. Mitchell, 2004, Correlation of structural development and differential expression of invasion-related molecules in schizonts of Plasmodium falciparum: Parasitology, v. 129, p. 273-87.
  103. Zhu, G., M. J. Marchewka, and J. S. Keithly, 2000, Cryptosporidium parvum appears to lack a plastid genome: Microbiology, v. 146 ( Pt 2), p. 315-21.
  104. Zuegge, J., S. Ralph, M. Schmuker, G. I. McFadden, and G. Schneider, 2001, Deciphering apicoplast targeting signals--feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins: Gene, v. 280, p. 19-26.
  105. Mercier, C., K. D. Adjogble, W. Däubener, and M. F. Delauw, 2005, Dense granules: are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites?: Int J Parasitol, v. 35, p. 829-49.
  106. Palis, J., and G. B. Segel, 1998, Developmental biology of erythropoiesis: Blood Rev, v. 12, p. 106-14.
  107. van Dooren, G. G., M. Marti, C. J. Tonkin, L. M. Stimmler, A. F. Cowman, and G. I. McFadden, 2005, Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum: Mol Microbiol, v. 57, p. 405-19. van Dooren, G. G., S. B. Reiff, C. Tomova, M. Meissner, B. M. Humbel, and B. Striepen, 2009, A novel dynamin-related protein has been recruited for apicoplast fission in Toxoplasma gondii: Curr Biol, v. 19, p. 267-76.
  108. Scholtyseck, E., and G. Piekarski, 1965, [Electron microscopic studies on merozoites of Eimeria (Eimeria perforans and E. stidae) and Toxoplasma gondii. On the systematic position of T. gondii]: Z Parasitenkd, v. 26, p. 91-115.
  109. Gachohi, J., R. Skilton, F. Hansen, P. Ngumi, and P. Kitala, 2012, Epidemiology of East Coast fever (Theileria parva infection) in Kenya: past, present and the future: Parasit Vectors, v. 5, p. 194. 103
  110. Mehnert, M., T. Sommer, and E. Jarosch, 2010, ERAD ubiquitin ligases: multifunctional tools for protein quality control and waste disposal in the endoplasmic reticulum: Bioessays, v. 32, p. 905-13.
  111. Semenza, J. C., K. G. Hardwick, N. Dean, and H. R. Pelham, 1990, ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway: Cell, v. 61, p. 1349-57.
  112. Murphy, S. C., B. U. Samuel, T. Harrison, K. D. Speicher, D. W. Speicher, M. E. Reid, R. Prohaska, P. S. Low, M. J. Tanner, N. Mohandas, and K. Haldar, 2004, Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection: Blood, v. 103, p. 1920-8.
  113. Radhamony, R. N., and S. M. Theg, 2006, Evidence for an ER to Golgi to chloroplast protein transport pathway: Trends Cell Biol, v. 16, p. 385-7.
  114. Adisa, A., F. R. Albano, J. Reeder, M. Foley, and L. Tilley, 2001, Evidence for a role for a Plasmodium falciparum homologue of Sec31p in the export of proteins to the surface of malaria parasite- infected erythrocytes: J Cell Sci, v. 114, p. 3377-86.
  115. Trelka, D. P., T. G. Schneider, J. C. Reeder, and T. F. Taraschi, 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, v. 106, p. 131-45.
  116. Morrison, D. A., 2009, Evolution of the Apicomplexa: where are we now?: Trends Parasitol, v. 25, p. 375-82.
  117. Lew, V. L., T. Tiffert, and H. Ginsburg, 2003, Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum-infected red blood cells: Blood, v. 101, p. 4189-94.
  118. Walliker, D., I. A. Quakyi, T. E. Wellems, T. F. McCutchan, A. Szarfman, W. T. London, L. M. Corcoran, T. R. Burkot, and R. Carter, 1987, Genetic analysis of the human malaria parasite Plasmodium falciparum: Science, v. 236, p. 1661-6.
  119. Goldberg, D. E., 2005, Hemoglobin degradation: Curr Top Microbiol Immunol, v. 295, p. 275-91.
  120. Cox, F. E., 2010, History of the discovery of the malaria parasites and their vectors: Parasit Vectors, v. 3, p. 5.
  121. Kilian, O., and P. G. Kroth, 2005, Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids: Plant J, v. 41, p. 175-83.
  122. Elmendorf, H. G., and K. Haldar, 1993, Identification and localization of ERD2 in the malaria parasite Plasmodium falciparum: separation from sites of sphingomyelin synthesis and implications for organization of the Golgi: EMBO J, v. 12, p. 4763-73.
  123. La Greca, N., A. R. Hibbs, C. Riffkin, M. Foley, and L. Tilley, 1997, Identification of an endoplasmic reticulum-resident calcium-binding protein with multiple EF-hand motifs in asexual stages of Plasmodium falciparum: Mol Biochem Parasitol, v. 89, p. 283-93.
  124. Ayong, L., G. Pagnotti, A. B. Tobon, and D. Chakrabarti, 2007, Identification of Plasmodium falciparum family of SNAREs: Mol Biochem Parasitol, v. 152, p. 113-22.
  125. Jomaa, H., J. Wiesner, S. Sanderbrand, B. Altincicek, C. Weidemeyer, M. Hintz, I. Türbachova, M. Eberl, J. Zeidler, H. K. Lichtenthaler, D. Soldati, and E. Beck, 1999, Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs: Science, v. 285, p. 1573-6.
  126. Moog, D., S. Stork, S. Zauner, and U. G. Maier, 2011, In silico and in vivo investigations of proteins of a minimized eukaryotic cytoplasm: Genome Biol Evol, v. 3, p. 375-82.
  127. Helenius, A., and M. Aebi, 2001, Intracellular functions of N-linked glycans: Science, v. 291, p. 2364-9.
  128. Krugliak, M., J. Zhang, and H. Ginsburg, 2002, Intraerythrocytic Plasmodium falciparum utilizes only a fraction of the amino acids derived from the digestion of host cell cytosol for the biosynthesis of its proteins: Mol Biochem Parasitol, v. 119, p. 249-56.
  129. Cowman, A. F., and B. S. Crabb, 2006, Invasion of red blood cells by malaria parasites: Cell, v. 124, p. 755-66.
  130. Lewis, M. J., and H. R. Pelham, 1992, Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum: Cell, v. 68, p. 353-64.
  131. Menard, and V. T. Heussler, 2006, Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids: Science, v. 313, p. 1287-90.
  132. Tomova, C., B. M. Humbel, W. J. Geerts, R. Entzeroth, J. C. Holthuis, and A. J. Verkleij, 2009, Membrane contact sites between apicoplast and ER in Toxoplasma gondii revealed by electron tomography: Traffic, v. 10, p. 1471-80.
  133. van Dooren, G. G., L. M. Stimmler, and G. I. McFadden, 2006, Metabolic maps and functions of the Plasmodium mitochondrion: FEMS Microbiol Rev, v. 30, p. 596-630.
  134. Oborník, M., M. Vancová, D. H. Lai, J. Janouškovec, P. J. Keeling, and J. Lukeš, 2011, Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of apicomplexa, Chromera velia: Protist, v. 162, p. 115-30.
  135. Gardner, M. J., J. E. Feagin, D. J. Moore, D. F. Spencer, M. W. Gray, D. H. Williamson, and R. J. Wilson, 1991a, Organisation and expression of small subunit ribosomal RNA genes encoded by a 35- kilobase circular DNA in Plasmodium falciparum: Mol Biochem Parasitol, v. 48, p. 77-88.
  136. Aikawa, M., 1971, Parasitological review. Plasmodium: the fine structure of malarial parasites: Exp Parasitol, v. 30, p. 284-320.
  137. Wilson, D. W., M. J. Lewis, and H. R. Pelham, 1993, pH-dependent binding of KDEL to its receptor in vitro: J Biol Chem, v. 268, p. 7465-8.
  138. Tawk, L., J. F. Dubremetz, P. Montcourrier, G. Chicanne, F. Merezegue, V. Richard, B. Payrastre, M. Meissner, H. J. Vial, C. Roy, K. Wengelnik, and M. Lebrun, 2011, Phosphatidylinositol 3- monophosphate is involved in toxoplasma apicoplast biogenesis: PLoS Pathog, v. 7, p. e1001286.
  139. Gardner, M. J., N. Goldman, P. Barnett, P. W. Moore, K. Rangachari, M. Strath, A. Whyte, D. H. Williamson, and R. J. Wilson, 1994, Phylogenetic analysis of the rpoB gene from the plastid- like DNA of Plasmodium falciparum: Mol Biochem Parasitol, v. 66, p. 221-31.
  140. Cox-Singh, J., T. M. Davis, K. S. Lee, S. S. Shamsul, A. Matusop, S. Ratnam, H. A. Rahman, D. J. Conway, and B. Singh, 2008, Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening: Clin Infect Dis, v. 46, p. 165-71.
  141. Gowda, D. C., and E. A. Davidson, 1999, Protein glycosylation in the malaria parasite: Parasitol Today, v. 15, p. 147-52.
  142. Tonkin, C. J., M. Kalanon, and G. I. McFadden, 2008b, Protein targeting to the malaria parasite plastid: Traffic, v. 9, p. 166-75.
  143. Gehde, N., C. Hinrichs, I. Montilla, S. Charpian, K. Lingelbach, and J. M. Przyborski, 2009, Protein unfolding is an essential requirement for transport across the parasitophorous vacuolar membrane of Plasmodium falciparum: Mol Microbiol, v. 71, p. 613-28.
  144. Scheel, A. A., and H. R. Pelham, 1996, Purification and characterization of the human KDEL receptor: Biochemistry, v. 35, p. 10203-9.
  145. Ward, G. E., L. G. Tilney, and G. Langsley, 1997, Rab GTPases and the unusual secretory pathway of plasmodium: Parasitol Today, v. 13, p. 57-62.
  146. Lippincott-Schwartz, J., L. C. Yuan, J. S. Bonifacino, and R. D. Klausner, 1989, Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER: Cell, v. 56, p. 801-13.
  147. Smith, M. H., H. L. Ploegh, and J. S. Weissman, 2011, Road to ruin: targeting proteins for degradation in the endoplasmic reticulum: Science, v. 334, p. 1086-90.
  148. Gardner, M. J., J. E. Feagin, D. J. Moore, K. Rangachari, D. H. Williamson, and R. J. Wilson, 1993, Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum: Nucleic Acids Res, v. 21, p. 1067-71.
  149. Vaidya, A. B., R. Akella, and K. Suplick, 1989, Sequences similar to genes for two mitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6-kilobase-pair DNA of a malarial parasite: Mol Biochem Parasitol, v. 35, p. 97-107.
  150. Ellgaard, L., M. Molinari, and A. Helenius, 1999, Setting the standards: quality control in the secretory pathway: Science, v. 286, p. 1882-8.
  151. Dalbey, R. E., and G. Von Heijne, 1992, Signal peptidases in prokaryotes and eukaryotes--a new protease family: Trends Biochem Sci, v. 17, p. 474-8.
  152. von Heijne, G., 1985, Signal sequences. The limits of variation: J Mol Biol, v. 184, p. 99-105.
  153. Ricci, F., 2012, Social implications of malaria and their relationships with poverty: Mediterr J Hematol Infect Dis, v. 4, p. e2012048.
  154. Ostermann, J., L. Orci, K. Tani, M. Amherdt, M. Ravazzola, Z. Elazar, and J. E. Rothman, 1993, Stepwise assembly of functionally active transport vesicles: Cell, v. 75, p. 1015-25.
  155. Margulis, L., 1971, Symbiosis and evolution: Sci Am, v. 225, p. 48-57.
  156. Crabb, B. S., B. M. Cooke, J. C. Reeder, R. F. Waller, S. R. Caruana, K. M. Davern, M. E. Wickham, G. V. Brown, R. L. Coppel, and A. F. Cowman, 1997, Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress: Cell, v. 89, p. 287-96.
  157. Kirk, K., and K. J. Saliba, 2007, Targeting nutrient uptake mechanisms in Plasmodium: Curr Drug Targets, v. 8, p. 75-88.
  158. McFadden, G. I., 2011, The apicoplast: Protoplasma, v. 248, p. 641-50.
  159. Lim, L., and G. I. McFadden, 2010, The evolution, metabolism and functions of the apicoplast: Philos Trans R Soc Lond B Biol Sci, v. 365, p. 749-63. Lingelbach, K., and K. A. Joiner, 1998, The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells: J Cell Sci, v. 111 ( Pt 11), p. 1467-75.
  160. Trager, W., M. A. Rudzinska, and P. C. Bradbury, 1966, The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infections in man: Bull World Health Organ, v. 35, p. 883-5.
  161. Xu, P., G. Widmer, Y. Wang, L. S. Ozaki, J. M. Alves, M. G. Serrano, D. Puiu, P. Manque, D. Akiyoshi, A. J. Mackey, W. R. Pearson, P. H. Dear, A. T. Bankier, D. L. Peterson, M. S. Abrahamsen, V. Kapur, S. Tzipori, and G. A. Buck, 2004, The genome of Cryptosporidium hominis: Nature, v. 431, p. 1107-12.
  162. Douglas, S., S. Zauner, M. Fraunholz, M. Beaton, S. Penny, L. T. Deng, X. Wu, M. Reith, T. Cavalier- Smith, and U. G. Maier, 2001, The highly reduced genome of an enslaved algal nucleus: Nature, v. 410, p. 1091-6.
  163. Ayong, L., A. Raghavan, T. G. Schneider, T. F. Taraschi, D. A. Fidock, and D. Chakrabarti, 2009, The longin domain regulates the steady-state dynamics of Sec22 in Plasmodium falciparum: Eukaryot Cell, v. 8, p. 1330-40.
  164. Ockenhouse, C. F., 1993, The molecular basis for the cytoadherence of Plasmodium falciparum- infected erythrocytes to endothelium: Semin Cell Biol, v. 4, p. 297-303.
  165. Quevillon, E., T. Spielmann, K. Brahimi, D. Chattopadhyay, E. Yeramian, and G. Langsley, 2003, The Plasmodium falciparum family of Rab GTPases: Gene, v. 306, p. 13-25.
  166. Hopkins, J., R. Fowler, S. Krishna, I. Wilson, G. Mitchell, and L. Bannister, 1999, The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis: Protist, v. 150, p. 283-95.
  167. Kitajima, A., S. Asatsuma, H. Okada, Y. Hamada, K. Kaneko, Y. Nanjo, Y. Kawagoe, K. Toyooka, K. Matsuoka, M. Takeuchi, A. Nakano, and T. Mitsui, 2009, The rice alpha-amylase glycoprotein is targeted from the Golgi apparatus through the secretory pathway to the plastids: Plant Cell, v. 21, p. 2844-58.
  168. Keenan, R. J., D. M. Freymann, R. M. Stroud, and P. Walter, 2001, The signal recognition particle: Annu Rev Biochem, v. 70, p. 755-75.
  169. Prudêncio, M., A. Rodriguez, and M. M. Mota, 2006, The silent path to thousands of merozoites: the Plasmodium liver stage: Nat Rev Microbiol, v. 4, p. 849-56.
  170. Pagola, S., P. W. Stephens, D. S. Bohle, A. D. Kosar, and S. K. Madsen, 2000, The structure of malaria pigment beta-haematin: Nature, v. 404, p. 307-10.
  171. Douzery, E. J., E. A. Snell, E. Bapteste, F. Delsuc, and H. Philippe, 2004, The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?: Proc Natl Acad Sci U S A, v. 101, p. 15386-91.
  172. 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, v. 9, p. 187-97.
  173. Sulli, C., Z. Fang, U. Muchhal, and S. D. Schwartzbach, 1999, Topology of Euglena chloroplast protein precursors within endoplasmic reticulum to Golgi to chloroplast transport vesicles: J Biol Chem, v. 274, p. 457-63.
  174. Klemba, M., W. Beatty, I. Gluzman, and D. E. Goldberg, 2004, Trafficking of plasmepsin II to the food vacuole of the malaria parasite Plasmodium falciparum: J Cell Biol, v. 164, p. 47-56. Kolakovich, K. A., I. Y. Gluzman, K. L. Duffin, and D. E. Goldberg, 1997, Generation of hemoglobin peptides in the acidic digestive vacuole of Plasmodium falciparum implicates peptide transport in amino acid production: Mol Biochem Parasitol, v. 87, p. 123-35.
  175. P. falciparum wurden mit dem ACP(I)-GFP-SDEL Konstrukt von Tonkin und Kollegen (Tonkin et al., 2006b) transfiziert und über einen Entwicklungszyklus hinweg analysiert. Die Expression des Reporterproteins erfolgt unter Kontrolle des PfHsp86 Promotors; zwischen ACP_BTS und GFP ist eine 42 bp Spacerregion eingefügt (Tonkin et al., 2006b). (R) frühes Ringstadium; (T) Trophozoitenstadium; (S) Schizontenstadium. Zu jedem Zeitpunkt wurden gleiche Zelläquivalente per SDS-Page aufgetrennt und mit anti-GFP Antikörpern immundetektiert. Anti-PfHsp70 dient als Ladekontrolle. GFP: in E.coli exprimiertes GFP. Größenstandard in kDa.
  176. Ralph, S. A., G. G. van Dooren, R. F. Waller, M. J. Crawford, M. J. Fraunholz, B. J. Foth, C. J. Tonkin, D. S. Roos, and G. I. McFadden, 2004b, Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast: Nat Rev Microbiol, v. 2, p. 203-16.
  177. Jackson, C. L., and J. E. Casanova, 2000, Turning on ARF: the Sec7 family of guanine-nucleotide- exchange factors: Trends Cell Biol, v. 10, p. 60-7.
  178. Sommer, M. S., S. B. Gould, P. Lehmann, A. Gruber, J. M. Przyborski, and U. G. Maier, 2007, Der1- mediated preprotein import into the periplastid compartment of chromalveolates?: Mol Biol Evol, v. 24, p. 918-28.
  179. Soll, J., and E. Schleiff, 2004, Protein import into chloroplasts: Nat Rev Mol Cell Biol, v. 5, p. 198-208.
  180. Tomova, C., W. J. Geerts, T. Müller-Reichert, R. Entzeroth, and B. M. Humbel, 2006, New comprehension of the apicoplast of Sarcocystis by transmission electron tomography: Biol Cell, v. 98, p. 535-45.
  181. Ellis, K. E., B. Clough, J. W. Saldanha, and R. J. Wilson, 2001, Nifs and Sufs in malaria: Mol Microbiol, v. 41, p. 973-81.
  182. Karnataki, A., A. Derocher, I. Coppens, C. Nash, J. E. Feagin, and M. Parsons, 2007a, Cell cycle- regulated vesicular trafficking of Toxoplasma APT1, a protein localized to multiple apicoplast membranes: Mol Microbiol, v. 63, p. 1653-68.
  183. Kappe, 2010, Plasmodium pyruvate dehydrogenase activity is only essential for the parasite's progression from liver infection to blood infection: Mol Microbiol, v. 75, p. 957-71.
  184. Hempel, F., G. Felsner, and U. G. Maier, 2010, New mechanistic insights into pre-protein transport across the second outermost plastid membrane of diatoms: Mol Microbiol, v. 76, p. 793-801.
  185. Keeling, P. J., 2009, Chromalveolates and the evolution of plastids by secondary endosymbiosis: J Eukaryot Microbiol, v. 56, p. 1-8.
  186. Wirth, C. C., and G. Pradel, 2012, Molecular mechanisms of host cell egress by malaria parasites: Int J Med Microbiol, v. 302, p. 172-8.
  187. Nagaraj, V. A., R. Arumugam, B. Gopalakrishnan, Y. S. Jyothsna, P. N. Rangarajan, and G. Padmanaban, 2008, Unique properties of Plasmodium falciparum porphobilinogen deaminase: J Biol Chem, v. 283, p. 437-44.
  188. Nagaraj, V. A., D. Prasad, P. N. Rangarajan, and G. Padmanaban, 2009b, Mitochondrial localization of functional ferrochelatase from Plasmodium falciparum: Mol Biochem Parasitol, v. 168, p. 109-12.
  189. Sharma, Y. D., 1991, Knobs, knob proteins and cytoadherence in falciparum malaria: Int J Biochem, v. 23, p. 775-89.
  190. Nagaraj, V. A., D. Prasad, R. Arumugam, P. N. Rangarajan, and G. Padmanaban, 2010b, Characterization of coproporphyrinogen III oxidase in Plasmodium falciparum cytosol: Parasitol Int, v. 59, p. 121-7.
  191. Nagaraj, V. A., R. Arumugam, D. Prasad, P. N. Rangarajan, and G. Padmanaban, 2010a, Protoporphyrinogen IX oxidase from Plasmodium falciparum is anaerobic and is localized to the mitochondrion: Mol Biochem Parasitol, v. 174, p. 44-52.
  192. Surolia, N., and A. Surolia, 2001, Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum: Nat Med, v. 7, p. 167-73.
  193. Mohmmed, and P. Malhotra, 2007, Food vacuole targeting and trafficking of falcipain-2, an important cysteine protease of human malaria parasite Plasmodium falciparum: Mol Biochem Parasitol, v. 156, p. 12-23. 102
  194. Fairhurst, R. M., G. M. Nayyar, J. G. Breman, R. Hallett, J. L. Vennerstrom, S. Duong, P. Ringwald, T. E. Wellems, C. V. Plowe, and A. M. Dondorp, 2012, Artemisinin-resistant malaria: research challenges, opportunities, and public health implications: Am J Trop Med Hyg, v. 87, p. 231- 41.
  195. Keeling, P. J., 2010, The endosymbiotic origin, diversification and fate of plastids: Philos Trans R Soc Lond B Biol Sci, v. 365, p. 729-48.
  196. Sullivan, D. J., I. Y. Gluzman, and D. E. Goldberg, 1996, Plasmodium hemozoin formation mediated by histidine-rich proteins: Science, v. 271, p. 219-22.
  197. Moustafa, A., B. Beszteri, U. G. Maier, C. Bowler, K. Valentin, and D. Bhattacharya, 2009, Genomic footprints of a cryptic plastid endosymbiosis in diatoms: Science, v. 324, p. 1724-6.
  198. Gilson, and J. M. Przyborski, 2012, Plasmodium falciparum-encoded exported hsp70/hsp40 chaperone/co-chaperone complexes within the host erythrocyte: Cell Microbiol, v. 14, p. 1784-95.
  199. Sagan, L., 1967, On the origin of mitosing cells: J Theor Biol, v. 14, p. 255-74.
  200. Keeling, P. J., 2013, The Number, Speed, and Impact of Plastid Endosymbioses in Eukaryotic Evolution: Annu Rev Plant Biol.
  201. Johnson, A. E., and M. A. van Waes, 1999, The translocon: a dynamic gateway at the ER membrane: Annu Rev Cell Dev Biol, v. 15, p. 799-842.
  202. Francis, S. E., D. J. Sullivan, and D. E. Goldberg, 1997, Hemoglobin metabolism in the malaria parasite Plasmodium falciparum: Annu Rev Microbiol, v. 51, p. 97-123.
  203. Mereschkowski, K. S., 1905, Über Natur und Ursprung der Chromatophoren im Pflanzenreiche, Biol. Centralbibl, p. 593-604; 689-691.
  204. Pasvol, G., R. J. Wilson, M. E. Smalley, and J. Brown, 1978, Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood: Ann Trop Med Parasitol, v. 72, p. 87-8.
  205. Hempel, F., A. Bozarth, M. S. Sommer, S. Zauner, J. M. Przyborski, and U. G. Maier, 2007, Transport of nuclear-encoded proteins into secondarily evolved plastids: Biol Chem, v. 388, p. 899-906.
  206. Perkins, S. L., and C. C. Austin, 2009, Four new species of Plasmodium from New Guinea lizards: integrating morphology and molecules: J Parasitol, v. 95, p. 424-33.
  207. Lambros, C., and J. P. Vanderberg, 1979, Synchronization of Plasmodium falciparum erythrocytic stages in culture: J Parasitol, v. 65, p. 418-20.
  208. Lemgruber, L., M. Kudryashev, C. Dekiwadia, D. T. Riglar, J. Baum, H. Stahlberg, S. A. Ralph, and F. Frischknecht, 2013, Cryo-electron tomography reveals four-membrane architecture of the Plasmodium apicoplast: Malar J, v. 12, p. 25. 107
  209. Wells, T. N., P. L. Alonso, and W. E. Gutteridge, 2009, New medicines to improve control and contribute to the eradication of malaria: Nat Rev Drug Discov, v. 8, p. 879-91.
  210. Müller, I. B., and J. E. Hyde, 2010, Antimalarial drugs: modes of action and mechanisms of parasite resistance: Future Microbiol, v. 5, p. 1857-73.
  211. Sachs, J., and P. Malaney, 2002, The economic and social burden of malaria: Nature, v. 415, p. 680-5.
  212. Maier, A. G., B. M. Cooke, A. F. Cowman, and L. Tilley, 2009, Malaria parasite proteins that remodel the host erythrocyte: Nat Rev Microbiol, v. 7, p. 341-54.
  213. Ellgaard, L., and A. Helenius, 2003, Quality control in the endoplasmic reticulum: Nat Rev Mol Cell Biol, v. 4, p. 181-91.
  214. Elford, B. C., G. M. Cowan, and D. J. Ferguson, 1995, Parasite-regulated membrane transport processes and metabolic control in malaria-infected erythrocytes: Biochem J, v. 308 ( Pt 2), p. 361-74.
  215. Varadharajan, S., S. Dhanasekaran, Z. Q. Bonday, P. N. Rangarajan, and G. Padmanaban, 2002, Involvement of delta-aminolaevulinate synthase encoded by the parasite gene in de novo haem synthesis by Plasmodium falciparum: Biochem J, v. 367, p. 321-7.
  216. He, C. Y., M. K. Shaw, C. H. Pletcher, B. Striepen, L. G. Tilney, and D. S. Roos, 2001, A plastid segregation defect in the protozoan parasite Toxoplasma gondii: EMBO J, v. 20, p. 330-9.
  217. Mullin, K. A., L. Lim, S. A. Ralph, T. P. Spurck, E. Handman, and G. I. McFadden, 2006, Membrane transporters in the relict plastid of malaria parasites: Proc Natl Acad Sci U S A, v. 103, p. 9572-7.
  218. De Matteis, 2007, The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130: Mol Biol Cell, v. 18, p. 1595-608.
  219. Elmendorf, H. G., and K. Haldar, 1994, Plasmodium falciparum exports the Golgi marker sphingomyelin synthase into a tubovesicular network in the cytoplasm of mature erythrocytes: J Cell Biol, v. 124, p. 449-62.
  220. Sciaky, N., J. Presley, C. Smith, K. J. Zaal, N. Cole, J. E. Moreira, M. Terasaki, E. Siggia, and J. Lippincott- Schwartz, 1997, Golgi tubule traffic and the effects of brefeldin A visualized in living cells: J Cell Biol, v. 139, p. 1137-55.
  221. Rossner, M., and K. M. Yamada, 2004, What's in a picture? The temptation of image manipulation: J Cell Biol, v. 166, p. 11-5.
  222. Goldberg, D. E., A. F. Slater, R. Beavis, B. Chait, A. Cerami, and G. B. Henderson, 1991, Hemoglobin degradation in the human malaria pathogen Plasmodium falciparum: a catabolic pathway initiated by a specific aspartic protease: J Exp Med, v. 173, p. 961-9.
  223. Shonhai, A., A. Boshoff, and G. L. Blatch, 2007, The structural and functional diversity of Hsp70 proteins from Plasmodium falciparum: Protein Sci, v. 16, p. 1803-18.
  224. Waller, R. F., P. J. Keeling, R. G. Donald, B. Striepen, E. Handman, N. Lang-Unnasch, A. F. Cowman, G. S. Besra, D. S. Roos, and G. I. McFadden, 1998, Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum: Proc Natl Acad Sci U S A, v. 95, p. 12352-7.
  225. Cowman, A. F., S. Karcz, D. Galatis, and J. G. Culvenor, 1991, A P-glycoprotein homologue of Plasmodium falciparum is localized on the digestive vacuole: J Cell Biol, v. 113, p. 1033-42.
  226. Tonkin, C. J., B. J. Foth, S. A. Ralph, N. Struck, A. F. Cowman, and G. I. McFadden, 2008a, Evolution of malaria parasite plastid targeting sequences: Proc Natl Acad Sci U S A, v. 105, p. 4781-5.
  227. van Dooren, G. G., C. Tomova, S. Agrawal, B. M. Humbel, and B. Striepen, 2008, Toxoplasma gondii Tic20 is essential for apicoplast protein import: Proc Natl Acad Sci U S A, v. 105, p. 13574-9.
  228. Lee, M. C., P. A. Moura, E. A. Miller, and D. A. Fidock, 2008, Plasmodium falciparum Sec24 marks transitional ER that exports a model cargo via a diacidic motif: Mol Microbiol, v. 68, p. 1535- 46.
  229. Vaughan, A. M., M. T. O'Neill, A. S. Tarun, N. Camargo, T. M. Phuong, A. S. Aly, A. F. Cowman, and S. H. Kappe, 2009, Type II fatty acid synthesis is essential only for malaria parasite late liver stage development: Cell Microbiol, v. 11, p. 506-20.
  230. Grigg, M. E., and N. Sundar, 2009, Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics: Int J Parasitol, v. 39, p. 925-33.
  231. Karnataki, A., A. E. DeRocher, J. E. Feagin, and M. Parsons, 2009, Sequential processing of the Toxoplasma apicoplast membrane protein FtsH1 in topologically distinct domains during intracellular trafficking: Mol Biochem Parasitol, v. 166, p. 126-33.
  232. Richard, D., C. A. MacRaild, D. T. Riglar, J. A. Chan, M. Foley, J. Baum, S. A. Ralph, R. S. Norton, and A. F. Cowman, 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, v. 285, p. 14815-22.
  233. Janouskovec, J., A. Horák, M. Oborník, J. Lukes, and P. J. Keeling, 2010, A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids: Proc Natl Acad Sci U S A, v. 107, p. 10949-54.
  234. Eastman, R. T., and D. A. Fidock, 2009, Artemisinin-based combination therapies: a vital tool in efforts to eliminate malaria: Nat Rev Microbiol, v. 7, p. 864-74.
  235. Fidock, D. A., T. Nomura, A. K. Talley, R. A. Cooper, S. M. Dzekunov, M. T. Ferdig, L. M. Ursos, A. B. Sidhu, B. Naudé, K. W. Deitsch, X. Z. Su, J. C. Wootton, P. D. Roepe, and T. E. Wellems, 2000, Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance: Mol Cell, v. 6, p. 861-71.
  236. Waller, R. F., M. B. Reed, A. F. Cowman, and G. I. McFadden, 2000, Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway: EMBO J, v. 19, p. 1794-802.
  237. Leiby, D. A., 2011, Transfusion-transmitted Babesia spp.: bull's-eye on Babesia microti: Clin Microbiol Rev, v. 24, p. 14-28.
  238. Yeh, E., and J. L. DeRisi, 2011, Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum: PLoS Biol, v. 9, p. e1001138. 115
  239. Ponts, N., A. Saraf, D. W. Chung, A. Harris, J. Prudhomme, M. P. Washburn, L. Florens, and K. G. Le Roch, 2011, Unraveling the ubiquitome of the human malaria parasite: J Biol Chem, v. 286, p. 40320-30.
  240. Kirkman, L. A., and K. W. Deitsch, 2012, Antigenic variation and the generation of diversity in malaria parasites: Curr Opin Microbiol, v. 15, p. 456-62.
  241. Cowman, A. F., D. Berry, and J. Baum, 2012, The cellular and molecular basis for malaria parasite invasion of the human red blood cell: J Cell Biol, v. 198, p. 961-71.
  242. Adl, S. M., A. G. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, L. Le Gall, D. H. Lynn, H. McManus, E. A. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov, and F. W. Spiegel, 2012, The revised classification of eukaryotes: J Eukaryot Microbiol, v. 59, p. 429-93.
  243. Sheiner, L., and B. Striepen, 2013, Protein sorting in complex plastids: Biochim Biophys Acta, v. 1833, p. 352-9.
  244. White, 2009, Artemisinin resistance in Plasmodium falciparum malaria: N Engl J Med, v. 361, p. 455-67.
  245. Combrinck, J. M., T. E. Mabotha, K. K. Ncokazi, M. A. Ambele, D. Taylor, P. J. Smith, H. C. Hoppe, and T. J. Egan, 2013, Insights into the role of heme in the mechanism of action of antimalarials: ACS Chem Biol, v. 8, p. 133-7.
  246. Gubbels, M. J., and M. T. Duraisingh, 2012, Evolution of apicomplexan secretory organelles: Int J Parasitol, v. 42, p. 1071-81.
  247. Orci, L., M. Ravazzola, P. Meda, C. Holcomb, H. P. Moore, L. Hicke, and R. Schekman, 1991, Mammalian Sec23p homologue is restricted to the endoplasmic reticulum transitional cytoplasm: Proc Natl Acad Sci U S A, v. 88, p. 8611-5.
  248. Wilson, I., 1993, Plastids better red than dead: Nature, v. 366, p. 638.
  249. Nebenführ, A., C. Ritzenthaler, and D. G. Robinson, 2002, Brefeldin A: deciphering an enigmatic inhibitor of secretion: Plant Physiol, v. 130, p. 1102-8.
  250. Lewis, M. J., D. J. Sweet, and H. R. Pelham, 1990, The ERD2 gene determines the specificity of the luminal ER protein retention system: Cell, v. 61, p. 1359-63.
  251. Serafini, T., L. Orci, M. Amherdt, M. Brunner, R. A. Kahn, and J. E. Rothman, 1991, ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP- binding protein: Cell, v. 67, p. 239-53.
  252. Panton, and R. J. Howard, 1987, Localization of Plasmodium falciparum histidine-rich protein 1 in the erythrocyte skeleton under knobs: Mol Biochem Parasitol, v. 25, p. 165-74.
  253. Gardner, M. J., D. H. Williamson, and R. J. Wilson, 1991b, A circular DNA in malaria parasites encodes an RNA polymerase like that of prokaryotes and chloroplasts: Mol Biochem Parasitol, v. 44, p. 115-23.
  254. Pouvelle, B., J. A. Gormley, and T. F. Taraschi, 1994, Characterization of trafficking pathways and membrane genesis in malaria-infected erythrocytes: Mol Biochem Parasitol, v. 66, p. 83-96.
  255. Nilsson, T., and G. Warren, 1994, Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus: Curr Opin Cell Biol, v. 6, p. 517-21.
  256. Röhrich, R. C., N. Englert, K. Troschke, A. Reichenberg, M. Hintz, F. Seeber, E. Balconi, A. Aliverti, G. Zanetti, U. Köhler, M. Pfeiffer, E. Beck, H. Jomaa, and J. Wiesner, 2005, Reconstitution of an apicoplast-localised electron transfer pathway involved in the isoprenoid biosynthesis of Plasmodium falciparum: FEBS Lett, v. 579, p. 6433-8.
  257. Seeber, F., 2002, Biogenesis of iron-sulphur clusters in amitochondriate and apicomplexan protists: Int J Parasitol, v. 32, p. 1207-17.
  258. Lanzer, M., H. Wickert, G. Krohne, L. Vincensini, and C. Braun Breton, 2006, Maurer's clefts: a novel multi-functional organelle in the cytoplasm of Plasmodium falciparum-infected erythrocytes: Int J Parasitol, v. 36, p. 23-36.
  259. Hanssen, E., P. J. McMillan, and L. Tilley, 2010b, Cellular architecture of Plasmodium falciparum- infected erythrocytes: Int J Parasitol, v. 40, p. 1127-35.
  260. Angrisano, F., Y. H. Tan, A. Sturm, G. I. McFadden, and J. Baum, 2012, Malaria parasite colonisation of the mosquito midgut--placing the Plasmodium ookinete centre stage: Int J Parasitol, v. 42, p. 519-27.
  261. Anantharaman, V., L. M. Iyer, S. Balaji, and L. Aravind, 2007, Adhesion molecules and other secreted host-interaction determinants in Apicomplexa: insights from comparative genomics: Int Rev Cytol, v. 262, p. 1-74.
  262. Wiek, S., A. F. Cowman, and K. Lingelbach, 2004, Double cross-over gene replacement within the sec 7 domain of a GDP-GTP exchange factor from Plasmodium falciparum allows the generation of a transgenic brefeldin A-resistant parasite line: Mol Biochem Parasitol, v. 138, p. 51-5.
  263. Tuteja, R., A. Pradhan, and S. Sharma, 2008, Plasmodium falciparum signal peptidase is regulated by phosphorylation and required for intra-erythrocytic growth: Mol Biochem Parasitol, v. 157, p. 137-47.
  264. Rosenthal, P. J., and S. R. Meshnick, 1996, Hemoglobin catabolism and iron utilization by malaria parasites: Mol Biochem Parasitol, v. 83, p. 131-9.
  265. Couffin, S., R. Hernandez-Rivas, T. Blisnick, and D. Mattei, 1998, Characterisation of PfSec61, a Plasmodium falciparum homologue of a component of the translocation machinery at the endoplasmic reticulum membrane of eukaryotic cells: Mol Biochem Parasitol, v. 92, p. 89-98.
  266. van Dooren, G. G., S. D. Schwartzbach, T. Osafune, and G. I. McFadden, 2001, Translocation of proteins across the multiple membranes of complex plastids: Biochim Biophys Acta, v. 1541, p. 34-53.
  267. Dubey, J. P., and G. Schares, 2011, Neosporosis in animals--the last five years: Vet Parasitol, v. 180, p. 90-108.
  268. Muraguri, G. R., H. K. Kiara, and N. McHardy, 1999, Treatment of East Coast fever: a comparison of parvaquone and buparvaquone: Vet Parasitol, v. 87, p. 25-37.
  269. Robinson, M. S., and J. S. Bonifacino, 2001, Adaptor-related proteins: Curr Opin Cell Biol, v. 13, p. 444-53.
  270. Vlachou, D., T. Schlegelmilch, E. Runn, A. Mendes, and F. C. Kafatos, 2006, The developmental migration of Plasmodium in mosquitoes: Curr Opin Genet Dev, v. 16, p. 384-91.
  271. Peyroche, A., B. Antonny, S. Robineau, J. Acker, J. Cherfils, and C. L. Jackson, 1999, Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain: Mol Cell, v. 3, p. 275-85.
  272. Nevin, W. D., and J. B. Dacks, 2009, Repeated secondary loss of adaptin complex genes in the Apicomplexa: Parasitol Int, v. 58, p. 86-94.
  273. Sato, S., B. Clough, L. Coates, and R. J. Wilson, 2004, Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum: Protist, v. 155, p. 117-25.
  274. Lim, L., M. Kalanon, and G. I. McFadden, 2009, New proteins in the apicoplast membranes: time to rethink apicoplast protein targeting: Trends Parasitol, v. 25, p. 197-200.
  275. Janse, A. Ager, W. R. Jacobs, J. C. Sacchettini, V. Heussler, P. Sinnis, and D. A. Fidock, 2008, The fatty acid biosynthesis enzyme FabI plays a key role in the development of liver-stage malarial parasites: Cell Host Microbe, v. 4, p. 567-78.
  276. Ndam, N. T., and P. Deloron, 2007, Molecular aspects of Plasmodium falciparum Infection during pregnancy: J Biomed Biotechnol, v. 2007, p. 43785.
  277. Quashie, N. B., L. C. Ranford-Cartwright, and H. P. de Koning, 2010, Uptake of purines in Plasmodium falciparum-infected human erythrocytes is mostly mediated by the human equilibrative nucleoside transporter and the human facilitative nucleobase transporter: Malar J, v. 9, p. 36.
  278. Kuehn, A., and G. Pradel, 2010, The coming-out of malaria gametocytes: J Biomed Biotechnol, v. 2010, p. 976827.
  279. Villarejo, A., S. Burén, S. Larsson, A. Déjardin, M. Monné, C. Rudhe, J. Karlsson, S. Jansson, P. Lerouge, N. Rolland, G. von Heijne, M. Grebe, L. Bako, and G. Samuelsson, 2005, Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast: Nat Cell Biol, v. 7, p. 1224-31.
  280. MacRae, J. I., E. Maréchal, C. Biot, and C. Y. Botté, 2012, The apicoplast: a key target to cure malaria: Curr Pharm Des, v. 18, p. 3490-504.
  281. Wastl, J., and U. G. Maier, 2000, Transport of proteins into cryptomonads complex plastids: J Biol Chem, v. 275, p. 23194-8.


* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten