Publikationsserver der Universitätsbibliothek Marburg

Titel:Der Nachweis eines Mitglieds der OMP85-Proteinfamilie im Apikoplasten von Toxoplasma gondii
Autor:Bietz, Irine
Weitere Beteiligte: Przyborski, Jude (PD Dr. )
Veröffentlicht:2012
URI:https://archiv.ub.uni-marburg.de/diss/z2012/0768
DOI: https://doi.org/10.17192/z2012.0768
URN: urn:nbn:de:hebis:04-z2012-07687
DDC:570 Biowissenschaften, Biologie
Titel (trans.):The verification of an OMP85-Protein family member in the apicoplast of Toxoplasma gondii
Publikationsdatum:2012-09-13
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Protein transport, Apicoplast, OMP85,TgOMP85, Toxoplasma gondii, OMP85,TgOMP85, Toxoplasma gondii, Apikoplast,Proteintransport

Zusammenfassung:
Der intrazelluläre Parasit Toxoplasma gondii zeichnet sich wie die meisten Mitglieder der Chromalveolaten durch den Besitz einer sekundären Plastide aus, die man als Apikoplasten bezeichnet. Diese Art von Plastide ist durch einen Vorgang der sekundären Endosymbiose entstanden, bei der ein Rhodophyt von einer eukaryotischen Zelle aufgenommen und im Laufe der Evolution als Organell etabliert wurde. Aufgrund des horizontalen Gentransfers zwischen dem Nukleus und der Plastide werden die meisten Proteine des Apikoplasten im Wirtsgenom kodiert und im ER synthetisiert. Proteine des Apikoplastenstromas müssen daher aus dem ER, über die insgesamt vier Membranen der Plastide mit Hilfe einer Proteinimportmaschinerie zu ihrem Bestimmungsort befördert werden. Wie dieser Import im Detail erfolgt, ist zum jetzigen Zeitpunkt noch unklar. Jedoch konnten einige Komponenten dieser Maschinerie, wie SELMA in der PPM und ein Tic20-Homolog in der innersten Membran des Apikoplasten identifiziert werden. Basierend auf bioinformatischen Analysen konnten zwei Proteine der OMP85-Familie im Genom von T. gondii identifiziert werden. Die Mitglieder dieser Familie können aufgrund ihrer Funktionalität zwei Subtypen (Toc75- und Sam50-Subtyp) zugeordnet werden. Während Proteine des Toc75-Subtyps am Transport von Proteinen über Membranen beteiligt sind, sind die des Sam50-Subtyps in der Integration von Proteinen in Membranen involviert. Im Rahmen dieser Arbeit wurde für eines der beiden in T. gondii identifizierten OMP85 Proteine (TgOMP85) eine Funktion im Proteinimport in die Plastide postuliert. Nach Überprüfung des Genmodells konnte TgOMP85 eindeutig der OMP85-Familie zugeordnet und im Apikoplasten des genannten Parasiten lokalisiert werden. Des Weiteren wurde der Nachweis erbracht, dass TgOMP85 eine funktionelle BTS-Sequenz aufweist, welche den Transport und die Lokalisation in den Apikoplasten vermittelt. Um die Vermutung, dass es sich bei TgOMP85 um eine, in der dritten Apikoplastenmembran lokalisierte, Komponente der Proteinimportmaschinerie handelt, bestätigen zu können, sind weiterführende Analysen nötig. Das zweite identifizierte Protein (TgSam50) könnte aufgrund seiner Gensequenz und mitochondrialen Lokalisation dem Sam50-Subtyp zugeordnet werden. Ob es jedoch tatsächlich an der Assemblierung und Integration von Proteinen in die äußere mitochondriale Membran involviert ist, kann zum jetzigen Zeitpunkt nicht beantwortet werden.

Bibliographie / References

  1. Toso MA, Omoto CK. (2007). Gregarina niphandrodes may lack both a plastid genome and organelle. J Eukaryot Microbiol. 54(1):66-72.
  2. Singh K, Bhakuni V. (2008). Toxoplasma gondii ferredoxin-NADP+ reductase: Role of ionic interactions in stabilization of native conformation and s tructural cooperativity. Proteins. 71(4):1879-88.
  3. Saier MH Jr. (2006). Protein secretion and m embrane insertion systems in gram-negative bacteria. J Membr Biol. 214(2):75-90.
  4. Gould SB, Sommer MS, Hadfi K, Zauner S, Kroth PG, Maier UG. (2006). Protein targeting into the complex plastid of cryptophytes. J Mol Evol. 62(6):674-81.
  5. Köhler S. (2005). Multi-membrane-bound structures of Apicomplexa: I. the architecture of the Toxoplasma gondii apicoplast. Parasitol Res. 96(4):258-72.
  6. Sam-Yellowe TY. (1996). Rhoptry organelles of the apicomplexa: Their role in host cell invasion and intracellular survival. Parasitol Today.12(8):308-16.
  7. Striepen B. und S oldati. D. (2007). Genetic manipulation of Toxoplasma gondii. In Toxoplasma gondii: The Model Apicomplexan -Perspective and Methods, L.M. Weiss and K.
  8. Kovács-Bogdán E, Soll J, Bölter B. (2010). Protein import into chloroplasts: the Tic complex and its regulation. Biochim Biophys Acta. 1803(6):740-7. Epub 2010 Jan 25.
  9. McFadden GI, van Dooren GG. (2004). Evolution: red algal genome affirms a c ommon origin of all plastids. Curr Biol. 14(13):R514-6.
  10. Sánchez-Pulido L, Devos D, Genevrois S, Vicente M, Valencia A. (2003). POTRA: a conserved domain in the FtsQ family and a c lass of beta-barrel outer membrane proteins. Trends Biochem Sci. 28(10):523-6.
  11. Dubey JP. (2002). A review of toxoplasmosis in wild birds. Vet Parasitol.;106(2):121-53.
  12. Cavalier-Smith T. (2002). Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol. 12(2):R62-4.
  13. Cabantous S, Waldo GS. (2006). In vivo and in vitro protein solubility assays using split GFP. Nat Methods. 3(10):845-54.
  14. Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR. (2009). Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat Rev Microbiol. 7(3):206-14.
  15. Qbadou S, Becker T, Mirus O, Tews I, Soll J, Schleiff E. (2006). The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J. 25(9):1836-47.
  16. Toxoplasma gondii scavenges host-derived lipoic acid despite its de no vo synthesis in the apicoplast. EMBO J. 25(13):3214-22.
  17. Schleiff E, Soll J. (2005). Membrane protein insertion: mixing eukaryotic and pr okaryotic concepts. EMBO Rep. 6(11):1023-7.
  18. Bos MP, Robert V, Tommassen J. (2007). Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain. EMBO Rep. (12):1149-54.
  19. Tetlow IJ, Bowsher CG, Emes MJ. (1996). Reconstitution of the hexose phosphate translocator from the envelope membranes of wheat endosperm amyloplasts. Biochem J.319 (Pt 3):717-23.
  20. Sklar JG, Wu T, Gronenberg LS, Malinverni JC, Kahne D, Silhavy TJ. (2007). Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli. Proc Natl Acad Sci U S A. 104(15):6400-5.
  21. Sommer MS, Daum B, Gross LE, Weis BL, Mirus O, Abram L, Maier UG, Kühlbrandt W, Schleiff E. (2011). Chloroplast Omp85 proteins change orientation during evolution. Proc Natl Acad Sci U S A. 108(33):13841-6.
  22. Palenik B. (2002). The genomics of symbiosis: hosts keep the baby and t he bath water.
  23. Gilson PR, McFadden GI. (1996). The miniaturized nuclear genome of eukaryotic endosymbiont contains genes that overlap, genes that are cotranscribed, and t he smallest known spliceosomal introns. Proc Natl Acad Sci U S A. 93(15):7737-42.
  24. Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N. (2003). An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem. 278(49):48520-3.
  25. Bullmann L, Haarmann R, Mirus O, Bredemeier R, Hempel F, Maier UG, Schleiff E. (2010). Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J Biol Chem. 285(9):6848-56.
  26. Conserved properties of polypeptide transport-associated (POTRA) domains derived from cyanobacterial Omp85. J Biol Chem. 285(23):18016-24.
  27. Gupta N, Zahn M M, Coppens I, Joiner KA, Voelker DR. (2005). Selective disruption of phosphatidylcholine metabolism of the intracellular parasite Toxoplasma gondii arrests its growth. J Biol Chem. 280(16):16345-53.
  28. Maier UG, Douglas SE, Cavalier-Smith T. (2000). The nucleomorph genomes of cryptophytes and chlorarachniophytes. Protist 151(2):103-9.
  29. The N-terminal domain of Tob55 has a receptor-like function in the biogenesis of mitochondrial beta-barrel proteins. J Cell Biol. 176(1):77-88.
  30. Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am. J Epidemiol. 154(4):357-65.
  31. Heins L, Mehrle A, Hemmler R, Wagner R, Küchler M, Hörmann F, Sveshnikov D, Soll J. (2002). The preprotein conducting channel at the inner envelope membrane of plastids.
  32. Hempel F, Bullmann L, Lau J, Zauner S, Maier UG. (2009). ERAD-derived preprotein transport across the second outermost plastid membrane of diatoms. Mol Biol Evol. 26(8):1781-90.
  33. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10(1):1-6.
  34. Chen K, Chen X, Schnell DJ. (2000). Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Physiol. 122(3):813- 22.
  35. Gentle IE, Burri L, Lithgow T. (2005). Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol. 58(5):1216-25.
  36. Tonkin CJ, Struck NS, Mullin KA, Stimmler LM, McFadden GI. (2006). Evidence for Golgi- independent transport from the early secretory pathway to the plastid in malaria parasites. Mol Microbiol. 61(3):614-30.
  37. Coppens I. (2006). Contribution of host lipids to Toxoplasma pathogenesis. Cell Microbiol. 8(1):1-9.
  38. Dubey JP. (1997). Bradyzoite-induced murine toxoplasmosis: stage conversion, pathogenesis, and tissue cyst formation in mice fed bradyzoites of different strains of Toxoplasma gondii. J Eukaryot Microbiol.44(6):592-602.
  39. Dubey JP. (2008). The history of Toxoplasma gondii the first 100 years. J Eukaryot Microbiol.55(6):467-75.
  40. Kessler F, Schnell DJ. (2006). The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic. 7(3):248-57.
  41. Conserved pore-forming regions in polypeptide-transporting proteins. FEBS J. 272(6):1367- 78.
  42. Functional importance of a conserved sequence motif in FhaC, a prototypic member of the TpsB/Omp85 superfamily. FEBS J. (22):4755-65.
  43. Meissner M, Schlüter D, Soldati D. (2002). Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science. 298(5594):837-40.
  44. Kim S, Malinverni JC, Sliz P, Silhavy TJ, Harrison SC, Kahne D. (2007). Structure and function of an es sential component of the outer membrane protein assembly machine. Science. 317(5840):961-4.
  45. Joiner KA, Fuhrman SA, Miettinen HM, Kasper LH, Mellman I. (1990). Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science. 249(4969):641-6.
  46. Robichon C, Luo J, Causey TB, Benner JS, Samuelson JC. (2011). Engineering Escherichia coli BL21(DE3) derivative strains to minimize E. coli protein contamination after purification by immobilized metal affinity chromatography. Appl Environ Microbiol. 77(13):4634-46.
  47. DeRocher AE, Coppens I, Karnataki A, Gilbert LA, Rome ME, Feagin JE, Bradley PJ, Parsons M. (2008). A thioredoxin family protein of the apicoplast periphery identifies abundant candidate transport vesicles in Toxoplasma gondii. Eukaryot Cell. 7(9):1518-29.
  48. Receptor for retrograde transport in the apicomplexan parasite Toxoplasma gondii. Eukaryot Cell. 4(2):432-42.
  49. Kleine T, Maier UG, Leister D. (2009). DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol. 60:115-38.
  50. Wunder T, Martin R, Löffelhardt W, Schleiff E, Steiner JM. (2007). The invariant phenylalanine of precursor proteins discloses the importance of Omp85 for protein translocation into cyanelles. BMC Evol Biol.7:236.
  51. Sveshnikova N, Grimm R, Soll J, Schleiff E. (2000). Topology studies of the chloroplast protein import channel Toc75. Biol Chem. 381(8):687-93.
  52. Sommer MS, Schleiff E. (2009). Molecular interactions within the plant TOC complex. Biol Chem. 390(8):739-44.
  53. Clantin B, Delattre AS, Rucktooa P, Saint N, Méli AC, Locht C, Jacob-Dubuisson F, Villeret V. (2007). Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science. 317(5840):957-61.
  54. Perry SE, Keegstra K. (1994). Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell. 6(1):93-105.
  55. Vuong P, Bennion D, Mantei J, Frost D, Misra R. (2008). Analysis of YfgL and Y aeT interactions through bioinformatics, mutagenesis, and biochemistry. J Bacteriol. 190(5):1507- 17.
  56. Ma Y, Kouranov A, LaSala SE, Schnell DJ. (1996). Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and t ranslocation of precursor proteins at the outer envelope. J Cell Biol. 134(2):315-27.
  57. Sato S. (2011). The apicomplexan plastid and its evolution. Cell Mol Life Sci. 68(8):1285-96.
  58. Cavalier-Smith T, Chao EE. (2006). Phylogeny and m egasystematics of phagotrophic heterokonts (kingdom Chromista). J Mol Evol. 62(4):388-420.
  59. Cavalier-Smith T. (2001). Obcells as proto-organisms: membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cells, and photosynthesis. J Mol Evol. 53(4-5):555-95.
  60. Stoebe B, Maier UG. (2002). One, two, three: nature's tool box for building plastids. Protoplasma 219(3-4):123-30.
  61. Richter S, Lamppa GK. (1998). A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc Natl Acad Sci U S A. 95(13):7463-8.
  62. Karnataki A, Derocher AE, Coppens I, Feagin JE, Parsons M. (2007). A membrane protease is targeted to the relict plastid of Toxoplasma via an internal signal sequence. Traffic. 8(11):1543-53.
  63. van Dooren GG, Reiff SB, Tomova C, Meissner M, Humbel BM, Striepen B. (2009). A novel dynamin-related protein has been recruited for apicoplast fission in Toxoplasma gondii.
  64. Spork S, Hiss JA, Mandel K, Sommer M, Kooij TW, Chu T, Schneider G, Maier UG, Przyborski JM. (2009). An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum. Eukaryot Cell. 8(8):1134-45.
  65. Derocher AE, Karnataki A, Vaney P, Parsons M. (2012). Apicoplast targeting of a T. gondii transmembrane protein requires a cytosolic tyrosine-based motif. Traffic. 10.1111/j.1600- 0854.
  66. Köhler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJ, Palmer JD, Roos DS. (1997). A plastid of probable green algal origin in Apicomplexan parasites. Science. 275(5305):1485-9.
  67. Fichera ME, Roos DS. (1997). A plastid organelle as a dr ug target in apicomplexan parasites. Nature. 390(6658):407-9.
  68. Hirsch S, Muckel E, Heemeyer F, von Heijne G, Soll J. (1994). A receptor component of the chloroplast protein translocation machinery. Science. 266(5193):1989-92.
  69. Assembly factor Omp85 recognizes its outer membrane protein substrates by a species- specific C-terminal motif. PLoS Biol. 4(11):e377.
  70. Sheiner L, Demerly JL, Poulsen N, Beatty WL, Lucas O , Behnke MS, White MW, Striepen B. (2011). A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor. PLoS Pathog. 7(12):e1002392.
  71. Mereschkowski ,K. (1905). Über Natur und Ursprung der Chromtophoren im Pflanzenreiche. Biol Centralbl (25), 593-604.
  72. Schulz GE. (2000). Beta-Barrel membrane proteins. Curr Opin Struct Biol. 10(4):443-7.
  73. Bos MP, Robert V, Tommassen J. (2007). Biogenesis of the gram-negative bacterial outer membrane. Annu Rev Microbiol. 61:191-214.
  74. Struyvé M, Moons M, Tommassen J. (1991). Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol. 218(1):141-8.
  75. Onufryk C, Crouch ML, Fang FC, Gross CA. (2005). Characterization of six lipoproteins in the sigmaE regulon. J Bacteriol.187(13):4552-61.
  76. Schleiff E, Soll J, Küchler M, Kühlbrandt W, Harrer R. (2003). Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol. 160(4):541-51.
  77. Kalanon M, Tonkin CJ, McFadden GI. (2009). Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot Cell. 8(8):1146-54.
  78. Laemmli UK. (1970). Cleavage of structural proteins during the assembly of the head o f bacteriophage T4. Nature. 227(5259):680-5.
  79. Wilson RJ, Denny PW, Preiser PR, Rangachari K, Roberts K, Roy A, Whyte A, Strath M, Moore DJ, Moore PW, Williamson DH. (1996). Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol. 261(2):155-72.
  80. Gilson PR, Su V, Slamovits CH, Reith ME, Keeling PJ, McFadden GI. (2006). Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature's smallest nucleus. Proc Natl Acad Sci U S A. 103(25):9566-71.
  81. Zhu G, Marchewka MJ, Keithly JS. (2000). Cryptosporidium parvum appears to lack a plastid genome. Microbiology. 146 (Pt 2):315-21.
  82. Zuegge J, Ralph S, Schmuker M, McFadden GI, Schneider G. (2001). Deciphering apicoplast targeting signals--feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene. 280(1-2):19-26.
  83. Mercier C, Adjogble KD, Däubener W, Delauw MF. (2005). Dense granules: are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites? Int J Parasitol. 35(8):829-49.
  84. Kutik S, Stojanovski D, Becker L, Becker T, Meinecke M, Krüger V, Prinz C, Meisinger C, Guiard B, Wagner R, Pfanner N, Wiedemann N. (2008). Dissecting membrane insertion of mitochondrial beta-barrel proteins. Cell. 132(6):1011-24.
  85. Towbin H, Staehelin T, Gordon J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and s ome applications. Biotechnology. 1992;24:145-9.
  86. Kutschera U, Niklas KJ. (2005). Endosymbiosis, cell evolution, and s peciation. Theory Biosci. 124(1):1-24.
  87. Sato S, Clough B, Coates L, Wilson RJ. (2004). Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist. 155(1):117-25.
  88. Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M, Hell K, Rapaport D, Neupert W. (2003). Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature. 426(6968):862-6.
  89. Kim K, Soldati D, Boothroyd JC. (1993). Gene replacement in Toxoplasma gondii with chloramphenicol acetyltransferase as selectable marker. Science. 262(5135):911-4.
  90. Sibley LD, Khan A, Ajioka JW, Rosenthal BM. (2009). Genetic diversity of Toxoplasma gondii in animals and humans. Philos Trans R Soc Lond B Biol Sci.;364(1530):2749-61.
  91. Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 419(6906):498-511.
  92. Pelletier L, Stern CA, Pypaert M, Sheff D, Ngô HM, Roper N, He CY, Hu K, Toomre D, Coppens I, Roos DS, Joiner KA, Warren G. (2002). Golgi biogenesis in Toxoplasma gondii. Nature 418(6897):548-52.
  93. Donald, R. G. K. & Roos, D. S. 1994 Homologous recombination and gene replacement at the dihydrofolate reductase/thymidylate synthase locus in Toxoplasma gondii. Mol. Biochem. Parasitol. 63, 243–253.
  94. Kilian O, Kroth PG. (2005). Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J. 41(2):175- 83.
  95. Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ, Kahne D. (2005). Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell.121(2):235-45.
  96. Kessler F, Blobel G, Patel HA, Schnell DJ. (1994). Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science. 266(5187):1035-9.
  97. Ho-Yen DO. (2001). Infection in the immunocompetent. Toxoplasmosis: a c omprehensive clinical guide (eds D.H.M. Joynson & T.G. Wreghitt). Cambridge, UK: Cambridge University Press.
  98. Mordue DG, Sibley LD. (1997). Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J Immunol. 159(9):4452-9.
  99. Schnell DJ, Kessler F, Blobel G. (1994). Isolation of components of the chloroplast protein import machinery. Science. 266(5187):1007-12.
  100. Wilson RJ, Williamson DH, Preiser P. (1994). Malaria and other Apicomplexans: the "plant" connection. Infect Agents Dis. 3(1):29-37.
  101. Membrane contact sites between apicoplast and ER in Toxoplasma gondii revealed by electron tomography. Traffic. (10):1471-80.
  102. Mitterauer T, Nanoff C, Ahorn H, Freissmuth M, Hohenegger M. (1999). Metal-dependent nucleotide binding to the Escherichia coli rotamase SlyD. Biochem J. 342 (Pt 1):33-9.
  103. Roos DS, Crawford MJ, Donald RG, Fraunholz M, Harb OS, He CY, Kissinger JC, Shaw MK, Striepen B. (2002). Mining the Plasmodium genome database to define organellar function: what does the apicoplast do? Philos Trans R Soc Lond B Biol Sci. 357(1417):35-46.
  104. Carruthers VB, Sibley LD. (1999). Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol Microbiol. 31(2):421-8.
  105. Roos, D. S., Donald, R. G. K., Morrissette, N. S. & Moulton,A. L. C. (1994). Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Meth. Cell Biol. 45, 27–63.
  106. Harb OS, Chatterjee B, Fraunholz MJ, Crawford MJ, Nishi M, Roos DS. (2004). Multiple functionally redundant signals mediate targeting to the apicoplast in the apicomplexan parasite Toxoplasma gondii. Eukaryot Cell. 3(3):663-74.
  107. Bölter B, Soll J, Schulz A, Hinnah S, Wagner R. (1998). Origin of a chloroplast protein importer. Origin of a chloroplast protein importer. Proc Natl Acad Sci U S A. 95(26):15831-6.
  108. Gould SB, Waller RF, McFadden GI. (2008). Plastid evolution. Annu Rev Plant Biol. 59:491-517.
  109. McFadden GI, Reith ME, Munholland J, Lang-Unnasch N. (1996). Plastid in human parasites. Nature. 381(6582):482.
  110. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA. (1988). Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 239(4839):487-91.
  111. Rapoport TA. (2007). Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature. 450(7170):663-9.
  112. Li HM, Chiu CC. (2010). Protein transport into chloroplasts. Annu Rev Plant Biol. 61:157-80.
  113. Herm-Götz A, Agop-Nersesian C, Münter S, Grimley JS, Wandless TJ, Frischknecht F, Meissner M. (2007). Rapid control of protein level in the apicomplexan Toxoplasma gondii. Nat Methods. 4(12):1003-5.
  114. Hinnah SC, Hill K, Wagner R, Schlicher T, Soll J. (1997). Reconstitution of a chloroplast protein import channel. EMBO J. 16(24):7351-60.
  115. Tsai B, Ye Y, Rapoport TA. (2002). Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat Rev Mol Cell Biol. 3(4):246-55.
  116. Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J. (2003). Role of a hi ghly conserved bacterial protein in outer membrane protein assembly. Science. 299(5604):262-5.
  117. Carruthers VB, Sibley LD. (1997). Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol. 73(2):114-23.
  118. Scholz C, Eckert B, Hagn F, Schaarschmidt P, Balbach J, Schmid FX. (2006). SlyD proteins from different species exhibit high prolyl isomerase and chaperone activities. Biochemistry.;45(1):20-33.
  119. Nielsen E, Akita M, Davila-Aponte J, Keegstra K. (1997). Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J. 16(5):935-46.
  120. Sibley LD, Messina M, Niesman IR. (2004). Stable DNA transformation in the obligate intracellular parasite Toxoplasma gondii by complementation of tryptophan auxotrophy. Proc Natl Acad Sci U S A. 91(12):5508-12.
  121. Chou ML, Chu CC, Chen LJ, Akita M, Li HM. (2006). Stimulation of transit-peptide release and ATP hydrolysis by a c ochaperone during protein import into chloroplasts. J Cell Biol. 175(6):893-900.
  122. Striepen B. (2007). Switching parasite proteins on and off. Nat Methods. 4(12):999-1000.
  123. Margulis L. (1971). Symbiosis and evolution. Sci Am. 225(2):48-57.
  124. Kaasch AJ, Joiner KA. (2000). Targeting and subcellular localization of Toxoplasma gondii catalase. Identification of peroxisomes in an apicomplexan parasite. J Biol Chem. 275(2):1112-8. Protist 2000 Aug;151(2):103-9.
  125. Jarvis P. (2008). Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179(2):257-85.
  126. Dahl EL, Shock JL, Shenai BR, Gut J, DeRisi JL, Rosenthal PJ. (2006). Tetracyclines specifically target the apicoplast of the malaria parasite Plasmodium falciparum. Antimicrob Agents Chemother. 50(9):3124-31.
  127. Waller RF, McFadden GI. (2005). The apicoplast: a r eview of the derived plastid of apicomplexan parasites. Curr Issues Mol Biol.;7(1):57-79.
  128. Rogers MB, Gilson PR, Su V, McFadden GI, Keeling PJ. (2007). The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol Biol Evol. (1):54-62.
  129. Lim L, McFadden GI. (2010). The evolution, metabolism and functions of the apicoplast.
  130. Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, Deng LT, Wu X, Reith M, Cavalier-Smith T, Maier UG. (2001). The highly reduced genome of an enslaved algal nucleus. Nature. 410(6832):1091-6.
  131. Gentle I, Gabriel K, Beech P, Waller R, Lithgow T. (2004). The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol. 164(1):19- 24.
  132. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Genevrois S, Steeghs L, Roholl P, Letesson JJ, van der Ley P. (2003). The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane. EMBO J.22(8):1780-9.
  133. Schwab JC, Beckers CJ, Joiner KA. (1994). The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc Natl Acad Sci U S A. 91(2):509-13.
  134. Palmer J.D. (2003). The symbiotic birth and spread of plastids: How many times and whodunit? J. Phycol. 39, 4-11.
  135. Martin AM, Liu T, Lynn BC, Sinai AP. (2007). The Toxoplasma gondii parasitophorous vacuole membrane: transactions across the border. J Eukaryot Microbiol. 54(1):25-8.
  136. Ding M, Clayton C, Soldati D. (2000). Toxoplasma gondii catalase: are there peroxisomes in toxoplasma? J Cell Sci. 113 (Pt 13):2409-19.
  137. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, Foth BJ, Tonkin CJ, Roos DS, McFadden GI. (2004). Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol. 2(3):203-16.
  138. Sommer MS, Gould SB, Lehmann P, Gruber A, Przyborski JM, Maier UG. (2007). Der1- mediated preprotein import into the periplastid compartment of chromalveolates? Mol Biol Evol. (4):918-28.
  139. Wilson RJ, Williamson DH. (1997). Extrachromosomal DNA in the Apicomplexa. Microbiol Mol Biol Rev. 61(1):1-16.
  140. Morrissette NS, Sibley LD. (2002). Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev.66(1):21-38.
  141. Soll J, Schleiff E. (2004). Protein import into chloroplasts. Nat Rev Mol Cell Biol. 5(3):198- 208.
  142. Tomova C, Geerts WJ, Müller-Reichert T, Entzeroth R, Humbel BM. (2006). New comprehension of the apicoplast of Sarcocystis by transmission electron tomography. Biol Cell. 98(9):535-45.
  143. Seedorf M, Waegemann K, Soll J. (1995). A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J. 7(3):401-11.
  144. Carrillo N, Ceccarelli EA. (2003). Open questions in ferredoxin-NADP+ reductase catalytic mechanism. Eur J Biochem. 270(9):1900-15.
  145. Dubey JP, Frenkel JK. (1976). Feline toxoplasmosis from acutely infected mice and the development of Toxoplasma cysts. J Protozool.23(4):537-46.
  146. Misra R. (2007). First glimpse of the crystal structure of YaeT's POTRA domains. ACS Chem Biol. 2(10):649-51.
  147. Cavalier-Smith T. (2003). Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci. Philos Trans R Soc Lond B Biol Sci. 358(1429):109-33.
  148. Keeling PJ. (2010). The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci. 365(1541):729-48.
  149. Sagan L. (1967). On the origin of mitosing cells. J Theor Biol. 14(3):255-74.
  150. Jacob-Dubuisson F, Villeret V, Clantin B, Delattre AS, Saint N. (2009). First structural insights into the TpsB/Omp85 superfamily. Biol Chem. 390(8):675-84.
  151. Schleiff E, Maier UG, Becker T. (2011). Omp85 in eukaryotic systems: one protein family with distinct functions. Biol Chem. 392(1-2):21-7.
  152. Goodman CD, McFadden GI. (2007). Fatty acid biosynthesis as a dr ug target in apicomplexan parasites. Curr Drug Targets. 8(1):15-30.
  153. Wülfing C, Lombardero J, Plückthun A. (1994). An Escherichia coli protein consisting of a domain homologous to FK506-binding proteins (FKBP) and a new metal binding motif. J Biol Chem.269(4):2895-901.
  154. Ertel F, Mirus O, Bredemeier R, Moslavac S, Becker T, Schleiff E. (2005). The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. J Biol Chem. 280(31):28281-9.
  155. Ye Y, Shibata Y, Yun C, Ron D, Rapoport TA. (2004). A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature. 429(6994):841-7.
  156. Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, Lang-Unnasch N, Cowman AF, Besra GS, Roos DS, McFadden GI. (1998). Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci U S A. 95(21):12352-7.
  157. van Dooren GG, Tomova C, Agrawal S, Humbel BM, Striepen B. (2008). Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc Natl Acad Sci U S A. 105(36):13574-9.
  158. Grigg ME, Sundar N. (2009). Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. Int J Parasitol.39(8):925-33.
  159. Waller RF, Reed MB, Cowman AF, McFadden GI. (2000). Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19(8):1794-802.
  160. May T, Soll J. (2000). 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell. 12(1):53-64.
  161. Ohad N, Shichrur K, Yalovsky S. (2007). The analysis of protein-protein interactions in plants by bimolecular fluorescence complementation. Plant Physiol. 145(4):1090-9.
  162. Kyte J, Doolittle RF. (1982). A simple method for displaying the hydropathic character of a protein. J Mol Biol. 157(1):105-32.
  163. Tenter AM, Heckeroth AR, Weiss LM. (2000). Toxoplasma gondii: from animals to humans.
  164. Dubey JP. (1998). Advances in the life cycle of Toxoplasma gondii. Int J Parasitol. 28(7):1019-24.
  165. Patron NJ, Waller RF, Archibald JM, Keeling PJ. (2005). Complex protein targeting to dinoflagellate plastids. J Mol Biol. 348(4):1015-24.
  166. Foth BJ, McFadden GI. (2003). The apicoplast: a plastid in Plasmodium falciparum and other Apicomplexan parasites. Int Rev Cytol.224:57-110.
  167. Coppens I, Dunn JD, Romano JD, Pypaert M, Zhang H, Boothroyd JC, Joiner KA. (2006). Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell.125(2):261-74.
  168. Tonkin CJ, Roos DS, McFadden GI. (2006). N-terminal positively charged amino acids, but not their exact position, are important for apicoplast transit peptide fidelity in Toxoplasma gondii. Mol Biochem Parasitol. 150(2):192-200.
  169. Goodman CD, Su V, McFadden GI. (2007). The effects of anti-bacterials on t he malaria parasite Plasmodium falciparum. Mol Biochem Parasitol. 152(2):181-91.
  170. Endo T, Yamano K. (2010). Transport of proteins across or into the mitochondrial outer membrane. Biochim Biophys Acta. 1803(6):706-14.
  171. Voulhoux R, Tommassen J. (2004). Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res Microbiol. 155(3):129-35.
  172. Rodríguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W, Bohnert HJ, Philippe H, Lang BF. (2005). Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. 15(14):1325-30.
  173. Cavalier-Smith T. (2000). Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5(4):174-82.
  174. Reumann S, Keegstra K. (1999). The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci. 4(8):302-307.
  175. Parsy CB, Chapman CJ, Barnes AC, Robertson JF, Murray A. (2007). Two-step method to isolate target recombinant protein from co-purified bacterial contaminant SlyD after immobilised metal affinity chromatography. J Chromatogr B Analyt Technol Biomed Life Sci. 853(1-2):314-9.
  176. Wastl J, Maier UG. (2000). Transport of proteins into cryptomonads complex plastids. J Biol Chem. 275(30):23194-8.
  177. Bredemeier R, Schlegel T, Ertel F, Vojta A, Borissenko L, Bohnsack MT, Groll M, von Haeseler A, Schleiff E. (2007). Functional and phylogenetic properties of the pore-forming beta-barrel transporters of the Omp85 family. J Biol Chem. 282(3):1882-90.


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