Two putative protein export regulators promote Plasmodium blood stage development in vivo

Molecular and Biochemical Parasitology

Volumn 191, Issue 1, 2013, Pages 44-52

  Matz, Joachim M ^a,b   Matuschewski, Kai ^a,b   Kooij, Taco W A ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Experimental genetics; Flow cytometry; Malaria; Plasmodium berghei; Protein export; PTEX translocon

Indexed keywords

EXP2 PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 101; PTEX150 PROTEIN; PTEX88 PROTEIN; REGULATOR PROTEIN; THIOREDOXIN 2; TRANSLOCON; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLOODSTREAM INFECTION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE DELETION; GENETIC TRANSFECTION; HOST CELL; MOUSE; NONHUMAN; PARASITE DEVELOPMENT; PLASMODIUM BERGHEI; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; TROPHOZOITE; WILD TYPE;

MURINAE; PLASMODIUM BERGHEI;

3′; 3′ UNTRANSLATED REGION; 5′; 5′ UNTRANSLATED REGION; ENDOPLASMIC RETICULUM; ER; EXPERIMENTAL GENETICS; FLOW CYTOMETRY; GFP; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN; HSP; MALARIA; PARASITE MULTIPLICATION RATE; PARASITOPHOROUS VACUOLE; PARASITOPHOROUS VACUOLE MEMBRANE; PBAT; PEXEL; PEXEL/VTS NEGATIVE EXPORTED PROTEINS; PFEMP1; PHOSPHATIDYLINOSITOL 3-PHOSPHATE; PI3P; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI ADAPTABLE TRANSFECTION PLASMID; PLASMODIUM EXPORT ELEMENT; PLASMODIUM FALCIPARUM ERYTHROCYTE MEMBRANE PROTEIN 1; PLASMODIUM TRANSLOCON OF EXPORTED PROTEINS; PMR; PNEPS; PROTEIN EXPORT; PTEX; PTEX TRANSLOCON; PV; PVM; SIL6; SILENT INTERGENIC LOCUS ON PLASMODIUM BERGHEI CHROMOSOME 6; THIOREDOXIN 2; TRX2; VACUOLAR TRANSPORT SIGNAL; VTS; WILD TYPE; WT; YELLOW FLUORESCENT PROTEIN; YFP;

ANIMALS; BLOOD; CALCIUM-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION; GENES, ESSENTIAL; GENES, PROTOZOAN; GENETIC COMPLEMENTATION TEST; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; PLASMODIUM BERGHEI; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, PEPTIDE;

EID: 84885447286     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2013.09.003     Document Type: Article

References (56)

1. A. Mbengue, X.Y. Yam, and C. Braun-Breton Human erythrocyte remodelling during Plasmodium falciparum malaria parasite growth and egress Br J Haematol 157 2012 171 179
2. T. Spielmann, G.N. Montagna, L. Hecht, and K. Matuschewski Molecular make-up of the Plasmodium parasitophorous vacuolar membrane Int J Med Microbiol 302 2012 179 186
3. J.A. Boddey, and A.F. Cowman Plasmodium nesting: remaking the erythrocyte from the inside out Annu Rev Microbiol 67 2013 243 269
4. M. Marti, and T. Spielmann Protein export in malaria parasites: many membranes to cross Curr Opin Microbiol 16 2013 445 451
5. D.I. Baruch, B.L. Pasloske, H.B. Singh, X. Bi, X.C. Ma, and M. Feldman Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes Cell 82 1995 77 87
6. J.D. Smith, C.E. Chitnis, A.G. Craig, D.J. Roberts, D.E. Hudson-Taylor, and D.S. Peterson Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes Cell 82 1995 101 110
7. X.Z. Su, V.M. Heatwole, S.P. Wertheimer, F. Guinet, J.A. Herrfeldt, and D.S. Peterson The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes Cell 82 1995 89 100
8. A.G. Maier, M. Rug, M.T. O'Neill, M. Brown, S.J. Chakravorty, and T. Szestak Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes Cell 134 2008 48 61
9. M. Cyrklaff, C.P. Sanchez, N. Kilian, C. Bisseye, J. Simpore, and F. Frischknecht Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes Science 334 2011 1283 1286
10. W. Nguitragool, A.A.B. Bokhari, A.D. Pillai, K. Rayavara, P. Sharma, and B. Turpin Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells Cell 145 2011 665 677
11. M. Marti, R.T. Good, M. Rug, E. Knuepfer, and A.F. Cowman Targeting malaria virulence and remodeling proteins to the host erythrocyte Science 306 2004 1930 1933
12. N.L. Hiller, S. Bhattacharjee, C. van Ooij, K. Liolios, T. Harrison, and C. Lopez-Estraño A host-targeting signal in virulence proteins reveals a secretome in malarial infection Science 306 2004 1934 1937
13. S. Bhattacharjee, R.V. Stahelin, K.D. Speicher, D.W. Speicher, and K. Haldar Endoplasmic reticulum PI(3)P lipid binding targets malaria proteins to the host cell Cell 148 2012 201 212
14. J.A. Boddey, A.N. Hodder, S. Günther, P.R. Gilson, H. Patsiouras, and E.A. Kapp An aspartyl protease directs malaria effector proteins to the host cell Nature 463 2010 627 631
15. I. Russo, S. Babbitt, V. Muralidharan, T. Butler, A. Oksman, and D.E. Goldberg Plasmepsin V licenses Plasmodium proteins for export into the host erythrocyte Nature 463 2010 632 636
16. H.H. Chang, A.M. Falick, P.M. Carlton, J.W. Sedat, J.L. DeRisi, and M.A. Marletta N-terminal processing of proteins exported by malaria parasites Mol Biochem Parasitol 160 2008 107 115
17. C. Grüring, A. Heiber, F. Kruse, S. Flemming, G. Franci, and S.F. Colombo Uncovering common principles in protein export of malaria parasites Cell Host Microbe 12 2012 717 729
18. A. Heiber, F. Kruse, C. Pick, C. Grüring, S. Flemming, and A. Oberli Identification of new PNEPs indicates a substantial non-PEXEL exportome and underpins common features in Plasmodium falciparum protein export PLoS Pathog 9 2013 e1003546
19. T.W.A. Kooij, J.M. Carlton, S.L. Bidwell, N. Hall, J. Ramesar, and C.J. Janse A Plasmodium whole-genome synteny map: indels and synteny breakpoints as foci for species-specific genes PLoS Pathog 1 2005 e44
20. J.M. Carlton, J.H. Adams, J.C. Silva, S.L. Bidwell, H. Lorenzi, and E. Caler Comparative genomics of the neglected human malaria parasite Plasmodium vivax Nature 455 2008 757 763
21. T.J. Sargeant, M. Marti, E. Caler, J.M. Carlton, K.M. Simpson, and T.P. Speed Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites Genome Biol 7 2006 R12
22. C. van Ooij, P.A. Tamez, S. Bhattacharjee, N.L. Hiller, T. Harrison, and K. Liolios The malaria secretome: from algorithms to essential function in blood stage infection PLoS Pathog 4 2008 e1000084
23. C. Pick, I. Ebersberger, T. Spielmann, I. Bruchhaus, and T. Burmester Phylogenomic analyses of malaria parasites and evolution of their exported proteins BMC Evol Biol 11 2011 167
24. J. Fonager, E.M. Pasini, J.A.M. Braks, O. Klop, J. Ramesar, and E.J. Remarque Reduced CD36-dependent tissue sequestration of Plasmodium-infected erythrocytes is detrimental to malaria parasite growth in vivo J Exp Med 209 2012 93 107
25. E.M. Pasini, J.A. Braks, J. Fonager, O. Klop, E. Aime, and R. Spaccapelo Proteomic and genetic analyses demonstrate that Plasmodium berghei blood stages export a large and diverse repertoire of proteins Mol Cell Proteomics 12 2013 426 448
26. T.F. de Koning-Ward, P.R. Gilson, J.A. Boddey, M. Rug, B.J. Smith, and A.T. Papenfuss A newly discovered protein export machine in malaria parasites Nature 459 2009 945 949
27. H.E. Bullen, S.C. Charnaud, M. Kalanon, D.T. Riglar, C. Dekiwadia, and N. Kangwanrangsan Biosynthesis, localization, and macromolecular arrangement of the Plasmodium falciparum translocon of exported proteins (PTEX) J Biol Chem 287 2012 7871 7884
28. S. Haase, and T.F. de Koning-Ward New insights into protein export in malaria parasites Cell Microbiol 12 2010 580 587
29. H.E. Bullen, B.S. Crabb, and P.R. Gilson Recent insights into the export of PEXEL/HTS-motif containing proteins in Plasmodium parasites Curr Opin Microbiol 15 2012 699 704
30. N. Gehde, C. Hinrichs, I. Montilla, S. Charpian, K. Lingelbach, and J.M. Przyborski Protein unfolding is an essential requirement for transport across the parasitophorous vacuolar membrane of Plasmodium falciparum Mol Microbiol 71 2009 613 628
31. T.W.A. Kooij, M.M. Rauch, and K. Matuschewski Expansion of experimental genetics approaches for Plasmodium berghei with versatile transfection vectors Mol Biochem Parasitol 185 2012 19 26
32. S. Kenthirapalan, A.P. Waters, K. Matuschewski, and T.W.A. Kooij Flow cytometry-assisted rapid isolation of recombinant Plasmodium berghei parasites exemplified by functional analysis of aquaglyceroporin Int J Parasitol 42 2012 1185 1192
33. C.J. Janse, B.M.D. Franke-Fayard, G.R. Mair, J. Ramesar, C. Thiel, and S. Engelmann High efficiency transfection of Plasmodium berghei facilitates novel selection procedures Mol Biochem Parasitol 145 2006 60 70
34. J.M. Haussig, K. Matuschewski, and T.W.A. Kooij Inactivation of a Plasmodium apicoplast protein attenuates formation of liver merozoites Mol Microbiol 81 2011 1511 1525
35. K.G. Le Roch, Y. Zhou, P.L. Blair, M. Grainger, J.K. Moch, and J.D. Haynes Discovery of gene function by expression profiling of the malaria parasite life cycle Science 301 2003 1503 1508
36. K. Matthews, M. Kalanon, S.A. Chisholm, A. Sturm, C.D. Goodman, and M.W.A. Dixon The Plasmodium translocon of exported proteins (PTEX) component thioredoxin-2 is important for maintaining normal blood-stage growth Mol Microbiol 89 2013 1167 1186
37. D.T. Riglar, K.L. Rogers, E. Hanssen, L. Turnbull, H.E. Bullen, and S.C. Charnaud Spatial association with PTEX complexes defines regions for effector export into Plasmodium falciparum-infected erythrocytes Nat Commun 4 2013 1415
38. C.J. Tonkin, G.G. van Dooren, T.P. Spurck, N.S. Struck, R.T. Good, and E. Handman Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method Mol Biochem Parasitol 137 2004 13 21
39. A. Ingmundson, C. Nahar, V. Brinkmann, M.J. Lehmann, and K. Matuschewski The exported Plasmodium berghei protein IBIS1 delineates membranous structures in infected red blood cells Mol Microbiol 83 2012 1229 1243
40. S. Haase, E. Hanssen, K. Matthews, M. Kalanon, and T.F. de Koning-Ward The exported protein PbCP1 localises to cleft-like structures in the rodent malaria parasite Plasmodium berghei PLoS ONE 8 2013 e61482
41. C. Currà, T. Pace, B.M.D. Franke-Fayard, L. Picci, L. Bertuccini, and M. Ponzi Erythrocyte remodeling in Plasmodium berghei infection: the contribution of SEP family members Traffic 13 2012 388 399
42. I.W. Boucher, P.J. McMillan, M. Gabrielsen, S.E. Akerman, J.A. Brannigan, and C. Schnick Structural and biochemical characterization of a mitochondrial peroxiredoxin from Plasmodium falciparum Mol Microbiol 61 2006 948 959
43. S. Kehr, N. Sturm, S. Rahlfs, J.M. Przyborski, and K. Becker Compartmentation of redox metabolism in malaria parasites PLoS Pathog 6 2010 e1001242
44. A. Sharma, A. Sharma, S. Dixit, and A. Sharma Structural insights into thioredoxin-2: a component of malaria parasite protein secretion machinery Sci Rep 1 2011 179
45. B. Franke-Fayard, J. Fonager, A. Braks, S.M. Khan, and C.J. Janse Sequestration and tissue accumulation of human malaria parasites: can we learn anything from rodent models of malaria? PLoS Pathog 6 2010 e1001032
46. N.Y. Jemmely, M. Niang, and P.R. Preiser Small variant surface antigens and Plasmodium evasion of immunity Future Microbiol 5 2010 663 682
47. C.S.S. Gomes-Santos, M.A. Itoe, C. Afonso, R. Henriques, R. Gardner, and N. Sepúlveda Highly dynamic host actin reorganization around developing Plasmodium inside hepatocytes PLoS ONE 7 2012 e29408
48. E.M. Kass, and M. Jasin Collaboration and competition between DNA double-strand break repair pathways FEBS Lett 584 2010 3703 3708
49. E. Mladenov, and G. Iliakis Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways Mutat Res 711 2011 61 72
50. B.S. Crabb, T.F. de Koning-Ward, and P.R. Gilson Protein export in Plasmodium parasites: from the endoplasmic reticulum to the vacuolar export machine Int J Parasitol 40 2010 509 513
51. C.J. Janse, P.H. van Vianen, H.J. Tanke, B. Mons, T. Ponnudurai, and J.P. Overdulve Plasmodium species: flow cytometry and microfluorometry assessments of DNA content and synthesis Exp Parasitol 64 1987 88 94
52. D. Barkan, H. Ginsburg, and J. Golenser Optimisation of flow cytometric measurement of parasitaemia in Plasmodium-infected mice Int J Parasitol 30 2000 649 653
53. M.B. Jiménez-Díaz, J. Rullas, T. Mulet, L. Fernández, C. Bravo, and D. Gargallo-Viola Improvement of detection specificity of Plasmodium-infected murine erythrocytes by flow cytometry using autofluorescence and YOYO-1 Cytometry A 67 2005 27 36
54. S.C. Bhakdi, P. Sratongno, P. Chimma, T. Rungruang, A. Chuncharunee, and H.P.H. Neumann Re-evaluating acridine orange for rapid flow cytometric enumeration of parasitemia in malaria-infected rodents Cytometry A 71 2007 662 667
55. M.B. Jiménez-Díaz, T. Mulet, V. Gómez, S. Viera, A. Alvarez, and H. Garuti Quantitative measurement of Plasmodium-infected erythrocytes in murine models of malaria by flow cytometry using bidimensional assessment of SYTO-16 fluorescence Cytometry A 75 2009 225 235
56. Y. Gerena, M. Gonzalez-Pons, and A.E. Serrano Cytofluorometric detection of rodent malaria parasites using red-excited fluorescent dyes Cytometry A 79 2011 965 972