Inactivation of a Plasmodium apicoplast protein attenuates formation of liver merozoites

Molecular Microbiology

Volumn 81, Issue 6, 2011, Pages 1511-1525

  Haussig, Joana M ^a   Matuschewski, Kai ^a   Kooij, Taco W A ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MEROZOITE SURFACE PROTEIN 1; PLASMODIUM APICOPLAST PROTEIN; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOPHELES STEPHENSI; APICOPLAST; ARTICLE; BLOOD BRAIN BARRIER; BRAIN MALARIA; CONTROLLED STUDY; DRUG POTENCY; EXPERIMENTAL INFECTION; FEMALE; HUMAN; HUMAN CELL; IMMUNIZATION; LIVER; LIVER MEROZOITE FORMATION; MEROSOME; MEROZOITE; MORPHOLOGY; MOUSE; NONHUMAN; PARASITE VECTOR; PARASITEMIA; PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REINFECTION; SPOROZOITE;

AMINO ACID SEQUENCE; ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; LIVER; MALARIA; MALARIA VACCINES; MEROZOITES; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; VACCINES, ATTENUATED; VIRULENCE; VIRULENCE FACTORS;

MUS; PLASMODIUM BERGHEI; RODENTIA;

EID: 80052705758     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07787.x     Document Type: Article

References (52)

1. Amino, R., Thiberge, S., Martin, B., Celli, S., Shorte, S., Frischknecht, F., and Ménard, R. (2006) Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 12: 220-224.
2. Baer, K., Klotz, C., Kappe, S.H.I., Schnieder, T., and Frevert, U. (2007) Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathog 3: e171.
3. Chitale, M., Hawkins, T., Park, C., and Kihara, D. (2009) ESG: extended similarity group method for automated protein function prediction. Bioinformatics 25: 1739-1745.
4. Cohen, J., Nussenzweig, V., Nussenzweig, R., Vekemans, J., and Leach, A. (2010) From the circumsporozoite protein to the RTS, S/AS candidate vaccine. Hum Vaccin 6: 90-96.
5. Dahl, E.L., and Rosenthal, P.J. (2007) Multiple antibiotics exert delayed effects against the Plasmodium falciparum apicoplast. Antimicrob Agents Chemother 51: 3485-3490.
6. van Dijk, M.R., Douradinha, B.G., Franke-Fayard, B.M.D., Heussler, V.T., van Dooren, M.W., van Schaijk, B.C.L., etal. (2005) Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci USA 102: 12194-12199.
7. Doolan, D.L., and Hoffman, S.L. (2000) The complexity of protective immunity against liver-stage malaria. J Immunol 165: 1453-1462.
8. Douradinha, B.G., van Dijk, M.R., Ataide, R., van Gemert, G.-J., Thompson, J., Franetich, J.-F., etal. (2007) Genetically attenuated P36p-deficient Plasmodium berghei sporozoites confer long-lasting and partial cross-species protection. Int J Parasitol 37: 1511-1519.
9. Draper, S.J., Goodman, A.L., Biswas, S., Forbes, E.K., Moore, A.C., Gilbert, S.C., and Hill, A.V.S. (2009) Recombinant viral vaccines expressing merozoite surface protein-1 induce antibody- and T cell-mediated multistage protection against malaria. Cell Host Microbe 5: 95-105.
10. Falae, A., Combe, A., Amaladoss, A., Carvalho, T.G., Ménard, R., and Bhanot, P. (2010) Role of Plasmodium berghei cGMP-dependent protein kinase in late liver stage development. J Biol Chem 285: 3282-3288.
11. Fichera, M.E., and Roos, D.S. (1997) A plastid organelle as a drug target in apicomplexan parasites. Nature 390: 407-409.
12. Foth, B.J., Ralph, S.A., Tonkin, C.J., Struck, N.S., Fraunholz, M.J., Roos, D.S., etal. (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299: 705-708.
13. Frevert, U., Engelmann, S., Zougbédé, S., Stange, J., Ng, B., Matuschewski, K., etal. (2005) Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol 3: e192.
14. Friesen, J., Silvie, O., Putrianti, E.D., Hafalla, J.C.R., Matuschewski, K., and Borrmann, S. (2010) Natural immunization against malaria: causal prophylaxis with antibiotics. Sci Transl Med 2: 40ra49.
15. Guinovart, C., Aponte, J.J., Sacarlal, J., Aide, P., Leach, A., Bassat, Q., etal. (2009) Insights into long-lasting protection induced by RTS, S/AS02A malaria vaccine: further results from a phase IIb trial in Mozambican children. PLoS ONE 4: e5165.
16. Haldar, K., Murphy, S.C., Milner, D.A., and Taylor, T.E. (2007) Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease. Annu Rev Pathol 2: 217-249.
17. Hoffman, S.L., Billingsley, P.F., James, E., Richman, A., Loyevsky, M., Li, T., etal. (2010) Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum Vaccin 6: 97-106.
18. Holder, A.A., and Freeman, R.R. (1981) Immunization against blood-stage rodent malaria using purified parasite antigens. Nature 294: 361-364.
19. Ishino, T., Boisson, B., Orito, Y., Lacroix, C., Bischoff, E., Loussert, C., etal. (2009) LISP1 is important for the egress of Plasmodium berghei parasites from liver cells. Cell Microbiol 11: 1329-1339.
20. Janouskovec, J., Horák, A., Oborník, M., Lukes, J., and Keeling, P.J. (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 107: 10949-10954.
21. Janse, C.J., Franke-Fayard, B.M.D., Mair, G.R., Ramesar, J., Thiel, C., Engelmann, S., etal. (2006) High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol Biochem Parasitol 145: 60-70.
22. Jobe, O., Lumsden, J., Mueller, A.-K., Williams, J., Silva-Rivera, H., Kappe, S.H.I., etal. (2007) Genetically attenuated Plasmodium berghei liver stages induce sterile protracted protection that is mediated by major histocompatibility complex Class I-dependent interferon-gamma-producing CD8+ T cells. J Infect Dis 196: 599-607.
23. Jomaa, H., Wiesner, J., Sanderbrand, S., Altincicek, B., Weidemeyer, C., Hintz, M., etal. (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285: 1573-1576.
24. Lackner, P., Beer, R., Heussler, V., Goebel, G., Rudzki, D., Helbok, R., etal. (2006) Behavioural and histopathological alterations in mice with cerebral malaria. Neuropathol Appl Neurobiol 32: 177-188.
25. Moorthy, V.S., and Ballou, W.R. (2009) Immunological mechanisms underlying protection mediated by RTS, S: a review of the available data. Malar J 8: 312.
26. Mota, M.M., Pradel, G., Vanderberg, J., Hafalla, J.C., Frevert, U., Nussenzweig, R.S., etal. (2001) Migration of Plasmodium sporozoites through cells before infection. Science 291: 141-144.
27. Mueller, A.-K., Labaied, M., Kappe, S.H.I., and Matuschewski, K. (2005a) Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433: 164-167.
28. Mueller, A.-K., Camargo, N., Kaiser, K., Andorfer, C., Frevert, U., Matuschewski, K., and Kappe, S.H.I. (2005b) Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 102: 3022-3027.
29. Mueller, A.-K., Deckert, M., Heiss, K., Goetz, K., Matuschewski, K., and Schlüter, D. (2007) Genetically attenuated Plasmodium berghei liver stages persist and elicit sterile protection primarily via CD8 T cells. Am J Pathol 171: 107-115.
30. Ngonseu, E., Chatterjee, S., and Wery, M. (1998) Blocked hepatic-stage parasites and decreased susceptibility to Plasmodium berghei infections in BALB/c mice. Parasitology 117: 419-423.
31. Nussenzweig, R.S., Vanderberg, J., Most, H., and Orton, C. (1967) Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature 216: 160-162.
32. Otto, T.D., Wilinski, D., Assefa, S., Keane, T.M., Sarry, L.R., Böhme, U., etal. (2010) New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol Microbiol 76: 12-24.
33. Pei, Y., Tarun, A.S., Vaughan, A.M., Herman, R.W., Soliman, J.M.B., Erickson-Wayman, A., and Kappe, S.H.I. (2010) Plasmodium pyruvate dehydrogenase activity is only essential for the parasite's progression from liver infection to blood infection. Mol Microbiol 75: 957-971.
34. Prudencio, M., Rodriguez, A., and Mota, M.M. (2006) The silent path to thousands of merozoites: the Plasmodium liver stage. Nat Rev Microbiol 4: 849-856.
35. Ralph, S.A., van Dooren, G.G., Waller, R.F., Crawford, M.J., Fraunholz, M.J., Foth, B.J., etal. (2004) Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2: 203-216.
36. Roestenberg, M., McCall, M., Hopman, J., Wiersma, J., Luty, A.J.F., van Gemert, G.-J., etal. (2009) Protection against a malaria challenge by sporozoite inoculation. N Engl J Med 361: 468-477.
37. Roestenberg, M., Teirlinck, A.C., McCall, M.B., Teelen, K., Makamdop, K.N., Wiersma, J., etal. (2011) Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 377: 1770-1776.
38. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N.G., Palmer, A.E., and Tsien, R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572.
39. Sibley, L.D. (2011) Invasion and intracellular survival by protozoan parasites. Immunol Rev 240: 72-91.
40. Silvie, O., Mota, M.M., Matuschewski, K., and Prudencio, M. (2008a) Interactions of the malaria parasite and its mammalian host. Curr Opin Microbiol 11: 352-359.
41. Silvie, O., Goetz, K., and Matuschewski, K. (2008b) A sporozoite asparagine-rich protein controls initiation of Plasmodium liver stage development. PLoS Pathog 4: e1000086.
42. de Souza, J.B., Hafalla, J.C.R., Riley, E.M., and Couper, K.N. (2010) Cerebral malaria: why experimental murine models are required to understand the pathogenesis of disease. Parasitology 137: 755-772.
43. Sturm, A., Amino, R., van de Sand, C., Regen, T., Retzlaff, S., Rennenberg, A., etal. (2006) Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313: 1287-1290.
44. Tarun, A.S., Peng, X., Dumpit, R.F., Ogata, Y., Silva-Rivera, H., Camargo, N., etal. (2008) A combined transcriptome and proteome survey of malaria parasite liver stages. Proc Natl Acad Sci USA 105: 305-310.
45. Tonkin, C.J., van Dooren, G.G., Spurck, T.P., Struck, N.S., Good, R.T., Handman, E., etal. (2004) Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 137: 13-21.
46. Tsuji, M., Mattei, D., Nussenzweig, R.S., Eichinger, D., and Zavala, F. (1994) Demonstration of heat-shock protein 70 in the sporozoite stage of malaria parasites. Parasitol Res 80: 16-21.
47. Vanderberg, J. (1975) Development of infectivity by the Plasmodium berghei sporozoite. J Parasitol 61: 43-50.
48. Vaughan, A.M., O'Neill, M.T., Tarun, A.S., Camargo, N., Phuong, T.M., Aly, A.S.I., etal. (2009) Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cell Microbiol 11: 506-520.
49. Waller, R.F., Reed, M.B., Cowman, A.F., and McFadden, G.I. (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 19: 1794-1802.
50. Wilson, R.J.M., Denny, P.W., Preiser, P.R., Rangachari, K., Roberts, K., Roy, A., etal. (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261: 155-172.
51. World Health Organization (2011) World Malaria Report 2010.
52. Yu, M., Kumar, T.R.S., Nkrumah, L.J., Coppi, A., Retzlaff, S., Li, C.D., etal. (2008) The fatty acid biosynthesis enzyme FabI plays a key role in the development of liver-stage malarial parasites. Cell Host Microbe 4: 567-578.