The novel putative transporter NPT1 plays a critical role in early stages of Plasmodium berghei sexual development

Molecular Microbiology

Volumn 81, Issue 5, 2011, Pages 1343-1357

  Boisson, Bertrand ^a,d   Lacroix, Céline ^a   Bischoff, Emmanuel ^b   Gueirard, Pascale ^a   Bargieri, Daniel Y ^a   Franke Fayard, Blandine ^c   Janse, Chris J ^c   Ménard, Robert ^a   Baldacci, Patricia ^a  

^a Biologie et Génétique du Paludisme   (France)

^b Parc Scientifique de Luminy   (France)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TRANSPORTER NPT1; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ASEXUAL REPRODUCTION; CELL MATURATION; CONTROLLED STUDY; FEMALE; GAMETE; GAMETOCYTE; GENETIC CODE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM BERGHEI; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RAT; SEXUAL DEVELOPMENT; SPECIES CONSERVATION;

ANIMALS; CULICIDAE; ERYTHROCYTES; GAMETOGENESIS; GENE EXPRESSION; HOST-PARASITE INTERACTIONS; MALARIA; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS; RATS; RATS, WISTAR; SEX DIFFERENTIATION; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE III;

MAMMALIA; PLASMODIUM BERGHEI;

EID: 80051934815     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07767.x     Document Type: Article

References (64)

1. Alano, P. (2007) Plasmodium falciparum gametocytes: still many secrets of a hidden life. Mol Microbiol 66: 291-302.
2. Billker, O., Dechamps, S., Tewari, R., Wenig, G., Franke-Fayard, B., and Brinkmann, V. (2004) Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117: 503-514.
3. Bruce, M.C., Alano, P., Duthie, S., and Carter, R. (1990) Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology 100 (Part 2):191-200.
4. Bruce, M.C., Carter, R.N., Nakamura, K., Aikawa, M., and Carter, R. (1994) Cellular location and temporal expression of the Plasmodium falciparum sexual stage antigen Pfs16. Mol Biochem Parasitol 65: 11-22.
5. Carter, R., and Graves, P. (1988) Gametocytes. In Malaria: Principles and Practice of Malariology. Wernsdorfer, W.H., and McGregor, I. (eds). Edinburgh: Churchill Livingstone, pp. 253-305.
6. Carter, R., Graves, P.M., Quakyi, I.A., and Good, M.F. (1989) Restricted or absent immune responses in human populations to Plasmodium falciparum gamete antigens that are targets of malaria transmission-blocking antibodies. J Exp Med 169: 135-147.
7. Dean, S., Marchetti, R., Kirk, K., and Matthews, K.R. (2009) A surface transporter family conveys the trypanosome differentiation signal. Nature 459: 213-217.
8. van Dijk, M.R., Janse, C.J., Thompson, J., Waters, A.P., Braks, J.A., Dodemont, H.J., etal. (2001) A central role for P48/45 in malaria parasite male gamete fertility. Cell 104: 153-164.
9. Dixon, M.W., Thompson, J., Gardiner, D.L., and Trenholme, K.R. (2008) Sex in Plasmodium: a sign of commitment. Trends Parasitol 24: 168-175.
10. Doerig, C., Baker, D., Billker, O., Blackman, M.J., Chitnis, C., Dhar Kumar, S., etal. (2009) Signalling in malaria parasites. The MALSIG consortium. Parasite 16: 169-182.
11. Dorin, D., Alano, P., Boccaccio, I., Ciceron, L., Doerig, C., Sulpice, R., and Parzy, D. (1999) An atypical mitogen-activated protein kinase (MAPK) homologue expressed in gametocytes of the human malaria parasite Plasmodium falciparum. Identification of a MAPK signature. J Biol Chem 274: 29912-29920.
12. Drakeley, C., Sutherland, C., Bousema, J.T., Sauerwein, R.W., and Targett, G.A. (2006) The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol 22: 424-430.
13. Eksi, S., Haile, Y., Furuya, T., Ma, L., Su, X., and Williamson, K.C. (2005) Identification of a subtelomeric gene family expressed during the asexual-sexual stage transition in Plasmodium falciparum. Mol Biochem Parasitol 143: 90-99.
14. Furuya, T., Mu, J., Hayton, K., Liu, A., Duan, J., Nkrumah, L., etal. (2005) Disruption of a Plasmodium falciparum gene linked to male sexual development causes early arrest in gametocytogenesis. Proc Natl Acad Sci USA 102: 16813-16818.
15. Gunther, K., Tummler, M., Arnold, H.H., Ridley, R., Goman, M., Scaife, J.G., and Lingelbach, K. (1991) An exported protein of Plasmodium falciparum is synthesized as an integral membrane protein. Mol Biochem Parasitol 46: 149-157.
16. 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.
17. Janse, C.J., and Waters, A.P. (1995) Plasmodium berghei: the application of cultivation and purification techniques to molecular studies of malaria parasites. Parasitol Today 11: 138-143.
18. Janse, C.J., Mons, B., Rouwenhorst, R.J., Van der Klooster, P.F., Overdulve, J.P., and Van der Kaay, H.J. (1985) In vitro formation of ookinetes and functional maturity of Plasmodium berghei gametocytes. Parasitology 91: 19-29.
19. Janse, C.J., van der Klooster, P.F., van der Kaay, H.J., van der Ploeg, M., and Overdulve, J.P. (1986) DNA synthesis in Plasmodium berghei during asexual and sexual development. Mol Biochem Parasitol 20: 173-182.
20. Janse, C.J., Franke-Fayard, B., and Waters, A.P. (2006a) Selection by flow-sorting of genetically transformed, GFP-expressing blood stages of the rodent malaria parasite, Plasmodium berghei. Nat Protoc 1: 614-623.
21. Janse, C.J., Franke-Fayard, B., Mair, G.R., Ramesar, J., Thiel, C., Engelmann, S., etal. (2006b) High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol Biochem Parasitol 145: 60-70.
22. Kappe, S.H., Gardner, M.J., Brown, S.M., Ross, J., Matuschewski, K., Ribeiro, J.M., etal. (2001) Exploring the transcriptome of the malaria sporozoite stage. Proc Natl Acad Sci USA 98: 9895-9900.
23. Kato, K., Sudo, A., Kobayashi, K., Sugi, T., Tohya, Y., and Akashi, H. (2009) Characterization of Plasmodium falciparum calcium-dependent protein kinase 4. Parasitol Int 58: 394-400.
24. Khan, S.M., Franke-Fayard, B., Mair, G.R., Lasonder, E., Janse, C.J., Mann, M., and Waters, A.P. (2005) Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 121: 675-687.
25. Kirk, K. (2004) Channels and transporters as drug targets in the Plasmodium-infected erythrocyte. Acta Trop 89: 285-298.
26. Kongkasuriyachai, D., Fujioka, H., and Kumar, N. (2004) Functional analysis of Plasmodium falciparum parasitophorous vacuole membrane protein (Pfs16) during gametocytogenesis and gametogenesis by targeted gene disruption. Mol Biochem Parasitol 133: 275-285.
27. Kooij, T.W., Carlton, J.M., Bidwell, S.L., Hall, N., Ramesar, J., Janse, C.J., and Waters, A.P. (2005) A Plasmodium whole-genome synteny map: indels and synteny breakpoints as foci for species-specific genes. PLoS Pathog 1: e44.
28. Lal, K., Delves, M.J., Bromley, E., Wastling, J.M., Tomley, F.M., and Sinden, R.E. (2009) Plasmodium male development gene-1 (mdv-1) is important for female sexual development and identifies a polarised plasma membrane during zygote development. Int J Parasitol 39: 755-761.
29. Lanfrancotti, A., Bertuccini, L., Silvestrini, F., and Alano, P. (2007) Plasmodium falciparum: mRNA co-expression and protein co-localisation of two gene products upregulated in early gametocytes. Exp Parasitol 116: 497-503.
30. Lasonder, E., Ishihama, Y., Andersen, J.S., Vermunt, A.M., Pain, A., Sauerwein, R.W., etal. (2002) Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 419: 537-542.
31. Lobo, C.A., and Kumar, N. (1998) Sexual differentiation and development in the malaria parasite. Parasitol Today 14: 146-150.
32. Lobo, C.A., Fujioka, H., Aikawa, M., and Kumar, N. (1999) Disruption of the Pfg27 locus by homologous recombination leads to loss of the sexual phenotype in P.falciparum. Mol Cell 3: 793-798.
33. McRobert, L., Taylor, C.J., Deng, W., Fivelman, Q.L., Cummings, R.M., Polley, S.D., etal. (2008) Gametogenesis in malaria parasites is mediated by the cGMP-dependent protein kinase. PLoS Biol 6: e139.
34. Mair, G.R., Braks, J.A., Garver, L.S., Wiegant, J.C., Hall, N., Dirks, R.W., etal. (2006) Regulation of sexual development of Plasmodium by translational repression. Science 313: 667-669.
35. Martin, R.E., Henry, R.I., Abbey, J.L., Clements, J.D., and Kirk, K. (2005) The 'permeome' of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol 6: R26.
36. Martin, R.E., Ginsburg, H., and Kirk, K. (2009) Membrane transport proteins of the malaria parasite. Mol Microbiol 74: 519-528.
37. Mons, B. (1986) Intra erythrocytic differentiation of Plasmodium berghei. Acta Leiden 54: 1-124.
38. Mons, B., Janse, C.J., Boorsma, E.G., and Van der Kaay, H.J. (1985) Synchronized erythrocytic schizogony and gametocytogenesis of Plasmodium berghei in vivo and in vitro. Parasitology 91: 423-430.
39. Natarajan, R., Thathy, V., Mota, M.M., Hafalla, J.C., Menard, R., and Vernick, K.D. (2001) Fluorescent Plasmodium berghei sporozoites and pre-erythrocytic stages: a new tool to study mosquito and mammalian host interactions with malaria parasites. Cell Microbiol 3: 371-379.
40. Olivieri, A., Camarda, G., Bertuccini, L., van de Vegte-Bolmer, M., Luty, A.J., Sauerwein, R., and Alano, P. (2009) The Plasmodium falciparum protein Pfg27 is dispensable for gametocyte and gamete production, but contributes to cell integrity during gametocytogenesis. Mol Microbiol 73: 180-193.
41. Pace, T., Olivieri, A., Sanchez, M., Albanesi, V., Picci, L., Siden Kiamos, I., etal. (2006) Set regulation in asexual and sexual Plasmodium parasites reveals a novel mechanism of stage-specific expression. Mol Microbiol 60: 870-882.
42. Pao, S.S., Paulsen, I.T., and Saier, M.H., Jr (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62: 1-34.
43. Paul, R.E., Coulson, T.N., Raibaud, A., and Brey, P.T. (2000) Sex determination in malaria parasites. Science 287: 128-131.
44. Ponzi, M., Siden-Kiamos, I., Bertuccini, L., Curra, C., Kroeze, H., Camarda, G., etal. (2009) Egress of Plasmodium berghei gametes from their host erythrocyte is mediated by the MDV-1/PEG3 protein. Cell Microbiol 11: 1272-1288.
45. Rangarajan, R., Bei, A.K., Jethwaney, D., Maldonado, P., Dorin, D., Sultan, A.A., and Doerig, C. (2005) A mitogen-activated protein kinase regulates male gametogenesis and transmission of the malaria parasite Plasmodium berghei. EMBO Rep 6: 464-469.
46. Saier, M.H., Jr, Beatty, J.T., Goffeau, A., Harley, K.T., Heijne, W.H., Huang, S.C., etal. (1999) The major facilitator superfamily. J Mol Microbiol Biotechnol 1: 257-279.
47. Sanchez, C.P., Dave, A., Stein, W.D., and Lanzer, M. (2010) Transporters as mediators of drug resistance in Plasmodium falciparum. Int J Parasitol 40: 1109-1118.
48. Siau, A., Silvie, O., Franetich, J.F., Yalaoui, S., Marinach, C., Hannoun, L., etal. (2008) Temperature shift and host cell contact up-regulate sporozoite expression of Plasmodium falciparum genes involved in hepatocyte infection. PLoS Pathog 4: e1000121.
49. Siden-Kiamos, I., Vlachou, D., Margos, G., Beetsma, A., Waters, A.P., Sinden, R.E., and Louis, C. (2000) Distinct roles for pbs21 and pbs25 in the in vitro ookinete to oocyst transformation of Plasmodium berghei. J Cell Sci 113 (Part 19): 3419-3426.
50. Silvestrini, F., Alano, P., and Williams, J.L. (2000) Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology 121 (Part 5):465-471.
51. Silvestrini, F., Bozdech, Z., Lanfrancotti, A., Di Giulio, E., Bultrini, E., Picci, L., etal. (2005) Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Mol Biochem Parasitol 143: 100-110.
52. Smith, T.G., Lourenco, P., Carter, R., Walliker, D., and Ranford-Cartwright, L.C. (2000) Commitment to sexual differentiation in the human malaria parasite, Plasmodium falciparum. Parasitology 121: 127-133.
53. Spaccapelo, R., Janse, C.J., Caterbi, S., Franke-Fayard, B., Bonilla, J.A., Syphard, L.M., etal. (2010) Plasmepsin 4-deficient Plasmodium berghei are virulence attenuated and induce protective immunity against experimental malaria. Am J Pathol 176: 205-217.
54. Staines, H.M., Derbyshire, E.T., Slavic, K., Tattersall, A., Vial, H., and Krishna, S. (2010) Exploiting the therapeutic potential of Plasmodium falciparum solute transporters. Trends Parasitol 26: 284-296.
55. Sturm, A., Graewe, S., Franke-Fayard, B., Retzlaff, S., Bolte, S., Roppenser, B., etal. (2009) Alteration of the parasite plasma membrane and the parasitophorous vacuole membrane during exo-erythrocytic development of malaria parasites. Protist 160: 51-63.
56. Talman, A.M., Domarle, O., McKenzie, F.E., Ariey, F., and Robert, V. (2004) Gametocytogenesis: the puberty of Plasmodium falciparum. Malar J 3: 24.
57. 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.
58. Taylor, C.J., McRobert, L., and Baker, D.A. (2008) Disruption of a Plasmodium falciparum cyclic nucleotide phosphodiesterase gene causes aberrant gametogenesis. Mol Microbiol 69: 110-118.
59. Thiberge, S., Blazquez, S., Baldacci, P., Renaud, O., Shorte, S., Menard, R., and Amino, R. (2007) In vivo imaging of malaria parasites in the murine liver. Nat Protoc 2: 1811-1818.
60. Thomson, D. (1914) The origin and development of gametes (crescents) in malignant tertian malaria: some observations on flagellation etc. Ann Trop Med Parasitol 8: 85-104.
61. 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.
62. WHO (2010) World Malaria Report. Geneva, Switzerland: World Health Organisation.
63. Young, J.A., Fivelman, Q.L., Blair, P.L., Vega, P., Le Roch, K.G., Zhou, Y., etal. (2005) The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol Biochem Parasitol 143: 67-79.
64. Young, J.A., Johnson, J.R., Benner, C., Yan, S.F., Chen, K., Le Roch, K.G., etal. (2008) In silico discovery of transcription regulatory elements in Plasmodium falciparum. BMC Genomics 9: 70.