Experimentally controlled downregulation of the histone chaperone FACT in Plasmodium berghei reveals that it is critical to male gamete fertility

Cellular Microbiology

Volumn 13, Issue 12, 2011, Pages 1956-1974

  Laurentino, Eliane C ^a   Taylor, Sonya ^b   Mair, Gunnar R ^a,c   Lasonder, Edwin ^d   Bartfai, Richard ^e   Stunnenberg, Hendrik G ^e   Kroeze, Hans ^a   Ramesar, Jai ^a   Franke Fayard, Blandine ^a   Khan, Shahid M ^a   Janse, Chris J ^a   Waters, Andrew P ^b  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; PROTEIN FACILITATES CHROMATIN TRANSCRIPTION; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; DNA BINDING; DNA REPLICATION; DOWN REGULATION; EXPERIMENTAL STUDY; FEMALE; FEMALE FERTILITY; GAMETE; GAMETOCYTE; GAMETOGENESIS; MALE FERTILITY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; OOCYST; OOKINETE; PLASMODIUM BERGHEI; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; ZYGOTE;

ANIMALS; ANOPHELES; CELL NUCLEUS; DNA REPLICATION; DNA, PROTOZOAN; DNA-BINDING PROTEINS; DOWN-REGULATION; EPITOPE MAPPING; FEMALE; FERTILITY; FLAGELLA; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENETIC VECTORS; GERM CELLS; HISTONE CHAPERONES; MICE; OOCYSTS; PLASMODIUM BERGHEI; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; PROTOZOAN PROTEINS; TRANSCRIPTION, GENETIC;

PLASMODIUM BERGHEI;

EID: 81355146458     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01683.x     Document Type: Article

References (62)

1. Balaji, S., Babu, M.M., Iyer, L.M., and Aravind, L. (2005) Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res 33: 3994-4006.
2. Beetsma, A.L., van de Wiel, T.J., Sauerwein, R.W., and Eling, W.M. (1998) Plasmodium berghei ANKA: purification of large numbers of infectious gametocytes. Exp Parasitol 88: 69-72.
3. Belotserkovskaya, R., Oh, S., Bondarenko, V.A., Orphanides, G., Studitsky, V.M., and Reinberg, D. (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090-1093.
4. Bischoff, E., and Vaquero, C. (2010) In silico and biological survey of transcription-associated proteins implicated in the transcriptional machinery during the erythrocytic development of Plasmodium falciparum. BMC Genomics 11: 34.
5. Biswas, D., Yu, Y., Prall, M., Formosa, T., and Stillman, D.J. (2005) The yeast FACT complex has a role in transcriptional initiation. Mol Cell Biol 25: 5812-5822.
6. Briquet, S., Boschet, C., Gissot, M., Tissandie, E., Sevilla, E., Franetich, J.F., etal. (2006) High-mobility-group box nuclear factors of Plasmodium falciparum. Eukaryot Cell 5: 672-682.
7. Chaal, B.K., Gupta, A.P., Wastuwidyaningtyas, B.D., Luah, Y.H., and Bozdech, Z. (2010) Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle. PLoS Pathog 6: e1000737.
8. Cui, L., and Miao, J. (2010) Chromatin-mediated epigenetic regulation in the malaria parasite Plasmodium falciparum. Eukaryot Cell 9: 1138-1149.
9. De Silva, E.K., Gehrke, A.R., Olszewski, K., Leon, I., Chahal, J.S., Bulyk, M.L., and Llinas, M. (2008) Specific DNA-binding by apicomplexan AP2 transcription factors. Proc Natl Acad Sci USA 105: 8393-8398.
10. 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.
11. van Dijk, M.R., van Schaijk, B.C., Khan, S.M., van Dooren, M.W., Ramesar, J., Kaczanowski, S., etal. (2010) Three members of the 6-cys protein family of Plasmodium play a role in gamete fertility. PLoS Pathog 6: e1000853.
12. Eitoku, M., Sato, L., Senda, T., and Horikoshi, M. (2008) Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell Mol Life Sci 65: 414-444.
13. Florens, L., Washburn, M.P., Raine, J.D., Anthony, R.M., Grainger, M., Haynes, J.D., etal. (2002) A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520-526.
14. Florens, L., Liu, X., Wang, Y., Yang, S., Schwartz, O., Peglar, M., etal. (2004) Proteomics approach reveals novel proteins on the surface of malaria-infected erythrocytes. Mol Biochem Parasitol 135: 1-11.
15. Formosa, T., Ruone, S., Adams, M.D., Olsen, A.E., Eriksson, P., Yu, Y., etal. (2002) Defects in SPT16 or POB3 (yFACT) in Saccharomyces cerevisiae cause dependence on the Hir/Hpc pathway: polymerase passage may degrade chromatin structure. Genetics 162: 1557-1571.
16. Gambus, A., Jones, R.C., Sanchez-Diaz, A., Kanemaki, M., van Deursen, F., Edmondson, R.D., and Labib, K. (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8: 358-366.
17. Gardner, M.J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., etal. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
18. Gill, J., Yogavel, M., Kumar, A., Belrhali, H., Jain, S.K., Rug, M., etal. (2009) Crystal structure of malaria parasite nucleosome assembly protein: distinct modes of protein localization and histone recognition. J Biol Chem 284: 10076-10087.
19. Gill, J., Kumar, A., Yogavel, M., Belrhali, H., Jain, S.K., Rug, M., etal. (2010) Structure, localization and histone binding properties of nuclear-associated nucleosome assembly protein from Plasmodium falciparum. Malar J 9: 90.
20. Gissot, M., Ting, L.M., Daly, T.M., Bergman, L.W., Sinnis, P., and Kim, K. (2008) High mobility group protein HMGB2 is a critical regulator of plasmodium oocyst development. J Biol Chem 283: 17030-17038.
21. Hall, N., Karras, M., Raine, J.D., Carlton, J.M., Kooij, T.W., Berriman, M., etal. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307: 82-86.
22. Hertel, L., De Andrea, M., Bellomo, G., Santoro, P., Landolfo, S., and Gariglio, M. (1999) The HMG protein T160 colocalizes with DNA replication foci and is down-regulated during cell differentiation. Exp Cell Res 250: 313-328.
23. 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.
24. Janse, C., and Waters, A.P. (2004) Sexual development of malaria parasites. In Malaria Parasites: Genomes and Molecular Biology. Waters, A.P., and Janse, C.J. (eds). Norwich: Horizon Scientific Press, pp. 445-474.
25. Janse, C.J., and Van Vianen, P.H. (1994) Flow cytometry in malaria detection. Methods Cell Biol 42 (Part B): 295-318.
26. 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 (Part 1): 19-29.
27. Janse, C.J., van Vianen, P.H., Tanke, H.J., Mons, B., Ponnudurai, T., and Overdulve, J.P. (1987) Plasmodium species: flow cytometry and microfluorometry assessments of DNA content and synthesis. Exp Parasitol 64: 88-94.
28. Janse, C.J., Ramesar, J., and Waters, A.P. (2006a) High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 1: 346-356.
29. 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.
30. Jiang, L., Lopez-Barragan, M.J., Jiang, H., Mu, J., Gaur, D., Zhao, K., etal. (2010) Epigenetic control of the variable expression of a Plasmodium falciparum receptor protein for erythrocyte invasion. Proc Natl Acad Sci USA 107: 2224-2229.
31. 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.
32. Kooij, T.W., Janse, C.J., and Waters, A.P. (2006) Plasmodium post-genomics: better the bug you know? Nat Rev Microbiol 4: 344-357.
33. Kumar, K., Singal, A., Rizvi, M.M., and Chauhan, V.S. (2008) High mobility group box (HMGB) proteins of Plasmodium falciparum: DNA binding proteins with pro-inflammatory activity. Parasitol Int 57: 150-157.
34. Lanzer, M., Wertheimer, S.P., de Bruin, D., and Ravetch, J.V. (1994) Chromatin structure determines the sites of chromosome breakages in Plasmodium falciparum. Nucleic Acids Res 22: 3099-3103.
35. 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.
36. Le Roch, K.G., Zhou, Y., Blair, P.L., Grainger, M., Moch, J.K., Haynes, J.D., etal. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508.
37. Maiorano, D., Lutzmann, M., and Mechali, M. (2006) MCM proteins and DNA replication. Curr Opin Cell Biol 18: 130-136.
38. 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.
39. Mair, G.R., Lasonder, E., Garver, L.S., Franke-Fayard, B.M., Carret, C.K., Wiegant, J.C., etal. (2010) Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog 6: e1000767.
40. Menard, R., and Janse, C. (1997) Gene targeting in malaria parasites. Methods 13: 148-157.
41. Miller, D., Brinkworth, M., and Iles, D. (2010) Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 139: 287-301.
42. Navadgi, V.M., Chandra, B.R., Mishra, P.C., and Sharma, A. (2006) The two Plasmodium falciparum nucleosome assembly proteins play distinct roles in histone transport and chromatin assembly. J Biol Chem 281: 16978-16984.
43. Okuhara, K., Ohta, K., Seo, H., Shioda, M., Yamada, T., Tanaka, Y., etal. (1999) A DNA unwinding factor involved in DNA replication in cell-free extracts of Xenopus eggs. Curr Biol 9: 341-350.
44. 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.
45. 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.
46. Puri, D., Dhawan, J., and Mishra, R.K. (2010) The paternal hidden agenda: epigenetic inheritance through sperm chromatin. Epigenetics 5: 386-391.
47. Ransom, M., Dennehey, B.K., and Tyler, J.K. (2010) Chaperoning histones during DNA replication and repair. Cell 140: 183-195.
48. Reininger, L., Billker, O., Tewari, R., Mukhopadhyay, A., Fennell, C., Dorin-Semblat, D., etal. (2005) A NIMA-related protein kinase is essential for completion of the sexual cycle of malaria parasites. J Biol Chem 280: 31957-31964.
49. Reininger, L., Tewari, R., Fennell, C., Holland, Z., Goldring, D., Ranford-Cartwright, L., etal. (2009) An essential role for the Plasmodium Nek-2 Nima-related protein kinase in the sexual development of malaria parasites. J Biol Chem 284: 20858-20868.
50. Schlesinger, M.B., and Formosa, T. (2000) POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics 155: 1593-1606.
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. Sinden, R.E. (1997) Infection of mosquitoes with rodent malaria. In The Molecular Biology of Insect Disease Vectors: A Methods Manual. Crampton, J.M. (ed.). London: Chapman and Hall, pp. 67-92.
53. Sotolongo, B., Lino, E., and Ward, W.S. (2003) Ability of hamster spermatozoa to digest their own DNA. Biol Reprod 69: 2029-2035.
54. van Spaendonk, R.M., Ramesar, J., van Wigcheren, A., Eling, W., Beetsma, A.L., van Gemert, G.J., etal. (2001) Functional equivalence of structurally distinct ribosomes in the malaria parasite, Plasmodium berghei. J Biol Chem 276: 22638-22647.
55. Tan, B.C., Chien, C.T., Hirose, S., and Lee, S.C. (2006) Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J 25: 3975-3985.
56. Tewari, R., Dorin, D., Moon, R., Doerig, C., and Billker, O. (2005) An atypical mitogen-activated protein kinase controls cytokinesis and flagellar motility during male gamete formation in a malaria parasite. Mol Microbiol 58: 1253-1263.
57. Westenberger, S.J., Cui, L., Dharia, N., and Winzeler, E. (2009) Genome-wide nucleosome mapping of Plasmodium falciparum reveals histone-rich coding and histone-poor intergenic regions and chromatin remodeling of core and subtelomeric genes. BMC Genomics 10: 610.
58. Wickham, M.E., Rug, M., Ralph, S.A., Klonis, N., McFadden, G.I., Tilley, L., and Cowman, A.F. (2001) Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J 20: 5636-5649.
59. Wittmeyer, J., and Formosa, T. (1997) The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol Cell Biol 17: 4178-4190.
60. Xin, H., Takahata, S., Blanksma, M., McCullough, L., Stillman, D.J., and Formosa, T. (2009) yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol Cell 35: 365-376.
61. Yuda, M., Iwanaga, S., Shigenobu, S., Mair, G.R., Janse, C.J., Waters, A.P., etal. (2009) Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Mol Microbiol 71: 1402-1414.
62. Yuda, M., Iwanaga, S., Shigenobu, S., Kato, T., and Kaneko, I. (2010) Transcription factor AP2-Sp and its target genes in malarial sporozoites. Mol Microbiol 75: 854-863.