The MYST family histone acetyltransferase regulates gene expression and cell cycle in malaria parasite Plasmodium falciparum

Molecular Microbiology

Volumn 78, Issue 4, 2010, Pages 883-902

  Miao, Jun ^a   Fan, Qi ^a   Cui, Long ^a   Li, Xiaolian ^a   Wang, Haiyan ^b   Ning, Gang ^c   Reese, Joseph C ^a   Cui, Liwang ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b KANSAS STATE UNIVERSITY   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE H4; PLASMODIUM FALCIPARUM MYST PROTEIN; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL GROWTH; CHEMOSENSITIVITY; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME LOCALIZATION; ERYTHROCYTE; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INSECT CELL; NONHUMAN; NUCLEUS ACCUMBENS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROKARYOTE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ACETYLATION; CELL CYCLE; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION REGULATION; GENES, ESSENTIAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HISTONE ACETYLTRANSFERASES; HISTONES; LYSINE; MICROSCOPY, FLUORESCENCE; MUTAGENESIS, INSERTIONAL; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS;

HEXAPODA; PLASMODIUM FALCIPARUM; PROKARYOTA;

EID: 78349297215     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07371.x     Document Type: Article

References (77)

1. Adachi, N., Kimura, A., and Horikoshi, M. (2002) A conserved motif common to the histone acetyltransferase Esa1 and the histone deacetylase Rpd3. J Biol Chem 277: 35688-35695.
2. Akhtar, A., and Becker, P.B. (2001) The histone H4 acetyltransferase MOF uses a C2HC zinc finger for substrate recognition. EMBO Reports 2: 113-118.
3. Akhtar, A., Zink, D., and Becker, P.B. (2000) Chromodomains are protein-RNA interaction modules. Nature 407: 405-409.
4. Alkhalil, A., Achur, R.N., Valiyaveettil, M., Ockenhouse, C.F., and Gowda, D.C. (2000) Structural requirements for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate proteoglycans of human placenta. J Biol Chem 275: 40357-40364.
5. Andrews, K.T., Walduck, A., Kelso, M.J., Fairlie, D.P., Saul, A., and Parsons, P.G. (2000) Anti-malarial effect of histone deacetylation inhibitors and mammalian tumour cytodifferentiating agents. Int J Parasitol 30: 761-768.
6. Andrews, K.T., Tran, T.N., Lucke, A.J., Kahnberg, P., Le, G.T., Boyle, G.M., et al. (2008) Potent antimalarial activity of histone deacetylase inhibitor analogues. Antimicrol Agents Chemother 52: 1454-1461.
7. Bird, A.W., Yu, D.Y., Pray-Grant, M.G., Qiu, Q., Harmon, K.E., Megee, P.C., et al. (2002) Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419: 411-415.
8. Borrow, J., Stanton, V.P., Jr, Andresen, J.M., Becher, R., Behm, F.G., Chaganti, R.S., et al. (1996) The translocation t(8;16)(p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB-binding protein. Nat Genet 14: 33-41.
9. Carrozza, M.J., Utley, R.T., Workman, J.L., and Cote, J. (2003) The diverse functions of histone acetyltransferase complexes. Trends Genet 19: 321-329.
10. 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.
11. Clarke, A.S., Lowell, J.E., Jacobson, S.J., and Pillus, L. (1999) Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol Cell Biol 19: 2515-2526.
12. Cole, P.A. (2008) Chemical probes for histone-modifying enzymes. Nat Chem Biol 4: 590-597.
13. Crabb, B.S., and Cowman, A.F. (1996) Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum. Proc Natl Acad Sci USA 93: 7289-7294.
14. Cui, L., Miao, J., and Cui, L. (2007a) Cytotoxic effect of curcumin on malaria parasite Plasmodium falciparum: inhibition of histone acetylation and generation of reactive oxygen species. Antimicrob Agents Chemother 51: 488-494.
15. Cui, L., Miao, J., Furuya, T., Li, X., Su, X.Z., and Cui, L. (2007b) PfGCN5-mediated histone H3 acetylation plays a key role in gene expression in Plasmodium falciparum. Eukaryot Cell 6: 1219-1227.
16. Cui, L., Miao, J., Furuya, T., Fan, Q., Li, X., Rathod, P.K., et al. (2008a) Histone acetyltransferase inhibitor anacardic acid causes changes in global gene expression during in vitro Plasmodium falciparum development. Eukaryot Cell 7: 1200-1210.
17. Cui, L., Fan, Q., Cui, L., and Miao, J. (2008b) Histone lysine methyltransferases and demethylases in Plasmodium falciparum. Int J Parasitol 38: 1083-1097.
18. Darkin-Rattray, S.J., Gurnett, A.M., Myers, R.W., Dulski, P.M., Crumley, T.M., Allocco, J.J., et al. (1996) Apicidin: a novel antiprotozoal agent that inhibits parasites histone deacetylase. Proc Natl Acad Sci USA 93: 13143-13147.
19. Deitsch, K., Driskill, C., and Wellems, T. (2001) Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res 29: 850-853.
20. Duraisingh, M.T., Voss, T.S., Marty, A.J., Duffy, M.F., Good, R.T., Thompson, J.K., et al. (2005) Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121: 13-24.
21. Fan, Q., An, L., and Cui, L. (2004) Plasmodium falciparum histone acetyltransferase, a yeast GCN5 homologue involved in chromatin remodeling. Eukaryot cell 3: 264-276.
22. Fan, Q., Miao, J., Cui, L., and Cui, L. (2009) Characterization of PRMT1 from Plasmodium falciparum. Biochem J 421: 107-118.
23. Fidock, D.A., and Wellems, T.E. (1997) Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Proc Natl Acad Sci USA 94: 10931-10936.
24. Flueck, C., Bartfai, R., Volz, J., Niederwieser, I., Salcedo-Amaya, A.M., Alako, B.T., et al. (2009) Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors. PLoS Pathog 5: e1000569.
25. Forler, D., Kocher, T., Rode, M., Gentzel, M., Izaurralde, E., and Wilm, M. (2003) An efficient protein complex purification method for functional proteomics in higher eukaryotes. Nat Biotechnol 21: 89-92.
26. Freitas-Junior, L.H., Hernandez-Rivas, R., Ralph, S.A., Montiel-Condado, D., Ruvalcaba-Salazar, O.K., Rojas-Meza, A.P., et al. (2005) Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121: 25-36.
27. Gelb, M.H. (2007) Drug discovery for malaria: a very challenging and timely endeavor. Currt Opin Chem Biol 11: 440-445.
28. Gomez, E.B., Nugent, R.L., Laria, S., and Forsburg, S.L. (2008) Schizosaccharomyces pombe histone acetyltransferase Mst1 (KAT5) is an essential protein required for damage response and chromosome segregation. Genetics 179: 757-771.
29. Ikura, T., Ogryzko, V.V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M., et al. (2000) Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102: 463-473.
30. Inselburg, J., and Banyal, H.S. (1984) Synthesis of DNA during the asexual cycle of Plasmodium falciparum in culture. Mol Biochem Parasitol 10: 79-87.
31. John, S., Howe, L., Tafrov, S.T., Grant, P.A., Sternglanz, R., and Workman, J.L. (2000) The something about silencing protein, Sas3, is the catalytic subunit of NuA3, a yTAF(II)30-containing HAT complex that interacts with the Spt16 subunit of the yeast CP (Cdc68/Pob3)-FACT complex. Genes Dev 14: 1196-1208.
32. Kamine, J., Elangovan, B., Subramanian, T., Coleman, D., and Chinnadurai, G. (1996) Identification of a cellular protein that specifically interacts with the essential cysteine region of the HIV-1 Tat transactivator. Virology 216: 357-366.
33. Kawahara, T., Siegel, T.N., Ingram, A.K., Alsford, S., Cross, G.A., and Horn, D. (2008) Two essential MYST-family proteins display distinct roles in histone H4K10 acetylation and telomeric silencing in trypanosomes. Mol Microbiol 69: 1054-1068.
34. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128: 693-705.
35. Kyes, S., Pinches, R., and Newbold, C. (2000) A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol Biochem Parasitol 105: 311-315.
36. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., and Jenuwein, T. (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120.
37. Lafon, A., Chang, C.S., Scott, E.M., Jacobson, S.J., and Pillus, L. (2007) MYST opportunities for growth control: yeast genes illuminate human cancer gene functions. Oncogene 26: 5373-5384.
38. Lambros, C., and Vanderberg, J.P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
39. Le Roch, K.G., Zhou, Y., Blair, P.L., Grainger, M., Moch, J.K., Haynes, J.D., et al. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508.
40. Lee, K.K., and Workman, J.L. (2007) Histone acetyltransferase complexes: one size doesn't fit all. Nat Rev 8: 284-295.
41. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
42. Lopez-Rubio, J.J., Gontijo, A.M., Nunes, M.C., Issar, N., Hernandez Rivas, R., and Scherf, A. (2007) 5' flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Mol Microbiol 66: 1296-1305.
43. Maier, A.G., Braks, J.A., Waters, A.P., and Cowman, A.F. (2006) Negative selection using yeast cytosine deaminase/uracil phosphoribosyl transferase in Plasmodium falciparum for targeted gene deletion by double crossover recombination. Mol Biochem Parasitol 150: 118-121.
44. Megee, P.C., Morgan, B.A., and Smith, M.M. (1995) Histone H4 and the maintenance of genome integrity. Gene Dev 9: 1716-1727.
45. Merrick, C.J., and Duraisingh, M.T. (2007) Plasmodium falciparum Sir2: an unusual sirtuin with dual histone deacetylase and ADP-ribosyltransferase activity. Eukaryot Cell 6: 2081-2091.
46. Miao, J., Fan, Q., Cui, L., Li, J., and Cui, L. (2006) The malaria parasite Plasmodium falciparum histones: organization, expression, and acetylation. Gene 369: 53-65.
47. Miao, J., Li, X.L., and Cui, L. (2010) Cloning of Plasmodium falciparum by single-cell sorting. Exp Parasitol 126: 198-202.
48. Min, J., Zhang, Y., and Xu, R.M. (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Gene Dev 17: 1823-1828.
49. Murr, R., Loizou, J.I., Yang, Y.G., Cuenin, C., Li, H., Wang, Z.Q., et al. (2006) Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 8: 91-99.
50. Nkrumah, L.J., Muhle, R.A., Moura, P.A., Ghosh, P., Hatfull, G.F., Jacobs, W.R., Jr, et al. (2006) Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat Methods 3: 615-621.
51. Perez-Toledo, K., Rojas-Meza, A.P., Mancio-Silva, L., Hernandez-Cuevas, N.A., Delgadillo, D.M., Vargas, M., et al. (2009) Plasmodium falciparum heterochromatin protein 1 binds to tri-methylated histone 3 lysine 9 and is linked to mutually exclusive expression of var genes. Nucleic Acids Res 37: 2596-2606.
52. Pillus, L. (2008) MYSTs mark chromatin for chromosomal functions. Curr Opin Cell Biol 20: 326-333.
53. Puig, O., Caspary, F., Rigaut, G., Rutz, B., Bouveret, E., Bragado-Nilsson, E., et al. (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24: 218-229.
54. Reifsnyder, C., Lowell, J., Clarke, A., and Pillus, L. (1996) Yeast SAS silencing genes and human genes associated with AML and HIV-1 Tat interactions are homologous with acetyltransferases. Nat Genet 14: 42-49.
55. Reilly, H.B., Wang, H., Steuter, J.A., Marx, A.M., and Ferdig, M.T. (2007) Quantitative dissection of clone-specific growth rates in cultured malaria parasites. Int J Parasitol 37: 1599-1607.
56. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Seraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030-1032.
57. Salanti, A., Staalsoe, T., Lavstsen, T., Jensen, A.T., Sowa, M.P., Arnot, D.E., et al. (2003) Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol 49: 179-191.
58. Selleck, W., Fortin, I., Sermwittayawong, D., Cote, J., and Tan, S. (2005) The Saccharomyces cerevisiae Piccolo NuA4 histone acetyltransferase complex requires the enhancer of Polycomb A domain and chromodomain to acetylate nucleosomes. Mol Cell Biol 25: 5535-5542.
59. Shia, W.J., Osada, S., Florens, L., Swanson, S.K., Washburn, M.P., and Workman, J.L. (2005) Characterization of the yeast trimeric-SAS acetyltransferase complex. J Biol Chem 280: 11987-11994.
60. Siegel, T.N., Kawahara, T., Degrasse, J.A., Janzen, C.J., Horn, D., and Cross, G.A. (2008) Acetylation of histone H4K4 is cell cycle regulated and mediated by HAT3 in Trypanosoma brucei. Mol Microbiol 67: 762-771.
61. Smilkstein, M., Sriwilaijaroen, N., Kelly, J.X., Wilairat, P., and Riscoe, M. (2004) Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob Agents Chemother 48: 1803-1806.
62. Smith, E.R., Eisen, A., Gu, W., Sattah, M., Pannuti, A., Zhou, J., et al. (1998) ESA1 is a histone acetyltransferase that is essential for growth in yeast. Proc Natl Acad Sci USA 95: 3561-3565.
63. Smith, A.T., Tucker-Samaras, S.D., Fairlamb, A.H., and Sullivan, W.J., Jr (2005) MYST family histone acetyltransferases in the protozoan parasite Toxoplasma gondii. Eukaryot Cell 4: 2057-2065.
64. Sutton, A., Shia, W.J., Band, D., Kaufman, P.D., Osada, S., Workman, J.L., and Sternglanz, R. (2003) Sas4 and Sas5 are required for the histone acetyltransferase activity of Sas2 in the SAS complex. J Biol Chem 278: 16887-16892.
65. Takechi, S., and Nakayama, T. (1999) Sas3 is a histone acetyltransferase and requires a zinc finger motif. Biochem Biophys Res Commun 266: 405-410.
66. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
67. Thomas, T., and Voss, A.K. (2007) The diverse biological roles of MYST histone acetyltransferase family proteins. Cell Cycle 6: 696-704.
68. Tonkin, C.J., Van Dooren, G.G., Spurck, T.P., Struck, N.S., Good, R.T., Handman, E., et al. (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.
69. Tonkin, C.J., Carret, C.K., Duraisingh, M.T., Voss, T.S., Ralph, S.A., Hommel, M., et al. (2009) Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol 7: e84.
70. Trager, W., and Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
71. Trelle, M.B., Salcedo-Amaya, A.M., Cohen, A.M., Stunnenberg, H.G., and Jensen, O.N. (2009) Global histone analysis by mass spectrometry reveals a high content of acetylated lysine residues in the malaria parasite Plasmodium falciparum. J Proteome Res 8: 3439-3450.
72. 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.
73. Utley, R.T., and Cote, J. (2003) The MYST family of histone acetyltransferases. Curr Top Microbiol Immunol 274: 203-236.
74. Vonlaufen, N., Naguleswaran, A., Coppens, I., and Sullivan, W.J., Jr (2010) MYST family lysine acetyltransferase facilitates ataxia telangiectasia mutated (ATM) kinase-mediated DNA damage response in Toxoplasma gondii. J Biol Chem 285: 11154-11161.
75. Westenberger, S.J., Cui, L., Dharia, N., Winzeler, E., and Cui, L. (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: e610.
76. Winzeler, E.A. (2008) Malaria research in the post-genomic era. Nature 455: 751-756.
77. Yang, X.J. (2004) The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res 32: 959-976.