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PMID: 20453074 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Chromatin-mediated epigenetic regulation in the malaria parasite Plasmodium falciparum.

Eukaryotic cell ·Vol. 9 ·No. 8 ·2010-08-00 ·Pages 1138-49

Cui L, Miao J

Abstract

Malaria is a major public health problem in many developing countries, with the malignant tertian parasite Plasmodium falciparum causing the most malaria-associated mortality. Extensive research, especially with the advancement of genomics and transfection tools, has highlighted the fundamental importance of chromatin-mediated gene regulation in the developmental program of this early-branching eukaryote. The Plasmodium parasite genomes reveal the existence of both canonical and variant histones that make up the nucleosomes, as well as a full collection of conserved enzymes for chromatin remodeling and histone posttranslational modifications (PTMs). Recent studies have identified a wide array of both conserved and novel histone PTMs in P. falciparum, indicating the presence of a complex and divergent "histone code." Genome-wide analysis has begun to decipher the nucleosome landscape and histone modifications associated with the dynamic organization of chromatin structures during the parasite's life cycle. Focused studies on malaria-specific phenomena such as antigenic variation and red cell invasion pathways shed further light on the involvement of epigenetic mechanisms in these processes. Here we review our current understanding of chromatin-mediated gene regulation in malaria parasites, with specific reference to exemplar studies on antigenic variation and host cell invasion.

MeSH Terms
Chromatin/metabolism Epigenesis, Genetic Histones/metabolism Malaria, Falciparum/parasitology Models, Genetic Plasmodium falciparum/genetics,growth & development
Chemicals
Chromatin Histones
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Cui Liwang
Department of Entomology, Pennsylvania State University, 501 ASI Bldg., University Park, PA 16802, USA. [email protected]
Miao Jun
References (157)
157 references, click to expand
  1. Chromatin modifications and their function.
    Cell. 2007 Feb 23;128(4):693-705 PMID: 17320507
  2. Activation, silencing and mutually exclusive expression within the var gene family of Plasmodium falciparum.
    Int J Parasitol. 2006 Aug;36(9):975-85 PMID: 16797552
  3. Active transcription is required for maintenance of epigenetic memory in the malaria parasite Plasmodium falciparum.
    J Mol Biol. 2008 Oct 3;382(2):288-97 PMID: 18656490
  4. A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria.
    Nature. 2006 Feb 23;439(7079):1004-8 PMID: 16382237
  5. Epigenomic modifications predict active promoters and gene structure in Toxoplasma gondii.
    PLoS Pathog. 2007 Jun;3(6):e77 PMID: 17559302
  6. Specific DNA-binding by apicomplexan AP2 transcription factors.
    Proc Natl Acad Sci U S A. 2008 Jun 17;105(24):8393-8 PMID: 18541913
  7. Toxoplasma H2A variants reveal novel insights into nucleosome composition and functions for this histone family.
    J Mol Biol. 2009 Sep 11;392(1):33-47 PMID: 19607843
  8. Identification by functional proteomics of a deubiquitinating/deNeddylating enzyme in Plasmodium falciparum.
    Mol Microbiol. 2006 Sep;61(5):1187-95 PMID: 16925553
  9. Hypervariability within the Rifin, Stevor and Pfmc-2TM superfamilies in Plasmodium falciparum.
    Nucleic Acids Res. 2006;34(22):6696-707 PMID: 17148488
  10. Variable switching rates of malaria virulence genes are associated with chromosomal position.
    Mol Microbiol. 2007 Jun;64(6):1486-98 PMID: 17555435
  11. Potential epigenetic regulatory proteins localise to distinct nuclear sub-compartments in Plasmodium falciparum.
    Int J Parasitol. 2010 Jan;40(1):109-21 PMID: 19765590
  12. Differential sub-nuclear localisation of repressive and activating histone methyl modifications in P. falciparum.
    Microbes Infect. 2009 Mar;11(3):403-7 PMID: 19136073
  13. Global patterns of histone modifications.
    Curr Opin Genet Dev. 2007 Apr;17(2):94-9 PMID: 17317148
  14. Antigenic variation in Plasmodium falciparum.
    Annu Rev Microbiol. 2008;62:445-70 PMID: 18785843
  15. Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites.
    EMBO Rep. 2007 Oct;8(10):959-65 PMID: 17762879
  16. Variant proteins of the Plasmodium falciparum RIFIN family show distinct subcellular localization and developmental expression patterns.
    Mol Biochem Parasitol. 2007 Nov;156(1):51-61 PMID: 17719658
  17. Translating the histone code.
    Science. 2001 Aug 10;293(5532):1074-80 PMID: 11498575
  18. Heterochromatin-mediated control of virulence gene expression.
    Mol Microbiol. 2006 Nov;62(3):612-20 PMID: 17076663
  19. Simultaneous transcription of duplicated var2csa gene copies in individual Plasmodium falciparum parasites.
    Genome Biol. 2009;10(10):R117 PMID: 19849836
  20. Chromatin associated sense and antisense noncoding RNAs are transcribed from the var gene family of virulence genes of the malaria parasite Plasmodium falciparum.
    RNA. 2009 Jan;15(1):116-27 PMID: 19037012
  21. Plasmodium falciparum histone acetyltransferase, a yeast GCN5 homologue involved in chromatin remodeling.
    Eukaryot Cell. 2004 Apr;3(2):264-76 PMID: 15075257
  22. Patterning chromatin: form and function for H2A.Z variant nucleosomes.
    Curr Opin Genet Dev. 2006 Apr;16(2):119-24 PMID: 16503125
  23. Mutually exclusive var gene expression in the malaria parasite: multiple layers of regulation.
    Trends Parasitol. 2008 Oct;24(10):455-61 PMID: 18771955
  24. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites.
    Cell. 2005 Apr 8;121(1):25-36 PMID: 15820676
  25. Selective di- or trimethylation of histone H3 lysine 76 by two DOT1 homologs is important for cell cycle regulation in Trypanosoma brucei.
    Mol Cell. 2006 Aug;23(4):497-507 PMID: 16916638
  26. Discovery of gene function by expression profiling of the malaria parasite life cycle.
    Science. 2003 Sep 12;301(5639):1503-8 PMID: 12893887
  27. Evidence that Plasmodium falciparum chromosome end clusters are cross-linked by protein and are the sites of both virulence gene silencing and activation.
    Mol Microbiol. 2006 Oct;62(1):72-83 PMID: 16942599
  28. Variant antigen gene expression in malaria.
    Cell Microbiol. 2006 Sep;8(9):1371-81 PMID: 16848786
  29. Cytotoxic effect of curcumin on malaria parasite Plasmodium falciparum: inhibition of histone acetylation and generation of reactive oxygen species.
    Antimicrob Agents Chemother. 2007 Feb;51(2):488-94 PMID: 17145789
  30. A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology.
    PLoS Pathog. 2010 Feb 26;6(2):e1000784 PMID: 20195509
  31. Identification of a novel post-translational modification in Plasmodium falciparum: protein sumoylation in different cellular compartments.
    Cell Microbiol. 2008 Oct;10(10):1999-2011 PMID: 18547337
  32. Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9333-8 PMID: 10430943
  33. Histone acetyltransferase complexes: one size doesn't fit all.
    Nat Rev Mol Cell Biol. 2007 Apr;8(4):284-95 PMID: 17380162
  34. Histone acetyltransferase inhibitor anacardic acid causes changes in global gene expression during in vitro Plasmodium falciparum development.
    Eukaryot Cell. 2008 Jul;7(7):1200-10 PMID: 18487348
  35. Plasmodium falciparum Sir2: an unusual sirtuin with dual histone deacetylase and ADP-ribosyltransferase activity.
    Eukaryot Cell. 2007 Nov;6(11):2081-91 PMID: 17827348
  36. Histone ubiquitination: triggering gene activity.
    Mol Cell. 2008 Mar 28;29(6):653-63 PMID: 18374642
  37. Drug inhibition of HDAC3 and epigenetic control of differentiation in Apicomplexa parasites.
    J Exp Med. 2009 Apr 13;206(4):953-66 PMID: 19349466
  38. Malaria. Cooperative silencing elements in var genes.
    Nature. 2001 Aug 30;412(6850):875-6 PMID: 11528468
  39. Genomic organisation and chromatin structure of Plasmodium falciparum chromosome ends.
    Mol Biochem Parasitol. 2000 Feb 25;106(1):169-74 PMID: 10743621
  40. Control of transcription through intragenic patterns of nucleosome composition.
    Cell. 2005 Dec 29;123(7):1187-90 PMID: 16377560
  41. Identification of a transcription factor in the mosquito-invasive stage of malaria parasites.
    Mol Microbiol. 2009 Mar;71(6):1402-14 PMID: 19220746
  42. Evidence for nucleosome depletion at active regulatory regions genome-wide.
    Nat Genet. 2004 Aug;36(8):900-5 PMID: 15247917
  43. The effect of Plasmodium falciparum Sir2a histone deacetylase on clonal and longitudinal variation in expression of the var family of virulence genes.
    Int J Parasitol. 2010 Jan;40(1):35-43 PMID: 19666023
  44. Histone H2AZ dimerizes with a novel variant H2B and is enriched at repetitive DNA in Trypanosoma brucei.
    J Cell Sci. 2005 Dec 15;118(Pt 24):5721-30 PMID: 16303849
  45. Prediction of the general transcription factors associated with RNA polymerase II in Plasmodium falciparum: conserved features and differences relative to other eukaryotes.
    BMC Genomics. 2005 Jul 23;6:100 PMID: 16042788
  46. Identification of active transcriptional regulatory modules by the functional assay of DNA from nucleosome-free regions.
    Genome Res. 2008 Jun;18(6):930-8 PMID: 18441229
  47. Histone sumoylation is associated with transcriptional repression.
    Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13225-30 PMID: 14578449
  48. Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum.
    PLoS Biol. 2009 Apr 14;7(4):e84 PMID: 19402747
  49. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum.
    Genome Res. 2004 Aug;14(8):1548-54 PMID: 15256513
  50. Tudor domain proteins in protozoan parasites and characterization of Plasmodium falciparum tudor staphylococcal nuclease.
    Int J Parasitol. 2008 Apr;38(5):513-26 PMID: 18035357
  51. A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling.
    Genome Res. 2004 Jun;14(6):1052-9 PMID: 15140830
  52. Stage-specific transcription of distinct repertoires of a multigene family during Plasmodium life cycle.
    Science. 2002 Jan 11;295(5553):342-5 PMID: 11786645
  53. Protein and nucleic acid synthesis during synchronized growth of Plasmodium falciparum.
    J Bacteriol. 1984 Dec;160(3):1165-7 PMID: 6389509
  54. Toxoplasma gondii and Cryptosporidium parvum lack detectable DNA cytosine methylation.
    Eukaryot Cell. 2008 Mar;7(3):537-40 PMID: 18178772
  55. Control of gene expression in Plasmodium falciparum - ten years on.
    Mol Biochem Parasitol. 2009 Mar;164(1):9-25 PMID: 19110008
  56. Shared epigenetic mechanisms control virulence factors in protozoan parasites.
    Curr Opin Microbiol. 2007 Dec;10(6):560-8 PMID: 18024150
  57. Reticulocyte-binding protein homologue 1 is required for sialic acid-dependent invasion into human erythrocytes by Plasmodium falciparum.
    Mol Microbiol. 2005 Jan;55(1):162-74 PMID: 15612925
  58. Plasmodium falciparum STEVOR proteins are highly expressed in patient isolates and located in the surface membranes of infected red blood cells and the apical tips of merozoites.
    Infect Immun. 2008 Jul;76(7):3329-36 PMID: 18474651
  59. SET8-mediated methylations of histone H4 lysine 20 mark silent heterochromatic domains in apicomplexan genomes.
    Mol Cell Biol. 2007 Aug;27(16):5711-24 PMID: 17562855
  60. Default Pathway of var2csa switching and translational repression in Plasmodium falciparum.
    PLoS One. 2008 Apr 23;3(4):e1982 PMID: 18431472
  61. Switching Plasmodium falciparum genes on and off for erythrocyte invasion.
    Trends Parasitol. 2008 Nov;24(11):517-24 PMID: 18805736
  62. Bromodomain: an acetyl-lysine binding domain.
    FEBS Lett. 2002 Feb 20;513(1):124-8 PMID: 11911891
  63. Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes.
    Science. 2005 Aug 26;309(5739):1384-7 PMID: 16123303
  64. Genetics of antigenic variation in Plasmodium falciparum.
    Curr Genet. 2009 Apr;55(2):103-10 PMID: 19242694
  65. Invasion of red blood cells by malaria parasites.
    Cell. 2006 Feb 24;124(4):755-66 PMID: 16497586
  66. PfGCN5-mediated histone H3 acetylation plays a key role in gene expression in Plasmodium falciparum.
    Eukaryot Cell. 2007 Jul;6(7):1219-27 PMID: 17449656
  67. Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites.
    Nucleic Acids Res. 2009 Jun;37(11):3788-98 PMID: 19380379
  68. The unusually large Plasmodium telomerase reverse-transcriptase localizes in a discrete compartment associated with the nucleolus.
    Nucleic Acids Res. 2005 Feb 18;33(3):1111-22 PMID: 15722485
  69. The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains.
    Trends Biochem Sci. 2003 Feb;28(2):69-74 PMID: 12575993
  70. Histone H2A.Z acetylation modulates an essential charge patch.
    Mol Cell. 2001 Jun;7(6):1329-35 PMID: 11430834
  71. Transcriptional and nucleosomal characterization of a subtelomeric gene cluster flanking a site of chromosomal rearrangements in Plasmodium falciparum.
    Nucleic Acids Res. 1994 Oct 11;22(20):4176-82 PMID: 7937144
  72. Histone lysine methyltransferases and demethylases in Plasmodium falciparum.
    Int J Parasitol. 2008 Aug;38(10):1083-97 PMID: 18299133
  73. 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. 2005 Jul 21;33(13):3994-4006 PMID: 16040597
  74. Epigenetics: a landscape takes shape.
    Cell. 2007 Feb 23;128(4):635-8 PMID: 17320500
  75. Epigenetic control of the variable expression of a Plasmodium falciparum receptor protein for erythrocyte invasion.
    Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2224-9 PMID: 20080673
  76. Clonally variant gene families in Plasmodium falciparum share a common activation factor.
    Mol Microbiol. 2009 Sep;73(6):1171-85 PMID: 19708920
  77. Stage-specific promoter activity from stably maintained episomes in Plasmodium falciparum.
    Int J Parasitol. 2002 Sep;32(10):1203-6 PMID: 12204219
  78. Plasmodium falciparum: Preinitiation complex occupancy of active and inactive promoters during erythrocytic stage.
    Exp Parasitol. 2009 Jan;121(1):46-54 PMID: 18951895
  79. Regulation of trypanosome DNA glycosylation by a SWI2/SNF2-like protein.
    Mol Cell. 2005 Feb 4;17(3):441-51 PMID: 15694344
  80. Characterization of PRMT1 from Plasmodium falciparum.
    Biochem J. 2009 Jun 12;421(1):107-18 PMID: 19344311
  81. A rhoptry-protein-associated mechanism of clonal phenotypic variation in rodent malaria.
    Nature. 1999 Apr 15;398(6728):618-22 PMID: 10217144
  82. The diverse functions of histone acetyltransferase complexes.
    Trends Genet. 2003 Jun;19(6):321-9 PMID: 12801725
  83. Histones and histone modifications in protozoan parasites.
    Cell Microbiol. 2006 Dec;8(12):1850-61 PMID: 17026479
  84. Ubiquitin-like modifiers and their deconjugating enzymes in medically important parasitic protozoa.
    Eukaryot Cell. 2007 Nov;6(11):1943-52 PMID: 17905920
  85. Nucleosome landscape and control of transcription in the human malaria parasite.
    Genome Res. 2010 Feb;20(2):228-38 PMID: 20054063
  86. Serial analysis of gene expression in Plasmodium falciparum reveals the global expression profile of erythrocytic stages and the presence of anti-sense transcripts in the malarial parasite.
    Mol Biol Cell. 2001 Oct;12(10):3114-25 PMID: 11598196
  87. A protein interaction network of the malaria parasite Plasmodium falciparum.
    Nature. 2005 Nov 3;438(7064):103-7 PMID: 16267556
  88. Histone H3 recognition and presentation by the WDR5 module of the MLL1 complex.
    Nat Struct Mol Biol. 2006 Aug;13(8):704-12 PMID: 16829959
  89. Recent advances in understanding chromatin remodeling by Swi/Snf complexes.
    Curr Opin Genet Dev. 2003 Apr;13(2):136-42 PMID: 12672490
  90. LC/ESI-MS demonstrates the absence of 5-methyl-2'-deoxycytosine in Plasmodium falciparum genomic DNA.
    Mol Biochem Parasitol. 2006 Dec;150(2):350-2 PMID: 16934885
  91. Plasmodium falciparum chromatin: nucleosomal organisation and histone-like proteins.
    Parasitol Res. 1994;80(3):255-8 PMID: 8036241
  92. Multivalent engagement of chromatin modifications by linked binding modules.
    Nat Rev Mol Cell Biol. 2007 Dec;8(12):983-94 PMID: 18037899
  93. The function of nuclear architecture: a genetic approach.
    Annu Rev Genet. 2004;38:305-45 PMID: 15568979
  94. 5' flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites.
    Mol Microbiol. 2007 Dec;66(6):1296-305 PMID: 18028313
  95. Apicomplexan UCHL3 retains dual specificity for ubiquitin and Nedd8 throughout evolution.
    Cell Microbiol. 2007 Jun;9(6):1601-10 PMID: 17371404
  96. 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. 2009 May;37(8):2596-606 PMID: 19270070
  97. Upregulation of expression of the reticulocyte homology gene 4 in the Plasmodium falciparum clone Dd2 is associated with a switch in the erythrocyte invasion pathway.
    Mol Biochem Parasitol. 2006 Feb;145(2):205-15 PMID: 16289357
  98. Programmed transcription of the var gene family, but not of stevor, in Plasmodium falciparum gametocytes.
    Eukaryot Cell. 2006 Aug;5(8):1206-14 PMID: 16896206
  99. PfADA2, a Plasmodium falciparum homologue of the transcriptional coactivator ADA2 and its in vivo association with the histone acetyltransferase PfGCN5.
    Gene. 2004 Jul 21;336(2):251-61 PMID: 15246536
  100. Differential association of Orc1 and Sir2 proteins to telomeric domains in Plasmodium falciparum.
    J Cell Sci. 2008 Jun 15;121(Pt 12):2046-53 PMID: 18525026
  101. Transcription and coregulation of multigene families in Plasmodium falciparum.
    Trends Parasitol. 2007 May;23(5):183-6; discussion 186-7 PMID: 17350338
  102. RNA meets chromatin.
    Genes Dev. 2005 Jul 15;19(14):1635-55 PMID: 16024654
  103. Transcriptional control and gene silencing in Plasmodium falciparum.
    Cell Microbiol. 2008 Oct;10(10):1935-46 PMID: 18637022
  104. Targeting histone deacetylase inhibitors for anti-malarial therapy.
    Curr Top Med Chem. 2009;9(3):292-308 PMID: 19355992
  105. The mammalian epigenome.
    Cell. 2007 Feb 23;128(4):669-81 PMID: 17320505
  106. Comparative analysis of apicomplexa and genomic diversity in eukaryotes.
    Genome Res. 2004 Sep;14(9):1686-95 PMID: 15342554
  107. Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3.
    Mol Cell. 2005 Oct 28;20(2):199-211 PMID: 16246723
  108. The pathogenic basis of malaria.
    Nature. 2002 Feb 7;415(6872):673-9 PMID: 11832955
  109. The language of covalent histone modifications.
    Nature. 2000 Jan 6;403(6765):41-5 PMID: 10638745
  110. Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei.
    Genes Dev. 2009 May 1;23(9):1063-76 PMID: 19369410
  111. Histone modification enzymes: novel targets for cancer drugs.
    Expert Opin Emerg Drugs. 2004 May;9(1):135-54 PMID: 15155140
  112. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers.
    Nat Struct Mol Biol. 2007 Nov;14(11):1025-1040 PMID: 17984965
  113. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses.
    J Exp Med. 1999 Nov 15;190(10):1393-404 PMID: 10562315
  114. Antigenic variation in Plasmodium falciparum: gene organization and regulation of the var multigene family.
    Eukaryot Cell. 2007 Sep;6(9):1511-20 PMID: 17644655
  115. Dynamic regulation of histone lysine methylation by demethylases.
    Mol Cell. 2007 Jan 12;25(1):1-14 PMID: 17218267
  116. Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes.
    Int J Parasitol. 2008 Jan;38(1):1-31 PMID: 17949725
  117. Genome-wide discovery and verification of novel structured RNAs in Plasmodium falciparum.
    Genome Res. 2008 Feb;18(2):281-92 PMID: 18096748
  118. Nucleosome positions predicted through comparative genomics.
    Nat Genet. 2006 Oct;38(10):1210-5 PMID: 16964265
  119. An operational definition of epigenetics.
    Genes Dev. 2009 Apr 1;23(7):781-3 PMID: 19339683
  120. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum.
    PLoS Biol. 2003 Oct;1(1):E5 PMID: 12929205
  121. Alterations in local chromatin environment are involved in silencing and activation of subtelomeric var genes in Plasmodium falciparum.
    Mol Microbiol. 2007 Oct;66(1):139-50 PMID: 17725559
  122. 5' sequence- and chromatin modification-dependent gene expression in Plasmodium falciparum erythrocytic stage.
    Mol Biochem Parasitol. 2008 Nov;162(1):40-51 PMID: 18692528
  123. Histone acetylase GCN5 enters the nucleus via importin-alpha in protozoan parasite Toxoplasma gondii.
    J Biol Chem. 2005 Feb 18;280(7):5902-8 PMID: 15591057
  124. Expression switching in the stevor and Pfmc-2TM superfamilies in Plasmodium falciparum.
    Mol Microbiol. 2007 Jun;64(6):1621-34 PMID: 17555442
  125. Deciphering the ubiquitin-mediated pathway in apicomplexan parasites: a potential strategy to interfere with parasite virulence.
    PLoS One. 2008 Jun 11;3(6):e2386 PMID: 18545708
  126. Epigenetic memory at malaria virulence genes.
    Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):899-902 PMID: 17209011
  127. Do protein motifs read the histone code?
    Bioessays. 2005 Feb;27(2):164-75 PMID: 15666348
  128. Erythrocyte invasion: vocabulary and grammar of the Plasmodium rhoptry.
    Parasitol Int. 2007 Dec;56(4):255-62 PMID: 17596999
  129. Epigenetic silencing of Plasmodium falciparum genes linked to erythrocyte invasion.
    PLoS Pathog. 2007 Aug 3;3(8):e107 PMID: 17676953
  130. Diverse expression patterns of subgroups of the rif multigene family during Plasmodium falciparum gametocytogenesis.
    PLoS One. 2008;3(11):e3779 PMID: 19020666
  131. Molecular cloning and nuclear localization of a histone deacetylase homologue in Plasmodium falciparum.
    Mol Biochem Parasitol. 1999 Mar 15;99(1):11-9 PMID: 10215020
  132. Poly(dA.dT) sequences exist as rigid DNA structures in nucleosome-free yeast promoters in vivo.
    Nucleic Acids Res. 2000 Nov 1;28(21):4083-9 PMID: 11058103
  133. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes.
    J Exp Med. 2005 Jun 6;201(11):1853-63 PMID: 15939796
  134. Synthesis of DNA during the asexual cycle of Plasmodium falciparum in culture.
    Mol Biochem Parasitol. 1984 Jan;10(1):79-87 PMID: 6420697
  135. Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes.
    EMBO J. 2003 Mar 3;22(5):1047-57 PMID: 12606570
  136. Genome-wide analysis of heterochromatin associates clonally variant gene regulation with perinuclear repressive centers in malaria parasites.
    Cell Host Microbe. 2009 Feb 19;5(2):179-90 PMID: 19218088
  137. Phylogenomics of the nucleosome.
    Nat Struct Biol. 2003 Nov;10(11):882-91 PMID: 14583738
  138. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum.
    Cell. 2005 Apr 8;121(1):13-24 PMID: 15820675
  139. The malaria parasite Plasmodium falciparum histones: organization, expression, and acetylation.
    Gene. 2006 Mar 15;369:53-65 PMID: 16410041
  140. Epigenetics in Apicomplexa: control of gene expression during cell cycle progression, differentiation and antigenic variation.
    Curr Opin Microbiol. 2007 Aug;10(4):357-62 PMID: 17719264
  141. Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens.
    Nat Rev Microbiol. 2009 Jul;7(7):493-503 PMID: 19503065
  142. Plasmodium falciparum Sir2 is an NAD+-dependent deacetylase and an acetyllysine-dependent and acetyllysine-independent NAD+ glycohydrolase.
    Biochemistry. 2008 Sep 23;47(38):10227-39 PMID: 18729382
  143. Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle.
    PLoS Pathog. 2010 Jan 22;6(1):e1000737 PMID: 20107518
  144. Widespread distribution of antisense transcripts in the Plasmodium falciparum genome.
    Mol Biochem Parasitol. 2004 Jul;136(1):35-42 PMID: 15138065
  145. The Plasmodium falciparum STEVOR multigene family mediates antigenic variation of the infected erythrocyte.
    PLoS Pathog. 2009 Feb;5(2):e1000307 PMID: 19229319
  146. Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells.
    Eukaryot Cell. 2002 Dec;1(6):926-35 PMID: 12477793
  147. Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations.
    Proc Natl Acad Sci U S A. 2005 Apr 12;102(15):5414-9 PMID: 15797990
  148. Core promoters are predicted by their distinct physicochemical properties in the genome of Plasmodium falciparum.
    Genome Biol. 2008;9(12):R178 PMID: 19094208
  149. 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. 2009 Dec 16;10:610 PMID: 20015349
  150. Histone mediated gene activation in Toxoplasma gondii.
    Mol Biochem Parasitol. 2006 Aug;148(2):109-16 PMID: 16644030
  151. Plasmodium biology: genomic gleanings.
    Cell. 2003 Dec 26;115(7):771-85 PMID: 14697197
  152. A genomic code for nucleosome positioning.
    Nature. 2006 Aug 17;442(7104):772-8 PMID: 16862119
  153. Nuclear non-coding RNAs are transcribed from the centromeres of Plasmodium falciparum and are associated with centromeric chromatin.
    J Biol Chem. 2008 Feb 29;283(9):5692-8 PMID: 18165241
  154. Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors.
    PLoS Pathog. 2009 Sep;5(9):e1000569 PMID: 19730695
  155. Dynamic histone H3 epigenome marking during the intraerythrocytic cycle of Plasmodium falciparum.
    Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9655-60 PMID: 19497874
  156. Global histone analysis by mass spectrometry reveals a high content of acetylated lysine residues in the malaria parasite Plasmodium falciparum.
    J Proteome Res. 2009 Jul;8(7):3439-50 PMID: 19351122
  157. Organismal differences in post-translational modifications in histones H3 and H4.
    J Biol Chem. 2007 Mar 9;282(10):7641-55 PMID: 17194708
Article Info
Journal
Eukaryotic cell
Abbr.
Eukaryot Cell
ISSN
1535-9786
Published
2010-08-00
Epub
2010-00-07
Pages
1138-49
Language
English
Region
United States
NLM ID
101130731
PMCID
PMC2918932
Subset
IM
Grants
NIAID NIH HHS · R01 AI064553 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

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Business Email

E-mail: [email protected]