Histone Deacetylases Play a Major Role in the Transcriptional Regulation of the Plasmodium falciparum Life Cycle
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{"title"=>"Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle", "type"=>"journal", "authors"=>[{"first_name"=>"Balbir K.", "last_name"=>"Chaal", "scopus_author_id"=>"6506775591"}, {"first_name"=>"Archna P.", "last_name"=>"Gupta", "scopus_author_id"=>"55491985700"}, {"first_name"=>"Brigitta D.", "last_name"=>"Wastuwidyaningtyas", "scopus_author_id"=>"35724784600"}, {"first_name"=>"Yen Hoon", "last_name"=>"Luah", "scopus_author_id"=>"35724015100"}, {"first_name"=>"Zbynek", "last_name"=>"Bozdech", "scopus_author_id"=>"7007157687"}], "year"=>2010, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-77649219343", "sgr"=>"77649219343", "pui"=>"358387595", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "pmid"=>"20107518", "doi"=>"10.1371/journal.ppat.1000737"}, "id"=>"41288a66-7409-3813-9dea-fa7f512b768f", "abstract"=>"The apparent paucity of molecular factors of transcriptional control in the genomes of Plasmodium parasites raises many questions about the mechanisms of life cycle regulation in these malaria parasites. Epigenetic regulation has been suggested to play a major role in the stage specific gene expression during the Plasmodium life cycle. To address some of these questions, we analyzed global transcriptional responses of Plasmodium falciparum to a potent inhibitor of histone deacetylase activities (HDAC). The inhibitor apicidin induced profound transcriptional changes in multiple stages of the P. falciparum intraerythrocytic developmental cycle (IDC) that were characterized by rapid activation and repression of a large percentage of the genome. A major component of this response was induction of genes that are otherwise suppressed during that particular stage of the IDC or specific for the exo-erythrocytic stages. In the schizont stage, apicidin induced hyperacetylation of histone lysine residues H3K9, H4K8 and the tetra-acetyl H4 (H4Ac4) and demethylation of H3K4me3. Interestingly, we observed overlapping patterns of chromosomal distributions between H4K8Ac and H3K4me3 and between H3K9Ac and H4Ac4. There was a significant but partial association between the apicidin-induced gene expression and histone modifications, which included a number of stage specific transcription factors. Taken together, inhibition of HDAC activities leads to dramatic de-regulation of the IDC transcriptional cascade, which is a result of both disruption of histone modifications and up-regulation of stage specific transcription factors. These findings suggest an important role of histone modification and chromatin remodeling in transcriptional regulation of the Plasmodium life cycle. This also emphasizes the potential of P. falciparum HDACs as drug targets for malaria chemotherapy.", "link"=>"http://www.mendeley.com/research/histone-deacetylases-play-major-role-transcriptional-regulation-plasmodium-falciparum-life-cycle", "reader_count"=>12, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Student > Doctoral Student"=>2, "Researcher"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>3, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Student > Doctoral Student"=>2, "Researcher"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>3, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>5, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/430121", "https://ndownloader.figshare.com/files/430141", "https://ndownloader.figshare.com/files/430163", "https://ndownloader.figshare.com/files/430191"], "description"=>"<div><p>The apparent paucity of molecular factors of transcriptional control in the genomes of <em>Plasmodium</em> parasites raises many questions about the mechanisms of life cycle regulation in these malaria parasites. Epigenetic regulation has been suggested to play a major role in the stage specific gene expression during the <em>Plasmodium</em> life cycle. To address some of these questions, we analyzed global transcriptional responses of <em>Plasmodium falciparum</em> to a potent inhibitor of histone deacetylase activities (HDAC). The inhibitor apicidin induced profound transcriptional changes in multiple stages of the <em>P. falciparum</em> intraerythrocytic developmental cycle (IDC) that were characterized by rapid activation and repression of a large percentage of the genome. A major component of this response was induction of genes that are otherwise suppressed during that particular stage of the IDC or specific for the exo-erythrocytic stages. In the schizont stage, apicidin induced hyperacetylation of histone lysine residues H3K9, H4K8 and the tetra-acetyl H4 (H4Ac4) and demethylation of H3K4me3. Interestingly, we observed overlapping patterns of chromosomal distributions between H4K8Ac and H3K4me3 and between H3K9Ac and H4Ac4. There was a significant but partial association between the apicidin-induced gene expression and histone modifications, which included a number of stage specific transcription factors. Taken together, inhibition of HDAC activities leads to dramatic de-regulation of the IDC transcriptional cascade, which is a result of both disruption of histone modifications and up-regulation of stage specific transcription factors. These findings suggest an important role of histone modification and chromatin remodeling in transcriptional regulation of the <em>Plasmodium</em> life cycle. This also emphasizes the potential of <em>P. falciparum</em> HDACs as drug targets for malaria chemotherapy.</p></div>", "links"=>[], "tags"=>["histone", "deacetylases", "transcriptional"], "article_id"=>144909, "categories"=>["Microbiology", "Physics", "Genetics"], "users"=>["Balbir K. Chaal", "Archna P. Gupta", "Brigitta D. Wastuwidyaningtyas", "Yen-Hoon Luah", "Zbynek Bozdech"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000737.s001", "https://dx.doi.org/10.1371/journal.ppat.1000737.s002", "https://dx.doi.org/10.1371/journal.ppat.1000737.s003", "https://dx.doi.org/10.1371/journal.ppat.1000737.s004"], "stats"=>{"downloads"=>6, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Histone_Deacetylases_Play_a_Major_Role_in_the_Transcriptional_Regulation_of_the_Plasmodium_falciparum_Life_Cycle/144909", "title"=>"Histone Deacetylases Play a Major Role in the Transcriptional Regulation of the <em>Plasmodium falciparum</em> Life Cycle", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-01-22 01:21:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/867109"], "description"=>"<p>A. Chromosomal display of genetic loci, represented by MOEs, that showed a significant increase in H4K8Ac in apicidin treated trophozoites (Δ = 1.7) and schizonts (Δ = 5). B. Chromosomal display of genetic loci that showed a significant increase in H3K9Ac (Δ = 2) and H4Ac4 (Δ = 3.5) in apicidin treated schizonts. C. Chromosomal display of genetic loci that showed a significant <i>decrease</i> in H3K4me3 (Δ = 4) and increase in H4K8Ac (Δ = 5) in apicidin treated schizonts. The position of each line reflects the location of each genetic loci within the <i>P. falciparum</i> 14 chromosomes. Venn diagrams show significant overlaps between different groups of genetic loci (shown above the line) and genes (shown in <i>italics</i> below the line) associated with apicidin altered histone modifications. P values for genetic loci and genes are shown above and below the Venn diagrams respectively. The insert graphs show the distribution of the enriched histone modifications within individual genes (bins of 500 base pairs). MOEs were divided into groups according to their distance from the putative ATG start codon.</p>", "links"=>[], "tags"=>["histone", "hyperacetylation", "induced"], "article_id"=>537566, "categories"=>["Microbiology", "Physics", "Genetics"], "users"=>["Balbir K. Chaal", "Archna P. Gupta", "Brigitta D. Wastuwidyaningtyas", "Yen-Hoon Luah", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000737.g003", "stats"=>{"downloads"=>3, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genome_wide_histone_hyperacetylation_induced_by_apicidin_/537566", "title"=>"Genome-wide histone hyperacetylation induced by apicidin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-22 02:06:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/867474"], "description"=>"<p>Genes induced by 2-fold or greater, in each individual time point in apicidin treated schizonts was determined. In brackets the number of genes associated with an apicidin induced histone modification in at least one locus corresponding to an MOE are shown. For each individual time point, the number of genes with both a change in RNA expression (>2-fold) and associated with an apicidin induced histone modification are shown. Blank boxes refer to P values >0.05. P values represented as <i>italics</i> correspond to negative correlation.</p>", "links"=>[], "tags"=>["loci", "altered", "histone", "modifications", "genes", "induced"], "article_id"=>537927, "categories"=>["Microbiology", "Physics", "Genetics"], "users"=>["Balbir K. Chaal", "Archna P. Gupta", "Brigitta D. Wastuwidyaningtyas", "Yen-Hoon Luah", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000737.t001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_between_the_genetic_loci_with_altered_histone_modifications_and_genes_induced_by_apicidin_/537927", "title"=>"Association between the genetic loci with altered histone modifications and genes induced by apicidin.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-01-22 02:12:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/867214"], "description"=>"<p>A. Distribution of acetylated H4K8 and H4K5 along the 5′ flanking upstream and coding regions. CHIPs were carried out with trophozoites treated with DMSO (0.005%) and apicidin (IC90) for 1 hour and with antibodies directed against either H4K8Ac or H4K5Ac. B. Distribution of H4K8Ac and H3K4me3 along the 5′ flanking upstream and coding regions of CSP. CHIPs were carried out with schizonts treated with DMSO (0.005%) and apicidin (IC90) for 1 hour and with antibodies directed against either H4K8Ac or H3K4me3. RTQ-PCR was carried out on immunoprecipated DNA and input genomic DNA obtained from DMSO and apicidin treated cells. The log<sub>2</sub> ratios of H4K8Ac (black bars) and H4K5Ac/H3K4me3 (white/gray bars) were calculated by using the ΔΔCt method (Ct of apicidin-treated immunoprecipitated target gene - Ct of apicidin-treated input target gene) minus (Ct of DMSO treated immunoprecipitated target gene-Ct of DMSO treated input target gene). Black box represents PCR fragment encoding the MOE. The insert boxes show the fold increase in H4K8Ac/H4K5Ac/H3K4me3 in apicidin treated samples, obtained from ChIP-chip data analysis. C and D. Trophozoites were treated with apicidin (IC90) for 1 hour. Protein samples were analyzed by SDS-PAGE followed by immunodetection using an antibody directed against H4K8Ac and H4K5Ac (C) or CSP and EBA-175 (D). Molecular weights are shown in kDa. − and + refers to DMSO and apicidin treated cells respectively.</p>", "links"=>[], "tags"=>["induces", "histone", "hyperacetylation", "promoter", "regions"], "article_id"=>537672, "categories"=>["Microbiology", "Physics", "Genetics"], "users"=>["Balbir K. Chaal", "Archna P. Gupta", "Brigitta D. Wastuwidyaningtyas", "Yen-Hoon Luah", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000737.g004", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Apicidin_induces_histone_hyperacetylation_along_promoter_regions_and_protein_expression_of_P_falciparum_genes_/537672", "title"=>"Apicidin induces histone hyperacetylation along promoter regions and protein expression of <i>P. falciparum</i> genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-22 02:07:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/866844"], "description"=>"<p>Highly synchronized <i>P. falciparum</i> cells: rings (6–14 hpi), trophozoites (20–28 hpi) and schizonts (34–42 hpi) were treated with DMSO (0.005%) and apicidin (IC90). RNA samples were collected at 0.5, 1, 2, 4 and 6 hours post treatment. cDNA, synthesized from the RNA samples, was labeled with Cy5 and hybridized against the Cy3 labeled 3D7 reference pool. The microarray data, which included mRNA abundance ratios between each time point sample and the 3D7 reference pool, was filtered as described in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000737#s4\" target=\"_blank\">material and methods</a>. A. For all stages, genes with a 2 or greater fold difference in expression induced by apicidin treatment in at least one time point are shown. B. For rings and trophozoites, genes with a 3 or greater fold difference in expression in at least two or one time points respectively are shown. For schizonts, genes with a 4 or greater fold difference in expression in at least one time point are shown. The transcription profile of the genes under normal developmental conditions is shown in the <i>P. falciparum</i> IDC transcriptome. The stage of the parasites used in the time course experiment is shown boxed in yellow.</p>", "links"=>[], "tags"=>["transcriptional", "apicidin"], "article_id"=>537300, "categories"=>["Microbiology", "Physics", "Genetics"], "users"=>["Balbir K. Chaal", "Archna P. Gupta", "Brigitta D. Wastuwidyaningtyas", "Yen-Hoon Luah", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000737.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_transcriptional_response_of_P_falciparum_to_apicidin_treatment_/537300", "title"=>"Global transcriptional response of <i>P. falciparum</i> to apicidin treatment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-22 02:01:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/866951"], "description"=>"<p><i>P. falciparum</i> cells were treated with DMSO (0.005%) and apicidin (IC90). Protein samples collected at 1, 2, 3 and 4 hours post treatment were analyzed by SDS-PAGE. PfHDAC1, Pfactin 1, core histone 3 (H3), core histone 4 (H4) and the H4K8Ac, H4Ac4, H3K9Ac and H3K4me3 sites were detected by immunodetection. Molecular weights are shown in kDa. − and + refers to DMSO and apicidin treated cells respectively.</p>", "links"=>[], "tags"=>["histone", "hyperacetylation", "induced"], "article_id"=>537410, "categories"=>["Microbiology", "Physics", "Genetics"], "users"=>["Balbir K. Chaal", "Archna P. Gupta", "Brigitta D. Wastuwidyaningtyas", "Yen-Hoon Luah", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000737.g002", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_histone_hyperacetylation_induced_by_apicidin_/537410", "title"=>"Global histone hyperacetylation induced by apicidin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-22 02:03:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/867349"], "description"=>"<p>A. Apicidin disrupts stage specific expression of the ApiAP2 proteins. B. Apicidin induces expression of transcription associated proteins. MOEs corresponding to individual genes and showing changes in gene expression and histone modifications induced by apicidin treatment are shown. The specific stage of expression, under normal developmental conditions, for each ApiAP2 protein is indicated on the right hand side. PfHDAC1 (PFI1260c), PfSir2 (PF13_0152), HDAC homologues (PF14_0489, PF14_0690 and PF10_0078), circumsporozoite protein (PFC0210c), erythrocyte binding antigen 175 (MAL7P1.176), apical membrane antigen 1 (PF11_0344), merozoite surface protein 6 (PF10_0346), ApiAP2 proteins (PF14_0633, PFF0200c, PF11_0404, PF14_0079, PF13_0097, PFL1075w, PF14 _0271, PFF1100c and PFD0200c), heterochromatin protein 1 (PFL1005c), Pfg27 (PF13_0011), Pfs16 (PFD0310w), Pfpeg-3 (PFL0795c), Pfpeg-4 (PF10_0164), Pf47 (PF13_0248), Pfg377 (PFL2405c), sporozoite surface protein 2 (PF13_0201), SPATR (PFB0570w), Pf52 (PFD0215c), PfGCN5 (PF08_0034), Pfactin 1 (PFL2215w) and PfMYST (PF11_0192).</p>", "links"=>[], "tags"=>["hdacs", "induces", "transcription"], "article_id"=>537807, "categories"=>["Microbiology", "Physics", "Genetics"], "users"=>["Balbir K. Chaal", "Archna P. Gupta", "Brigitta D. Wastuwidyaningtyas", "Yen-Hoon Luah", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000737.g005", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibition_of_HDACs_induces_expression_of_transcription_associated_proteins_/537807", "title"=>"Inhibition of HDACs induces expression of transcription associated proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-22 02:10:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/867507"], "description"=>"<p>Genes repressed by 2-fold or greater, in each individual time point in apicidin treated schizonts was determined. In brackets the number of genes associated with an apicidin induced histone modification in at least one locus corresponding to an MOE are shown. For each individual time point, the number of genes with both a change in RNA expression (>2-fold) and associated with an apicidin induced histone modification are shown. Blank boxes refer to P values >0.05. P values represented as <b>bold</b> or in <i>italics</i> correspond to positive and negative correlation respectively.</p>", "links"=>[], "tags"=>["loci", "altered", "histone", "modifications", "genes", "repressed"], "article_id"=>537960, "categories"=>["Microbiology", "Physics", "Genetics"], "users"=>["Balbir K. Chaal", "Archna P. Gupta", "Brigitta D. Wastuwidyaningtyas", "Yen-Hoon Luah", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000737.t002", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_between_the_genetic_loci_with_altered_histone_modifications_and_genes_repressed_by_apicidin_/537960", "title"=>"Association between the genetic loci with altered histone modifications and genes repressed by apicidin.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-01-22 02:12:40"}

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  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"16", "full-text"=>"14", "pdf"=>"9", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}

Relative Metric

{"start_date"=>"2010-01-01T00:00:00Z", "end_date"=>"2010-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Biochemistry", "average_usage"=>[283, 565, 720, 852, 970, 1070, 1168, 1258, 1336, 1411, 1487, 1571, 1640, 1709, 1776, 1843, 1906, 1969, 2031, 2086, 2152, 2221, 2286, 2361, 2419, 2480, 2543, 2598, 2665, 2731, 2802, 2868, 2932, 2996, 3053, 3114, 3169, 3232, 3289, 3355, 3413, 3473, 3530, 3595, 3648, 3711, 3764, 3810, 3863]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[280, 562, 725, 863, 974, 1083, 1177, 1268, 1347, 1421, 1489, 1570, 1638, 1706, 1763, 1823, 1890, 1951, 2016, 2076, 2134, 2192, 2257, 2319, 2378, 2438, 2501, 2572, 2634, 2700, 2759, 2825, 2887, 2936, 3007, 3070, 3121, 3184, 3237, 3304, 3363, 3425, 3484, 3531, 3612, 3663, 3718, 3771]}, {"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[306, 610, 768, 915, 1043, 1164, 1255, 1349, 1432, 1511, 1592, 1674, 1744, 1817, 1889, 1950, 2028, 2087, 2153, 2217, 2274, 2349, 2418, 2488, 2558, 2616, 2686, 2745, 2809, 2869, 2938, 3008, 3071, 3131, 3189, 3258, 3320, 3389, 3446, 3503, 3552, 3613, 3677, 3744, 3788, 3842, 3907, 3966, 4015]}, {"subject_area"=>"/Biology and life sciences/Parasitology", "average_usage"=>[277, 573, 714, 825, 931, 1032, 1126, 1207, 1278, 1351, 1422, 1495, 1558, 1626, 1696, 1747, 1811, 1888, 1954, 2005, 2095, 2149, 2214, 2277, 2318, 2389, 2436, 2493, 2567, 2666, 2727, 2784, 2871, 2936, 2984, 3058, 3116, 3178, 3223, 3295, 3360, 3423, 3504, 3579, 3645, 3716, 3757, 3826, 3873]}]}
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