Dynamic Epigenetic Regulation of Gene Expression during the Life Cycle of Malaria Parasite Plasmodium falciparum
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{"title"=>"Dynamic Epigenetic Regulation of Gene Expression during the Life Cycle of Malaria Parasite Plasmodium falciparum", "type"=>"journal", "authors"=>[{"first_name"=>"Archna P.", "last_name"=>"Gupta", "scopus_author_id"=>"55491985700"}, {"first_name"=>"Wai Hoe", "last_name"=>"Chin", "scopus_author_id"=>"55575290900"}, {"first_name"=>"Lei", "last_name"=>"Zhu", "scopus_author_id"=>"55808916200"}, {"first_name"=>"Sachel", "last_name"=>"Mok", "scopus_author_id"=>"25641686200"}, {"first_name"=>"Yen Hoon", "last_name"=>"Luah", "scopus_author_id"=>"35724015100"}, {"first_name"=>"Eng How", "last_name"=>"Lim", "scopus_author_id"=>"57197385255"}, {"first_name"=>"Zbynek", "last_name"=>"Bozdech", "scopus_author_id"=>"7007157687"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-84880964724", "pui"=>"369459533", "doi"=>"10.1371/journal.ppat.1003170", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "sgr"=>"84880964724", "pmid"=>"23468622"}, "id"=>"538070af-6daa-367d-b014-3a7d5dc12d2b", "abstract"=>"Epigenetic mechanisms are emerging as one of the major factors of the dynamics of gene expression in the human malaria parasite, Plasmodium falciparum. To elucidate the role of chromatin remodeling in transcriptional regulation associated with the progression of the P. falciparum intraerythrocytic development cycle (IDC), we mapped the temporal pattern of chromosomal association with histone H3 and H4 modifications using ChIP-on-chip. Here, we have generated a broad integrative epigenomic map of twelve histone modifications during the P. falciparum IDC including H4K5ac, H4K8ac, H4K12ac, H4K16ac, H3K9ac, H3K14ac, H3K56ac, H4K20me1, H4K20me3, H3K4me3, H3K79me3 and H4R3me2. While some modifications were found to be associated with the vast majority of the genome and their occupancy was constant, others showed more specific and highly dynamic distribution. Importantly, eight modifications displaying tight correlations with transcript levels showed differential affinity to distinct genomic regions with H4K8ac occupying predominantly promoter regions while others occurred at the 5' ends of coding sequences. The promoter occupancy of H4K8ac remained unchanged when ectopically inserted at a different locus, indicating the presence of specific DNA elements that recruit histone modifying enzymes regardless of their broad chromatin environment. In addition, we showed the presence of multivalent domains on the genome carrying more than one histone mark, highlighting the importance of combinatorial effects on transcription. Overall, our work portrays a substantial association between chromosomal locations of various epigenetic markers, transcriptional activity and global stage-specific transitions in the epigenome.", "link"=>"http://www.mendeley.com/research/dynamic-epigenetic-regulation-gene-expression-during-life-cycle-malaria-parasite-plasmodium-falcipar", "reader_count"=>34, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>10, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>10, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>24, "Medicine and Dentistry"=>1, "Chemistry"=>2, "Social Sciences"=>1, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>24}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}}, "reader_count_by_country"=>{"United States"=>2, "United Kingdom"=>1, "France"=>1, "Kenya"=>1, "Germany"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/974436"], "description"=>"<p>(A) <i>PCC-based correlation of the dynamic histone occupancy profiles</i>. The bar charts show examples of pair wise correlation distributions between the dynamic profiles of the individual histone marks calculated analogously to the correlations with steady state mRNA levels (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003170#ppat-1003170-g003\" target=\"_blank\">Figure 3</a>). Line graphs give the randomized distribution of PCC. <i>P</i> value (P) and skewness (S) are shown below each graph. (B) <i>Hierarchical clustering of histone mark associations</i>. The heat maps represent hierarchical clustering of the skewness (S) values of the PCC distributions for every marked histone pair. High positive skew (red) and low negative skew (blue) indicate positive and negative correlations with the marked histone pairs, respectively. (C) <i>Sequential ChIP-on-chip for H3K9ac and H3K56ac</i>. The sequential ChIP-on-chip was carried out with ring stage parasites using anti-H3K56ac antibody followed by anti-H3K9ac antibody. Immunoprecipitation was also done using anti-H3K56ac antibody or anti-H3K9ac antibody separately. Data was averaged from 2 separate experiments and probes with ChIP/input signal ratio above 1 for bead control were subtracted for further analysis. The chart (above) shows the probes overlapping between the sequential ChIP and probes shared in common between both histone marks when used individually (ChIP/input >1). Chromosomal distribution (below) of H3K56ac (orange), H3K9ac (green) and sequential (purple) ChIP enrichment of probes as seen at chromosome 4. Each vertical line depicts the position of a probe on the chromosome.</p>", "links"=>[], "tags"=>["histone"], "article_id"=>642476, "categories"=>["Biotechnology", "Genetics", "Microbiology"], "users"=>["Archna P. Gupta", "Wai Hoe Chin", "Lei Zhu", "Sachel Mok", "Yen-Hoon Luah", "Eng-How Lim", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003170.g006", "stats"=>{"downloads"=>1, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Combinatorial_histone_modifications_/642476", "title"=>"Combinatorial histone modifications.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 13:58:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/974433"], "description"=>"<p>(A) <i>Correlation of H4K8ac occupancy with transcription</i>. The dynamic occupancy profiles for H4K8ac (leftmost panel) was correlated to the corresponding mRNA profiles using Pearson Correlation Coefficient (PCC, also r). The PCC was calculated between each dynamic H4K8ac occupancy profile and mRNA abundance profile of the corresponding gene. The PCC distribution was plotted along bins ranging from −1 to +1 (x-axis) as the number of probes in each bin (bar graph in the middle). A total of 3,356 probes showed r (PCC)≥0.4 which represents a good correlation in the IDC timing (rightmost panels). In addition 2090 probes showed no correlation (r between 0.4 and −0.4) and 1632 probes showed a negative correlation (r≤−0.4) with expression. Out of 7,260 loci linked with the dynamic H4K8ac occupancy profiles, we did not obtain expression data for 182 probes. The scale bar refers to log<sub>2</sub> ratios of mean-centered profiles across the IDC. (B) <i>Correlations of the 13 histone-mark-occupancy profiles with transcription</i>. Similar to H4K8ac (panel A), the distribution of PCC (r) correlations between the dynamic occupancy and steady state mRNA profiles were calculated for all 13 studied histone marks. Similarly, the data were arranged into bins of PCC ranging from −1 to +1 (x-axis) and plotted against the number of probes in each bin for actual distribution (bar graphs) and randomized distribution (line graphs). The statistical significance of the observed distribution (<i>P</i>, tested against the randomized distributions) and the degree of skewness (S, positive values towards positive PCCs) of the PCC distribution is presented at the right bottom of each graph (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003170#s4\" target=\"_blank\">Materials and Methods</a>). Eight histone marks exhibit statistically significant correlation with transcript levels (purple graphs) while 5 marks show a neutral relationship with transcript levels (green bars).</p>", "links"=>[], "tags"=>["histone", "occupancy"], "article_id"=>642473, "categories"=>["Biotechnology", "Genetics", "Microbiology"], "users"=>["Archna P. Gupta", "Wai Hoe Chin", "Lei Zhu", "Sachel Mok", "Yen-Hoon Luah", "Eng-How Lim", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003170.g003", "stats"=>{"downloads"=>3, "page_views"=>44, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_of_histone_mark_occupancy_with_transcription_/642473", "title"=>"Association of histone mark occupancy with transcription.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 13:57:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/974431"], "description"=>"<p>(A) <i>mRNA transcriptome and dynamic occupancy profiles of 13 histone marks across the IDC</i>. The phaseograms depict the cascades of the dynamic occupancy profiles (<i>P</i><0.05 and fold change ≥1.5 across the IDC, see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003170#ppat-1003170-g001\" target=\"_blank\">Figure 1B</a>) for the 13 histone marks. The yellow/blue color scale represents lowess smoothed profiles calculated from centered curves of relative occupancy ratios measured by ChIP/input (log<sub>2</sub>) for the 6 time points (TP1-6 representing 0 to 48 hpi). The mRNA transcriptome presented on the left was assembled similarly. The gene/probe order in each phaseogram was determined independently using Fast Fourier transformation (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003170#s4\" target=\"_blank\">Materials and Methods</a>). (B) <i>Distribution of the peak occupancy of the 13 histone marks along the IDC</i>. The bar chart shows the maximum occupancy of histone marks at 3 life cycle stages for the dynamic profiles included in the phaseograms (panel A). The percentage represented (by bar size) as well as the probe number (number within the bar) depicts the distribution of the corresponding occupancy profiles that peak at TP1 or TP2 (0–16 hpi), TP3 or TP4 (17–32 hpi) and TP5 or TP6 (33–48 hpi). In our culturing set up, these time points correspond to the three main IDC developmental stages, ring, trophozoite and schizont, respectively.</p>", "links"=>[], "tags"=>["histone", "occupancy"], "article_id"=>642471, "categories"=>["Biotechnology", "Genetics", "Microbiology"], "users"=>["Archna P. Gupta", "Wai Hoe Chin", "Lei Zhu", "Sachel Mok", "Yen-Hoon Luah", "Eng-How Lim", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003170.g002", "stats"=>{"downloads"=>2, "page_views"=>63, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dynamics_of_histone_occupancy_across_the_P_falciparum_IDC_/642471", "title"=>"Dynamics of histone occupancy across the <i>P. falciparum</i> IDC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 13:57:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/974435"], "description"=>"<p>(A) <i>Cloning strategy for ectopic integration of promoter regions</i>. Four promoter regions (1.5–2 kb upstream of the ATG) corresponding to upstream regions of MAL13P1.122, PF14_0705, PFD0240c and PFC0210c were cloned upstream of the luciferase reporter gene pLN-luc (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003170#s4\" target=\"_blank\">Materials and Methods</a>). <i>P. falciparum</i> strain Dd2<sup>attB</sup> was transfected with the above vectors to achieve integration at the <i>cg6</i> locus and the transgenic cell lines were selected on blasticidin. Primer pair P2/P4 was used to confirm integration (data not shown). (B) <i>H4K8ac occupancy at the four ectopically integrated promoter regions</i>. The graphs represent real time PCR results carried out on H4K8ac-immunoprecipitated DNA from rings (R), trophozoites (T) and schizonts (S). In order to distinguish between the endogenous and luciferase tagged promoter, specific primers were designed to amplify regions spanning the 3′ end of the promoter and either the start of the endogenous gene or the start of the luciferase gene. The positions of forward (F) and reverse (R) primers are shown in panel A. Grey lines refer to the ChIP enrichment of the native <i>cg6</i> locus in the untransfected parasites. Orange and green lines represent the ChIP enrichment of native promoters and integrated promoters, respectively, in the transfectants. The error bars give the standard deviation from triplicate experiments.</p>", "links"=>[], "tags"=>["modification", "patterns", "ectopically"], "article_id"=>642475, "categories"=>["Biotechnology", "Genetics", "Microbiology"], "users"=>["Archna P. Gupta", "Wai Hoe Chin", "Lei Zhu", "Sachel Mok", "Yen-Hoon Luah", "Eng-How Lim", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003170.g005", "stats"=>{"downloads"=>2, "page_views"=>41, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histone_modification_patterns_on_ectopically_integrated_promoters_/642475", "title"=>"Histone modification patterns on ectopically integrated promoters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 13:58:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/974434"], "description"=>"<p>The plots on the left represent the frequency (percentage) of transcription-linked histone marks that are characterized by their dynamic occupancy profiles with positive (r≥0.4) or negative (r≤−0.4) correlation with expression. The frequency of these transcription-linked profiles is plotted along an average gene corresponding to the genetic locus/probe positioning within the gene. In particular, the data was arranged into 500 bp bins ranging from 1500 bp upstream of the ATG start codon (“Promoter”) to +3000 bp into the gene (“Coding body”). The frequency (y-axis) is expressed as the percentage of transcription-linked profiles versus the total number of occupancy profiles (both dynamic and constitutive) for either positive (dark green, above the x-axis) or negative (light green, below the x-axis). The vertical dotted line marks the position of the ATG start codon. Functional enrichment analyses identified over-represented pathways (<i>P</i><0.05) as compared to their respective frequency in the genome for genes associated with each transcription-linked modification (right).</p>", "links"=>[], "tags"=>["positioning", "transcription-linked", "histone"], "article_id"=>642474, "categories"=>["Biotechnology", "Genetics", "Microbiology"], "users"=>["Archna P. Gupta", "Wai Hoe Chin", "Lei Zhu", "Sachel Mok", "Yen-Hoon Luah", "Eng-How Lim", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003170.g004", "stats"=>{"downloads"=>1, "page_views"=>34, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_positioning_and_biological_significance_of_the_transcription_linked_histone_marks_/642474", "title"=>"Gene positioning and biological significance of the transcription-linked histone marks.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 13:58:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/974429"], "description"=>"<p>(A) <i>Schematics of the work flow</i>. <i>P. falciparum</i> cells were harvested at 8, 16, 24, 32, 40 and 48 hpi corresponding to time points TP1, TP2, TP3, TP4, TP5 and TP6, respectively, during the 48 h IDC. The same cells were used to carry out all experiments including ChIP-on-chip, transcriptome analysis and western blot assays. (B) <i>The summary of the occupancy of 13 histone marks in the P. falciparum genome</i>. The bar graph depicts a total count of microarray probes with positive ChIP signal which corresponds to an association of the genetic loci with the histone marks. For this analysis, only probes with a positive signal for at least 2 consecutive time points (out of 6) were considered. The graph includes the total count of genetic loci (represented by microarray probes) associated with each histone mark (orange bars), only loci with an oscillating occupancy profile (log<sub>2</sub> ChIP/input) across the IDC defined by <i>P</i><0.05 (green bars), and dynamic occupancy profile across the IDC defined by <i>P</i><0.05 and ≥1.5 fold change (purple bars). The latter are referred to as “dynamic histone marks” and “dynamic occupancy profiles” in the text. Due to the lack of triplicates (scarcity of ChIP material) and consequent inability to calculate <i>P</i> values, only the ≥1.5 fold change criteria was applied to the dynamic occupancy profiles of H3K14ac, H4K20me3 and H4R3me2, (marked by an asterisk). The total count of microarray probes is 14,773. (C) <i>Chromosomal projection of histone occupancy for chromosome 2 at TP2</i>. Position and height of each vertical line reflect the location on the chromosome and ChIP/input ratio, respectively, of the corresponding probe. Black rectangles highlight apparently similar patterns between different histone marks. (D) <i>Enrichment of histone modifications along P. falciparum genes</i>. The graphs represent ChIP signal (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003170#s4\" target=\"_blank\">Materials and Methods</a>) plotted along <i>P falciparum</i> genes against the probe position relative to translation start codon (ATG) starting −1000 bp (upstream) to +3000 bp (within the ORF) (note that transcriptional start sites remain largely unmapped in <i>P. falciparum</i>). For each of the 6 time points across the IDC, the lowess smoothed profiles of the ChIP signal is plotted for three gene groups including 10% of total genes at the top (Top), in the middle (Middle) and at the bottom (Bottom) of the gene list ranked by their mRNA levels at the particular time point. The vertical line in grey indicates the position of the ATG. For these graphs, all histone-mark-occupancy results were used, including both the constitutive and dynamic occupancy profiles.</p>", "links"=>[], "tags"=>["modified", "histones", "occupancy"], "article_id"=>642469, "categories"=>["Biotechnology", "Genetics", "Microbiology"], "users"=>["Archna P. Gupta", "Wai Hoe Chin", "Lei Zhu", "Sachel Mok", "Yen-Hoon Luah", "Eng-How Lim", "Zbynek Bozdech"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003170.g001", "stats"=>{"downloads"=>0, "page_views"=>50, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overview_of_modified_histones_occupancy_during_the_P_falciparum_IDC_/642469", "title"=>"Overview of modified histones occupancy during the <i>P. falciparum</i> IDC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 13:57:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/974460", "https://ndownloader.figshare.com/files/974461", "https://ndownloader.figshare.com/files/974462", "https://ndownloader.figshare.com/files/974463", "https://ndownloader.figshare.com/files/974464", "https://ndownloader.figshare.com/files/974465", "https://ndownloader.figshare.com/files/974466", "https://ndownloader.figshare.com/files/974467", "https://ndownloader.figshare.com/files/974468"], "description"=>"<div><p>Epigenetic mechanisms are emerging as one of the major factors of the dynamics of gene expression in the human malaria parasite, <i>Plasmodium falciparum</i>. To elucidate the role of chromatin remodeling in transcriptional regulation associated with the progression of the <i>P. falciparum</i> intraerythrocytic development cycle (IDC), we mapped the temporal pattern of chromosomal association with histone H3 and H4 modifications using ChIP-on-chip. Here, we have generated a broad integrative epigenomic map of twelve histone modifications during the <i>P. falciparum</i> IDC including H4K5ac, H4K8ac, H4K12ac, H4K16ac, H3K9ac, H3K14ac, H3K56ac, H4K20me1, H4K20me3, H3K4me3, H3K79me3 and H4R3me2. While some modifications were found to be associated with the vast majority of the genome and their occupancy was constant, others showed more specific and highly dynamic distribution. Importantly, eight modifications displaying tight correlations with transcript levels showed differential affinity to distinct genomic regions with H4K8ac occupying predominantly promoter regions while others occurred at the 5′ ends of coding sequences. The promoter occupancy of H4K8ac remained unchanged when ectopically inserted at a different locus, indicating the presence of specific DNA elements that recruit histone modifying enzymes regardless of their broad chromatin environment. In addition, we showed the presence of multivalent domains on the genome carrying more than one histone mark, highlighting the importance of combinatorial effects on transcription. Overall, our work portrays a substantial association between chromosomal locations of various epigenetic markers, transcriptional activity and global stage-specific transitions in the epigenome.</p> </div>", "links"=>[], "tags"=>["epigenetic", "malaria", "parasite"], "article_id"=>642483, "categories"=>["Biotechnology", "Genetics", "Microbiology"], "users"=>["Archna P. Gupta", "Wai Hoe Chin", "Lei Zhu", "Sachel Mok", "Yen-Hoon Luah", "Eng-How Lim", "Zbynek Bozdech"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003170.s001", "https://dx.doi.org/10.1371/journal.ppat.1003170.s002", "https://dx.doi.org/10.1371/journal.ppat.1003170.s003", "https://dx.doi.org/10.1371/journal.ppat.1003170.s004", "https://dx.doi.org/10.1371/journal.ppat.1003170.s005", "https://dx.doi.org/10.1371/journal.ppat.1003170.s006", "https://dx.doi.org/10.1371/journal.ppat.1003170.s007", "https://dx.doi.org/10.1371/journal.ppat.1003170.s008", "https://dx.doi.org/10.1371/journal.ppat.1003170.s009"], "stats"=>{"downloads"=>18, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Dynamic_Epigenetic_Regulation_of_Gene_Expression_during_the_Life_Cycle_of_Malaria_Parasite_Plasmodium_falciparum__/642483", "title"=>"Dynamic Epigenetic Regulation of Gene Expression during the Life Cycle of Malaria Parasite <em>Plasmodium falciparum</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-03-01 14:01:56"}

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Relative Metric

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