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{"title"=>"The Specification and Global Reprogramming of Histone Epigenetic Marks during Gamete Formation and Early Embryo Development in C. elegans", "type"=>"journal", "authors"=>[{"first_name"=>"Mark", "last_name"=>"Samson", "scopus_author_id"=>"54884656700"}, {"first_name"=>"Margaret M.", "last_name"=>"Jow", "scopus_author_id"=>"8652603900"}, {"first_name"=>"Catherine C.L.", "last_name"=>"Wong", "scopus_author_id"=>"25937007700"}, {"first_name"=>"Colin", "last_name"=>"Fitzpatrick", "scopus_author_id"=>"42761427400"}, {"first_name"=>"Aaron", "last_name"=>"Aslanian", "scopus_author_id"=>"8752792800"}, {"first_name"=>"Israel", "last_name"=>"Saucedo", "scopus_author_id"=>"56398184800"}, {"first_name"=>"Rodrigo", "last_name"=>"Estrada", "scopus_author_id"=>"56397781800"}, {"first_name"=>"Takashi", "last_name"=>"Ito", "scopus_author_id"=>"16161533900"}, {"first_name"=>"Sung kyu Robin", "last_name"=>"Park", "scopus_author_id"=>"55178120900"}, {"first_name"=>"John R.", "last_name"=>"Yates", "scopus_author_id"=>"35352109200"}, {"first_name"=>"Diana S.", "last_name"=>"Chu", "scopus_author_id"=>"36819052100"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"600311136", "sgr"=>"84908315044", "pmid"=>"25299455", "scopus"=>"2-s2.0-84908315044", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "doi"=>"10.1371/journal.pgen.1004588", "issn"=>"15537404"}, "id"=>"591b1a3d-4ea9-30d2-a60e-2b0cb07b49c6", "abstract"=>"Author Summary Successful reproduction depends upon the receipt and processing of distinct chromatin packages from sperm and oocytes. This includes not only a unique complement of DNA, but information in the form of proteins, such as histones, that differentially package the DNA in each cell type. For example, histone variants and post-translationally modified histones can carry epigenetic information across generations. Such information is then reprogrammed in the new embryo to ensure proper development. However, it is unclear how many of these marks are established during gamete formation and reprogrammed after fertilization. We define a signature histone variant and post-translational modification profile of sperm chromatin from C. elegans. This profile is established during sperm formation in part by exchanging canonical histones with sperm-specific histone proteins. Histone variants and modifications passed from sperm and oocytes are differentially removed or retained, suggesting that the embryo can reprogram epigenetic information from each parent distinctly. These C. elegans studies reveal that both conserved and novel histone modification and exchange mechanisms are used across diverse species to establish and reprogram epigenetic information.", "link"=>"http://www.mendeley.com/research/specification-global-reprogramming-histone-epigenetic-marks-during-gamete-formation-early-embryo-dev", "reader_count"=>63, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>10, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>10, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>45, "Medicine and Dentistry"=>3, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>45}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "Belgium"=>1, "United States"=>3, "France"=>2}, "group_count"=>5}

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• http://doi.org/10.1534/genetics.118.301353
• http://doi.org/10.1016/j.ydbio.2020.06.008
• http://doi.org/10.5653/cerm.2016.43.2.59
• http://doi.org/10.1152/physrev.00010.2017
• http://doi.org/10.1186/s12915-017-0398-y
• http://doi.org/10.1186/s13148-016-0265-7
• http://doi.org/10.1038/s41598-018-23612-y
• http://doi.org/10.1126/science.aam5339
• http://doi.org/10.1530/REP-15-0562
• http://doi.org/10.1002/em.22203
• http://doi.org/10.1016/j.scitotenv.2019.133835
• http://doi.org/10.1093/biohorizons/hzx007
• http://doi.org/10.1038/s41598-019-55979-x
• http://doi.org/10.1042/BST20190944
• http://doi.org/10.1146/annurev-genet-112618-043505
• http://doi.org/10.7554/eLife.21728

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• {"id"=>"520281157192417280", "text"=>"Global Reprogramming of Histone Epigenetic Marks during Gamete Formation #coolscience http://t.co/W3ITECByMM", "created_at"=>"2014-10-09T18:34:28Z", "user"=>"foodskop", "user_name"=>"foodskop", "user_profile_image"=>"http://pbs.twimg.com/profile_images/192905183/FoodSkopLogo1_normal.jpg"}
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• {"files"=>["https://ndownloader.figshare.com/files/1712289"], "description"=>"<p>+++ high levels, ++ moderate levels, + low levels, − not detectable. The H2Aub profile reflects the staining patterns from E6C5, ABE569, and #308 antibodies except where denoted by (*) which is from E6C5 antibody only.</p><p>Summary of the profiles of histone post-translational modifications during spermatogenesis and after fertilization.</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199776, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.t002", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_the_profiles_of_histone_post_translational_modifications_during_spermatogenesis_and_after_fertilization_/1199776", "title"=>"Summary of the profiles of histone post-translational modifications during spermatogenesis and after fertilization.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712242"], "description"=>"<p><b>A</b>) A schematic of paternal and maternal chromatin processing before and after fertilization. <b>B–F</b>) Immunostaining of embryos in different stages show that HTAS-1 (green in merged images) is retained in paternal (p) chromatin while HTZ-1 (red) is removed from paternal and maternal (m) chromatin in the 1-cell embryo. DNA is shown in blue. The scale bar represents 10 µm and applies to all panels. <b>B</b>) 1-cell embryos after fertilization. The oocyte pronucleus is undergoing meiotic divisions while the paternal pronucleus is decondensing. <b>C</b>) After DNA replication, the pronuclei migrate to the center of the embryo. <b>D</b>) Chromosomes align on the metaphase plate before segregation. <b>E</b>) 2-cell embryos <b>F</b>) 4-cell embryos. P₂ marks the transcriptionally silent P₂ germline precursor cell.</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199744, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.g003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histone_H2A_variants_have_different_fates_in_the_new_embryo_/1199744", "title"=>"Histone H2A variants have different fates in the new embryo.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712287"], "description"=>"<p><b>A)</b> Schematic of overlapping stages that restructure sperm chromatin to establish paternal epigenetic information during spermatogenesis. Bars represent the presence and levels of key markers, the vertical red line represents the point fertilization occurs. The stages include: 1) H2Aub removal from chromatin (yellow) as HTAS-1 (green) is incorporated and retained in the new embryo. 2) Removal of many histone PTMs (pink) prior to meiotic divisions that result in the erasure of paternal epigenetic marks. Some histone PTMs are retained (purple). 3) Putative <i>C. elegans</i> protamines, SPCH-1, 2, 3 (SPCH, blue) begin incorporating during meiosis and are found at high levels in spermatids. <b>B</b> and <b>C</b>) Schematic comparison of key events during spermatogenesis between <b>B</b>) <i>C. elegans</i> and <b>C</b>) mouse (inspired by <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588-Rathke2\" target=\"_blank\">[92]</a>). Notably, HTAS-1 is incorporated and retained in <i>C. elegans</i> while some histone variants are transiently incorporated to facilitate transition and protamine incorporation in mouse. Also, the post-meiotic transcriptional burst and histone hyperacetylation seen during mouse spermatogenesis are not observed during <i>C. elegans</i> spermatogenesis.</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199774, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.g007", "stats"=>{"downloads"=>3, "page_views"=>126, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_stages_of_chromatin_remodeling_events_in_C_elegans_during_spermatogenesis_and_post_fertilization_/1199774", "title"=>"Summary of stages of chromatin remodeling events in <i>C. elegans</i> during spermatogenesis and post-fertilization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712281"], "description"=>"<p>Immunostaining of dissected and fixed hermaphrodite gonads with antibodies specific to methylated histones (green) and DNA stained with DAPI (red). Before fertilization, oocytes are numbered with the −1 oocyte adjacent to the spermatheca. Polar bodies are denoted by ‘pb’, ‘mat’ is maternal, ‘pat’ is paternal. Scale bars represent 10 µm for all panels. <b>A</b>) H3K36me1 levels are high on both pronuclei after fertilization but absent on the paternal X chromosome, which is shown enlarged in the inset (top is merged image, bottom is H3K36me1 staining shown in grayscale). <b>B</b>) H4K20me1 is detectable as small foci on both pronuclei after fertilization with levels increasing on all chromosomes following oocyte meiosis. <b>C</b>) H3K79me2 levels are high on both pronuclei, low in 1 to 4-cell stage embryos, then high after the 16-cell stage. <b>D</b>) H3K79me3 is present on the maternal pronucleus but not the paternal after fertilization. Levels of H3K79me3 are very low after oocyte meiotic divisions and rise again after the 8-cell stage.</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199771, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.g006", "stats"=>{"downloads"=>0, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histone_methylation_dynamics_on_the_paternal_and_maternal_chromatin_in_the_embryo_/1199771", "title"=>"Histone methylation dynamics on the paternal and maternal chromatin in the embryo.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712215"], "description"=>"<p><b>A–E</b>) Western blot analysis of sperm and embryo lysates loaded with equivalent amounts of DNA. <b>A</b>) Histone H3: 12, 24, 60 and 120 ng; <b>B</b>) Histone H4: 24, 48, 120, and 240 ng; <b>C</b>) HTZ-1: 24, 48, 120, and 240 ng; <b>D</b>) HTAS-1: 12, 24, 60 and 120 ng; <b>E</b>) SPCH-1, 2, 3: 12, 24, 60 and 120 ng. Bands shown were quantified using ImageJ software (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#s4\" target=\"_blank\">Methods</a>). <b>F</b>) Western analysis detection of histone post-translational modification (PTMs) in acid-solubilized sperm and embryo chromatin samples. The left panel shows western signals for the histone PTMs indicated. Right panels show spectral counts for histone PTMs identified by MuDPIT analysis (from <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen-1004588-t001\" target=\"_blank\">Table 1</a>). Green text indicates western and proteomic identification correspond. Black text indicates western and proteomic identification did not correspond. ‘na’ is not applicable because identification by proteomics of ubiquitination was not included in PTM counts (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#s4\" target=\"_blank\">Methods</a>). The anti-H2AK119ub antibody (#87, see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588.s020\" target=\"_blank\">Table S7</a>) recognizes the corresponding residue K120 in <i>C. elegans</i> (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588.s013\" target=\"_blank\">File S5</a>).</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199718, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.g001", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Canonical_histones_are_retained_in_C_elegans_sperm_/1199718", "title"=>"Canonical histones are retained in <i>C. elegans</i> sperm.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712230"], "description"=>"<p>Immunolocalization of isolated and fixed <i>C. elegans</i> male gonads. <b>A</b>) DNA stained with DAPI (blue), HTAS-1 (green), HTZ-1 (red), merged image of HTAS-1 (green), HTZ-1 (red) and DAPI (blue). Scale bar represents 50 µm. <b>B–E</b>) Immunostaining of individual nuclei from late stages of sperm formation (as found in the proximal end of the gonad marked with the dotted line in A). The scale bar represents 2 µm and applies to all panels in B–F. <b>B</b>) Histone H3 dimethylated at lysine 9 (H3K9me2), which marks the X chromosome (white arrows). <b>C</b>) HTZ-1. <b>D</b>) HTAS-1. Yellow arrows mark regions of under-representation of HTAS-1 and HTZ-1 that are not the X chromosome. <b>E</b>) HTZ-1 and HTAS-1 are detectable immediately after meiotic divisions as sperm chromatin condenses. Contrast-adjusted black and white images of DNA, HTZ-1, and HTAS-1 staining of the early spermatid nuclei shown in panels C and D that show HTZ-1 and HTAS-1 are detectable. See <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588.s002\" target=\"_blank\">Figure S2</a> for contrast-adjusted images of later spermatid nuclei. <b>F</b>) SPCH proteins (SPCH-1, 2, 3) (green) are detectable on DNA as sperm DNA condenses for meiotic divisions. Levels of SPCH proteins increase dramatically after meiosis, particularly around spermatid DNA.</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199732, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.g002", "stats"=>{"downloads"=>0, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HTAS_1_is_incorporated_as_sperm_chromosomes_condense_/1199732", "title"=>"HTAS-1 is incorporated as sperm chromosomes condense.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712299", "https://ndownloader.figshare.com/files/1712300", "https://ndownloader.figshare.com/files/1712301", "https://ndownloader.figshare.com/files/1712302", "https://ndownloader.figshare.com/files/1712303", "https://ndownloader.figshare.com/files/1712304", "https://ndownloader.figshare.com/files/1712305", "https://ndownloader.figshare.com/files/1712306", "https://ndownloader.figshare.com/files/1712307", "https://ndownloader.figshare.com/files/1712308", "https://ndownloader.figshare.com/files/1712309", "https://ndownloader.figshare.com/files/1712310", "https://ndownloader.figshare.com/files/1712311", "https://ndownloader.figshare.com/files/1712312", "https://ndownloader.figshare.com/files/1712313", "https://ndownloader.figshare.com/files/1712314", "https://ndownloader.figshare.com/files/1712315", "https://ndownloader.figshare.com/files/1712316", "https://ndownloader.figshare.com/files/1712317", "https://ndownloader.figshare.com/files/1712318", "https://ndownloader.figshare.com/files/1712319"], "description"=>"<div><p>In addition to the DNA contributed by sperm and oocytes, embryos receive parent-specific epigenetic information that can include histone variants, histone post-translational modifications (PTMs), and DNA methylation. However, a global view of how such marks are erased or retained during gamete formation and reprogrammed after fertilization is lacking. To focus on features conveyed by histones, we conducted a large-scale proteomic identification of histone variants and PTMs in sperm and mixed-stage embryo chromatin from <i>C. elegans</i>, a species that lacks conserved DNA methylation pathways. The fate of these histone marks was then tracked using immunostaining. Proteomic analysis found that sperm harbor ∼2.4 fold lower levels of histone PTMs than embryos and revealed differences in classes of PTMs between sperm and embryos. Sperm chromatin repackaging involves the incorporation of the sperm-specific histone H2A variant HTAS-1, a widespread erasure of histone acetylation, and the retention of histone methylation at sites that mark the transcriptional history of chromatin domains during spermatogenesis. After fertilization, we show HTAS-1 and 6 histone PTM marks distinguish sperm and oocyte chromatin in the new embryo and characterize distinct paternal and maternal histone remodeling events during the oocyte-to-embryo transition. These include the exchange of histone H2A that is marked by ubiquitination, retention of HTAS-1, removal of the H2A variant HTZ-1, and differential reprogramming of histone PTMs. This work identifies novel and conserved features of paternal chromatin that are specified during spermatogenesis and processed in the embryo. Furthermore, our results show that different species, even those with diverged DNA packaging and imprinting strategies, use conserved histone modification and removal mechanisms to reprogram epigenetic information.</p></div>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199786, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004588.s001", "https://dx.doi.org/10.1371/journal.pgen.1004588.s002", "https://dx.doi.org/10.1371/journal.pgen.1004588.s003", "https://dx.doi.org/10.1371/journal.pgen.1004588.s004", "https://dx.doi.org/10.1371/journal.pgen.1004588.s005", "https://dx.doi.org/10.1371/journal.pgen.1004588.s006", "https://dx.doi.org/10.1371/journal.pgen.1004588.s007", "https://dx.doi.org/10.1371/journal.pgen.1004588.s008", "https://dx.doi.org/10.1371/journal.pgen.1004588.s009", "https://dx.doi.org/10.1371/journal.pgen.1004588.s010", "https://dx.doi.org/10.1371/journal.pgen.1004588.s011", "https://dx.doi.org/10.1371/journal.pgen.1004588.s012", "https://dx.doi.org/10.1371/journal.pgen.1004588.s013", "https://dx.doi.org/10.1371/journal.pgen.1004588.s014", "https://dx.doi.org/10.1371/journal.pgen.1004588.s015", "https://dx.doi.org/10.1371/journal.pgen.1004588.s016", "https://dx.doi.org/10.1371/journal.pgen.1004588.s017", "https://dx.doi.org/10.1371/journal.pgen.1004588.s018", "https://dx.doi.org/10.1371/journal.pgen.1004588.s019", "https://dx.doi.org/10.1371/journal.pgen.1004588.s020", "https://dx.doi.org/10.1371/journal.pgen.1004588.s021"], "stats"=>{"downloads"=>53, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Specification_and_Global_Reprogramming_of_Histone_Epigenetic_Marks_during_Gamete_Formation_and_Early_Embryo_Development_in_C_elegans_/1199786", "title"=>"The Specification and Global Reprogramming of Histone Epigenetic Marks during Gamete Formation and Early Embryo Development in <i>C. elegans</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712254"], "description"=>"<p>Immunostaining of fixed 1-cell embryos. The scale bar represents 10 µm and applies to all panels. The paternal DNA (blue dotted ovals) stained with the DNA dye DAPI (blue) and the monoclonal E6C5 antibody that recognizes H2Aub (green) <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588-Vassilev1\" target=\"_blank\">[73]</a> and the following (in red): <b>A</b>) H2Aub recognized by the ABE569 antibody <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588-Farcas1\" target=\"_blank\">[72]</a>. <b>B</b>) H2Aub recognized by the polyclonal #308 antibody <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588-Nakagawa1\" target=\"_blank\">[54]</a>. <b>C</b>) K48-linkage specific polyubiquitin (Ub-K48) that can target proteins for degradation via the <b>D</b>) proteasome. <b>E</b>) K63-linkage specific polyubiquitin (Ub-K63) tags targets, like <b>F</b>) Membranous Organelles (MOs), for autophagy <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588-AlRawi1\" target=\"_blank\">[76]</a>. The white arrowheads mark regions of staining that does not overlap with H2Aub staining. The overlapping staining suggests that H2Aub may be processed by either autophagy (like MOs) or by the proteasome after fertilization.</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199749, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.g004", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Paternal_histone_H2A_is_ubiquitinated_and_removed_after_fertilization_/1199749", "title"=>"Paternal histone H2A is ubiquitinated and removed after fertilization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712272"], "description"=>"<p>Immunostaining of dissected and fixed hermaphrodite gonads with antibodies against acetylated histones (green) and DNA stained with DAPI (red). Before fertilization, oocytes are numbered with the −1 oocyte adjacent to the spermatheca. Top insets from 1-cell embryos undergoing oocyte meiotic divisions show merged images of enlarged maternal and paternal pronuclei. Bottom insets show acetylated histone staining only. Polar bodies are denoted by ‘pb’, ‘mat’ is maternal, ‘pat’ is paternal. Scale bars represent 10 µm for all panels. <b>A</b>) H4K16ac levels are high in oocytes and the female pronucleus after fertilization, but absent on that paternal pronucleus. Levels are low until the 4-cell stage and are strong by the 16-cell stage. <b>B</b>) H3K27ac is present in oocytes and the female pronucleus but absent on the paternal pronucleus after fertilization. Levels increase gradually to become high in 2-cell embryos. <b>C</b>) H4K5ac <b>D</b>) H4K12ac and <b>E</b>) H2Apan-ac levels are strong in oocytes and the female pronucleus during meiotic divisions but are absent on sperm. Levels increase to become high in 2-cell embryos. <b>F</b>) H2BK12ac (corresponding to H2BK7 in <i>C. elegans</i>, see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588.s013\" target=\"_blank\">File S5</a>) is not detectable in oocytes adjacent to the spermatheca or on maternal and paternal pronuclei after fertilization. Levels increase in 4-cell embryos. <b>G</b>) H4K8ac and <b>H</b>) H3K23ac are strong on maternal chromatin and weak, but present, on paternal pronuclei. Levels are high on both after meiotic divisions.</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199762, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.g005", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Paternal_and_maternal_chromatin_differ_in_acetylation_status_after_sperm_entry_/1199762", "title"=>"Paternal and maternal chromatin differ in acetylation status after sperm entry.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-09 03:52:16"}
• {"files"=>["https://ndownloader.figshare.com/files/1712288"], "description"=>"<p>Amino acid numbering (starting at the amino acid after the starting methionine, see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#pgen.1004588.s013\" target=\"_blank\">File S5</a>) following the convention of the histone field is shown for <i>C. elegans</i> and the corresponding site in mouse. The number of occurrences (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004588#s4\" target=\"_blank\">Methods</a>) of acetylation (ac), methylation (me), di-methylation (me2), and tri-methylation (me3) are shown for identified modification sites from each histone subtype.</p><p>Post-translational modification sites of core histone proteins identified by MudPIT analysis in embryos and sperm.</p>", "links"=>[], "tags"=>["DNA methylation pathways", "sperm", "histone variants", "histone H 2A", "chromatin", "HTAS", "diverged DNA packaging", "Histone Epigenetic Marks", "histone PTMs", "htz", "embryo", "6 histone PTM marks"], "article_id"=>1199775, "categories"=>["Uncategorised"], "users"=>["Mark Samson", "Margaret M. Jow", "Catherine C. L. Wong", "Colin Fitzpatrick", "Aaron Aslanian", "Israel Saucedo", "Rodrigo Estrada", "Takashi Ito", "Sung-kyu Robin Park", "John R. Yates III", "Diana S. Chu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004588.t001", "stats"=>{"downloads"=>2, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Post_translational_modification_sites_of_core_histone_proteins_identified_by_MudPIT_analysis_in_embryos_and_sperm_/1199775", "title"=>"Post-translational modification sites of core histone proteins identified by MudPIT analysis in embryos and sperm.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-10-09 03:52:16"}

PMC Usage Stats | Further Information

• {"unique-ip"=>"59", "full-text"=>"54", "pdf"=>"24", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"34", "supp-data"=>"220", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
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• {"unique-ip"=>"50", "full-text"=>"39", "pdf"=>"20", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"35", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
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• {"unique-ip"=>"37", "full-text"=>"86", "pdf"=>"17", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"28", "supp-data"=>"17", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
• {"unique-ip"=>"17", "full-text"=>"47", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
• {"unique-ip"=>"27", "full-text"=>"26", "pdf"=>"14", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"18", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
• {"unique-ip"=>"36", "full-text"=>"33", "pdf"=>"16", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"23", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
• {"unique-ip"=>"19", "full-text"=>"16", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
• {"unique-ip"=>"19", "full-text"=>"16", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
• {"unique-ip"=>"24", "full-text"=>"24", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
• {"unique-ip"=>"28", "full-text"=>"24", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"4", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
• {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
• {"unique-ip"=>"19", "full-text"=>"19", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
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• {"unique-ip"=>"17", "full-text"=>"19", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
• {"unique-ip"=>"15", "full-text"=>"12", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"4"}
• {"unique-ip"=>"25", "full-text"=>"19", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"18", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
• {"unique-ip"=>"18", "full-text"=>"22", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
• {"unique-ip"=>"18", "full-text"=>"17", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
• {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
• {"unique-ip"=>"25", "full-text"=>"29", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
• {"unique-ip"=>"28", "full-text"=>"31", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"15", "supp-data"=>"20", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
• {"unique-ip"=>"15", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"20", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
• {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
• {"unique-ip"=>"19", "full-text"=>"17", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"14", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
• {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
• {"unique-ip"=>"13", "full-text"=>"10", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
• {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
• {"unique-ip"=>"22", "full-text"=>"18", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"21", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
• {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"3", "year"=>"2017", "month"=>"6"}
• {"unique-ip"=>"12", "full-text"=>"16", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
• {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
• {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
• {"unique-ip"=>"29", "full-text"=>"46", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
• {"unique-ip"=>"27", "full-text"=>"23", "pdf"=>"15", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
• {"unique-ip"=>"20", "full-text"=>"17", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
• {"unique-ip"=>"20", "full-text"=>"21", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
• {"unique-ip"=>"18", "full-text"=>"20", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
• {"unique-ip"=>"19", "full-text"=>"20", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
• {"unique-ip"=>"13", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
• {"unique-ip"=>"20", "full-text"=>"22", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
• {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
• {"unique-ip"=>"28", "full-text"=>"23", "pdf"=>"13", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"12", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
• {"unique-ip"=>"17", "full-text"=>"18", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
• {"unique-ip"=>"22", "full-text"=>"25", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
• {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
• {"unique-ip"=>"27", "full-text"=>"28", "pdf"=>"9", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
• {"unique-ip"=>"20", "full-text"=>"21", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
• {"unique-ip"=>"17", "full-text"=>"16", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
• {"unique-ip"=>"23", "full-text"=>"24", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
• {"unique-ip"=>"24", "full-text"=>"22", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
• {"unique-ip"=>"20", "full-text"=>"17", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
• {"unique-ip"=>"16", "full-text"=>"19", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
• {"unique-ip"=>"20", "full-text"=>"18", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
• {"unique-ip"=>"13", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
• {"unique-ip"=>"13", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"28", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
• {"unique-ip"=>"14", "full-text"=>"16", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"56", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
• {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
• {"unique-ip"=>"15", "full-text"=>"24", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"22", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
• {"unique-ip"=>"15", "full-text"=>"17", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
• {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
• {"unique-ip"=>"15", "full-text"=>"25", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"43", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
• {"unique-ip"=>"12", "full-text"=>"8", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
• {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
• {"unique-ip"=>"21", "full-text"=>"93", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}
• {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2020", "month"=>"11"}
• {"unique-ip"=>"7", "full-text"=>"4", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
• {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2021", "month"=>"1"}
• {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"1", "year"=>"2021", "month"=>"2"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[291]}, {"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[285]}, {"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[306, 482]}]}

F1000Prime