MU2 and HP1a Regulate the Recognition of Double Strand Breaks in Drosophila melanogaster
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{"title"=>"MU2 and HP1a regulate the recognition of double strand breaks in Drosophila melanogaster", "type"=>"journal", "authors"=>[{"first_name"=>"Raghuvar", "last_name"=>"Dronamraju", "scopus_author_id"=>"26647399300"}, {"first_name"=>"James M.", "last_name"=>"Mason", "scopus_author_id"=>"24356191900"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"21966530", "sgr"=>"80053099460", "doi"=>"10.1371/journal.pone.0025439", "scopus"=>"2-s2.0-80053099460", "pui"=>"362619264", "isbn"=>"10.1371/journal.pone.0025439", "issn"=>"19326203"}, "id"=>"90d21e2b-019b-3cae-87c4-eccd9dd13e67", "abstract"=>"Chromatin structure regulates the dynamics of the recognition and repair of DNA double strand breaks; open chromatin enhances the recruitment of DNA damage response factors, while compact chromatin is refractory to the assembly of radiation-induced repair foci. MU2, an orthologue of human MDC1, a scaffold for ionizing radiation-induced repair foci, is a widely distributed chromosomal protein in Drosophila melanogaster that moves to DNA repair foci after irradiation. Here we show using yeast 2 hybrid screens and co-immunoprecipitation that MU2 binds the chromoshadow domain of the heterochromatin protein HP1 in untreated cells. We asked what role HP1 plays in the formation of repair foci and cell cycle control in response to DNA damage. After irradiation repair foci form in heterochromatin but are shunted to the edge of heterochromatic regions an HP1-dependent manner, suggesting compartmentalized repair. Hydroxyurea-induced repair foci that form at collapsed replication forks, however, remain in the heterochromatic compartment. HP1a depletion in irradiated imaginal disc cells increases apoptosis and disrupts G2/M arrest. Further, cells irradiated in mitosis produced more and brighter repair foci than to cells irradiated during interphase. Thus, the interplay between MU2 and HP1a is dynamic and may be different in euchromatin and heterochromatin during DNA break recognition and repair.", "link"=>"http://www.mendeley.com/research/mu2-hp1a-regulate-recognition-double-strand-breaks-drosophila-melanogaster", "reader_count"=>31, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>13, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Other"=>2, "Student > Master"=>1, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>13, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Other"=>2, "Student > Master"=>1, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>11, "Agricultural and Biological Sciences"=>17}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>11}, "Unspecified"=>{"Unspecified"=>3}}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/732430"], "description"=>"<p>Control or HP1a dsRNA-treated S2 cells were irradiated and stained with propidium iodide and subjected to FACS analysis. Control cells that were unirradiated (A), treated with 5 Gy (B) or 10 Gy (C) of ionizing radiation are shown in the top row. HP1a-dsRNA treated cells with 0 Gy (D), 5 Gy (E) and 10 Gy (F) of IR are shown in the bottom row. G1-phase cells are shown in the red peak to the left, G2/M cells are shown in the red peak to the right, and S-phase cells are shown in the hatched peak. Mitotic cells comprise 3–4% of an asynchronous population of S2 cells. Therefore, most of the cells in the G2/M peak are in G2. Proportions of cells at S and G2/M phases of the cycle are also shown numerically.</p>", "links"=>[], "tags"=>["depletion", "affects", "s2"], "article_id"=>402787, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025439.g007", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HP1a_depletion_affects_cell_cycle_in_S2_cells_/402787", "title"=>"HP1a depletion affects cell cycle in S2 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-23 00:46:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/732531"], "description"=>"<p>Apoptosis and the regulation of mitotic checkpoints in the wing imaginal discs are shown in response to IR. Wing imaginal discs from OreR (control), homozygous <i>mu2<sup>a</sup></i>, heterozygous <i>Su(var)205<sup>05</sup>/CyO</i>, and double mutant <i>Su(var)205<sup>05</sup>/CyO; mu2<sup>a</sup></i> third instar wandering larvae were dissected 3 h after ionizing irradiation and stained with acridine orange. Briefly, the discs were dissected in PBS, rinsed twice with PBS, mounted and observed under a fluorescence microscope. (A) The discs were incubated in acridine orange, which detects apoptosis as green spots in the body of the discs. The data are graphed as the mean + standard deviation of counts from four discs each in three independent experiments. (B) Discs were fixed in 4% paraformaldehyde, block permeabilized and immunostained with anti-PH3 antibody to detect mitosis. The data are graphed as the mean + standard deviation of counts from four discs each in three independent experiments.</p>", "links"=>[], "tags"=>["checkpoint"], "article_id"=>402892, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025439.g008", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Apoptosis_and_G2_M_checkpoint_in_wing_discs_/402892", "title"=>"Apoptosis and G2/M checkpoint in wing discs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-23 00:48:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/731620"], "description"=>"<p>S2 cells were cultured under logarithmic conditions, plated into 8-well chambered plates and exposed to irradiation. Cells received a dose of 25 Gy in 30 seconds and fixed immediately, or 2 or 5 min after irradiation. At 0 min a few small γH2Av foci are found in DAPI-rich regions (first row). After two minutes these grow and show a definite migration (second row). By five minutes the foci are at the periphery of the heterochromatic regions (third row). γH2Av is shown in green. Insets are the fluorescence profiles on γH2Av (green) and DAPI (blue).</p>", "links"=>[], "tags"=>["foci"], "article_id"=>401981, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025439.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expulsion_of_947_H2Av_foci_from_heterochromatin_/401981", "title"=>"Expulsion of γH2Av foci from heterochromatin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-23 00:33:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/731792"], "description"=>"<p>S2 cells were treated with dsRNA specific to HP1a for 3 days. (A) At the end of treatment cells were harvested and used for westerns to detect the change in protein levels or plated for irradiation. The western blot shows a decrease in the level of HP1a, but not HP1b or -c. (B) The effects of HP1a dsRNA on the migration of the γH2Av foci to the periphery of heterochromatin are shown. Cells were treated to 25 Gy (5 Gy/min), fixed using 4% paraformaldehyde and stained with anti-γH2Av (green), anti-HP1a (red), and DAPI (blue). In control cells (upper row) the foci are at the periphery of the DAPI-rich regions (arrow). In HP1a dsRNA treated cells (lower row) the DAPI-rich regions are not well organized, and the repair foci are not expelled from these regions. The extreme DAPI-poor regions (arrowhead) may be nucleoli and do not accumulate repair foci.</p>", "links"=>[], "tags"=>["hp1a", "depletion", "focal"], "article_id"=>402151, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025439.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_HP1a_depletion_on_focal_movement_/402151", "title"=>"Effects of HP1a depletion on focal movement.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-23 00:35:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/731907"], "description"=>"<p>Cultured S2 cells were irradiated with 25 Gy (5 Gy/min), fixed using 4% paraformaldehyde and immunostained using anti-γH2Av antibodies (red), as a mark for DSBs and anti-HP1a antibodies (green). DNA was identified by DAPI (blue). (A) Unirradiated S2 cells immunostained with HP1a and γH2Av antibodies show localization of HP1a to DAPI-rich regions and minimal staining of γH2Av. (B) The HP1a staining pattern relative to DAPI in irradiated cells does not change in comparison to controls, and HP1a does not co-localize with the γH2Av foci upon irradiation. Note that the γH2Av foci are almost always on the periphery of the DAPI-rich regions. (C) Dynamics of HP1a proteins in cells transfected with eGFP-HP1a, treated with a 364 nm laser in a region designated by the arrowhead and followed for 150 sec. HP1a is not recruited to the laser induced breaks, although the overall level of HP1 in the nucleus, especially in the chromocenter, seems to decrease. (D) Dynamics of ATM in cells transfected with EGFP-ATM and treated with a 364 nm laser in a region designated by the arrowhead and followed for 150 sec. ATM can be seen in the treated region by 30 sec and remains for at least another two minutes.</p>", "links"=>[], "tags"=>["recruited", "irif", "induced"], "article_id"=>402269, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025439.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HP1a_is_not_recruited_to_IRIF_and_laser_induced_breaks_/402269", "title"=>"HP1a is not recruited to IRIF and laser induced breaks.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-23 00:37:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/369720", "https://ndownloader.figshare.com/files/369755", "https://ndownloader.figshare.com/files/369815", "https://ndownloader.figshare.com/files/369860"], "description"=>"<div><p>Chromatin structure regulates the dynamics of the recognition and repair of DNA double strand breaks; open chromatin enhances the recruitment of DNA damage response factors, while compact chromatin is refractory to the assembly of radiation-induced repair foci. MU2, an orthologue of human MDC1, a scaffold for ionizing radiation-induced repair foci, is a widely distributed chromosomal protein in <em>Drosophila melanogaster</em> that moves to DNA repair foci after irradiation. Here we show using yeast 2 hybrid screens and co-immunoprecipitation that MU2 binds the chromoshadow domain of the heterochromatin protein HP1 in untreated cells. We asked what role HP1 plays in the formation of repair foci and cell cycle control in response to DNA damage. After irradiation repair foci form in heterochromatin but are shunted to the edge of heterochromatic regions an HP1-dependent manner, suggesting compartmentalized repair. Hydroxyurea-induced repair foci that form at collapsed replication forks, however, remain in the heterochromatic compartment. HP1a depletion in irradiated imaginal disc cells increases apoptosis and disrupts G2/M arrest. Further, cells irradiated in mitosis produced more and brighter repair foci than to cells irradiated during interphase. Thus, the interplay between MU2 and HP1a is dynamic and may be different in euchromatin and heterochromatin during DNA break recognition and repair.</p> </div>", "links"=>[], "tags"=>["mu2", "hp1a", "strand", "breaks"], "article_id"=>133047, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0025439.s001", "https://dx.doi.org/10.1371/journal.pone.0025439.s002", "https://dx.doi.org/10.1371/journal.pone.0025439.s003", "https://dx.doi.org/10.1371/journal.pone.0025439.s004"], "stats"=>{"downloads"=>6, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/MU2_and_HP1a_Regulate_the_Recognition_of_Double_Strand_Breaks_in_Drosophila_melanogaster_/133047", "title"=>"MU2 and HP1a Regulate the Recognition of Double Strand Breaks in <em>Drosophila melanogaster</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-23 00:50:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/732270"], "description"=>"<p>Non-synchronized S2 cells were grown under logarithmic conditions, plated in 8-well chambered slides and exposed to irradiation of 25 Gy (5 Gy/min). Immediately after irradiation S2 cells were immunostained and scored for mitotic cells under a confocal microscope based on PH3 staining. (A) Cells were fixed and stained with anti-HP1a antibody (red) and anti-PH3 (green). Different phases of mitosis are shown. (B) Unirradiated cells stained with anti-γH2Av (red) and anti-PH3 (green) showing an absence of IRIFs. (C) γH2Av foci are formed in irradiated mitotic cells. Staining as in (B). An interphase cell (arrow) and a cell in late prophase (arrowhead) are shown in the upper row. The middle and lower rows show cells in anaphase and telophase. Note that the γH2Av foci are less intense at telophase. (D) Graph showing the intensity of chromosomal γH2Av staining at various stages of mitosis relative to PH3, a marker for mitotic chromosomes.</p>", "links"=>[], "tags"=>["molecular biology", "cell biology"], "article_id"=>402629, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025439.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HP1_and_947_H2Av_dynamics_during_mitosis_/402629", "title"=>"HP1 and γH2Av dynamics during mitosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-23 00:43:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/732055"], "description"=>"<p>Experiments were conducted to understand the interaction between HP1a and MU2 in heterochromatin. Cells were treated with HU for 16 h, fixed in 4% paraformaldehyde and observed using confocal microscopy. Staining of S2 cells using anti-γH2Av or anti-MU2 (green) as a mark for DSBs, anti-HP1a (red), and DAPI (blue). (A) Control S2 cells treated with PBS. (B) γH2Av foci are formed in the DAPI rich regions and co-localize with HP1a protein. Note that the foci formed upon HU treatment are not on the periphery of the DAPI-rich domain. (C) MU2 protein co-localized with the HP1a in HU treated cells.</p>", "links"=>[], "tags"=>["stalled", "replication"], "article_id"=>402419, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025439.g005", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MU2_and_947_H2Av_recognize_stalled_replication_forks_/402419", "title"=>"MU2 and γH2Av recognize stalled replication forks.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-23 00:40:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/731497"], "description"=>"<p>Nuclear extracts were prepared from mGFP-MU2 embryos, and pulldowns were performed using anti-GFP and anti-HP1a antibodies. (A) Western blots were performed to detect HP1a in the immunoprecipitates of mGFP-MU2 from Drosophila embryos. (B) mGFP-MU2 was detected from immunoprecipitation reactions performed using anti-HP1a antibodies from transgenic mGFP-MU2 embryos. (C) The interaction between HP1a and MU2 was detected <i>in vitro</i> in GST pull down experiments using a GST-MU2 fragment as bait and nuclear extracts prepared from S2 cells as prey. A fragment of MU2 (aa 900–1000) was cloned in the pGEX4T1 vector and immobilized on glutathione sepharose beads. Beads were incubated with nuclear extracts from S2 cells, washed extensively and detected by western with anti-HP1a antibodies. (D) S2 cells were transfected with the vectors encoding full length MU2 or truncated MU2 as eGFP tagged constructs, as described in materials and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025439#s4\" target=\"_blank\">methods</a>. Co-localization of eGFP tagged full length MU2 protein (Full-MU2) in the DAPI-rich region is seen in cultured S2 cells (upper row of panels), the MU2 protein deleted of the HP1a binding region (ΔHP1-MU2) is excluded from DAPI-rich regions (lower row of panels). DAPI rich regions corresponding to the HP1a-rich regions.</p>", "links"=>[], "tags"=>["mu2"], "article_id"=>401855, "categories"=>["Molecular Biology", "Cell Biology"], "users"=>["Raghuvar Dronamraju", "James M. Mason"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025439.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interaction_of_MU2_and_HP1a_/401855", "title"=>"Interaction of MU2 and HP1a.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-23 00:30:55"}

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Relative Metric

{"start_date"=>"2011-01-01T00:00:00Z", "end_date"=>"2011-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[301, 573, 717, 840, 956, 1063, 1159, 1248, 1327, 1406, 1478, 1557, 1626, 1700, 1772, 1843, 1910, 1980, 2052, 2124, 2192, 2263, 2328, 2391, 2443, 2496, 2564, 2629, 2698, 2771, 2834, 2897, 2959, 3021, 3077, 3144, 3193]}]}
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