Mouse HORMAD1 and HORMAD2, Two Conserved Meiotic Chromosomal Proteins, Are Depleted from Synapsed Chromosome Axes with the Help of TRIP13 AAA-ATPase
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{"title"=>"Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase", "type"=>"journal", "authors"=>[{"first_name"=>"Lukasz", "last_name"=>"Wojtasz", "scopus_author_id"=>"23098733400"}, {"first_name"=>"Katrin", "last_name"=>"Daniel", "scopus_author_id"=>"26641039700"}, {"first_name"=>"Ignasi", "last_name"=>"Roig", "scopus_author_id"=>"24345435300"}, {"first_name"=>"Ewelina", "last_name"=>"Bolcun-Filas", "scopus_author_id"=>"16041407200"}, {"first_name"=>"Huiling", "last_name"=>"Xu", "scopus_author_id"=>"55493778700"}, {"first_name"=>"Verawan", "last_name"=>"Boonsanay", "scopus_author_id"=>"11839041200"}, {"first_name"=>"Christian R.", "last_name"=>"Eckmann", "scopus_author_id"=>"35271582500"}, {"first_name"=>"Howard J.", "last_name"=>"Cooke", "scopus_author_id"=>"27170895100"}, {"first_name"=>"Maria", "last_name"=>"Jasin", "scopus_author_id"=>"7005221713"}, {"first_name"=>"Scott", "last_name"=>"Keeney", "scopus_author_id"=>"7005614687"}, {"first_name"=>"Michael J.", "last_name"=>"McKay", "scopus_author_id"=>"7102276356"}, {"first_name"=>"Attila", "last_name"=>"Toth", "scopus_author_id"=>"16551533700"}], "year"=>2009, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537390", "arxiv"=>"http://dx.plos.org/10.1371/journal.pgen.1000702", "scopus"=>"2-s2.0-73449091167", "sgr"=>"73449091167", "pui"=>"358052058", "isbn"=>"1553-7404 (Electronic) 1553-7390 (Linking)", "pmid"=>"19851446", "doi"=>"10.1371/journal.pgen.1000702"}, "id"=>"80eae6e9-5957-3939-bd9d-f1a2c2989580", "abstract"=>"Meiotic crossovers are produced when programmed double-strand breaks (DSBs) are repaired by recombination from homologous chromosomes (homologues). In a wide variety of organisms, meiotic HORMA-domain proteins are required to direct DSB repair towards homologues. This inter-homologue bias is required for efficient homology search, homologue alignment, and crossover formation. HORMA-domain proteins are also implicated in other processes related to crossover formation, including DSB formation, inhibition of promiscuous formation of the synaptonemal complex (SC), and the meiotic prophase checkpoint that monitors both DSB processing and SCs. We examined the behavior of two previously uncharacterized meiosis-specific mouse HORMA-domain proteins--HORMAD1 and HORMAD2--in wild-type mice and in mutants defective in DSB processing or SC formation. HORMADs are preferentially associated with unsynapsed chromosome axes throughout meiotic prophase. We observe a strong negative correlation between SC formation and presence of HORMADs on axes, and a positive correlation between the presumptive sites of high checkpoint-kinase ATR activity and hyper-accumulation of HORMADs on axes. HORMADs are not depleted from chromosomes in mutants that lack SCs. In contrast, DSB formation and DSB repair are not absolutely required for depletion of HORMADs from synapsed axes. A simple interpretation of these findings is that SC formation directly or indirectly promotes depletion of HORMADs from chromosome axes. We also find that TRIP13 protein is required for reciprocal distribution of HORMADs and the SYCP1/SC-component along chromosome axes. Similarities in mouse and budding yeast meiosis suggest that TRIP13/Pch2 proteins have a conserved role in establishing mutually exclusive HORMAD-rich and synapsed chromatin domains in both mouse and yeast. Taken together, our observations raise the possibility that involvement of meiotic HORMA-domain proteins in the regulation of homologue interactions is conserved in mammals.", "link"=>"http://www.mendeley.com/research/mouse-hormad1-hormad2-two-conserved-meiotic-chromosomal-proteins-depleted-synapsed-chromosome-axes-h", "reader_count"=>106, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>9, "Student > Doctoral Student"=>4, "Researcher"=>33, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>1, "Student > Master"=>8, "Other"=>1, "Student > Bachelor"=>7, "Lecturer"=>4, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>9, "Student > Doctoral Student"=>4, "Researcher"=>33, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>1, "Student > Master"=>8, "Other"=>1, "Student > Bachelor"=>7, "Lecturer"=>4, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>20, "Agricultural and Biological Sciences"=>77, "Medicine and Dentistry"=>4, "Social Sciences"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>77}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>20}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"United States"=>6, "United Kingdom"=>2, "Germany"=>1, "India"=>1}, "group_count"=>4}

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  • {"files"=>["https://ndownloader.figshare.com/files/879373"], "description"=>"<p>SYCP3, HORMAD2 and either γH2AX (A, column 1) or SYCP1 (A, columns 2–5, B and C) were detected by IF on nuclear surface spreads of WT spermatocytes. Bars, 10 µm. (A) HORMAD2 preferentially associates with forming AEs and unsynapsed axes during leptotene and zygotene (columns 1 and 2). During pachytene and diplotene, HORMAD2 is present at high levels only on unsynapsed regions of sex chromosomes (asterisks, columns 3 and 4). A slight increase in HORMAD2 staining on desynapsing autosomes can be detected in some diplotene cells on over-exposed images (column 5). Arrows and arrowheads point to synapsed and unsynapsed axes, respectively, in columns 2, 4, and 5. (B) Enlarged view of autosomes and sex chromosomes during pachytene. High levels of HORMAD2 are present on unsynapsed regions of the X and Y. HORMAD2 signal is lower on synapsed autosomes (arrow) than on synapsed regions of sex chromosomes (arrowhead). (C) Enlarged view of zygotene chromosomes. HORMAD2 does not accumulate on SYCP3-rich ends of unsynapsed AEs in the majority of cases (arrows).</p>", "links"=>[], "tags"=>["localization", "wt"], "article_id"=>549822, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g003", "stats"=>{"downloads"=>2, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HORMAD2_localization_in_WT_spermatocytes_/549822", "title"=>"HORMAD2 localization in WT spermatocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 02:43:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/880671"], "description"=>"<p>SYCP3 and either HORMAD1 or HORMAD2 were detected by IF on nuclear spreads of a mixed population of WT and <i>Syce1−/−</i> spermatocytes. Matched exposures are shown for WT zygotene (A and B, top rows) and the <i>Syce1−/−</i> mutant (A and B, bottom rows). Bars, 10 µm.</p>", "links"=>[], "tags"=>["depletion", "hormads", "chromosome"], "article_id"=>551116, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g012", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SC_formation_is_required_for_the_depletion_of_HORMADs_from_chromosome_axes_/551116", "title"=>"SC formation is required for the depletion of HORMADs from chromosome axes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:18:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/435795", "https://ndownloader.figshare.com/files/435834", "https://ndownloader.figshare.com/files/435884", "https://ndownloader.figshare.com/files/435933", "https://ndownloader.figshare.com/files/435994", "https://ndownloader.figshare.com/files/436072", "https://ndownloader.figshare.com/files/436123", "https://ndownloader.figshare.com/files/436176", "https://ndownloader.figshare.com/files/436212"], "description"=>"<div><p>Meiotic crossovers are produced when programmed double-strand breaks (DSBs) are repaired by recombination from homologous chromosomes (homologues). In a wide variety of organisms, meiotic HORMA-domain proteins are required to direct DSB repair towards homologues. This inter-homologue bias is required for efficient homology search, homologue alignment, and crossover formation. HORMA-domain proteins are also implicated in other processes related to crossover formation, including DSB formation, inhibition of promiscuous formation of the synaptonemal complex (SC), and the meiotic prophase checkpoint that monitors both DSB processing and SCs. We examined the behavior of two previously uncharacterized meiosis-specific mouse HORMA-domain proteins—HORMAD1 and HORMAD2—in wild-type mice and in mutants defective in DSB processing or SC formation. HORMADs are preferentially associated with unsynapsed chromosome axes throughout meiotic prophase. We observe a strong negative correlation between SC formation and presence of HORMADs on axes, and a positive correlation between the presumptive sites of high checkpoint-kinase ATR activity and hyper-accumulation of HORMADs on axes. HORMADs are not depleted from chromosomes in mutants that lack SCs. In contrast, DSB formation and DSB repair are not absolutely required for depletion of HORMADs from synapsed axes. A simple interpretation of these findings is that SC formation directly or indirectly promotes depletion of HORMADs from chromosome axes. We also find that TRIP13 protein is required for reciprocal distribution of HORMADs and the SYCP1/SC-component along chromosome axes. Similarities in mouse and budding yeast meiosis suggest that TRIP13/Pch2 proteins have a conserved role in establishing mutually exclusive HORMAD-rich and synapsed chromatin domains in both mouse and yeast. Taken together, our observations raise the possibility that involvement of meiotic HORMA-domain proteins in the regulation of homologue interactions is conserved in mammals.</p></div>", "links"=>[], "tags"=>["hormad1", "conserved", "meiotic", "chromosomal", "are", "depleted", "synapsed", "chromosome", "axes", "trip13", "aaa-atpase"], "article_id"=>145929, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000702.s001", "https://dx.doi.org/10.1371/journal.pgen.1000702.s002", "https://dx.doi.org/10.1371/journal.pgen.1000702.s003", "https://dx.doi.org/10.1371/journal.pgen.1000702.s004", "https://dx.doi.org/10.1371/journal.pgen.1000702.s005", "https://dx.doi.org/10.1371/journal.pgen.1000702.s006", "https://dx.doi.org/10.1371/journal.pgen.1000702.s007", "https://dx.doi.org/10.1371/journal.pgen.1000702.s008", "https://dx.doi.org/10.1371/journal.pgen.1000702.s009"], "stats"=>{"downloads"=>19, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Mouse_HORMAD1_and_HORMAD2_Two_Conserved_Meiotic_Chromosomal_Proteins_Are_Depleted_from_Synapsed_Chromosome_Axes_with_the_Help_of_TRIP13_AAA_ATPase/145929", "title"=>"Mouse HORMAD1 and HORMAD2, Two Conserved Meiotic Chromosomal Proteins, Are Depleted from Synapsed Chromosome Axes with the Help of TRIP13 AAA-ATPase", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-10-23 01:38:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/880521"], "description"=>"<p>Indicated proteins were detected by IF on nuclear spreads of WT zygotene (A, top row), WT pachytene (A, middle row) and <i>Dmc1−/−</i> (A, bottom row, and panel B) spermatocytes. Arrows and arrowheads indicate examples of synapsed and unsynapsed axes, respectively. Bars, 10 µm. (A) Matched exposures of nuclei that were spread and immunostained in parallel are shown. SYCP1 levels on non-homologously synapsed chromosomes in the mutant are comparable to, or slightly lower than, levels on homologously synapsed chromosomes in WT zygotene cells. Overall, the HORMAD1 signal on both unsynapsed and synapsed axes is higher in <i>Dmc1−/−</i> cells than in WT zygotene cells. Nevertheless, HORMAD1 signal is reduced on synapsed axes as compared to unsynapsed axes (n = 100 cells). Asterisk marks sex chromosomes (A, middle row). (B) HORMAD2 signal is depleted from synapsed axes in the mutant (n = 100 cells). (C) and (D) Quantification of SYCP1 and corresponding HORMAD1 or HORMAD2 IF signals on synapsed and unsynapsed chromosome axes (numbers of chromosomes analyzed are indicated on top of the graphs; matched exposures for each category were taken from 15 randomly selected cells for each experiment). Background-corrected total signal intensity of HORMAD1 (C, green), HORMAD2 (D, green) and SYCP1 (C and D, red) are shown for each chromosome axis at the indicated stages. Signal intensity units are arbitrary, and thus can not be compared between panels C and D. Signal intensities are plotted on a logarithmic scale to allow comparison of both high and low levels of signal. Chromosomes with background level staining are plotted on the X axis. Median signal intensities are marked by horizontal lines.</p>", "links"=>[], "tags"=>["depleted", "axes", "non-homologous", "sc"], "article_id"=>550970, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g011", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HORMADs_are_depleted_from_axes_that_undergo_non_homologous_SC_formation_in_Dmc1_8722_8722_mutants_/550970", "title"=>"HORMADs are depleted from axes that undergo non-homologous SC formation in <i>Dmc1−/−</i> mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:16:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/879511"], "description"=>"<p>SYCP3, HORMAD1 and HORMAD2 were detected by IF on nuclear surface spreads of WT spermatocytes of the indicated stages. Both single-channel and merged images are shown. Despite extensive co-localization of HORMAD1 and -2, their patterns differ during zygotene and diplotene. High HORMAD2 levels often persist on synapsed chromosome axes that show little HORMAD1 staining (B). In diplotene, HORMAD1 accumulates to high levels on desynapsing autosomes, while HORMAD2 levels are high only on sex chromosome axes (D). Bars, 10 µm. (E) Quantification of HORMAD1 and -2 localization differences on “Y”-shaped zygotene chromosome axes marked by SYCP3. HORMAD1 and -2 largely co-localize and both appear to be depleted to similar extents from synapsed axes on 71.5% of “Y”-shaped chromosomes (brown-framed cartoon, bar and image). However, in 28.5% of the cases, high HORMAD2 levels are observed further along the synapsed axes (green-framed cartoon, bar and image). (F) Quantification of overlap between high levels of HORMADs on axes and SYCP1 staining. Close to the branching point of ”Y”-shaped zygotene chromosomes, high levels of HORMAD1 and -2 are observed on synapsed axes in 10% and 36% of cases, respectively (green-framed cartoon and bars). HORMAD1 and -2 levels decline at the branching point of ”Y”-shaped zygotene chromosomes in 71.9% and 51.2% of cases, respectively (orange-framed cartoon and bars). HORMAD1 and -2 declines at a distance from the branching point of chromosomes in 18.5% and 12.8% of the cases, respectively (red-framed cartoon and bars).</p>", "links"=>[], "tags"=>["hormad2", "depleted", "synapsed"], "article_id"=>549959, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g004", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HORMAD1_and_HORMAD2_are_depleted_with_different_timing_from_synapsed_axes_/549959", "title"=>"HORMAD1 and HORMAD2 are depleted with different timing from synapsed axes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 02:45:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/879086"], "description"=>"<p>Cryo-sections of adult testis were immunostained with anti-SYCP3 and either anti-HORMAD1 (A–C) or anti-HORMAD2 (D–F) antibodies. DNA was detected by DAPI. Overview of several immunostained tubules is shown in A and D. Epithelial cycle stages (Roman numerals) of testis tubules were determined based on SYCP3 localization pattern and DNA staining. HORMAD1/2 levels are highest in nuclei of early/mid pachytene cells (tubule stages I–IV) and decrease as cells progress to late-pachytene and diplotene (tubule stages VIII–XI). Bars are 100 µm in A and D, 10 µm in B, C, E and F. Boxes 1 and 2 from Panel A are shown at higher magnification in B and C. High HORMAD1 levels are detected in the nuclei of spermatocytes marked by chromosome axis component SYCP3. Axis-like staining of HORMAD1 is widespread across nuclei in zygotene (C,*) and diplotene (C, arrow). During pachytene, axis-like staining of HORMAD1 is restricted to a small chromatin domain, which appears to be the sex body based on DNA morphology (B, arrow). Boxes 1 and 2 from Panel D are shown at higher magnification in E and F. HORMAD2 is detected in the nuclei of spermatocytes marked by chromosome axis component SYCP3. Axis-like staining of HORMAD2 is widespread across nuclei in zygotene (F,*). During pachytene (E, arrow) and diplotene (F, arrow) the axis-like staining of HORMAD2 is restricted to a small chromatin domain, which appears to be the sex body. No specific accumulation of HORMAD1 and -2 is observed in sperm, spermatid and any testicular somatic cells, e.g.: Sertoli cells (arrowhead in B and E) and myoid cells (+ in B).</p>", "links"=>[], "tags"=>["hormad1", "-2", "restricted", "meiotic", "germ"], "article_id"=>549524, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Testicular_expression_of_HORMAD1_and_2_is_restricted_to_meiotic_germ_cells_/549524", "title"=>"Testicular expression of HORMAD1 and -2 is restricted to meiotic germ cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 02:38:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/880991"], "description"=>"<p>SYCP3, SYCP1 and either HORMAD1 (A) or HORMAD2 (B) were detected on nuclear spreads of <i>Trip13<sup>hypo</sup></i> spermatocytes by IF. High levels of HORMADs remain associated with chromosome axes following SC formation during zygotene and pachytene. No additional accumulation of HORMAD1 and -2 can be observed on desynapsing chromosome axes during diplotene. Arrows and arrowheads point to examples of synapsed and unsynapsed axes, respectively. Asterisks mark the sex chromosomes. Bars, 10 µm.</p>", "links"=>[], "tags"=>["depletion", "hormads", "synapsed", "chromosome"], "article_id"=>551430, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g014", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TRIP13_is_required_for_depletion_of_HORMADs_from_synapsed_chromosome_axes_/551430", "title"=>"TRIP13 is required for depletion of HORMADs from synapsed chromosome axes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:23:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/879748"], "description"=>"<p>Indicated proteins and centromeres were detected by IF on nuclear spreads of male meiotic cells. In pachytene cells (A), low amounts of HORMAD1 remain on the synapsed autosomes, with the highest signal in the vicinity of centromeres. During the first metaphase (B, C) and interkinesis/second prophase (D), SYCP3 marks centromeres and the region between sister centromeres, respectively. HORMAD1 co-localizes with SYCP3 during both stages (B, D), whereas HORMAD2 is detectable only during metaphase I at SYCP3 foci (C). Bars, 10 µm.</p>", "links"=>[], "tags"=>["centromeres"], "article_id"=>550196, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g006", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HORMADs_associate_with_centromeres_during_meiosis_/550196", "title"=>"HORMADs associate with centromeres during meiosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:03:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/880840"], "description"=>"<p>The indicated proteins (SYCP3, SYCP1, γH2AX, and HORMAD1 and -2) were detected by IF on nuclear spreads of <i>Spo11−/−</i> spermatocytes. Examples are indicated of synapsed axes (arrows) and unsynapsed axes (arrowheads). Asterisks indicate pseudo-sex bodies. Bars, 10 µm. (A) Levels of both HORMADs are reduced in regions where SC formation has occurred, even though the SC is frequently if not exclusively between non-homologous axes (n = 100 cells examined). (B, C) HORMAD1/2 levels are higher on unsynapsed vs. synapsed axes both within and outside pseudo-sex bodies, but show hyper-accumulation on axes within pseudo-sex bodies in a subset of cells. The top rows of panels B and C show examples of “pachytene-like” cells (i.e., cells with a pseudo-sex body and extensive synapsis) that have comparable HORMAD levels within vs. outside of the pseudo-sex body. The bottom rows show examples of “pachytene-like” cells that have elevated HORMAD staining of axes within the pseudo-sex body. The percentage of cells in each category is indicated (n = 199 for HORMAD1, n = 144 for HORMAD2).</p>", "links"=>[], "tags"=>["localization", "patterns", "cells", "lacking", "spo11-dependent", "dsb"], "article_id"=>551281, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g013", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HORMAD_localization_patterns_in_cells_lacking_SPO11_dependent_DSB_formation_/551281", "title"=>"HORMAD localization patterns in cells lacking SPO11-dependent DSB formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:21:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/879636"], "description"=>"<p>SYCP3, SYCP1 and either HORMAD1 or -2 were stained on nuclear spreads of WT zygotene and pachytene spermatocytes. Images of 15 cells were captured from each stage with identical camera settings. SYCP1 and HORMAD1 or HORMAD2 IF signal levels were measured on synapsed and unsynapsed chromosome axes (chromosome numbers are indicated on top of the graphs). Background-corrected total signal intensities of HORMAD1 (A, green), HORMAD2 (B, green) and SYCP1 (A and B, red) are shown for each examined chromosome axes at the indicated stages. Units of signal intensities are arbitrary and can not be compared between the two experiments (A and B). Signal intensities are plotted on logarithmic scale to allow comparison of both high and low levels of signal. Chromosomes with background level staining are plotted on the X axis and set to 10<sup>0</sup> = 1 value. Median signal intensities are marked by horizontal lines. (C, D) Negative correlation between HORMAD1/2 and SYCP1 staining on synapsed axes of zygotene chromosomes. HORMAD1 or HORMAD2 signal intensities are plotted against the SYCP1 signal intensities for synapsed regions. Trendlines, Pearson's <i>r</i> values and numbers of chromosomes analyzed are shown in both scatter plots. (E, F) Gradients of HORMAD1/2 staining along synapsing bivalents. Signal intensity profiles of SYCP1 and either HORMAD1 (E) or HORMAD2 (F) along the axes of representative examples of “Y”-shaped chromosomes. The intensity profiles were generated along the dashed lines overlaid on the chromosome images. The chromosome in (F) is an example where HORMAD2 signal intensity is higher on just-synapsed double axes than on unsynapsed single axes. Arrows indicate synaptic branching points.</p>", "links"=>[], "tags"=>["axis-associated", "hormad1", "hormad2"], "article_id"=>550082, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g005", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantification_of_axis_associated_HORMAD1_and_HORMAD2_staining_/550082", "title"=>"Quantification of axis-associated HORMAD1 and HORMAD2 staining.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:01:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/880359"], "description"=>"<p>(A) IF analysis of nuclear spreads from <i>Smc1β−/−</i> spermatocytes. HORMADs persist on unsynapsed axes but are depleted from synapsed regions in cells judged to be equivalent to late zygotene or early pachytene based on the condensation of chromosome axes (n = 100 cells). (B) HORMAD1 and -2 levels are reduced in regions of inappropriate synapsis between sister chromatids in <i>Rec8−/−</i> mutant spermatocytes (n = 100 cells). Arrows and arrowheads point to examples of synapsed and unsynapsed chromosome axes, respectively. Bars, 10 µm.</p>", "links"=>[], "tags"=>["axis", "sc", "sc-defective", "cohesin"], "article_id"=>550809, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g010", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Negative_correlation_between_HORMAD1_2_axis_association_and_SC_formation_in_SC_defective_cohesin_mutants_/550809", "title"=>"Negative correlation between HORMAD1/2 axis association and SC formation in SC-defective cohesin mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:13:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/879969"], "description"=>"<p>SYCP3, HORMAD1 and SYCP1 were detected by IF on nuclear surface spreads of WT oocytes at leptotene (from 16.5 dpc ovaries; A), zygotene (16.5 dpc; B), pachytene (16.5 dpc; C), and diplotene/dictyate (19.5 dpc; D). HORMAD1 preferentially localizes to unsynapsed chromosome axes and is depleted from synapsed axes during zygotene, pachytene and diplotene. HORMAD1 re-accumulates on desynapsing axes in all diplotene stage oocytes (n = 100 cells) and co-localizes with SYCP3 until AEs are disassembled during the dictyate stage (D). Arrows and arrowheads indicate synapsed and unsynapsed axes, respectively. Bars, 10 µm.</p>", "links"=>[], "tags"=>["localization", "wt"], "article_id"=>550419, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g007", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HORMAD1_localization_in_WT_oocytes_/550419", "title"=>"HORMAD1 localization in WT oocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:06:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/879222"], "description"=>"<p>SYCP3, HORMAD1 and either γH2AX (A, columns 1 and 2) or SYCP1 (A, columns 3–5, B and C) were detected by IF on nuclear surface spreads of WT spermatocytes. Bars, 10 µm. (A) HORMAD1 preferentially associates with unsynapsed chromosome axes (arrowheads). During leptotene and zygotene HORMAD1-enriched chromosome axes overlap with γH2AX-enriched chromatin (columns 1 and 2). Arrows point to synapsed axes in columns 3 and 5. Asterisks mark sex chromosomes in columns 4 and 5. (B) Enlarged view of autosomes and sex chromosomes during pachytene. High levels of HORMAD1 are present on unsynapsed regions of X and Y chromosomes. HORMAD1 signal is reduced more on synapsed autosomes (arrow) than on synapsed regions of sex chromosomes (arrowhead). (C) Enlarged view of zygotene chromosomes. HORMAD1 does not accumulate on SYCP3-rich ends of unsynapsed AEs in the majority of cases (arrows).</p>", "links"=>[], "tags"=>["localization", "wt"], "article_id"=>549668, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HORMAD1_localization_in_WT_spermatocytes_/549668", "title"=>"HORMAD1 localization in WT spermatocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 02:41:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/880143"], "description"=>"<p>SYCP3, HORMAD2 and SYCP1 were detected by IF on nuclear surface spreads of WT oocytes at leptotene (16.5 dpc; A), zygotene (16.5 dpc; B), pachytene (16.5 dpc; C), and diplotene/dictyate (19.5 and 21.5 dpc; D). HORMAD2 preferentially localizes to unsynapsed regions of chromosome axes throughout prophase, and is depleted from synapsed axes during zygotene, pachytene and diplotene. HORMAD2 re-accumulates on desynapsing axes in all diplotene stage oocytes (n = 100 cells) and co-localizes with SYCP3 until AEs are disassembled during the dictyate stage (D). Note that HORMAD2 signal is more uneven and more punctate than HORMAD1 during diplotene (compare with <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000702#pgen-1000702-g007\" target=\"_blank\">Figure 7D</a>). Arrows and arrowheads indicate synapsed and unsynapsed axes, respectively. Bars, 10 µm.</p>", "links"=>[], "tags"=>["localization", "wt"], "article_id"=>550593, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g008", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HORMAD2_localization_in_WT_oocytes_/550593", "title"=>"HORMAD2 localization in WT oocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:09:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/880275"], "description"=>"<p>“Standard” nuclear surface spreads (A) and “disrupted” nuclear surface spreads (B) were prepared from WT spermatocytes as described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000702#s4\" target=\"_blank\">Materials and Methods</a>. Indicated proteins were detected by IF. One autosome and the X and Y chromosomes are marked by a, x and y, respectively. Bars, 10 µm. (A) Immunostaining of “standard” nuclear spreads. Enlarged view of the pseudo-autosomal regions is shown. Anti-HORMAD1 immunostaining is much stronger on unsynapsed sex chromosomes than on synapsed autosomes, which are marked by SYCP1 staining (top row) and by accumulation of RPA (bottom row). Strong RPA accumulation is also observed in the synapsed pseudoautosomal region (enlarged box in bottom row) of sex chromosomes. HORMAD1 level is reduced in this region less than on synapsed autosomes (enlarged box top and bottom row). (B) Immunostaining of “disrupted” nuclear spreads. Autosomes that were synapsed in vivo but that had lost synapsis during spreading were identified either by morphology (upper row) or by high intensity RPA staining (bottom row). Disruption of synapsis due to the modified spreading procedure does not lead to an increase in anti-HORMAD1 staining, with anti-HORMAD1 immunostaining continuing to be much stronger on the sex chromosomes than on the autosomes. Sex chromosomes are identified by either their morphology (top row) or by low levels of RPA (bottom row).</p>", "links"=>[], "tags"=>["hormad1", "staining", "synapsed", "axes", "epitope", "masking"], "article_id"=>550719, "categories"=>["Molecular Biology", "Developmental Biology", "Genetics", "Cell Biology"], "users"=>["Lukasz Wojtasz", "Katrin Daniel", "Ignasi Roig", "Ewelina Bolcun-Filas", "Huiling Xu", "Verawan Boonsanay", "Christian R. Eckmann", "Howard J. Cooke", "Maria Jasin", "Scott Keeney", "Michael J. McKay", "Attila Toth"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000702.g009", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reduced_HORMAD1_staining_on_synapsed_axes_is_not_likely_to_be_a_consequence_of_epitope_masking_by_the_SC_/550719", "title"=>"Reduced HORMAD1 staining on synapsed axes is not likely to be a consequence of epitope masking by the SC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-23 00:11:59"}

PMC Usage Stats | Further Information

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