The Stress Response Factors Yap6, Cin5, Phd1, and Skn7 Direct Targeting of the Conserved Co-Repressor Tup1-Ssn6 in S. cerevisiae
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{"title"=>"The stress response factors Yap6, Cin5, Phd1, and Skn7 direct targeting of the conserved co-repressor Tup1-Ssn6 in S. cerevisiae", "type"=>"journal", "authors"=>[{"first_name"=>"Sean E.", "last_name"=>"Hanlon", "scopus_author_id"=>"7003563890"}, {"first_name"=>"Jason M.", "last_name"=>"Rizzo", "scopus_author_id"=>"39561571300"}, {"first_name"=>"Deirdre C.", "last_name"=>"Tatomer", "scopus_author_id"=>"55915793200"}, {"first_name"=>"Jason D.", "last_name"=>"Lieb", "scopus_author_id"=>"7005815585"}, {"first_name"=>"Michael J.", "last_name"=>"Buck", "scopus_author_id"=>"7201363637"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"21552514", "sgr"=>"79955736398", "doi"=>"10.1371/journal.pone.0019060", "scopus"=>"2-s2.0-79955736398", "pui"=>"361723832", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "issn"=>"19326203"}, "id"=>"41b3762d-cc0d-3eab-9dd4-2a517071c5ab", "abstract"=>"Maintaining the proper expression of the transcriptome during development or in response to a changing environment requires a delicate balance between transcriptional regulators with activating and repressing functions. The budding yeast transcriptional co-repressor Tup1-Ssn6 is a model for studying similar repressor complexes in multicellular eukaryotes. Tup1-Ssn6 does not bind DNA directly, but is directed to individual promoters by one or more DNA-binding proteins, referred to as Tup1 recruiters. This functional architecture allows the Tup1-Ssn6 to modulate the expression of genes required for the response to a variety of cellular stresses. To understand the targeting or the Tup1-Ssn6 complex, we determined the genomic distribution of Tup1 and Ssn6 by ChIP-chip. We found that most loci bound by Tup1-Ssn6 could not be explained by co-occupancy with a known recruiting cofactor and that deletion of individual known Tup1 recruiters did not significantly alter the Tup1 binding profile. These observations suggest that new Tup1 recruiting proteins remain to be discovered and that Tup1 recruitment typically depends on multiple recruiting cofactors. To identify new recruiting proteins, we computationally screened for factors with binding patterns similar to the observed Tup1-Ssn6 genomic distribution. Four top candidates, Cin5, Skn7, Phd1, and Yap6, all known to be associated with stress response gene regulation, were experimentally confirmed to physically interact with Tup1 and/or Ssn6. Incorporating these new recruitment cofactors with previously characterized cofactors now explains the majority of Tup1 targeting across the genome, and expands our understanding of the mechanism by which Tup1-Ssn6 is directed to its targets.", "link"=>"http://www.mendeley.com/research/stress-response-factors-yap6-cin5-phd1-skn7-direct-targeting-conserved-corepressor-tup1ssn6-s-cerevi", "reader_count"=>62, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>9, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>4, "Other"=>3, "Student > Master"=>6, "Student > Bachelor"=>10, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>9, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>4, "Other"=>3, "Student > Master"=>6, "Student > Bachelor"=>10, "Professor"=>5}, "reader_count_by_subject_area"=>{"Engineering"=>4, "Unspecified"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>13, "Agricultural and Biological Sciences"=>39, "Chemistry"=>2, "Computer Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>4}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>39}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>13}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>3}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/780556"], "description"=>"<p>282 sites bound by Tup1 during exponential growth in rich media were identified by ChIP-chip using a TAP-tagged protein and whole-genome tiled microarrays. For each target, the Z-score for the highest array element within the peak, as identified by ChIPOTle <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Buck2\" target=\"_blank\">[55]</a> is shown. Mock experiments performed in a wild-type strain lacking a TAP-tagged protein are also shown. The 282 Tup1 bound sites were sorted by p-value and split into three groups: 68 sites that are co-occupied by a known Tup1 recruiting protein (top), 109 sites not co-occupied by a known recruiting protein (middle), and 105 sites with no available cofactor binding data. Tup1 binding sites without cofactor data were located in regions of the genome that were not present on the microarrays used in the cofactor binding study <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Harbison1\" target=\"_blank\">[30]</a>. Tup1 binding was also measured by ChIP-chip for strains carrying deletions of the known Tup1 recruiting cofactors Aft1, Rfx1, Mig1, Nrg1, Rox1, Sko1, and Sut1. DNA-binding cofactors are shown on the right, with occupancy as determined by ChIP-chip indicated in red (P<0.001 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Harbison1\" target=\"_blank\">[30]</a>). The following number of biological replicates were performed: Tup1, 21; Ssn6, 2; Mock, 4; recruiter deletion strains, 3–4.</p>", "links"=>[], "tags"=>["sites", "bound", "tup1", "co-occupied"], "article_id"=>450924, "categories"=>["Genetics", "Microbiology"], "users"=>["Sean E. Hanlon", "Jason M. Rizzo", "Deirdre C. Tatomer", "Jason D. Lieb", "Michael J. Buck"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019060.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Only_a_fraction_of_sites_bound_by_Tup1_in_rich_media_are_co_occupied_by_known_cofactors_/450924", "title"=>"Only a fraction of sites bound by Tup1 in rich media are co-occupied by known cofactors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-28 00:15:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/390756", "https://ndownloader.figshare.com/files/390813", "https://ndownloader.figshare.com/files/390853", "https://ndownloader.figshare.com/files/390896", "https://ndownloader.figshare.com/files/390972", "https://ndownloader.figshare.com/files/391006", "https://ndownloader.figshare.com/files/391030"], "description"=>"<div><p>Maintaining the proper expression of the transcriptome during development or in response to a changing environment requires a delicate balance between transcriptional regulators with activating and repressing functions. The budding yeast transcriptional co-repressor Tup1-Ssn6 is a model for studying similar repressor complexes in multicellular eukaryotes. Tup1-Ssn6 does not bind DNA directly, but is directed to individual promoters by one or more DNA-binding proteins, referred to as Tup1 recruiters. This functional architecture allows the Tup1-Ssn6 to modulate the expression of genes required for the response to a variety of cellular stresses. To understand the targeting or the Tup1-Ssn6 complex, we determined the genomic distribution of Tup1 and Ssn6 by ChIP-chip. We found that most loci bound by Tup1-Ssn6 could not be explained by co-occupancy with a known recruiting cofactor and that deletion of individual known Tup1 recruiters did not significantly alter the Tup1 binding profile. These observations suggest that new Tup1 recruiting proteins remain to be discovered and that Tup1 recruitment typically depends on multiple recruiting cofactors. To identify new recruiting proteins, we computationally screened for factors with binding patterns similar to the observed Tup1-Ssn6 genomic distribution. Four top candidates, Cin5, Skn7, Phd1, and Yap6, all known to be associated with stress response gene regulation, were experimentally confirmed to physically interact with Tup1 and/or Ssn6. Incorporating these new recruitment cofactors with previously characterized cofactors now explains the majority of Tup1 targeting across the genome, and expands our understanding of the mechanism by which Tup1-Ssn6 is directed to its targets.</p> </div>", "links"=>[], "tags"=>["factors", "skn7", "targeting", "conserved", "co-repressor", "tup1-ssn6"], "article_id"=>137191, "categories"=>["Genetics", "Microbiology"], "users"=>["Sean E. Hanlon", "Jason M. Rizzo", "Deirdre C. Tatomer", "Jason D. Lieb", "Michael J. Buck"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019060.s001", "https://dx.doi.org/10.1371/journal.pone.0019060.s002", "https://dx.doi.org/10.1371/journal.pone.0019060.s003", "https://dx.doi.org/10.1371/journal.pone.0019060.s004", "https://dx.doi.org/10.1371/journal.pone.0019060.s005", "https://dx.doi.org/10.1371/journal.pone.0019060.s006", "https://dx.doi.org/10.1371/journal.pone.0019060.s007"], "stats"=>{"downloads"=>30, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Stress_Response_Factors_Yap6_Cin5_Phd1_and_Skn7_Direct_Targeting_of_the_Conserved_Co_Repressor_Tup1_Ssn6_in_S_cerevisiae_/137191", "title"=>"The Stress Response Factors Yap6, Cin5, Phd1, and Skn7 Direct Targeting of the Conserved Co-Repressor Tup1-Ssn6 in <em>S. cerevisiae</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-04-28 01:59:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/780907"], "description"=>"<p>(A) The average downstream gene expression for the targets (P<0.001) and non-targets (P>0.05) of the four new recruiters in <i>tup1Δ</i> strain is plotted <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Green1\" target=\"_blank\">[7]</a>. The number of sites is listed and error bars represent standard error. The significance for the difference between the bound (P<0.001) and unbound sites (P>0.05) was determined by t-Test; <b>*</b> P<0.001, <b>**</b> P<1×10<sup>−4</sup>, <b>***</b> P<1×10<sup>−5</sup>. (B) Tup1 targets were separated based on the number of recruiters bound (P<0.001; <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Harbison1\" target=\"_blank\">[30]</a>), including the four new candidate recruiters (Cin5, Phd1, Yap6, and Skn7). The average enrichment (Z-score) for Tup1, Ssn6, or Mock experiment for each group is shown. The number of targets in each group is shown in parenthesis and error bars represent standard error. (C) Regression model including new candidate recruiters. This model describes how recruiter occupancies, as measured by ChIP-chip, can be used to predict Tup1 occupancy at a genomic region. (D) The log<sub>2</sub> ratio for each Tup1 recruiting protein is shown on the left, with the parameter estimate for the regression model on top. Tup1 binding predicted by the model is shown with the experimental Tup1 and Ssn6 occupancy. All data is sorted by the experimental Tup1 occupancy.</p>", "links"=>[], "tags"=>["tup1", "recruiters"], "article_id"=>451276, "categories"=>["Genetics", "Microbiology"], "users"=>["Sean E. Hanlon", "Jason M. Rizzo", "Deirdre C. Tatomer", "Jason D. Lieb", "Michael J. Buck"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019060.g005", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_New_Tup1_recruiters_improve_the_model_for_Tup1_recruitment_/451276", "title"=>"New Tup1 recruiters improve the model for Tup1 recruitment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-28 00:21:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/781000"], "description"=>"<p>Regression results for both the initial and final model.</p>", "links"=>[], "tags"=>["genetics and genomics", "microbiology"], "article_id"=>451372, "categories"=>["Genetics", "Microbiology"], "users"=>["Sean E. Hanlon", "Jason M. Rizzo", "Deirdre C. Tatomer", "Jason D. Lieb", "Michael J. Buck"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019060.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regression_results_for_both_the_initial_and_final_model_/451372", "title"=>"Regression results for both the initial and final model.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-04-28 00:22:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/780651"], "description"=>"<p>(A and B) The average enrichment (Z-score) in wild-type and recruiter deletion strains is plotted for (A) Tup1 targets bound (<i>P<</i>0.001) by a given transcription factor <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Harbison1\" target=\"_blank\">[30]</a>, or (B) Tup1 targets containing a binding site (P<0.005) for a given transcription factor <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-MacIsaac1\" target=\"_blank\">[31]</a>. To control for differences in IP efficiency between experiments Tup1 binding values were standardized to wild-type Tup1 binding by scaling Tup1 binding in each deletion strain so that the average Tup1 occupancy across all bound regions is the same for all experiments. The number of Tup1 targets in each group is indicated in parentheses and error bars represent standard error. (C) Tup1 targets were binned based on the number of recruiters bound to the target (P<0.001; <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Harbison1\" target=\"_blank\">[30]</a>). Average enrichment (Z-score) for Tup1, Ssn6, or mock ChIPs for each group was calculated. The number of targets in each group is indicated in parentheses and error bars represent standard error. (D) Tup1 occupancy is plotted for Tup1 bound regulatory regions as a function of the number of bound recruiter proteins (Black) and for all regulatory regions, including the Tup1 bound regions, (Red) as a function of the number transcription factors bound at the regulatory region. The linear regression line and coefficient for both datasets is shown.</p>", "links"=>[], "tags"=>["tup1", "recruiters", "binding", "correlated"], "article_id"=>451019, "categories"=>["Genetics", "Microbiology"], "users"=>["Sean E. Hanlon", "Jason M. Rizzo", "Deirdre C. Tatomer", "Jason D. Lieb", "Michael J. Buck"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019060.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_individual_Tup1_recruiters_has_little_effect_on_Tup1_binding_and_Tup1_binding_is_correlated_with_the_presence_of_multiple_recruiters_/451019", "title"=>"Deletion of individual Tup1 recruiters has little effect on Tup1 binding, and Tup1 binding is correlated with the presence of multiple recruiters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-28 00:16:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/780806"], "description"=>"<p>Strains carrying Myc-tagged candidate recruiters (Cin5, Phd1, Yap6, or Skn7), previously characterized recruiters (Sut1, Nrg1, or Sko1), or a protein that was not predicted to interact with Tup1 (Hap3) were immunoprecipitated with anti-Ssn6 antibodies (A and B), or with anti-HA antibodies (to immunoprecipitate HA-tagged Tup1) (C). Inputs (left) and immunoprecipitated material (right) were immunoblotted with anti-Ssn6 antibody, anti-HA antibody (to detect Tup1), or anti-MYC (to detect recruiter proteins). (D) The interactions between Tup1-Ssn6 and predicted recruiters are not mediated by DNA. Strains carrying a Myc-tagged characterized recruiter (Nrg1) or predicted recruiters (Cin5, Phd1, Yap6, or Skn7) were immunoprecipitated with anti-Ssn6 antibodies in the presence (+) or absence (−) of DNAse I. Inputs (left) and immunoprecipitated material (right) were immunoblotted with anti-Ssn6 antibody (top), anti-HA antibody (middle) or anti-MYC (bottom).</p>", "links"=>[], "tags"=>["recruiters"], "article_id"=>451180, "categories"=>["Genetics", "Microbiology"], "users"=>["Sean E. Hanlon", "Jason M. Rizzo", "Deirdre C. Tatomer", "Jason D. Lieb", "Michael J. Buck"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019060.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Candidate_recruiters_physically_interact_with_Tup1_Ssn6_/451180", "title"=>"Candidate recruiters physically interact with Tup1-Ssn6.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-28 00:19:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/780728"], "description"=>"<p>Tup1 binding data was compared to ChIP-chip data from 204 transcription factors <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Harbison1\" target=\"_blank\">[30]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-MacIsaac1\" target=\"_blank\">[31]</a> and <i>tup1Δ</i> expression data <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Green1\" target=\"_blank\">[7]</a> using five tests (see text and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#s4\" target=\"_blank\">Material and Methods</a> for details). The percentile rank for each test and average percentile rank across all five tests is shown for the top 20 candidate transcription factors. Known Tup1 recruiting proteins are indicated by red text. Transcription factors previously shown to physically interact with Tup1 or Ssn6 are indicated with a black dot <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019060#pone.0019060-Breitkreutz1\" target=\"_blank\">[57]</a> and the transcription factors whose own promoters are bound by Tup1 are indicated by a red dot. Predicted Tup1 recruiters that were studied further are indicated with underlined text.</p>", "links"=>[], "tags"=>["tup1"], "article_id"=>451103, "categories"=>["Genetics", "Microbiology"], "users"=>["Sean E. Hanlon", "Jason M. Rizzo", "Deirdre C. Tatomer", "Jason D. Lieb", "Michael J. Buck"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019060.g003", "stats"=>{"downloads"=>2, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Prediction_of_novel_Tup1_recruiters_/451103", "title"=>"Prediction of novel Tup1 recruiters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-28 00:18:23"}

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