Expression Atlas of the Deubiquitinating Enzymes in the Adult Mouse Retina, Their Evolutionary Diversification and Phenotypic Roles
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{"title"=>"Expression Atlas of the Deubiquitinating Enzymes in the Adult Mouse Retina, Their Evolutionary Diversification and Phenotypic Roles", "type"=>"journal", "authors"=>[{"first_name"=>"Mariona", "last_name"=>"Esquerdo", "scopus_author_id"=>"57186655000"}, {"first_name"=>"Xavier", "last_name"=>"Grau-Bové", "scopus_author_id"=>"55980817300"}, {"first_name"=>"Alejandro", "last_name"=>"Garanto", "scopus_author_id"=>"26025578600"}, {"first_name"=>"Vasileios", "last_name"=>"Toulis", "scopus_author_id"=>"57186687400"}, {"first_name"=>"Sílvia", "last_name"=>"Garcia-Monclús", "scopus_author_id"=>"56669739700"}, {"first_name"=>"Erica", "last_name"=>"Millo", "scopus_author_id"=>"57186417700"}, {"first_name"=>"Ma José", "last_name"=>"López-Iniesta", "scopus_author_id"=>"57186712600"}, {"first_name"=>"Víctor", "last_name"=>"Abad-Morales", "scopus_author_id"=>"57186697300"}, {"first_name"=>"Iñaki", "last_name"=>"Ruiz-Trillo", "scopus_author_id"=>"6508015789"}, {"first_name"=>"Gemma", "last_name"=>"Marfany", "scopus_author_id"=>"6603803974"}], "year"=>2016, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84961262797", "pui"=>"608997102", "scopus"=>"2-s2.0-84961262797", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0150364", "pmid"=>"26934049"}, "id"=>"b25dc516-11ad-38fc-a9b6-7b26c7aff499", "abstract"=>"Ubiquitination is a relevant cell regulatory mechanism to determine protein fate and function. Most data has focused on the role of ubiquitin as a tag molecule to target substrates to proteasome degradation, and on its impact in the control of cell cycle, protein homeostasis and cancer. Only recently, systematic assays have pointed to the relevance of the ubiquitin pathway in the development and differentiation of tissues and organs, and its implication in hereditary diseases. Moreover, although the activity and composition of ubiquitin ligases has been largely addressed, the role of the deubiquitinating enzymes (DUBs) in specific tissues, such as the retina, remains mainly unknown. In this work, we undertook a systematic analysis of the transcriptional levels of DUB genes in the adult mouse retina by RT-qPCR and analyzed the expression pattern by in situ hybridization and fluorescent immunohistochemistry, thus providing a unique spatial reference map of retinal DUB expression. We also performed a systematic phylogenetic analysis to understand the origin and the presence/absence of DUB genes in the genomes of diverse animal taxa that represent most of the known animal diversity. The expression landscape obtained supports the potential subfunctionalization of paralogs in those families that expanded in vertebrates. Overall, our results constitute a reference framework for further characterization of the DUB roles in the retina and suggest new candidates for inherited retinal disorders.", "link"=>"http://www.mendeley.com/research/expression-atlas-deubiquitinating-enzymes-adult-mouse-retina-evolutionary-diversification-phenotypic", "reader_count"=>14, "reader_count_by_academic_status"=>{"Researcher"=>3, "Student > Ph. D. Student"=>8, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>3, "Student > Ph. D. Student"=>8, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>9, "Veterinary Science and Veterinary Medicine"=>1}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>9}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Chile"=>1, "Spain"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/4804606"], "description"=>"<p>Most analyzed genes render a consistent expression pattern when comparing mRNA and protein localization in the wild type mouse retina. The merge immunohistochemistry show DUBs immunodetected in red, and nuclei counter-staining with DAPI (in blue). Details in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150364#pone.0150364.s003\" target=\"_blank\">S3 Fig</a>. <b>RPE</b>- Retinal pigmented epithelium; <b>Phr</b>- Photoreceptor cell layer; <b>ONL</b>- Outer nuclear layer; <b>OPL</b>. Outer plexiform layer; <b>INL</b>- Inner nuclear layer, <b>IPL</b>- Inner plexiform layer; <b>GCL</b>- Ganglion cell layer.</p>", "links"=>[], "tags"=>["Adult Mouse Retina", "tissue", "reference", "protein", "ubiquitin", "role", "adult mouse retina", "DUB genes", "expression", "analysis", "Phenotypic Roles Ubiquitination"], "article_id"=>3091186, "categories"=>["Biophysics", "Biochemistry", "Genetics", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology"], "users"=>["Mariona Esquerdo", "Xavier Grau-Bové", "Alejandro Garanto", "Vasileios Toulis", "Sílvia Garcia-Monclús", "Erica Millo", "Ma José López-Iniesta", "Víctor Abad-Morales", "Iñaki Ruiz-Trillo", "Gemma Marfany"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0150364.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Comparison_of_mRNA_and_protein_immunodetection_of_selected_DUBs_in_mouse_retinal_cryosections_/3091186", "title"=>"Comparison of mRNA and protein immunodetection of selected DUBs in mouse retinal cryosections.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-03-02 07:10:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/4804651"], "description"=>"<p>Protein sequences from the catalytic region of each enzyme group were queried in complete genome sequences of 14 animal taxa and aligned. The protein domain architectures including the catalytic and accessory domain motifs are represented next to each DUB member (A, JAMM; B, MJD; C, OTU; D, UCH; and D, USP). Black dots indicate presence of the ortholog, whereas white dots indicate homologs that cannot be confidently assigned to a DUB type (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150364#sec010\" target=\"_blank\">Results</a>). Question marks represent statistically supported clades of uncharacterized DUBs. DUB sequences that are highly similar and cluster closely together appear collapsed under a common name. In general, invertebrates have a single representative member of the collapsed branch, whereas vertebrate genomes show one member of each paralog (species circled in black). <i>Acropora digitifera</i> USP homologs were excluded from the analysis as they impaired the resolution of the USP phylogeny. Genes reported to produce an abnormal neuronal phenotype when mutated are circled in magenta, whilst genes producing abnormal eye or retinal phenotype are circled in green. Genes whose mutation is lethal during developmental stages are circled in blue. An schematic summary of the DUB mRNA localization in the mouse retina (from ISH) is also presented next to the corresponding family. The intensity of the color indicates hybridization signal intensity. Retinal layers appear indicated as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150364#pone.0150364.g002\" target=\"_blank\">Fig 2</a>.</p>", "links"=>[], "tags"=>["Adult Mouse Retina", "tissue", "reference", "protein", "ubiquitin", "role", "adult mouse retina", "DUB genes", "expression", "analysis", "Phenotypic Roles Ubiquitination"], "article_id"=>3091219, "categories"=>["Biophysics", "Biochemistry", "Genetics", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology"], "users"=>["Mariona Esquerdo", "Xavier Grau-Bové", "Alejandro Garanto", "Vasileios Toulis", "Sílvia Garcia-Monclús", "Erica Millo", "Ma José López-Iniesta", "Víctor Abad-Morales", "Iñaki Ruiz-Trillo", "Gemma Marfany"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0150364.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Phylogenetic_analysis_of_DUB_genes_and_neuronal_retinal_phenotype_/3091219", "title"=>"Phylogenetic analysis of DUB genes and neuronal/retinal phenotype.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-03-02 07:10:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/4804345", "https://ndownloader.figshare.com/files/4804360", "https://ndownloader.figshare.com/files/4804384", "https://ndownloader.figshare.com/files/4804399", "https://ndownloader.figshare.com/files/4804426", "https://ndownloader.figshare.com/files/4804441", "https://ndownloader.figshare.com/files/4804459", "https://ndownloader.figshare.com/files/4804474"], "description"=>"<div><p>Ubiquitination is a relevant cell regulatory mechanism to determine protein fate and function. Most data has focused on the role of ubiquitin as a tag molecule to target substrates to proteasome degradation, and on its impact in the control of cell cycle, protein homeostasis and cancer. Only recently, systematic assays have pointed to the relevance of the ubiquitin pathway in the development and differentiation of tissues and organs, and its implication in hereditary diseases. Moreover, although the activity and composition of ubiquitin ligases has been largely addressed, the role of the deubiquitinating enzymes (DUBs) in specific tissues, such as the retina, remains mainly unknown. In this work, we undertook a systematic analysis of the transcriptional levels of DUB genes in the adult mouse retina by RT-qPCR and analyzed the expression pattern by <i>in situ</i> hybridization and fluorescent immunohistochemistry, thus providing a unique spatial reference map of retinal DUB expression. We also performed a systematic phylogenetic analysis to understand the origin and the presence/absence of DUB genes in the genomes of diverse animal taxa that represent most of the known animal diversity. The expression landscape obtained supports the potential subfunctionalization of paralogs in those families that expanded in vertebrates. Overall, our results constitute a reference framework for further characterization of the DUB roles in the retina and suggest new candidates for inherited retinal disorders.</p></div>", "links"=>[], "tags"=>["Adult Mouse Retina", "tissue", "reference", "protein", "ubiquitin", "role", "adult mouse retina", "DUB genes", "expression", "analysis", "Phenotypic Roles Ubiquitination"], "article_id"=>3090982, "categories"=>["Biophysics", "Biochemistry", "Genetics", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology"], "users"=>["Mariona Esquerdo", "Xavier Grau-Bové", "Alejandro Garanto", "Vasileios Toulis", "Sílvia Garcia-Monclús", "Erica Millo", "Ma José López-Iniesta", "Víctor Abad-Morales", "Iñaki Ruiz-Trillo", "Gemma Marfany"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0150364.s001", "https://dx.doi.org/10.1371/journal.pone.0150364.s002", "https://dx.doi.org/10.1371/journal.pone.0150364.s003", "https://dx.doi.org/10.1371/journal.pone.0150364.s004", "https://dx.doi.org/10.1371/journal.pone.0150364.s005", "https://dx.doi.org/10.1371/journal.pone.0150364.s006", "https://dx.doi.org/10.1371/journal.pone.0150364.s007", "https://dx.doi.org/10.1371/journal.pone.0150364.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Expression_Atlas_of_the_Deubiquitinating_Enzymes_in_the_Adult_Mouse_Retina_Their_Evolutionary_Diversification_and_Phenotypic_Roles/3090982", "title"=>"Expression Atlas of the Deubiquitinating Enzymes in the Adult Mouse Retina, Their Evolutionary Diversification and Phenotypic Roles", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2016-03-02 07:10:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/4804687"], "description"=>"<p>Heatmap representing the number of classified genes in each analyzed genome. Increasing intensity reflects increasing number of genes. Only orthologs marked with black dots in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150364#pone.0150364.g004\" target=\"_blank\">Fig 4</a> are considered. <i>Acropora digitifera</i> USP homologs, excluded from the phylogenetic classification, are marked as not analyzed (NA).</p>", "links"=>[], "tags"=>["Adult Mouse Retina", "tissue", "reference", "protein", "ubiquitin", "role", "adult mouse retina", "DUB genes", "expression", "analysis", "Phenotypic Roles Ubiquitination"], "article_id"=>3091255, "categories"=>["Biophysics", "Biochemistry", "Genetics", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology"], "users"=>["Mariona Esquerdo", "Xavier Grau-Bové", "Alejandro Garanto", "Vasileios Toulis", "Sílvia Garcia-Monclús", "Erica Millo", "Ma José López-Iniesta", "Víctor Abad-Morales", "Iñaki Ruiz-Trillo", "Gemma Marfany"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0150364.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Counts_of_classified_DUB_homologs_/3091255", "title"=>"Counts of classified DUB homologs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-03-02 07:10:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/4804549"], "description"=>"<p>Sections from wild-type C57BL/6J mouse retinas were hybridized using digoxigenin-labelled antisense riboprobes. Their corresponding sense riboprobes (negative controls) stained for the same length of time (lower panels in each row) are in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0150364#pone.0150364.s001\" target=\"_blank\">S1 Fig</a>. The antisense <i>Rhodopsin</i> probe, which strongly labels the inner photoreceptor segment, was used as a positive control for the assay. <b>RPE</b>- Retinal pigmented epithelium; <b>Phr</b>- Photoreceptor cell layer; <b>ONL</b>- Outer nuclear layer; <b>OPL</b>. Outer plexiform layer; <b>INL</b>- Inner nuclear layer, <b>IPL</b>- Inner plexiform layer; <b>GCL</b>- Ganglion cell layer.</p>", "links"=>[], "tags"=>["Adult Mouse Retina", "tissue", "reference", "protein", "ubiquitin", "role", "adult mouse retina", "DUB genes", "expression", "analysis", "Phenotypic Roles Ubiquitination"], "article_id"=>3091144, "categories"=>["Biophysics", "Biochemistry", "Genetics", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology"], "users"=>["Mariona Esquerdo", "Xavier Grau-Bové", "Alejandro Garanto", "Vasileios Toulis", "Sílvia Garcia-Monclús", "Erica Millo", "Ma José López-Iniesta", "Víctor Abad-Morales", "Iñaki Ruiz-Trillo", "Gemma Marfany"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0150364.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_i_In_situ_i_hybridization_of_genes_encoding_DUB_enzymes_on_retinal_cryosections_/3091144", "title"=>"<i>In situ</i> hybridization of genes encoding DUB enzymes on retinal cryosections.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-03-02 07:10:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/4804513"], "description"=>"<p>Gene expression values are the average of three independent samples (measured in three replicates), each sample contained retinas from three individuals. The expression levels are obtained as a ratio with <i>Gapdh</i> expression (used for normalization) per 10<sup>4</sup>. The Z-score has been calculated for the whole set of genes per each sample, and mean and standard deviation has been obtained, so that the results can be directly compared among them. Negative values indicate when genes are expressed below the global mean of the gene expression obtained in the analysis, and positive values when genes are more highly expressed. To simplify the comparison, the graph starts at the negative values, being 0 the mean value of gene expression for the whole set of genes (87 in total) in each sample. <b>JAMM</b>- JAB1/MPN/MOV34 motif proteases; <b>MJD</b>- Machado-Joseph Disease protein domain proteases; <b>UCH</b>- Ubiquitin C-Terminal Hydrolases; <b>OTU</b>- Ovarian Tumor proteases; <b>USP</b>- Ubiquitin-Specific Proteases.</p>", "links"=>[], "tags"=>["Adult Mouse Retina", "tissue", "reference", "protein", "ubiquitin", "role", "adult mouse retina", "DUB genes", "expression", "analysis", "Phenotypic Roles Ubiquitination"], "article_id"=>3091102, "categories"=>["Biophysics", "Biochemistry", "Genetics", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology"], "users"=>["Mariona Esquerdo", "Xavier Grau-Bové", "Alejandro Garanto", "Vasileios Toulis", "Sílvia Garcia-Monclús", "Erica Millo", "Ma José López-Iniesta", "Víctor Abad-Morales", "Iñaki Ruiz-Trillo", "Gemma Marfany"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0150364.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Relative_expression_levels_of_the_five_subfamilies_of_DUB_enzymes_/3091102", "title"=>"Relative expression levels of the five subfamilies of DUB enzymes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-03-02 07:10:46"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}

Relative Metric

{"start_date"=>"2016-01-01T00:00:00Z", "end_date"=>"2016-12-31T00:00:00Z", "subject_areas"=>[]}
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