Exon-Level Transcriptome Profiling in Murine Breast Cancer Reveals Splicing Changes Specific to Tumors with Different Metastatic Abilities
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{"title"=>"Exon-Level transcriptome profiling in murine breast cancer reveals splicing changes specific to tumors with different metastatic abilities", "type"=>"journal", "authors"=>[{"first_name"=>"Amandine", "last_name"=>"Bemmo", "scopus_author_id"=>"25653573700"}, {"first_name"=>"Christel", "last_name"=>"Dias", "scopus_author_id"=>"18233286100"}, {"first_name"=>"April A.N.Rose", "last_name"=>"Rose", "scopus_author_id"=>"23969393800"}, {"first_name"=>"Caterina", "last_name"=>"Russo", "scopus_author_id"=>"8064832500"}, {"first_name"=>"Peter", "last_name"=>"Siegel", "scopus_author_id"=>"56876504200"}, {"first_name"=>"Jacek", "last_name"=>"Majewski", "scopus_author_id"=>"35986079400"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-77957772409", "doi"=>"10.1371/journal.pone.0011981", "sgr"=>"77957772409", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"20700505", "issn"=>"19326203", "pui"=>"359742718"}, "id"=>"bc2bad62-60e8-3084-b766-15701e0a4282", "abstract"=>"BACKGROUND Breast cancer is the second most frequent type of cancer affecting women. We are increasingly aware that changes in mRNA splicing are associated with various characteristics of cancer. The most deadly aspect of cancer is metastasis, the process by which cancer spreads from the primary tumor to distant organs. However, little is known specifically about the involvement of alternative splicing in the formation of macroscopic metastases. Our study investigates transcript isoform changes that characterize tumors of different abilities to form growing metastases. METHODS AND FINDINGS To identify alternative splicing events (ASEs) that are associated with the fully metastatic phenotype in breast cancer, we used Affymetrix Exon Microarrays to profile mRNA isoform variations genome-wide in weakly metastatic (168FARN and 4T07) and highly metastatic (4T1) mammary carcinomas. Statistical analysis identified significant expression changes in 7606 out of 155,994 (4%) exons and in 1725 out of 189,460 (1%) intronic regions, which affect 2623 out of 16,654 (16%) genes. These changes correspond to putative alternative isoforms-several of which are novel-that are differentially expressed between tumors of varying metastatic phenotypes. Gene pathway analysis showed that 1224 of genes expressing alternative isoforms were involved in cell growth, cell interactions, cell proliferation, cell migration and cell death and have been previously linked to cancers and genetic disorders. We chose ten predicted splice variants for RT-PCR validation, eight of which were successfully confirmed (MED24, MFI2, SRRT, CD44, CLK1 and HNRNPH1). These include three novel intron retentions in CD44, a gene in which isoform variations have been previously associated with the metastasis of several cancers. CONCLUSION Our findings reveal that various genes are differently spliced and/or expressed in association with the metastatic phenotype of tumor cells. Identification of metastasis-specific isoforms may contribute to the development of improved breast cancer stage identification and targeted therapies.", "link"=>"http://www.mendeley.com/research/exonlevel-transcriptome-profiling-murine-breast-cancer-reveals-splicing-changes-specific-tumors-diff", "reader_count"=>50, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>7, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>2, "Student > Master"=>4, "Other"=>4, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>7, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>2, "Student > Master"=>4, "Other"=>4, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>7}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>3, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>28, "Medicine and Dentistry"=>3, "Sports and Recreations"=>1, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>28}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>4}}, "reader_count_by_country"=>{"United Kingdom"=>2, "France"=>1, "Germany"=>1, "India"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/836953"], "description"=>"<p>I(Ex-Ey): Intron between exon x and exon y.</p><p>The gene name<sup>1</sup>, the probe set ID<sup>2</sup> and the relative probe set location<sup>3</sup> in the gene are indicated. For each pairwise comparison, the T-test p-value<sup>4</sup> and the log<sub>2</sub>(fold-change)<sup>5</sup> are given. The nature of the isoform change<sup>6</sup> is shown (CE: cassette exon, II: intronic sequence inclusion, 3′ UTR: differential 3′ UTR). An existing RefSeq, mRNA, or EST supporting the event is also mentioned<sup>7</sup>.</p>", "links"=>[], "tags"=>["alternatively", "probe"], "article_id"=>507322, "categories"=>["Genetics", "Plant Biology", "Medicine"], "users"=>["Amandine Bemmo", "Christel Dias", "April A. N. Rose", "Caterina Russo", "Peter Siegel", "Jacek Majewski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011981.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_List_of_some_alternatively_expressed_probe_sets_/507322", "title"=>"List of some alternatively expressed probe sets.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-08-06 02:02:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/416910", "https://ndownloader.figshare.com/files/416922", "https://ndownloader.figshare.com/files/416936", "https://ndownloader.figshare.com/files/416955", "https://ndownloader.figshare.com/files/416970", "https://ndownloader.figshare.com/files/416980", "https://ndownloader.figshare.com/files/416998", "https://ndownloader.figshare.com/files/417018", "https://ndownloader.figshare.com/files/417041", "https://ndownloader.figshare.com/files/417086", "https://ndownloader.figshare.com/files/417181"], "description"=>"<div><h3>Background</h3><p>Breast cancer is the second most frequent type of cancer affecting women. We are increasingly aware that changes in mRNA splicing are associated with various characteristics of cancer. The most deadly aspect of cancer is metastasis, the process by which cancer spreads from the primary tumor to distant organs. However, little is known specifically about the involvement of alternative splicing in the formation of macroscopic metastases. Our study investigates transcript isoform changes that characterize tumors of different abilities to form growing metastases.</p><h3>Methods and Findings</h3><p>To identify alternative splicing events (ASEs) that are associated with the fully metastatic phenotype in breast cancer, we used Affymetrix Exon Microarrays to profile mRNA isoform variations genome-wide in weakly metastatic (168FARN and 4T07) and highly metastatic (4T1) mammary carcinomas. Statistical analysis identified significant expression changes in 7606 out of 155,994 (4%) exons and in 1725 out of 189,460 (1%) intronic regions, which affect 2623 out of 16,654 (16%) genes. These changes correspond to putative alternative isoforms—several of which are novel—that are differentially expressed between tumors of varying metastatic phenotypes. Gene pathway analysis showed that 1224 of genes expressing alternative isoforms were involved in cell growth, cell interactions, cell proliferation, cell migration and cell death and have been previously linked to cancers and genetic disorders. We chose ten predicted splice variants for RT-PCR validation, eight of which were successfully confirmed (MED24, MFI2, SRRT, CD44, CLK1 and HNRNPH1). These include three novel intron retentions in CD44, a gene in which isoform variations have been previously associated with the metastasis of several cancers.</p><h3>Conclusion</h3><p>Our findings reveal that various genes are differently spliced and/or expressed in association with the metastatic phenotype of tumor cells. Identification of metastasis-specific isoforms may contribute to the development of improved breast cancer stage identification and targeted therapies.</p></div>", "links"=>[], "tags"=>["exon-level", "transcriptome", "profiling", "murine", "cancer", "reveals", "splicing", "changes", "tumors", "metastatic", "abilities"], "article_id"=>142298, "categories"=>["Genetics", "Cell Biology", "Medicine"], "users"=>["Amandine Bemmo", "Christel Dias", "April A. N. Rose", "Caterina Russo", "Peter Siegel", "Jacek Majewski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0011981.s001", "https://dx.doi.org/10.1371/journal.pone.0011981.s002", "https://dx.doi.org/10.1371/journal.pone.0011981.s003", "https://dx.doi.org/10.1371/journal.pone.0011981.s004", "https://dx.doi.org/10.1371/journal.pone.0011981.s005", "https://dx.doi.org/10.1371/journal.pone.0011981.s006", "https://dx.doi.org/10.1371/journal.pone.0011981.s007", "https://dx.doi.org/10.1371/journal.pone.0011981.s008", "https://dx.doi.org/10.1371/journal.pone.0011981.s009", "https://dx.doi.org/10.1371/journal.pone.0011981.s010", "https://dx.doi.org/10.1371/journal.pone.0011981.s011"], "stats"=>{"downloads"=>46, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Exon_Level_Transcriptome_Profiling_in_Murine_Breast_Cancer_Reveals_Splicing_Changes_Specific_to_Tumors_with_Different_Metastatic_Abilities/142298", "title"=>"Exon-Level Transcriptome Profiling in Murine Breast Cancer Reveals Splicing Changes Specific to Tumors with Different Metastatic Abilities", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-08-06 00:38:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/836723"], "description"=>"<p>Over- or under- expressed genes in 4T1 compared to 168FARN and 4T07 are respectively indicated by a green or a red color of the gene-product icon. The over- or under-expression rate is proportional to the color intensity. Genes that are not colored are those that are not differentially expressed or spliced in our data. The top functions or diseases where the gene-product are involved are cancer, tissue development, cell-to-cell signaling and interaction.</p>", "links"=>[], "tags"=>["molecular", "interactions", "containing", "differentially", "spliced", "genes", "cancer", "tumors", "varying", "metastatic"], "article_id"=>507080, "categories"=>["Genetics", "Plant Biology", "Medicine"], "users"=>["Amandine Bemmo", "Christel Dias", "April A. N. Rose", "Caterina Russo", "Peter Siegel", "Jacek Majewski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011981.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_network_of_molecular_interactions_containing_differentially_spliced_or_expressed_genes_between_breast_cancer_tumors_of_varying_metastatic_phenotype_/507080", "title"=>"A network of molecular interactions containing differentially spliced or expressed genes between breast cancer tumors of varying metastatic phenotype.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-06 01:58:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/836508"], "description"=>"<p>A: Visualization of the expression pattern of MED24 gene showing an alternative start in 4T1. In the top panel, the horizontal scale corresponds to each probe set within the gene from the 5′ to 3′ ends. The blue bars indicate the comparison between 168FARN and 4T1 samples. From top to bottom we plotted the log<sub>2</sub>(fold-change) in expression, between the samples compared, and the statistical significance, −log<sub>10</sub>(p-value). The bottom panel shows the log<sub>10</sub>(expression intensity) of individual probe sets (from the top panel) in samples 168FARN and 4T1. Note that the seven last probe sets and the 3′ UTR region that are over-expressed only in 4T1 indicate an additional isoform in 4T1 starting from exon 20 start. B: Visualization of the expression pattern of SRRT gene showing an intron inclusion. In the top panel, the horizontal scale corresponds to each probe set within the gene from the 5′ to 3′ ends. The blue bars indicate the comparison between 168FARN and 4T1 samples. From top to bottom we plotted the the log<sub>2</sub>(fold-change) in gene-level normalized intensity between the samples compared and the statistical significance, −log<sub>10</sub>(p-value). The bottom panel shows the log<sub>10</sub>(gene-level normalized intensity) of individual probe sets (from the top panel) in samples 168FARN and 4T1. We note an intron inclusion between exons 5 and 6 in samples 168FARN. C: Visualization of the expression pattern of CD44 gene showing several internal cassette exons and three novel intron inclusions. In the top panel, the horizontal scale corresponds to each probe set within the gene from the 5′ to 3′ ends. The blue bars indicate the comparison between 4T07 and 4T1. From top to bottom we plotted the log<sub>2</sub>(fold-change) in expression, between the samples compared. The bottom panel shows a close-up of the CD44 region containing the differentially expressed exons and introns. The first custom track displays the fold-changes and the second custom track displays the sequencing alignment of the three retained introns. We note that in this example, exons 8, 11 and 13, two intronic sequences between exons 5 and 6, and one intronic sequence between exons 9 and 10, are over-expressed in the 4T1 sample.</p>", "links"=>[], "tags"=>["visualization", "patterns", "isoform"], "article_id"=>506871, "categories"=>["Genetics", "Plant Biology", "Medicine"], "users"=>["Amandine Bemmo", "Christel Dias", "April A. N. Rose", "Caterina Russo", "Peter Siegel", "Jacek Majewski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011981.g001", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Examples_of_visualization_of_gene_expression_patterns_showing_isoform_variations_/506871", "title"=>"Examples of visualization of gene expression patterns showing isoform variations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-06 01:54:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/836872"], "description"=>"<p>The gene pathway analysis retrieved biological functions and/or diseases<sup>1</sup> that were most significant to the candidate genes. For each function or disease, the number of significant genes<sup>2</sup> involved is mentioned. The right-tailed Fischer's exact test p-value<sup>3</sup> associated with a biological function or disease determines the likelihood that our set of significant genes has more molecules associated with the biological function or disease than the reference set of molecules is due by random chance. A gene could be involved in more than one function or disease.</p>", "links"=>[], "tags"=>["over-represented", "functions", "diseases", "genes", "isoform", "variations", "whole-transcript"], "article_id"=>507237, "categories"=>["Genetics", "Plant Biology", "Medicine"], "users"=>["Amandine Bemmo", "Christel Dias", "April A. N. Rose", "Caterina Russo", "Peter Siegel", "Jacek Majewski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011981.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Top_height_over_represented_biological_functions_and_diseases_for_genes_with_isoform_variations_or_whole_transcript_expression_differences_/507237", "title"=>"Top height over-represented biological functions and diseases for genes with isoform variations or whole-transcript expression differences.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-08-06 02:00:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/836916"], "description"=>"<p>For each gene, the symbol and the RefSeq accession number<sup>1</sup>, the biological function<sup>2</sup>, the type of splicing event<sup>3</sup> and the pathological implication<sup>4</sup> are given<sup>3</sup>.</p>", "links"=>[], "tags"=>["having", "implications", "processes"], "article_id"=>507283, "categories"=>["Genetics", "Plant Biology", "Medicine"], "users"=>["Amandine Bemmo", "Christel Dias", "April A. N. Rose", "Caterina Russo", "Peter Siegel", "Jacek Majewski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011981.t003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Examples_of_significant_genes_in_the_gene_pathway_having_important_implications_in_normal_biological_processes_and_cancer_/507283", "title"=>"Examples of significant genes, in the gene pathway, having important implications in normal biological processes and cancer.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-08-06 02:01:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/836609"], "description"=>"<p>The tumor samples are plotted on the x-axis, and the number of tumor-specific intron inclusion on the y-axis.</p>", "links"=>[], "tags"=>["tumor-specific", "over-expressed", "intronic"], "article_id"=>506977, "categories"=>["Genetics", "Plant Biology", "Medicine"], "users"=>["Amandine Bemmo", "Christel Dias", "April A. N. Rose", "Caterina Russo", "Peter Siegel", "Jacek Majewski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011981.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proportions_of_tumor_specific_over_expressed_intronic_regions_/506977", "title"=>"Proportions of tumor-specific over-expressed intronic regions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-06 01:56:17"}

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