piggyBac Transposon Somatic Mutagenesis with an Activated Reporter and Tracker (PB-SMART) for Genetic Screens in Mice
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{"title"=>"Piggybac transposon somatic mutagenesis with an activated reporter and tracker (PB-SMART) for genetic screens in mice", "type"=>"journal", "authors"=>[{"first_name"=>"Sean F.", "last_name"=>"Landrette", "scopus_author_id"=>"8238733500"}, {"first_name"=>"Jonathan C.", "last_name"=>"Cornett", "scopus_author_id"=>"54388774600"}, {"first_name"=>"Thomas K.", "last_name"=>"Ni", "scopus_author_id"=>"57189849007"}, {"first_name"=>"Marcus W.", "last_name"=>"Bosenberg", "scopus_author_id"=>"6701771116"}, {"first_name"=>"Tian", "last_name"=>"Xu", "scopus_author_id"=>"7401627116"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-80054844707", "sgr"=>"80054844707", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0026650", "pmid"=>"22039523", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"362791003"}, "id"=>"91e7321a-f242-317a-a061-f15ed9cfd410", "abstract"=>"Somatic forward genetic screens have the power to interrogate thousands of genes in a single animal. Retroviral and transposon mutagenesis systems in mice have been designed and deployed in somatic tissues for surveying hematopoietic and solid tumor formation. In the context of cancer, the ability to visually mark mutant cells would present tremendous advantages for identifying tumor formation, monitoring tumor growth over time, and tracking tumor infiltrations and metastases into wild-type tissues. Furthermore, locating mutant clones is a prerequisite for screening and analyzing most other somatic phenotypes. For this purpose, we developed a system using the piggyBac (PB) transposon for somatic mutagenesis with an activated reporter and tracker, called PB-SMART. The PB-SMART mouse genetic screening system can simultaneously induce somatic mutations and mark mutated cells using bioluminescence or fluorescence. The marking of mutant cells enable analyses that are not possible with current somatic mutagenesis systems, such as tracking cell proliferation and tumor growth, detecting tumor cell infiltrations, and reporting tissue mutagenesis levels by a simple ex vivo visual readout. We demonstrate that PB-SMART is highly mutagenic, capable of tumor induction with low copy transposons, which facilitates the mapping and identification of causative insertions. We further integrated a conditional transposase with the PB-SMART system, permitting tissue-specific mutagenesis with a single cross to any available Cre line. Targeting the germline, the system could also be used to conduct F1 screens. With these features, PB-SMART provides an integrated platform for individual investigators to harness the power of somatic mutagenesis and phenotypic screens to decipher the genetic basis of mammalian biology and disease.", "link"=>"http://www.mendeley.com/research/piggybac-transposon-somatic-mutagenesis-activated-reporter-tracker-pbsmart-genetic-screens-mice", "reader_count"=>26, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>18, "Medicine and Dentistry"=>3, "Business, Management and Accounting"=>1, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>18}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}}, "reader_count_by_country"=>{"United States"=>2}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/720480"], "description"=>"<p>(<b>A</b>) Insertions (wide arrows) upstream of the M-isoform of <i>Mitf</i> were mapped from five kidney tumors. (<b>B</b>) Quantitative PCR reveals that <i>Mitf</i> transcripts are upregulated in all five kidney tumors (KT1, KT2, KT3, KT4, and KT5) compared to two wild-type kidneys (wt-K). (<b>C</b>) Kidney tumors possessed similar histological profiles, featuring packets of spindle-shaped epitheliod cells, indicating carcinoma (scale bar, 50 µm). (<b>D</b>) Histological analysis shows SRBC morphology (scale bar, 100 µm). (<b>E</b>) Insertions (wide arrows) in intron 7 or 8 of <i>Gli2</i> were mapped from eleven SRBC tumors.</p>", "links"=>[], "tags"=>["oncogenes", "tumors"], "article_id"=>390846, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas K. Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026650.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_driver_oncogenes_in_solid_tumors_from_Luc_PB_mut_7_Act_PBase_mice_/390846", "title"=>"Identification of driver oncogenes in solid tumors from <i>Luc-PB[mut]7;Act-PBase</i> mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-21 00:14:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/720689"], "description"=>"<p>(<b>A</b>) Luciferase signal labels a melanoma in this <i>Luc-PB[mut]7;Act-PBase;Braf<sup>V600E</sup>;Tyr-CreER</i> mouse (white arrowheads). The left panel shows a light image while the right panel overlays the luciferase signal. (<b>B</b>) Luciferase signal enabled the identification of tumor cell infiltration into distant organs of a <i>Luc-PB[mut]7;Act-PBase;Pten<sup>+/-</sup></i> mouse that developed lymphoma. The enlarged thymus (Thy) and lymph nodes (LN) were strongly luciferase-positive. Strong signal was also seen emanating from a distinct portion of the liver (Liv, white dashed line). (<b>C</b>) H&E staining of liver from the luciferase-positive region reveals extensive lymphocyte infiltration (scale bar, 200 µm).</p>", "links"=>[], "tags"=>["infiltration"], "article_id"=>391049, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas K. Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026650.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tracking_tumor_formation_and_infiltration_with_Luc_PB_mut_7_/391049", "title"=>"Tracking tumor formation and infiltration with <i>Luc-PB[mut]7</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-21 00:17:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/720378"], "description"=>"<p>(<b>A</b>) The Actin promoter (black pointed box) and myc-splice donor sequence (blue box) are engineered in the <i>PB[mut]</i> transposon to ectopically express downstream genes or partial transcripts. A splice acceptor and transcriptional termination sequences (pink box) truncate transcripts initiating upstream of the transposon insertion site. <i>PB[mut]</i> is inserted within an internal TTAA sequence of the luciferase gene to create <i>Luc-PB[mut]</i>. Transposase excises <i>PB[mut]</i> from the luciferase gene, restoring the luciferase expression and thus labeling cells. (<b>B</b>) By <i>ex vivo</i> luciferase imaging, PB mutagenesis occurs in <i>Luc-PB[mut]7;Act-PBase</i> mice (right) but not in single transgenic littermates (left and middle). Units, photons·s<sup>−1</sup>·cm<sup>−2</sup>·sr<sup>−1</sup>.(<b>C</b>) Quantitative PCR analysis of transposon excision in the <i>Luc-PB[mut]7</i> line demonstrates a 30-fold increase in transposition activity between <i>Act-PBase</i> and <i>Act-PBaseER</i> (top). The difference in mutagenesis activity levels driven by <i>Act-PBaseER</i> (middle) and <i>Act-PBase</i> lines (right) can be differentiated by the luciferase PB reporter. Units, photons·s<sup>−1</sup>·cm<sup>−2</sup>·sr<sup>−1</sup>. (<b>D</b>) Tumor-free survival curves over the span of 50 weeks show that <i>Luc-PB[mut]7;Act-PBase</i>(<i>Cre</i>) mice succumb to tumors while <i>Luc-PB[mut]7</i>(<i>Cre</i>) and <i>Act-PBase</i>(<i>Cre</i>) littermates remain relatively tumor-free.</p>", "links"=>[], "tags"=>["inducing", "mutations", "mutagenesis", "levels", "pb", "transposon"], "article_id"=>390726, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas K. Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026650.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simultaneously_inducing_mutations_and_reporting_mutagenesis_activity_levels_with_a_PB_transposon_system_/390726", "title"=>"Simultaneously inducing mutations and reporting mutagenesis activity levels with a PB transposon system.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-21 00:12:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/721049"], "description"=>"<p>Insertional frequency in tumors induced by <i>Luc-PB[mut]7</i> and <i>PB[mut-RFP]7</i>.</p>", "links"=>[], "tags"=>["tumors", "induced"], "article_id"=>391409, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas K. Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026650.t001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Insertional_frequency_in_tumors_induced_by_Luc_PB_mut_7_and_PB_mut_RFP_7_/391409", "title"=>"Insertional frequency in tumors induced by <i>Luc-PB[mut]7</i> and <i>PB[mut-RFP]7</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-21 00:23:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/720772"], "description"=>"<p>(<b>A</b>) Activation of the conditional <i>LSL-PBase</i> enables tissue-specific mutagenesis by crossing transgenic mice to available Cre lines. (<b>B</b>) <i>Luc-PB[mut]7;LSL-PBase;Ksp-Cre</i> transgenics (red bars) undergo PB mutagenesis specifically in the seminal vesicles and kidneys, reported by luciferase signal. Control mouse: <i>Luc-PB[mut]7;LSL-PBase</i> (blue bars). Units, photons·s<sup>−1</sup>·cm<sup>−2</sup>·sr<sup>−1</sup>. (<b>C</b>) PB mutagenesis throughout the skin of <i>Luc-PB[mut]7;LSL-PBase;K14-Cre</i> mice (red bar) is reported by luciferase signal. Control mouse: <i>Luc-PB[mut]7;K14-Cre</i> (blue bar). Units, photons·s<sup>−1</sup>·cm<sup>−2</sup>·sr<sup>−1</sup>. (<b>D</b>) <i>Tyr-CreER</i> conditionally activates <i>Braf<sup>V600E</sup></i> and PB mutagenesis specifically in melanocytes of quadruple transgenic mice (<i>Luc-PB[mut]7;LSL-PBase;Braf<sup>CA</sup>;Tyr-CreER</i>, red bars). The expansion of this cell population at three, nine, and eleven months (left, middle and right, respectively) is tracked <i>ex vivo</i> by luciferase signal. Control mouse: <i>Luc-PB[mut]7;BrafCA;Tyr-CreER</i> (blue bars). Units, photons·s<sup>−1</sup>·cm<sup>−2</sup>·sr<sup>−1</sup>.</p>", "links"=>[], "tags"=>["genetics and genomics", "Computational biology", "pathology"], "article_id"=>391132, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas K. Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026650.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tissue_specific_PB_SMART_/391132", "title"=>"Tissue-specific PB-SMART.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-21 00:18:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/720581"], "description"=>"<p>(<b>A</b>) <i>PB[mut-RFP]</i> couples RFP expression with ectopic expression of a downstream gene or partial gene transcript via the IRES (brown box). CS (purple box) prevents unwanted RFP expression from transgene concatamers. (<b>B</b>) <i>PB[mut-RFP]</i> mobilization in HEK 293 cells induces RFP-positive clones that colocalize with myc-tagged proteins ectopically expressed by the mutator transposon. (<b>C</b>) Transgenic lines carrying two to 200 copies of <i>PB[mut-RFP]</i> were generated. (<b>D</b>) Significant PB transposition-induced embryonic lethality was observed when high-copy lines were crossed to <i>Act-PBase</i>. (<b>E</b>) Low-copy <i>PB[mut-RFP]</i> lines crossed to <i>Act-PBase</i> mobilized the mutator transposon as determined by PCR with primers directed against sequences flanking the transposon. A 212-bp excision product was specifically detected in double transgenics but not in single transgenic littermates. A 700-bp unexcised product was observed in all <i>PB[mut-RFP]</i> mice. (<b>F</b>) Shown here in the dorsal skin of a <i>PB[mut-RFP]2a;Act-PBase</i> mouse, RFP-positive foci can be detected <i>ex vivo</i> over background signal. Units, photons·s<sup>−1</sup>·sr<sup>−1</sup>·ìM<sup>−1</sup>. (<b>G</b>) RFP-marked tumor formation (arrowhead) can be visualized <i>ex vivo</i> as seen in the upper panels showing a <i>PB[mut-RFP]2b;Act-PBase</i> mouse. In the lower panels, a stomach tumor dissected from a <i>PB[mut-RFP]7;Act-PBase</i> mouse is strongly RFP-positive. Units, photons·s<sup>−1</sup>·sr<sup>−1</sup>·µM<sup>−1</sup>.</p>", "links"=>[], "tags"=>["inducing", "mutations", "tracking", "mutated", "cells", "pb", "transposon"], "article_id"=>390937, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas K. Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026650.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simultaneously_inducing_mutations_and_tracking_mutated_cells_with_a_PB_transposon_system_/390937", "title"=>"Simultaneously inducing mutations and tracking mutated cells with a PB transposon system.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-21 00:15:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/721004"], "description"=>"<p>Mutator orientation in tumors induced by <i>Luc-PB[mut]7</i> and <i>PB[mut-RFP]7</i>.</p>", "links"=>[], "tags"=>["tumors", "induced"], "article_id"=>391365, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas K. Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026650.t002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutator_orientation_in_tumors_induced_by_Luc_PB_mut_7_and_PB_mut_RFP_7_/391365", "title"=>"Mutator orientation in tumors induced by <i>Luc-PB[mut]7</i> and <i>PB[mut-RFP]7</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-21 00:22:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/720883"], "description"=>"<p>(<b>A</b>) Luciferase signal marks clones of mutated cells in <i>Luc-PB[mut]7;LSL-PBase;K14-Cre</i> mice. (<b>B</b>) PB-induced alopecia in a <i>PB[mut]7;LSL-PBase;K14-Cre; Pten<sup>lox/+</sup></i> mouse, (yellow dashed line) shows strong luciferase signal corresponding to hair loss (middle). Fully shaved, luciferase signal demarcates the specific region of alopecia (right). (<b>C</b>) Cytokeratin staining (green) of wild-type dorsal skin shows the normal thickness of the mouse epidermis (white arrowhead). DAPI (blue) marks cell nuclei. (<b>D</b>) Staining as in (c) from the region of alopecia reveals substantial thickening of the epidermis (white arrowhead). (<b>E</b>) A transposon insertion upstream of <i>Myc</i> was mapped to the affected region of skin. (<b>F</b>) Skin-specific mutagenesis in <i>Luc-PB[mut]7;LSL-PBase;K14-Cre</i> mice induces tumor formation and luciferase-labeled tumor cells. The white arrow corresponds to region of luciferase signal that develops into a larger tumor over time. Units, photons·s<sup>−1</sup>·cm<sup>−2</sup>·sr<sup>−1</sup>. (<b>G</b>) Insertion sites (wide arrows) in <i>Gli2</i> were mapped in multiple skin tumors. (<b>H</b>) By quantitative PCR, <i>Gli2</i> transcripts were upregulated in each skin tumor (BCC1, BCC2, BCC3, and BCC4) compared to WT skin. (<b>I</b>) The skin tumors bear resemblance to human basal cell carcinoma according to histological analysis, consistent with the activation of the <i>Hedgehog</i> pathway (scale bar, 50 µm).</p>", "links"=>[], "tags"=>["induction", "phenotypes", "cre-activated", "pb"], "article_id"=>391238, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas K. Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026650.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tissue_specific_induction_of_skin_phenotypes_by_Cre_activated_PB_mutagenesis_/391238", "title"=>"Tissue-specific induction of skin phenotypes by Cre-activated PB mutagenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-21 00:20:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/365090", "https://ndownloader.figshare.com/files/365129"], "description"=>"<div><p>Somatic forward genetic screens have the power to interrogate thousands of genes in a single animal. Retroviral and transposon mutagenesis systems in mice have been designed and deployed in somatic tissues for surveying hematopoietic and solid tumor formation. In the context of cancer, the ability to visually mark mutant cells would present tremendous advantages for identifying tumor formation, monitoring tumor growth over time, and tracking tumor infiltrations and metastases into wild-type tissues. Furthermore, locating mutant clones is a prerequisite for screening and analyzing most other somatic phenotypes. For this purpose, we developed a system using the <em>piggyBac</em> (PB) transposon for somatic mutagenesis with an activated reporter and tracker, called PB-SMART. The PB-SMART mouse genetic screening system can simultaneously induce somatic mutations and mark mutated cells using bioluminescence or fluorescence. The marking of mutant cells enable analyses that are not possible with current somatic mutagenesis systems, such as tracking cell proliferation and tumor growth, detecting tumor cell infiltrations, and reporting tissue mutagenesis levels by a simple <em>ex vivo</em> visual readout. We demonstrate that PB-SMART is highly mutagenic, capable of tumor induction with low copy transposons, which facilitates the mapping and identification of causative insertions. We further integrated a conditional transposase with the PB-SMART system, permitting tissue-specific mutagenesis with a single cross to any available Cre line. Targeting the germline, the system could also be used to conduct F1 screens. With these features, PB-SMART provides an integrated platform for individual investigators to harness the power of somatic mutagenesis and phenotypic screens to decipher the genetic basis of mammalian biology and disease.</p> </div>", "links"=>[], "tags"=>["piggybac", "transposon", "somatic", "mutagenesis", "activated", "tracker", "screens", "mice"], "article_id"=>132146, "categories"=>["Biological Sciences", "Cell Biology", "Genetics"], "users"=>["Sean F. Landrette", "Jonathan C. Cornett", "Thomas Ni", "Marcus W. Bosenberg", "Tian Xu"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0026650.s001", "https://dx.doi.org/10.1371/journal.pone.0026650.s002"], "stats"=>{"downloads"=>7, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/piggyBac_Transposon_Somatic_Mutagenesis_with_an_Activated_Reporter_and_Tracker_PB_SMART_for_Genetic_Screens_in_Mice/132146", "title"=>"piggyBac Transposon Somatic Mutagenesis with an Activated Reporter and Tracker (PB-SMART) for Genetic Screens in Mice", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-10-21 00:35:46"}

PMC Usage Stats | Further Information

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Relative Metric

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