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      Snoo and Dpp Act as Spatial and Temporal Regulators Respectively of Adult Progenitor Cells in the Drosophila Trachea

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      PLoS Genetics
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          Abstract

          Clusters of differentiated cells contributing to organ structures retain the potential to re-enter the cell cycle and replace cells lost during development or upon damage. To do so, they must be designated spatially and respond to proper activation cues. Here we show that in the case of Drosophila differentiated larval tracheal cells, progenitor potential is conferred by the spatially restricted activity of the Snoo transcription cofactor. Furthermore, Dpp signalling regulated by endocrine hormonal cues provides the temporal trigger for their activation. Finally, we elucidate the genetic network elicited by Snoo and Dpp activity. These results illustrate a regulatory mechanism that translates intrinsic potential and extrinsic cues into the facultative stem cell features of differentiated progenitors.

          Author Summary

          An important feature of organs is their ability to maintain their structure and function in spite of natural or accidental cell loss. This capacity is often sustained by so-called stem cells, which are able to provide new cells of the different types in the organ. In addition, some specialized cells, known as facultative stem cells, also retain the ability to re-enter the cell cycle and replace lost tissue. This process has to be very precisely regulated to provide for the maintenance of the tissues and organs while preventing uncontrolled cellular growth. We have analysed this mechanism in the Drosophila trachea; there, a group of Differentiated Adult Progenitor cells (or DAP cells) share the features of facultative stem cells as they remain quiescent during larval growth, reactivate their proliferation at the last larval stage and give rise to the different cell types of the adult tracheal network during metamorphosis. The DAP cells, conversely to the majority of the larval cells, do not enter endocycle and by doing so they acquire the features of adult progenitor cells. In this paper we identify the regulatory mechanism that integrates spatial and temporal cues to precisely activate the tracheal adult progenitor program.

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          Most cited references29

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          The UCSC Genome Browser database: update 2011

          The University of California, Santa Cruz Genome Browser (http://genome.ucsc.edu) offers online access to a database of genomic sequence and annotation data for a wide variety of organisms. The Browser also has many tools for visualizing, comparing and analyzing both publicly available and user-generated genomic data sets, aligning sequences and uploading user data. Among the features released this year are a gene search tool and annotation track drag-reorder functionality as well as support for BAM and BigWig/BigBed file formats. New display enhancements include overlay of multiple wiggle tracks through use of transparent coloring, options for displaying transformed wiggle data, a ‘mean+whiskers’ windowing function for display of wiggle data at high zoom levels, and more color schemes for microarray data. New data highlights include seven new genome assemblies, a Neandertal genome data portal, phenotype and disease association data, a human RNA editing track, and a zebrafish Conservation track. We also describe updates to existing tracks.
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            Direct and long-range action of a DPP morphogen gradient.

            During development of the Drosophila wing, the decapentaplegic (dpp) gene is expressed in a stripe of cells along the anteroposterior compartment boundary and gives rise to a secreted protein that exerts a long-range organizing influence on both compartments. Using clones of cells that express DPP, or in which DPP receptor activity has been constitutively activated or abolished, we show that DPP acts directly and at long range on responding cells, rather than by proxy through the short-range induction of other signaling molecules. Further, we show that two genes, optomotor-blind and spalt are transcriptionally activated at different distances from DPP-secreting cells and provide evidence that these genes respond to different threshold concentrations of DPP protein. We propose that DPP acts as a gradient morphogen during wing development.
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              Ski and SnoN, potent negative regulators of TGF-beta signaling.

              Ski and the closely related SnoN were discovered as oncogenes by their ability to transform chicken embryo fibroblasts upon overexpression. While elevated expressions of Ski and SnoN have also been reported in many human cancer cells and tissues, consistent with their pro-oncogenic activity, emerging evidence also suggests a potential anti-oncogenic activity for both. In addition, Ski and SnoN have been implicated in regulation of cell differentiation, especially in the muscle and neuronal lineages. Multiple cellular partners of Ski and SnoN have been identified in an effort to understand the molecular mechanisms underlying the complex roles of Ski and SnoN. In this review, we summarize recent findings on the biological functions of Ski and SnoN, their mechanisms of action and how their levels of expression are regulated.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                4 March 2016
                March 2016
                : 12
                : 3
                : e1005909
                Affiliations
                [1 ]Institut de Biologia Molecular de Barcelona (CSIC), Barcelona, Catalonia, Spain
                [2 ]Institute for Research in Biomedicine (IRB Barcelona), Barcelona, Catalonia, Spain
                Harvard Medical School, Howard Hughes Medical Institute, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NJVD JC. Performed the experiments: NJVD. Analyzed the data: NJVD JC. Contributed reagents/materials/analysis tools: NJVD JC. Wrote the paper: NJVD JC.

                Article
                PGENETICS-D-15-02472
                10.1371/journal.pgen.1005909
                4778947
                26942411
                9a1b7088-5737-45c8-bd5a-e2726e352580
                © 2016 Djabrayan, Casanova

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 October 2015
                : 10 February 2016
                Page count
                Figures: 4, Tables: 0, Pages: 15
                Funding
                NJVD was supported by NSF PRFB DBI-1308908. This work has been supported by the Generalitat de Catalunya and the Spanish Ministerio de Ciencia e Innovacion. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Respiratory System
                Trachea
                Medicine and Health Sciences
                Anatomy
                Respiratory System
                Trachea
                Biology and life sciences
                Cell biology
                Signal transduction
                Cell signaling
                Signaling cascades
                DPP signaling cascade
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cell Cycle and Cell Division
                Biology and life sciences
                Genetics
                Epigenetics
                RNA interference
                Biology and life sciences
                Genetics
                Gene expression
                RNA interference
                Biology and life sciences
                Genetics
                Genetic interference
                RNA interference
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                RNA interference
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Stem Cells
                Research and Analysis Methods
                Model Organisms
                Animal Models
                Drosophila Melanogaster
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Drosophila
                Drosophila Melanogaster
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Larvae
                Biology and Life Sciences
                Cell Biology
                Signal Transduction
                Cell Signaling
                Membrane Receptor Signaling
                Hormone Receptor Signaling
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Genetics
                Genetics

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