BMP Signaling and the Maintenance of Primordial Germ Cell Identity in Drosophila Embryos

The specification of primordial germ cells (PGCs) and subsequent maintenance of germ-line identity in Drosophila embryos has long been thought to occur solely under the control of cell-autonomous factors deposited in the posterior pole plasm during oogenesis. However, here we document a novel role f...

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Vydáno v:	PloS one Ročník 9; číslo 2; s. e88847
Hlavní autoři:	Deshpande, Girish, Willis, Elinor, Chatterjee, Sandip, Fernandez, Robert, Dias, Kristen, Schedl, Paul
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States Public Library of Science 14.02.2014 Public Library of Science (PLoS)
Témata:	Animals Autocrine Communication Biology Bone morphogenetic proteins Bone Morphogenetic Proteins - metabolism Cell division Cell Nucleus - metabolism Cell signaling Coalescence Coalescing Down-Regulation Drosophila Drosophila melanogaster - cytology Drosophila melanogaster - embryology Drosophila Proteins - metabolism Embryo, Nonmammalian - cytology Embryo, Nonmammalian - metabolism Embryonic Development Embryos Gene expression Germ cells Germ Cells - cytology Germ Cells - metabolism Homology Insects Maintenance Molecular biology Oogenesis Phosphorylation Signal Transduction Signaling Stem cells
ISSN:	1932-6203, 1932-6203
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Abstract	The specification of primordial germ cells (PGCs) and subsequent maintenance of germ-line identity in Drosophila embryos has long been thought to occur solely under the control of cell-autonomous factors deposited in the posterior pole plasm during oogenesis. However, here we document a novel role for somatic BMP signaling in the maintenance of PGC fate during the period leading up to embryonic gonad coalescence. We find that PGCs fail to maintain their germline identity when BMP signaling is compromised. They initiate but are unable to properly assemble the germline stem cell-specific organelle, the spectrosome, and they lose expression of the germline-specific gene Vasa. BMP signaling must, however, be finely tuned as there are deleterious consequences to PGCs when the pathway is excessively active. We show that one mechanism used to calibrate the effects of BMP signals is dependent on the Ubc9 homolog Lesswright (Lwr).
AbstractList	The specification of primordial germ cells (PGCs) and subsequent maintenance of germ-line identity in Drosophila embryos has long been thought to occur solely under the control of cell-autonomous factors deposited in the posterior pole plasm during oogenesis. However, here we document a novel role for somatic BMP signaling in the maintenance of PGC fate during the period leading up to embryonic gonad coalescence. We find that PGCs fail to maintain their germline identity when BMP signaling is compromised. They initiate but are unable to properly assemble the germline stem cell-specific organelle, the spectrosome, and they lose expression of the germline-specific gene Vasa. BMP signaling must, however, be finely tuned as there are deleterious consequences to PGCs when the pathway is excessively active. We show that one mechanism used to calibrate the effects of BMP signals is dependent on the Ubc9 homolog Lesswright (Lwr). The specification of primordial germ cells (PGCs) and subsequent maintenance of germ-line identity in Drosophila embryos has long been thought to occur solely under the control of cell-autonomous factors deposited in the posterior pole plasm during oogenesis. However, here we document a novel role for somatic BMP signaling in the maintenance of PGC fate during the period leading up to embryonic gonad coalescence. We find that PGCs fail to maintain their germline identity when BMP signaling is compromised. They initiate but are unable to properly assemble the germline stem cell-specific organelle, the spectrosome, and they lose expression of the germline-specific gene Vasa. BMP signaling must, however, be finely tuned as there are deleterious consequences to PGCs when the pathway is excessively active. We show that one mechanism used to calibrate the effects of BMP signals is dependent on the Ubc9 homolog Lesswright (Lwr).The specification of primordial germ cells (PGCs) and subsequent maintenance of germ-line identity in Drosophila embryos has long been thought to occur solely under the control of cell-autonomous factors deposited in the posterior pole plasm during oogenesis. However, here we document a novel role for somatic BMP signaling in the maintenance of PGC fate during the period leading up to embryonic gonad coalescence. We find that PGCs fail to maintain their germline identity when BMP signaling is compromised. They initiate but are unable to properly assemble the germline stem cell-specific organelle, the spectrosome, and they lose expression of the germline-specific gene Vasa. BMP signaling must, however, be finely tuned as there are deleterious consequences to PGCs when the pathway is excessively active. We show that one mechanism used to calibrate the effects of BMP signals is dependent on the Ubc9 homolog Lesswright (Lwr).
Audience	Academic
Author	Chatterjee, Sandip Dias, Kristen Willis, Elinor Schedl, Paul Fernandez, Robert Deshpande, Girish
AuthorAffiliation	National Cancer Institute, United States of America 2 Institute of Gene Biology RAS, Moscow, Russian Federation 1 Department of Molecular Biology, Princeton University, Princeton, New Jersey, United States of America
AuthorAffiliation_xml	– name: 1 Department of Molecular Biology, Princeton University, Princeton, New Jersey, United States of America – name: 2 Institute of Gene Biology RAS, Moscow, Russian Federation – name: National Cancer Institute, United States of America
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24551179$$D View this record in MEDLINE/PubMed
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Cites_doi	10.1074/jbc.M003949200 10.1242/dev.121.6.1815 10.1111/j.1440-169X.2009.01108.x 10.1242/dev.118.2.401 10.1002/dvg.1020160104 10.1093/genetics/144.4.1673 10.1074/jbc.C300028200 10.1242/dev.02415 10.1242/dev.128.6.965 10.1038/nrm3011 10.1126/science.1208146 10.1016/S0074-7696(01)03007-8 10.1242/dev.120.4.947 10.1093/genetics/155.4.1741 10.1101/gad.494808 10.1016/j.gep.2008.08.001 10.1126/science.290.5490.328 10.1016/j.cell.2008.01.038 10.1038/nrg3294 10.1002/dvdy.20503 10.1016/S0960-9822(98)70091-0 10.1146/annurev.cellbio.21.012704.131525 10.1038/358387a0 10.1016/j.cub.2004.07.018 10.1242/dev.01026 10.1016/S0092-8674(00)81424-5 10.1126/science.1085222 10.1242/dev.022434
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Current address: Department of Chemical Biology, Scripps Research Institute, La Jolla, California, United States of America Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: GD EW PS. Performed the experiments: GD EW SC RF KD. Analyzed the data: GD EW SC RF KD. Wrote the paper: GD EW PS. Current address: Department of Biology, California State University, Northridge, California, United States of America Current address: Molecular Biophysics & Biochemistry BBS Program, New Haven, Connecticut, United States of America Current address: School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America
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SubjectTerms	Animals Autocrine Communication Biology Bone morphogenetic proteins Bone Morphogenetic Proteins - metabolism Cell division Cell Nucleus - metabolism Cell signaling Coalescence Coalescing Down-Regulation Drosophila Drosophila melanogaster - cytology Drosophila melanogaster - embryology Drosophila Proteins - metabolism Embryo, Nonmammalian - cytology Embryo, Nonmammalian - metabolism Embryonic Development Embryos Gene expression Germ cells Germ Cells - cytology Germ Cells - metabolism Homology Insects Maintenance Molecular biology Oogenesis Phosphorylation Signal Transduction Signaling Stem cells
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Title	BMP Signaling and the Maintenance of Primordial Germ Cell Identity in Drosophila Embryos
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