Nucleoporin98-96 Function Is Required for Transit Amplification Divisions in the Germ Line of Drosophila melanogaster
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{"title"=>"Nucleoporin98-96 function is required for transit amplification divisions in the germ line of Drosophila melanogaster", "type"=>"journal", "authors"=>[{"first_name"=>"Benjamin B.", "last_name"=>"Parrott", "scopus_author_id"=>"53364298200"}, {"first_name"=>"Yuting", "last_name"=>"Chiang", "scopus_author_id"=>"53363312000"}, {"first_name"=>"Alicia", "last_name"=>"Hudson", "scopus_author_id"=>"53363802300"}, {"first_name"=>"Angshuman", "last_name"=>"Sarkar", "scopus_author_id"=>"7202675034"}, {"first_name"=>"Antoine", "last_name"=>"Guichet", "scopus_author_id"=>"55990365000"}, {"first_name"=>"Cordula", "last_name"=>"Schulz", "scopus_author_id"=>"7102628737"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"21949861", "sgr"=>"80052828297", "doi"=>"10.1371/journal.pone.0025087", "scopus"=>"2-s2.0-80052828297", "pui"=>"362568135", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "issn"=>"19326203"}, "id"=>"69617887-0ef8-353e-9902-ff332ca16aae", "abstract"=>"Production of specialized cells from precursors depends on a tightly regulated sequence of proliferation and differentiation steps. In the gonad of Drosophila melanogaster, the daughters of germ line stem cells (GSC) go through precisely four rounds of transit amplification divisions to produce clusters of 16 interconnected germ line cells before entering a stereotypic differentiation cascade. Here we show that animals harbouring a transposon insertion in the center of the complex nucleoporin98-96 (nup98-96) locus had severe defects in the early steps of this developmental program, ultimately leading to germ cell loss and sterility. A phenotypic analysis indicated that flies carrying the transposon insertion, designated nup98-96(2288), had dramatically reduced numbers of germ line cells. In contrast to controls, mutant testes contained many solitary germ line cells that had committed to differentiation as well as abnormally small clusters of two, four or eight differentiating germ line cells. This indicates that mutant GSCs rather differentiated than self-renewed, and that these GSCs and their daughters initiated the differentiation cascade after zero, or less than four rounds of amplification divisions. This phenotype remained unaffected by hyper-activation of signalling pathways that normally result in excessive proliferation of GSCs and their daughters. Expression of wildtype nup98-96 specifically in the germ line cells of mutant animals fully restored development of the GSC lineage, demonstrating that the effect of the mutation is cell-autonomous. Nucleoporins are the structural components of the nucleopore and have also been implicated in transcriptional regulation of specific target genes. The nuclear envelopes of germ cells and general nucleocytoplasmic transport in nup98-96 mutant animals appeared normal, leading us to propose that Drosophila nup98-96 mediates the transport or transcription of targets required for the developmental timing between amplification and differentiation.", "link"=>"http://www.mendeley.com/research/nucleoporin9896-function-required-transit-amplification-divisions-germ-line-drosophila-melanogaster", "reader_count"=>18, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>1, "Professor"=>2, "Unspecified"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>1, "Professor"=>2, "Unspecified"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>10, "Chemistry"=>1, "Unspecified"=>2}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>2, "Spain"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/735067"], "description"=>"<p>(A–E) Images showing nuclear localization around nuclei of early stage germ line cells (see insets) and nurse cells. Small arrows in insets point to early stage germ cell nuclei in the germaria and large arrows in images point to nurse cell nuclei in egg chambers. Immunofluorescence-labelling as indicated. (A, B) Apical region of (A) a wildtype and (B) a <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> ovariole. (C) The apical region of a wildtype ovariole. (D) The germarium and (E) an egg chamber of a <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> ovariole. (F–I) Immuno-labelling of single nurse cell nuclei, antibodies and genotypes as indicated. Asterisks: apical tips of germaria, scale bars: 20 µm.</p>", "links"=>[], "tags"=>["cells", "animals"], "article_id"=>405421, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Benjamin B. Parrott", "Yuting Chiang", "Alicia Hudson", "Angshuman Sarkar", "Antoine Guichet", "Cordula Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025087.g004", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Germ_cells_from_nup98_96_2288_Df_3R_mbc_R1_animals_have_normal_nuclear_envelopes_/405421", "title"=>"Germ cells from <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> animals have normal nuclear envelopes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:43:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/734938"], "description"=>"<p>(A) Top: Intron-exon structure of the <i>nup98-96</i> locus. Coding region in dark grey. Gene products as indicated. Bottom: Rescue constructs containing the whole transcription unit for <i>nup98-96</i> or <i>nup98</i> only. Arrowhead: Pogo-insertion in <i>nup98-96<sup>2288</sup></i>, arrow: RNAi-sequences. (B-E) Bright field images of whole testes. Genotypes as indicated. Arrows point to sperm. Asterisks mark the apical tips. Scale bars: 100 µm. (F) Western blot analysis. Genotypes and antibodies as indicated. The Nup96 antibody does not detect a 95 kd protein in extracts from mutant animals. Instead, the Nup96 antibody detects a high molecular weight bands that may be abnormal Nup96 protein or Nup98-Nup96 polyprotein. The Nup98 antibody detects extremely low levels a 95 kd protein in the mutant compared to the control. (G, H) Apical tips of adult testes with germ line expression of (G) UAST-<i>nup98-96</i>-RNAi (arrow points to a single spermatocyte), and (H) UAST-<i>nup98-96</i>. Asterisks mark the apical tips. Scale bars: 30 µm.</p>", "links"=>[], "tags"=>["disrupt"], "article_id"=>405292, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Benjamin B. Parrott", "Yuting Chiang", "Alicia Hudson", "Angshuman Sarkar", "Antoine Guichet", "Cordula Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025087.g003", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutations_in_nup98_96_disrupt_gametogenesis_/405292", "title"=>"Mutations in <i>nup98-96</i> disrupt gametogenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:43:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/734702"], "description"=>"<p>(A) Drawing showing the stages of germ line cell differentiation in testes. GSC: germ line stem cell, GB: gonialblast, SG: spermatogonia, SC: spermatocytes. Black circles: somatic support cells enclosing the germ line cells. (B, C) <i>In situ</i> hybridization with a <i>piwi</i>-RNA-probe to (B) <i>w<sup>1118</sup></i> and (C) <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> mutant embryos. Anterior to the left. (D–J) 3<sup>rd</sup> instar larval testes. (D, E) DNA in D) the apical region of a wildtype (wt), and (E) a whole <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> testis. Arrows point to early stage germ line cell nuclei, arrowheads point to spermatocyte nuclei that are in addition outlined by grey dotted circles. The small, strong DAPI-positive signals at the posterior (right) end of the testes correspond to the nuclei of somatic precursor cells that will develop into the most basal somatic structures of the testes during pupal stage. (F–L) FasIII and asterisks label the hub. Arrowheads point to spectrosomes, small arrow points to the small, branched fusomes as normally seen in the spermatogonia, large arrows point to the wide, long, branched fusomes as normally seen in the spermatocytes. (F) Apical region of a wildtype testis. (G, H) High magnification of apical tips of testes from (G) wildtype and (H) <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1.</i> (I, J) Whole <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> testes. Note the inset in (I) showing the spectrosome (green) and DNA (red) in a single, large germ line cell. (K, L) Apical regions of adult testes from (K) wildtype and (L) <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1.</i> Scale bars: 30 µm.</p>", "links"=>[], "tags"=>["cells", "maintained", "stages", "differentiate", "mutant"], "article_id"=>405050, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Benjamin B. Parrott", "Yuting Chiang", "Alicia Hudson", "Angshuman Sarkar", "Antoine Guichet", "Cordula Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025087.g001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Germ_line_cells_are_not_maintained_at_early_stages_and_differentiate_in_nup98_96_2288_Df_3R_mbc_R1_mutant_testes_/405050", "title"=>"Germ line cells are not maintained at early stages and differentiate in <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> mutant testes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:41:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/735222"], "description"=>"<p>Immuno-labelling of germaria, antibodies and genotypes as indicated. (A, B) nuclear Groucho (red) and cytoplasmic Vasa (green); (C, D) nuclear phosphorylated Jun-Kinase (red) and cytoplasmic Vasa (green); note that some germaria (arrowheads) are empty in the <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> mutant ovaries; (E, F) cytoplasmic Sex-lethal in GSCs and gonialblasts; (G, H) nuclear phosphorylated Histone-H3 (red) and cytoplasmic Vasa (green); (I, J) Anti-BRDU (green) and DAPI (red). Asterisks: apical tips, arrows point to intra-cellular protein localizations, scale bars: 50 µm.</p>", "links"=>[], "tags"=>["cells", "mutant", "animals", "localization"], "article_id"=>405574, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Benjamin B. Parrott", "Yuting Chiang", "Alicia Hudson", "Angshuman Sarkar", "Antoine Guichet", "Cordula Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025087.g005", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Germ_line_cells_from_nup98_96_2288_Df_3R_mbc_R1_mutant_animals_have_normal_protein_localization_patterns_/405574", "title"=>"Germ line cells from <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> mutant animals have normal protein localization patterns.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:44:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/735365"], "description"=>"<p>(A, B) Immuno-labelling of germaria from (A) wildtype and (B) <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> mutant females. Arrowheads point to Bam-negative GSCs (circled in grey), arrows point to Bam-positive cells, scale bars: 50 µm. (C-J) Adult testes, genotypes as indicated. (C–F) DNA-labelling (DAPI), arrows point to early stage germ line cells. (G) Whole <i>stet<sup>1</sup>; nup98-96<sup>2288</sup></i> testis showing a single spermatocyte (arrowhead) with a spectrosome (arrow). (H, I) Hyper-activation of signalling pathways results in accumulation of early stage germ line cells. (H) Apical region of a testis with germ line expression of <i>dpp</i>, and (I) whole testis with germ line expression of <i>upd</i>. (J) Whole <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> testis with germ line expression of <i>upd</i>. Arrow points to single spermatocyte. Asterisks mark the testes tips, scale bars: 30 µm.</p>", "links"=>[], "tags"=>["acts", "upstream", "signalling", "pathways", "regulating", "germ"], "article_id"=>405712, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Benjamin B. Parrott", "Yuting Chiang", "Alicia Hudson", "Angshuman Sarkar", "Antoine Guichet", "Cordula Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025087.g006", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nup98_96_acts_upstream_of_signalling_pathways_regulating_early_stage_germ_line_cells_/405712", "title"=>"Nup98-96 acts upstream of signalling pathways regulating early stage germ line cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:45:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/734838"], "description"=>"<p>(A) Drawing showing the organization of GSCs and their daughters in a wildtype germarium. GSC: germ line stem cell, CB: cystoblast, CC: cystocytes, EC: egg chamber, FC: follicle cells, black marking in germ line cells: spectrosomes and branched fusomes. (B, C) Germaria. Asterisks mark the apical tips, arrowheads point to spectrosomes in the GSCs (grey dotted circles), arrows point to branched fusomes. Note that only a section of the fusomes is in focal plane. Scale bars: 50 µm. (D) Histogram depicting the number of Vasa-positive germ line cells in the germaria at different time points post-eclosion. Genotypes are as indicated.</p>", "links"=>[], "tags"=>["mutant"], "article_id"=>405194, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Benjamin B. Parrott", "Yuting Chiang", "Alicia Hudson", "Angshuman Sarkar", "Antoine Guichet", "Cordula Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025087.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Germ_line_cell_loss_in_nup98_96_2288_Df_3R_mbc_R1_mutant_germaria_/405194", "title"=>"Germ line cell loss in <i>nup98-96<sup>2288</sup>/Df(3R)mbc-R1</i> mutant germaria.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:42:42"}

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