E-Cadherin Is Required for Centrosome and Spindle Orientation in Drosophila Male Germline Stem Cells
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{"title"=>"E-Cadherin is required for centrosome and spindle orientation in Drosophila male germline stem cells", "type"=>"journal", "authors"=>[{"first_name"=>"Mayu", "last_name"=>"Inaba", "scopus_author_id"=>"36554133200"}, {"first_name"=>"Hebao", "last_name"=>"Yuan", "scopus_author_id"=>"34973543300"}, {"first_name"=>"Viktoria", "last_name"=>"Salzmann", "scopus_author_id"=>"36554625000"}, {"first_name"=>"Margaret T.", "last_name"=>"Fuller", "scopus_author_id"=>"7202312374"}, {"first_name"=>"Yukiko M.", "last_name"=>"Yamashita", "scopus_author_id"=>"7402954283"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-77957935563", "doi"=>"10.1371/journal.pone.0012473", "sgr"=>"77957935563", "isbn"=>"1932-6203", "pmid"=>"20824213", "issn"=>"19326203", "pui"=>"359771478"}, "id"=>"f29fa9e0-5cc9-3f1d-bff6-42a80269f175", "abstract"=>"Many adult stem cells reside in a special microenvironment known as the niche, where they receive essential signals that specify stem cell identity. Cell-cell adhesion mediated by cadherin and integrin plays a crucial role in maintaining stem cells within the niche. In Drosophila melanogaster, male germline stem cells (GSCs) are attached to niche component cells (i.e., the hub) via adherens junctions. The GSC centrosomes and spindle are oriented toward the hub-GSC junction, where E-cadherin-based adherens junctions are highly concentrated. For this reason, adherens junctions are thought to provide a polarity cue for GSCs to enable proper orientation of centrosomes and spindles, a critical step toward asymmetric stem cell division. However, understanding the role of E-cadherin in GSC polarity has been challenging, since GSCs carrying E-cadherin mutations are not maintained in the niche. Here, we tested whether E-cadherin is required for GSC polarity by expressing a dominant-negative form of E-cadherin. We found that E-cadherin is indeed required for polarizing GSCs toward the hub cells, an effect that may be mediated by Apc2. We also demonstrated that E-cadherin is required for the GSC centrosome orientation checkpoint, which prevents mitosis when centrosomes are not correctly oriented. We propose that E-cadherin orchestrates multiple aspects of stem cell behavior, including polarization of stem cells toward the stem cell-niche interface and adhesion of stem cells to the niche supporting cells.", "link"=>"http://www.mendeley.com/research/ecadherin-required-centrosome-spindle-orientation-drosophila-male-germline-stem-cells", "reader_count"=>81, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>6, "Researcher"=>24, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>4, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>9}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>6, "Researcher"=>24, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>4, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>9}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>17, "Agricultural and Biological Sciences"=>53, "Medicine and Dentistry"=>4, "Veterinary Science and Veterinary Medicine"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>53}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>17}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>2, "Japan"=>1, "France"=>3, "Germany"=>2}, "group_count"=>6}

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  • {"files"=>["https://ndownloader.figshare.com/files/832598"], "description"=>"<p>(A) Model of Apc2 linking the adherens junction and the centrosome. Orange; cadherin. Green; microtubule. (B, C) GFP-Apc2 expressed by nos-gal4 at 18°C preferentially localized to the hub-GSC cortex junction (B), while it was evenly distributed throughout the GSC cortex when expressed at 25°C (C). Oriented centrosomes (at 18°C) and misoriented centrosomes (at 25°C) are indicated with arrowheads. GSCs in the right focal plane to judge its cortical localization are marked by dotted lines (4 GSCs in panel B, 3 GSCs in panel C). The hub is stained with Fas III. (D) Quantification of centrosome misorientation upon expression of GFP-Apc2 at 18°C or 25°C. Essentially the same results were obtained in more than three repeated experiments. (E) Apc2 localizes to the hub-GSC junction in testes expressing E-cad<sup>DEFL</sup>. (F) Apc2 is evenly distributed throughout the GSC cortex in testes expressing E-cad<sup>dCR4h</sup>. Cortical sites with prominent Apc2 localization are indicated with yellow lines.</p>", "links"=>[], "tags"=>["cortical", "apc2"], "article_id"=>502965, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Mayu Inaba", "Hebao Yuan", "Viktoria Salzmann", "Margaret T. Fuller", "Yukiko M. Yamashita"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012473.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_E_cad_dCR4h_results_in_even_cortical_distribution_of_the_Apc2_protein_/502965", "title"=>"Expression of E-cad<sup>dCR4h</sup> results in even cortical distribution of the Apc2 protein.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:49:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/832476"], "description"=>"<p>(A) Definition of GSC centrosome orientation. GSCs were scored as misoriented when neither of the two centrosomes was juxtaposed to the hub-GSC interface. (B) Examples of GSCs with misoriented centrosomes (arrowheads) upon expression of E-cad<sup>dCR4h</sup>. γ-tubulin (centrosomes). (C) Examples of GSCs with oriented centrosomes (arrows) upon expression of E-cad<sup>DEFL</sup> (D) Quantification of GSC centrosome misorientation upon expression of E-cad<sup>dCR4h</sup> or E-cad<sup>DEFL</sup>. Siblings without the nos-gal4 driver from the same cross served as controls. n>300 GSCs per data point. (E) An example of a dedifferentiating spermatogonium observed in testis expressing E-cad<sup>dCR4h</sup>. Multiple germs cells (including one attached to the hub) is connected by disintegrating ring canals and fusomes (arrowheads). Pavarotti-GFP marks ring canals, and Adducin-like marks fusome. (F) Quantification of dedifferentiation upon expression of E-cad<sup>dCR4h</sup> or E-cad<sup>DEFL</sup>. Siblings without the nos-gal4 driver from the same cross served as controls. n>700 GSCs per data point.</p>", "links"=>[], "tags"=>["gsc", "centrosome"], "article_id"=>502846, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Mayu Inaba", "Hebao Yuan", "Viktoria Salzmann", "Margaret T. Fuller", "Yukiko M. Yamashita"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012473.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_E_cad_dCR4h_results_in_GSC_centrosome_misorientation_/502846", "title"=>"Expression of E-cad<sup>dCR4h</sup> results in GSC centrosome misorientation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:47:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/832759"], "description"=>"<p>(A) Examples of GSCs with misoriented spindles upon expression of E-cad<sup>dCR4h</sup>. Phospho-histone H3 (mitotic chromosomes). (B) An example of a GSC with an oriented spindle in an E-cad<sup>DEFL</sup>-expressing testis. (C) Quantification of GSC centrosome orientation (% misoriented centrosomes/total interphase GSCs) and spindle misorientation (% misoriented spindles/total mitotic GSCs). The fold difference (centrosome misorientation frequency/spindle misorientation frequency) is shown at the top of graph. n>250 GSCs per data point for centrosome orientation. n>30 mitotic GSCs per data point for spindle orientation. For <i>apc2</i> and <i>cnn</i> mutants, heterozygous siblings from the same cross served as controls. (D) Model for E-cadherin function in multiple stem cell behaviors. The E-cadherin-based adherens junction serves as a polarity cue for stem cell orientation and also maintains stem cells in the niche. The intracellular domain of E-cadherin recruits Apc2 (directly or indirectly) and factor(s) that participate in the centrosome orientation checkpoint.</p>", "links"=>[], "tags"=>["misoriented", "spindle", "mitotic"], "article_id"=>503127, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Mayu Inaba", "Hebao Yuan", "Viktoria Salzmann", "Margaret T. Fuller", "Yukiko M. Yamashita"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012473.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_E_cad_dCR4h_results_in_misoriented_spindle_in_mitotic_GSCs_/503127", "title"=>"Expression of E-cad<sup>dCR4h</sup> results in misoriented spindle in mitotic GSCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:52:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/414734", "https://ndownloader.figshare.com/files/414769"], "description"=>"<div><p>Many adult stem cells reside in a special microenvironment known as the niche, where they receive essential signals that specify stem cell identity. Cell-cell adhesion mediated by cadherin and integrin plays a crucial role in maintaining stem cells within the niche. In <em>Drosophila melanogaster</em>, male germline stem cells (GSCs) are attached to niche component cells (<em>i.e.</em>, the hub) via adherens junctions. The GSC centrosomes and spindle are oriented toward the hub-GSC junction, where E-cadherin-based adherens junctions are highly concentrated. For this reason, adherens junctions are thought to provide a polarity cue for GSCs to enable proper orientation of centrosomes and spindles, a critical step toward asymmetric stem cell division. However, understanding the role of E-cadherin in GSC polarity has been challenging, since GSCs carrying E-cadherin mutations are not maintained in the niche. Here, we tested whether E-cadherin is required for GSC polarity by expressing a dominant-negative form of E-cadherin. We found that E-cadherin is indeed required for polarizing GSCs toward the hub cells, an effect that may be mediated by Apc2. We also demonstrated that E-cadherin is required for the GSC centrosome orientation checkpoint, which prevents mitosis when centrosomes are not correctly oriented. We propose that E-cadherin orchestrates multiple aspects of stem cell behavior, including polarization of stem cells toward the stem cell-niche interface and adhesion of stem cells to the niche supporting cells.</p></div>", "links"=>[], "tags"=>["E-cadherin", "centrosome", "spindle", "germline", "cells"], "article_id"=>141889, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Mayu Inaba", "Hebao Yuan", "Viktoria Salzmann", "Margaret T. Fuller", "Yukiko M. Yamashita"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0012473.s001", "https://dx.doi.org/10.1371/journal.pone.0012473.s002"], "stats"=>{"downloads"=>10, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/E_Cadherin_Is_Required_for_Centrosome_and_Spindle_Orientation_in_Drosophila_Male_Germline_Stem_Cells/141889", "title"=>"E-Cadherin Is Required for Centrosome and Spindle Orientation in <em>Drosophila</em> Male Germline Stem Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-08-31 00:31:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/832343"], "description"=>"<p>(A) Experimental scheme. Wild type E-cad<sup>DEFL</sup> or dominant-negative E-cad<sup>dCR4h</sup> was expressed in GSCs using the germline-specific driver, nos-gal4. (B) E-cad<sup>dCR4h</sup> was distributed throughout the entire GSC cortex, with a preference for the hub-GSC interface. The color of the text corresponds to the pseudocolored antibody staining or GFP signal in this and subsequent figures. GFP is shown in a separate panel (B') in gray scale. Vasa (germ cells). Asterisk (Hub). The scale bar represents 10 µm in this and subsequent figures. (C) E-cad<sup>DEFL</sup> localizes to the hub-GSC interface. Arrow indicates GSCs with a higher expression level of E-cad<sup>DEFL</sup>. The localization of E-cad<sup>dCR4h</sup> and E-cad<sup>DEFL</sup> was monitored by GFP, since both E-cad<sup>dCR4h</sup> and E-cad<sup>DEFL</sup> contain GFP-tag at their C-termini. (D) GSC number was not affected by expression of E-cad<sup>dCR4h</sup> or E-cad<sup>DEFL</sup>. Data are reported as mean ± S.D. in this and in subsequent graphs. n>45 testes per data point. (E) Percent of testes containing at least one GFP-positive clone at 2, 8, and 16 days after heatshock. n>60 testes per data point.</p>", "links"=>[], "tags"=>["localize", "hub-gsc"], "article_id"=>502713, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Mayu Inaba", "Hebao Yuan", "Viktoria Salzmann", "Margaret T. Fuller", "Yukiko M. Yamashita"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012473.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_E_cad_dCR4h_does_not_properly_localize_to_the_hub_GSC_interface_/502713", "title"=>"E-cad<sup>dCR4h</sup> does not properly localize to the hub-GSC interface.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:45:13"}

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