The Molecular Chaperone Hsp90α Is Required for Meiotic Progression of Spermatocytes beyond Pachytene in the Mouse
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{"title"=>"The molecular chaperone hsp90a is required for meiotic progression of spermatocytes beyond pachytene in the mouse", "type"=>"journal", "authors"=>[{"first_name"=>"Iwona", "last_name"=>"Grad", "scopus_author_id"=>"6602549158"}, {"first_name"=>"Christopher R.", "last_name"=>"Cederroth", "scopus_author_id"=>"9242388300"}, {"first_name"=>"Joël", "last_name"=>"Walicki", "scopus_author_id"=>"6602347863"}, {"first_name"=>"Corinne", "last_name"=>"Grey", "scopus_author_id"=>"8969890500"}, {"first_name"=>"Sofia", "last_name"=>"Barluenga", "scopus_author_id"=>"6603552770"}, {"first_name"=>"Nicolas", "last_name"=>"Winssinger", "scopus_author_id"=>"6603677031"}, {"first_name"=>"Bernard", "last_name"=>"de Massy", "scopus_author_id"=>"6701725512"}, {"first_name"=>"Serge", "last_name"=>"Nef", "scopus_author_id"=>"6603613020"}, {"first_name"=>"Didier", "last_name"=>"Picard", "scopus_author_id"=>"7101818870"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"79251495443", "doi"=>"10.1371/journal.pone.0015770", "pui"=>"361173974", "pmid"=>"21209834", "scopus"=>"2-s2.0-79251495443", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"98af5e88-a33c-3d67-bbcf-832ec61d2b58", "abstract"=>"<p>The molecular chaperone Hsp90 has been found to be essential for viability in all tested eukaryotes, from the budding yeast to Drosophila. In mammals, two genes encode the two highly similar and functionally largely redundant isoforms Hsp90α and Hsp90β. Although they are co-expressed in most if not all cells, their relative levels vary between tissues and during development. Since mouse embryos lacking Hsp90β die at implantation, and despite the fact that Hsp90 inhibitors being tested as anti-cancer agents are relatively well tolerated, the organismic functions of Hsp90 in mammals remain largely unknown. We have generated mouse lines carrying gene trap insertions in the <italic>Hsp90α</italic> gene to investigate the global functions of this isoform. Surprisingly, mice without Hsp90α are apparently normal, with one major exception. Mutant male mice, whose Hsp90β levels are unchanged, are sterile because of a complete failure to produce sperm. While the development of the male reproductive system appears to be normal, spermatogenesis arrests specifically at the pachytene stage of meiosis I. Over time, the number of spermatocytes and the levels of the meiotic regulators and Hsp90 interactors Hsp70-2, NASP and Cdc2 are reduced. We speculate that Hsp90α may be required to maintain and to activate these regulators and/or to disassemble the synaptonemal complex that holds homologous chromosomes together. The link between fertility and Hsp90 is further supported by our finding that an Hsp90 inhibitor that can cross the blood-testis barrier can partially phenocopy the genetic defects.</p>", "link"=>"http://www.mendeley.com/research/molecular-chaperone-hsp90a-required-meiotic-progression-spermatocytes-beyond-pachytene-mouse", "reader_count"=>58, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>12, "Student > Doctoral Student"=>6, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>2, "Student > Master"=>7, "Student > Bachelor"=>3, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>12, "Student > Doctoral Student"=>6, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>2, "Student > Master"=>7, "Student > Bachelor"=>3, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>15, "Agricultural and Biological Sciences"=>37, "Medicine and Dentistry"=>2, "Chemistry"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>37}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>15}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>1, "Spain"=>1}, "group_count"=>0}

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  • {"files"=>["https://ndownloader.figshare.com/files/808614"], "description"=>"<p>(A) Schematic representation of the disruption of the mouse <i>Hsp90aa1</i> gene by insertion of a gene trap (GT) in intron 10 (in mutant mouse line 1). Open and black boxes indicate non-coding and coding exons, respectively. The gene trap consists of a splice acceptor (SA), a β-galactosidase-neomycin resistance fusion (βGeo) and an SV40 polyadenylation site. (B) Immunoblots showing the expression of Hsp90α and Hsp90β in a panel of tissues in wild-type (WT) and mutant (gt/gt) mice (of 136 days postnatal). The Ponceau S staining of the immunoblot filter gives an indication of protein loading.</p>", "links"=>[], "tags"=>["disruption"], "article_id"=>478979, "categories"=>["Biochemistry", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Iwona Grad", "Christopher R. Cederroth", "Joël Walicki", "Corinne Grey", "Sofia Barluenga", "Nicolas Winssinger", "Bernard de Massy", "Serge Nef", "Didier Picard"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015770.g001", "stats"=>{"downloads"=>9, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_disruption_of_the_Hsp90_945_gene_in_the_mouse_/478979", "title"=>"Functional disruption of the Hsp90α gene in the mouse.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-31 02:29:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/809190"], "description"=>"<p>(A) Reduction of testis weight upon intraperitoneal administration of pochoxime A or vehicle. n = 6 for treated, n = 5 for control animals; p = 0.01. (B) Exterior morphology of mouse testes at P25 after administration of pochoxime A or vehicle. Testis size is reduced, in some cases atrophic (asterix). C, vehicle; P, pochoxime A.</p>", "links"=>[], "tags"=>["hsp90", "inhibitor", "pochoxime", "affects", "testis"], "article_id"=>479546, "categories"=>["Biochemistry", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Iwona Grad", "Christopher R. Cederroth", "Joël Walicki", "Corinne Grey", "Sofia Barluenga", "Nicolas Winssinger", "Bernard de Massy", "Serge Nef", "Didier Picard"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015770.g007", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Hsp90_inhibitor_pochoxime_affects_testis_growth_/479546", "title"=>"The Hsp90 inhibitor pochoxime affects testis growth.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-31 02:39:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/403639", "https://ndownloader.figshare.com/files/403650", "https://ndownloader.figshare.com/files/403666", "https://ndownloader.figshare.com/files/403684"], "description"=>"<div><p>The molecular chaperone Hsp90 has been found to be essential for viability in all tested eukaryotes, from the budding yeast to Drosophila. In mammals, two genes encode the two highly similar and functionally largely redundant isoforms Hsp90α and Hsp90β. Although they are co-expressed in most if not all cells, their relative levels vary between tissues and during development. Since mouse embryos lacking Hsp90β die at implantation, and despite the fact that Hsp90 inhibitors being tested as anti-cancer agents are relatively well tolerated, the organismic functions of Hsp90 in mammals remain largely unknown. We have generated mouse lines carrying gene trap insertions in the <em>Hsp90α</em> gene to investigate the global functions of this isoform. Surprisingly, mice without Hsp90α are apparently normal, with one major exception. Mutant male mice, whose Hsp90β levels are unchanged, are sterile because of a complete failure to produce sperm. While the development of the male reproductive system appears to be normal, spermatogenesis arrests specifically at the pachytene stage of meiosis I. Over time, the number of spermatocytes and the levels of the meiotic regulators and Hsp90 interactors Hsp70-2, NASP and Cdc2 are reduced. We speculate that Hsp90α may be required to maintain and to activate these regulators and/or to disassemble the synaptonemal complex that holds homologous chromosomes together. The link between fertility and Hsp90 is further supported by our finding that an Hsp90 inhibitor that can cross the blood-testis barrier can partially phenocopy the genetic defects.</p> </div>", "links"=>[], "tags"=>["molecular", "chaperone", "meiotic", "progression", "spermatocytes", "pachytene"], "article_id"=>139750, "categories"=>["Biochemistry", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Iwona Grad", "Christopher R. Cederroth", "Joël Walicki", "Corinne Grey", "Sofia Barluenga", "Nicolas Winssinger", "Bernard de Massy", "Serge Nef", "Didier Picard"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0015770.s001", "https://dx.doi.org/10.1371/journal.pone.0015770.s002", "https://dx.doi.org/10.1371/journal.pone.0015770.s003", "https://dx.doi.org/10.1371/journal.pone.0015770.s004"], "stats"=>{"downloads"=>3, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Molecular_Chaperone_Hsp90_Is_Required_for_Meiotic_Progression_of_Spermatocytes_beyond_Pachytene_in_the_Mouse/139750", "title"=>"The Molecular Chaperone Hsp90α Is Required for Meiotic Progression of Spermatocytes beyond Pachytene in the Mouse", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-12-31 02:42:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/809003"], "description"=>"<p>Absence of the diplotene stage in <i>hsp90α<sup>gt/gt</sup></i> mutant germ cells of animals at P28. Staining of Sycp1 (in green) and Sycp3 (in red) reveals normal chromosome synapsis in <i>hsp90α<sup>gt/g</sup></i><sup>t</sup> (gt/gt) mutant germ cells until pachytene. There is a complete absence of diplotene spreads in <i>hsp90α<sup>gt/gt</sup></i> mutants. Blue, DAPI staining of DNA.</p>", "links"=>[], "tags"=>["spreads", "meiotic"], "article_id"=>479363, "categories"=>["Biochemistry", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Iwona Grad", "Christopher R. Cederroth", "Joël Walicki", "Corinne Grey", "Sofia Barluenga", "Nicolas Winssinger", "Bernard de Massy", "Serge Nef", "Didier Picard"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015770.g005", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chromosome_spreads_of_meiotic_cells_/479363", "title"=>"Chromosome spreads of meiotic cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-31 02:36:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/808927"], "description"=>"<p>RNA samples are from P44 mice. (A) Markers of testis compartments. Insl3 and Star, Amh, and Pou5f1 are for Leydig, Sertoli, and germ cells, respectively. (B) Complete absence of post-meiotic markers. (C) Markers of advanced stages of meiosis.</p>", "links"=>[], "tags"=>["rt-pcr", "markers", "indicates", "pachytene", "germ", "cells", "mutant"], "article_id"=>479281, "categories"=>["Biochemistry", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Iwona Grad", "Christopher R. Cederroth", "Joël Walicki", "Corinne Grey", "Sofia Barluenga", "Nicolas Winssinger", "Bernard de Massy", "Serge Nef", "Didier Picard"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015770.g004", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantitative_RT_PCR_analysis_of_specific_markers_indicates_pachytene_arrest_in_the_germ_cells_of_hsp90_945_gt_gt_mutant_mouse_testis_/479281", "title"=>"Quantitative RT-PCR analysis of specific markers indicates pachytene arrest in the germ cells of <i>hsp90α</i><sup>gt/gt</sup> mutant mouse testis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-31 02:34:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/808806"], "description"=>"<p>(A) Histological sections of testes of of wild-type (WT) and mutant (gt/gt) mice at 15, 21, 44 and 111 days after birth. In the righthand panels, arrows point out apoptotic nuclei and the asterisk in the P111 section indicates degenerating tubules. (B) Flow cytometric analysis of the DNA contents of the whole testis cell population at P44. (C) TUNEL analysis of sections of P21 testes.</p>", "links"=>[], "tags"=>["apoptosis", "mutant"], "article_id"=>479170, "categories"=>["Biochemistry", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Iwona Grad", "Christopher R. Cederroth", "Joël Walicki", "Corinne Grey", "Sofia Barluenga", "Nicolas Winssinger", "Bernard de Massy", "Serge Nef", "Didier Picard"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015770.g003", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Meiotic_arrest_and_apoptosis_in_hsp90_gt_gt_mutant_testis_/479170", "title"=>"Meiotic arrest and apoptosis in <i>hsp90α<sup>gt/gt</sup></i> mutant testis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-31 02:32:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/809101"], "description"=>"<p>The results shown are from a representative analysis of testis extracts from wild-type and mutant animals from P12 until completion of the first wave of spermatogenesis at P44. GAPDH serves as loading control. Note that the order of the sample pairs is reversed for the P16 and P18 samples at the center of the blots (area highlighted by hairlines).</p>", "links"=>[], "tags"=>["hsp90-", "hsp70-related"], "article_id"=>479453, "categories"=>["Biochemistry", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Iwona Grad", "Christopher R. Cederroth", "Joël Walicki", "Corinne Grey", "Sofia Barluenga", "Nicolas Winssinger", "Bernard de Massy", "Serge Nef", "Didier Picard"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015770.g006", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immunoblot_analysis_of_a_panel_of_Hsp90_and_Hsp70_related_proteins_/479453", "title"=>"Immunoblot analysis of a panel of Hsp90- and Hsp70-related proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-31 02:37:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/808699"], "description"=>"<p>(A) Morphology of seminal vesicles and testis of wild-type (WT) and <i>hsp90α<sup>gt/gt</sup></i> mutant (gt/gt) mice at P44. (B) Time course analysis of testis weight in WT and mutant (gt/gt) animals. n≥4. (C) No mature sperm cells could be detected in the epididymis of one year old <i>hsp90α<sup>gt/g</sup></i><sup>t</sup> animals.</p>", "links"=>[], "tags"=>["leads", "atrophic", "testis"], "article_id"=>479062, "categories"=>["Biochemistry", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Iwona Grad", "Christopher R. Cederroth", "Joël Walicki", "Corinne Grey", "Sofia Barluenga", "Nicolas Winssinger", "Bernard de Massy", "Serge Nef", "Didier Picard"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0015770.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Absence_of_Hsp90_945_leads_to_atrophic_testis_and_azoospermia_/479062", "title"=>"Absence of Hsp90α leads to atrophic testis and azoospermia.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-31 02:31:02"}

PMC Usage Stats | Further Information

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