title: Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation.
abstract: Telomeres and centromeres have traditionally been considered to perform distinct roles. During meiotic prophase, in a conserved chromosomal configuration called the bouquet, telomeres gather to the nuclear membrane (NM), often near centrosomes. We found previously that upon disruption of the fission yeast bouquet, centrosomes failed to insert into the NM at meiosis I and nucleate bipolar spindles. Hence, the trans-NM association of telomeres with centrosomes during prophase is crucial for efficient spindle formation. Nonetheless, in approximately half of bouquet-deficient meiocytes, spindles form properly. Here, we show that bouquet-deficient cells can successfully undergo meiosis using centromere-centrosome contact instead of telomere-centrosome contact to generate spindle formation. Accordingly, forced association between centromeres and centrosomes fully rescued the spindle defects incurred by bouquet disruption. Telomeres and centromeres both stimulate focal accumulation of the SUN domain protein Sad1 beneath the centrosome, suggesting a molecular underpinning for their shared spindle-generating ability. Our observations demonstrate an unanticipated level of interchangeability between the two most prominent chromosomal landmarks.
authors: Telomere Biology Section, Laboratory of Biochemistry and Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892 Telomere Biology Laboratory, Cancer Research UK, London Research Institute, London WC2A 3LY, England, UK.
authors: Alex
authors: A
authors: Fennell
authors: Telomere Biology Section, Laboratory of Biochemistry and Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892 Telomere Biology Laboratory, Cancer Research UK, London Research Institute, London WC2A 3LY, England, UK.
authors: Alfonso
authors: A
authors: Fernández-Álvarez
authors: Chromosome Maintenance Group, UCL Cancer Institute, University College London, London WC1E 6DD, England, UK.
authors: Kazunori
authors: K
authors: Tomita
authors: Telomere Biology Section, Laboratory of Biochemistry and Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892 Telomere Biology Laboratory, Cancer Research UK, London Research Institute, London WC2A 3LY, England, UK julie.cooper@nih.gov.
authors: Julia Promisel
authors: JP
authors: Cooper
mesh_terms: D018797:Cell Cycle Proteins / Q000096:biosynthesis / Q000235:genetics; D002503:Centromere / Q000235:genetics*; D018385:Centrosome / Q000378:metabolism*; D002843:Chromatin / Q000235:genetics; D015825:Chromosomes, Fungal / Q000235:genetics; D004398:Dyneins / Q000235:genetics; D004722:Endoribonucleases / Q000235:genetics; D049452:Green Fluorescent Proteins / Q000096:biosynthesis / Q000235:genetics; D008540:Meiosis; D009685:Nuclear Envelope / Q000378:metabolism; D009687:Nuclear Proteins / Q000235:genetics; D012568:Schizosaccharomyces / Q000166:cytology / Q000235:genetics*; D029702:Schizosaccharomyces pombe Proteins / Q000096:biosynthesis / Q000235:genetics / Q000378:metabolism; D008941:Spindle Apparatus / Q000235:genetics*; D016615:Telomere / Q000235:genetics*; D034501:Telomere-Binding Proteins / Q000096:biosynthesis / Q000235:genetics
chemical_list: C510171:Bqt1 protein, S pombe; D018797:Cell Cycle Proteins; D002843:Chromatin; C507869:Hrs1 protein, S pombe; C107314:Mis6 protein, S pombe; D009687:Nuclear Proteins; C093512:SAD1 protein, S pombe; D029702:Schizosaccharomyces pombe Proteins; D034501:Telomere-Binding Proteins; C490196:nuf2 protein, S pombe; D049452:Green Fluorescent Proteins; C568524:Dcr1 protein, S pombe; D004722:Endoribonucleases; C505433:Dhc1 protein, S pombe; D004398:Dyneins