title: Mechanism and regulation of rapid telomere prophase movements in mouse meiotic chromosomes.
abstract: Telomere-led rapid prophase movements (RPMs) in meiotic prophase have been observed in diverse eukaryote species. A shared feature of RPMs is that the force that drives the chromosomal movements is transmitted from the cytoskeleton, through the nuclear envelope, to the telomeres. Studies in mice suggested that dynein movement along microtubules is transmitted to telomeres through SUN1/KASH5 nuclear envelope bridges to generate RPMs. We monitored RPMs in mouse seminiferous tubules using 4D fluorescence imaging and quantitative motion analysis to characterize patterns of movement in the RPM process. We find that RPMs reflect a combination of nuclear rotation and individual chromosome movements. The telomeres move along microtubule tracks that are apparently continuous with the cytoskeletal network and exhibit characteristic arrangements at different stages of prophase. Quantitative measurements confirmed that SUN1/KASH5, microtubules, and dynein, but not actin, were necessary for RPMs and that defects in meiotic recombination and synapsis resulted in altered RPMs.
authors.affiliation: Program in Cell Cycle and Cancer Biology, Oklahoma Medical Research Foundation, Oklahoma City, OK 73104, USA.
authors.forename: Chih-Ying
authors.initials: CY
authors.lastname: Lee
authors.affiliation: Laboratory of Developmental and Regenerative Biology, Institute of Medical Biology, 8A Biomedical Grove, Immunos, Singapore 138648, Singapore.
authors.forename: Henning F
authors.initials: HF
authors.lastname: Horn
authors.affiliation: Laboratory of Developmental and Regenerative Biology, Institute of Medical Biology, 8A Biomedical Grove, Immunos, Singapore 138648, Singapore.
authors.forename: Colin L
authors.initials: CL
authors.lastname: Stewart
authors.affiliation: Laborotory of Nuclear Dynamics and Architecture, Institute of Medical Biology, 8A Biomedical Grove, Immunos, Singapore 138648, Singapore.
authors.forename: Brian
authors.initials: B
authors.lastname: Burke
authors.affiliation: Department of Biomedical Sciences, Cornell University, Ithaca, NY 14850, USA.
authors.forename: Ewelina
authors.initials: E
authors.lastname: Bolcun-Filas
authors.affiliation: Department of Biomedical Sciences, Cornell University, Ithaca, NY 14850, USA.
authors.forename: John C
authors.initials: JC
authors.lastname: Schimenti
authors.affiliation: Program in Cell Cycle and Cancer Biology, Oklahoma Medical Research Foundation, Oklahoma City, OK 73104, USA; Department of Cell Biology, University of Oklahoma Health Science Center, Oklahoma City, OK 73104, USA.
authors.forename: Michael E
authors.initials: ME
authors.lastname: Dresser
authors.affiliation: Program in Cell Cycle and Cancer Biology, Oklahoma Medical Research Foundation, Oklahoma City, OK 73104, USA; Department of Cell Biology, University of Oklahoma Health Science Center, Oklahoma City, OK 73104, USA. Electronic address: roberto-pezza@omrf.org.
authors.forename: Roberto J
authors.initials: RJ
authors.lastname: Pezza
mesh_terms: D000818:Animals; D018797:Cell Cycle Proteins / Q000378:metabolism; D003598:Cytoskeletal Proteins; D008297:Male; D051379:Mice; D008810:Mice, Inbred C57BL; D008869:Microtubule-Associated Proteins / Q000378:metabolism; D008870:Microtubules / Q000378:metabolism; D009685:Nuclear Envelope / Q000378:metabolism / Q000648:ultrastructure; D009687:Nuclear Proteins / Q000378:metabolism; D011418:Prophase; D012671:Seminiferous Tubules / Q000378:metabolism / Q000648:ultrastructure*; D016615:Telomere / Q000235:genetics* / Q000648:ultrastructure
chemical_list: D018797:Cell Cycle Proteins; D003598:Cytoskeletal Proteins; C575644:KASH5 protein, mouse; D008869:Microtubule-Associated Proteins; D009687:Nuclear Proteins; C464932:SUN1 protein, mouse