Mechanism and Regulation of Rapid Telomere Prophase Movements in Mouse Meiotic Chromosomes

Chih Ying Lee, Henning Horn, Colin L. Stewart, Brian Burke, Ewelina Bolcun-Filas, John C. Schimenti, Michael E. Dresser, Roberto J. Pezza

Research output: Contribution to journalArticle

25 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)551-563
Number of pages13
JournalCell Reports
Volume11
Issue number4
DOIs
Publication statusPublished - 28 Apr 2015

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Dyneins
Prophase
Telomere
Chromosomes
Actins
Lead
Fluorescence
Imaging techniques
Defects
Microtubules
Nuclear Envelope
Chromosome Pairing
Seminiferous Tubules
Optical Imaging
Eukaryota
Cytoskeleton
Genetic Recombination
Motion analysis

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Lee, C. Y., Horn, H., Stewart, C. L., Burke, B., Bolcun-Filas, E., Schimenti, J. C., ... Pezza, R. J. (2015). Mechanism and Regulation of Rapid Telomere Prophase Movements in Mouse Meiotic Chromosomes. Cell Reports, 11(4), 551-563. https://doi.org/10.1016/j.celrep.2015.03.045

Mechanism and Regulation of Rapid Telomere Prophase Movements in Mouse Meiotic Chromosomes. / Lee, Chih Ying; Horn, Henning; Stewart, Colin L.; Burke, Brian; Bolcun-Filas, Ewelina; Schimenti, John C.; Dresser, Michael E.; Pezza, Roberto J.

In: Cell Reports, Vol. 11, No. 4, 28.04.2015, p. 551-563.

Research output: Contribution to journalArticle

Lee, CY, Horn, H, Stewart, CL, Burke, B, Bolcun-Filas, E, Schimenti, JC, Dresser, ME & Pezza, RJ 2015, 'Mechanism and Regulation of Rapid Telomere Prophase Movements in Mouse Meiotic Chromosomes', Cell Reports, vol. 11, no. 4, pp. 551-563. https://doi.org/10.1016/j.celrep.2015.03.045
Lee, Chih Ying ; Horn, Henning ; Stewart, Colin L. ; Burke, Brian ; Bolcun-Filas, Ewelina ; Schimenti, John C. ; Dresser, Michael E. ; Pezza, Roberto J. / Mechanism and Regulation of Rapid Telomere Prophase Movements in Mouse Meiotic Chromosomes. In: Cell Reports. 2015 ; Vol. 11, No. 4. pp. 551-563.
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