Microtubule-organizing center formation at telomeres induces meiotic telomere clustering

Yoshida, Masashi; Katsuyama, Satoshi; Tateho, Kazuki; Nakamura, Hiromitsu; Miyoshi, Junpei; Ohba, Tatsunori; Matsuhara, Hirotada; Miki, Futaba; Okazaki, Keishi; Haraguchi, Tokuko; Niwa, Osami; Hiraoka, Yasushi; Yamamoto, Ayumu

doi:10.1083/jcb.201207168

Cited by 48 publications

(71 citation statements)

References 52 publications

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“…Interestingly, Kms1 is also required for normal meiotic prophase, suggesting that the KASH proteins might play discrete roles in meiosis and mitosis, as suggested by our genetic analysis (Fig. 4D,F) (Shimanuki et al, 1997;Yoshida et al, 2013). …”

Section: Evidence For Both Dispersive and Conservative Aspects Of Spbsupporting

confidence: 60%

The KASH protein Kms2 coordinates mitotic remodeling of the spindle pole body

Wälde

King

2014

Journal of Cell Science

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Defects in the biogenesis of the spindle pole body (SPB), the yeast centrosome equivalent, can lead to monopolar spindles and mitotic catastrophe. The KASH domain protein Kms2 and the SUN domain protein Sad1 colocalize within the nuclear envelope at the site of SPB attachment during interphase and at the spindle poles during mitosis in Schizosaccharomyces pombe. We show that Kms2 interacts with the essential SPB components Cut12 and Pcp1 and the Polo kinase Plo1. Depletion of Kms2 delays mitotic entry and leads to defects in the insertion of the SPB into the nuclear envelope, disrupting stable bipolar spindle formation. These effects are mediated in part by a delay in the recruitment of Plo1 to the SPB at mitotic entry. Plo1 activity supports mitotic SPB remodeling by driving a burst of incorporation of Cut12 and Pcp1. Thus, a fission yeast SUN-KASH complex plays an important role in supporting the remodeling of the SPB at mitotic entry.

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Section: Evidence For Both Dispersive and Conservative Aspects Of Spbsupporting

confidence: 60%

The KASH protein Kms2 coordinates mitotic remodeling of the spindle pole body

Wälde

King

2014

Journal of Cell Science

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“…On the basis of studies done in C. elegans, Schizosaccharomyces pombe, maize and mouse, we reasoned that the microtubule cytoskeleton was a good candidate to drive these nuclear rotations 15,17,18,30,31 . We first examined in more detail the organization of microtubules in region 1 germline cysts.…”

Section: Microtubules Are Required For Centromere Dynamicsmentioning

confidence: 99%

Microtubule-driven nuclear rotations promote meiotic chromosome dynamics

et al. 2015

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At the onset of meiosis, each chromosome needs to find its homologue and pair to ensure proper segregation. In Drosophila, pairing occurs during the mitotic cycles preceding meiosis. Here we show that germ cell nuclei undergo marked movements during this developmental window. We demonstrate that microtubules and Dynein are driving nuclear rotations and are required for centromere pairing and clustering. We further found that Klaroid (SUN) and Klarsicht (KASH) co-localize with centromeres at the nuclear envelope and are required for proper chromosome motions and pairing. We identified Mud (NuMA in vertebrates) as co-localizing with centromeres, Klarsicht and Klaroid. Mud is also required to maintain the integrity of the nuclear envelope and for the correct assembly of the synaptonemal complex. Our findings reveal a mechanism for chromosome pairing in Drosophila, and indicate that microtubules, centrosomes and associated proteins play a crucial role in the dynamic organization of chromosomes inside the nucleus.

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“…These proteins tether telomeres to the INM to ensure bouquet formation. Then, at the INM, telomeres are associated with the transmembrane linker of nucleoskeleton and cytoskeleton (LINC) complex that is composed of SUN and KASH domain proteins (Ding et al, 2007;Yoshida et al, 2013). This transmembrane complex transduces cytoskeletal forces to telomeres and drives telomere clustering along the INM and, therefore, chromosome movements (Starr and Fridolfsson, 2010).…”

Section: Introductionmentioning

confidence: 99%

The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

et al. 2017

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Telomere bouquet formation, a highly conserved meiotic event, plays an important role in homologous pairing and therefore progression of meiosis; however, the underlying molecular mechanism remains largely unknown. Here, we identified ZYGOTENE1 (ZYGO1), a novel F-box protein in rice (Oryza sativa), and verified its essential role in bouquet formation during early meiosis. In zygo1 mutants, zygotene chromosome aggregation and telomere clustering failed to occur. The suppressed telomere clustering in homologous pairing aberration in rice meiosis1 (pair1) zygo1 and rice completion of meiotic recombination (Oscom1) zygo1 double mutants, together with the altered localization of OsSAD1 (a SUN protein associated with the nuclear envelope) in zygo1, showed that ZYGO1 has a significant function in bouquet formation. In addition, the interaction between ZYGO1 and rice SKP1-like protein 1 suggested that ZYGO1 might modulate bouquet formation as a component of the SKP1-Cullin1-F-box complex. Although double-strand break formation and early recombination element installation occurred normally, zygo1 mutants showed defects in full-length pairing and synaptonemal complex assembly. Furthermore, crossover (CO) formation was disturbed, and foci of Human enhancer of invasion 10 were restricted to the partially synapsed chromosome regions, indicating that CO reduction might be caused by the failure of full-length chromosome alignment in zygo1. Therefore, we propose that ZYGO1 mediates bouquet formation to efficiently promote homolog pairing, synapsis, and CO formation in rice meiosis.

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Microtubule-organizing center formation at telomeres induces meiotic telomere clustering

Abstract: Telomere-localized SUN and KASH proteins induce formation of a microtubule-based “telocentrosome” that fosters microtubule motor-dependent telomere clustering.

Cited by 48 publications

References 52 publications

The KASH protein Kms2 coordinates mitotic remodeling of the spindle pole body

The KASH protein Kms2 coordinates mitotic remodeling of the spindle pole body

Microtubule-driven nuclear rotations promote meiotic chromosome dynamics

The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

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