Meiotic behaviours of chromosomes and microtubules in budding yeast: relocalization of centromeres and telomeres during meiotic prophase

Hayashi, Aki; Ogawa, Hideyuki; Kohno, Kenji; Gasser, Susan M.; Hiraoka, Yasushi

doi:10.1046/j.1365-2443.1998.00215.x

Cited by 75 publications

(86 citation statements)

References 50 publications

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“…CFP was PCR amplified from pDH3 (Yeast Resource Center, University of Washington, Seattle, WA) and inserted into the NruI site of RAP1, as described for Rap1-GFP (64). Digestion with SpeI targeted plasmid integration for 2-step gene replacement.…”

Section: Discussionmentioning

confidence: 99%

MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae

Conrad

Lee

Wilkerson

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

139

254

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In meiotic prophase, telomeres associate with the nuclear envelope and accumulate adjacent to the centrosome/spindle pole to form the chromosome bouquet, a well conserved event that in Saccharomyces cerevisiae requires the meiotic telomere protein Ndj1p. Ndj1p interacts with Mps3p, a nuclear envelope SUN domain protein that is required for spindle pole body duplication and for sister chromatid cohesion. Removal of the Ndj1p-interaction domain from MPS3 creates an ndj1⌬-like separation-of-function allele, and Ndj1p and Mps3p are codependent for stable association with the telomeres. SUN domain proteins are found in the nuclear envelope across phyla and are implicated in mediating interactions between the interior of the nucleus and the cytoskeleton. Our observations indicate a general mechanism for meiotic telomere movements.meiosis ͉ SUN ͉ telomere ͉ nondisjunction H omologous chromosome pairing and recombination during meiotic prophase are required to orient chromosomes for disjunction and haploidization during the meiotic divisions. Early in meiotic prophase, telomeres attach to and move along the nuclear envelope to concentrate transiently in one sector of the nucleus, generally adjacent to the centrosome, forming the chromosome bouquet, a widely conserved arrangement (1-7). Bouquet formation may promote homologous chromosome pairing and also may help to untangle chromosomes, to regulate recombination at telomeres, to regulate crossover distribution, to coordinate or synchronize chromosomal events by propagating signals from the telomeres, and/or to facilitate synaptonemal complex formation (see refs. 1, 5, and 7-10). Despite the wide conservation of bouquet formation, the molecular mechanisms responsible for telomere attachments and movements in meiosis are poorly understood.In Saccharomyces cerevisiae, the meiotic bouquet resembles that of multicellular organisms (11)(12)(13)(14). Ndj1p is a meiosisspecific protein that accumulates at telomeres in S. cerevisiae (15,16) and is required for bouquet formation (17). Deletion of NDJ1 delays axial element formation, homolog pairing, synapsis and onset of the first meiotic division, causes an elevated frequency of nondisjunction and of ectopic recombination, and reduces spore formation and viability (15-21). Early recombination intermediates form between homologs with wild-type kinetics in ndj1⌬, suggesting that some aspect of bouquet formation is required for the normal coupling of the molecular and cytological events of pairing (22).A large-scale two-hybrid screen (23) identified an interaction between NDJ1 and MPS3/NEP98 (24, 25). Mps3p is an essential, integral membrane protein that is concentrated at the spindle pole body (SPB), the S. cerevisiae centrosome equivalent, and is present at lower levels throughout the nuclear membrane. Mps3p is required for duplication of the SPB (24, 25) and also functions in karyogamy and in sister chromatid cohesion (25,26). The present study demonstrates a critical requirement for the Ndj1p-Mps3p interaction for bouquet forma...

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Section: Discussionmentioning

confidence: 99%

MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae

Conrad

Lee

Wilkerson

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

139

254

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“…To confirm the effect of the clb5 clb6 mutation on telomere dynamics, we examined intranuclear foci formed by the telomeric marker protein Rap1-GFP (Hayashi et al 1998). Disengagement of Rap1 foci from the nuclear periphery was delayed in clb5 clb6 when To quantify subnuclear positioning of a telomere, the area of the nucleus is measured and equally divided into three zones (Zone I, Zone II, and Zone III).…”

Section: Timely Telomere Dislodgement Is Dependent On Expression Of Smentioning

confidence: 99%

Release of yeast telomeres from the nuclear periphery is triggered by replication and maintained by suppression of Ku-mediated anchoring

Ebrahimi

Donaldson²

2008

Genes Dev.

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The perinuclear localization of Saccharomyces cerevisiae telomeres provides a useful model for studying mechanisms that control chromosome positioning. Telomeres tend to be localized at the nuclear periphery during early interphase, but following S phase they delocalize and remain randomly positioned within the nucleus. We investigated whether DNA replication causes telomere delocalization from the nuclear periphery. Using live-cell fluorescence microscopy, we show that delaying DNA replication causes a corresponding delay in the dislodgment of telomeres from the nuclear envelope, demonstrating that replication of individual telomeres causes their delocalization. Telomere delocalization is not simply the result of recruitment to a replication factory in the nuclear interior, since we found that telomeric DNA replication can occur either at the nuclear periphery or in the nuclear interior. The telomere-binding complex Ku is one of the factors that localizes telomeres to the nuclear envelope. Using a gene locus tethering assay, we show that Ku-mediated peripheral positioning is switched off after DNA replication. Based on these findings, we propose that DNA replication causes telomere delocalization by triggering stable repression of the Ku-mediated anchoring pathway. In addition to maintaining genetic information, DNA replication may therefore regulate subnuclear organization of chromatin.[Keywords: Telomere; replication; nuclear organization; Saccharomyces cerevisiae] Supplemental material is available at http://www.genesdev.org.

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“…S. cerevisiae Nuf2 also disappears from the centromere during meiosis (Hayashi et al, 1998;Asakawa et al, 2005). The biological significance of dissociation of the Ndc80 and Mis12 complexes during meiotic prophase remains unknown.…”

Section: Mis12 and Ndc80 Complexes: Facultative Components Of The Kinmentioning

confidence: 99%

Reconstruction of the Kinetochore during Meiosis in Fission Yeast Schizosaccharomyces pombe

Hayashi

Asakawa

Haraguchi

et al. 2006

MBoC

Self Cite

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During the transition from mitosis to meiosis, the kinetochore undergoes significant reorganization, switching from a bipolar to a monopolar orientation. To examine the centromere proteins that are involved in fundamental reorganization in meiosis, we observed the localization of 22 mitotic and 2 meiotic protein components of the kinetochore during meiosis in living cells of the fission yeast. We found that the 22 mitotic proteins can be classified into three groups: the Mis6-like group, the NMS (Ndc80-Mis12-Spc7) group, and the DASH group, based on their meiotic behavior. Mis6-like group proteins remain at the centromere throughout meiosis. NMS group proteins disappear from the centromere at the onset of meiosis and reappear at the centromere in two steps in late prophase. DASH group proteins appear shortly before metaphase of meiosis I. These observations suggest that Mis6-like group proteins constitute the structural basis of the centromere and that the NMS and DASH group proteins reassemble to establish the functional metaphase kinetochore. On the other hand, the meiosis-specific protein Moa1, which plays an important role in forming the meiotic monopolar kinetochore, is loaded onto the centromere significantly earlier than the NMS group, whereas another meiosis-specific protein, Sgo1, is loaded at times similar to the NMS group.

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Meiotic behaviours of chromosomes and microtubules in budding yeast: relocalization of centromeres and telomeres during meiotic prophase

Cited by 75 publications

References 50 publications

MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae

MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae

Release of yeast telomeres from the nuclear periphery is triggered by replication and maintained by suppression of Ku-mediated anchoring

Reconstruction of the Kinetochore during Meiosis in Fission Yeast Schizosaccharomyces pombe

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