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• W2024064038 abstract "Proper chromosome segregation depends on correct attachments between microtubules and kinetochores. Budding yeast have been thought to achieve these attachments with different kinetics than other eukaryotes. Now, deploying specialized data processing techniques to achieve super-resolution images, Marco et al. demonstrate that this tractable cell-cycle model system shares more similarities with plants and animals than previously thought. Proper chromosome segregation depends on correct attachments between microtubules and kinetochores. Budding yeast have been thought to achieve these attachments with different kinetics than other eukaryotes. Now, deploying specialized data processing techniques to achieve super-resolution images, Marco et al. demonstrate that this tractable cell-cycle model system shares more similarities with plants and animals than previously thought. Dividing eukaryotic cells face a universal challenge—in order to deliver duplicated chromosomes to separate daughter cells, they must establish stable connections between a pair of sister kinetochores residing on each mitotic chromosome and microtubules of the mitotic spindle. This process, known as chromosome biorientation, involves molecular machines and regulatory feedback circuits that are conserved throughout all simple and complex eukaryotes. Malformed attachments, such as when a pair of kinetochores attach to the same pole (“syntelic” attachments), cannot properly segregate, and result in aneuploidy, are linked to birth defects and cancer promotion in animals and humans. Several model systems are used to study mitosis, with S. cerevisiae being one of the most powerful and popular. Unlike most animal and plant cells, this budding yeast uses a closed mitosis where the nuclear envelope remains intact throughout M phase. The spindle pole body (SPB) is embedded in the nuclear envelope and nucleates intranuclear microtubules that attach to kinetochores throughout the cell cycle. A prevailing view has been that biorientation occurs early in budding yeast, before M phase, as opposed to biorientation in animal and plant cells that occurs gradually throughout M phase in an apparently random cycle of microtubule-kinetochore destabilization and reattachment. In this issue of Cell, Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar revisit this issue by directly imaging yeast kinetochores during chromosome biorientation. They are by no means the first to make such a measurement, but their approach is the most comprehensive and direct to date, and their results clarify a number of outstanding questions in the field. Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar use three assays to measure chromosome biorientation. First, they image fixed cells in 3D where the SPB and all kinetochores are labeled. Because the distance between SPBs in a cell is related to mitotic progression, the degree of pairing and position of kinetochores on the mitotic spindle can be related to mitotic progression using a statistically valid sample. They then image living cells bearing a GFP mark at the centromere of chromosome IV (“GFP-CEN IV”) to directly measure sister kinetochore dynamics and position, although at a single kinetochore pair and for a limited period of time—photobleaching limits data collection to ∼3 min, a small portion of a full mitosis. These dynamic data are then related to a population sample of fixed GFP-CEN IV cells. The attachment state of sister kinetochore pairs is determined by direct measurement of the distance between CEN IV pairs using software that identifies and tracks sister kinetochores. As they use sophisticated Gaussian fitting to identify the position of each kinetochore (Dorn et al., 2005Dorn J.F. Jaqaman K. Rines D.R. Jelson G.S. Sorger P.K. Danuser G. Biophys. J. 2005; 89: 2835-2854Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar), they can achieve resolution improvements comparable to optical super-resolution techniques in living cells (Schermelleh et al., 2010Schermelleh L. Heintzmann R. Leonhardt H. J. Cell Biol. 2010; 190: 165-175Crossref PubMed Scopus (977) Google Scholar). Combining the direct, dynamic data with the fixed cell “snapshot” data, Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar directly measure the position of kinetochore pairs on the spindle throughout M phase and build a comprehensive picture of the establishment of biorientation during M phase in yeast. The first surprising result of Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar involves the establishment of biorientation during M phase. Given a closed mitosis, microtubule-kinetochore attachments that persist throughout the cell cycle, and several reports of a bilobed distribution of kinetochores on the metaphase plate (He et al., 2001He X. Rines D.R. Espelin C.W. Sorger P.K. Cell. 2001; 106: 195-206Abstract Full Text Full Text PDF PubMed Scopus (218) Google Scholar), it has been presumed that yeast sister kinetochores are largely bioriented in M phase because resolution of any maloriented pairs happens earlier in S and G2. By directly imaging and identifying sister kinetochore pairs, Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar observe that ∼50% of sister pairs are maloriented upon entry into M phase, and this proportion gradually reduces until just before initiation of anaphase. As expected, this gradual establishment of biorientation is dependent on Ipl1, the S. cerevisiae ortholog of the Aurora B kinase, which is a component of the chromosome passenger complex that phosphorylates several kinetochore components and destabilizes kinetochore-microtubule attachments (Biggins et al., 1999Biggins S. Severin F.F. Bhalla N. Sassoon I. Hyman A.A. Murray A.W. Genes Dev. 1999; 13: 532-544Crossref PubMed Scopus (340) Google Scholar, Carmena and Earnshaw, 2003Carmena M. Earnshaw W.C. Nat. Rev. Mol. Cell Biol. 2003; 4: 842-854Crossref PubMed Scopus (992) Google Scholar, Tanaka et al., 2002Tanaka T.U. Rachidi N. Janke C. Pereira G. Galova M. Schiebel E. Stark M.J.R. Nasmyth K. Cell. 2002; 108: 317-329Abstract Full Text Full Text PDF PubMed Scopus (574) Google Scholar). This random detachment allows released kinetochores another chance to bind a microtubule from the opposing pole and thus to gradually establish bioriented attachment. This mechanism is similar to the pathway observed in animal cells, allowing Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar to propose that prometaphase in budding yeast serves the same function as it does in plants and animals (Figure 1). In all three of their assays, Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar consistently observe that kinetochores are located a specified distance, ∼0.4 um, from the SPB. Because the SPB nucleates most of the spindle microtubules, this implies that the length of spindle microtubules is tightly regulated. Images of bipolar spindles therefore show two “lobes” or distributions of kinetochores ∼0.4 um from each SPB. This “bilobed” distribution has often been assumed to represent bioriented sister kinetochores stretched across the midzone of the spindle (He et al., 2001He X. Rines D.R. Espelin C.W. Sorger P.K. Cell. 2001; 106: 195-206Abstract Full Text Full Text PDF PubMed Scopus (218) Google Scholar). However, the snapshot assay clearly reveals maloriented and bioriented kinetochore pairs in each of the lobes. They do record cases of pairs stretched across the midzone, but these are relatively rare at any point in time—most bioriented pairs exist within the same lobe, although over the course of full M phase, about half of the sisters in a cell traverse the midzone at least once. How spindle microtubule length is regulated isn’t completely revealed in this study, although it seems likely that factors that control that control microtubule stability will be involved. Indeed, Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar find that mutations in Stu2, which promotes microtubule stability, fail to establish biorientation probably because microtubules cannot achieve lengths sufficient to extend from one SPB across the midzone and attach to free kinetochores in the opposite lobe. Deletion of Cin8, a kinesin-5 motor that helps define the length of kinetochore-attached microtubules, resulted in less-defined kinetochore lobes, consistent with previous results (Gardner et al., 2008Gardner M.K. Bouck D.C. Paliulis L.V. Meehl J.B. O’Toole E.T. Haase J. Soubry A. Joglekar A.P. Winey M. Salmon E.D. et al.Cell. 2008; 135: 894-906Abstract Full Text Full Text PDF PubMed Scopus (132) Google Scholar). Kinetochores in Δcin8 cells show increased transits across the spindle midzone and higher tubulin density in the midzone and thus probably have more microtubules that extend from one side of the spindle to the other. The conclusions of Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar differ from previous work that used fluorescence recovery after photobleaching (FRAP) to monitor the switching of kinetochores between each side of the spindle in living cells (Pearson et al., 2004Pearson C.G. Yeh E. Gardner M. Odde D. Salmon E.D. Bloom K. Curr. Biol. 2004; 14: 1962-1967Abstract Full Text Full Text PDF PubMed Scopus (133) Google Scholar). This previous work concluded that such events were rare and that most sister kinetochores in a yeast mitotic spindle were bioriented well before anaphase initiates. Although Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar directly visualize significant numbers of sister pairs that have yet to biorient in M phase mitotic spindles, they detect small numbers of transits across the midzone. The next phase in this work is to use a much more photon-efficient method to minimize damage in live-cell imaging, perhaps a light sheet microscope similar to that used by Capoulade et al., 2011Capoulade J. Wachsmuth M. Hufnagel L. Knop M. Nat. Biotechnol. 2011; 29: 835-839Crossref PubMed Scopus (130) Google Scholar to follow yeast kinetochores through a full mitosis and to directly examine their dynamics. If Marco et al., 2013Marco E. Dorn J.F. Hsu P.-h. Jaqaman K. Sorger P.K. Danuser G. Cell. 2013; 154 (this issue): 1127-1139Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar are correct, mitosis in the simple eukaryote S. cerevisiae will prove to even more closely resemble the process that is now known in animal and plant cells. Work in the Swedlow lab on chromosome segregation and imaging is funded by the BBSRC (BB/H013024/1), the MRC (MR/K015869/1), and the Wellcome Trust (095931/Z/11/Z). S. cerevisiae Chromosomes Biorient via Gradual Resolution of Syntely between S Phase and AnaphaseMarco et al.CellAugust 29, 2013In BriefSuper-resolution imaging approaches debunk an assumption that yeasts biorient their chromosomes with different kinetics than plant and animal cells. Full-Text PDF Open Archive" @default.
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• W2024064038 title "At the (Kineto)chore, Yeast Really Are Like People" @default.
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