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Review
. 2013 Aug;194(4):817-46.
doi: 10.1534/genetics.112.145276.

The composition, functions, and regulation of the budding yeast kinetochore

Sue Biggins  1
Affiliations
Review

The composition, functions, and regulation of the budding yeast kinetochore

Sue Biggins. Genetics. 2013 Aug.

Abstract

The propagation of all organisms depends on the accurate and orderly segregation of chromosomes in mitosis and meiosis. Budding yeast has long served as an outstanding model organism to identify the components and underlying mechanisms that regulate chromosome segregation. This review focuses on the kinetochore, the macromolecular protein complex that assembles on centromeric chromatin and maintains persistent load-bearing attachments to the dynamic tips of spindle microtubules. The kinetochore also serves as a regulatory hub for the spindle checkpoint, ensuring that cell cycle progression is coupled to the achievement of proper microtubule-kinetochore attachments. Progress in understanding the composition and overall architecture of the kinetochore, as well as its properties in making and regulating microtubule attachments and the spindle checkpoint, is discussed.

Keywords: biorientation; budding yeast; kinetochore; microtubules; spindle checkpoint.

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Figures

Figure 1
Figure 1
Key structures that mediate chromosome segregation. A cartoon of a budding yeast cell shows three populations of microtubules in green (astral, kinetochore, and interpolar) that emanate from the spindle pole bodies (SPBs). The nucleus is shown in blue with SPBs embedded in its nuclear envelope (black) and the kinetochores on the chromosomes are shown in red.
Figure 2
Figure 2
Steps leading to bioriented kinetochore attachments. (A) The kinetochore initially makes a lateral attachment to a microtubule. (B) The kinetochore is transported toward the pole. The transport can either be mediated by motor and regulatory proteins (left), or the microtubule can depolymerize until the kinetochore is attached to the end of the microtubule (right). Note that sometimes the microtubule polymerizes to prevent the kinetochore from detaching if a proper end-on attachment is not made. (C) Once the chromosomes are near the pole, the sister kinetochores attach to microtubules from opposite poles. (D) The sister kinetochores make stable, bioriented attachments that are under tension until anaphase is initiated.
Figure 3
Figure 3
Types of kinetochore–microtubule attachments. (A) Bioriented (amphitelic) attachments occur when sister kinetochores bind to microtubules from opposite poles. (B) Syntelic attachments occur when both sister kinetochores attach to microtubules from the same pole. (C) Monotelic attachments occur when a single sister kinetochore binds to a microtubule from one pole.
Figure 4
Figure 4
Schematic of the yeast centromere. The conserved structure is ∼120 bp and contains three elements, CDEI, CDEII, and CDEIII. CDE1 is 8–10 bp and binds to the Cbf1 protein. CDEIII is 26 bp and binds to the CBF3 complex that consists of Ndc10, Cep3, Ctf13, and Skp1. The CDEII element is AT rich and wraps around the centromeric nucleosome.
Figure 5
Figure 5
Model for the inner kinetochore. One possible model, based on Cho and Harrison (2012), suggests that the Ndc10 homodimer within the CBF3 complex interacts with CDEI and CDEIII to loop the centromeric DNA. Ndc10 also recruits the Scm3 chaperone that deposits Cse4, leading to the specialized inner centromere structure.
Figure 6
Figure 6
Model for the budding yeast kinetochore. (A) Schematic indicating the rough position and stoichiometry of the budding yeast kinetochore subcomplexes. (B) Electron microscope image of a purified yeast kinetochore particle bound to a microtubule, originally published in Gonen et al. (2012). There is a ring that encircles the microtubule and globular domains that could represent KMN that touch the microtubule. Bar, 200 μm.
Figure 7
Figure 7
Spindle checkpoint pathway. Mps1 phosphorylates Spc105 to recruit the Bub1/3 proteins. Once Bub1/3 are bound to phosphorylated Spc105, the Mad1/Mad2 complex is recruited to the kinetochore. The open form of Mad2 is converted to a closed form, and the closed Mad2 binds to Cdc20 and eventually forms a mitotic checkpoint complex (containing Bub3, Mad2, Mad3, and Cdc20) that inhibits the progression into anaphase.
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References

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