The Proteomic Landscape of Centromeric Chromatin Reveals an Essential Role for the Ctf19CCAN Complex in Meiotic Kinetochore Assembly

Borek, Weronika E.; Vincenten, Nadine; Duro, Eris; Makrantoni, Vasso; Spanos, Christos; Sarangapani, Krishna K.; Alves, Flávia de Lima; Kelly, David A.; Asbury, Charles L.; Rappsilber, Juri; Marston, Adèle L.

doi:10.1016/j.cub.2020.10.025

Cited by 16 publications

(16 citation statements)

References 82 publications

(153 reference statements)

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“…Budding yeast meiotic kinetochores have a similar composition to mitotic kinetochores, with the addition of meiosis-specific factors ( (27,216); see also below). However, the pathways that govern the assembly and maintenance of kinetochores may differ in meiosis compared to mitosis since kinetochore integrity and viability in budding yeast meiosis relies on CCAN subunits that are dispensable for mitotic growth (26). In the budding mitotic yeast cell cycle, kinetochores remain fully assembled except for a brief period during S phase (127).…”

Section: Architecture Of Meiotic Kinetochoresmentioning

confidence: 99%

The Four Causes: The Functional Architecture of Centromeres and Kinetochores

McAinsh

Marston

2022

Annu. Rev. Genet.

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Kinetochores are molecular machines that power chromosome segregation during the mitotic and meiotic cell divisions of all eukaryotes. Aristotle explains how we think we have knowledge of a thing only when we have grasped its cause. In our case, to gain understanding of the kinetochore, the four causes correspond to questions that we must ask: ( a) What are the constituent parts, ( b) how does it assemble, ( c) what is the structure and arrangement, and ( d) what is the function? Here we outline the current blueprint for the assembly of a kinetochore, how functions are mapped onto this architecture, and how this is shaped by the underlying pericentromeric chromatin. The view of the kinetochore that we present is possible because an almost complete parts list of the kinetochore is now available alongside recent advances using in vitro reconstitution, structural biology, and genomics. In many organisms, each kinetochore binds to multiple microtubules, and we propose a model for how this ensemble-level architecture is organized, drawing on key insights from the simple one microtubule–one kinetochore setup in budding yeast and innovations that enable meiotic chromosome segregation. Expected final online publication date for the Annual Review of Genetics, Volume 56 is November 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

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Section: Architecture Of Meiotic Kinetochoresmentioning

confidence: 99%

The Four Causes: The Functional Architecture of Centromeres and Kinetochores

McAinsh

Marston

2022

Annu. Rev. Genet.

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“…Thus, we asked whether Spo13's function in preventing sporulation at meiosis I depends on the integrity of kinetochores. Deletion of subunits of the inner kinetochore Ctf19-complex, such as Mcm21 or Iml3, is compatible with proliferation but prevents kinetochore reassembly at entry into metaphase I, leading to massive chromosome miss-segregation (Mehta et al, 2014;Borek et al, 2021). Thus, mcm21D and iml3D mutants produce four spores of low viability (3 and 18%, respectively).…”

Section: Control Of Spore Formation By Spo13 Does Not Require Intact ...mentioning

confidence: 99%

The Spo13/Meikin pathway confines the onset of gamete differentiation to meiosis II in yeast

Mengoli

Rojas

et al. 2022

The EMBO Journal

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Sexual reproduction requires genome haploidization by the two divisions of meiosis and a differentiation program to generate gametes. Here, we have investigated how sporulation, the yeast equivalent of gamete differentiation, is coordinated with progression through meiosis. Spore differentiation is initiated at metaphase II when a membrane-nucleating structure, called the meiotic plaque, is assembled at the centrosome. While all components of this structure accumulate already at entry into meiosis I, they cannot assemble because centrosomes are occupied by Spc72, the receptor of the c-tubulin complex. Spc72 is removed from centrosomes by a pathway that depends on the polo-like kinase Cdc5 and the meiosis-specific kinase Ime2, which is unleashed by the degradation of Spo13/Meikin upon activation of the anaphasepromoting complex at anaphase I. Meiotic plaques are finally assembled upon reactivation of Cdk1 at entry into metaphase II. This unblocking-activation mechanism ensures that only singlecopy genomes are packaged into spores and might serve as a paradigm for the regulation of other meiosis II-specific processes.

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“…In support of these results, a recent study on proteomic analysis of the mitotic and meiotic kinetochores revealed an extensive reorganization of kinetochore during meiosis, specifically during prophase I to metaphase I transition with respect to mitosis. [60] Hence, mitotically non-essential Mcm proteins play unique and critical roles in the assembly of the meiotic kinetochore. Rigorous analysis of the meiotic kinetochores using biochemical, proteomics, and imaging tools may reveal exciting results in terms of content, quantity, and temporal appearance of the constituent proteins at the kinetochore and how it may differ from a mitotic kinetochore.…”

Section: Kinetochore Assemblymentioning

confidence: 99%

Minichromosome maintenance proteins in eukaryotic chromosome segregation

et al. 2021

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Minichromosome maintenance (Mcm) proteins are well-known for their functions in DNA replication. However, their roles in chromosome segregation are yet to be reviewed in detail. Following the discovery in 1984, a group of Mcm proteins, known as the ARS-nonspecific group consisting of Mcm13, Mcm16-19, and Mcm21-22, were characterized as bonafide kinetochore proteins and were shown to play significant roles in the kinetochore assembly and high-fidelity chromosome segregation. This review focuses on the structure, function, and evolution of this group of Mcm proteins. Our in silico analysis of the physical interactors of these proteins reveals that they share non-overlapping functions despite being copurified in biochemically stable complexes. We have discussed the contrasting results reported in the literature and experimental strategies to address them. Taken together, this review focuses on the structure-function of the ARS-nonspecific Mcm proteins and their evolutionary flexibility to maintain genome stability in various organisms.

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The Proteomic Landscape of Centromeric Chromatin Reveals an Essential Role for the Ctf19CCAN Complex in Meiotic Kinetochore Assembly

Cited by 16 publications

References 82 publications

The Four Causes: The Functional Architecture of Centromeres and Kinetochores

The Four Causes: The Functional Architecture of Centromeres and Kinetochores

The Spo13/Meikin pathway confines the onset of gamete differentiation to meiosis II in yeast

Minichromosome maintenance proteins in eukaryotic chromosome segregation

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