Evolutionary Turnover of Kinetochore Proteins: A Ship of Theseus?

Drinnenberg, Ines A.; Henikoff, Steven; Malik, Harmit S.

doi:10.1016/j.tcb.2016.01.005

Cited by 88 publications

(76 citation statements)

References 116 publications

(152 reference statements)

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“…S1A–C) (Cheerambathur and Desai, 2014; Chen and Mellone, 2016; Drinnenberg et al, 2016; Earnshaw, 2015; Fukagawa and Earnshaw, 2014; Hori and Fukagawa, 2012; Lampert and Westermann, 2011; McKinley and Cheeseman, 2015; Muller and Almouzni, 2014; Westhorpe and Straight, 2013). We generated polyclonal antibodies to the Ascaris histone H3 variant CENP-A, the inner kinetochore protein CENP-C, and the outer kinetochore protein NDC80 (see Supplemental Information).…”

Section: Resultsmentioning

confidence: 99%

“…A prevailing model of holocentric chromosomes is that multiple centromeric regions, kinetochores, and microtubule attachment sites are punctuated along the length of the chromosome (Drinnenberg et al, 2016; Maddox et al, 2004; McKinley and Cheeseman, 2015; Melters et al, 2012; Steiner and Henikoff, 2015). During nematode programmed DNA elimination, chromosomes break and some chromosome fragments are retained while others are lost.…”

Section: Introductionmentioning

confidence: 99%

“…To test whether the centromeres/kinetochores or microtubule attachment play a regulatory role during Ascaris DNA elimination, we generated antibodies to the histone H3 variant CENP-A (also known as CenH3), the epigenetic mark of centromeres (Black and Bassett, 2008; Chen and Mellone, 2016; De Rop et al, 2012; Drinnenberg et al, 2016; Earnshaw, 2015; Fukagawa and Earnshaw, 2014; McKinley and Cheeseman, 2015 ), and antibodies to components of the kinetochore. Our immunofluorescence staining data showed that CENP-A is reduced in chromosome regions that will be lost during DNA elimination, indicating centromere/kinetochore function is compromised in regions that will be eliminated.…”

Section: Introductionmentioning

confidence: 99%

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Differential Chromosomal Localization of Centromeric Histone CENP-A Contributes to Nematode Programmed DNA Elimination

et al. 2016

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SUMMARY Stability of the genome is paramount to organisms. However, diverse eukaryotes carry out programmed DNA elimination, in which portions or entire chromsomes are lost in early development or during sex determination. During early development of the parasitic nematode, Ascaris suum, 13% of the genome is eliminated. How different genomic segments are reproducibly retained or discarded is unknown. Here we show that centromeric histone CENP-A localization plays a key role in this process. We show that Ascaris chromosomes are holocentric during germline mitoses, with CENP-A distributed along their length. Prior to DNA elimination in the 4-cell embryo, CENP-A is significantly diminished in chromosome regions that will be lost. This leads to the absence of kinetochores and microtubule attachment sites necessary for chromosome segregation, resulting in loss of these regions upon mitosis. Our data suggest that changes in CENP-A localization specify which portions of chromosomes will be lost during programmed DNA elimination.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Differential Chromosomal Localization of Centromeric Histone CENP-A Contributes to Nematode Programmed DNA Elimination

et al. 2016

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“…The DNA sequence at regional centromeres evolves so rapidly and extensively that homology is often undetectable across short evolutionary time scales. Even the core sets of proteins associated with centromeres can vary across eukaryotic taxa (Drinnenberg et al 2016). Despite diversity, certain dominant themes reoccur in centromere organization.…”

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confidence: 99%

Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence

et al. 2017

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During cell division, spindle fibers attach to chromosomes at centromeres. The DNA sequence at regional centromeres is fast evolving with no conserved genetic signature for centromere identity. Instead CENH3, a centromere-specific histone H3 variant, is the epigenetic signature that specifies centromere location across both plant and animal kingdoms. Paradoxically, CENH3 is also adaptively evolving. An ongoing question is whether CENH3 evolution is driven by a functional relationship with the underlying DNA sequence. Here, we demonstrate that despite extensive protein sequence divergence, CENH3 histones from distant species assemble centromeres on the same underlying DNA sequence. We first characterized the organization and diversity of centromere repeats in wild-type Arabidopsis thaliana. We show that A. thaliana CENH3-containing nucleosomes exhibit a strong preference for a unique subset of centromeric repeats. These sequences are largely missing from the genome assemblies and represent the youngest and most homogeneous class of repeats. Next, we tested the evolutionary specificity of this interaction in a background in which the native A. thaliana CENH3 is replaced with CENH3s from distant species. Strikingly, we find that CENH3 from Lepidium oleraceum and Zea mays, although specifying epigenetically weaker centromeres that result in genome elimination upon outcrossing, show a binding pattern on A. thaliana centromere repeats that is indistinguishable from the native CENH3. Our results demonstrate positional stability of a highly diverged CENH3 on independently evolved repeats, suggesting that the sequence specificity of centromeres is determined by a mechanism independent of CENH3.

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“…In contrast, proteins of the outer kinetochore are nearly universally conserved, including in the kinetoplastid Trypanosoma, which also lacks canonical CCAN proteins (Akiyoshi and Gull 2014;Senaratne and Drinnenberg 2017). Identifying the chromatin counterparts of the CCAN in these lineages and determining whether insect holocentromeres are polycentric or diffuse are issues that remain to be addressed (Drinnenberg et al 2016).…”

Section: Insect Holocentromeres Lack Cenh3mentioning

confidence: 99%

Remarkable Evolutionary Plasticity of Centromeric Chromatin

Henikoff

Thakur

Kasinathan

et al. 2017

Cold Spring Harb Symp Quant Biol

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Centromeres were familiar to cell biologists in the late 19th century, but for most eukaryotes the basis for centromere specification has remained enigmatic. Much attention has been focused on the cenH3 (CENP-A) histone variant, which forms the foundation of the centromere. To investigate the DNA sequence requirements for centromere specification, we applied a variety of epigenomic approaches, which have revealed surprising diversity in centromeric chromatin properties. Whereas each point centromere of budding yeast is occupied by a single precisely positioned tetrameric nucleosome with one cenH3 molecule, the "regional" centromeres of fission yeast contain unphased presumably octameric nucleosomes with two cenH3s. In Caenorhabditis elegans, kinetochores assemble all along the chromosome at sites of cenH3 nucleosomes that resemble budding yeast point centromeres, whereas holocentric insects lack cenH3 entirely. The "satellite" centromeres of most animals and plants consist of cenH3-containing particles that are precisely positioned over homogeneous tandem repeats, but in humans, different α-satellite subfamilies are occupied by CENP-A nucleosomes with very different conformations. We suggest that this extraordinary evolutionary diversity of centromeric chromatin architectures can be understood in terms of the simplicity of the task of equal chromosome segregation that is continually subverted by selfish DNA sequences.

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Evolutionary Turnover of Kinetochore Proteins: A Ship of Theseus?

Cited by 88 publications

References 116 publications

Differential Chromosomal Localization of Centromeric Histone CENP-A Contributes to Nematode Programmed DNA Elimination

Differential Chromosomal Localization of Centromeric Histone CENP-A Contributes to Nematode Programmed DNA Elimination

Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence

Remarkable Evolutionary Plasticity of Centromeric Chromatin

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