Stable complex formation of CENP-B with the CENP-A nucleosome

Fujita, Ryosuke; Otake, Kazuo; Arimura, Yasuhiro; Horikoshi, Naoki; Miya, Yuta; Shiga, T.; Osakabe, Akihisa; Tachiwana, Hiroaki; Ohzeki, Jun Ichirou; Larionov, Vladimir; Masumoto, Hiroshi; Kurumizaka, Hitoshi

doi:10.1093/nar/gkv405

Cited by 58 publications

(69 citation statements)

References 70 publications

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“…In human, CENP-B binds to a specific sequence called the CENP-B box within alpha satellite DNA and induces efficient de novo CENP-A recruitment, leading to stable centromere formation (Ikeno et al, 1998;Ohzeki, Nakano, Okada, & Masumoto, 2002;Okada et al, 2007;Fachinetti et al, 2015;Fujita et al, 2015). Surprisingly, there is no consensus sequence for CENP-B boxes in both OwlAlp1 and OwlAlp2, and in fact, signals of CENP-B were hardly detected by immunofluorescent microscopy (Kugou et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Alpha satellite DNA‐repeat OwlAlp1 forms centromeres in Azara’s owl monkey

2019

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Centromeres play crucial roles in faithful chromosome segregation and genome integrity. In simian primates, centromeres possess tandem array of alpha satellite DNA (also referred to as alphoid DNA). Average sizes of alpha satellite repeat units vary between species, for example, 171 bp in human and 343–344 bp in many platyrrhini species (New World monkeys). Interestingly, Azara's owl monkey (Aotus azarae), a platyrrhini species, possesses alpha satellite DNA of two distinct unit sizes, OwlAlp1 (185 bp) and OwlAlp2 (344 bp), both of which present as megasatellite DNAs in the genome. It is, however, unknown which repeat sequence is responsible for functional centromere formation. To investigate the localization of centromeres in vivo, we carried out chromatin immunoprecipitation (ChIP) assay using Azara's owl monkey cells. We found that CENP‐A, a histone H3 variant essential for centromere formation, was enriched at OwlAlp1, but not at OwlAlp2. Moreover, CENP‐A was detected only at constricted regions of chromosomes by immunofluorescent microscopy. In contrast, trimethylation of histone H3‐K9 (H3K9me3), a marker of heterochromatin, was enriched at both OwlAlp1 and OwlAlp2. Our results show that the shorter alpha satellite repeat, OwlAlp1, is selectively used for centromere formation in this monkey.

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Section: Discussionmentioning

confidence: 99%

Alpha satellite DNA‐repeat OwlAlp1 forms centromeres in Azara’s owl monkey

2019

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“…Several recent and older observations support a role of CENP-B in the stabilization of centromere structure. For instance, CENP-B appears to contribute to the phasing of CENP-A nucleosomes on centromeric DNA and to the typical unwrapping of its nucleosomal termini [146], and it increases the stability of reconstituted CENP-A nucleosomes [201], likely through a direct interaction with the N-terminal region of CENP-A [199]. Furthermore, CENP-B binds directly to CENP-C, supporting a second pathway of CENP-C recruitment in addition to that based on the interaction of CENP-C with the CENP-A C-terminal tail [159,199].…”

Section: The Inner Kinetochorementioning

confidence: 99%

A Molecular View of Kinetochore Assembly and Function

Musacchio

Desai

2017

Biology

484

589

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Kinetochores are large protein assemblies that connect chromosomes to microtubules of the mitotic and meiotic spindles in order to distribute the replicated genome from a mother cell to its daughters. Kinetochores also control feedback mechanisms responsible for the correction of incorrect microtubule attachments, and for the coordination of chromosome attachment with cell cycle progression. Finally, kinetochores contribute to their own preservation, across generations, at the specific chromosomal loci devoted to host them, the centromeres. They achieve this in most species by exploiting an epigenetic, DNA-sequence-independent mechanism; notable exceptions are budding yeasts where a specific sequence is associated with centromere function. In the last 15 years, extensive progress in the elucidation of the composition of the kinetochore and the identification of various physical and functional modules within its substructure has led to a much deeper molecular understanding of kinetochore organization and the origins of its functional output. Here, we provide a broad summary of this progress, focusing primarily on kinetochores of humans and budding yeast, while highlighting work from other models, and present important unresolved questions for future studies.

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“…One possibility is that the b/n-box dimer configuration is somehow optimal for kinetochore functioning. CENP-B binds DNA at a 17 bp b-box sequence that is located in the linker DNA between nucleosomes (Fujita et al 2015;Hasson et al 2013;Henikoff et al 2015). The b/n-box dimer configuration enables a single CENP-B dimer to bind simultaneously to both of the bboxes in neighboring dimers within an HOR (Yoda et al 1998;Tawaramoto et al 2003).…”

Section: Influence Of Modular B/n-box Dimer Structurementioning

confidence: 99%

A Game of Thrones at Human Centromeres II. A new molecular/evolutionary model

Rice

2019

Preprint

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Human centromeres are remarkable in four ways: they are i) defined epigenetically by an elevated concentration of the histone H3 variant CENP-A, ii) inherited epigenetically by trans-generational cary-over of nucleosomes containing CENP-A, iii) formed over unusually long and complex tandem repeats (Higher Order Repeats, HORs) that extend over exceptionally long arrays of DNA (up to 8 Mb), and iv) evolve in such a rapid and punctuated manner that most HORs on orthologous chimp and human chromosomes are in different clades. What molecular and evolutionary processes generated these distinctive characteristics? Here I motivate and construct a new model for the formation, expansion/contraction, homogenization and rapid evolution of human centromeric repeat arrays that is based on fork-collapse during DNA replication (in response to proteins bound to DNA and/or collisions between DNA and RNA polymerases) followed by out-of-register re-initiation of replication via Break-Induced Repair (BIR). The model represents a new form of molecular drive. It predicts rapid and sometimes punctuated evolution of centromeric HORs due to a new form of intragenomic competition that is based on two features: i) the rate of tandem copy number expansion, and ii) resistance to invasion by pericentric heterochromatin within a centromere's HOR array. These features determine which variant array elements will eventually occupy a pivotal region within a centromeric repeat array (switch-point) that gradually expands to populate the entire array. In humans, continuous HOR turnover is predicted due to intra-array competition between three repeat types with an intransitive hierarchy: A < B < C < A, where A = short, single-dimer HORs containing one monomer that binds centromere protein-B (CENP-B) and another that does not, B = moderately longer HORs composed of ≥ 2 dimers, and C = substantially longer HORs that lose their dimeric modular structure. Continuous turnover of proteins that bind centromeric DNA (but these proteins are not constituents of the kinetochore) and polygenic variation influencing position-effect variegation are predicted to cause rapid turnover of centromeric repeats in species lacking HORs and/or CENP-B binding at centromeres. Evolution at centromeres is a molecular 'Game-of-Thrones' because centromeric sequences 'reign' due to an epigenetic 'crown' of CENP-A that is perpetually 'usurped' by new sequences that more rapidly assemble large 'armies' of tandem repeats and/or resist 'invasion' from a surrounding 'frontier' of percentric heterochromatin. These 'regal transitions' occur in a backdrop of slashing and decapitation (fork-collapse generating truncated sister chromatids) in the context of promiscuous sex that is frequently incestuous (out-of-register BIR between sibling chromatids).

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Stable complex formation of CENP-B with the CENP-A nucleosome

Cited by 58 publications

References 70 publications

Alpha satellite DNA‐repeat OwlAlp1 forms centromeres in Azara’s owl monkey

Alpha satellite DNA‐repeat OwlAlp1 forms centromeres in Azara’s owl monkey

A Molecular View of Kinetochore Assembly and Function

A Game of Thrones at Human Centromeres II. A new molecular/evolutionary model

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