Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1

Shinichi Machida; Motoki Takaku; Masae Ikura; Jiying Sun; Hidekazu Suzuki; Wataru Kobayashi; Aiko Kinomura; Akihisa Osakabe; Hiroaki Tachiwana; Yasunori Horikoshi; Atsuhiko Fukuto; Ryo Matsuda; Kiyoe Ura; Satoshi Tashiro; Tsuyoshi Ikura; Hitoshi Kurumizaka

doi:10.1038/srep04863

Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1

Shinichi Machida, Motoki Takaku, Masae Ikura, Jiying Sun, Hidekazu Suzuki, Wataru Kobayashi, Aiko Kinomura, Akihisa Osakabe, Hiroaki Tachiwana, Yasunori Horikoshi, Atsuhiko Fukuto, Ryo Matsuda, Kiyoe Ura, Satoshi Tashiro, Tsuyoshi Ikura, Hitoshi Kurumizaka

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35 Citations (Scopus)

Abstract

Homologous recombination plays essential roles in mitotic DNA double strand break (DSB) repair and meiotic genetic recombination. In eukaryotes, RAD51 promotes the central homologous-pairing step during homologous recombination, but is not sufficient to overcome the reaction barrier imposed by nucleosomes. RAD54, a member of the ATP-dependent nucleosome remodeling factor family, is required to promote the RAD51-mediated homologous pairing in nucleosomal DNA. In higher eukaryotes, most nucleosomes form higher-ordered chromatin containing the linker histone H1. However, the mechanism by which RAD51/RAD54-mediated homologous pairing occurs in higher-ordered chromatin has not been elucidated. In this study, we found that a histone chaperone, Nap1, accumulates on DSB sites in human cells and DSB repair is substantially decreased in Nap1-knockdown cells. We determined that Nap1 binds to RAD54, enhances the RAD54-mediated nucleosome remodeling by evicting histone H1 and eventually stimulates the RAD51-mediated homologous pairing in higher-ordered chromatin containing histone H1.

Original language	English
Article number	4863 (2014)
Number of pages	11
Journal	Scientific Reports
Volume	4
DOIs	https://doi.org/10.1038/srep04863
Publication status	Published - 6 May 2015

Keywords

chromatin remodeling
DNA recombination

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10.1038/srep04863

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Machida, S., Takaku, M., Ikura, M., Sun, J., Suzuki, H., Kobayashi, W., Kinomura, A., Osakabe, A., Tachiwana, H., Horikoshi, Y., Fukuto, A., Matsuda, R., Ura, K., Tashiro, S., Ikura, T., & Kurumizaka, H. (2015). Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1. Scientific Reports, 4, Article 4863 (2014). https://doi.org/10.1038/srep04863

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title = "Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1",

abstract = "Homologous recombination plays essential roles in mitotic DNA double strand break (DSB) repair and meiotic genetic recombination. In eukaryotes, RAD51 promotes the central homologous-pairing step during homologous recombination, but is not sufficient to overcome the reaction barrier imposed by nucleosomes. RAD54, a member of the ATP-dependent nucleosome remodeling factor family, is required to promote the RAD51-mediated homologous pairing in nucleosomal DNA. In higher eukaryotes, most nucleosomes form higher-ordered chromatin containing the linker histone H1. However, the mechanism by which RAD51/RAD54-mediated homologous pairing occurs in higher-ordered chromatin has not been elucidated. In this study, we found that a histone chaperone, Nap1, accumulates on DSB sites in human cells and DSB repair is substantially decreased in Nap1-knockdown cells. We determined that Nap1 binds to RAD54, enhances the RAD54-mediated nucleosome remodeling by evicting histone H1 and eventually stimulates the RAD51-mediated homologous pairing in higher-ordered chromatin containing histone H1.",

keywords = "chromatin remodeling, DNA recombination",

author = "Shinichi Machida and Motoki Takaku and Masae Ikura and Jiying Sun and Hidekazu Suzuki and Wataru Kobayashi and Aiko Kinomura and Akihisa Osakabe and Hiroaki Tachiwana and Yasunori Horikoshi and Atsuhiko Fukuto and Ryo Matsuda and Kiyoe Ura and Satoshi Tashiro and Tsuyoshi Ikura and Hitoshi Kurumizaka",

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doi = "10.1038/srep04863",

language = "English",

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Machida, S, Takaku, M, Ikura, M, Sun, J, Suzuki, H, Kobayashi, W, Kinomura, A, Osakabe, A, Tachiwana, H, Horikoshi, Y, Fukuto, A, Matsuda, R, Ura, K, Tashiro, S, Ikura, T & Kurumizaka, H 2015, 'Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1', Scientific Reports, vol. 4, 4863 (2014). https://doi.org/10.1038/srep04863

TY - JOUR

T1 - Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1

AU - Machida, Shinichi

AU - Takaku, Motoki

AU - Ikura, Masae

AU - Sun, Jiying

AU - Suzuki, Hidekazu

AU - Kobayashi, Wataru

AU - Kinomura, Aiko

AU - Osakabe, Akihisa

AU - Tachiwana, Hiroaki

AU - Horikoshi, Yasunori

AU - Fukuto, Atsuhiko

AU - Matsuda, Ryo

AU - Ura, Kiyoe

AU - Tashiro, Satoshi

AU - Ikura, Tsuyoshi

AU - Kurumizaka, Hitoshi

PY - 2015/5/6

Y1 - 2015/5/6

N2 - Homologous recombination plays essential roles in mitotic DNA double strand break (DSB) repair and meiotic genetic recombination. In eukaryotes, RAD51 promotes the central homologous-pairing step during homologous recombination, but is not sufficient to overcome the reaction barrier imposed by nucleosomes. RAD54, a member of the ATP-dependent nucleosome remodeling factor family, is required to promote the RAD51-mediated homologous pairing in nucleosomal DNA. In higher eukaryotes, most nucleosomes form higher-ordered chromatin containing the linker histone H1. However, the mechanism by which RAD51/RAD54-mediated homologous pairing occurs in higher-ordered chromatin has not been elucidated. In this study, we found that a histone chaperone, Nap1, accumulates on DSB sites in human cells and DSB repair is substantially decreased in Nap1-knockdown cells. We determined that Nap1 binds to RAD54, enhances the RAD54-mediated nucleosome remodeling by evicting histone H1 and eventually stimulates the RAD51-mediated homologous pairing in higher-ordered chromatin containing histone H1.

AB - Homologous recombination plays essential roles in mitotic DNA double strand break (DSB) repair and meiotic genetic recombination. In eukaryotes, RAD51 promotes the central homologous-pairing step during homologous recombination, but is not sufficient to overcome the reaction barrier imposed by nucleosomes. RAD54, a member of the ATP-dependent nucleosome remodeling factor family, is required to promote the RAD51-mediated homologous pairing in nucleosomal DNA. In higher eukaryotes, most nucleosomes form higher-ordered chromatin containing the linker histone H1. However, the mechanism by which RAD51/RAD54-mediated homologous pairing occurs in higher-ordered chromatin has not been elucidated. In this study, we found that a histone chaperone, Nap1, accumulates on DSB sites in human cells and DSB repair is substantially decreased in Nap1-knockdown cells. We determined that Nap1 binds to RAD54, enhances the RAD54-mediated nucleosome remodeling by evicting histone H1 and eventually stimulates the RAD51-mediated homologous pairing in higher-ordered chromatin containing histone H1.

KW - chromatin remodeling

KW - DNA recombination

UR - http://dx.doi.org/10.1038/srep04863

U2 - 10.1038/srep04863

DO - 10.1038/srep04863

M3 - Article

SN - 2045-2322

VL - 4

JO - Scientific Reports

JF - Scientific Reports

M1 - 4863 (2014)

ER -

Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1

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