Nucleolin Participates in DNA Double-Strand Break-Induced Damage Response through MDC1-Dependent Pathway

Kobayashi, Junya; Fujimoto, Hiroko; Sato, Jun; Hayashi, Ikue; Burma, Sandeep; Matsuura, Shinya; Chen, David J.; Komatsu, Kenshi

doi:10.1371/journal.pone.0049245

Cited by 66 publications

(66 citation statements)

References 49 publications

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“…After finishing the repair of damaged DNA, γ-H2AX foci disappear, and the checkpoint is closed, which allows re-entry into the cell cycle. In mammalian cells, γ-H2AX could accumulate around damaged chromatin (14,(47)(48)(49). In the present study, γ-H2AX appeared in nuclear foci within 1 h following exposure to IR.…”

Section: Discussionsupporting

confidence: 59%

MIIP gene expression is associated with radiosensitivity in human nasopharyngeal carcinoma cells

et al. 2018

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Abstract. The present study aims to investigate the radiosensitization effect of the migration and invasion inhibitory protein (MIIP) gene on nasopharyngeal carcinoma (NPC) cells. The MIIP gene was transfected into NPC 5-8F and CNE2 cells. The level of MIIP was analyzed by quantitative reverse transcription-polymerase chain reaction analysis and western blot. The changes in radiosensitivity of the cells were analyzed by colony formation assay. The changes in cell apoptosis and cycle distribution following irradiation were detected by flow cytometry. The expression of BCL2 associated X, apoptosis regulator/B-cell lymphoma 2 was evaluated using western blot. DNA damage was analyzed by counting γ-H2AX foci. The expression levels of γ-H2AX were evaluated by immunofluorescence and western blot. In a previous study by the authors, the results indicated that the expression of MIIP gene evidently increased in MIIP-transfected 5-8F (5-8F OE) and MIIP-transfected CNE2 (CNE2 OE) cells compared with the parental or negative control cells. In the present study, the survival rate of 5-8F OE and CNE2 OE cells markedly decreased following irradiation (0, 2, 4, 6 and 8 Gy) compared with the negative control (5-8F NC and CNE2 NC) and the untreated (5-8F and CNE2) groups. The expression of MIIP was able to increase apoptosis, which resulted in G2/M cell cycle arrest and DNA damage repair was attenuated in 5-8F and CNE2 cells following irradiation as measured by the accumulation of γ-H2AX. It was indicated that MIIP expression is associated with the radiosensitivity of NPC cells and has a significant role in regulating cell radiosensitivity.

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Section: Discussionsupporting

confidence: 59%

MIIP gene expression is associated with radiosensitivity in human nasopharyngeal carcinoma cells

et al. 2018

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“…Recently, it has been proposed that histone chaperones play a central role in chromatin disassembly connected with DNA repair and transcription recovery following DNA damage (7,9,13,35). Thus, histone chaperones such as HIRA (13), FACT (12), nucleolin (14), APLF (6) Asf1 (9), CAF-1 (10), DAXX (11), p400 (15), NAP1L1, and NAP1L4 (7) actively promote transient chromatin disorganization and histone reshaping in response to DNA damage (8). Because SET/ TAF-Iβ belongs to the NAP1 family, it is tempting to hypothesize a role-similar to that described for the above-mentioned histone chaperones-for SET/TAF-Iβ in chromatin reshaping in response to DNA lesions.…”

Section: Discussionmentioning

confidence: 99%

“…In fact, histone chaperones have emerged as key players in the transient disorganization of chromatin required in the DNA repair process. Thus, the histone chaperones aprataxin-PNK-like factor (APLF) (6), antisilencing function 1 (Asf1) (9), chromatin assembly factor 1 (CAF-1) (10), death domain-associated protein 6 (DAXX) (11), facilitating chromatin transcription (FACT) (12), histone regulator A (HIRA) (13), nucleolin (14), p400 (15), and nucleosome assembly protein 1-like 1 (NAP1L1) and 1-like 4 (NAP1L4) (7) are recruited to damaged chromatin, thereby promoting histone dynamics in response to DNA damage. Recently, SET/TAF-1β was found to be recruited to DNA breaks to modulate the DNA damage response through the retention of certain chromatin proteins, resulting in chromatin compaction (16).…”

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confidence: 99%

Structural basis for inhibition of the histone chaperone activity of SET/TAF-Iβ by cytochromec

González‐Arzola

Dı́az-Moreno

Cano-González

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

119

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Chromatin is pivotal for regulation of the DNA damage process insofar as it influences access to DNA and serves as a DNA repair docking site. Recent works identify histone chaperones as key regulators of damaged chromatin’s transcriptional activity. However, understanding how chaperones are modulated during DNA damage response is still challenging. This study reveals that the histone chaperone SET/TAF-Iβ interacts with cytochrome c following DNA damage. Specifically, cytochrome c is shown to be translocated into cell nuclei upon induction of DNA damage, but not upon stimulation of the death receptor or stress-induced pathways. Cytochrome c was found to competitively hinder binding of SET/TAF-Iβ to core histones, thereby locking its histone-binding domains and inhibiting its nucleosome assembly activity. In addition, we have used NMR spectroscopy, calorimetry, mutagenesis, and molecular docking to provide an insight into the structural features of the formation of the complex between cytochrome c and SET/TAF-Iβ. Overall, these findings establish a framework for understanding the molecular basis of cytochrome c-mediated blocking of SET/TAF-Iβ, which subsequently may facilitate the development of new drugs to silence the oncogenic effect of SET/TAF-Iβ’s histone chaperone activity.

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“…The NBS1 protein interacts with several functional proteins, including ATM, and these interactions are vital for various DDRs. Several years ago, we found that NBS1 physically and functionally interacts with the histone modification enzyme RNF20 and the chromatin remodeler-like factor nucleolin, and these interactions play a key role in ATMdependent cell cycle checkpoint pathways and DSB repair (mainly homologous recombination (HR) repair) (Nakamura et al, 2011;Kobayashi et al, 2012). In this review, we mainly focus on the functions of NBS1 and its relationship with histone modification and chromatin remodeling in DDRs induced by DSBs.…”

Section: Introductionmentioning

confidence: 99%

“…Several years ago, we identified the major nucleolar protein nucleolin as a novel binding partner of γ-H2AX (Kobayashi et al, 2012). As well as interacting with γ-H2AX, nucleolin also interacts with NBS1 following IR.…”

Section: Introductionmentioning

confidence: 99%

Chromatin modification and NBS1: their relationship in DNA double-strand break repair

2015

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The importance of chromatin modification, including histone modification and chromatin remodeling, for DNA double-strand break (DSB) repair, as well as transcription and replication, has been elucidated. Phosphorylation of H2AX to γ-H2AX is one of the first responses following DSB detection, and this histone modification is important for the DSB damage response by triggering several events, including the accumulation of DNA damage response-related proteins and subsequent homologous recombination (HR) repair. The roles of other histone modifications such as acetylation, methylation and ubiquitination have also been recently clarified, particularly in the context of HR repair. NBS1 is a multifunctional protein that is involved in various DNA damage responses. Its recently identified binding partner RNF20 is an E3 ubiquitin ligase that facilitates the monoubiquitination of histone H2B, a process that is crucial for recruitment of the chromatin remodeler SNF2h to DSB damage sites. Evidence suggests that SNF2h functions in HR repair, probably through regulation of end-resection. Moreover, several recent reports have indicated that SNF2h can function in HR repair pathways as a histone remodeler and that other known histone remodelers can also participate in DSB damage responses. On the other hand, information about the roles of such chromatin modifications and NBS1 in non-homologous end joining (NHEJ) repair of DSBs and stalled fork-related damage responses is very limited; therefore, these aspects and processes need to be further studied to advance our understanding of the mechanisms and molecular players involved.

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Nucleolin Participates in DNA Double-Strand Break-Induced Damage Response through MDC1-Dependent Pathway

Cited by 66 publications

References 49 publications

MIIP gene expression is associated with radiosensitivity in human nasopharyngeal carcinoma cells

MIIP gene expression is associated with radiosensitivity in human nasopharyngeal carcinoma cells

Structural basis for inhibition of the histone chaperone activity of SET/TAF-Iβ by cytochromec

Chromatin modification and NBS1: their relationship in DNA double-strand break repair

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