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YB-1 disrupts mismatch repair complex formation, interferes with MutSα recruitment on mismatch and inhibits mismatch repair through interacting with PCNA

Oncogene volume 33, pages 5065–5077 (2014)Cite this article

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Abstract

Y-box binding protein-1 (YB-1) is highly expressed in tumors and it participates in various cellular processes. Previous studies indicated that YB-1 binds to mispaired DNA and interacts with several mismatch repair (MMR)-related factors. However, its role in the MMR system remains undefined. Here, we found that YB-1 represses mutS homolog 6 (MSH6)-containing MMR complex formation and reduces MutSα mismatch binding activity by disrupting interactions among MMR-related factors. In an effort to elucidate how YB-1 exerts this inhibitory effect, we have identified two functional proliferating cell nuclear antigen (PCNA)-interacting protein (PIP)-boxes that mediate YB-1/PCNA interaction and locate within the C-terminal region of YB-1. This interaction is critical for the regulatory role of YB-1 in repressing MutSα mismatch binding activity, disrupting MutSα/PCNA/G/T heteroduplex ternary complex formation and inhibiting in vitro MMR activity. The differential regulation of 3′ and 5′ nick-directed MMR activity by YB-1 was also observed. Moreover, YB-1 overexpression is associated with the alteration of microsatellite pattern and the enhancement of N-methyl-N′-nitro-N-nitrosoguanidine (MNNG)-induced and spontaneous mutations. Furthermore, upregulation of other PIP-box-containing proteins, such as myeloid cell leukemia-1 (Mcl-1) and inhibitor of growth protein 1b (ING1b), has no impact on MMR complex formation and mutation accumulation, thus revealing the significant effect of YB-1 on regulating the MMR system. In conclusion, our study suggests that YB-1 functions as a PCNA-interacting factor to exert its regulatory role on the MMR process and involves in the induction of genome instability, which may partially account for the oncogenic potential of YB-1.

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Acknowledgements

This study was supported by the following grants to Dr Yan-Hwa Wu Lee: the National Health Research Institute (NHRI-EX100-10014BI, NHRI-EX101-10014BI and NHRI-EX102-10014BI), the National Science Council (NSC-94-2320-B-010-005, NSC-95-2320-B-010-049-MY3, NSC-97-2320-B-010-014-MY3, NSC-97-2320-B-009-003-MY3, NSC-100-2320-B-009-007-MY3, NSC-101-2811-B-009-006 and NSC-102-2811-B-009-007) and the ‘Aim for the Top University Program’ of the National Yang-Ming University, the National Chiao-Tung University and the Ministry of Education, Taiwan, Republic of China. We thank Dr Tsung-Sheng Su and Dr Tzu-Hao Cheng for helpful discussions and suggestions, Dr Josef Jiricny, Dr Hsin-Fang Yang-Yen and Dr Zee-Fen Chang for kindly providing plasmids used in this study, Dr Shr-Jeng Leu for sharing experiences on baculovirus expression system and Dr Li-Li Li for critical reading and comments on this manuscript. We acknowledge the High-throughput Genome Analysis Core Facility of National Core Facility Program for Biotechnology, Taiwan (NSC 101-2319-B-010-001), for capillary electrophoresis and DNA sequencing.

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  1. Y-W Chang and R-T Mai: These authors contributed equally to this work.

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  1. Institute of Biochemistry and Molecular Biology, School of Life Sciences, National Yang-Ming University, Taipei, Taiwan

    Y-W Chang, R-T Mai, C-C Lin, C-C Chiu & Y-H Wu Lee

  2. Department of Biological Science and Technology, College of Biological Science and Technology, National Chiao-Tung University, Hsinchu, Taiwan

    R-T Mai & Y-H Wu Lee

  3. Department of Clinical Laboratory Sciences and Medical Biotechnology, National Taiwan University Hospital, Taipei, Taiwan

    W-H Fang

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Chang, YW., Mai, RT., Fang, WH. et al. YB-1 disrupts mismatch repair complex formation, interferes with MutSα recruitment on mismatch and inhibits mismatch repair through interacting with PCNA. Oncogene 33, 5065–5077 (2014). https://doi.org/10.1038/onc.2013.450

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