DNA Damage Triggers the Nuclear Accumulation of RASSF6 Tumor Suppressor Protein via CDK9 and BAF53 To Regulate p53 Target Gene Transcription

REFERENCES

• Allen NP, Donninger H, Vos MD, Eckfeld K, Hesson L, Gordon L, Birrer MJ, Latif F, Clark GJ. 2007. RASSF6 is a novel member of the RASSF family of tumor suppressors. Oncogene 26:6203–6211. https://doi.org/10.1038/sj.onc.1210440.
   PubMed Web of Science ®Google Scholar
• Ikeda M, Hirabayashi S, Fujiwara N, Mori H, Kawata A, Iida J, Bao Y, Sato Y, Iida T, Sugimura H, Hata Y. 2007. Ras-association domain family protein 6 induces apoptosis via both caspase-dependent and caspase-independent pathways. Exp Cell Res 313:1484–1495. https://doi.org/10.1016/j.yexcr.2007.02.013.
   PubMed Web of Science ®Google Scholar
• Iwasa H, Jiang X, Hata Y. 2015. RASSF6; the putative tumor suppressor of the RASSF family. Cancers (Basel) 7:2415–2426. https://doi.org/10.3390/cancers7040899.
   PubMed Web of Science ®Google Scholar
• Hesson LB, Dunwell TL, Cooper WN, Catchpoole D, Brini AT, Chiaramonte R, Griffiths M, Chalmers AD, Maher ER, Latif F. 2009. The novel RASSF6 and RASSF10 candidate tumour suppressor genes are frequently epigenetically inactivated in childhood leukaemias. Mol Cancer 8:42. https://doi.org/10.1186/1476-4598-8-42.
   PubMed Web of Science ®Google Scholar
• Richter AM, Pfeifer GP, Dammann RH. 2009. The RASSF proteins in cancer; from epigenetic silencing to functional characterization. Biochim Biophys Acta 1796:114–128. https://doi.org/10.1016/j.bbcan.2009.03.004.
   PubMed Web of Science ®Google Scholar
• Wen Y, Wang Q, Zhou C, Yan D, Qiu G, Yang C, Tang H, Peng Z. 2011. Decreased expression of RASSF6 is a novel independent prognostic marker of a worse outcome in gastric cancer patients after curative surgery. Ann Surg Oncol 18:3858–3867. https://doi.org/10.1245/s10434-011-1668-5.
   PubMed Web of Science ®Google Scholar
• Djos A, Martinsson T, Kogner P, Carén H. 2012. The RASSF gene family members RASSF5, RASSF6 and RASSF7 show frequent DNA methylation in neuroblastoma. Mol Cancer 11:40. https://doi.org/10.1186/1476-4598-11-40.
   PubMed Web of Science ®Google Scholar
• Liang YY, Chen MY, Hua YJ, Chen S, Zheng LS, Cao X, Peng LX, Xie P, Huang BJ, Sun R, Wang L, Xiang YQ, Guo X, Qian CN. 2014. Downregulation of Ras association domain family member 6 (RASSF6) underlies the treatment resistance of highly metastatic nasopharyngeal carcinoma cells. PLoS One 9:e100843. https://doi.org/10.1371/journal.pone.0100843.
   Google Scholar
• Mezzanotte JJ, Hill V, Schmidt ML, Shinawi T, Tommasi S, Krex D, Schackert G, Pfeifer GP, Latif F, Clark GJ. 2014. RASSF6 exhibits promoter hypermethylation in metastatic melanoma and inhibits invasion in melanoma cells. Epigenetics 9:1496–1503. https://doi.org/10.4161/15592294.2014.983361.
   PubMed Web of Science ®Google Scholar
• Guo W, Dong Z, Guo Y, Shen S, Guo X, Kuang G, Yang Z. 2016. Decreased expression and frequent promoter hypermethylation of RASSF2 and RASSF6 correlate with malignant progression and poor prognosis of gastric cardia adenocarcinoma. Mol Carcinog 55:1655–1666. https://doi.org/10.1002/mc.22416.
   PubMed Web of Science ®Google Scholar
• Ye HL, Li DD, Lin Q, Zhou Y, Zhou QB, Zeng B, Fu ZQ, Gao WC, Liu YM, Chen RW, Li ZH, Chen RF. 2015. Low RASSF6 expression in pancreatic ductal adenocarcinoma is associated with poor survival. World J Gastroenterol 21:6621–6630. https://doi.org/10.3748/wjg.v21.i21.6621.
   PubMed Web of Science ®Google Scholar
• Tan S, Bian X, Wu B, Chen X. 2019. RASSF6 is downregulated in human bladder cancers and regulates doxorubicin sensitivity and mitochondrial membrane potential via the Hippo signaling pathway. Onco Targets Ther 12:9189–9200. https://doi.org/10.2147/OTT.S217041.
   PubMed Web of Science ®Google Scholar
• Younesian S, Shahkarami S, Ghaffari P, Alizadeh S, Mehrasa R, Ghaffari SH. 2019. Residual methylation of tumor suppressor gene promoters, RASSF6 and RASSF10, as novel biomarkers for minimal residual disease detection in adult acute lymphoblastic leukemia. Ann Hematol 98:2719–2727. https://doi.org/10.1007/s00277-019-03775-y.
   PubMed Web of Science ®Google Scholar
• Ikeda M, Kawata A, Nishikawa M, Tateishi Y, Yamaguchi M, Nakagawa K, Hirabayashi S, Bao Y, Hidaka S, Hirata Y, Hata Y. 2009. Hippo pathway-dependent and -independent roles of RASSF6. Sci Signal 2:ra59. https://doi.org/10.1126/scisignal.2000300.
   PubMed Web of Science ®Google Scholar
• Withanage K, Nakagawa K, Ikeda M, Kurihara H, Kudo T, Yang Z, Sakane A, Sasaki T, Hata Y. 2012. Expression of RASSF6 in kidney and the implication of RASSF6 and the Hippo pathway in the sorbitol-induced apoptosis in renal proximal tubular epithelial cells. J Biochem 152:111–119. https://doi.org/10.1093/jb/mvs056.
   PubMed Web of Science ®Google Scholar
• Iwasa H, Kudo T, Maimaiti S, Ikeda M, Maruyama J, Nakagawa K, Hata Y. 2013. The RASSF6 tumor suppressor protein regulates apoptosis and the cell cycle via MDM2 protein and p53 protein. J Biol Chem 288:30320–30329. https://doi.org/10.1074/jbc.M113.507384.
   PubMed Web of Science ®Google Scholar
• Sarkar A, Iwasa H, Hossain S, Xu X, Sawada T, Shimizu T, Maruyama J, Arimoto-Matsuzaki K, Hata Y. 2017. Domain analysis of Ras-association domain family member 6 upon interaction with MDM2. FEBS Lett 591:260–272. https://doi.org/10.1002/1873-3468.12551.
   PubMed Web of Science ®Google Scholar
• Shimizu T, Nakamura T, Inaba H, Iwasa H, Maruyama J, Arimoto-Matsuzaki K, Nakata T, Nishina H, Hata Y. 2020. The RAS-interacting chaperone UNC119 drives the RASSF6-MDM2-p53 axis and antagonizes RAS-mediated malignant transformation. J Biol Chem 295:11214–11230. https://doi.org/10.1074/jbc.RA120.012649.
   PubMed Web of Science ®Google Scholar
• Hossain S, Iwasa H, Sarkar A, Maruyama J, Arimoto-Matsuzaki K, Hata Y. 2018. The RASSF6 tumor suppressor protein regulates apoptosis and the cell cycle progression via retinoblastoma protein. Mol Cell Biol 38:e00046-18. https://doi.org/10.1128/MCB.00046-18.
   Google Scholar
• Wang M, Gu C, Qi T, Tang W, Wang L, Wang S, Zeng X. 2007. BAF53 interacts with p53 and functions in p53-mediated p21-gene transcription. J Biochem 142:613–620. https://doi.org/10.1093/jb/mvm176.
   PubMed Web of Science ®Google Scholar
• Oh J, Sohn DH, Ko M, Chung H, Jeon SH, Seong RH. 2008. BAF60a interacts with p53 to recruit the SWI/SNF complex. J Biol Chem 283:11924–11934. https://doi.org/10.1074/jbc.M705401200.
   PubMed Web of Science ®Google Scholar
• Han J, Kim T, Moon S, Park J-H, Lee W, Ko Y-J, Ryu K-S, Yun J-H, Lee W. 2021. NMR spectroscopy uncovers direct interaction between BAF60A and p53. Biochem Biophys Res Commun 534:815–821. https://doi.org/10.1016/j.bbrc.2020.10.101.
   PubMed Web of Science ®Google Scholar
• Iwasa H, Kuroyanagi H, Maimaiti S, Ikeda M, Nakagawa K, Hata Y. 2013. Characterization of RSF-1, the Caenorhabditis elegans homolog of the Ras-association domain family protein 1. Exp Cell Res 319:1–11. https://doi.org/10.1016/j.yexcr.2012.10.008.
   PubMed Web of Science ®Google Scholar
• Zhao K, Wang W, Rando OJ, Xue Y, Swiderek K, Kuo A, Crabtree GR. 1998. Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95:625–636. https://doi.org/10.1016/S0092-8674(00)81633-5.
   PubMed Web of Science ®Google Scholar
• Van Duyne R, Guendel I, Narayanan A, Gregg E, Shafagati N, Tyagi M, Easley R, Klase Z, Nekhai S, Kehn-Hall K, Kashanchi F. 2011. Varying modulation of HIV-1 LTR activity by Baf complexes. J Mol Biol 411:581–596. https://doi.org/10.1016/j.jmb.2011.06.001.
   PubMed Web of Science ®Google Scholar
• Avruch J, Xavier R, Bardeesy N, Zhang XF, Praskova M, Zhou D, Xia F. 2009. Rassf family of tumor suppressor polypeptides. J Biol Chem 284:11001–11005. https://doi.org/10.1074/jbc.R800073200.
   PubMed Web of Science ®Google Scholar
• Sherwood V, Recino A, Jeffries A, Ward A, Chalmers AD. 2009. The N-terminal RASSF family: a new group of Ras-association-domain-containing proteins, with emerging links to cancer formation. Biochem J 425:303–311. https://doi.org/10.1042/BJ20091318.
   PubMed Web of Science ®Google Scholar
• Underhill-Day N, Hill V, Latif F. 2011. N-terminal RASSF family: RASSF7-RASSF10. Epigenetics 6:284–292. https://doi.org/10.4161/epi.6.3.14108.
   PubMed Web of Science ®Google Scholar
• Iwasa H, Hossain S, Hata Y. 2018. Tumor suppressor C-RASSF proteins. Cell Mol Life Sci 75:1773–1787. https://doi.org/10.1007/s00018-018-2756-5.
   PubMed Web of Science ®Google Scholar
• Reeves ME, Firek M, Chen ST, Amaar Y. 2013. The RASSF1 gene and the opposing effects of the RASSF1A and RASSF1C isoforms on cell proliferation and apoptosis. Mol Biol Int 2013:145096. https://doi.org/10.1155/2013/145096.
   PubMedGoogle Scholar
• Vlahov N, Scrace S, Soto MS, Grawenda AM, Bradley L, Pankova D, Papaspyropoulos A, Yee KS, Buffa F, Goding CR, Timpson P, Sibson N, O'Neill E. 2015. Alternate RASSF1 transcripts control SRC activity, E-cadherin contacts, and YAP-mediated invasion. Curr Biol 25:3019–3034. https://doi.org/10.1016/j.cub.2015.09.072.
   PubMed Web of Science ®Google Scholar
• Xu X, Iwasa H, Hossain S, Sarkar A, Maruyama J, Arimoto-Matsuzaki K, Hata Y. 2017. BCL-XL binds and antagonizes RASSF6 tumor suppressor to suppress p53 expression. Genes Cells 22:993–1003. https://doi.org/10.1111/gtc.12541.
   PubMed Web of Science ®Google Scholar
• Iwasa H, Sarkar A, Shimizu T, Sawada T, Hossain S, Xu X, Maruyama J, Arimoto-Matsuzaki K, Withanage K, Nakagawa K, Kurihara H, Kuroyanagi H, Hata Y. 2018. UNC119 is a binding partner of tumor suppressor Ras-association domain family 6 and induces apoptosis and cell cycle arrest by MDM2 and p53. Cancer Sci 109:2767–2780. https://doi.org/10.1111/cas.13706.
   PubMed Web of Science ®Google Scholar
• Yu DS, Zhao R, Hsu EL, Cayer J, Ye F, Guo Y, Shyr Y, Cortez D. 2010. Cyclin-dependent kinase 9-cyclin K functions in the replication stress response. EMBO Rep 11:876–882. https://doi.org/10.1038/embor.2010.153.
   PubMed Web of Science ®Google Scholar