The DNA Damage Transducer RNF8 Facilitates Cancer Chemoresistance and Progression through Twist Activation

Molecular Cell

Volumn 63, Issue 6, 2016, Pages 1021-1033

  Lee, Hong Jen ^a,b   Li, Chien Feng ^c,d   Ruan, Diane ^a,b   Powers, Scott ^a   Thompson, Patricia A ^a,b   Frohman, Michael A ^a   Chan, Chia Hsin ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b Stony Brook Medicine   (United States)

^c NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^d Chi Mei Foundational Medical Center   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DAMAGE TRANSDUCER RNF8; LIGASE; PROTEIN; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; DNA BINDING PROTEIN; LUCIFERASE; LYSINE; NUCLEAR PROTEIN; RNF8 PROTEIN, HUMAN; SMALL INTERFERING RNA; TWIST RELATED PROTEIN 1; TWIST1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; CELL INVASION; CELL SELF-RENEWAL; CONTROLLED STUDY; FEMALE; GENE ACTIVATION; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; MCF 7 CELL LINE; MDA MB 231 CELL LINE; METASTASIS; METASTASIS INHIBITION; MIGRATION; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN LOCALIZATION; TISSUE SECTION; TUMOR PROMOTION; UBIQUITINATION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CANCER TRANSPLANTATION; DISEASE COURSE; DNA DAMAGE; DRUG EFFECTS; DRUG RESISTANCE; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENETICS; MCF-7 CELL LINE; METABOLISM; MORTALITY; NUDE MOUSE; PATHOLOGY; REPORTER GENE; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE PROGRESSION; DNA DAMAGE; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; HUMANS; LUCIFERASES; LYSINE; MCF-7 CELLS; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; NUCLEAR PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TWIST-RELATED PROTEIN 1; UBIQUITINATION;

EID: 84991701993     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.08.009     Document Type: Article

References (58)

1. Andre, F., Zielinski, C.C., Optimal strategies for the treatment of metastatic triple-negative breast cancer with currently approved agents. Ann. Oncol., 23(Suppl 6), 2012 vi46–51.
2. Bennett, E.J., Harper, J.W., DNA damage: ubiquitin marks the spot. Nat. Struct. Mol. Biol. 15 (2008), 20–22.
3. Berndsen, C.E., Wolberger, C., New insights into ubiquitin E3 ligase mechanism. Nat. Struct. Mol. Biol. 21 (2014), 301–307.
4. Biggar, K.K., Li, S.S., Non-histone protein methylation as a regulator of cellular signalling and function. Nat. Rev. Mol. Cell Biol. 16 (2015), 5–17.
5. Carracedo, A., Weiss, D., Leliaert, A.K., Bhasin, M., de Boer, V.C., Laurent, G., Adams, A.C., Sundvall, M., Song, S.J., Ito, K., et al. A metabolic prosurvival role for PML in breast cancer. J. Clin. Invest. 122 (2012), 3088–3100.
6. Cerami, E., Gao, J., Dogrusoz, U., Gross, B.E., Sumer, S.O., Aksoy, B.A., Jacobsen, A., Byrne, C.J., Heuer, M.L., Larsson, E., et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2 (2012), 401–404.
7. Chan, C.H., Li, C.F., Yang, W.L., Gao, Y., Lee, S.W., Feng, Z., Huang, H.Y., Tsai, K.K., Flores, L.G., Shao, Y., et al. The Skp2-SCF E3 ligase regulates Akt ubiquitination, glycolysis, herceptin sensitivity, and tumorigenesis. Cell 149 (2012), 1098–1111.
8. Chan, C.H., Morrow, J.K., Li, C.F., Gao, Y., Jin, G., Moten, A., Stagg, L.J., Ladbury, J.E., Cai, Z., Xu, D., et al. Pharmacological inactivation of Skp2 SCF ubiquitin ligase restricts cancer stem cell traits and cancer progression. Cell 154 (2013), 556–568.
9. Chan, C.H., Jo, U., Kohrman, A., Rezaeian, A.H., Chou, P.C., Logothetis, C., Lin, H.K., Posttranslational regulation of Akt in human cancer. Cell Biosci., 4, 2014, 59.
10. Ciriello, G., Gatza, M.L., Beck, A.H., Wilkerson, M.D., Rhie, S.K., Pastore, A., Zhang, H., McLellan, M., Yau, C., Kandoth, C., et al., TCGA Research Network. Comprehensive Molecular Portraits of Invasive Lobular Breast Cancer. Cell 163 (2015), 506–519.
11. Cohen, P., Tcherpakov, M., Will the ubiquitin system furnish as many drug targets as protein kinases?. Cell 143 (2010), 686–693.
12. Cojoc, M., Mäbert, K., Muders, M.H., Dubrovska, A., A role for cancer stem cells in therapy resistance: cellular and molecular mechanisms. Semin. Cancer Biol. 31 (2015), 16–27.
13. Dent, R., Trudeau, M., Pritchard, K.I., Hanna, W.M., Kahn, H.K., Sawka, C.A., Lickley, L.A., Rawlinson, E., Sun, P., Narod, S.A., Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 13 (2007), 4429–4434.
14. Dontu, G., Abdallah, W.M., Foley, J.M., Jackson, K.W., Clarke, M.F., Kawamura, M.J., Wicha, M.S., In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17 (2003), 1253–1270.
15. Fischer, K.R., Durrans, A., Lee, S., Sheng, J., Li, F., Wong, S.T., Choi, H., El Rayes, T., Ryu, S., Troeger, J., et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature 527 (2015), 472–476.
16. Geetha, T., Kenchappa, R.S., Wooten, M.W., Carter, B.D., TRAF6-mediated ubiquitination regulates nuclear translocation of NRIF, the p75 receptor interactor. EMBO J. 24 (2005), 3859–3868.
17. Grzegrzolka, J., Biala, M., Wojtyra, P., Kobierzycki, C., Olbromski, M., Gomulkiewicz, A., Piotrowska, A., Rys, J., Podhorska-Okolow, M., Dziegiel, P., Expression of EMT Markers SLUG and TWIST in Breast Cancer. Anticancer Res. 35 (2015), 3961–3968.
18. Haupt, S., Buckley, D., Pang, J.M., Panimaya, J., Paul, P.J., Gamell, C., Takano, E.A., Lee, Y.Y., Hiddingh, S., Rogers, T.M., et al. Targeting Mdmx to treat breast cancers with wild-type p53. Cell Death Dis., 6, 2015, e1821.
19. Hoeller, D., Dikic, I., Targeting the ubiquitin system in cancer therapy. Nature 458 (2009), 438–444.
20. Holohan, C., Van Schaeybroeck, S., Longley, D.B., Johnston, P.G., Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer 13 (2013), 714–726.
21. Hong, J., Zhou, J., Fu, J., He, T., Qin, J., Wang, L., Liao, L., Xu, J., Phosphorylation of serine 68 of Twist1 by MAPKs stabilizes Twist1 protein and promotes breast cancer cell invasiveness. Cancer Res. 71 (2011), 3980–3990.
22. Horiuchi, D., Kusdra, L., Huskey, N.E., Chandriani, S., Lenburg, M.E., Gonzalez-Angulo, A.M., Creasman, K.J., Bazarov, A.V., Smyth, J.W., Davis, S.E., et al. MYC pathway activation in triple-negative breast cancer is synthetic lethal with CDK inhibition. J. Exp. Med. 209 (2012), 679–696.
23. Huen, M.S., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M.B., Chen, J., RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131 (2007), 901–914.
24. Kalluri, R., Weinberg, R.A., The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119 (2009), 1420–1428.
25. Khan, M.A., Chen, H.C., Zhang, D., Fu, J., Twist: a molecular target in cancer therapeutics. Tumour Biol. 34 (2013), 2497–2506.
26. Kim, S.J., Nakayama, S., Miyoshi, Y., Taguchi, T., Tamaki, Y., Matsushima, T., Torikoshi, Y., Tanaka, S., Yoshida, T., Ishihara, H., et al. Determination of the specific activity of CDK1 and CDK2 as a novel prognostic indicator for early breast cancer. Ann Oncol. 19 (2008), 68–72.
27. Kreike, B., van Kouwenhove, M., Horlings, H., Weigelt, B., Peterse, H., Bartelink, H., van de Vijver, M.J., Gene expression profiling and histopathological characterization of triple-negative/basal-like breast carcinomas. Breast Cancer Res., 9, 2007, R65.
28. Lander, R., Nordin, K., LaBonne, C., The F-box protein Ppa is a common regulator of core EMT factors Twist, Snail, Slug, and Sip1. J. Cell Biol. 194 (2011), 17–25.
29. Lander, R., Nasr, T., Ochoa, S.D., Nordin, K., Prasad, M.S., Labonne, C., Interactions between Twist and other core epithelial-mesenchymal transition factors are controlled by GSK3-mediated phosphorylation. Nat. Commun., 4, 2013, 1542.
30. Lawson, D.A., Bhakta, N.R., Kessenbrock, K., Prummel, K.D., Yu, Y., Takai, K., Zhou, A., Eyob, H., Balakrishnan, S., Wang, C.Y., et al. Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells. Nature 526 (2015), 131–135.
31. Lehmann, B.D., Bauer, J.A., Chen, X., Sanders, M.E., Chakravarthy, A.B., Shyr, Y., Pietenpol, J.A., Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Invest. 121 (2011), 2750–2767.
32. Li, C.W., Xia, W., Lim, S.O., Hsu, J.L., Huo, L., Wu, Y., Li, L.Y., Lai, C.C., Chang, S.S., Hsu, Y.H., et al. AKT1 inhibits epithelial-to-mesenchymal transition in breast cancer through phosphorylation-dependent Twist1 degradation. Cancer Res. 76 (2016), 1451–1462.
33. Lok, G.T., Sy, S.M., Dong, S.S., Ching, Y.P., Tsao, S.W., Thomson, T.M., Huen, M.S., Differential regulation of RNF8-mediated Lys48- and Lys63-based poly-ubiquitylation. Nucleic Acids Res. 40 (2012), 196–205.
34. Mani, S.A., Guo, W., Liao, M.J., Eaton, E.N., Ayyanan, A., Zhou, A.Y., Brooks, M., Reinhard, F., Zhang, C.C., Shipitsin, M., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133 (2008), 704–715.
35. Mattiroli, F., Sixma, T.K., Lysine-targeting specificity in ubiquitin and ubiquitin-like modification pathways. Nat. Struct. Mol. Biol. 21 (2014), 308–316.
36. Morel, A.P., Hinkal, G.W., Thomas, C., Fauvet, F., Courtois-Cox, S., Wierinckx, A., Devouassoux-Shisheboran, M., Treilleux, I., Tissier, A., Gras, B., et al. EMT inducers catalyze malignant transformation of mammary epithelial cells and drive tumorigenesis towards claudin-low tumors in transgenic mice. PLoS Genet., 8, 2012, e1002723.
37. Orthwein, A., Fradet-Turcotte, A., Noordermeer, S.M., Canny, M.D., Brun, C.M., Strecker, J., Escribano-Diaz, C., Durocher, D., Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science 344 (2014), 189–193.
38. Pan, D., Zhu, Y., Zhou, Z., Wang, T., You, H., Jiang, C., Lin, X., The CBM complex underwrites NF-κB activation to promote HER2-associated tumor malignancy. Mol. Cancer Res. 14 (2016), 93–102.
39. Perou, C.M., Molecular stratification of triple-negative breast cancers. Oncologist 15:Suppl 5 (2010), 39–48.
40. Phu, L., Izrael-Tomasevic, A., Matsumoto, M.L., Bustos, D., Dynek, J.N., Fedorova, A.V., Bakalarski, C.E., Arnott, D., Deshayes, K., Dixit, V.M., et al. Improved quantitative mass spectrometry methods for characterizing complex ubiquitin signals. Mol Cell Proteomics, 10, 2011 M110.003756.
41. Puisieux, A., Brabletz, T., Caramel, J., Oncogenic roles of EMT-inducing transcription factors. Nat. Cell Biol. 16 (2014), 488–494.
42. Rai, R., Li, J.M., Zheng, H., Lok, G.T., Deng, Y., Huen, M.S., Chen, J., Jin, J., Chang, S., The E3 ubiquitin ligase Rnf8 stabilizes Tpp1 to promote telomere end protection. Nat. Struct. Mol. Biol. 18 (2011), 1400–1407.
43. Sampieri, K., Fodde, R., Cancer stem cells and metastasis. Semin. Cancer Biol. 22 (2012), 187–193.
44. Shi, J., Wang, Y., Zeng, L., Wu, Y., Deng, J., Zhang, Q., Lin, Y., Li, J., Kang, T., Tao, M., et al. Disrupting the interaction of BRD4 with diacetylated Twist suppresses tumorigenesis in basal-like breast cancer. Cancer Cell 25 (2014), 210–225.
45. Singh, A., Settleman, J., EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 29 (2010), 4741–4751.
46. Skaar, J.R., Pagan, J.K., Pagano, M., SCF ubiquitin ligase-targeted therapies. Nat. Rev. Drug Discov. 13 (2014), 889–903.
47. Surade, S., Blundell, T.L., Structural biology and drug discovery of difficult targets: the limits of ligandability. Chem. Biol. 19 (2012), 42–50.
48. Thiery, J.P., Acloque, H., Huang, R.Y., Nieto, M.A., Epithelial-mesenchymal transitions in development and disease. Cell 139 (2009), 871–890.
49. Thorslund, T., Ripplinger, A., Hoffmann, S., Wild, T., Uckelmann, M., Villumsen, B., Narita, T., Sixma, T.K., Choudhary, C., Bekker-Jensen, S., Mailand, N., Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage. Nature 527 (2015), 389–393.
50. Vesuna, F., Lisok, A., Kimble, B., Domek, J., Kato, Y., van der Groep, P., Artemov, D., Kowalski, J., Carraway, H., van Diest, P., Raman, V., Twist contributes to hormone resistance in breast cancer by downregulating estrogen receptor-α. Oncogene 31 (2012), 3223–3234.
51. Wang, Z., Liu, P., Inuzuka, H., Wei, W., Roles of F-box proteins in cancer. Nat. Rev. Cancer 14 (2014), 233–247.
52. Xue, J., Lv, D.D., Jiao, S., Zhao, W., Li, X., Sun, H., Yan, B., Fan, L., Hu, R.G., Fang, J., pVHL mediates K63-linked ubiquitination of nCLU. PLoS ONE, 7, 2012, e35848.
53. Yang, J., Mani, S.A., Donaher, J.L., Ramaswamy, S., Itzykson, R.A., Come, C., Savagner, P., Gitelman, I., Richardson, A., Weinberg, R.A., Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117 (2004), 927–939.
54. Yang, M.H., Wu, M.Z., Chiou, S.H., Chen, P.M., Chang, S.Y., Liu, C.J., Teng, S.C., Wu, K.J., Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol. 10 (2008), 295–305.
55. Yang, W.H., Lan, H.Y., Huang, C.H., Tai, S.K., Tzeng, C.H., Kao, S.Y., Wu, K.J., Hung, M.C., Yang, M.H., RAC1 activation mediates Twist1-induced cancer cell migration. Nat Cell Biol. 14 (2012), 366–374.
56. Ye, X., Weinberg, R.A., Epithelial-Mesenchymal Plasticity: A Central Regulator of Cancer Progression. Trends Cell Biol. 25 (2015), 675–686.
57. Zheng, H., Kang, Y., Multilayer control of the EMT master regulators. Oncogene 33 (2014), 1755–1763.
58. Zhong, J., Ogura, K., Wang, Z., Inuzuka, H., Degradation of the transcription factor Twist, an oncoprotein that promotes cancer metastasis. Discov. Med. 15 (2013), 7–15.