ASPP2 controls epithelial plasticity and inhibits metastasis through β 2-catenin-dependent regulation of ZEB1

Nature Cell Biology

Volumn 16, Issue 11, 2014, Pages 1092-1104

  Wang, Yihua ^a   Bu, Fangfang ^b,c   Royer, Christophe ^a,d   Serres, Sébastien ^d   Larkin, James R ^d   Soto, Manuel Sarmiento ^d   Sibson, Nicola R ^d   Salter, Victoria ^a   Fritzsche, Florian ^a,e   Turnquist, Casmir ^a   Koch, Sofia ^a   Zak, Jaroslav ^a   Zhong, Shan ^a   Wu, Guobin ^f   Liang, Anmin ^f   Olofsen, Patricia A ^a   Moch, Holger ^e   Hancock, David C ^g   Downward, Julian ^g   Goldin, Robert D ^h   Zhao, Jian ^b,c   Tong, Xin ^b,c   Guo, Yajun ^b,c   Lu, Xin ^a   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c CHINESE PLA GENERAL HOSPITAL   (China)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^f Guangxi Cancer Institute   (China)

^g IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^h ST MARY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; PROTEIN ASPP2; PROTEIN P53; PROTEINASE ACTIVATED RECEPTOR 3; RAS PROTEIN; TRANSCRIPTION FACTOR ZEB1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; WNT PROTEIN; APOPTOSIS REGULATORY PROTEIN; CTNNB1 PROTEIN, HUMAN; CTNNB1 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; KRUPPEL LIKE FACTOR; TP53BP2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRP53BP2 PROTEIN, MOUSE; ZEB1 PROTEIN, HUMAN; ZEB1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER SURVIVAL; CELL TRANSFORMATION; COMPLEX FORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIAL PLASTICITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; MESENCHYMAL TO EPITHELIAL TRANSITION; METASTASIS INHIBITION; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; ANIMAL; GENE EXPRESSION REGULATION; METABOLISM; METASTASIS; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE; WNT SIGNALING PATHWAY;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BETA CATENIN; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; NEOPLASM METASTASIS; PHOSPHORYLATION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; WNT SIGNALING PATHWAY;

EID: 84908479373     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3050     Document Type: Article

References (67)

1. Thiery, J. P., Acloque, H., Huang, R. Y. & Nieto, M. A. Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890 (2009).
2. Thiery, J. P. & Sleeman, J. P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142 (2006).
3. Sleeman, J. P. & Thiery, J. P. SnapShot: the epithelial-mesenchymal transition. Cell 145, 162-162e1 (2011).
4. Wang, Y. et al. Critical role for transcriptional repressor Snail2 in transformation by oncogenic RAS in colorectal carcinoma cells. Oncogene 29, 4658-4670 (2010).
5. Carew, R. M., Wang, B. & Kantharidis, P. The role of EMT in renal fibrosis. Cell Tissue Res. 347, 103-116 (2012).
6. Auersperg, N. et al. E-cadherin induces mesenchymal-to-epithelial transition in human ovarian surface epithelium. Proc. Natl Acad. Sci. USA 96, 6249-6254 (1999).
7. Law, M. E. et al. Glucocorticoids and histone deacetylase inhibitors cooperate to block the invasiveness of basal-like breast cancer cells through novel mechanisms. Oncogene 32, 1316-1329 (2013).
8. Aigner, K. et al. The transcription factor ZEB1 (6EF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 26, 6979-6988 (2007).
9. Sottocornola, R. et al. ASPP2 binds Par-3 and controls the polarity and proliferation of neural progenitors during CNS development. Dev. Cell 19, 126-137 (2010).
10. Cong, W. et al. ASPP2 regulates epithelial cell polarity through the PAR complex. Curr. Biol. 20, 1408-1414 (2010).
11. Vives, V. et al. ASPP2 is a haploinsufficient tumor suppressor that cooperates with p53 to suppress tumor growth. Genes Dev. 20, 1262-1267 (2006).
12. Bergamaschi, D. et al. ASPP1 and ASPP2: common activators of p53 family members. Mol. Cell. Biol. 24, 1341-1350 (2004).
13. Samuels-Lev, Y. et al. ASPP proteins specifically stimulate the apoptotic function of p53. Mol. Cell 8, 781-794 (2001).
14. Trigiante, G. & Lu, X. ASPP [corrected] and cancer. Nat. Rev. Cancer 6, 217-226 (2006).
15. Bergamaschi, D. et al. iASPP oncoprotein is a key inhibitor of p53 conserved from worm to human. Nat. Genet. 33, 162-167 (2003).
16. Zhao, J. et al. Epigenetic silence of ankyrin-repeat-containing, SH3-domain-containing, and proline-rich-region-containing protein 1 (ASPP1) and ASPP2 genes promotes tumor growth in hepatitis B virus-positive hepatocellular carcinoma. Hepatology 51, 142-153 (2010).
17. Sarraf, S. A. & Stancheva, I. Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol. Cell 15, 595-605 (2004).
18. Liu, Z. J. et al. Downregulated mRNA expression of ASPP and the hypermethylation of the 5'-untranslated region in cancer cell lines retaining wild-type p53. FEBS Lett. 579, 1587-1590 (2005).
19. Liu, W. K., Jiang, X. Y., Ren, J. K. & Zhang, Z. X. Expression pattern of the ASPP family members in endometrial endometrioid adenocarcinoma. Onkologie 33, 500-503 (2010).
20. Sgroi, D. C. et al. In vivo gene expression profile analysis of human breast cancer progression. Cancer Res. 59, 5656-5661 (1999).
21. Tordella, L. et al. ASPP2 suppresses squamous cell carcinoma via RelA/p65-mediated repression of p63. Proc. Natl Acad. Sci. USA 110, 17969-17974 (2013).
22. Lossos, I. S., Natkunam, Y., Levy, R. & Lopez, C. D. Apoptosis stimulating protein of p53 (ASPP2) expression differs in diffuse large B-cell and follicular center lymphoma: correlation with clinical outcome. Leuk. Lymphoma 43, 2309-2317 (2002).
23. Vandewalle, C, Van Roy, F. & Berx, G. The role of the ZEB family of transcription factors in development and disease. Cell. Mol. Life Sci. 66, 773-787 (2009).
24. Dressler, G. R. The cellular basis of kidney development. Annu. Rev. Cell Dev. Biol. 22, 509-529 (2006).
25. Sanchez-Tillo, E. et al. ß-catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness. Proc. Natl Acad. Sci. USA 108, 19204-19209 (2011).
26. Santner, S. J. et al. Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells. Breast Cancer Res. Treat. 65, 101-110 (2001).
27. Tang, B. et al. TGF-ß switches from tumor suppressor to prometastatic factor in a model of breast cancer progression. J. Clin. Invest. 112, 1116-1124 (2003).
28. Stadler, S. C. & Allis, C. D. Linking epithelial-to-mesenchymal-transition and epigenetic modifications. Semin. Cancer Biol. 22, 404-410 (2012).
29. Gorina, S. & Pavletich, N. P. Structure of the p53 tumor suppressor bound to the ankyrin and SH3 domains of 53BP2. Science 274, 1001-1005 (1996).
30. Shirasawa, S., Furuse, M., Yokoyama, N. & Sasazuki, T. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 260, 85-88 (1993).
31. Dajee, M., Tarutani, M., Deng, H., Cai, T. & Khavari, P. A. Epidermal Ras blockade demonstrates spatially localized Ras promotion of proliferation and inhibition of differentiation. Oncogene 21, 1527-1538 (2002).
32. Molina-Arcas, M., Hancock, D. C., Sheridan, C., Kumar, M. S. & Downward, J. Coordinate direct input of both KRAS and IGF1 receptor to activation of PI3 kinase in KRAS-mutant lung cancer. Cancer Discov. 3, 548-563 (2013).
33. Kim, T. et al. p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J. Exp. Med. 208, 875-883 (2011).
34. Zeller, E., Hammer, K., Kirschnick, M. & Braeuning, A. Mechanisms of RAS/β-catenin interactions. Arch. Toxicol. 87, 611-632 (2013).
35. Wang, Z. et al. N terminus of ASPP2 binds to Ras and enhances Ras/Raf/MEK/ERK activation to promote oncogene-induced senescence. Proc. Natl Acad. Sci. USA 110, 312-317 (2013).
36. Wang, Y. et al. ASPP1 and ASPP2 bind active RAS, potentiate RAS signalling and enhance p53 activity in cancer cells. Cell Death Differ. 20, 525-534 (2013).
37. Lee, M. H., Koria, P., Qu, J. & Andreadis, S. T. JNK phosphorylates β-catenin and regulates adherens junctions. FASEB J. 23, 3874-3883 (2009).
38. Maher, M. T., Mo, R., Flozak, A. S., Peled, O. N. & Gottardi, C. J. β-catenin phosphorylated at serine 45 is spatially uncoupled from β-catenin phosphorylated in the GSK3 domain: implications for signaling. PLoS ONE 5, e10184 (2010).
39. Sadot, E. et al. Regulation of S33/S37 phosphorylated β-catenin in normal and transformed cells. J. Cell Sci. 115, 2771-2780 (2002).
40. Faux, M. C., Coates, J. L., Kershaw, N. J., Layton, M. J. & Burgess, A. W. Independent interactions of phosphorylated β-catenin with E-cadherin at cell-cell contacts and APC at cell protrusions. PLoS ONE 5, e14127 (2010).
41. Moon, R. T., Kohn, A. D., De Ferrari, G. V. & Kaykas, A. WNT and β-catenin signalling: diseases and therapies. Nat. Rev. Genet. 5, 691-701 (2004).
42. Debnath, J. & Brugge, J. S. Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 5, 675-688 (2005).
43. Yang, J. et al. Molecular cytogenetic characteristics of the human hepatocellular carcinoma cell line HCCLM3 with high metastatic potential: comparative genomic hybridization and multiplex fluorescence in situ hybridization. Cancer Genet. Cytogenet. 158, 180-183 (2005).
44. Tsai, J. H., Donaher, J. L., Murphy, D. A., Chau, S. & Yang, J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 22, 725-736 (2012).
45. Ocana, O. H. et al. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 22, 709-724 (2012).
46. Yang, J. et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939 (2004).
47. Serres, S. et al. Molecular MRI enables early and sensitive detection of brain metastases. Proc. Natl Acad. Sci. USA 109, 6674-6679 (2012).
48. Carbonell, W. S., Ansorge, O., Sibson, N. & Muschel, R. The vascular basement membrane as "soil" in brain metastasis. PLoS ONE 4, e5857 (2009).
49. Chao, Y. L., Shepard, C. R. & Wells, A. Breast carcinoma cells re-express E-cadherin during mesenchymal to epithelial reverting transition. Mol. Cancer 9, 179 (2010).
50. Kim, N. G., Koh, E., Chen, X. & Gumbiner, B. M. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc. Natl Acad. Sci. USA 108, 11930-11935 (2011).
51. Llanos, S. et al. Inhibitory member of the apoptosis-stimulating proteins of the p53 family (iASPP) interacts with protein phosphatase 1 via a noncanonical binding motif. J. Biol. Chem. 286, 43039-43044 (2011).
52. Liu, C. Y. et al. PP1 cooperates with ASPP2 to dephosphorylate and activate TAZ. J. Biol. Chem. 286, 5558-5566 (2011).
53. Bertocchi, C., Vaman Rao, M. & Zaidel-Bar, R. Regulation of adherens junction dynamics by phosphorylation switches. J. Signal Transduction 2012, 125295 (2012).
54. McCaffrey, L. M., Montalbano, J., Mihai, C. & Macara, I. G. Loss of the Par3 polarity protein promotes breast tumorigenesis and metastasis. Cancer Cell 22, 601-614 (2012).
55. Xue, B., Krishnamurthy, K., Allred, D. C. & Muthuswamy, S. K. Loss of Par3 promotes breast cancer metastasis by compromising cell-cell cohesion. Nat. Cell Biol. 15, 189-200 (2013).
56. Wang, X. D. et al. SUMO-modified nuclear cyclin D1 bypasses Ras-induced senescence. Cell Death Differ. 18, 304-314 (2011).
57. Wang, Y. et al. Autophagic activity dictates the cellular response to oncogenic RAS. Proc. Natl Acad. Sci. USA 109, 13325-13330 (2012).
58. Debnath, J., Muthuswamy, S. K. & Brugge, J. S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268 (2003).
59. Vooijs, M., Jonkers, J. & Berns, A. A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep. 2, 292-297 (2001).
60. Carretero, J. et al. Integrative genomic and proteomic analyses identify targets for Lkb1-deficient metastatic lung tumors. Cancer Cell 17, 547-559 (2010).
61. Notari, M. et al. Inhibitor of apoptosis-stimulating protein of p53 (iASPP) prevents senescence and is required for epithelial stratification. Proc. Natl Acad. Sci. USA 108, 16645-16650 (2011).
62. McAteer, M. A. et al. In vivo magnetic resonance imaging of acute brain inflammation using microparticles of iron oxide. Nat. Med. 13, 1253-1258 (2007).
63. Liang, B. et al. Myeloid differentiation factor 88 promotes growth and metastasis of human hepatocellular carcinoma. Clin. Cancer Res. 19, 2905-2916 (2013).
64. Urakami, S. et al. Epigenetic inactivation of Wnt inhibitory factor-1 plays an important role in bladder cancer through aberrant canonical Wnt/β-catenin signaling pathway. Clin. Cancer Res. 12, 383-391 (2006).
65. Montserrat, N. et al. Repression of E-cadherin by SNAIL, ZEB1, and TWIST in invasive ductal carcinomas of the breast: a cooperative effort? Hum. Pathol. 42, 103-110 (2011).
66. Rubin, M. A. et al. E-cadherin expression in prostate cancer: a broad survey using high-density tissue microarray technology. Hum. Pathol. 32, 690-697 (2001).
67. Theurillat, J. P. et al. NY-ESO-1 protein expression in primary breast carcinoma and metastases: correlation with CD8+ T-cell and CD79a+ plasmacytic/B-cell infiltration. Int. J. Cancer 120, 2411-2417 (2007).