Blocking β-catenin binding to the ZBP1 promoter represses ZBP1 expression, leading to increased proliferation and migration of metastatic breast-cancer cells

Journal of Cell Science

Volumn 122, Issue 11, 2009, Pages 1895-1905

  Gu, Wei ^a   Pan, Feng ^b   Singer, Robert H ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell proliferation; Metastasis; Promoter methylation; Wnt catenin signaling; ZBP1 repression

Indexed keywords

BETA CATENIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; ZIPCODE BINDING PROTEIN 1;

ARTICLE; BREAST CANCER; CANCER CELL; CELL CYCLE REGULATION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DEMETHYLATION; DOWN REGULATION; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE REPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN METHYLATION; PROTEIN RNA BINDING;

BETA CATENIN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DNA METHYLATION; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; MOLECULAR SEQUENCE DATA; NEOPLASM METASTASIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA INTERFERENCE; RNA, MESSENGER;

EID: 69449102426     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.045278     Document Type: Article

References (57)

1. Abe, T., Toyota, M., Suzuki, H., Murai, M., Akino, K., Ueno, M. Nojima, M., Yawata, A., Miyakawa, H., Suga, T. et al. (2005). Upregulation of BNIP3 by 5-aza-2′-deoxycytidine sensitizes pancreatic cancer cells to hypoxia-mediated cell death. J. Gastroenterol. 40, 504-510.
2. Bender, C. M., Pao, M. M. and Jones, P. A. (1998). Inhibition of DNA methylation by 5-aza-2′-deoxycytidine suppresses the growth of human tumor cell lines. Cancer Res. 58, 95-101.
3. Bernstein, P. L., Herrick, D. J., Prokipcak, R. D. and Ross, J. (1992). Control of c-myc mRNA half-fife in vitro by a protein capable of binding to a coding region stability determinant. Genes Dev. 6, 642-654.
4. Biliran, H., Jr, Wang, Y., Banerjee, S., Xu, H., Heng, H., Thakur, A., Bollig, A., Sarkar, F. H. and Liao, J. D. (2005). Overexpression of cyclin D1 promotes tumor cell growth and confers resistance to cisplatin-mediated apoptosis in an elastase-myc transgene-expressing pancreatic tumor cell line. Clin. Cancer Res. 11, 6075-6086.
5. Capodieci, P., Donovan, M, Buchinsky, H., Jeffers, Y., Cordon-Cardo, C., Gerald, W., Edelson, J, Shenoy, S. M. and Singer, R. H. (2005). Gene expression profiling in single cells within tissue. Nat. Methods 2, 663-665.
6. Clark, S. J., Harrison, J., Paul, C. L. and Frommer, M. (1994). High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22, 2990-2997.
7. Condeelis, J. and Singer, R. H. (2005). How and why does beta-actin mRNA target? Biol. Cell 97, 97-110.
8. Coniglio, S. J., Zavarella, S. and Symons, M. H. (2008). Pak1 and Pak2 mediate tumor cell invasion through distinct signaling mechanisms. Mol. Cell. Biol. 28, 4162-4172.
9. Cory, A. H., Owen, T. C., Barltrop, J. A. and Cory, J. G. (1991). Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun. 3, 207-212.
10. El-Osta, A. (2004). The rise and fail of genomic methylation in cancer. Leukemia 18, 233-237.
11. Farina, K. L., Huttelmaier, S., Musunuru, K., Darnell, R. and Singer, R. H. (2003). Two ZBP1 KH domains facilitate beta-actin mRNA localization, granule formation, and cytoskeletal attachment. J. Cell Biol. 160, 77-87.
12. Gavert, N. and Ben-Ze'ev, A. (2007). beta-Catenin signaling in biological control and cancer. J Cell Biochem. 102, 820-828.
13. Go, W., Wells, A. L., Pan, F. and Singer, R. H. (2008). Feedback regulation between ZBP1 and {beta}-catenin mRNAs in breast cancer cells. Mol. Cell. Biol. 28, 4963-4974.
14. Gumbiner, B. M. (2000). Regulation of cadherin adhesive activity. J. Cell Biol. 148, 399-404.
15. Harris, T. J. and Peifer, M. (2005). Decisions, decisions: beta-catenin chooses between adhesion and transcription. Trends Cell Biol. 15, 234-237.
16. Huttelmaier, S., Zenklusen, D., Lederer, M., Dictenberg, J., Lorenz, M., Meng, X., Bassell, G. J., Condeelis, J. and Singer, R. H. (2005). Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438, 512-515.
17. Ioannidis, P., Trangas, T., Dimitriadis, E., Samiotaki, M., Kyriazoglou, I., Tsiapalis, C. M., Kittas, C., Agnantis, N., Nielsen, F. C., Nielsen, J. et al. (2001). C-MYC and IGF-II mRNA-binding protein (CRD-BP/IMP-1) in benign and malignant mesenchymal tumors. Int. J. Cancer 94, 480-484.
18. Ioannidis, P., Mahaira, L., Papadopoulou, A., Teixeira, M. R., Heim, S., Andersen, J. A., Evangelou, E., Dafni U., Pandis, N. and Trangas, T. (2003a). 8q24 Copy number gains and expression of the c-myc mRNA stabilizing protein CRD-BP in primary breast carcinomas. Int. J. Cancer 104, 54-59.
19. Ioannidis, P., Mahaira, L., Papadopoulou, A., Teixeira, M. R., Heim, S., Andersen, J. A., Evangelou, E., Dafni, U., Pandis, N. and Trangas, T. (2003b). CRD-BP: a c-Myc mRNA stabilizing protein with an oncofetal pattern of expression. Anticancer Res. 23, 2179-2183.
20. Ioannidis, P., Mahaira, L. G., Perez, S. A., Gritzapis A. D., Sotiropoulou, P. A., Kavalakis, G. J., Antsaklis, A. I., Baxevanis, C. N. and Papamichail, M. (2005). CRD-BP/IMP1 expression characterizes cord blood CD34+ stem cells and affects c-myc and IGF-II expression in MCF-7 cancer cells. J. Biol. Chem. 230, 20086-20093.
21. Iyer, V. R., Horak C. E., Scafe, C. S., Botstein, D., Snyder, M. and Brown, P. O. (2001). Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409, 533-538.
22. Jones, P. A. and Taylor, S. M. (1980). Cellular differentiation, cytidine analogs and DNA methylation. Cell 20, 85-93.
23. Jones, P. A. and Takai, D. (2001). The role of DNA methylation in mammalian epigenetics. Science 293, 1068-1070.
24. Jones, P. A. and Baylin, S. B. (2002). The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3, 415-428.
25. Kislauskis, E. H. and Singer, R. H. (1992) Determinants of mRNA localization. Curr. Opin. Cell Biol. 4, 975-978.
26. Kislauskis, E. H., Zhu, X. and Singer, R. H. (1997). beta-Actin messenger RNA localization and protein synthesis augment cell motility. J. Cell Biol. 136, 1263-1270.
27. Kobel, M., Weidensdorfer, D, Reinke, C., Lederer, M., Schmitt, W. D., Zeng, K., Thomssen, C., Hauptmann, S. and Huttelmaier, S. (2007). Expression of the RNA-binding protein IMP1 correlates with poor prognosis in ovarian carcinoma. Oncogene 26, 7584-7589.
28. Lapidus, K., Wyckoff, J., Mouneimne, G., Lorenz, M., Soon, L., Condeelis, J. S. and Singer, R. H. (2007). ZBP1 enhances cell polarity and reduces chemotaxis. J. Cell Sci. 120, 3173-3178.
29. Leeds, P., Kren, B. T., Boylan, J. M., Betz, N. A., Steer, C. J., Gruppuso, P. A. and Ross, J. (1997). Developmental regulation of CRD-BP, an RNA-binding protein that stabilizes c-myc mRNA in vitro. Oncogene 14, 1279-1286.
30. Lelekakis, M., Moseley, J. M., Martin, T. J., Hards, D., Williams, E., Ho, P., Lowen, D., Javni, J., Miller, F. R., Slavin, J. et al. (1999). A novel orthotopic model of breast cancer metastasis to bone. Clin. Exp. Metastasis 17, 163-170.
31. Lemm, I. and Ross, J. (2002). Regulation of c-myc mRNA decay by translational pausing in a coding region instability determinant. Mol. Cell. Biol. 22, 3959-3969.
32. Liao, B., Patel, M., Hu, Y., Charles, S., Herrick, D. J. and Brewer, G. (2004). Targeted knockdown of the RNA-binding protein CRD-BP promotes cell proliferation via an insulin-like growth factor II-dependent pathway in human K562 leukemia cells. J. Biol. Chem. 279, 48716-48724.
33. Marone, R., Hess, D., Dankort, D., Muller, W. J., Hynes, N. E. and Badache, A. (2004). Memo mediates ErbB2-driven cell motility. Nat. Cell Biol. 6, 515-522.
34. Mingle, L. A., Okuhama, N. N., Shi, J., Singer, R. H., Condeelis, J. and Liu, G. (2005). Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J. Cell Sci. 118, 2425-2433.
35. Momparler, R. L. (2003). Cancer epigenetics. Oncogene 22, 6479-6483.
36. Moreau, P., Rousseau, P., Rouas-Freiss, N., Le Discorde, M, Dausset, J. and Carosella, E. D. (2002). HLA-G protein processing and transport to the cell surface. Cell Mol. Life Sci. 59, 1460-1466.
37. Nelson, W. J. and Nusse, R. (2004). Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487.
38. Nielsen, F. C., Nielsen, J. and Christiansen, J. (2001). A family of IGF-II mRNA binding proteins (IMP) involved in RNA trafficking. Scand. J. Clin. Lab. Invest. Suppl. 234, 93-99.
39. Nielsen, J., Christiansen, J., Lykke-Andersen, J., Johnsen, A. H., Wewer, U. M. and Nielsen, F. C. (1999). A family of insulin-like growth factor II mRNA-binding proteins represses translation in late development. Mol. Cell. Biol. 19, 1262-1270.
40. Noubissi, F. K., Elcheva, I., Bhatia, N., Shakoori, A., Ougolkov, A., Liu, J., Minamoto, T., Ross, J., Fuchs, S. Y. and Spiegelman, V. S. (2006). CRD-BP mediates stabilization of betaTrCP1 and c-myc mRNA in response to beta-catenin signalling. Nature 441, 898-901.
41. Oberman, F., Rand, K., Maizels, Y., Rubinstein, A. M. and Yisraeli, J. K. (2007). VICKZ proteins mediate cell migration via their RNA binding activity. RNA 13, 1558-1569.
42. Pan, F., Huttelmaier, S., Singer, R. H. and Gu, W. (2007). ZBP2 Facilitates Binding of ZBP1 to {beta}-Actin mRNA during Transcription. Mol. Cell. Biol. 27, 8340-8351.
43. Ross, A. F., Oleynikov, Y., Kislauskis, E. H., Taneja, K. L. and Singer, R. H. (1997). Characterization of a beta-actin mRNA zipcode-binding protein. Mol. Cell. Biol. 17, 2158-2165.
44. Ross, J., Lemm, I. and Berberet, B. (2001). Overexpression of an mRNA-binding protein in human colorectal cancer. Oncogene 20, 6544-6550.
45. Shestakova, E. A., Singer, R. H. and Condeelis, J. (2001). The physiological significance of beta -actin mRNA localization in determining cell polarity and directional motility. Proc. Natl. Acad Sci. USA 98, 7045-7050.
46. Stohr, N., Lederer, M., Reinke, C., Meyer, S., Hatzfeld, M, Singer, R. H. and Huttelmaier, S. (2006). ZBP1 regulates mRNA stability during cellular stress. J. Cell Biol. 175, 527-534.
47. Stove, V., Van de Walle, I., Naessens, E., Coene, E., Stove, C., Plum, J. and Verhasselt, B. (2005). Human immunodeficiency virus Nef induces rapid internalization of the T-cell coreceptor CD8alphabeta. J. Virol. 79, 11422-11433.
48. Tessier, C. R., Doyle, G. A., Clark, B. A., Pitot, H. C. and Ross, J. (2004). Mammary tumor induction in transgenic mice expressing an RNA-binding protein. Cancer Res. 64, 209-214.
49. Tsou, J. A., Hagen, J. A., Carpenter, C. L. and Laird-Offringa, I. A. (2002). DNA methylation analysis: a powerful new tool for lung cancer diagnosis. Oncogene 21, 5450-5461.
50. Vega, S., Morales, A. V., Ocana, O. H., Valdes, F., Fabregat, I. and Nieto, M. A. (2004). Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18, 1131-1143.
51. Vikesaa, J., Hansen, T. V., Jonson, L., Borup, R., Wewer, U. M., Christiansen, J. and Nielsen, F. C. (2006). RNA-binding IMP's promote cell adhesion and invadopodia formation. EMBO J. 25, 1456-1468.
52. Wang, W., Wyckoff, J. B., Frohlich, V. C., Oleynikov, Y., Huttelmaier, S., Zavadil, J., Cermak, L., Bottinger, E. P., Singer, R. H., White, J. G. et al. (2002). Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res. 62, 6278-6288.
53. Wang, W., Goswami, S., Lapidus, K., Wells, A. L., Wyckoff, J. B., Sahai, E., Singer, R. H., Segall, J. E. and Condeelis, J. S. (2004). Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res. 64, 8585-8594.
54. Yisraeli, J. K. (2005). VICKZ proteins: a multi-talented family of regulatory RNA-binding proteins. Biol. Cell 97, 87-96.
55. Yu, Q., Geng, Y. and Sicinski, P. (2001). Specific protection against breast cancers by cyclin D1 ablation. Nature 411, 1017-1021.
56. Zajchowski, D. A., Bartholdi, M. F., Gong, Y., Webster, L, Liu, H. L. Munishkin, A, Beauheim, C., Harvey, S., Ethier, S. P. and Johnson, P. H. (2001). Identification of gene expression profiles that predict the aggressive behavior of breast cancer cells. Cancer Res. 61, 5168-5178.
57. Zhu, W. G., Hileman, T., Ke, Y., Wang, P., Lu, S., Duan, W., Dai, Z., Tong, T., Villalona-Calero, M. A., Plass, C. et al. (2004). 5-aza-2′-deoxycytidine activates the p53/p21Waf1/Cip1 pathway to inhibit cell proliferation. J. Biol. Chem. 279, 15161-15166.