MicroRNA-141 and microRNA-146b-5p inhibit the prometastatic mesenchymal characteristics through the RNA-binding protein AUF1 targeting the transcription factor ZEB1 and the protein kinase AKT

Journal of Biological Chemistry

Volumn 289, Issue 45, 2014, Pages 31433-31447

  Al Khalaf, Huda H ^a,b   Aboussekhra, Abdelilah ^a  

^a KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^b KING ABDULAZIZ CITY FOR SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; CELL CULTURE; DIAGNOSIS; ENZYMES; GENE THERAPY; GLYCOPROTEINS; PROTEINS; TRANSCRIPTION; TUMORS;

INVERSE CORRELATION; MRNA-BINDING PROTEIN; ONCOGENIC POTENTIAL; OSTEOSARCOMA CELLS; POST-TRANSCRIPTIONAL; RNA-BINDING PROTEIN; THERAPEUTIC INTERVENTION; UNTRANSLATED REGIONS;

RNA;

CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2A; EPITHELIAL CELL ADHESION MOLECULE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; MICRORNA; MICRORNA 141; MICRORNA 146B; NERVE CELL ADHESION MOLECULE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN KINASE B; PROTEIN P16; PROTEIN P21; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR TWIST2; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; 3' UNTRANSLATED REGION; HNRNP D0; HOMEODOMAIN PROTEIN; MIRN141 MICRORNA, HUMAN; MIRN146 MICRORNA, HUMAN; PROTEIN BINDING; TRANSCRIPTION FACTOR; ZEB1 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; AUF1 GENE; BINDING SITE; CANCER INHIBITION; CANCER PROGNOSIS; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE TARGETING; HUMAN; METASTASIS INHIBITION; MIGRATION INHIBITION; MOLECULAR DYNAMICS; OSTEOSARCOMA CELL LINE; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN RNA BINDING; PROTEIN STABILITY; RNA STABILITY; SEQUENCE ALIGNMENT; TURNOVER TIME; UPREGULATION; CHEMISTRY; CYTOLOGY; MESODERM; METABOLISM; METASTASIS; MOLECULAR GENETICS; NEOPLASM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROGNOSIS; SEQUENCE HOMOLOGY;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; CELL PROLIFERATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN D; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; MICRORNAS; MOLECULAR SEQUENCE DATA; NEOPLASM METASTASIS; NEOPLASMS; PROGNOSIS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSCRIPTION FACTORS;

EID: 84909953901     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.593004     Document Type: Article

References (49)

1. Ciafrè, S. A., and Galardi, S. (2013) microRNAs and RNA-binding proteins: a complex network of interactions and reciprocal regulations in cancer. RNA Biol. 10, 935-942
2. Kim, H. H., Kuwano, Y., Srikantan, S., Lee, E. K., Martindale, J. L., and Gorospe, M. (2009) HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 23, 1743-1748
3. Tominaga, K., Srikantan, S., Lee, E. K., Subaran, S. S., Martindale, J. L., Abdelmohsen, K., and Gorospe, M. (2011) Competitive regulation of nucleolin expression by HuR and miR-494. Mol. Cell Biol. 31, 4219-4231
4. Wagner, B. J., DeMaria, C. T., Sun, Y., Wilson, G. M., and Brewer, G. (1998) Structure and genomic organization of the human AUF1 gene: alternative pre-mRNA splicing generates four protein isoforms. Genomics 48, 195-202
5. Kajita, Y., Nakayama, J., Aizawa, M., and Ishikawa, F. (1995) The UUAG-specific RNA binding protein, heterogeneous nuclear ribonucleoprotein D0: common modular structure and binding properties of the 2xRBD-Gly family. J. Biol. Chem. 270, 22167-22175
6. White, E. J., Brewer, G., and Wilson, G. M. (2013) Post-transcriptional control of gene expression by AUF1: mechanisms, physiological targets, and regulation. Biochim. Biophys. Acta 1829, 680-688
7. Gratacós, F. M., and Brewer, G. (2010) The role of AUF1 in regulated mRNA decay. Wiley Interdiscip. Rev. RNA 1, 457-473
8. Lal, A., Mazan-Mamczarz, K., Kawai, T., Yang, X., Martindale, J. L., and Gorospe, M. (2004) Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23, 3092-3102
9. 1WAF1 expression by suppressing AUF1-dependent mRNA decay. PLoS One 8, e70133
10. 6INK4a positively regulates cyclin D1 and E2F1 through negative control of AUF1. PLoS One 6, e21111
11. Brewer, G., Saccani, S., Sarkar, S., Lewis, A., and Pestka, S. (2003) Increased interleukin-10 mRNA stability in melanoma cells is associated with decreased levels of A + U-rich element binding factor AUF1. J. Interferon Cytokine Res. 23, 553-564
12. Liao, B., Hu, Y., and Brewer, G. (2007) Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nat. Struct. Mol. Biol. 14, 511-518
13. Sarkar, S., Sinsimer, K. S., Foster, R. L., Brewer, G., and Pestka, S. (2008) AUF1 isoform-specific regulation of anti-inflammatory IL10 expression in monocytes. J. Interferon Cytokine Res. 28, 679-691
14. Palanisamy, V., Park, N. J., Wang, J., and Wong, D. T. (2008) AUF1 and HuR proteins stabilize interleukin-8 mRNA in human saliva. J. Dent. Res. 87, 772-776
15. Zucconi, B. E., and Wilson, G. M. (2011) Modulation of neoplastic gene regulatory pathways by the RNA-binding factor AUF1. Front. Biosci. 16, 2307-2325
16. Arcondéguy, T., Lacazette, E., Millevoi, S., Prats, H., and Touriol, C. (2013) VEGF-A mRNA processing, stability and translation: a paradigm for intricate regulation of gene expression at the post-transcriptional level. Nucleic Acids Res. 41, 7997-8010
17. Abdelmohsen, K., Tominaga-Yamanaka, K., Srikantan, S., Yoon, J. H., Kang, M. J., and Gorospe, M. (2012) RNA-binding protein AUF1 represses Dicer expression. Nucleic Acids Res. 40, 11531-11544
18. Iorio, M. V., and Croce, C. M. (2012) MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol. Med. 4, 143-159
19. Hao, J., Zhang, Y., Deng, M., Ye, R., Zhao, S., Wang, Y., Li, J., and Zhao, Z. (2014) MicroRNA control of epithelial-mesenchymal transition in cancer stem cells. Int. J. Cancer 135, 1019-1027
20. Lamouille, S., Xu, J., and Derynck, R. (2014) Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178-196
21. Al-Khalaf, H. H., Mohideen, P., Nallar, S. C., Kalvakolanu, D. V., and Aboussekhra, A. (2013) The cyclin-dependent kinase inhibitor p16INK4a physically interacts with transcription factor Sp1 and cyclin-dependent kinase 4 to transactivate microRNA-141 and microRNA-146b-5p spontaneously and in response to ultraviolet light-induced DNA damage. J. Biol. Chem. 288, 35511-35525
22. Asirvatham, A. J., Gregorie, C. J., Hu, Z., Magner, W. J., and Tomasi, T. B. (2008) MicroRNA targets in immune genes and the Dicer/Argonaute and ARE machinery components. Mol. Immunol. 45, 1995-2006
23. INK4a inhibits both CDK4- and CDK2-associated kinase activity by reassortment of cyclin-CDK-inhibitor complexes. Mol. Cell Biol. 19, 1981-1989
24. Wang, W., Martindale, J. L., Yang, X., Chrest, F. J., and Gorospe, M. (2005) Increased stability of the p16 mRNA with replicative senescence. EMBO Rep. 6, 158-164
25. Al-Haj, L., Blackshear, P. J., and Khabar, K. S. (2012) Regulation of p21/CIP1/WAF-1 mediated cell-cycle arrest by RNase L and tristetraprolin, and involvement of AU-rich elements. Nucleic Acids Res. 40, 7739-7752
26. Knopfová, L., Beneš, P., Pekarčíková, L., Hermanová, M., Masařík, M., Pernicová, Z., Souček, K., and Smarda, J. (2012) c-Myb regulates matrix metalloproteinases 1/9, and cathepsin D: implications for matrix-dependent breast cancer cell invasion and metastasis. Mol. Cancer 11, 15
27. Jurmeister, S., Baumann, M., Balwierz, A., Keklikoglou, I., Ward, A., Uhlmann, S., Zhang, J. D., Wiemann, S., and Sahin, Ö. (2012) MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actinregulatory proteins FHOD1 and PPM1F. Mol. Cell Biol. 32, 633-651
28. Adams, C. J., Pike, A. C., Maniam, S., Sharpe, T. D., Coutts, A. S., Knapp, S., La Thangue, N. B., and Bullock, A. N. (2012) The p53 cofactor Strap exhibits an unexpected TPR motif and oligonucleotide-binding (OB)-fold structure. Proc. Natl. Acad. Sci. U.S.A. 109, 3778-3783
29. Zhao, G., Wang, B., Liu, Y., Zhang, J. G., Deng, S. C., Qin, Q., Tian, K., Li, X., Zhu, S., Niu, Y., Gong, Q., and Wang, C. Y. (2013) miRNA-141, downregulated in pancreatic cancer, inhibits cell proliferation and invasion by directly targeting MAP4K4. Mol. Cancer Ther. 12, 2569-2580
30. Geraldo, M. V., Yamashita, A. S., and Kimura, E. T. (2012) MicroRNA miR-146b-5p regulates signal transduction of TGF-β by repressing SMAD4 in thyroid cancer. Oncogene 31, 1910-1922
31. Klemke, R. L., Cai, S., Giannini, A. L., Gallagher, P. J., de Lanerolle, P., and Cheresh, D. A. (1997) Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137, 481-492
32. Yoeli-Lerner, M., Yiu, G. K., Rabinovitz, I., Erhardt, P., Jauliac, S., and Toker, A. (2005) Akt blocks breast cancer cell motility and invasion through the transcription factor NFAT. Mol. Cell 20, 539-550
33. Alessi, D. R., James, S. R., Downes, C. P., Holmes, A. B., Gaffney, P. R., Reese, C. B., and Cohen, P. (1997) Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr. Biol. 7, 261-269
34. Lauvrak, S. U., Munthe, E., Kresse, S. H., Stratford, E. W., Namløs, H. M., Meza-Zepeda, L. A., and Myklebost, O. (2013) Functional characterisation of osteosarcoma cell lines and identification of mRNAs and miRNAs associated with aggressive cancer phenotypes. Br. J. Cancer 109, 2228-2236
35. Waf1/Cip1. Oncogene 29, 2262-2271
36. Gouble, A., Grazide, S., Meggetto, F., Mercier, P., Delsol, G., and Morello, D. (2002) A new player in oncogenesis: AUF1/hnRNPD overexpression leads to tumorigenesis in transgenic mice. Cancer Res. 62, 1489-1495
37. Trojanowicz, B., Brodauf, L., Sekulla, C., Lorenz, K., Finke, R., Dralle, H., and Hoang-Vu, C. (2009) The role of AUF1 in thyroid carcinoma progression. Endocr. Relat. Cancer 16, 857-871
38. Mazan-Mamczarz, K., Hagner, P. R., Dai, B., Wood, W. H., Zhang, Y., Becker, K. G., Liu, Z., and Gartenhaus, R. B. (2008) Identification of transformation-related pathways in a breast epithelial cell model using a ribonomics approach. Cancer Res. 68, 7730-7735
39. Chappell, W. H., Steelman, L. S., Long, J. M., Kempf, R. C., Abrams, S. L., Franklin, R. A., Bäsecke, J., Stivala, F., Donia, M., Fagone, P., Malaponte, G., Mazzarino, M. C., Nicoletti, F., Libra, M., Maksimovic-Ivanic, D., Mijatovic, S., Montalto, G., Cervello, M., Laidler, P., Milella, M., Tafuri, A., Bonati, A., Evangelisti, C., Cocco, L., Martelli, A. M., and McCubrey, J. A. (2011) Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR inhibitors: rationale and importance to inhibiting these pathways in human health. Oncotarget 2, 135-164
40. Suman, S., Kurisetty, V., Das, T. P., Vadodkar, A., Ramos, G., Lakshmanaswamy, R., and Damodaran, C. (2014) Activation of AKT signaling promotes epithelial-mesenchymal transition and tumor growth in colorectal cancer cells. Mol. Carcinog. 53, E151-E160
41. Grille, S. J., Bellacosa, A., Upson, J., Klein-Szanto, A. J., van Roy, F., Lee-Kwon, W., Donowitz, M., Tsichlis, P. N., and Larue, L. (2003) The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res. 63, 2172-2178
42. Almhanna, K., Strosberg, J., and Malafa, M. (2011) Targeting AKT protein kinase in gastric cancer. Anticancer Res. 31, 4387-4392
43. Liao, Y., and Hung, M. C. (2010) Physiological regulation of Akt activity and stability. Am. J. Transl. Res. 2, 19-42
44. Korpal, M., Lee, E. S., Hu, G., and Kang, Y. (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 283, 14910-14914
45. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., and Brabletz, T. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589
46. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y., and Goodall, G. J. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593-601
47. Zhang, Y., Yan, W., Jung, Y. S., and Chen, X. (2013) PUMA cooperates with p21 to regulate mammary epithelial morphogenesis and epithelial-to-Mesenchymal transition. PLoS One 8, e66464
48. Liu, M., Casimiro, M. C., Wang, C., Shirley, L. A., Jiao, X., Katiyar, S., Ju, X., Li, Z., Yu, Z., Zhou, J., Johnson, M., Fortina, P., Hyslop, T., Windle, J. J., and Pestell, R. G. (2009) p21CIP1 attenuates Ras- and c-Myc-dependent breast tumor epithelial mesenchymal transition and cancer stem cell-like gene expression in vivo. Proc. Natl. Acad. Sci. U.S.A. 106, 19035-19039
49. Li, X. L., Hara, T., Choi, Y., Subramanian, M., Francis, P., Bilke, S., Walker, R. L., Pineda, M., Zhu, Y., Yang, Y., Luo, J., Wakefield, L. M., Brabletz, T., Park, B. H., Sharma, S., Chowdhury, D., Meltzer, P. S., and Lal, A. (2014) A p21-ZEB1 complex inhibits epithelial-mesenchymal transition through the microRNA 183-96-182 cluster. Mol. Cell Biol. 34, 533-550