Regulatory interplay between miR-21, JAG1 and 17beta-estradiol (E2) in breast cancer cells

Biochemical and Biophysical Research Communications

Volumn 423, Issue 2, 2012, Pages 234-239

  Selcuklu, S Duygu ^a   Donoghue, Mark T A ^a,b   Kerin, Michael J ^a   Spillane, Charles ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

Breast cancer; Estrogen receptor (ER) status; MicroRNA; MiR 21

Indexed keywords

ESTRADIOL; JAGGED1; MICRORNA 21;

ARTICLE; BREAST CANCER; CELL STRAIN MCF 7; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

3' UNTRANSLATED REGIONS; BREAST NEOPLASMS; CALCIUM-BINDING PROTEINS; CELL LINE, TUMOR; DOWN-REGULATION; ESTRADIOL; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICRORNAS; PROMOTER REGIONS, GENETIC;

EID: 84862866422     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.05.074     Document Type: Article

References (40)

1. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
2. Deng S., Calin G.A., Croce C.M., Coukos G., Zhang L. Mechanisms of microRNA deregulation in human cancer. Cell Cycle 2008, 7:2643-2646.
3. Croce C.M. Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 2009, 10:704-714.
4. Wiggins J.F., Ruffino L., Kelnar K., Omotola M., Patrawala L., Brown D., Bader A.G. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 2010, 70:5923-5930.
5. Friedman J.M., Liang G., Liu C.C., Wolff E.M., Tsai Y.C., Ye W., Zhou X., Jones P.A. The putative tumor suppressor microRNA-101 modulates the cancer epigenome by repressing the polycomb group protein EZH2. Cancer Res. 2009, 69:2623-2629.
6. Medina P.P., Nolde M., Slack F.J. OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 2010, 467:86-90.
7. Selcuklu S.D., Donoghue M.T., Spillane C. MiR-21 as a key regulator of oncogenic processes. Biochem. Soc. Trans. 2009, 37:918-925.
8. Zhu W., Yang L., Du Z. MicroRNA regulation and tissue-specific protein interaction network. PLoS ONE 2011, 6:e25394.
9. Hashimi S.T., Fulcher J.A., Chang M.H., Gov L., Wang S., Lee B. MicroRNA profiling identifies miR-34a and miR-21 and their target genes JAG1 and WNT1 in the coordinate regulation of dendritic cell differentiation. Blood 2009, 114:404-414.
10. Reedijk M., Pinnaduwage D., Dickson B.C., Mulligan A.M., Zhang H., Bull S.B., O'Malley F.P., Egan S.E., Andrulis I.L. JAG1 expression is associated with a basal phenotype and recurrence in lymph node-negative breast cancer. Breast Cancer Res. Treat. 2008, 111:439-448.
11. Snijders A.M., Schmidt B.L., Fridlyand J., Dekker N., Pinkel D., Jordan R.C., Albertson D.G. Rare amplicons implicate frequent deregulation of cell fate specification pathways in oral squamous cell carcinoma. Oncogene 2005, 24:4232-4242.
12. Simon D., Giordano T.J., Hammer G. Upregulated JAG1 Enhances Cell Proliferation in Adrenocortical Carcinoma. Clin. Cancer Res. 2012, 18:2452-2464.
13. Reedijk M., Odorcic S., Chang L., Zhang H., Miller N., McCready D.R., Lockwood G., Egan S.E. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res. 2005, 65:8530-8537.
14. Dickson B.C., Mulligan A.M., Zhang H., Lockwood G., O'Malley F.P., Egan S.E., Reedijk M. High-level JAG1 mRNA and protein predict poor outcome in breast cancer. Mod. Pathol. 2007, 20:685-693.
15. Shimizu M., Cohen B., Goldvasser P., Berman H., Virtanen C., Reedijk M. Plasminogen activator uPA is a direct transcriptional target of the JAG1-Notch receptor signaling pathway in breast cancer. Cancer Res. 2011, 71:277-286.
16. Hofmann J.J., Luisa Iruela-Arispe M. Notch expression patterns in the retina: an eye on receptor-ligand distribution during angiogenesis. Gene Expr. Patterns 2007, 7:461-470.
17. Katoh M. Notch ligand, JAG1, is evolutionarily conserved target of canonical WNT signaling pathway in progenitor cells. Int. J. Mol. Med. 2006, 17:681-685.
18. Cohen B., Shimizu M., Izrailit J., Ng N.F., Buchman Y., Pan J.G., Dering J., Reedijk M. Cyclin D1 is a direct target of JAG1-mediated Notch signaling in breast cancer. Breast Cancer Res. Treat. 2010, 123:113-124.
19. Soares R., Balogh G., Guo S., Gartner F., Russo J., Schmitt F. Evidence for the notch signaling pathway on the role of estrogen in angiogenesis. Mol. Endocrinol. 2004, 18:2333-2343.
20. Wickramasinghe N.S., Manavalan T.T., Dougherty S.M., Riggs K.A., Li Y., Klinge C.M. Estradiol downregulates miR-21 expression and increases miR-21 target gene expression in MCF-7 breast cancer cells. Nucleic Acids Res. 2009, 37:2584-2595.
21. Yan L.X., Wu Q.N., Zhang Y., Li Y.Y., Liao D.Z., Hou J.H., Fu J., Zeng M.S., Yun J.P., Wu Q.L., Zeng Y.X., Shao J.Y. Knockdown of miR-21 in human breast cancer cell lines inhibits proliferation, in vitro migration and in vivo tumor growth. Breast Cancer Res. 2011, 13:R2.
22. Zhu S., Wu H., Wu F., Nie D., Sheng S., Mo Y.Y. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res. 2008, 18:350-359.
23. Wang Z., Li Y., Banerjee S., Kong D., Ahmad A., Nogueira V., Hay N., Sarkar F.H. Down-regulation of Notch-1 and Jagged-1 inhibits prostate cancer cell growth, migration and invasion, and induces apoptosis via inactivation of Akt, mTOR, and NF-kappaB signaling pathways. J. Cell. Biochem. 2010, 109:726-736.
24. Zhang Y., Wang Z., Ahmed F., Banerjee S., Li Y., Sarkar F.H. Down-regulation of Jagged-1 induces cell growth inhibition and S phase arrest in prostate cancer cells. Int. J. Cancer 2006, 119:2071-2077.
25. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
26. Krek A., Grun D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., MacMenamin P., da Piedade I., Gunsalus K.C., Stoffel M., Rajewsky N. Combinatorial microRNA target predictions. Nat. Genet. 2005, 37:495-500.
27. Enright A.J., John B., Gaul U., Tuschl T., Sander C., Marks D.S. MicroRNA targets in Drosophila. Genome Biol. 2003, 5:R1.
28. Landgraf P., Rusu M., Sheridan R., Sewer A., Iovino N., Aravin A., Pfeffer S., Rice A., Kamphorst A.O., Landthaler M., Lin C., Socci N.D., Hermida L., Fulci V., Chiaretti S., Foa R., Schliwka J., Fuchs U., Novosel A., Muller R.U., Schermer B., Bissels U., Inman J., Phan Q., Chien M., Weir D.B., Choksi R., De Vita G., Frezzetti D., Trompeter H.I., Hornung V., Teng G., Hartmann G., Palkovits M., Di Lauro R., Wernet P., Macino G., Rogler C.E., Nagle J.W., Ju J., Papavasiliou F.N., Benzing T., Lichter P., Tam W., Brownstein M.J., Bosio A., Borkhardt A., Russo J.J., Sander C., Zavolan M., Tuschl T. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007, 129:1401-1414.
29. Gaur A., Jewell D.A., Liang Y., Ridzon D., Moore J.H., Chen C., Ambros V.R., Israel M.A. Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res. 2007, 67:2456-2468.
30. Liu H., Kohane I.S. Tissue and process specific microRNA-mRNA co-expression in mammalian development and malignancy. PLoS ONE 2009, 4:e5436.
31. Saha Roy S., Vadlamudi R.K. Role of estrogen receptor signaling in breast cancer metastasis. Int. J. Breast Cancer 2012, 2012:654698.
32. Zheng S., Huang J., Zhou K., Zhang C., Xiang Q., Tan Z., Wang T., Fu X. 17beta-Estradiol enhances breast cancer cell motility and invasion via extra-nuclear activation of actin-binding protein ezrin. PLoS ONE 2011, 6:e22439.
33. Sanchez A.M., Flamini M.I., Baldacci C., Goglia L., Genazzani A.R., Simoncini T. Estrogen receptor-alpha promotes breast cancer cell motility and invasion via focal adhesion kinase and N-WASP. Mol. Endocrinol. 2010, 24:2114-2125.
34. Ariazi E.A., Cunliffe H.E., Lewis-Wambi J.S., Slifker M.J., Willis A.L., Ramos P., Tapia C., Kim H.R., Yerrum S., Sharma C.G., Nicolas E., Balagurunathan Y., Ross E.A., Jordan V.C. Estrogen induces apoptosis in estrogen deprivation-resistant breast cancer through stress responses as identified by global gene expression across time. Proc. Natl. Acad. Sci. USA 2011, 108:18879-18886.
35. Lobanova Y.S., Scherbakov A.M., Shatskaya V.A., Krasil'nikov M.A. Mechanism of estrogen-induced apoptosis in breast cancer cells: role of the NF-kappaB signaling pathway. Biochemistry (Mosc) 2007, 72:320-327.
36. Bhat-Nakshatri P., Wang G., Collins N.R., Thomson M.J., Geistlinger T.R., Carroll J.S., Brown M., Hammond S., Srour E.F., Liu Y., Nakshatri H. Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucleic Acids Res. 2009, 37:4850-4861.
37. O. Paris, L. Ferraro, O.M. Grober, M. Ravo, M.R. De Filippo, G. Giurato, G. Nassa, R. Tarallo, C. Cantarella, F. Rizzo, A. Di Benedetto, M. Mottolese, V. Benes, C. Ambrosino, E. Nola, A. Weisz, Direct regulation of microRNA biogenesis and expression by estrogen receptor beta in hormone-responsive breast cancer, Oncogene (2012), [Epub ahead of print]. http://dx.doi.org/10.1038./onc.2011.583.
38. Yu X., Zhang X., Dhakal I.B., Beggs M., Kadlubar S., Luo D. Induction of cell proliferation and survival genes by estradiol-repressed microRNAs in breast cancer cells. BMC Cancer 2012, 12:29.
39. Cochrane D.R., Cittelly D.M., Howe E.N., Spoelstra N.S., McKinsey E.L., LaPara K., Elias A., Yee D., Richer J.K. MicroRNAs link estrogen receptor alpha status and Dicer levels in breast cancer. Horm. Cancer 2010, 1:306-319.
40. Ferraro L., Ravo M., Nassa G., Tarallo R., De Filippo M.R., Giurato G., Cirillo F., Stellato C., Silvestro S., Cantarella C., Rizzo F., Cimino D., Friard O., Biglia N., De Bortoli M., Cicatiello L., Nola E., Weisz A. Effects of oestrogen on MicroRNA Expression in hormone-responsive breast cancer cells. Horm. Cancer 2012, 3:65-78.