Hypoxia-mediated downregulation of miRNA biogenesis promotes tumour progression

Nature Communications

Volumn 5, Issue , 2014, Pages

  Rupaimoole, Rajesha ^a,b   Wu, Sherry Y ^a   Pradeep, Sunila ^a   Ivan, Cristina ^a   Pecot, Chad V ^c   Gharpure, Kshipra M ^a,b   Nagaraja, Archana S ^a,b   Armaiz Pena, Guillermo N ^a   McGuire, Michael ^a   Zand, Behrouz ^a   Dalton, Heather J ^a   Filant, Justyna ^a   Miller, Justin Bottsford ^a   Lu, Chunhua ^a   Sadaoui, Nouara C ^a,b   Mangala, Lingegowda S ^a   Taylor, Morgan ^a   Van Den Beucken, Twan ^d   Koch, Elizabeth ^d,e   Rodriguez Aguayo, Cristian ^a   Huang, Li ^a   Bar Eli, Menashe ^a   Wouters, Bradly G ^d,e   Radovich, Milan ^f   Ivan, Mircea ^f   Calin, George A ^a   Zhang, Wei ^a   Lopez Berestein, Gabriel ^a   Sood, Anil K ^a   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY HEALTH NETWORK   (Canada)

^f INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; DROSHA PROTEIN; MICRORNA; PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR ELK 1; TRANSCRIPTION FACTOR ETS 1; UNCLASSIFIED DRUG; DEAD BOX PROTEIN; DICER1 PROTEIN, HUMAN; DROSHA PROTEIN, HUMAN; ETS1 PROTEIN, HUMAN; RIBONUCLEASE III; VASCULOTROPIN A;

CANCER; DISEASE PREVALENCE; ENZYME ACTIVITY; HYPOXIA; RNA; TUMOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CANCER GROWTH; CELL MATURATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; RNA SEQUENCE; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL HYPOXIA; DISEASE COURSE; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEOPLASMS; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL HYPOXIA; CELL LINE, TUMOR; DEAD-BOX RNA HELICASES; DISEASE PROGRESSION; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE, NUDE; MICRORNAS; MODELS, BIOLOGICAL; NEOPLASMS; PROTO-ONCOGENE PROTEIN C-ETS-1; RIBONUCLEASE III; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84923276259     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6202     Document Type: Article

References (47)

1. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
2. Lee, Y. S. & Dutta, A. MicroRNAs in cancer. Annu. Rev. Pathol. 4, 199-227 (2009).
3. Calin, G. A. et al. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. New Engl. J. Med. 353, 1793-1801 (2005).
4. Croce, C. M. & Calin, G. A. miRNAs, cancer, and stem cell division. Cell 122, 6-7 (2005).
5. Hwang, H. W. & Mendell, J. T. MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br. J. Cancer 94, 776-780 (2006).
6. Porkka, K. P. et al. MicroRNA expression profiling in prostate cancer. Cancer Res. 67, 6130-6135 (2007).
7. Lu, J. et al. MicroRNA expression profiles classify human cancers. Nature 435, 834-838 (2005).
8. Merritt, W. M. et al. Dicer, Drosha, and outcomes in patients with ovarian cancer. New Engl. J. Med. 359, 2641-2650 (2008).
9. Dedes, K. J. et al. Down-regulation of the miRNA master regulators Drosha and Dicer is associated with specific subgroups of breast cancer. Eur. J. Cancer 47, 138-150 (2011).
10. Lin, R. J. et al. microRNA signature and expression of Dicer and Drosha can predict prognosis and delineate risk groups in neuroblastoma. Cancer Res. 70, 7841-7850 (2010).
11. Karube, Y. et al. Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci. 96, 111-115 (2005).
12. Tokumaru, S., Suzuki, M., Yamada, H., Nagino, M. & Takahashi, T. let-7 regulates Dicer expression and constitutes a negative feedback loop. Carcinogenesis 29, 2073-2077 (2008).
13. Martello, G. et al. A microRNA targeting dicer for metastasis control. Cell 141, 1195-1207 (2010).
14. Su, X. et al. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 467, 986-990 (2010).
15. Ho, J. J. et al. Functional importance of Dicer protein in the adaptive cellular response to hypoxia. J. Biol. Chem. 287, 29003-29020 (2012).
16. 2. Nature 497, 383-387 (2013).
17. van den Beucken, T. et al. Hypoxia promotes stem cell phenotypes and poor prognosis through epigenetic regulation of DICER. Nat. Commun. 5, 5203 doi:10.1038/ncomms6203 (2014).
18. Harris, A. L. Hypoxia - a key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47 (2002).
19. Shannon, A. M., Bouchier-Hayes, D. J., Condron, C. M. & Toomey, D. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat. Rev. 29, 297-307 (2003).
20. Vaupel, P. & Mayer, A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev. 26, 225-239 (2007).
21. Loges, S., Mazzone, M., Hohensinner, P. & Carmeliet, P. Silencing or fueling metastasis with VEGF inhibitors: antiangiogenesis revisited. Cancer Cell 15, 167-170 (2009).
22. Winter, S. C. et al. Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers. Cancer Res. 67, 3441-3449 (2007).
23. Wang, B. D. et al. Prostate apoptosis response protein 4 sensitizes human colon cancer cells to chemotherapeutic 5-FU through mediation of an NF kappaB and microRNA network. Mol. Cancer 9, 98 (2010).
24. Wang, X., Zhao, X., Gao, P. & Wu, M. c-Myc modulates microRNA processing via the transcriptional regulation of Drosha. Sci. Rep. 3, 1942(2013).
25. Ren, M. et al. Correlation between hepatitis B virus protein and microRNA processor Drosha in cells expressing HBV. Antiviral Res. 94, 225-231 (2012).
26. Gupta, M., Zak, R., Libermann, T. A. & Gupta, M. P. Tissue-restricted expression of the cardiac alpha-myosin heavy chain gene is controlled by a downstream repressor element containing a palindrome of two ets-binding sites. Mol. Cell. Biol. 18, 7243-7258 (1998).
27. Oikawa, M. et al. Hypoxia induces transcription factor ETS-1 via the activity of hypoxia-inducible factor-1. Biochem. Biophys. Res. Commun. 289, 39-43 (2001).
28. Yan, S. F. et al. Hypoxia-associated induction of early growth response-1 gene expression. J. Biol. Chem. 274, 15030-15040 (1999).
29. Yang, S. H., Vickers, E., Brehm, A., Kouzarides, T. & Sharrocks, A. D. Temporal recruitment of the mSin3A-histone deacetylase corepressor complex to the ETS domain transcription factor Elk-1. Mol. Cell. Biol. 21, 2802-2814 (2001).
30. Miyamoto-Sato, E. et al. A comprehensive resource of interacting protein regions for refining human transcription factor networks. PLoS ONE 5, e9289 (2010).
31. Merritt, W. M. et al. Anti-angiogenic properties of metronomic topotecan in ovarian carcinoma. Cancer Biol. Ther. 8, 1596-1603 (2009).
32. Mancuso, M. R. et al. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J. Clin. Invest. 116, 2610-2621 (2006).
33. Yamagishi, N. et al. Chronic inhibition of tumor cell-derived VEGF enhances the malignant phenotype of colorectal cancer cells. BMC Cancer 13, 229 (2013).
34. Yang, M. H. et al. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol. 10, 295-305 (2008).
35. Sahlgren, C., Gustafsson, M. V., Jin, S., Poellinger, L. & Lendahl, U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc. Natl Acad. Sci. USA 105, 6392-6397 (2008).
36. Kumar, M. S. et al. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev. 23, 2700-2704 (2009).
37. Fan, M. et al. Comprehensive analysis of microRNA (miRNA) targets in breast cancer cells. J. Biol. Chem. 288, 27480-27493 (2013).
38. Pecot, C. V., Calin, G. A., Coleman, R. L., Lopez-Berestein, G. & Sood, A. K. RNA interference in the clinic: challenges and future directions. Nat. Rev. Cancer 11, 59-67 (2011).
39. Pecot, C. V. et al. Tumour angiogenesis regulation by the miR-200 family. Nat. Commun. 4, 2427 (2013).
40. Nishimura, M. et al. Therapeutic synergy between microRNA and siRNA in ovarian cancer treatment. Cancer Discov. 3, 1302-1315 (2013).
41. Armaiz-Pena, G. N. et al. Src activation by beta-adrenoreceptors is a key switch for tumour metastasis. Nat. Commun. 4, 1403 (2013).
42. Wu, S. Y. et al. 20-OMe-phosphorodithioate-modified siRNAs show increased loading into the RISC complex and enhanced anti-tumour activity. Nat. Commun. 5, 3459 (2014).
43. Landen, Jr C. N. et al. Therapeutic EphA2 gene targeting in vivo using neutral liposomal small interfering RNA delivery. Cancer Res. 65, 6910-6918 (2005).
44. Sood, A. K. et al. Stress hormone-mediated invasion of ovarian cancer cells. Clin. Cancer Res. 12, 369-375 (2006).
45. Kim, S. W. et al. A sensitive non-radioactive northern blot method to detect small RNAs. Nucleic Acids Res. 38, e98 (2010).
46. Shahzad, M. M. et al. Stress effects on FosB-and interleukin-8 (IL8)-driven ovarian cancer growth and metastasis. J. Biol. Chem. 285, 35462-35470 (2010).
47. Lu, C. et al. Regulation of tumor angiogenesis by EZH2. Cancer Cell 18, 185-197 (2010).