miR-17 inhibition enhances the formation of kidney cancer spheres with stem cell/tumor initiating cell properties

Oncotarget

Volumn 6, Issue 8, 2015, Pages 5567-5581

  Lichner, Zsuzsanna ^a,b   Saleh, Carol ^a   Subramaniam, Venkateswaran ^a   Seivwright, Annetta ^b   Prud'homme, Gerald Joseph ^a,b   Yousef, George Makram ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cancer stem cell Tumor initiating cell; Clear cell renal cell carcinoma; Epithelial to mesenchymal transition; MicroRNA

Indexed keywords

CD24 ANTIGEN; CELL MARKER; HERMES ANTIGEN; MICRORNA; MICRORNA 17; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; MIRN17 MICRORNA, HUMAN; PROTEIN SERINE THREONINE KINASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MORPHOLOGY; CANCER SPHERE; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CANCER; MALE; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL GROWTH; DRUG SCREENING; GENETIC TRANSFECTION; GENETICS; KIDNEY CARCINOMA; KIDNEY TUMOR; METABOLISM; MULTICELLULAR SPHEROID; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CARCINOMA, RENAL CELL; CELL GROWTH PROCESSES; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; KIDNEY NEOPLASMS; MALE; MICE; MICE, INBRED NOD; MICRORNAS; NEOPLASTIC STEM CELLS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84925611849     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1901     Document Type: Article

References (48)

1. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105-11.
2. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755-68.
3. Prud'homme GJ. Cancer stem cells and novel targets for antitumor strategies. Curr Pharm Des. 2012;18:2838-49.
4. Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO, et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci USA. 2011;108:7950-5.
5. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704-15.
6. Han X, Fang X, Lou X, Hua D, Ding W, Foltz G, et al. Silencing SOX2 Induced Mesenchymal-Epithelial Transition and Its Expression Predicts Liver and Lymph Node Metastasis of CRC Patients. PLoS One. 2012;7:e41335.
7. Liu WF, Ji SR, Sun JJ, Zhang Y, Liu ZY, Liang AB, et al. CD146 Expression Correlates with Epithelial-Mesenchymal Transition Markers and a Poor Prognosis in Gastric Cancer. Int J Mol Sci. 2012;13:6399-406.
8. Sun Y, Wang BE, Leong KG, Yue P, Li L, Jhunjhunwala S, et al. Androgen deprivation causes epithelial-mesenchymal transition in the prostate: implications for androgen-deprivation therapy. Cancer Res. 2012;72:527-36.
9. Battula VL, Evans KW, Hollier BG, Shi Y, Marini FC, Ayyanan A, et al. Epithelial-mesenchymal transition-derived cells exhibit multilineage differentiation potential similar to mesenchymal stem cells. Stem Cells. 2010;28:1435-45.
10. Garcia-Sanchez O, Lopez-Hernandez FJ, Lopez-Novoa JM. An integrative view on the role of TGF-beta in the progressive tubular deletion associated with chronic kidney disease. Kidney Int. 2010;77:950-5.
11. Bottinger EP, Bitzer M. TGF-beta signaling in renal disease. J Am Soc Nephrol. 2002;13:2600-10.
12. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5:744-9.
13. Rouviere O, Bouvier R, Negrier S, Badet L, Lyonnet D. Nonmetastatic renal-cell carcinoma: is it really possible to define rational guidelines for post-treatment follow-up? Nat Clin Pract Oncol. 2006;3:200-13.
14. Siegel R, Ma J, Zou Z, Jamal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64:9-29.
15. Di LG, Buonerba C, Biglietto M, Scognamiglio F, Chiurazzi B, Riccardi F, et al. The therapy of kidney cancer with biomolecular drugs. Cancer Treat Rev. 2010;36 Suppl 3:S16-S20.
16. Bussolati B, Bruno S, Grange C, Ferrando U, Camussi G. Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J. 2008;22:3696-705.
17. Zhong Y, Guan K, Guo S, Zhou C, Wang D, Ma W, et al. Spheres derived from the human SK-RC-42 renal cell carcinoma cell line are enriched in cancer stem cells. Cancer Lett. 2010;299:150-60.
18. Melton C, Judson RL, Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature. 2010;463:621-6.
19. Mallanna SK, Rizzino A. Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells. Dev Biol. 2010;344:16-25.
20. Liu C, Tang DG. MicroRNA regulation of cancer stem cells. Cancer Res. 2011;71:5950-4.
21. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res. 2008;68:7846-54.
22. Xiong M, Jiang L, Zhou Y, Qiu W, Fang L, Tan R, et al. The miR-200 family regulates TGF-beta1-induced renal tubular epithelial to mesenchymal transition through Smad pathway by targeting ZEB1 and ZEB2 expression. Am J Physiol Renal Physiol. 2012;302:F369-F379.
23. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA. Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol. 2010;148:3-15.
24. Floor S, van Staveren WC, Larsimont D, Dumont JE, Maenhaut C. Cancer cells in epithelial-to-mesenchymal transition and tumor-propagating-cancer stem cells: distinct, overlapping or same populations. Oncogene. 2011;30:4609-21.
25. Zoller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer. 2011;11:254-67.
26. Conant JL, Peng Z, Evans MF, Naud S, Cooper K. Sarcomatoid renal cell carcinoma is an example of epithelial-mesenchymal transition. J Clin Pathol. 2011;64:1088-92.
27. Dreesen O, Brivanlou AH. Signaling pathways in cancer and embryonic stem cells. Stem Cell Rev. 2007;3:7-17.
28. Oshimori N, Fuchs E. Paracrine TGF-beta signaling counterbalances BMP-mediated repression in hair follicle stem cell activation. Cell Stem Cell. 2012;10:63-75.
29. Flynt AS, Lai EC. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet. 2008;9:831-42.
30. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, et al. A microRNA polycistron as a potential human oncogene. Nature. 2005;435:828-33.
31. Dews M, Fox JL, Hultine S, Sundaram P, Wang W, Liu YY, et al. The myc-miR-17~92 axis blunts TGF{beta} signaling and production of multiple TGF{beta}-dependent antiangiogenic factors. Cancer Res. 2010;70:8233-46.
32. Frank NY, Schatton T, Frank MH. The therapeutic promise of the cancer stem cell concept. J Clin Invest. 2010;120:41-50.
33. White NM, Yousef GM. Translating molecular signatures of renal cell carcinoma into clinical practice. J Urol. 2011;186:9-11.
34. Blagosklonny MV. Cancer stem cell and cancer stemloids: from biology to therapy. Cancer Biol Ther 2007;6:1684-90.
35. Blagosklonny MV. Target for cancer therapy: proliferating cells or stem cells. Leukemia 2006;20:385-91.
36. Debeb BG, Zhang X, Krishnamurthy S, Gao H, Cohen E, Li L, et al. Characterizing cancer cells with cancer stem cell-like features in 293T human embryonic kidney cells. Mol Cancer. 2010;9:180.
37. Zhong Y, Guan K, Guo S, Zhou C, Wang D, Ma W, et al. Spheres derived from the human SK-RC-42 renal cell carcinoma cell line are enriched in cancer stem cells. Cancer Lett. 2010;299:150-60.
38. Concepcion CP, Bonetti C, Ventura A. The microRNA-17-92 family of microRNA clusters in development and disease. Cancer J. 2012;18:262-7.
39. Chow TF, Mankaruos M, Scorilas A, Youssef Y, Girgis A, Mossad S, et al. The miR-17-92 cluster is over expressed in and has an oncogenic effect on renal cell carcinoma. J Urol. 2010;183:743-51.
40. Yu Z, Willmarth NE, Zhou J, Katiyar S, Wang M, Liu Y, et al. microRNA 17/20 inhibits cellular invasion and tumor metastasis in breast cancer by heterotypic signaling. Proc Natl Acad Sci USA. 2010;107:8231-6.
41. Girgis AH, Iakovlev VV, Beheshti B, Bayani J, Squire JA, Bui A, et al. Multilevel Whole-Genome Analysis Reveals Candidate Biomarkers in Clear Cell Renal Cell Carcinoma. Cancer Res. 2012.
42. Stembalska A, Blin N, Ramsey D, Sasiadek MM. Three distinct regions of deletion on 13q in squamous cell carcinoma of the larynx. Oncol Rep. 2006;16:417-21.
43. Schwarzenbach H, Muller V, Milde-Langosch K, Steinbach B, Pantel K. Evaluation of cell-free tumour DNA and RNA in patients with breast cancer and benign breast disease. Mol Biosyst. 2011;7:2848-54.
44. Petrocca F, Vecchione A, Croce CM. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res. 2008;68:8191-4.
45. Lichner Z, Mejia-Guerrero S, Ignacak M, Krizova A, Bao TT, Girgis AH, et al. Pleiotropic action of renal cell carcinoma-dysregulated miRNAs on hypoxia-related signaling pathways. Am J Pathol. 2012;180:1675-87.
46. Sjolund J, Bostrom AK, Lindgren D, Manna S, Moustakas A, Ljungberg B, et al. The notch and TGF-beta signaling pathways contribute to the aggressiveness of clear cell renal cell carcinoma. PLoS One. 2011;6:e23057.
47. Sun T, Sun BC, Zhao XL, Zhao N, Dong XY, Che N, et al. Promotion of tumor cell metastasis and vasculogenic mimicry by way of transcription coactivation by Bcl-2 and Twist1: a study of hepatocellular carcinoma. Hepatology. 2011;54:1690-706.
48. Iakovlev VV, Gabril M, Dubinski W, Scorilas A, Youssef YM, Faragalla H, et al. Microvascular density as an independent predictor of clinical outcome in renal cell carcinoma: an automated image analysis study. Lab Invest. 2012;92:46-56.