Stress response of glioblastoma cells mediated by miR-17-5p targeting PTEN and the passenger strand miR-17-3p targeting MDM2

Oncotarget

Volumn 3, Issue 12, 2012, Pages 1653-1668

  Li, Haoran ^a,b   Yang, Burton B ^a,b  

^a Sunnybrook Health Sciences Centre   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Drug resistance; MicroRNA; MiR 17; Stem cell; Stress response

Indexed keywords

CARMUSTINE; CD133 ANTIGEN; DOCETAXEL; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; MICRORNA 17 3P; MICRORNA 17 5P; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN MDM2; TEMOZOLOMIDE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; CANCER RESISTANCE; CANCER STEM CELL; CELL CYCLE G1 PHASE; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; COLONY FORMATION; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSFECTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; NUTRITION; PHENOTYPE; PROTEIN RNA BINDING; PROTEIN TARGETING; UPREGULATION;

EID: 84874733206     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.810     Document Type: Article

References (70)

1. Nana-Sinkam SP and Croce CM. Clinical Applications for microRNAs in Cancer. Clin Pharmacol Ther. Epub 2012 Dec 5
2. Huang Z, Cheng L, Guryanova OA, Wu Q and Bao S. Cancer stem cells in glioblastoma--molecular signaling and therapeutic targeting. Protein &cell. 2010; 1(7):638-655.
3. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG and Parada LF. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012; 488(7412):522-526.
4. Kiriakidou M, Tan GS, Lamprinaki S, De Planell-Saguer M, Nelson PT and Mourelatos Z. An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell. 2007; 129(6):1141-1151.
5. Guo L and Lu Z. The fate of miRNA strand through evolutionary analysis: implication for degradation as merely carrier strand or potential regulatory molecule? PLoS One. 2010; 5(6):e11387.
6. Matranga C, Tomari Y, Shin C, Bartel DP and Zamore PD. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell. 2005 123(4):607-620.
7. Lujambio A and Lowe SW. The microcosmos of cancer. Nature. 2012; 482(7385):347-355.
8. Bagnoli M, De Cecco L, Granata A, Nicoletti R, Marchesi E, Alberti P, Valeri B, Libra M, Barbareschi M, Raspagliesi F, Mezzanzanica D and Canevari S. Identification of a chrXq27.3 microRNA cluster associated with early relapse in advanced stage ovarian cancer patients. Oncotarget. 2011; 2(12):1265-1278.
9. Erkan EP, Breakefield XO and Saydam O. miRNA signature of schwannomas: possible role(s) of "tumor suppressor" miRNAs in benign tumors. Oncotarget. 2011; 2(3):265-270.
10. Sozzi G, Pastorino U and Croce CM. MicroRNAs and lung cancer: from markers to targets. Cell Cycle. 2011; 10(13):2045-2046.
11. Srikantan S, Gorospe M and Abdelmohsen K. Senescence-associated microRNAs linked to tumorigenesis. Cell Cycle. 2011; 10(19):3211-3212.
12. Lee DY, Deng Z, Wang CH and Yang BB. MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc Natl Acad Sci U S A. 2007; 104(51):20350-20355.
13. Chen Y and Stallings RL. Differential patterns of microRNA expression in neuroblastoma are correlated with prognosis, differentiation, and apoptosis. Cancer research. 2007; 67(3):976-983.
14. Croce CM and Calin GA. miRNAs, cancer, and stem cell division. Cell. 2005; 122(1):6-7.
15. Pekarsky Y and Croce CM. Is miR-29 an oncogene or tumor suppressor in CLL? Oncotarget. 2010; 1(3):224-227.
16. Viticchie G, Lena AM, Latina A, Formosa A, Gregersen LH, Lund AH, Bernardini S, Mauriello A, Miano R, Spagnoli LG, Knight RA, Candi E and Melino G. MiR-203 controls proliferation, migration and invasive potential of prostate cancer cell lines. Cell Cycle. 2011; 10(7):1121-1131.
17. Nohata N, Sone Y, Hanazawa T, Fuse M, Kikkawa N, Yoshino H, Chiyomaru T, Kawakami K, Enokida H, Nakagawa M, Shozu M, Okamoto Y and Seki N. miR-1 as a tumor suppressive microRNA targeting TAGLN2 in head and neck squamous cell carcinoma. Oncotarget. 2011; 2(1-2):29-42.
18. Schetter AJ and Harris CC. MicroRNAs as molecular classifiers for cancer. Cell Cycle. 2011; 10(17):2827-2828.
19. Rutnam ZJ and Yang BB. The involvement of microRNAs in malignant transformation. Histol Histopathol. 2012; 27(10):1263-1270.
20. Smits M, Nilsson J, Mir SE, van der Stoop PM, HullemanE, Niers JM, de Witt Hamer PC, Marquez VE, Cloos J, Krichevsky AM, Noske DP, Tannous BA and Wurdinger T. miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget. 2010; 1(8):710-720.
21. Speranza MC, Frattini V, Pisati F, Kapetis D, Porrati P, Eoli M, Pellegatta S and Finocchiaro G. NEDD9, a novel target of miR-145, increases the invasiveness of glioblastoma. Oncotarget. 2012; 3(7):723-734.
22. Fang L, Deng Z, Shatseva T, Yang J, Peng C, Du WW, Yee AJ, Ang LC, He C, Shan SW and Yang BB. MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-beta8. Oncogene. 2011; 30(7):806-821.
23. Bonauer A and Dimmeler S. The microRNA-17-92 cluster: still a miRacle? Cell Cycle. 2009; 8(23):3866-3873.
24. Fang L, Du WW, Yang W, Rutnam ZJ, Peng C, Li H, O'Malley YQ, Askeland RW, Sugg S, Liu M, Mehta T, Deng Z and Yang BB.MiR-93 enhances angiogenesis and metastasis by targeting LATS2. Cell Cycle. 2012,11(23);4352-4365
25. Rutnam ZJ, Wight TN and Yang BB. miRNAs regulate expression and function of extracellular matrix molecules. Matrix Biol. 2012.
26. Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell. 2008; 133(2):217-222.
27. Shan SW, Lee DY, Deng Z, Shatseva T, Jeyapalan Z, Du WW, Zhang Y, Xuan JW, Yee SP, Siragam V and Yang BB. MicroRNA MiR-17 retards tissue growth and represses fibronectin expression. Nat Cell Biol. 2009; 11(8):1031-1038.
28. Asuthkar S, Velpula KK, Chetty C, Gorantla B and Rao JS. Epigenetic Regulation of miRNA-211 by MMP-9 Governs Glioma Cell Apoptosis, Chemosensitivity and Radiosensitivity. Oncotarget. 2012; 3(11):1439-1454.
29. Malzkorn B, Wolter M, Liesenberg F, Grzendowski M, Stuhler K, Meyer HE and Reifenberger G. Identification and functional characterization of microRNAs involved in the malignant progression of gliomas. Brain Pathol. 2010; 20(3):539-550.
30. Ernst A, Campos B, Meier J, Devens F, Liesenberg F, Wolter M, Reifenberger G, Herold-Mende C, Lichter P and Radlwimmer B. De-repression of CTGF via the miR-17-92 cluster upon differentiation of human glioblastoma spheroid cultures. Oncogene. 2010; 29(23):3411-3422.
31. Tamminga J, Kathiria P, Koturbash I and Kovalchuk O. DNA damage-induced upregulation of miR-709 in the germline downregulates BORIS to counteract aberrant DNA hypomethylation. Cell Cycle. 2008; 7(23):3731-3736.
32. Mansfield JH, Harfe BD, Nissen R, Obenauer J, Srineel J, Chaudhuri A, Farzan-Kashani R, Zuker M, Pasquinelli AE, Ruvkun G, Sharp PA, Tabin CJ and McManus MT. MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nature genetics. 2004; 36(10):1079-1083.
33. Cufi S, Vazquez-Martin A, Oliveras-Ferraros C, Quirantes R, Segura-Carretero A, Micol V, Joven J, Bosch-Barrera J, Del Barco S, Martin-Castillo B, Vellon L and Menendez JA. Metformin lowers the threshold for stress-induced senescence: a role for the microRNA-200 family and miR-205. Cell Cycle. 2012; 11(6):1235-1246.
34. Hu Y, Matkovich SJ, Hecker PA, Zhang Y, Edwards JR and Dorn GW, 2nd. Epitranscriptional orchestration of genetic reprogramming is an emergent property of stress-regulated cardiac microRNAs. Proc Natl Acad Sci U S A. 2012; 109(48):19864-19869.
35. Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R and Frank W. Transcriptional control of gene expression by microRNAs. Cell. 2010; 140(1):111-122.
36. Srikantan S, Marasa BS, Becker KG, Gorospe M and Abdelmohsen K. Paradoxical microRNAs: individual gene repressors, global translation enhancers. Cell Cycle. 2011; 10(5):751-759.
37. Marsit CJ, Eddy K and Kelsey KT. MicroRNA responses to cellular stress. Cancer research. 2006; 66(22):10843-10848.
38. Loscalzo J. The cellular response to hypoxia: tuning the system with microRNAs. The Journal of clinical investigation. 2010; 120(11):3815-3817.
39. Pothof J, Verkaik NS, Hoeijmakers JH and van Gent DC. MicroRNA responses and stress granule formation modulate the DNA damage response. Cell Cycle. 2009; 8(21):3462-3468.
40. Mavrakis KJ, Leslie CS and Wendel HG. Cooperative control of tumor suppressor genes by a network of oncogenic microRNAs. Cell Cycle. 2011; 10(17):2845-2849.
41. Portal MM. MicroRNA regulation masters basal transcription: Clash of the Titans. Cell Cycle. 2011; 10(19):3219-3220.
42. Ory B and Ellisen LW. A microRNA-dependent circuit controlling p63/p73 homeostasis: p53 family cross-talk meets therapeutic opportunity. Oncotarget. 2011; 2(3):259-264.
43. Musumeci M, Coppola V, Addario A, Patrizii M, Maugeri-Sacca M, Memeo L, Colarossi C, Francescangeli F, Biffoni M, Collura D, Giacobbe A, D'Urso L, Falchi M, Venneri MA, Muto G, De Maria R, et al. Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer. Oncogene. 2011; 30(41):4231-4242.
44. Zhang H, Li QY, Guo ZZ, Guan Y, Du J, Lu YY, Hu YY, Liu P, Huang S and Su SB. Serum levels of microRNAs can specifically predict liver injury of chronic hepatitis B. World J Gastroenterol. 2012; 18(37):5188-5196.
45. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C and Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010; 468(7325):829-833.
46. Levin VA, Panchabhai SC, Shen L, Kornblau SM, QiuY and Baggerly KA. Different changes in protein and phosphoprotein levels result from serum starvation of high-grade glioma and adenocarcinoma cell lines. Journal of proteome research. 2010; 9(1):179-191.
47. Hossain A, Kuo MT and Saunders GF. Mir-17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Molecular and cellular biology. 2006; 26(21):8191-8201.
48. Brekman A, Singh KE, Polotskaia A, Kundu N and Bargonetti J. A p53-independent role of Mdm2 in estrogen-mediated activation of breast cancer cell proliferation. Breast cancer research : BCR. 2011; 13(1):R3.
49. de Groot JF, Fuller G, Kumar AJ, Piao Y, Eterovic K, Ji Y and Conrad CA. Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro-oncology. 2010; 12(3):233-242.
50. Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ and Van Meir EG. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro-oncology. 2005; 7(2):134-153.
51. Jiang BH and Liu LZ. PI3K/PTEN signaling in angiogenesis and tumorigenesis. Advances in cancer research. 2009; 102:19-65.
52. Thomas R and Kim MH. A HIF-1alpha-dependent autocrine feedback loop promotes survival of serum-deprived prostate cancer cells. The Prostate. 2009; 693):263-275.
53. Shatseva T, Lee DY, Deng Z and Yang BB. MicroRNA miR-199a-3p regulates cell proliferation and survival by targeting caveolin-2. Journal of cell science. 2011; 124Pt 16):2826-2836.
54. Mateescu B, Batista L, Cardon M, Gruosso T, de Feraudy Y, Mariani O, Nicolas A, Meyniel JP, Cottu P, Sastre-Garau X and Mechta-Grigoriou F. miR-141 and miR-200a act on ovarian tumorigenesis by controlling oxidative stress response. Nature medicine. 2011; 17(12):1627-1635.
55. Mendell JT and Olson EN. MicroRNAs in stress signaling and human disease. Cell. 2012; 148(6):1172-1187.
56. Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, Dillehay LE, Madan A, Semenza GL and Bedi A. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1alpha. Genes &development. 2000; 14(1):34-44.
57. Liu C and Tang DG. MicroRNA regulation of cancer stem cells. Cancer research. 2011; 71(18):5950-5954.
58. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J and Song E. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 2007; 131(6):1109-1123.
59. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, Maira G, Parati EA, Stassi G, Larocca LM and De Maria R. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature. 2010; 468(7325):824-828.
60. Carney BJ and Shah K. Migration and fate of therapeutic stem cells in different brain disease models. Neuroscience. 2011; 197:37-47.
61. Kolenda J, Jensen SS, Aaberg-Jessen C, Christensen K, Andersen C, Brunner N and Kristensen BW. Effects of hypoxia on expression of a panel of stem cell and chemoresistance markers in glioblastoma-derived spheroids. Journal of neuro-oncology. 2011; 1031):43-58.
62. Ying M, Wang S, Sang Y, Sun P, Lal B, Goodwin CR, Guerrero-Cazares H, Quinones-Hinojosa A, Laterra J and Xia S. Regulation of glioblastoma stem cells by retinoic acid: role for Notch pathway inhibition. Oncogene. 2011; 30(31):3454-3467.
63. Rutnam ZJ and Yang BB. The non-coding 3' UTR of CD44 induces metastasis by regulating extracellular matrix functions. J Cell Sci. 2012; 125(Pt 8):2075-2085.
64. Kahai S, Lee SC, Lee DY, Yang J, Li M, Wang CH, Jiang Z, Zhang Y, Peng C and Yang BB. MicroRNA miR-378 regulates nephronectin expression modulating osteoblast differentiation by targeting GalNT-7. PLoS One. 2009; 4(10):e7535.
65. Siragam V, Rutnam ZJ, Yang W, Fang L, Luo L, Yang X, Li M, Deng Z, Qian J, Peng C and Yang BB. MicroRNA miR-98 inhibits tumor angiogenesis and invasion by targeting activin receptor-like kinase-4 and matrix metalloproteinase-11. Oncotarget. 2012; 3(11):1370-1385.
66. Yang X, Rutnam ZJ, Jiao C, Wei D, Xie Y, Du J, Zhong L and Yang BB. An anti-let-7 sponge decoys and decays endogenous let-7 functions. Cell Cycle. 2012; 11(16):3097-3108.
67. Jeyapalan Z, Deng Z, Shatseva T, Fang L, He C and Yang BB. Expression of CD44 3'-untranslated region regulates endogenous microRNA functions in tumorigenesis and angiogenesis. Nucleic acids research. 2011; 39(8):3026-3041.
68. Wang CH, Lee DY, Deng Z, Jeyapalan Z, Lee SC, Kahai S, Lu WY, Zhang Y and Yang BB. MicroRNA miR-328 regulates zonation morphogenesis by targeting CD44 expression. PLoS One. 2008; 3(6):e2420.
69. LaPierre DP, Lee DY, Li SZ, Xie YZ, Zhong L, Sheng W, Deng Z and Yang BB. The ability of versican to simultaneously cause apoptotic resistance and sensitivity. Cancer Res. 2007; 67(10):4742-4750.
70. Lee DY, Jeyapalan Z, Fang L, Yang J, Zhang Y, Yee AY, Li M, Du WW, Shatseva T and Yang BB. Expression of versican 3'-untranslated region modulates endogenous microRNA functions. PLoS One. 2010; 5(10):e13599.