Combination treatment with doxorubicin and microRNA-21 inhibitor synergistically augments anticancer activity through upregulation of tumor suppressing genes

International Journal of Oncology

Volumn 46, Issue 4, 2015, Pages 1589-1600

  Zhang, Shanshan ^a   Han, Lei ^b,c,d   Wei, Jianwei ^b,c,d   Shi, Zhendong ^b,c,d   Pu, Peiyu ^b,c,d   Zhang, Jianning ^b,c,d   Yuan, Xubo ^a   Kang, Chunsheng ^b,c,d  

^a TIANJIN UNIVERSITY   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^d Chinese Glioma Cooperative Group (CGCG)   (China)

Author keywords

Co treatment; DNA methyltransferase 1; Doxorubicin; Glioblastoma; microRNA 21; Tumor suppressor genes

Indexed keywords

ANTINEOPLASTIC AGENT; DNA METHYLTRANSFERASE 1; DOXORUBICIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MICRORNA 21 INHIBITOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN P21; RECK PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; VON HIPPEL LINDAU PROTEIN; ANTINEOPLASTIC ANTIBIOTIC; MICRORNA; MIRN21 MICRORNA, HUMAN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CELL PROLIFERATION; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; GENE EXPRESSION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; METASTASIS; PRIORITY JOURNAL; TUMOR CELL; TUMOR INVASION; TUMOR SUPPRESSOR GENE; UPREGULATION; ANTAGONISTS AND INHIBITORS; BRAIN NEOPLASMS; CELL MOTION; DRUG EFFECTS; DRUG POTENTIATION; GENE EXPRESSION REGULATION; GENETICS; TUMOR CELL LINE;

ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DOXORUBICIN; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; GLIOBLASTOMA; HUMANS; MICRORNAS; UP-REGULATION;

EID: 84923095860     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.2841     Document Type: Article

References (58)

1. WILSON TA, KARAJANNIS MA and HARTER DH: Glioblastoma multi-forme: State of the art and future therapeutics. Surg Neurol Int 5: 64, 2014.
2. HANDE KR: Clinical applications of Anticancer drugs targeted to topoisomerase II. Biochim Biophys Acta 1400: 173-184, 1998.
3. SWIFT L P, REPHAELI A, NUDELMAN A, PHILLIPS DR and CUTTS SM: Doxorubicin-DNA adducts induce a non-topoisomerase II-mediated form of Cell death. Cancer Res 66: 4863-4871, 2006.
4. HANAFY FM, SALEM T, EL-AZIZ, A, EL-FIKY B and SHOKAIR M: Infuence of Anticancer drugs on DNA methylation in liver of female mice. Am J Mol Biol 1: 62-69, 2011.
5. YU J, ZHANG H, GU J, et al: Methylation profles of thirty four promoter-CpG islands and concordant methylation behaviours of sixteen genes that may contribute to Carcinogenesis of astrocy-toma. BMC Cancer 4: 65, 2004.
6. HORIGUCHI K, TOMIZAWA Y, TOSAKA M, et al: Epigenetic inactiva-tion of RASSF1A candidate tumor suppressor Gene at 3p21.3 in brain tumors. Oncogene 22: 7862-7865, 2003.
7. WIENCKE JK, ZHENG S, JELLUMA N, et al: Methylation of the PTEN promoter defnes low-grade gliomas and secondary glioblastoma. Neuro Oncol 9: 271-279, 2007.
8. CANKOVIC M, MIKKELSEN T, ROSENBLUM ML and ZARBO RJ: A simplified laboratory validated assay for MGMT promoter hypermethylation analysis of glioma specimens from formalin-fxed paraffn-embedded tissue. Lab Invest 87: 392-397, 2007.
9. BIRD A: DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21, 2002.
10. VIJAYARAGHAVALU S and LABHASETWAR V: Effcacy of decitabine-loaded nanogels in overcoming Cancer drug resistance is mediated via sustained DNA methyltransferase 1 (DNMT1) depletion. Cancer Lett 331: 122-129, 2013.
11. ROBERT MF, MORIN S, BEAULIEU N, et al: DNMT1 is required to maintain CpG methylation and aberrant Gene silencing in human Cancer cells. Nat Genet 33: 61-65, 2003.
12. ZHOU W, CHEN H, HONG X, NIU X and LU Q: Knockdown of DNA methyltransferase-1 inhibits proliferation and derepresses tumor suppressor genes in myeloma cells. Oncol Lett 8: 2130-2134, 2014.
13. YOKOCHI T and ROBERTSON KD: Doxorubicin inhibits DNMT1, resulting in conditional apoptosis. Mol Pharmacol 66: 1415-1420, 2004.
14. FARAZI TA, SPITZER JI, MOROZOV P and TUSCHL T: Mirnas in human cancer. J Pathol 223: 102-115, 2011.
15. GAUR AB, HOLBECK SL, COLBURN NH and ISRAEL MA: Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro Oncol 13: 580-590, 2011.
16. ZIYAN W, SHUHUA Y, XIUFANG W and XIAOYUN L: MicroRNA-21 is involved in osteosarcoma Cell invasion and migration. Med Oncol 28: 1469-1474, 2011.
17. KIM N, KIM H, JUNG I, KIM Y, KIM D and HAN YM: Expression profles of miRNAs in human embryonic stem cells during hepa-tocyte differentiation. Hepatol Res 41: 170-183, 2011.
18. GABRIELY G, WURDINGER T, KESARI S, et al: MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28: 5369-5380, 2008.
19. CHAN JA, KRICHEVSKY AM and KOSIK KS: MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65: 6029-6033, 2005.
20. QIU LY and BAE YH: Self-assembled polyethylenimine-graft-polyb(epsilon-caprolactone) micelles as potential dual carriers of genes and Anticancer drugs. Biomaterials 28: 4132-4142, 2007.
21. CHENG D, CAO N, CHEN J, YU X and SHUAI X: Multifunctional nanocarrier mediated co-delivery of doxorubicin and siRNA for synergistic enhancement of glioma apoptosis in rat. Biomaterials 33: 1170-1179, 2012.
22. JIN W, WU L, LIANG K, LIU B, LU Y and FAN Z: Roles of the PI-3K and MEK pathways in Ras-mediated chemoresistance in breast Cancer cells. Br J Cancer 89: 185-191, 2003.
23. LI B, LI J, XU WW, et al: Suppression of esophageal tumor growth and chemoresistance by directly targeting the PI3K/AKT pathway. Oncotarget 5: 11576-115872014.
24. OKI E, BABA H, TOKUNAGA E, et al: Akt phosphorylation associates with LOH of PTEN and leads to chemoresistance for gastric cancer. Int J Cancer 117: 376-380, 2005.
25. CHOE G, HORVATH S, CLOUGHESY T F, et al: Analysis of the phos-phatidylinositol 3'-kinase signaling pathway in glioblastoma patients in vivo. Cancer Res 63: 2742-2746, 2003.
26. HUANG PH, MUKASA A, BONAVIA R, et al: Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc Natl Acad Sci USA 104: 12867-12872, 2007.
27. MARTINEZ R and ESTELLER M: The DNA methylome of glioblas-toma multiforme. Neurobiol Dis 39: 40-46, 2010.
28. DAVALOS V, MOUTINHO C, VILLANUEVA A, et al: Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis. Oncogene 31: 2062-2074, 2012.
29. WANG XF, SHI ZM, WANG XR, et al: MiR-181d acts as a tumor suppressor in glioma by targeting K-ras and Bcl-2. J Cancer Res Clin Oncol 138: 573-584, 2012.
30. SHI ZD, QIAN XM, ZHANG JX, et al: BASI, a potent small molecular inhibitor, inhibits glioblastoma progression by targeting microRNA-mediated beta-catenin signaling. CNS Neurosci Ther 20: 830-839, 2014.
31. BARTEL DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297, 2004.
32. CONG N, DU P, ZHANG A, et al: Downregulated microRNA-200a promotes EMT and tumor growth through the wnt/beta-catenin pathway by targeting the E-cadherin repressors ZEB1/ZEB2 in gastric adenocarcinoma. Oncol Rep 29: 1579-1587, 2013.
33. SU J, ZHANG A, SHI Z, et al: MicroRNA-200a suppresses the Wnt/beta-catenin signaling pathway by interacting with beta-catenin. Int J Oncol 40: 1162-1170, 2012.
34. KULIS M and ESTELLER M: DNA methylation and cancer. Adv Genet 70: 27-56, 2010.
35. BAYLIN SB and HERMAN JG: DNA hypermethylation in tumorigen-esis: Epigenetics joins genetics. Trends Genet 16: 168-174, 2000.
36. KATO K, LONG NK, MAKITA H, et al: Effects of green tea poly-phenol on methylation status of RECK Gene and Cancer Cell invasion in Oral squamous Cell carcinoma cells. Br J Cancer 99: 647-654, 2008.
37. LOPEZ-SERRA P and ESTELLER M: DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene 31: 1609-1622, 2012.
38. ALAKHOVA DY, ZHAO Y, LI S and KABANOV AV: Effect of doxoru-bicin/pluronic SP1049C on tumorigenicity, aggressiveness, DNA methylation and stem Cell markers in murine leukemia. PLoS One 8: E72238, 2013.
39. MUTZE K, LANGER R, SCHUMACHER F, et al: DNA methyltrans-ferase 1 as a predictive biomarker and potential therapeutic target for chemotherapy in gastric cancer. Eur J Cancer 47: 1817-1825, 2011.
40. CLEMENTS EG, MOHAMMAD H P, LEADEM BR, et al: DNMT1 modulates Gene expression without its catalytic activity partially through its interactions with histone-modifying enzymes. Nucleic Acids Res 40: 4334-4346, 2012.
41. NASONKIN IO, MERBS SL, LAZO K, et al: Conditional knockdown of DNA methyltransferase 1 reveals a key role of retinal pigment epithelium integrity in photoreceptor outer segment morphogenesis. Development 140: 1330-1341, 2013.
42. XU M, GAO J, DU YQ, et al: Reduction of pancreatic Cancer Cell viability and induction of apoptosis mediated by siRNA targeting DNMT1 through suppression of total DNA methyltransferase activity. Mol Med Rep 3: 699-704, 2010.
43. KUNDAKOVIC M, CHEN Y, COSTA E and GRAYSON DR: DNA methyl-transferase inhibitors coordinately induce expression of the human reelin and glutamic acid decarboxylase 67 genes. Mol Pharmacol 71: 644-653, 2007.
44. MORTUSEWICZ O, SCHERMELLEH L, WALTER J, CARDOSO MC and LEONHARDT H: Recruitment of DNA methyltransferase I to DNA repair sites. Proc Natl Acad Sci USA 102: 8905-8909, 2005.
45. RAJENDRAN G, SHANMUGANANDAM K, BENDRE A, MUZUMDAR D, GOEL A and SHIRAS A: Epigenetic regulation of DNA methyltrans-ferases: DNMT1 and DNMT3B in gliomas. J Neurooncol 104: 483-494, 2011.
46. LUJAMBIO A, ROPERO S, BALLESTAR E, et al: Genetic unmasking of an epigenetically silenced microRNA in human Cancer cells. Cancer Res 67: 1424-1429, 2007.
47. BADER AG, BROWN D and WINKLER M: The promise of microRNA replacement therapy. Cancer Res 70: 7027-7030, 2010.
48. GAO W, SHEN H, LIU L, XU J, XU J and SHU Y: MiR-21 over-expression in human primary squamous Cell lung carcinoma is associated with poor patient prognosis. J Cancer Res Clin Oncol 137: 557-566, 2011.
49. LAKOMY R, SANA J, HANKEOVA S, et al: MiR-195, miR-196b, miR-181c, miR-21 expression levels and O-6-methylguanine-DNA methyltransferase methylation status are associated with clinical outcome in glioblastoma patients. Cancer Sci 102: 2186-2190, 2011.
50. SHI Z, ZHANG J, QIAN X, et al: AC1MMYR2, an inhibitor of dicer-mediated biogenesis of Oncomir miR-21, reverses epithe-lial-mesenchymal transition and suppresses tumor growth and progression. Cancer Res 73: 5519-5531, 2013.
51. HAN L, YUE X, ZHOU X, et al: MicroRNA-21 expression is regulated by beta-catenin/STAT3 pathway and promotes glioma Cell invasion by direct targeting RECK. CNS Neurosci Ther 18: 573-583, 2012.
52. ZHANG KL, HAN L, CHEN LY, et al: Blockage of a miR-21/EGFR regulatory feedback loop augments anti-EGFR therapy in glio-blastomas. Cancer Lett 342: 139-149, 2014.
53. REN Y, ZHOU X, MEI M, et al: MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol. BMC Cancer 10: 27, 2010.
54. REN Y, KANG CS, YUAN XB, et al: Co-delivery of as-miR-21 and 5-FU by poly(amidoamine) dendrimer attenuates human glioma Cell growth in vitro. J Biomater Sci Polym Ed 21: 303-314, 2010.
55. QIAN X, REN Y, SHI Z, et al: Sequence-dependent synergistic inhibition of human glioma Cell lines by combined temozolomide and miR-21 inhibitor Gene therapy. Mol Pharm 9: 2636-2645, 2012.
56. THIERY J P, ACLOQUE H, HUANG RY and NIETO MA: Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890, 2009.
57. ZAVADIL J, NARASIMHAN M, BLUMENBERG M and SCHNEIDER RJ: Transforming growth factor-beta and microRNA: Mrna regulatory networks in epithelial plasticity. Cells Tissues Organs 185: 157-161, 2007.
58. HAN L, YANG Y, YUE X, et al: Inactivation of PI3K/AKT signaling inhibits glioma Cell growth through modulation of beta-catenin-mediated transcription. Brain Res 1366: 9-17, 2010.