Contribution of microRNAs to radio- and chemoresistance of brain tumors and their therapeutic potential

European Journal of Pharmacology

Volumn 684, Issue 1-3, 2012, Pages 8-18

  Chistiakov, Dimitry A ^a   Chekhonin, Vladimir P ^a,b  

^a PIROGOV RUSSIAN NATIONAL RESEARCH MEDICAL UNIVERSITY   (Russian Federation)

^b Serbsky State Research Center of Forensic and Social Psychiatry   (Russian Federation)

Author keywords

Cancer stem cell; Cancer therapy; Chemoresistance; Glioma; microRNA; Radioresistanse

Indexed keywords

ANTINEOPLASTIC AGENT; BEVACIZUMAB; CARBOPLATIN; CD33 ANTIGEN; CYTOCHROME P450 1B1; ETOPOSIDE; FLUOROURACIL; GEFITINIB; GLIAL FIBRILLARY ACIDIC PROTEIN; HYDROXYUREA; IMATINIB; IMMUNOLIPOSOME; KAEMPFEROL; MICRORNA; MICRORNA 100; MICRORNA 125B; MICRORNA 145; MICRORNA 21; MICRORNA 222; MYELIN PROTEIN; ONCOLYTIC HERPES VIRUS; PACLITAXEL; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; POLYAMIDOAMINE; POLYETHYLENEIMINE; POLYURETHAN; RESVERATROL; TEMOZOLOMIDE; TENIPOSIDE; UNINDEXED DRUG;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; BRAIN TUMOR; CANCER INHIBITION; CANCER INVASION; CANCER STEM CELL; CANCER SURVIVAL; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CHEMOSENSITIZATION; DRUG BINDING SITE; DRUG DELIVERY SYSTEM; DRUG DOSE ESCALATION; DRUG TARGETING; GENE EXPRESSION PROFILING; GLIOBLASTOMA; GLIOMA; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN SYNTHESIS INHIBITION; RADIATION EXPOSURE; RADIOSENSITIZATION; REVIEW; RNA PROCESSING; SUICIDE GENE THERAPY; TRANSCRIPTION REGULATION; TUMOR CELL; TUMOR GROWTH; UNSPECIFIED SIDE EFFECT; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MOLECULAR TARGETED THERAPY; RADIATION TOLERANCE;

EID: 84860836067     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2012.03.031     Document Type: Review

References (158)

1. K. Al-Nedawi, B. Meehan, and J. Rak Microvesicles: messengers and mediators of tumor progression Cell Cycle 8 2009 2014 2018
2. Y. An, and W.M. Ongkeko ABCG2: the key to chemoresistance in cancer stem cells? Oncol. Rep. 23 2010 997 1003
3. A.M. Anesti, G.R. Simpson, T. Price, H.S. Pandha, and R.S. Coffin Expression of RNA interference triggers from an oncolytic herpes simplex virus results in specific silencing in tumour cells in vitro and tumours in vivo BMC Cancer 10 2010 486
4. J.M. Angelastro, and M.W. Lamé Overexpression of CD133 promotes drug resistance in C6 glioma cells Mol. Cancer Res. 8 2010 1105 1115
5. M.A. Antonyak, B. Li, L.K. Boroughs, J.L. Johnson, J.E. Druso, K.L. Bryant, D.A. Holowka, and R.A. Cerione Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells Proc. Natl. Acad. Sci. U. S. A. 108 2011 4852 4857
6. K. Al-Nedawi, B. Meehan, J. Micallef, V. Lhotak, L. May, and A. Guha Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells Nat. Cell Biol. 10 2008 619 624 (Pubitemid 351627382)
7. K. Al-Nedawi, B. Meehan, and J. Rak Microvesicles: messengers and mediators of tumor progression Cell Cycle 8 2009 2014 2018
8. E. Aronica, J.A. Gorter, E.A. van Vliet, W.G. Spliet, C.W. van Veelen, and P.C. van Rijen Overexpression of the human major vault protein in gangliogliomas Epilepsia 44 2003 1166 1175 (Pubitemid 37100042)
9. S. Bao, Q. Wu, R.E. McLendon, Y. Hao, Q. Shi, A.B. Hjelmeland, M.W. Dewhirst, D.D. Bigner, and J.N. Rich Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 444 2006 756 760 (Pubitemid 44949604)
10. S. Bao, Q. Wu, S. Sathornsumetee, Y. Hao, Z. Li, A.B. Hjelmeland, Q. Shi, R.E. McLendon, D.D. Bigner, and J.N. Rich Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor Cancer Res. 66 2006 7843 7848 (Pubitemid 44299144)
11. S. Bao, Q. Wu, Z. Li, S. Sathornsumetee, H. Wang, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich Targeting cancer stem cells through L1CAM suppresses glioma growth Cancer Res. 68 2008 6043 6048
12. J.A. Barnett, D.L. Urbauer, G.I. Murray, G.N. Fuller, and A.B. Heimberger Cytochrome P450 1B1 expression in glial cell tumors: an immunotherapeutic target Clin. Cancer Res. 13 2007 3559 3567 (Pubitemid 46955116)
13. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
14. A. Ben-Baruch Site-specific metastasis formation: chemokines as regulators of tumor cell adhesion, motility and invasion Cell Adh. Migr. 3 2009 328 333
15. D. Beier, P. Hau, M. Proescholdt, A. Lohmeier, J. Wischhusen, P.J. Oefner, L. Aigner, A. Brawanski, U. Bogdahn, and C.P. Beier CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles Cancer Res. 67 2007 4010 4015 (Pubitemid 46815044)
16. D. Beier, J. Wischhusen, W. Dietmaier, P. Hau, M. Proescholdt, A. Brawanski, U. Bogdahn, and C.P. Beier CD133 expression and cancer stem cells predict prognosis in high-grade oligodendroglial tumors Brain Pathol. 18 2008 370 377 (Pubitemid 351782845)
17. W. Berger, S. Spiegl-Kreinecker, J. Buchroithner, L. Elbling, C. Pirker, J. Fischer, and M. Miksche Overexpression of the human major vault protein in astrocytic brain tumor cells Int. J. Cancer 94 2001 377 382 (Pubitemid 32906068)
18. M.P. Boldin, K.D. Taganov, D.S. Rao, L. Yang, J.L. Zhao, M. Kalwani, Y. Garcia-Flores, M. Luong, A. Devrekanli, J. Xu, G. Sun, J. Tay, P.S. Linsley, and D. Baltimore miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice J. Exp. Med. 208 2011 1189 1201
19. R.D. Bruno, and V.C. Njar Targeting cytochrome P450 enzymes: a new approach in anti-cancer drug development Bioorg. Med. Chem. 15 2007 5047 5060 (Pubitemid 46880385)
20. C. Calabrese, H. Poppleton, M. Kocak, T.L. Hogg, C. Fuller, B. Hamner, E.Y. Oh, M.W. Gaber, D. Finklestein, M. Allen, A. Frank, I.T. Bayazitov, and S.S. Zakharenko A perivascular niche for brain tumor stem cells Cancer Cell 11 2007 69 82 (Pubitemid 46054518)
21. Cancer Genome Atlas Research Network Comprehensive genomic characterization defines human glioblastoma genes and core pathways Nature 455 2008 1061 1068
22. S. Cascio, A. D'Andrea, R. Ferla, E. Surmacz, E. Gulotta, V. Amodeo, V. Bazan, N. Gebbia, and A. Russo miR-20b modulates VEGF expression by targeting HIF-1 alpha and STAT3 in MCF-7 breast cancer cells J. Cell. Physiol. 224 2010 242 249
23. M.A. Chaudhry, H. Sachdeva, and R.A. Omaruddin Radiation-induced micro-RNA modulation in glioblastoma cells differing in DNA-repair pathways DNA Cell Biol. 29 2010 553 561
24. G. Chen, W. Zhu, D. Shi, L. Lv, C. Zhang, P. Liu, and W. Hu MicroRNA-181a sensitizes human malignant glioma U87MG cells to radiation by targeting Bcl-2 Oncol. Rep. 23 2010 997 1003
25. T. Chen Overcoming drug resistance by regulating nuclear receptors Adv. Drug Deliv. Rev. 62 2010 1257 1264
26. J.X. Cheng, B.L. Liu, and X. Zhang How powerful is CD133 as a cancer stem cell marker in brain tumors? Cancer Treat. Rev. 35 2009 403 408
27. V.P. Chekhonin, O.I. Gurina, O.V. Ykhova, A.E. Ryabinina, E.A. Tsibulkina, and Y.A. Zhirkov Polyethylene glycol-conjugated immunoliposomes specific for olfactory ensheathing glial cells Bull. Exp. Biol. Med. 145 2008 449 451
28. V.P. Chekhonin, E.A. Tsibulkina, A.E. Ryabinina, Y.A. Zhirkov, E.A. Savchenko, and V.I. Shvets Immunoliposomal containers as systems of directed transport of minor interfering RNA into Schwann cells Bull. Exp. Biol. Med. 146 2008 451 454
29. V.P. Chekhonin, V.P. Baklaushev, G.M. Yusubalieva, and O.I. Gurina Targeted transport of 125I-labeled antibody to GFAP and AMVB1 in an experimental rat model of C6 glioma J. Neuroimmune Pharmacol. 4 2009 28 34
30. V.P. Chekhonin, V.P. Baklaushev, G.M. Yusubalieva, A.E. Belorusova, M.V. Gulyaev, E.B. Tsitrin, N.F. Grinenko, O.I. Gurina, and Y.A. Pirogov Targeted delivery of liposomal nanocontainers to the peritumoral zone of glioma by means of monoclonal antibodies against GFAP and the extracellular loop of Cx43 Nanomedicine 8 2012 63 70
31. S.A. Ciafré, S. Galardi, A. Mangiola, M. Ferracin, C.G. Liu, G. Sabatino, M. Negrini, G. Maira, C.M. Croce, and M.G. Farace Extensive modulation of a set of microRNAs in primary glioblastoma Biochem. Biophys. Res. Commun. 334 2005 1351 1358 (Pubitemid 41074723)
32. V. Clément, V. Dutoit, D. Marino, P.Y. Dietrich, and I. Radovanovic Limits of CD133 as a marker of glioma self-renewing cells Int. J. Cancer 125 2009 244 248
33. S. Dauchy, F. Dutheil, R.J. Weaver, F. Chassoux, C. Daumas-Duport, P.O. Couraud, J.M. Scherrmann, I. De Waziers, and X. Declèves ABC transporters, cytochromes P450 and their main transcription factors: expression at the human blood-brain barrier J. Neurochem. 107 2008 1518 1528
34. S. Davis, B. Lollo, S. Freier, and C. Esau Improved targeting of miRNA with antisense oligonucleotides Nucleic Acids Res. 34 2006 2294 2304 (Pubitemid 43985667)
35. C.E. De Kogel, and J.H.M. Schellenes Imatinib Oncologist 12 2007 1390 1394
36. J.L. Dembinski, E.L. Spaeth, J. Fueyo, C. Gomez-Manzano, M. Studeny, M. Andreeff, and F.C. Marini Reduction of nontarget infection and systemic toxicity by targeted delivery of conditionally replicating viruses transported in mesenchymal stem cells Cancer Gene Ther. 17 2010 289 297
37. M. Dey, I.V. Ulasov, and M.S. Lesniak Virotherapy against malignant glioma stem cells Cancer Lett. 289 2010 1 10
38. J. Ding, S. Huang, S. Wu, Y. Zhao, L. Liang, M. Yan, C. Ge, J. Yao, T. Chen, D. Wan, H. Wang, J. Gu, M. Yao, J. Li, H. Tu, and X. He Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA Nat. Cell Biol. 12 2010 390 399
39. P.B. Dirks Brain tumour stem cells: the undercurrents of human brain cancer and their relationship to neural stem cells Philos. Trans. R. Soc. Lond. B Biol. Sci. 363 2008 139 152 (Pubitemid 350174572)
40. G. Dresemann Imatinib (STI571) plus hydroxyurea: safety and efficacy in pre-treated, progressive glioblastoma multiforme (GBM) patients (pts) Proc. Am. Soc. Clin. Oncol. 23 2004 119
41. M.S. Ebert, J.R. Neilson, and P.A. Sharp MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells Nat. Methods 4 2007 721 726 (Pubitemid 47338166)
42. A. Eramo, L. Ricci-Vitiani, A. Zeuner, R. Pallini, F. Lotti, G. Sette, E. Pilozzi, C. Peschle, and R. De Maria Chemotherapy resistance of glioblastoma stem cells Cell Death Differ. 13 2006 1238 1241 (Pubitemid 43905604)
43. J. Felsberg, P.S. Yan, T.H. Huang, U. Milde, J. Schramm, O.D. Wiestler, G. Reifenberger, T. Pietsch, and A. Waha DNA methylation and allelic losses on chromosome arm 14q in oligodendroglial tumours Neuropathol. Appl. Neurobiol. 32 2006 517 524 (Pubitemid 44401513)
44. E. Ferretti, E. De Smaele, A. Po, L. Di Marcotullio, E. Tosi, M.S. Espinola, C. Di Rocco, R. Riccardi, F. Giangaspero, A. Farcomeni, I. Nofroni, P. Laneve, U. Gioia, E. Caffarelli, I. Bozzoni, I. Screpanti, and A. Gulino MicroRNA profiling in human medulloblastoma Int. J. Cancer 124 2009 568 577
45. C. Folkins, S. Man, P. Xu, Y. Shaked, D.J. Hicklin, and R.S. Kerbel Anticancer therapies combining antiangiogenic and tumor cell cytotoxic effects reduce the tumor stem-like cell fraction in glioma xenograft tumors Cancer Res. 67 2007 3560-3544
46. C. Folkins, Y. Shaked, S. Man, T. Tang, C.R. Lee, Z. Zhu, R.M. Hoffman, and R.S. Kerbel Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1 Cancer Res. 69 2009 7243 7251
47. N. Gagliano, F. Costa, C. Cossetti, L. Pettinari, R. Bassi, M. Chiriva-Internati, E. Cobos, M. Gioia, and S. Pluchino Glioma-astrocyte interaction modifies the astrocyte phenotype in a co-culture experimental model Oncol. Rep. 22 2009 1349 1356
48. H. Gal, G. Pandi, A.A. Kanner, Z. Ram, G. Lithwick-Yanai, N. Amariglio, G. Rechavi, and D. Givol MIR-451 and Imatinib mesylate inhibit tumor growth of glioblastoma stem cells Biochem. Biophys. Res. Commun. 376 2008 86 90
49. A.I. Garcia, M. Buisson, P. Bertrand, R. Rimokh, E. Rouleau, B.S. Lopez, R. Lidereau, I. Mikaélian, and S. Mazoyer Down-regulation of BRCA1 expression by miR-146a and miR-146b-5p in triple negative sporadic breast cancers EMBO Mol. Med. 3 2011 279 290
50. R. Galli, E. Binda, U. Orfanelli, B. Cipelletti, A. Gritti, S. De Vitis, R. Fiocco, C. Foroni, F. Dimeco, and A. Vescovi Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma Cancer Res. 64 2004 7011 7021 (Pubitemid 39331011)
51. J. Godlewski, H.B. Newton, E.A. Chiocca, and S.E. Lawler MicroRNAs and glioblastoma; the stem cell connection Cell Death Differ. 17 2010 221 228
52. P. González-Gómez, P. Sánchez, and H. Mira MicroRNAs as regulators of neural stem cell-related pathways in glioblastoma multiforme Mol. Neurobiol. 44 2011 235 249
53. M.W. Graner, O. Alzate, A.M. Dechkovskaia, J.D. Keene, J.H. Sampson, D.A. Mitchell, and D.D. Bigner Proteomic and immunologic analyses of brain tumor exosomes FASEB J. 23 2009 1541 1557
54. J.P. Hagan, and C.M. Croce MicroRNAs in carcinogenesis Cytogenet. Genome Res. 118 2007 252 259 (Pubitemid 350125264)
55. Z.Q. Han, M. Assenberg, B.L. Liu, Y.B. Wang, G. Simpson, S. Thomas, and R.S. Goffin Development of a second-generation oncolytic Herpes simplex virus expressing TNFalpha for cancer therapy J. Gene Med. 9 2007 99 106 (Pubitemid 46444487)
56. Haraguchi, T., Nakano, H., Tagawa, T., Ohki, T., Ueno, Y., Yoshida, T., Iba, H., in press. A potent 2′-O-methylated RNA-based microRNA inhibitor with unique secondary structures. Nucleic Acids Res. doi: 10.1093/nar/gkr1317.
57. J. Hardcastle, K. Kurozumi, N. Dmitrieva, M.P. Sayers, S. Ahmad, P. Waterman, R. Weissleder, E.A. Chiocca, and B. Kaur Enhanced antitumor efficacy of vasculostatin (Vstat120) expressing oncolytic HSV-1 Mol. Ther. 18 2010 285 294
58. J. He, Z. Shan, L. Li, F. Liu, Z. Liu, M. Song, and H. Zhu Expression of glioma stem cell marker CD133 and O6-methylguanine-DNA methyltransferase is associated with resistance to radiotherapy in gliomas Oncol. Rep. 26 2011 1305 1313
59. M. Herlevsen, G. Oxford, C. Ptak, J. Shabanowitz, D.F. Hunt, M. Conaway, and T. Theodorescu A novel model to identify interaction partners of the PTEN tumor suppressor gene in human bladder cancer Biochem. Biophys. Res. Commun. 352 2007 549 555 (Pubitemid 44838521)
60. A.B. Hjelmeland, Q. Wu, S. Wickman, C. Eyler, J. Heddleston, Q. Shi, J.D. Lathia, J. Macswords, J. Lee, R.E. McLendon, and J.N. Rich Targeting A20 decreases glioma stem cell survival and tumor growth PLoS Biol. 8 2010 e1000319
61. J. Hu, C. Jiang, H.K. Ng, J.C. Pang, and C.Y. Tong Chromosome 14q may harbor multiple tumor suppressor genes in primary glioblastoma multiforme Chin. Med. J. (Engl) 115 2002 1201 1204 (Pubitemid 34947343)
62. P.H. Huang, A.M. Xu, and F.M. White Oncogenic EGFR signaling networks in glioma Sci. Signal. 2 2009 re6
63. F.M. Iwamoto, K.R. Lamborn, J.G. Kuhn, P.Y. Wen, W.K. Yung, M.R. Gilbert, S.M. Chang, F.S. Lieberman, M.D. Prados, and H.A. Fine A phase I/II trial of the histone deacetylase inhibitor romidepsin for adults with recurrent malignant glioma: North American Brain Tumor Consortium Study 03-03 Neuro Oncol. 13 2011 509 516
64. F. Jafarifar, P. Yao, S.M. Eswarappa, and P.L. Fox Repression of VEGFA by CA-rich element-binding microRNAs is modulated by hnRNP L EMBO J. 30 2011 1324 1334
65. G. Jiang, Z.P. Wei, D.S. Pei, Y. Xin, Y.Q. Liu, and J.N. Zheng A novel approach to overcome temozolomide resistance in glioma and melanoma: inactivation of MGMT by gene therapy Biochem. Biophys. Res. Commun. 406 2011 311 314
66. F. Jin, L. Zhao, Y.J. Guo, W.J. Zhao, H. Zhang, H.T. Wang, T. Shao, S.L. Zhang, Y.J. Wei, J. Feng, X.B. Jiang, and H.Y. Zhao Influence of Etoposide on anti-apoptotic and multidrug resistance-associated protein genes in CD133 positive U251 glioblastoma stem-like cells Brain Res. 1336 2010 103 111
67. H. Kambara, H. Okano, E.A. Chiocca, and Y. Saeki An oncolytic HSV-1 mutant expressing ICP34.5 under control of a nestin promoter increases survival of animals even when symptomatic from a brain tumor Cancer Res. 65 2005 2832 2839 (Pubitemid 40490086)
68. M.K. Kang, and S.K. Kang Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma Stem Cells Dev. 16 2007 837 847
69. M. Katakowski, B. Buller, X. Wang, T. Rogers, and M. Chopp Functional microRNA is transferred between glioma cells Cancer Res. 70 2010 8259 8263
70. T. Kilic, J.A. Alberta, P.R. Zdunek, M. Acar, P. Iannarelli, T. O'Reilly, E. Buchdunger, P.M. Black, and C.D. Stiles Intracranial inhibition of platelet-derived growth factor-mediated glioblastoma cell growth by an orally active kinase inhibitor of the 2-phenylaminopyrimidine class Cancer Res. 60 2000 5143 5150
71. S.J. Kim, H. Uehara, S. Yazici, J.E. Busby, T. Nakamura, J. He, M. Maya, C. Logothetis, P. Mathew, X. Wang, K.A. Do, D. Fan, and I.J. Fidler Targeting platelet-derived growth factor receptor on endothelial cells of multidrug-resistant prostate cancer J. Natl. Cancer Inst. 98 2006 783 793 (Pubitemid 43983302)
72. E. Kirches, C. Scherlach, P. von Bossanyi, T. Schneider, R. Szibor, E. Kutz, M. Warich-Kirches, and K. Dietzmann MGMT- and P450 3A-inhibitors do not sensitize glioblastoma cell cultures against nitrosoureas Clin. Neuropathol. 18 1999 1 8 (Pubitemid 29039721)
73. B. Kefas, J. Godlewski, L. Comeau, Y. Li, R. Abounader, M. Hawkinson, J. Lee, H. Fine, E.A. Chiocca, S. Lawler, and B. Purow microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma Brain Res. 1236 2008 185 193
74. I. Lavon, D. Zrihan, A. Granit, O. Einstein, N. Fainstein, M.A. Cohen, M.A. Cohen, B. Zelikovitch, Y. Shoshan, S. Spektor, B.E. Reubinoff, Y. Felig, O. Gerlitz, T. Ben-Hur, Y. Smith, and T. Siegal Gliomas display a microRNA expression profile reminiscent of neural precursor cells Neuro Oncol. 12 2010 422 433
75. S. Lawler, and E.A. Chiocca Emerging functions of microRNAs in glioblastoma J. Neurooncol 92 2009 297 306
76. S.T. Lee, K. Chu, H.J. Oh, W.S. Im, J.Y. Lim, S.K. Kim, S.K. Kim, C.K. Park, K.H. Jung, S.K. Lee, M. Kim, and J.K. Roh Let-7 microRNA inhibits the proliferation of human glioblastoma cells DNA Cell Biol. 29 2010 553 561
77. K.M. Lee, E.J. Choi, and I.A. Kim microRNA-7 increases radiosensitivity of human cancer cells with activated EGFR-associated signaling Radiother. Oncol. 101 2011 171 176
78. Y. Li, W. Li, Y. Yang, Y. Lu, C. He, G. Hu, H. Liu, J. Chen, J. He, and H. Yu MicroRNA-21 targets LRRFIP1 and contributes to VM-26 resistance in glioblastoma multiforme Brain Res. 1286 2009 13 18
79. W.Q. Li, Y.M. Li, B.B. Tao, Y.C. Lu, G.H. Hu, H.M. Liu, Y. Xu, and H.Y. Yu Downregulation of ABCG2 expression in glioblastoma cancer stem cells with miRNA-328 may decrease their chemoresistance Med. Sci. Monit. 16 2010 HY27 HY30
80. Z. Li, S. Hu, J. Wang, J. Cai, L. Xiao, L. Yu, and Z. Wang MiR-27a modulates MDR1/P-glycoprotein expression by targeting HIPK2 in human ovarian cancer cells Gynecol. Oncol. 119 2010 125 130
81. X. Li, Y.Z. Pan, G.M. Seigel, Z.H. Hu, M. Huang, and A.M. Yu Breast cancer resistance protein BCRP/ABCG2 regulatory microRNAs (hsa-miR-328, -519c and -520h) and their differential expression in stem-like ABCG2 + cancer cells Biochem. Pharmacol. 81 2011 783 792
82. Y. Li, S. Zhao, Y. Zhen, Q. Li, L. Teng, A. Asai, and K. Kawamoto A miR-21 inhibitor enhances apoptosis and reduces G(2)-M accumulation induced by ionizing radiation in human glioblastoma U251 cells Brain Tumor Pathol. 28 2011 209 214
83. T.C. Liu, T. Zhang, H. Fukuhara, T. Kuroda, T. Todo, R.L. Martuza, S.D. Rabkin, and A. Kurtz Oncolytic HSV armed with platelet factor 4, an antiangiogenic agent, shows enhanced efficacy Mol. Ther. 14 2006 789 797 (Pubitemid 44752718)
84. G. Liu, X. Yuan, Z. Zeng, P. Tunici, H. Ng, I.R. Abdulkadir, L. Lu, D. Irvin, K.L. Black, and J.S. Yu Analysis of gene expression and chemoresistance of CD133 + cancer stem cells in glioblastoma Mol. Cancer 5 2006 67
85. L.Z. Liu, C. Li, Q. Chen, Y. Jing, R. Carpenter, Y. Jiang, H.F. Kung, L. Lai, and B.H. Jiang MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression PLoS One 6 2011 e19139
86. D.N. Louis, H. Ohgaki, O.D. Wiestler, W.K. Cavenee, P.C. Burger, A. Jouvet, B.W. Scheithauer, and P. Kleihues The 2007 WHO classification of tumors of the central nervous system Acta Neuropathol. 114 2007 97 109 (Pubitemid 47103521)
87. J.P. Lopez, J. Wang-Rodriguez, C. Chang, J.S. Chen, F.S. Pardo, J. Aguilera, and W.M. Ongkeko Gefitinib inhibition of drug resistance to doxorubicin by inactivating ABCG2 in thyroid cancer cell lines Arch. Otolaryngol. Head Neck Surg. 133 2007 1022 1027 (Pubitemid 47607585)
88. H. Lu, and D.J. Waxman Antitumor activity of methoxymorpholinyl doxorubicin: potentiation by cytochrome P450 3A metabolism Mol. Pharmacol. 67 2005 212 219 (Pubitemid 40069981)
89. C. Lu, and A. Shervington Chemoresistance in gliomas Mol. Cell. Biochem. 312 2008 71 80
90. J.M. Markert, P.G. Liechty, W. Wang, S. Gaston, E. Braz, M. Karrasch, L.B. Nabors, M. Markiewicz, A.D. Lakeman, C.A. Palmer, J.N. Parker, R.J. Whitley, and G.Y. Gillespie Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM Mol. Ther. 17 2007 199 207
91. A.M. McCord, M. Jamal, E.S. Williams, K. Camphausen, and P.J. Tofilon CD133 + glioblastoma stem-like cells are radiosensitive with a defective DNA damage response compared with established cell lines Clin. Cancer Res. 15 2009 5145 5153
92. G. Meister, M. Landthaler, Y. Dorsett, and T. Tuschl Sequence-specific inhibition of microRNA- and siRNA-induced RNA silencing RNA 10 2004 544 550 (Pubitemid 38241013)
93. J. Meister, and M.H. Schmidt miR-126 and miR-126*: new players in cancer ScientificWorldJournal 10 2010 2090 2100
94. T. Mohri, M. Nakajima, S. Takagi, S. Komagata, and T. Yokoi MicroRNA regulates human vitamin D receptor Int. J. Cancer 125 2009 1328 1333
95. J.J. Moser, and M.J. Fritzler The microRNA and messengerRNA profile of the RNA-induced silencing complex in human primary astrocyte and astrocytoma cells PLoS One 5 2010 e13445
96. E. Nakai, K. Park, T. Yawata, T. Chihara, A. Kumazawa, H. Nakabayashi, and K. Shimizu Enhanced MDR1 expression and chemoresistance of cancer stem cells derived from glioblastoma Cancer Invest. 27 2009 901 908
97. W.L. Ng, D. Yan, X. Zhang, Y.Y. Mo, and Y. Wang Over-expression of miR-100 is responsible for the low-expression of ATM in the human glioma cell line: M059J DNA Repair (Amst) 9 2010 1170 1175
98. O.M. Niemoeller, M. Niyazi, S. Corradini, F. Zehentmayr, M. Li, K. Lauber, and G. Belka MicroRNA expression profiles in human cancer cells after ionizing radiation Radiat. Oncol. 6 2011 29
99. A.T. Ogden, A.E. Waziri, R.A. Lochhead, D. Fusco, K. Lopez, J.A. Ellis, J. Kang, M. Assanah, G.M. McKhann, M.B. Sisiti, P.C. McCormicj, P. Canoll, and J.N. Bruce Identification of A2B5 + CD133-tumor-initiating cells in adult human gliomas Neurosurgery 62 2008 505 514 (Pubitemid 351489297)
100. N. Oka, A. Soeda, A. Inagaki, M. Onodera, H. Maruyama, A. Hara, T. Kunisada, H. Mori, and T. Iwama VEGF promotes tumorigenesis and angiogenesis of human glioblastoma stem cells Biochem. Biophys. Res. Commun. 360 2007 553 559 (Pubitemid 47048135)
101. N. Oka, A. Soeda, S. Noda, and T. Iwama Brain tumor stem cell from an adenoid glioblastoma multiforme Neurol. Med. Chir. 49 2009 146 151
102. Y.Z. Pan, W. Gao, and A.M. Yu MicroRNAs regulate CYP3A4 expression via direct and indirect targeting Drug Metab. Dispos. 37 2009 2112 2127
103. Y.Z. Pan, M.E. Morris, and A.M. Yu MicroRNA-328 negatively regulates the expression of breast cancer resistance protein (BCRP/ABCG2) in human cancer cells Mol. Pharmacol. 75 2009 1374 1379
104. T. Papagiannakopoulos, A. Shapiro, and K.S. Kosik MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells Cancer Res. 68 2008 8164 8172
105. L.H. Patterson, and G.I. Murray Tumour cytochrome P450 and drug activation Curr. Pharm. Des. 8 2002 1335 1347 (Pubitemid 34591350)
106. M. Pradhan, L.A. Bembinster, S.C. Baumgarten, and J. Frasor Proinflammatory cytokines enhance estrogen-dependent expression of the multidrug transporter gene ABCG2 through estrogen receptor and NF{kappa}B cooperativity at adjacent response elements J. Biol. Chem. 285 2010 31100 31106
107. S. Prasad, J. Ravindran, and B.B. Aggarwal NF-kappaB and cancer: how intimate is this relationship Mol. Cell. Biochem. 336 2010 25 37
108. J. Qi, J.Y. Yu, H.R. Shcherbata, J. Mathieu, A.J. Wang, S. Seal, W. Zhou, B.M. Stadler, D. Bourgin, L. Wang, A. Nelson, C. Ware, C. Raymond, L.P. Lim, J. Magnus, I. Ivanovska, R. Diaz, A. Ball, M.A. Cleary, and H. Ruohola-Baker MicroRNAs regulate human embryonic stem cell division Cell Cycle 8 2009 3729 3741
109. W. Qin, Y. Shi, B. Zhao, C. Yao, L. Jin, J. Ma, and Y. Jin miR-24 regulates apoptosis by targeting the open reading frame (ORF) region of FAF1 in cancer cells PLoS One 5 2010 e9429
110. S.A. Rao, V. Santosh, and K. Somasundaram Genome-wide expression profiling identifies deregulated miRNAs in malignant astrocytoma Mod. Pathol. 23 2010 1404 1417
111. E. Raymond, A.A. Brandes, C. Dittrich, P. Fumoleau, B. Coudert, P.M.J. Clement, M. Frenay, R. Rampling, R. Stupp, J.M. Kros, M.C. Heinrich, T. Gorlia, D. Lacombe, and M.J. van den Bent Phase II study of imatinib in patients with recurrent gliomas of various histologies: a European Organisation for Research and Treatment of Cancer Brain Tumor Group Study J. Clin. Oncol. 26 2008 4659 4665
112. D.A. Reardon, M.J. Egorin, J.A. Quinn, J.N. Rich Sr., I. Gururangan, J.J. Vredenburgh, A. Desjardins, S. Sathornsumetee, J.M. Provenzale, J.E. Herndon II, J.M. Dowell, M.A. Badruddoja, R.E. McLendon, T.F. Lagattuta, K.P. Kicielinski, K. Dresemann, J.H. Sampson, A.H. Friedman, A.J. Salvado, and H.S. Friedman Phase II study of imatinib mesylate plus hydroxyurea in adults with recurrent glioblastoma multiforme J. Clin. Oncol. 23 2005 9359 9368
113. J. Rebetz, D. Tian, A. Persson, B. Widegren, L.G. Salford, E. Englund, and X. Fan Glial progenitor-like phenotype in low-grade glioma and enhanced CD133-expression and neuronal lineage differentiation potential in high-grade glioma PLoS One 3 2008 e1936
114. Y. Ren, C.S. Kang, X.B. Yuan, X. Zhou, P. Xu, L. Han, G.X. Wang, Z. Jia, Y. Zhong, S. Yu, J. Sheng, and P.Y. Pu 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 2010 303 314
115. Y. Ren, X. Zhou, M. Mei, X.B. Yuan, L. Han, G.X. Wang, Z.F. Jia, P. Xu, P.Y. Pu, and C.S. Kang MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol BMC Cancer 10 2010 27
116. M. Ropolo, A. Daga, F. Griffero, M. Foresta, G. Casartelli, A. Zunino, A. Poggi, E. Cappelli, G. Zona, R. Spaziante, G. Corte, and G. Frosina Comparative analysis of DNA repair in stem and nonstem glioma cell cultures Mol. Cancer Res. 7 2009 383 392
117. A. Salmaggi, A. Boiardi, M. Gelati, A. Russo, C. Calatozzolo, E. Ciusani, F.L. Sciacca, A. Ottolina, E.A. Parati, C. La Porta, G. Alessandri, C. Marras, D. Croci, and M. De Rossi Glioblastoma derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype Glia 54 2006 850 860 (Pubitemid 44671990)
118. J. Sana, M. Hajduch, J. Michalek, R. Vyzula, and O. Slaby MicroRNAs and glioblastoma: roles in core signalling pathways and potential clinical implications Cell Mol. Med. 15 2011 1636 1644
119. M. Scherr, L. Venturini, K. Battmer, M. Schaller-Schoenitz, D. Schaefer, I. Dallmann, A. Ganser, and M. Eder Lentivirus-mediated antagomir expression for specific inhibition of miRNA function Nucleic Acids Res. 35 2007 e149
120. A. Schulte, H.S. Günther, H.S. Phillips, D. Kemming, T. Martens, S. Kharbanda, R.H. Soriano, Z. Modrusan, S. Zapf, M. Westphal, and K. Lamszus A distinct subset of glioma cell lines with stem cell-like properties reflects the transcriptional phenotype of glioblastomas and overexpresses CXCR4 as therapeutic target Glia 59 2011 590 602
121. Q. Shen, Y. Wang, E. Kokovay, G. Lin, S.M. Chuang, S.K. Goderie, B. Roysam, and S. Temple Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions Cell Stem Cell 3 2008 289 300
122. T. Shen, Y.H. Kuang, C.R. Ashby, Y. Lei, A. Chen, Y. Zhou, X. Chen, A.K. Tiwari, E. Hopper-Borge, J. Ouyang, and Z.S. Chen Imatinib and nilotinib reverse multidrug resistance in cancer cells by inhibiting the efflux activity of the MRP7 (ABCC10) PLoS One 4 2009 e7520 e
123. A. Shervington, and C. Lu Expression of multidrug resistance genes in normal and cancer stem cells Cancer Invest. 26 2008 535 542 (Pubitemid 351892589)
124. L. Shi, Z. Cheng, J. Zhang, R. Li, P. Zhao, Z. Fu, and Y. You hsa-mir-181a and hsa-mir-181b function as tumor suppressors in human glioma cells Brain Res. 1236 2008 185 193
125. L. Shi, J. Chen, J. Yang, T. Pan, S. Zhang, and Z. Wang MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax/Bcl-2 ratio and caspase-3 activity Brain Res. 1352 2010 255 264
126. L. Shi, S. Zhang, K. Feng, F. Wu, Y. Wan, Z. Wang, J. Zhang, Y. Wang, W. Yan, Z. Fu, and Y. You MicroRNA-125b-2 confers human glioblastoma stem cells resistance to temozolomide through the mitochondrial pathway of apoptosis Int. J. Oncol. 40 2012 119 129
127. T. Shimada, and Y. Fujii-Kuriyama Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1 Cancer Sci. 95 2004 1 6 (Pubitemid 38208399)
128. S.K. Singh, C. Hawkins, I.D. Clarke, J.A. Squire, J. Bayani, T. Hide, R.M. Henkelman, M.D. Cusimano, and P.B. Dirks Identification of human brain tumour initiating cells Nature 432 2004 396 401 (Pubitemid 39551674)
129. J. Skog, T. Würdinger, S. van Rijn, D.H. Meijer, L. Gainche, M. Sena-Esteves, W.T. Curry Jr., B.S. Carter, A.M. Krichevsky, and X.O. Breakefield Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers Nat. Cell Biol. 10 2008 1470 1476
130. A.M. Sonabend, I.V. Ulasov, M.A. Tyler, A.A. Rivera, J.M. Mathis, and M.S. Lesniak Mesenchymal stem cells effectively deliver an oncolytic adenovirus to intracranial glioma Stem Cells 26 2008 831 841
131. R. Stupp, W.P. Mason, M.J. van den Bent, M. Weller, B. Fisher, M.J. Taphoorn, K. Belanger, A.A. Brandes, C. Marosi, U. Bogdahn, J. Curschmann, R.C. Janzer, S.K. Ludwin, T. Gorlia, A. Allgeier, D. Lacombe, J.G. Cairncross, E. Eisenhauer, and R.O. Mirimanoff Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma N. Engl. J. Med. 352 2005 987 996 (Pubitemid 40349501)
132. M.L. Suvà, N. Riggi, M. Janiszewska, I. Radovanovic, P. Provero, J.C. Stehle, K. Baumer, M.A. Le Bitoux, D. Marino, L. Cironi, V.E. Marquez, V. Clément, and I. Stamenkovic EZH2 is essential for glioblastoma cancer stem cell maintenance Cancer Res. 69 2009 9211 9218
133. S. Takagi, M. Nakajima, T. Mohri, and T. Yokoi Post-transcriptional regulation of human pregnane X receptor by micro-RNA affects the expression of cytochrome P450 3A4 J. Biol. Chem. 283 2008 9674 9680
134. N. Thon, K. Damianoff, J. Hegermann, S. Grau, B. Krebs, O. Schnell, J.C. Tonn, and R. Goldbrunner Presence of pluripotent CD133 + cell correlates with malignancy of gliomas Mol. Cell. Neurosci. 43 2010 51 59
135. S. Tian, S. Huang, S. Wu, W. Guo, J. Li, and X. He MicroRNA-1285 inhibits the expression of p53 by directly targeting its 3′ untranslated region Biochem. Biophys. Res. Commun. 396 2010 435 439
136. C. Tomuleasa, O. Soritau, D. Rus-Ciuca, H. Ioani, S. Susman, M. Petrescu, T. Timis, D. Cernea, G. Kacso, A. Irimie, and I.S. Florian Functional and molecular characterization of glioblastoma multiforme-derived cancer stem cells J. BUON 15 2010 583 591
137. K.K. To, R.W. Robey, T. Knutsen, Z. Zhan, T. Ried, and S.E. Bates Escape from hsa-miR-519c enables drug-resistant cells to maintain high expression of ABCG2 Mol. Cancer Ther. 8 2009 2959 2968
138. Y. Tsuchiya, M. Nakajima, S. Takagi, T. Taniya, and T. Yokoi MicroRNA regulates the expression of human cytochrome P450 1B1 Cancer Res. 66 2006 9090 9098 (Pubitemid 44521128)
139. J.D. Turner, R. Williamson, K.K. Almefty, P. Nakaji, R. Porter, V. Tse, and M.Y. Kalani The many roles of microRNAs in brain tumor biology Neurosurg. Focus 28 2010 E3
140. E. Turrini, S. Haenisch, S. Laechelt, T. Diewock, O. Bruhn, and I. Cascorbi MicroRNA profiling in K-562 cells under imatinib treatment: influence of miR-212 and miR-328 on ABCG2 expression Pharmacogenet. Genomics 22 2012 198 205
141. K. Ujifuku, N. Mitsutake, S. Takakura, M. Matsuse, V. Saenko, K. Suzuki, K. Hayashi, T. Matsuo, K. Kamada, I. Nagata, and S. Yamashita miR-195, miR-455-3p and miR-10a (*) are implicated in acquired temozolomide resistance in glioblastoma multiforme cells Cancer Lett. 296 2010 241 248
142. B.L. Urquhart, R.G. Tirona, and R.B. Kim Nuclear receptors and the regulation of drug-metabolizing enzymes and drug transporters: implications for interindividual variability in response to drugs J. Clin. Pharmacol. 47 2007 566 578 (Pubitemid 46632158)
143. V. Valiunas, Y.Y. Polosina, H. Miller, I.A. Potapova, L. Valiuniene, S. Doronin, R.T. Mathias, R.B. Robinson, M.R. Rosen, I.S. Cohen, and P.R. Brink Connexin-specific cell-to-cell transfer of short interfering RNA by gap junctions J. Physiol. 568 2005 459 468 (Pubitemid 41555451)
144. J. Wang, H. Wang, Z. Li, Q. Wu, J.D. Lathia, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich c-Myc is required for maintenance of glioma cancer stem cells PLoS One 3 2008 e3769
145. F. Wang, X. Xue, J. Wei, Y. An, J. Yao, H. Cai, J. Wu, C. Dai, Z. Qian, Z. Xu, and Y. Miao hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations Br. J. Cancer 103 2010 567 574
146. P. Wang, J. Rao, H. Yang, H. Zhao, and L. Yang PPM1D silencing by lentiviral-mediated RNA interference inhibits proliferation and invasion of human glioma cells J. Huazhong Univ. Sci. Technolog. Med. Sci. 31 2011 94 99
147. H. Wang, J.F. Yamamoto, C. Caberto, B. Saltzman, R. Decker, T.M. Vogt, L. Yokochi, S. Chanock, L.R. Wilkens, and L. Le Marchand Genetic variation in the bioactivation pathway for polycyclic hydrocarbons and heterocyclic amines in relation to risk of colorectal neoplasia Carcinogenesis 32 2011 203 209
148. C. Wild-Bode, M. Weller, A. Rimner, J. Dichgans, and W. Wick Sublethal irradiation promotes migration and invasiveness of glioma cells: implications for radiotherapy of human glioblastoma Cancer Res. 61 2001 2744 2750 (Pubitemid 32685864)
149. M.L. Wu, H. Li, D.C. Wu, X.W. Wang, X.Y. Chen, Q.Y. Kong, J.X. Ma, Y. Gao, and J. Liu CYP1A1 and CYP1B1 expressions in medulloblastoma cells are AhR-independent and have no direct link with resveratrol-induced differentiation and apoptosis Neurosci. Lett. 384 2007 33 37 (Pubitemid 40826613)
150. C. Wu, J. Lin, M. Hong, Y. Choudhury, P. Balani, D. Leung, L.H. Dang, Y. Zhao, J. Zeng, and S. Wang Combinatorial control of suicide gene expression by tissue-specific promoter and microRNA regulation for cancer therapy Mol. Ther. 17 2009 2058 2066
151. T. Würdinger, B.A. Tannous, O. Saydam, J. Skog, S. Grau, J. Soutschek, R. Weissleder, X.O. Breakefield, and A.M. Krichevsky miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells Cancer Cell 14 2008 382 393
152. W. Yang, D.Y. Lee, and Y. Ben-David The roles of microRNAs in tumorigenesis and angiogenesis Int. J. Physiol. Pathophysiol. Pharmacol. 3 2011 140 155
153. Y.P. Yang, Y. Chien, G.Y. Chiou, J.Y. Cherng, M.L. Wang, W.L. Lo, Y.L. Chang, P.I. Huang, Y.W. Chen, Y.H. Shih, M.T. Chen, and S.H. Chiou Inhibition of cancer stem cell-like properties and reduced chemoradioresistance of glioblastoma Biomaterials 33 2012 1462 1476
154. R.L. Yong, N. Shinojima, J. Fueyo, J. Gumin, G.G. Vecil, and F.C. Marini Human bone marrow-derived mesenchymal stem cells for intravascular delivery of oncolytic adenovirus Delta24-RGD to human gliomas Cancer Res. 69 2009 8932 8940
155. M. Zhang, T. Song, L. Yang, R. Chen, L. Wu, Z. Yang, and J. Fang Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients J. Exp. Clin. Cancer Res. 27 2008 85
156. C. Zhang, G. Wang, C. Kang, Y. Du, and P. Pu Up-regulation of p27(kip1) by miR-221/222 antisense oligonucleotides enhances the radiosensitivity of U251 glioblastoma Zhonghua Yi Xue Yi Chuan Xue Za Zhi 26 2009 634 638 (Article in Chinese)
157. X. Zhou, J. Zhang, Q. Jia, Y. Ren, Y. Wang, L. Shi, N. Liu, G. Wang, P. Pu, Y. You, and C. Kang Reduction of miR-21 induces glioma cell apoptosis via activating caspases 9 and 3 Oncol. Rep. 24 2010 195 201
158. H. Zhu, H. Wu, X. Liu, B.R. Evans, D.J. Medina, C.G. Liu, and Y.M. Yang Role of microRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells Biochem. Pharmacol. 76 2008 582 588