Current progress for the use of miRNAs in glioblastoma treatment

Molecular Neurobiology

Volumn 48, Issue 3, 2013, Pages 757-768

  Tivnan, Amanda ^a   McDonald, Kerrie Leanne ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Glioblastoma; In vivo; MicroRNA; Treatment

Indexed keywords

CISPLATIN; MICRORNA; MICRORNA 101; MICRORNA 10B; MICRORNA 146A; MICRORNA 26A; MICRORNA 34A; MIRAVIRSEN; PACLITAXEL; TEMOZOLOMIDE;

APOPTOSIS; BLOOD BRAIN BARRIER; CANCER GROWTH; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER RESISTANCE; CELL MIGRATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM DISEASE; CHEMOSENSITIVITY; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENE TARGETING; GLIOBLASTOMA; HUMAN; MICROARRAY ANALYSIS; NERVE CELL DIFFERENTIATION; REVIEW; RNA INTERFERENCE; SUICIDE GENE THERAPY; SURVIVAL RATE;

BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; DRUG RESISTANCE, NEOPLASM; GLIOBLASTOMA; HUMANS; MICRORNAS;

EID: 84888015789     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8464-0     Document Type: Review

References (144)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97-109. doi: 10.1007/s00401-007-0243-4
2. Fuller GN (2008) The WHO classification of tumours of the central nervous system, 4th edition. Arch Pathol Lab Med 132(6):906. doi: 10.1043/1543-2165
3. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987-996. doi: 10.1056/NEJMoa043330
4. Monticone M, Daga A, Candiani S, Romeo F, Mirisola V, Viaggi S, Melloni I, Pedemonte S, Zona G, Giaretti W, Pfeffer U, Castagnola P (2012) Identification of a novel set of genes reflecting different in vivo invasive patterns of human GBM cells. BMC cancer 12:358. doi: 10.1186/1471-2407-12-358
5. Okajima K, Ohta Y (2012) Diagnostic imaging of high-grade astrocytoma: heterogeneity of clinical manifestation, image characteristics, and histopathological findings. Brain and Nerve = Shinkei kenkyu no shinpo 64(10):1151-1157
6. McDonald KL, McDonnell J, Muntoni A, Henson JD, Hegi ME, von Deimling A, Wheeler HR, Cook RJ, Biggs MT, Little NS, Robinson BG, Reddel RR, Royds JA (2010) Presence of alternative lengthening of telomeres mechanism in patients with glioblastoma identifies a less aggressive tumor type with longer survival. J Neuropathol Exp Neurol 69(7):729-736. doi: 10.1097/NEN.0b013e3181e576cf
7. Fowler A, Thomson D, Giles K, Maleki S, Mreich E, Wheeler H, Leedman P, Biggs M, Cook R, Little N, Robinson B, McDonald K (2011) miR-124a is frequently down-regulated in glioblastoma and is involved in migration and invasion. Eur J Cancer 47(6):953-963. doi: 10.1016/j.ejca.2010.11.026
8. Gautam P, Nair SC, Gupta MK, Sharma R, Polisetty RV, Uppin MS, Sundaram C, Puligopu AK, Ankathi P, Purohit AK, Chandak GR, Harsha HC, Sirdeshmukh R (2012) Proteins with altered levels in plasma from glioblastoma patients as revealed by iTRAQ-based quantitative proteomic analysis. PLoS One 7(9):e46153. doi: 10.1371/journal.pone.0046153
9. Persano L, Rampazzo E, Basso G, Viola G (2013) Glioblastoma cancer stem cells: role of the microenvironment and therapeutic targeting. Biochem Pharmacol 85(5):612-622. doi: 10.1016/j.bcp.2012.10.001
10. Calin GA, Croce CM (2006) MicroRNA signatures in human cancers. Nat Rev Cancer 6(11):857-866. doi: 10.1038/nrc1997
11. Delfino KR, Serao NV, Southey BR, Rodriguez-Zas SL (2011) Therapy-, gender- and race-specific microRNA markers, target genes and networks related to glioblastoma recurrence and survival. Cancer Genomics Proteomics 8(4):173-183
12. Huse JT, Holland E, DeAngelis LM (2013) Glioblastoma: molecular analysis and clinical implications. Ann Rev Med 64:59-70. doi: 10.1146/annurev-med- 100711-143028
13. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS (2006) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67. doi: 10.1186/1476-4598-5-67
14. Srinivasan S, Patric IR, Somasundaram K (2011) A ten-microRNA expression signature predicts survival in glioblastoma. PLoS One 6(3):e17438. doi: 10.1371/journal.pone.0017438
15. Visnyei K, Onodera H, Damoiseaux R, Saigusa K, Petrosyan S, De Vries D, Ferrari D, Saxe J, Panosyan EH, Masterman-Smith M, Mottahedeh J, Bradley KA, Huang J, Sabatti C, Nakano I, Kornblum HI (2011) A molecular screening approach to identify and characterize inhibitors of glioblastoma stem cells. Mol Cancer Ther 10(10):1818-1828. doi: 10.1158/1535-7163.MCT-11-0268
16. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352(10):997-1003. doi: 10.1056/NEJMoa043331
17. Hegi ME, Liu L, Herman JG, Stupp R, Wick W, Weller M, Mehta MP, Gilbert MR (2008) Correlation of O6-methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity. J Clin Oncol Off J Am Soc Clin Oncol 26(25):4189-4199. doi: 10.1200/JCO.2007.11.5964
18. Parkinson JF, Wheeler HR, Clarkson A, McKenzie CA, Biggs MT, Little NS, Cook RJ, Messina M, Robinson BG, McDonald KL (2008) Variation of O(6)-methylguanine-DNA methyltransferase (MGMT) promoter methylation in serial samples in glioblastoma. J Neurooncol 87(1):71-78. doi: 10.1007/s11060-007-9486- 0
19. Yoshimoto K, Mizoguchi M, Hata N, Murata H, Hatae R, Amano T, Nakamizo A, Sasaki T (2012) Complex DNA repair pathways as possible therapeutic targets to overcome temozolomide resistance in glioblastoma. Frontiers in oncology 2:186. doi: 10.3389/fonc.2012.00186
20. Lakomy R, Sana J, Hankeova S, Fadrus P, Kren L, Lzicarova E, Svoboda M, Dolezelova H, Smrcka M, Vyzula R, Michalek J, Hajduch M, Slaby O (2011) 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(12):2186-2190. doi: 10.1111/j.1349-7006. 2011.02092.x
21. Pegg AE (1984) Methylation of the O6 position of guanine in DNA is the most likely initiating event in carcinogenesis by methylating agents. Cancer investigation 2(3):223-231
22. Wick W, Hartmann C, Engel C, Stoffels M, Felsberg J, Stockhammer F, Sabel MC, Koeppen S, Ketter R, Meyermann R, Rapp M, Meisner C, Kortmann RD, Pietsch T, Wiestler OD, Ernemann U, Bamberg M, Reifenberger G, von Deimling A, Weller M (2009) NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol Off J Am Soc Clin Oncol 27(35):5874-5880. doi: 10.1200/JCO.2009.23.6497
23. Wurdinger T, Tannous BA (2009) Glioma angiogenesis: towards novel RNA therapeutics. Cell Adhes Migr 3(2):230-235
24. de Fougerolles A, Vornlocher HP, Maraganore J, Lieberman J (2007) Interfering with disease: a progress report on siRNA-based therapeutics. Nat Rev Drug Disc 6(6):443-453. doi: 10.1038/nrd2310
25. Thery C (2011) Exosomes: secreted vesicles and intercellular communications. F1000 biology reports 3:15. doi: 10.3410/B3-15
26. Hu G, Drescher KM, Chen XM (2012) Exosomal miRNAs: biological properties and therapeutic potential. Front Genet 3:56. doi: 10.3389/fgene.2012.00056
27. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z, Milosevic J, Tkacheva OA, Divito SJ, Jordan R, Lyons-Weiler J, Watkins SC, Morelli AE (2012) Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119(3):756-766. doi: 10.1182/blood-2011-02-338004
28. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10(12):1470-1476. doi: 10.1038/ncb1800
29. Katakowski M, Buller B, Wang X, Rogers T, Chopp M (2010) Functional microRNA is transferred between glioma cells. Cancer Res 70(21):8259-8263. doi: 10.1158/0008-5472.CAN-10-0604
30. Lee RC, Feinbaum RL, Ambros V (1993) The C. Elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843-854
31. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic acids research 39 (Database issue):D152-157. doi: 10.1093/nar/gkq1027
32. Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65(14):6029-6033. doi: 10.1158/0008-5472.CAN-05-0137
33. Ciafre SA, Galardi S, Mangiola A, Ferracin M, Liu CG, Sabatino G, Negrini M, Maira G, Croce CM, Farace MG (2005) Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun 334(4):1351-1358. doi: 10.1016/j.bbrc.2005.07.030
34. Moller HG, Rasmussen AP, Andersen HH, Johnsen KB, Henriksen M, Duroux M (2013) A systematic review of microRNA in glioblastoma multiforme: micro-modulators in the mesenchymal mode of migration and invasion. Mol Neurobiol 47(1):131-144. doi: 10.1007/s12035-012-8349-7
35. Esquela-Kerscher A, Slack FJ (2006) Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 6(4):259-269. doi: 10.1038/nrc1840
36. Ryan BM, Robles AI, Harris CC (2010) Genetic variation in microRNA networks: the implications for cancer research. Nat Rev Cancer 10(6):389-402. doi: 10.1038/nrc2867
37. Wang Q, Li P, Li A, Jiang W, Wang H, Wang J, Xie K (2012) Plasma specific miRNAs as predictive biomarkers for diagnosis and prognosis of glioma. Journal of experimental & clinical cancer research: CR 31:97. doi: 10.1186/1756-9966-31-97
38. Lages E, Guttin A, El Atifi M, Ramus C, Ipas H, Dupre I, Rolland D, Salon C, Godfraind C, deFraipont F, Dhobb M, Pelletier L, Wion D, Gay E, Berger F, Issartel JP (2011) MicroRNA and target protein patterns reveal physiopathological features of glioma subtypes. PLoS One 6(5):e20600. doi: 10.1371/journal.pone.0020600
39. Novakova J, Slaby O, Vyzula R, Michalek J (2009) MicroRNA involvement in glioblastoma pathogenesis. Biochem Biophys Res Commun 386(1):1-5. doi: 10.1016/j.bbrc.2009.06.034
40. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, Krichevsky AM (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28(17):5369-5380. doi: 10.1128/MCB.00479-08
41. Ilhan-Mutlu A, Wagner L, Wohrer A, Jungwirth S, Marosi C, Fischer P, Preusser M (2012) Blood alterations preceding clinical manifestation of glioblastoma. Cancer Investig 30(9):625-629. doi: 10.3109/07357907.2012.725443
42. Ilhan-Mutlu A, Wagner L, Wohrer A, Furtner J, Widhalm G, Marosi C, Preusser M (2012) Plasma MicroRNA-21 concentration may be a useful biomarker in glioblastoma patients. Cancer Investig 30(8):615-621. doi: 10.3109/07357907. 2012.708071
43. Ma R, Yan W, Zhang G, Lv H, Liu Z, Fang F, Zhang W, Zhang J, Tao T, You Y, Jiang T, Kang X (2012) Upregulation of miR-196b confers a poor prognosis in glioblastoma patients via inducing a proliferative phenotype. PLoS One 7(6):e38096. doi: 10.1371/journal.pone.0038096
44. Zhang W, Zhang J, Hoadley K, Kushwaha D, Ramakrishnan V, Li S, Kang C, You Y, Jiang C, Song SW, Jiang T, Chen CC (2012) miR-181d: a predictive glioblastoma biomarker that downregulates MGMT expression. Neuro-Oncology 14(6):712-719. doi: 10.1093/neuonc/nos089
45. Niyazi M, Zehentmayr F, Niemoller OM, Eigenbrod S, Kretzschmar H, Schulze-Osthoff K, Tonn JC, Atkinson M, Mortl S, Belka C (2011) MiRNA expression patterns predict survival in glioblastoma. Radiat Oncol 6:153. doi: 10.1186/1748-717X-6-153
46. Roth P, Wischhusen J, Happold C, Chandran PA, Hofer S, Eisele G, Weller M, Keller A (2011) A specific miRNA signature in the peripheral blood of glioblastoma patients. J Neurochem 118(3):449-457. doi: 10.1111/j.1471-4159. 2011.07307.x
47. Wuchty S, Arjona D, Li A, Kotliarov Y, Walling J, Ahn S, Zhang A, Maric D, Anolik R, Zenklusen JC, Fine HA (2011) Prediction of associations between microRNAs and gene expression in glioma biology. PLoS One 6(2):e14681. doi: 10.1371/journal.pone.0014681
48. Guan Y, Mizoguchi M, Yoshimoto K, Hata N, Shono T, Suzuki SO, Araki Y, Kuga D, Nakamizo A, Amano T, Ma X, Hayashi K, Sasaki T (2010) MiRNA-196 is upregulated in glioblastoma but not in anaplastic astrocytoma and has prognostic significance. Clin Cancer Res Official J Am Assoc Cancer Res 16(16):4289-4297. doi: 10.1158/1078-0432.CCR-10-0207
49. Wooten EC, Fults D, Duggirala R, Williams K, Kyritsis AP, Bondy ML, Levin VA, O'Connell P (1999) A study of loss of heterozygosity at 70 loci in anaplastic astrocytoma and glioblastoma multiforme with implications for tumor evolution. Neuro-Oncology 1(3):169-176
50. Guessous F, Zhang Y, Kofman A, Catania A, Li Y, Schiff D, Purow B, Abounader R (2010) microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 9(6):1031-1036
51. Li WB, Ma MW, Dong LJ, Wang F, Chen LX, Li XR (2011) MicroRNA-34a targets notch1 and inhibits cell proliferation in glioblastoma multiforme. Cancer Biol Ther 12(6):477-483. doi: 10.4161/cbt.12.6.16300
52. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, Johnson E, Marcinkiewicz L, Jiang J, Yang Y, Schmittgen TD, Lopes B, Schiff D, Purow B, Abounader R (2009) MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 69(19):7569-7576. doi: 10.1158/0008-5472.CAN-09-0529
53. Silber J, Jacobsen A, Ozawa T, Harinath G, Pedraza A, Sander C, Holland EC, Huse JT (2012) miR-34a repression in proneural malignant gliomas upregulates expression of its target PDGFRA and promotes tumorigenesis. PLoS One 7(3):e33844. doi: 10.1371
54. Papagiannakopoulos T, Shapiro A, Kosik KS (2008) MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 68(19):8164-8172. doi: 10.1158/0008-5472.CAN-08-1305
55. Quintavalle C, Donnarumma E, Iaboni M, Roscigno G, Garofalo M, Romano G, Fiore D, De Marinis P, Croce CM, Condorelli G (2012) Effect of miR-21 and miR-30b/c on TRAIL-induced apoptosis in glioma cells. Oncogene. doi: 10.1038/onc.2012.410
56. Ren Y, Zhou X, Mei M, Yuan XB, Han L, Wang GX, Jia ZF, Xu P, Pu PY, Kang CS (2010) MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol. BMC cancer 10:27. doi: 10.1186/1471-2407-10-27
57. Corsten MF, Miranda R, Kasmieh R, Krichevsky AM, Weissleder R, Shah K (2007) MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res 67(19):8994-9000. doi: 10.1158/0008-5472.CAN-07-1045
58. Gaur AB, Holbeck SL, Colburn NH, Israel MA (2011) Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro-Oncology 13(6):580-590. doi: 10.1093/neuonc/nor033
59. Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nature methods 4(9):721-726. doi: 10.1038/nmeth1079
60. Sumazin P, Yang X, Chiu HS, Chung WJ, Iyer A, Llobet-Navas D, Rajbhandari P, Bansal M, Guarnieri P, Silva J, Califano A (2011) An extensive microRNA-mediated network of RNA-RNA interactions regulates established oncogenic pathways in glioblastoma. Cell 147(2):370-381. doi: 10.1016/j.cell.2011.09.041
61. Mei J, Bachoo R, Zhang CL (2011) MicroRNA-146a inhibits glioma development by targeting Notch1. Mol Cell Biol 31(17):3584-3592. doi: 10.1128/MCB.05821-11
62. Wong ST, Zhang XQ, Zhuang JT, Chan HL, Li CH, Leung GK (2012) MicroRNA-21 inhibition enhances in vitro chemosensitivity of temozolomide-resistant glioblastoma cells. Anticancer Res 32(7):2835-2841
63. Yang YP, Chien Y, Chiou GY, Cherng JY, Wang ML, Lo WL, Chang YL, Huang PI, Chen YW, Shih YH, Chen MT, Chiou SH (2012) Inhibition of cancer stem cell-like properties and reduced chemoradioresistance of glioblastoma using microRNA145 with cationic polyurethane-short branch PEI. Biomaterials 33(5):1462-1476. doi: 10.1016/j.biomaterials.2011.10.071
64. Asuthkar S, Velpula KK, Chetty C, Gorantla B, Rao JS (2012) Epigenetic regulation of miRNA-211 by MMP-9 governs glioma cell apoptosis, chemosensitivity and radiosensitivity. Oncotarget 3(11):1439-1454
65. Meng W, Jiang L, Lu L, Hu H, Yu H, Ding D, Xiao K, Zheng W, Guo H, Ma W (2012) Anti-miR-155 oligonucleotide enhances chemosensitivity of U251 cell to taxol by inducing apoptosis. Cell Biol Int 36(7):653-659. doi: 10.1042/CBI20100918
66. Ryan J, Tivnan A, Fay J, Bryan K, Meehan M, Creevey L, Lynch J, Bray IM, O'Meara A, Davidoff AM, Stallings RL (2012) MicroRNA-204 increases sensitivity of neuroblastoma cells to cisplatin and is associated with a favourable clinical outcome. Br J Cancer 107(6):967-976. doi: 10.1038/bjc.2012.356
67. Gottesman MM (2002) Mechanisms of cancer drug resistance. Annu Rev Med 53:615-627. doi: 10.1146/annurev.med.53.082901.103929
68. Sasaki A, Udaka Y, Tsunoda Y, Yamamoto G, Tsuji M, Oyamada H, Oguchi K, Mizutani T (2012) Analysis of p53 and miRNA expression after irradiation of glioblastoma cell lines. Anticancer Res 32(11):4709-4713
69. Ujifuku K, Mitsutake N, Takakura S, Matsuse M, Saenko V, Suzuki K, Hayashi K, Matsuo T, Kamada K, Nagata I, Yamashita S (2010) miR-195, miR-455-3p and miR-10a are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Lett 296(2):241-248. doi: 10.1016/j.canlet.2010.04.013
70. Takeuchi K, Shibata M, Kashiyama E, Umehara K (2012) Expression levels of multidrug resistance-associated protein 4 (MRP4) in human leukemia and lymphoma cell lines, and the inhibitory effects of the MRP-specific inhibitor MK-571 on methotrexate distribution in rats. Exp Ther Med 4(3):524-532. doi: 10.3892/etm.2012.627
71. Quezada C, Peignan L, Segura R, Riquelme F, Melo R, Rojas ZD, Ayach F, San Martin R, Carcamo JG (2011) Study of resistance to chemotherapy mediated by ABC transporters in biopsies of glioblastoma multiforme. Revista medica de Chile 139(4):415-424. doi: S0034-98872011000400001
72. Abe T, Hasegawa S, Taniguchi K, Yokomizo A, Kuwano T, Ono M, Mori T, Hori S, Kohno K, Kuwano M (1994) Possible involvement of multidrug-resistance- associated protein (MRP) gene expression in spontaneous drug resistance to vincristine, etoposide and adriamycin in human glioma cells. Int J Cancer J Int du cancer 58(6):860-864
73. Decleves X, Fajac A, Lehmann-Che J, Tardy M, Mercier C, Hurbain I, Laplanche JL, Bernaudin JF, Scherrmann JM (2002) Molecular and functional MDR1-Pgp and MRPs expression in human glioblastoma multiforme cell lines. Int J Cancer J Int du cancer 98(2):173-180
74. Burkhart CA, Watt F, Murray J, Pajic M, Prokvolit A, Xue C, Flemming C, Smith J, Purmal A, Isachenko N, Komarov PG, Gurova KV, Sartorelli AC, Marshall GM, Norris MD, Gudkov AV, Haber M (2009) Small-molecule multidrug resistance-associated protein 1 inhibitor reversan increases the therapeutic index of chemotherapy in mouse models of neuroblastoma. Cancer Res 69(16):6573-6580. doi: 10.1158/0008-5472.CAN-09-1075
75. Yuan F, Salehi HA, Boucher Y, Vasthare US, Tuma RF, Jain RK (1994) Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res 54(17):4564-4568
76. Nau R, Sorgel F, Eiffert H (2010) Penetration of drugs through the blood-cerebrospinal fluid/blood-brain barrier for treatment of central nervous system infections. Clin Microbiol Rev 23(4):858-883. doi: 10.1128/CMR.00007-10
77. Yoon CH, Kim SJ, Shin BS, Lee KC, Yoo SD (2006) Rapid screening of blood-brain barrier penetration of drugs using the immobilized artificial membrane phosphatidylcholine column chromatography. J Biomol Screen 11(1):13-20. doi: 10.1177/1087057105281656
78. Gabathuler R (2010) Approaches to transport therapeutic drugs across the blood-brain barrier to treat brain diseases. Neurobiol Dis 37(1):48-57. doi: 10.1016/j.nbd.2009.07.028
79. Li WQ, Li YM, Tao BB, Lu YC, Hu GH, Liu HM, He J, Xu Y, Yu HY (2010) Downregulation of ABCG2 expression in glioblastoma cancer stem cells with miRNA-328 may decrease their chemoresistance. Med Sci Monit Int Med J Exp Clin Res 16(10):HY27-30
80. Jeon HM, Sohn YW, Oh SY, Kim SH, Beck S, Kim S, Kim H (2011) ID4 imparts chemoresistance and cancer stemness to glioma cells by derepressing miR-9-mediated suppression of SOX2. Cancer Res 71(9):3410-3421. doi: 10.1158/0008-5472.CAN-10-3340
81. Almog N, Ma L, Schwager C, Brinkmann BG, Beheshti A, Vajkoczy P, Folkman J, Hlatky L, Abdollahi A (2012) Consensus micro RNAs governing the switch of dormant tumors to the fast-growing angiogenic phenotype. PLoS One 7(8):e44001. doi: 10.1371/journal.pone.0044001
82. Chen L, Zhang W, Yan W, Han L, Zhang K, Shi Z, Zhang J, Wang Y, Li Y, Yu S, Pu P, Jiang C, Jiang T, Kang C (2012) The putative tumor suppressor miR-524-5p directly targets Jagged-1 and Hes-1 in glioma. Carcinogenesis 33(11):2276-2282. doi: 10.1093/carcin/bgs261
83. Choudhury Y, Tay FC, Lam DH, Sandanaraj E, Tang C, Ang BT, Wang S (2012) Attenuated adenosine-to-inosine editing of microRNA-376a promotes invasiveness of glioblastoma cells. J Clin Investig 122(11):4059-4076. doi: 10.1172/JCI62925
84. Gabriely G, Yi M, Narayan RS, Niers JM, Wurdinger T, Imitola J, Ligon KL, Kesari S, Esau C, Stephens RM, Tannous BA, Krichevsky AM (2011) Human glioma growth is controlled by microRNA-10b. Cancer Res 71(10):3563-3572. doi: 10.1158/0008-5472.CAN-10-3568
85. Godlewski J, Nowicki MO, Bronisz A, Williams S, Otsuki A, Nuovo G, Raychaudhury A, Newton HB, Chiocca EA, Lawler S (2008) Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res 68(22):9125-9130. doi: 10.1158/0008-5472.CAN-08- 2629
86. Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH, Sohn-Lee C, le Sage C, Agami R, Tuschl T, Holland EC (2009) The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev 23(11):1327-1337. doi: 10.1101/gad.1777409
87. Lin J, Teo S, Lam DH, Jeyaseelan K, Wang S (2012) MicroRNA-10b pleiotropically regulates invasion, angiogenicity and apoptosis of tumor cells resembling mesenchymal subtype of glioblastoma multiforme. Cell death & disease 3:e398. doi: 10.1038/cddis.2012.134
88. Lu ZJ, Liu SY, Yao YQ, Zhou YJ, Zhang S, Dai L, Tian HW, Zhou Y, Deng HX, Yang JL, Luo F (2011) The effect of miR-7 on behavior and global protein expression in glioma cell lines. Electrophoresis 32(24):3612-3620. doi: 10.1002/elps.201100230
89. Papagiannakopoulos T, Friedmann-Morvinski D, Neveu P, Dugas JC, Gill RM, Huillard E, Liu C, Zong H, Rowitch DH, Barres BA, Verma IM, Kosik KS (2012) Pro-neural miR-128 is a glioma tumor suppressor that targets mitogenic kinases. Oncogene 31(15):1884-1895. doi: 10.1038/onc.2011.380
90. Smits M, Mir SE, Nilsson RJ, van der Stoop PM, Niers JM, Marquez VE, Cloos J, Breakefield XO, Krichevsky AM, Noske DP, Tannous BA, Wurdinger T (2011) Down-regulation of miR-101 in endothelial cells promotes blood vessel formation through reduced repression of EZH2. PLoS One 6(1):e16282. doi: 10.1371/journal.pone.0016282
91. Smits M, Nilsson J, Mir SE, van der Stoop PM, Hulleman E, Niers JM, de Witt Hamer PC, Marquez VE, Cloos J, Krichevsky AM, Noske DP, Tannous BA, Wurdinger T (2010) miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget 1(8):710-720
92. Wang XF, Shi ZM, Wang XR, Cao L, Wang YY, Zhang JX, Yin Y, Luo H, Kang CS, Liu N, Jiang T, You YP (2012) MiR-181d acts as a tumor suppressor in glioma by targeting K-ras and Bcl-2. J Cancer Res Clin Oncol 138(4):573-584. doi: 10.1007/s00432-011-1114-x
93. Xia H, Cheung WK, Ng SS, Jiang X, Jiang S, Sze J, Leung GK, Lu G, Chan DT, Bian XW, Kung HF, Poon WS, Lin MC (2012) Loss of brain-enriched miR-124 microRNA enhances stem-like traits and invasiveness of glioma cells. J Biol Chem 287(13):9962-9971. doi: 10.1074/jbc.M111.332627
94. Zhang C, Kang C, You Y, Pu P, Yang W, Zhao P, Wang G, Zhang A, Jia Z, Han L, Jiang H (2009) Co-suppression of miR-221/222 cluster suppresses human glioma cell growth by targeting p27kip1 in vitro and in vivo. Int J Oncol 34(6):1653-1660
95. Zhang CZ, Zhang JX, Zhang AL, Shi ZD, Han L, Jia ZF, Yang WD, Wang GX, Jiang T, You YP, Pu PY, Cheng JQ, Kang CS (2010) MiR-221 and miR-222 target PUMA to induce cell survival in glioblastoma. Molecular cancer 9:229. doi: 10.1186/1476-4598-9-229
96. Lee SJ, Kim SJ, Seo HH, Shin SP, Kim D, Park CS, Kim KT, Kim YH, Jeong JS, Kim IH (2012) Over-expression of miR-145 enhances the effectiveness of HSVtk gene therapy for malignant glioma. Cancer Lett 320(1):72-80. doi: 10.1016/j.canlet.2012.01.029
97. Hwang do W, Son S, Jang J, Youn H, Lee S, Lee D, Lee YS, Jeong JM, Kim WJ, Lee DS (2011) A brain-targeted rabies virus glycoprotein-disulfide linked PEI nanocarrier for delivery of neurogenic microRNA. Biomaterials 32(21):4968-4975. doi: 10.1016/j.biomaterials.2011.03.047
98. Guo J, Niu R, Huang W, Zhou M, Shi J, Zhang L, Liao H (2012) Growth factors from tumor microenvironment possibly promote the proliferation of glioblastoma-derived stem-like cells in vitro. Pathology oncology research: POR 18(4):1047-1057. doi: 10.1007/s12253-012-9543-7
99. Candolfi M, King GD, Yagiz K, Curtin JF, Mineharu Y, Muhammad AK, Foulad D, Kroeger KM, Barnett N, Josien R, Lowenstein PR, Castro MG (2012) Plasmacytoid dendritic cells in the tumor microenvironment: immune targets for glioma therapeutics. Neoplasia 14(8):757-770
100. Hardee ME, Marciscano AE, Medina-Ramirez CM, Zagzag D, Narayana A, Lonning SM, Barcellos-Hoff MH (2012) Resistance of glioblastoma-initiating cells to radiation mediated by the tumor microenvironment can be abolished by inhibiting transforming growth factor-beta. Cancer Res 72(16):4119-4129. doi: 10.1158/0008-5472.CAN-12-0546
101. Jamal M, Rath BH, Tsang PS, Camphausen K, Tofilon PJ (2012) The brain microenvironment preferentially enhances the radioresistance of CD133(+) glioblastoma stem-like cells. Neoplasia 14(2):150-158
102. Jackson C, Ruzevick J, Phallen J, Belcaid Z, Lim M (2011) Challenges in immunotherapy presented by the glioblastoma multiforme microenvironment. Clin Dev Immunol. doi: 10.1155/2011/732413
103. Heddleston JM, Hitomi M, Venere M, Flavahan WA, Yang K, Kim Y, Minhas S, Rich JN, Hjelmeland AB (2011) Glioma stem cell maintenance: the role of the microenvironment. Curr Pharm Des 17(23):2386-2401
104. Charles N, Holland EC (2010) The perivascular niche microenvironment in brain tumor progression. Cell Cycle 9(15):3012-3021. doi: 10.4161/cc.9.15.12710
105. Hoelzinger DB, Demuth T, Berens ME (2007) Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment. J Natl Cancer Institute 99(21):1583-1593. doi: 10.1093/jnci/djm187
106. Inc RT (2012) Regulus is focused on the discovery and development of miRNA therapeutics. http://www.regulusrx.com/therapeutic-areas/
107. Therapeutics M (2013) Pipeline of miRNA therapeutics. http://www.miragentherapeutics.com/7/Pipeline/
108. Therapeutics M (2012) Pipeline of miRNA therpaueitcs lead candidates. http://www.mirnatherapeutics.com.
109. Judge AD, Sood V, Shaw JR, Fang D, McClintock K, MacLachlan I (2005) Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat Biotechnol 23(4):457-462. doi: 10.1038/nbt1081
110. Hollins AJ, Omidi Y, Benter IF, Akhtar S (2007) Toxicogenomics of drug delivery systems: exploiting delivery system-induced changes in target gene expression to enhance siRNA activity. Journal of drug targeting 15(1):83-88. doi: 10.1080/10611860601151860
111. Akhtar S, Benter I (2007) Toxicogenomics of non-viral drug delivery systems for RNAi: potential impact on siRNA-mediated gene silencing activity and specificity. Advanced drug delivery reviews 59(2-3):164-182. doi: 10.1016/j.addr.2007.03.010
112. Omidi Y, Hollins AJ, Benboubetra M, Drayton R, Benter IF, Akhtar S (2003) Toxicogenomics of non-viral vectors for gene therapy: a microarray study of lipofectin- and oligofectamine-induced gene expression changes in human epithelial cells. Journal of drug targeting 11(6):311-323. doi: 10.1080/10611860310001636908
113. Omidi Y, Hollins AJ, Drayton RM, Akhtar S (2005) Polypropylenimine dendrimer-induced gene expression changes: the effect of complexation with DNA, dendrimer generation and cell type. Journal of drug targeting 13(7):431-443. doi: 10.1080/10611860500418881
114. Akhtar S, Benter IF (2007) Nonviral delivery of synthetic siRNAs in vivo. J Clin Invest 117(12):3623-3632. doi: 10.1172/JCI33494
115. Zukiel R, Nowak S, Wyszko E, Rolle K, Gawronska I, Barciszewska MZ, Barciszewski J (2006) Suppression of human brain tumor with interference RNA specific for tenascin-C. Cancer biology & therapy 5(8):1002-1007
116. Guo D, Wang B, Han F, Lei T (2010) RNA interference therapy for glioblastoma. Expert Opin Biol Ther 10(6):927-936. doi: 10.1517/14712598.2010. 481667
117. Kirui DK, Khalidov I, Wang Y, Batt CA (2012) Targeted near-IR hybrid magnetic nanoparticles for in vivo cancer therapy and imaging. Nanomedicine: nanotechnology, biology, and medicine. doi: 10.1016/j.nano.2012.11.009
118. Ryvolova M, Chomoucka J, Drbohlavova J, Kopel P, Babula P, Hynek D, Adam V, Eckschlager T, Hubalek J, Stiborova M, Kaiser J, Kizek R (2012) Modern micro and nanoparticle-based imaging techniques. Sensors (Basel) 12(11):14792-14820. doi: 10.3390/s121114792
119. Nduom EK, Bouras A, Kaluzova M, Hadjipanayis CG (2012) Nanotechnology applications for glioblastoma. Neurosurgery clinics of North America 23(3):439-449. doi: 10.1016/j.nec.2012.04.006
120. Tivnan A, Orr WS, Gubala V, Nooney R, Williams DE, McDonagh C, Prenter S, Harvey H, Domingo-Fernandez R, Bray IM, Piskareva O, Ng CY, Lode HN, Davidoff AM, Stallings RL (2012) Inhibition of neuroblastoma tumor growth by targeted delivery of microRNA-34a using anti-disialoganglioside GD2 coated nanoparticles. PLoS One 7(5):e38129. doi: 10.1371/journal.pone.0038129
121. Bray I, Tivnan A, Bryan K, Foley NH, Watters KM, Tracey L, Davidoff AM, Stallings RL (2011) MicroRNA-542-5p as a novel tumor suppressor in neuroblastoma. Cancer Lett 303(1):56-64. doi: 10.1016/j.canlet.2011.01.016
122. Foley NH, Bray IM, Tivnan A, Bryan K, Murphy DM, Buckley PG, Ryan J, O'Meara A, O'Sullivan M, Stallings RL (2010) MicroRNA-184 inhibits neuroblastoma cell survival through targeting the serine/threonine kinase AKT2. Molecular cancer 9:83. doi: 10.1186/1476-4598-9-83
123. Babar IA, Cheng CJ, Booth CJ, Liang X, Weidhaas JB, Saltzman WM, Slack FJ (2012) Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc Natl Acad Sci U S A 109(26):E1695-1704. doi: 10.1073/pnas.1201516109
124. Piao L, Zhang M, Datta J, Xie X, Su T, Li H, Teknos TN, Pan Q (2012)
125. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29(4):341-345. doi: 10.1038/nbt.1807
126. Ikeda M, Bhattacharjee AK, Kondoh T, Nagashima T, Tamaki N (2002) Synergistic effect of cold mannitol and Na(+)/Ca(2+) exchange blocker on blood-brain barrier opening. Biochem Biophys Res Commun 291(3):669-674. doi: 10.1006/bbrc.2002.6495
127. Campbell M, Kiang AS, Kenna PF, Kerskens C, Blau C, O'Dwyer L, Tivnan A, Kelly JA, Brankin B, Farrar GJ, Humphries P (2008) RNAi-mediated reversible opening of the blood-brain barrier. The journal of gene medicine 10(8):930-947. doi: 10.1002/jgm.1211
128. Singh SK, Vartanian A, Burrell K, Zadeh G (2012) A microRNA link to glioblastoma heterogeneity. Cancers 4:846-872
129. Godlewski J, Bronisz A, Nowicki MO, Chiocca EA, Lawler S (2010) microRNA-451: A conditional switch controlling glioma cell proliferation and migration. Cell Cycle 9(14):2742-2748
130. Hegi ME, Rajakannu P, Weller M (2012) Epidermal growth factor receptor: a re-emerging target in glioblastoma. Curr Opin Neurol 25(6):774-779. doi: 10.1097/WCO.0b013e328359b0bc
131. Kang MK, Kang SK (2007) Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma. Stem cells and development 16(5):837-847. doi: 10.1089/scd.2007.0006
132. Wu Z, Sun L, Wang H, Yao J, Jiang C, Xu W, Yang Z (2012) MiR-328 expression is decreased in high-grade gliomas and is associated with worse survival in primary glioblastoma. PLoS One 7(10):e47270. doi: 10.1371/journal.pone.0047270
133. Kefas B, Comeau L, Erdle N, Montgomery E, Amos S, Purow B (2010) Pyruvate kinase M2 is a target of the tumor-suppressive microRNA-326 and regulates the survival of glioma cells. Neuro-Oncology 12(11):1102-1112. doi: 10.1093/neuonc/noq080
134. Bai Y, Liao H, Liu T, Zeng X, Xiao F, Luo L, Guo H, Guo L (2013) MiR-296-3p regulates cell growth and multi-drug resistance of human glioblastoma by targeting ether-a-go-go (EAG1). Eur J Cancer 49(3):710-724. doi: 10.1016/j.ejca.2012.08.020
135. Katakowski M, Zheng X, Jiang F, Rogers T, Szalad A, Chopp M (2010) MiR-146b-5p suppresses EGFR expression and reduces in vitro migration and invasion of glioma. Cancer investigation 28(10):1024-1030. doi: 10.3109/07357907.2010.512596
136. Lee HK, Bier A, Cazacu S, Finniss S, Xiang C, Twito H, Poisson LM, Mikkelsen T, Slavin S, Jacoby E, Yalon M, Toren A, Rempel SA, Brodie C (2013) MicroRNA-145 is downregulated in glial tumors and regulates glioma cell migration by targeting connective tissue growth factor. PLoS One 8(2):e54652. doi: 10.1371/journal.pone.0054652
137. Speranza MC, Frattini V, Pisati F, Kapetis D, Porrati P, Eoli M, Pellegatta S, Finocchiaro G (2012) NEDD9, a novel target of miR-145, increases the invasiveness of glioblastoma. Oncotarget 3(7):723-734
138. Zhang Y, Chao T, Li R, Liu W, Chen Y, Yan X, Gong Y, Yin B, Qiang B, Zhao J, Yuan J, Peng X (2009) MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J Mol Med (Berl) 87(1):43-51. doi: 10.1007/s00109-008-0403-6
139. Wan Y, Fei XF, Wang ZM, Jiang DY, Chen HC, Yang J, Shi L, Huang Q (2012) Expression of miR-125b in the new, highly invasive glioma stem cell and progenitor cell line SU3. Chinese journal of cancer 31(4):207-214. doi: 10.5732/cjc.011.10336
140. Wu N, Xiao L, Zhao X, Zhao J, Wang J, Wang F, Cao S, Lin X (2012) miR-125b regulates the proliferation of glioblastoma stem cells by targeting E2F2. FEBS Lett 586(21):3831-3839. doi: 10.1016/j.febslet.2012.08.023
141. Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Yu M, Vandenberg SR, Ginzinger DG, James CD, Costello JF, Bergers G, Weiss WA, Alvarez-Buylla A, Hodgson JG (2008) miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC medicine 6:14. doi: 10.1186/1741-7015-6-14
142. Loftus JC, Ross JT, Paquette KM, Paulino VM, Nasser S, Yang Z, Kloss J, Kim S, Berens ME, Tran NL (2012) miRNA expression profiling in migrating glioblastoma cells: regulation of cell migration and invasion by miR-23b via targeting of Pyk2. PLoS One 7(6):e39818. doi: 10.1371
143. Fox JL, Dews M, Minn AJ, Thomas-Tikhonenko A (2013) Targeting of TGFbeta signature and its essential component CTGF by miR-18 correlates with improved survival in glioblastoma. RNA 19(2):177-190. doi: 10.1261/rna.036467.112
144. Wu DG, Wang YY, Fan LG, Luo H, Han B, Sun LH, Wang XF, Zhang JX, Cao L, Wang XR, You YP, Liu N (2011) MicroRNA-7 regulates glioblastoma cell invasion via targeting focal adhesion kinase expression. Chinese medical journal 124(17):2616-2621