Potential role of miRNAs and their inhibitors in glioma treatment

Expert Review of Anticancer Therapy

Volumn 10, Issue 11, 2010, Pages 1753-1762

  Asadi Moghaddam, Kaveh ^a   Chiocca, E Antonio ^a   Lawler, Sean E ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

glioblastoma; miRNA; therapeutics

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; MICRORNA; NANOPARTICLE; TRANSFORMING GROWTH FACTOR BETA2; VIRUS VECTOR;

ADENO ASSOCIATED VIRUS; BINDING SITE; BRAIN METASTASIS; BRAIN TUMOR; CANCER GENE THERAPY; GENE EXPRESSION REGULATION; GENE SILENCING; GENE THERAPY; GLIOBLASTOMA; GLIOMA; HUMAN; MICROARRAY ANALYSIS; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; REVIEW; RNA BINDING; RNA TRANSLATION;

BRAIN NEOPLASMS; GLIOMA; HUMANS; MICRORNAS;

EID: 78649244799     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/era.10.168     Document Type: Review

References (65)

1. Stupp R, Mason W, van den Bent M et al Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352(10), 987-996 (2005).
2. Fulda S, Wick W, Weller M, Debatin K. Smac agonists sensitize for Apo2L/TRAIL-or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 8(8), 808-815 (2002).
3. Zhu Y, Parada L. The molecular and genetic basis of neurological tumours. Nat. Rev. Cancer 2(8), 616-626 (2002).
4. Esquela-Kerscher A, Slack F. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 6(4), 259-269 (2006). • Nice review of the roles of miRNAs in cancer.
5. Bartel D. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2), 281-297 (2004).
6. Hobert O. Gene regulation by transcription factors and microRNAs. Science 319(5871), 1785-1786 (2008).
7. Bartel D. MicroRNAs: targeting and regulatory functions. Cell 136(2), 215-233 (2009). • • Review of more advanced concepts in the miRNA field. Examines more detailed aspects of targeting mechanisms.
8. Tay Y, Zhang J, Thomson A, Lim B, Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455(7216), 1124-1128 (2008).
9. Lytle J, Yario T, Steitz J. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR. Proc. Natl Acad. Sci. USA 104(23), 9667-9672 (2007).
10. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 455(7209), 58-63 (2008).
11. Ciafre S, Galardi S, Mangiola A et al Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem. Biophys. Res. Commun. 334(4), 1351-1358 (2005).
12. Kefas B, Godlewski J, Comeau L et al. microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res. 68(10), 3566-3572 (2008). • One of the first functional studies of miRNA involvement in glioblastoma multiforme. Nice story develops from identification of EGF receptor as a target, to downregulation in tumor cells, and then further targets based on functional observations.
13. Webster RJ, Giles KM, Price KJ et al. Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J. Biol. Chem. 284(9), 5731-5741 (2009).
14. Gaur A, Jewell DA, Liang Y et al. Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res. 67(6), 2456-2468 (2007).
15. Xia H, Qi Y, Ng SS et al. MicroRNA-15b regulates cell cycle progression by targeting cyclins in glioma cells. Biochem. Biophys. Res. Commun. 380(2), 205-210 (2009).
16. Chan J, Krichevsky A, Kosik K. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 65(14), 6029-6033 (2005).
17. • Earliest functional study of miRNA involvement in glioblastoma multiforme, and strong evidence that miR?21 is a major oncomir.
18. Godlewski J, Nowicki M, Bronisz A et al. 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 (2008). • Identification of a miRNA/target pair, followed by further phenotypic studies to show that miR-128 affects cancer cell self-renewal as predicted based on its targeting of Bmi-1.
19. Corsten MF, Miranda R, Kasmieh R et al. 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 (2007).
20. Panner A, James CD, Berger MS, Pieper RO. mTOR controls FLIPS translation and TRAIL sensitivity in glioblastoma multiforme cells. Mol. Cell Biol. 25(20), 8809-8823 (2005).
21. Papagiannakopoulos T, Shapiro A, Kosik KS. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res. 68(19), 8164-8172 (2008). •• A more systems-based approach to looking at miRNA function. There may be more such studies in the future.
22. Gabriely G, Wurdinger T, Kesari S et al. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol. Cell Biol. 28(17), 5369-5380 (2008). • • Comprehensive analysis of miR-21 targets and phenotypes. A very good study.
23. Chen Y, Liu W, Chao T et al. MicroRNA-21 down-regulates the expression of tumor suppressor PDCD4 in human glioblastoma cell T98G. Cancer Lett. 272(2), 197-205 (2008).
24. Huse JT, Brennan C, Hambardzumyan D et al. The PTEN-regulating microRNA miR-26a is amplifed in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev. 23(11), 1327-1337 (2009). • Identifes a miR?26 involvement in glioblastoma multiforme on the basis of known genetic alterations.
25. Kim H, Huang W, Jiang X et al. Integrative genome analysis reveals an oncomir/oncogene cluster regulating glioblastoma survivorship. Proc. Natl Acad. Sci. USA 107(5), 2183-2188 (2010).
26. He L, He X, Lim LP et al. A microRNA component of the p53 tumour suppressor network. Nature 447(7148), 1130-1134 (2007).
27. Li Y, Guessous F, Zhang Y et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res. 69(19), 7569-7576 (2009).
28. Guessous F, Zhang Y, Kofman A et al. microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 9(6) 1031-1036 (2010).
29. Silber J, Lim D, Petritsch C et al. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med. 6, 14(2008). • Demonstrates the role of miR?124 and miR-137 using glioma stem cell-like cultures.
30. Lujambio A, Ropero S, Ballestar E et al. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 67(4), 1424-1429 (2007).
31. Makeyev E, Zhang J, Carrasco M, Maniatis T. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell. 27(3), 435-448 (2007).
32. Visvanathan J, Lee S, Lee B, Lee JW, Lee SK. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 21(7), 744-749 (2007).
33. Conaco C, Otto S, Han JJ, Mandel G. Reciprocal actions of REST and a microRNA promote neuronal identity Proc. Natl Acad. Sci. USA 103(7), 2422-2427 (2006).
34. Smirnova L, Grafe A, Seiler A et al. Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci. 21(6), 1469-1477 (2005).
35. Wu L, Belasco JG. Micro-RNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol. Cell Biol. 25(21), 9198-9208 (2005).
36. Nelson PT, Baldwin DA, Kloosterman WP et al. RAKE and LNA-ISH reveal microRNA expression and localization in archival human brain. RNA 12(2), 187-191 (2006).
37. Xia HF, He TZ, Liu CM et al. MiR-125b expression affects the proliferation and apoptosis of human glioma cells by targeting Bmf. Cell. Physiol. Biochem. 23 (4-6), 347-358 (2009).
38. Sanai N, Alvarez-Buylla A, Berger M. Neural stem cells and the origin of gliomas. N. Engl. J. Med. 353(8), 811-822 (2005).
39. Kloosterman W, Plasterk R. The diverse functions of microRNAs in animal development and disease. Dev. Cell 11(4), 441-450 (2006).
40. Bruggeman S, Hulsman D, Tanger E et al. Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. Cancer Cell 12(4), 328-341 (2007).
41. Molofsky A, Pardal R, Iwashita T et al. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425(6961), 962-967 (2003).
42. Pardal R, Molofsky A, He S, Morrison S. Stem cell self-renewal and cancer cell proliferation are regulated by common networks that balance the activation of proto-oncogenes and tumor suppressors. Cold Spring Harb. Symp. Quant. Biol. 70, 177-185 (2005).
43. Sparmann A, van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 6(11), 846-856 (2006).
44. Fasano CA, Dimos JT, Ivanova NB, Lowry N, Lemischka IR, Temple S. shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 1(1), 87-99 (2007).
45. Weiss GJ, Bemis LT, Nakajima E et al. EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to geftinib and EGFR expression in cell lines. Ann. Oncol. 19(6), 1053-1059 (2008).
46. Zhang Y, Chao T, Li R et al. MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J. Mol. Med. 87(1), 43-51 (2009).
47. Xia H, Qi Y, Ng SS et al. MicroRNA-146b inhibits glioma cell migration and invasion by targeting MMPs. Brain Res. 1269, 158-165 (2009).
48. Slaby O, Lakomy R, Fadrus P et al. MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma 57(3), 264-269 (2010).
49. Liu T, Papagiannakopoulos T, Puskar K et al. Detection of a microRNA signal in an in vivo expression set of mRNAs. PLoS One 2(8), e804 (2007).
50. le Sage C, Nagel R, Egan DA et al. Regulation of the p27 (Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J. 26(15), 3699-3708 (2007).
51. Mizumatsu S, Tamiya T, Ono Y et al. Expression of cell cycle regulator p27Kip1 is correlated with survival of patients with astrocytoma. Clin. Cancer Res. 5(3), 551-557 (1999).
52. Medina R, Zaidi SK, Liu CG et al. MicroRNAs 221 and 222 bypass quiescence and compromise cell survival. Cancer Res. 68(8), 2773-2780 (2008).
53. Wurdinger T, Tannous BA, Saydam O et al. miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 14(5), 382-393 (2008).
54. Kim J, Krichevsky A, Grad Y et al. Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc. Natl Acad. Sci. USA 101(1), 360-365 (2004).
55. Kefas B, Comeau L, Floyd DH et al. The neuronal microRNA miR-326 acts in a feedback loop with notch and has therapeutic potential against brain tumors. J. Neurosci. 29(48), 15161-15168 (2009).
56. Cau E, Blader P. Notch activity in the nervous system: to switch or not switch? Neural Dev. 4, 36(2009).
57. Crawford M, Brawner E, Batte K et al MicroRNA-126 inhibits invasion in non-small cell lung carcinoma cell lines. Biochem. Biophys. Res. Commun. 373(4), 607-612 (2008).
58. Godlewski J, Nowicki MO, Bronisz A et al MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells. Mol. Cell 37(5), 620-632 (2010). • Identification of complex regulation of glioma growth and invasion by a single miRNA. Shows how detailed mechanistic studies of miRNAs may reveal novel aspects of the disease.
59. Tong AW, Nemunaitis J. Modulation of miRNA activity in human cancer: a new paradigm for cancer gene therapy? Cancer Gene Ther. 15(6), 341-355 (2008).
60. Davis S, Lollo B, Freier S, Esau C. Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res. 34(8), 2294-2304 (2006).
61. Kota J, Chivukula RR, O'Donnell KA et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137(6), 1005-1017 (2009). • • Shows how a miRNA can prevent tumor formation very effectively in vivo.
62. Takeshita F, Patrawala L, Osaki M et al Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes. Mol. Ther. 18(1), 181-187 (2010).
63. Lawler SE, Prezzi PP, Chiocca EA. Genetic strategies for brain tumor therapy. Cancer Gene Ther. 13(3), 225-233 (2006).
64. Hau P, Jachimczak P, Bogdahn U. Treatment of malignant gliomas with TGF-p2 antisense oligonucleotides. Expert Rev. Anticancer Ther. 9(11), 1663-1674 (2009).
65. Brown BD, Naldini L. Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nat. Rev. Genet. 10(8), 578-585 (2009). • • Overview of the potential therapeutic impact of and strategies to exploit miRNAs therapeutically.