Therapeutic potential of targeting microRNA-10b in established intracranial glioblastoma: First steps toward the clinic

EMBO Molecular Medicine

Volumn 8, Issue 3, 2016, Pages 268-287

  Teplyuk, Nadiya M ^a   Uhlmann, Erik J ^a   Gabriely, Galina ^a   Volfovsky, Natalia ^b   Wang, Yang ^a   Teng, Jian ^a   Karmali, Priya ^c   Marcusson, Eric ^c   Peter, Merlene ^a   Mohan, Athul ^a   Kraytsberg, Yevgenya ^a   Cialic, Ron ^a   Chiocca, E Antonio ^d   Godlewski, Jakub ^d   Tannous, Bakhos ^a   Krichevsky, Anna M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b FLATIRON INSTITUTE   (United States)

^c REGULUS THERAPEUTICS   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Alternative splicing; Brain tumor; MicroRNA; Oligonucleotide therapeutics; Stem cells

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; MICRORNA 10B; ANTINEOPLASTIC AGENT; MICRORNA; MIRN10 MICRORNA, MOUSE;

5' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE REGULATION; CONTROLLED STUDY; FEMALE; GENE; GENE TARGETING; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MBNL1 3 GENE; MOUSE; NONHUMAN; OSMOTIC PUMP; PRIORITY JOURNAL; RSRC1 GENE; SART3 GENE; SYSTEMIC THERAPY; TUMOR GROWTH; ALLOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; TREATMENT OUTCOME; XENOGRAFT;

ALLOGRAFTS; ANIMALS; ANTINEOPLASTIC AGENTS; DISEASE MODELS, ANIMAL; GLIOBLASTOMA; HETEROGRAFTS; HUMANS; MICE; MICRORNAS; OLIGONUCLEOTIDES, ANTISENSE; TREATMENT OUTCOME;

EID: 84975709454     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201505495     Document Type: Article

References (68)

1. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760
2. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233
3. Batzri S, Korn ED (1973) Single bilayer liposomes prepared without sonication. Biochim Biophys Acta 298: 1015-1019
4. Bogdahn U, Hau P, Stockhammer G, Venkataramana NK, Mahapatra AK, Suri A, Balasubramaniam A, Nair S, Oliushine V, Parfenov V et al (2011) Targeted therapy for high-grade glioma with the TGF-beta2 inhibitor trabedersen: results of a randomized and controlled phase IIb study. Neuro Oncol 13: 132-142
5. Boutz PL, Stoilov P, Li Q, Lin CH, Chawla G, Ostrow K, Shiue L, Ares M Jr, Black DL (2007) A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21: 1636-1652
6. Bredel M, Bredel C, Juric D, Harsh GR, Vogel H, Recht LD, Sikic BI (2005) Functional network analysis reveals extended gliomagenesis pathway maps and three novel MYC-interacting genes in human gliomas. Cancer Res 65: 8679-8689
7. Cancer Genome Atlas Research N (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455: 1061-1068.
8. Chi SW, Hannon GJ, Darnell RB (2012) An alternative mode of microRNA target recognition. Nat Struct Mol Biol 19: 321-327
9. Dong CG, Wu WK, Feng SY, Wang XJ, Shao JF, Qiao J (2012) Co-inhibition of microRNA-10b and microRNA-21 exerts synergistic inhibition on the proliferation and invasion of human glioma cells. Int J Oncol 41: 1005-1012
10. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210
11. Festing MF, Altman DG (2002) Guidelines for the design and statistical analysis of experiments using laboratory animals. ILAR J 43: 244-258
12. Fleming VA, Geng C, Ladd AN, Lou H (2012) Alternative splicing of the neurofibromatosis type 1 pre-mRNA is regulated by the muscleblind-like proteins and the CUG-BP and ELAV-like factors. BMC Mol Biol 13: 35
13. Gabriely G, Teplyuk NM, Krichevsky AM (2011a) Context effect: microRNA-10b in cancer cell proliferation, spread and death. Autophagy 7: 1384-1386
14. Gabriely G, Yi M, Narayan RS, Niers JM, Wurdinger T, Imitola J, Ligon KL, Kesari S, Esau C, Stephens RM et al (2011b) Human glioma growth is controlled by microRNA-10b. Cancer Res 71: 3563-3572
15. Gabut M, Samavarchi-Tehrani P, Wang X, Slobodeniuc V, O'Hanlon D, Sung HK, Alvarez M, Talukder S, Pan Q, Mazzoni EO et al (2011) An alternative splicing switch regulates embryonic stem cell pluripotency and reprogramming. Cell 147: 132-146
16. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64: 7011-7021
17. Geary RS, Norris D, Yu R, Bennett CF (2015) Pharmacokinetics, biodistribution and cell uptake of antisense oligonucleotides. Adv Drug Deliv Rev 87: 46-51
18. Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, Hook L, Nelson JA (2010) A viral microRNA down-regulates multiple cell cycle genes through mRNA 5′UTRs. PLoS Pathog 6: e1000967
19. Guessous F, Alvarado-Velez M, Marcinkiewicz L, Zhang Y, Kim J, Heister S, Kefas B, Godlewski J, Schiff D, Purow B et al (2013) Oncogenic effects of miR-10b in glioblastoma stem cells. J Neurooncol 112: 153-163
20. Han H, Irimia M, Ross PJ, Sung HK, Alipanahi B, David L, Golipour A, Gabut M, Michael IP, Nachman EN et al (2013) MBNL proteins repress ES-cell-specific alternative splicing and reprogramming. Nature 498: 241-245
21. Han X, Yan S, Weijie Z, Feng W, Liuxing W, Mengquan L, Qingxia F (2014) Critical role of miR-10b in transforming growth factor-beta1-induced epithelial-mesenchymal transition in breast cancer. Cancer Gene Ther 21: 60-67
22. Helwak A, Kudla G, Dudnakova T, Tollervey D (2013) Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153: 654-665
23. Holt I, Jacquemin V, Fardaei M, Sewry CA, Butler-Browne GS, Furling D, Brook JD, Morris GE (2009) Muscleblind-like proteins: similarities and differences in normal and myotonic dystrophy muscle. Am J Pathol 174: 216-227
24. Jaafar-Maalej C, Diab R, Andrieu V, Elaissari A, Fessi H (2010) Ethanol injection method for hydrophilic and lipophilic drug-loaded liposome preparation. J Liposome Res 20: 228-243
25. Jangi M, Sharp PA (2014) Building robust transcriptomes with master splicing factors. Cell 159: 487-498
26. Kalsotra A, Cooper TA (2011) Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet 12: 715-729
27. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8: e1000412
28. Lang MF, Yang S, Zhao C, Sun G, Murai K, Wu X, Wang J, Gao H, Brown CE, Liu X et al (2012) Genome-wide profiling identified a set of miRNAs that are differentially expressed in glioblastoma stem cells and normal neural stem cells. PLoS ONE 7: e36248
29. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W et al (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9: 391-403
30. Lee I, Ajay SS, Yook JI, Kim HS, Hong SH, Kim NH, Dhanasekaran SM, Chinnaiyan AM, Athey BD (2009) New class of microRNA targets containing simultaneous 5′-UTR and 3′-UTR interaction sites. Genome Res 19: 1175-1183
31. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20
32. Li QJ, Zhou L, Yang F, Wang GX, Zheng H, Wang DS, He Y, Dou KF (2012) MicroRNA-10b promotes migration and invasion through CADM1 in human hepatocellular carcinoma cells. Tumour Biol 33: 1455-1465
33. Liang Y, Diehn M, Watson N, Bollen AW, Aldape KD, Nicholas MK, Lamborn KR, Berger MS, Botstein D, Brown PO et al (2005) Gene expression profiling reveals molecularly and clinically distinct subtypes of glioblastoma multiforme. Proc Natl Acad Sci USA 102: 5814-5819
34. 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 Dis 3: e398
35. Listerman I, Sun J, Gazzaniga FS, Lukas JL, Blackburn EH (2013) The major reverse transcriptase-incompetent splice variant of the human telomerase protein inhibits telomerase activity but protects from apoptosis. Cancer Res 73: 2817-2828
36. 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
37. Liu M, Roth A, Yu M, Morris R, Bersani F, Rivera MN, Lu J, Shioda T, Vasudevan S, Ramaswamy S et al (2013a) The IGF2 intronic miR-483 selectively enhances transcription from IGF2 fetal promoters and enhances tumorigenesis. Genes Dev 27: 2543-2548
38. Liu Y, Li M, Zhang G, Pang Z (2013b) MicroRNA-10b overexpression promotes non-small cell lung cancer cell proliferation and invasion. Eur J Med Res 18: 41
39. Lytle JR, Yario TA, Steitz JA (2007) 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: 9667-9672
40. Ma L, Teruya-Feldstein J, Weinberg RA (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688
41. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG, Teruya-Feldstein J, Bell GW, Weinberg RA (2010) Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol 28: 341-347
42. Maguire CA, Meijer DH, LeRoy SG, Tierney LA, Broekman ML, Costa FF, Breakefield XO, Stemmer-Rachamimov A, Sena-Esteves M (2008) Preventing growth of brain tumors by creating a zone of resistance. Mol Ther 16: 1695-1702
43. Makeyev EV, Zhang J, Carrasco MA, Maniatis T (2007) The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27: 435-448
44. Moretti F, Thermann R, Hentze MW (2010) Mechanism of translational regulation by miR-2 from sites in the 5′ untranslated region or the open reading frame. RNA 16: 2493-2502
45. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, Hamou MF, de Tribolet N, Regli L, Wick W, Kouwenhoven MC et al (2008) Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol 26: 3015-3024
46. Murayama K, Kobayashi T, Imaizumi T, Matsunaga K, Kuramoto T, Shigemori M, Shichijo S, Itoh K (2000) Expression of the SART3 tumor-rejection antigen in brain tumors and induction of cytotoxic T lymphocytes by its peptides. J Immunother 23: 511-518
47. Mussnich P, D'Angelo D, Leone V, Croce CM, Fusco A (2013) The High Mobility Group A proteins contribute to thyroid cell transformation by regulating miR-603 and miR-10b expression. Mol Oncol 7: 531-542
48. Nakata K, Ohuchida K, Mizumoto K, Kayashima T, Ikenaga N, Sakai H, Lin C, Fujita H, Otsuka T, Aishima S et al (2011) MicroRNA-10b is overexpressed in pancreatic cancer, promotes its invasiveness, and correlates with a poor prognosis. Surgery 150: 916-922
49. Nakayama I, Shibazaki M, Yashima-Abo A, Miura F, Sugiyama T, Masuda T, Maesawa C (2013) Loss of HOXD10 expression induced by upregulation of miR-10b accelerates the migration and invasion activities of ovarian cancer cells. Int J Oncol 43: 63-71
50. Nishida N, Yamashita S, Mimori K, Sudo T, Tanaka F, Shibata K, Yamamoto H, Ishii H, Doki Y, Mori M (2012) MicroRNA-10b is a prognostic indicator in colorectal cancer and confers resistance to the chemotherapeutic agent 5-fluorouracil in colorectal cancer cells. Ann Surg Oncol 19: 3065-3071
51. Orom UA, Nielsen FC, Lund AH (2008) MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30: 460-471
52. Ouyang H, Gore J, Deitz S, Korc M (2014) microRNA-10b enhances pancreatic cancer cell invasion by suppressing TIP30 expression and promoting EGF and TGF-beta actions. Oncogene 33: 4664-4674
53. Panda AC, Sahu I, Kulkarni SD, Martindale JL, Abdelmohsen K, Vindu A, Joseph J, Gorospe M, Seshadri V (2014) miR-196b-mediated translation regulation of mouse insulin2 via the 5′UTR. PLoS ONE 9: e101084
54. Park CY, Jeker LT, Carver-Moore K, Oh A, Liu HJ, Cameron R, Richards H, Li Z, Adler D, Yoshinaga Y et al (2012) A resource for the conditional ablation of microRNAs in the mouse. Cell Rep 1: 385-391
55. Rich JN, Bao S (2007) Chemotherapy and cancer stem cells. Cell Stem Cell 1: 353-355
56. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401
57. Sun L, Hui AM, Su Q, Vortmeyer A, Kotliarov Y, Pastorino S, Passaniti A, Menon J, Walling J, Bailey R et al (2006) Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell 9: 287-300
58. Sun XJ, Liu H, Zhang P, Zhang XD, Jiang ZW, Jiang CC (2013) miR-10b promotes migration and invasion in nasopharyngeal carcinoma cells. Asian Pac J Cancer Prev 14: 5533-5537
59. Teng J, Hejazi S, Badr CE, Tannous BA (2014) Systemic anticancer neural stem cells in combination with a cardiac glycoside for glioblastoma therapy. Stem Cells 32: 2021-2032
60. Teplyuk NM, Mollenhauer B, Gabriely G, Giese A, Kim E, Smolsky M, Kim RY, Saria MG, Pastorino S, Kesari S et al (2012) MicroRNAs in cerebrospinal fluid identify glioblastoma and metastatic brain cancers and reflect disease activity. Neuro Oncol 14: 689-700
61. Teplyuk NM, Uhlmann EJ, Wong AH, Karmali P, Basu M, Gabriely G, Jain A, Wang Y, Chiocca EA, Stephens R et al (2015) MicroRNA-10b inhibition reduces E2F1-mediated transcription and miR-15/16 activity in glioblastoma. Oncotarget 6: 3770-3783
62. Tsai NP, Lin YL, Wei LN (2009) MicroRNA mir-346 targets the 5′-untranslated region of receptor-interacting protein 140 (RIP140) mRNA and up-regulates its protein expression. Biochem J 424: 411-418
63. Venables JP, Klinck R, Koh C, Gervais-Bird J, Bramard A, Inkel L, Durand M, Couture S, Froehlich U, Lapointe E et al (2009) Cancer-associated regulation of alternative splicing. Nat Struct Mol Biol 16: 670-676
64. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP et al (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110
65. Wakimoto H, Kesari S, Farrell CJ, Curry WT Jr, Zaupa C, Aghi M, Kuroda T, Stemmer-Rachamimov A, Shah K, Liu TC et al (2009) Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 69: 3472-3481
66. Wakimoto H, Mohapatra G, Kanai R, Curry WT Jr, Yip S, Nitta M, Patel AP, Barnard ZR, Stemmer-Rachamimov AO, Louis DN et al (2012) Maintenance of primary tumor phenotype and genotype in glioblastoma stem cells. Neuro Oncol 14: 132-144
67. Wang YY, Ye ZY, Zhao ZS, Li L, Wang YX, Tao HQ, Wang HJ, He XJ (2013) Clinicopathologic significance of miR-10b expression in gastric carcinoma. Hum Pathol 44: 1278-1285
68. Zhou H, Rigoutsos I (2014) MiR-103a-3p targets the 5′UTR of GPRC5A in pancreatic cells. RNA 20: 1431-1439