High-throughput microRNA profiling of pediatric high-grade gliomas

Neuro-Oncology

Volumn 16, Issue 2, 2014, Pages 228-240

  Miele, Evelina ^a,g   Buttarelli, Francesca Romana ^a   Arcella, Antonella ^c   Begalli, Federica ^a   Garg, Neha ^a   Silvano, Marianna ^a   Po, Agnese ^a   Baldi, Caterina ^a   Carissimo, Giuseppe ^a   Antonelli, Manila ^b   Spinelli, Gian Paolo ^a   Capalbo, Carlo ^a   Donofrio, Vittoria ^d   Morra, Isabella ^e   Nozza, Paolo ^f   Gulino, Alberto ^a,g   Giangaspero, Felice ^b   Ferretti, Elisabetta ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c IRCCS NEUROMED   (Italy)

^d Santobono Pausilipon Children Hospital   (Italy)

^e REGINA MARGHERITA CHILDREN S HOSPITAL   (Italy)

^f G GASLINI INSTITUTE   (Italy)

^g ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

cancer; expression profiling; microRNA; pediatric gliomas

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MICRORNA; MICRORNA 106B; MICRORNA 15A; MICRORNA 15B; MICRORNA 16; MICRORNA 17; MICRORNA 18A; MICRORNA 191; MICRORNA 193B; MICRORNA 19A; MICRORNA 19B; MICRORNA 20A; MICRORNA 25; MICRORNA 29B; MICRORNA 29C; MICRORNA 30B; MICRORNA 30D; MICRORNA 337; MICRORNA 365A; MICRORNA 425; MICRORNA 431; MICRORNA 665; MICRORNA 92; MICRORNA 92A; MICRORNA 93; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN MDM2; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADOLESCENT; ADULT; ADULT DISEASE; ADULT HIGH GRADE GLIOMA; AGED; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CHILD; CHILDHOOD CANCER; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; GENE EXPRESSION; GLIOMA; GLIOMA CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MIDDLE AGED; PEDIATRIC HIGH GRADE GLIOMA; PRESCHOOL CHILD; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SCHOOL CHILD; WESTERN BLOTTING; YOUNG ADULT;

CANCER; EXPRESSION PROFILING; MICRORNA; PEDIATRIC GLIOMAS;

ADOLESCENT; ADULT; AGED; BLOTTING, WESTERN; BRAIN; BRAIN NEOPLASMS; CASE-CONTROL STUDIES; CELL PROLIFERATION; CHILD; CHILD, PRESCHOOL; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION PROFILING; GLIOMA; HUMANS; IN SITU HYBRIDIZATION; MALE; MICRORNAS; MIDDLE AGED; NEOPLASM GRADING; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; RETROSPECTIVE STUDIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED;

EID: 84893122766     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/not215     Document Type: Article

References (67)

1. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007; 114(2):97-109.
2. Kaatsch P, Rickert CH, Kuhl J, Schuz J, Michaelis J. Population-based epidemiologic data on brain tumors in German children. Cancer. 2001;92(12):3155-3164.
3. Fangusaro J. Pediatric high grade glioma: a review and update on tumor clinical characteristics and biology. Front Oncol. 2012;2:105.
4. Spinelli GP, Miele E, Lo Russo G, et al. Chemotherapy and target therapy in the management of adult high- grade gliomas. Curr Cancer Drug Targets. 2012;12(8):1016-1031.
5. Paugh BS, Qu C, Jones C, et al. Integrated molecular genetic profiling of pediatric high-grade gliomas reveals key differences with the adult disease. J Clin Oncol. 2010;28(18):3061-3068.
6. Haque T, Faury D, Albrecht S, et al. Gene expression profiling from formalin-fixed paraffin-embedded tumors of pediatric glioblastoma. Clin Cancer Res. 2007;13(21):6284-6292.
7. Johnson R, Wright KD, Gilbertson RJ. Molecular profiling of pediatric brain tumors: insight into biology and treatment. Curr Oncol Rep. 2009;11(1):68-72.
8. Bax DA, Mackay A, Little SE, et al. A distinct spectrum of copy number aberrations in pediatric high-grade gliomas. Clin Cancer Res. 2010; 16(13):3368-3377.
9. Jones C, Perryman L, Hargrave D. Paediatric and adult malignant glioma: close relatives or distant cousins?. Nat Rev Clin Oncol. 2012; 9(7):400-413.
10. Schwartzentruber J, Korshunov A, Liu XY, et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature. 2012;482(7384):226-231.
11. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 2006;6(4):259-269.
12. He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature. 2005;435(7043):828-833.
13. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006;6(11):857-866.
14. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834-838.
15. De Smaele E, Ferretti E, Gulino A. MicroRNAs as biomarkers for CNS cancer and other disorders. Brain Res. 2010;1338:100-111.
16. Kosik KS. The neuronal microRNAsystem.Nat Rev Neurosci. 2006;7(12): 911-920.
17. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG. Regulation of miRNA expression during neural cell specification. Eur J Neurosci. 2005;21(6):1469-1477.
18. Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005;65(14): 6029-6033.
19. Ciafre SA, Galardi S, Mangiola A, et al. Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun. 2005;334(4):1351-1358.
20. Corsten MF, Miranda R, Kasmieh R, Krichevsky AM,Weissleder R, Shah K. MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res. 2007;67(19):8994-9000.
21. Silber J, Lim DA, 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. 2008;6:14.
22. 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. 2008;68(10): 3566-3572.
23. Conti A, Aguennouz M, La Torre D, et al. miR-21 and 221 upregulation and miR-181b downregulation in human grade II-IV astrocytic tumors. J Neurooncol. 2009;93(3):325-332.
24. Shi L, Cheng Z, Zhang J, et al. hsa-mir-181a and hsa-mir-181b function as tumor suppressors in human glioma cells. Brain Res. 2008;1236: 185-193.
25. Jiang J, Sun X, Wang W, et al. Tumor microRNA-335 expression is associated with poor prognosis in human glioma. Med Oncol. 2012; 29(5):3472-3477.
26. Wu Z, Sun L, Wang H, et al. MiR-328 expression is decreased in high-grade gliomas and is associated with worse survival in primary glioblastoma. PLoS One. 2012;7(10):e47270.
27. Hermansen SK, Dahlrot RH, Nielsen BS, Hansen S, Kristensen BW. MiR-21 expression in the tumor cell compartment holds unfavorable prognostic value in gliomas. J Neurooncol. 2013;111(1):71-81.
28. Huse JT, Brennan C, Hambardzumyan D, et al. The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev. 2009;23(11):1327-1337.
29. Yang G, Zhang R, Chen X, et al. MiR-106a inhibits glioma cell growth by targeting E2F1 independent of p53 status. J Mol Med (Berl). 2011; 89(10):1037-1050.
30. Malzkorn B,Wolter M, Liesenberg F, et al. Identification and functional characterization of microRNAsinvolvedin the malignant progression of gliomas. Brain Pathol. 2010;20(3):539-550.
31. Olive V, Jiang I, He L. mir-17-92, a cluster of miRNAs in the midst of the cancer network. Int J Biochem Cell Biol. 2010;42(8):1348-1354.
32. Tagawa H, Karube K, Tsuzuki S, Ohshima K, Seto M. Synergistic action of the microRNA-17 polycistron and Myc in aggressive cancer development. Cancer Sci. 2007;98(9):1482-1490.
33. Lu S, Wang S, Geng S, Ma S, Liang Z, Jiao B. Increased Expression of microRNA-17 Predicts Poor Prognosis in Human Glioma. J Biomed Biotechnol. 2012;2012:970761.
34. Ferretti E, De Smaele E, Po A, et al. MicroRNA profiling in human medulloblastoma. Int J Cancer. 2009;124(3):568-577.
35. Ferretti E, De Smaele E, Miele E, et al. Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 2008;27(19):2616-2627.
36. Venkataraman S, Birks DK, Balakrishnan I, et al. MicroRNA 218 acts as a tumor suppressor by targeting multiple cancer phenotype-associated genes in medulloblastoma. J Biol Chem. 2013;288(3):1918-1928.
37. Costa FF, Bischof JM, Vanin EF, et al. Identification of microRNAs as potential prognostic markers in ependymoma. PLoS One. 2011;6(10): e25114.
38. Ho CY, Bar E, Giannini C, et al. MicroRNA profiling in pediatric pilocytic astrocytoma reveals biologically relevant targets, including PBX3, NFIB, and METAP2. Neuro Oncol. 2013;15(1):69-82.
39. Birks DK, Barton VN, Donson AM, Handler MH, Vibhakar R, Foreman NK. Survey of MicroRNA expression in pediatric brain tumors. Pediatr Blood Cancer. 2011;56(2):211-216.
40. Ferretti E, Di Marcotullio L, Gessi M, et al. Alternative splicing of the ErbB-4 cytoplasmic domain and its regulation by hedgehog signaling identify distinct medulloblastoma subsets. Oncogene. 2006;25(55): 7267-7273.
41. Po A, Ferretti E, Miele E, et al. Hedgehog controls neural stem cells through p53-independent regulation of Nanog. EMBO J. 2010;29(15): 2646-2658.
42. Gaspar N, Marshall L, Perryman L, et al. MGMT-independent temozolomide resistance in pediatric glioblastoma cells associated with a PI3-kinase-mediated HOX/stem cell gene signature. Cancer Res. 2010;70(22):9243-9252.
43. Takeshita I, Takaki T, Kuramitsu M, et al. Characteristics of an established human glioma cell line, KNS-42. Neurol Med Chir (Tokyo). 1987;27(7):581-587.
44. de Biase D, Visani M, Morandi L, et al. miRNAs expression analysis in paired fresh/frozen and dissected formalin fixed and paraffin embedded glioblastoma using real-time pCR. PLoS One. 2012;7(4): e35596.
45. Sung T, Miller DC, Hayes RL, Alonso M, Yee H, Newcomb EW. Preferential inactivation of the p53 tumor suppressor pathway and lack of EGFR amplification distinguish de novo high grade pediatric astrocytomas from de novo adult astrocytomas. Brain Pathol. 2000; 10(2):249-259.
46. Puget S, Philippe C, Bax DA, et al. Mesenchymal transition and PDGFRA amplification/mutation are key distinct oncogenic events in pediatric diffuse intrinsic pontine gliomas. PLoS One. 2012;7(2): e30313.
47. Northcott PA, Fernandez LA, Hagan JP, et al. The miR-17/92 polycistron is up-regulated in sonic hedgehog-driven medulloblastomas and induced by N-myc in sonic hedgehog-treated cerebellar neural precursors. Cancer Res. 2009;69(8):3249-3255.
48. Luo H, Zou J, Dong Z, Zeng Q, Wu D, Liu L. Up-regulated miR-17 promotes cell proliferation, tumour growth and cell cycle progression by targeting the RND3 tumour suppressor gene in colorectal carcinoma. Biochem J. 2012;442(2):311-321.
49. Fontana L, Fiori ME, Albini S, et al. Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS One 2008 3(5) e2236.
50. Osada H, Takahashi T. let-7 and miR-17-92: small-sized major players in lung cancer development. Cancer Sci. 2011;102(1):9-17.
51. Zhou H, Guo JM, Lou YR, et al. Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using microRNA as a marker. J Mol Med (Berl). 2013;88(7):709-717.
52. DahmaneN,SanchezP, GittonY, et al.TheSonicHedgehog-Glipathway regulates dorsal brain growth and tumorigenesis. Development. 2001; 128(24):5201-5212.
53. Uziel T, Karginov FV, Xie S, et al. The miR-17-92 cluster collaborates with the Sonic Hedgehog pathway in medulloblastoma. Proc Natl Acad Sci USA. 2009;106(8):2812-2817.
54. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol. 2007;17(2): 165-172.
55. Garg N, Po A, Miele E, et al. microRNA-17-92 cluster is a direct Nanog target and controls neural stem cells through Trp53inp1. EMBO J. 2013;32(21):2819-2832.
56. Phillips HS, Kharbanda S, Chen R, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006; 9(3):157-173.
57. Faury D, Nantel A, Dunn SE, et al. Molecular profiling identifies prognostic subgroups of pediatric glioblastoma and shows increased YB-1 expression in tumors. J Clin Oncol. 2007;25(10):1196-1208.
58. Schiffman JD, Hodgson JG, VandenBerg SR, et al. Oncogenic BRAF mutation with CDKN2A inactivation is characteristic of a subset of pediatric malignant astrocytomas. Cancer Res. 2010;70(2):512-519.
59. Bielen A, Perryman L, Box GM, et al. Enhanced efficacy of IGF1R inhibition in pediatric glioblastoma by combinatorial targeting of PDGFR a/b. Mol Cancer Ther. 2011;10(8):1407-1418.
60. Plate KH, Breier G,Weich HA, Mennel HD, RisauW. Vascular endothelial growth factor and glioma angiogenesis: coordinate induction of VEGF receptors, distribution of VEGF protein and possible in vivo regulatory mechanisms. Int J Cancer. 1994;59(4):520-529.
61. Goldlust SA, Cavaliere R, Newton HB, et al. Bevacizumab for glioblastoma refractory to vascular endothelial growth factor receptor inhibitors. J Neurooncol. 2012;107(2):407-411.
62. Kamal MM, Sathyan P, Singh SK, et al. REST regulates oncogenic properties of glioblastoma stemcells. Stem Cells. 2012;30(3):405-414.
63. Schiebe M, Ohneseit P, Hoffmann W, Meyermann R, Rodemann HP, Bamberg M. Analysis of mdm2 and p53 gene alterations in glioblastomas and its correlation with clinical factors. J Neurooncol. 2000;49(3):197-203.
64. Becher OJ, Hambardzumyan D, Fomchenko EI, et al. Gli activity correlates with tumor grade in platelet-derived growth factorinduced gliomas. Cancer Res. 2008;68(7):2241-2249.
65. Hulleman E, Helin K. Molecular mechanisms in gliomagenesis. Adv Cancer Res. 2005;94:1-27.
66. Hong L, Lai M, Chen M, et al. The miR-17-92 cluster of microRNAs confers tumorigenicity by inhibiting oncogene-induced senescence. Cancer Res. 2010;70(21):8547-8557.
67. Ernst A, Campos B, Meier J, et al. De-repression of CTGFvia the miR-17- 92 cluster upon differentiation of human glioblastoma spheroid cultures. Oncogene. 2010;29(23):3411-3422