Targeting the SMO oncogene by miR-326 inhibits glioma biological behaviors and stemness

Neuro-Oncology

Volumn 17, Issue 2, 2015, Pages 243-253

  Du, Wenzhong ^a   Liu, Xing ^a   Chen, Lingchao ^a   Dou, Zhijin ^a   Lei, Xuhui ^a   Chang, Liang ^b   Cai, Jinquan ^a   Cui, Yuqiong ^a   Yang, Dongbo ^a   Sun, Ying ^a   Li, Yongli ^a   Jiang, Chuanlu ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

glioma; hedgehog; miRNA; SMO; stemness

Indexed keywords

LIPOCORTIN 5; MICRORNA; MICRORNA 326; SMALL INTERFERING RNA; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; MIRN326 MICRORNA, HUMAN; SMO PROTEIN, HUMAN;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GRADING; CANCER STEM CELL; CARCINOGENICITY; CELL COUNTING; CHILD; CLINICAL ARTICLE; FEMALE; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LUCIFERASE ASSAY; MALE; MIDDLE AGED; MOUSE; NONHUMAN; ONCOGENE; PRESCHOOL CHILD; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; SURVIVAL TIME; TUMOR DIFFERENTIATION; TUMOR VOLUME; UPREGULATION; WESTERN BLOTTING; YOUNG ADULT; ANIMAL; BAGG ALBINO MOUSE; BRAIN TUMOR; GLIOBLASTOMA; KAPLAN MEIER METHOD; METABOLISM; NUDE MOUSE; SIGNAL TRANSDUCTION; SURVIVAL RATE; TUMOR CELL LINE;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; GLIOBLASTOMA; HEDGEHOG PROTEINS; HUMANS; KAPLAN-MEIER ESTIMATE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; NEOPLASTIC STEM CELLS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SURVIVAL RATE; UP-REGULATION;

EID: 84924959079     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nou217     Document Type: Article

References (50)

1. Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459-466.
2. Garner JM, Fan M, Yang CH, et al. Constitutive activation of signal transducer and activator of transcription 3 (STAT3) and nuclear factor kB signaling in glioblastoma cancer stem cells regulates the Notch pathway. J Biol Chem. 2013;288(36):26167-26176.
3. Sareddy GR, Kesanakurti D, Kirti PB, et al. Nonsteroidal anti-inflammatory drugs diclofenac and celecoxib attenuates Wnt/beta-catenin/Tcf signaling pathway in human glioblastoma cells. Neurochem Res. 2013;38(11):2313-2322.
4. Kim E, Kim M, Woo DH, et al. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells. Cancer Cell. 2013; 23(6):839-852.
5. Clement V, Sanchez P, de Tribolet N, et al. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol. 2007;17(2):165-172.
6. Echelard Y, Epstein DJ, St-Jacques B, et al. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 1993;75(7): 1417-1430.
7. Stone DM, Hynes M, Armanini M, et al. The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature. 1996;384(6605):129-134.
8. Jiang J, Hui CC. Hedgehog signaling in development and cancer. Dev Cell. 2008;15(6):801-812.
9. Gao J, Graves S, Koch U, et al. Hedgehog signaling is dispensable for adult hematopoietic stem cell function. Cell Stem Cell. 2009; 4(6):548-558.
10. Zhang Z, Lv X, Jiang J, et al. Dual roles of Hh signaling in the regulation of somatic stem cell self-renewal and germline stem cell maintenance in Drosophila testis. Cell Res. 2013;23(4): 573-576.
11. Milla LA, Arros A, Espinoza N, et al. Neogenin1 is a sonic hedgehog target in medulloblastoma and is necessary for cell cycle progression. Int J Cancer. 2014;134(1):21-31.
12. Tang S, Bonaroti J, Unlu S, et al. Sweating the small stuff: microRNAs and genetic changes define pancreatic cancer. Pancreas. 2013;42(5):740-759.
13. Pinho FG, Frampton AE, Nunes J, et al. Downregulation of microRNA-515-5p by the estrogen receptor modulates sphingosine kinase 1 and breast cancer cell proliferation. Cancer Res. 2013;73(19):5936-5948.
14. Siemens H, Neumann J, Jackstadt R, et al. Detection of miR-34a promoter methylation in combination with elevated expression of c-Met and beta-catenin predicts distant metastasis of colon cancer. Clin Cancer Res. 2013;19(3):710-720.
15. Cai J, Wu J, Zhang H, et al. miR-186 downregulation correlates with poor survival in lung adenocarcinoma, where it interferes with cell-cycle regulation. Cancer Res. 2013;73(2):756-766.
16. Agatheeswaran S, Singh S, Biswas S, et al. BCR-ABL mediated repression of miR-223 results in the activation of MEF2C and PTBP2 in chronic myeloid leukemia. Leukemia. 2013;27(7): 1578-1580.
17. Li H, Yang BB. Stress response of glioblastoma cells mediated by miR-17-5p targeting PTEN and the passenger strand miR-17-3p targeting MDM2. Oncotarget. 2012;3(12):1653-1668.
18. Shi Z, Zhang J, Qian X, et al. AC1MMYR2, an inhibitor of dicer-mediated biogenesis of Oncomir miR-21, reverses epithelial-mesenchymal transition and suppresses tumor growth and progression. Cancer Res. 2013;73(17):5519-5531.
19. Liu C, Tang DG. MicroRNA regulation of cancer stem cells. Cancer Res. 2011;71(18):5950-5954.
20. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-297.
21. Aranha MM, Santos DM, Sola S, et al. miR-34a regulates mouse neural stem cell differentiation. PloS One. 2011;6(8): e21396.
22. Chen L, Zhang A, Li Y, et al. MiR-24 regulates the proliferation and invasion of glioma by ST7L via beta-catenin/Tcf-4 signaling. Cancer Lett. 2013;329(2):174-180.
23. Zhang KL, Han L, Chen LY, et al. Blockage of a miR-21/EGFR regulatory feedback loop augments anti-EGFR therapy in glioblastomas. Cancer Lett. 2014;342(1):139-149.
24. Beier D, Hau P, Proescholdt M, et al. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 2007;67(9): 4010-4015.
25. Obernosterer G, Martinez J, Alenius M. Locked nucleic acid-based in situ detection of microRNAs in mouse tissue sections. Nat Protoc. 2007;2(6):1508-1514.
26. Du WZ, Feng Y, Wang XF, et al. Curcumin suppresses malignant glioma cells growth and induces apoptosis by inhibition of SHH/GLI1 signaling pathway in vitro and vivo. CNS Neurosci Ther. 2013;19(12):926-936.
27. Chen L, Zhang J, Feng Y, et al. MiR-410 regulates MET to influence the proliferation and invasion of glioma. Int J Biochem Cell Biol. 2012;44(11):1711-1717.
28. Zhou X, Ren Y, Moore L, et al. Downregulation of miR-21 inhibits EGFR pathway and suppresses the growth of human glioblastoma cells independent of PTEN status. Lab Invest. 2010; 90(2):144-155.
29. Zhu ZH, Sun BY, Ma Y, et al. Three immunomarker support vector machines-based prognostic classifiers for stage IB non-small-cell lung cancer. J Clin Oncol. 2009;27(7):1091-1099.
30. 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. 2009;29(48): 15161-15168.
31. Zhou J, Xu T, Yan Y, et al. MicroRNA-326 functions as a tumor suppressor in glioma by targeting the Nin one binding protein (NOB1). PloS One. 2013;8(7):e68469.
32. Kefas B, Comeau L, Erdle N, et al. Pyruvate kinase M2 is a target of the tumor-suppressive microRNA-326 and regulates the survival of glioma cells. Neuro Oncol. 2010;12(11):1102-1112.
33. Zbinden M, Duquet A, Lorente-Trigos A, et al. NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J. 2010; 29(15):2659-2674.
34. Ehtesham M, Sarangi A, Valadez JG, et al. Ligand-dependent activation of the hedgehog pathway in glioma progenitor cells. Oncogene. 2007;26(39):5752-5761.
35. Dlugosz AA, Talpaz M. Following the hedgehog to new cancer therapies. New Engl J Med. 2009;361(12):1202-1205.
36. Atwood SX, Li M, Lee A, et al. GLI activation by atypical protein kinase C iota/lambda regulates the growth of basal cell carcinomas. Nature. 2013;494(7438):484-488.
37. Bohinc B, Michelotti G, Diehl AM. Hedgehog signaling in human medullary thyroid carcinoma: a novel signaling pathway. Thyroid. 2013;23(9):1119-1126.
38. Shao J, Zhang L, Gao J, et al. Aberrant expression of PTCH (patched gene) and Smo (smoothened gene) in human pancreatic cancerous tissues and its association with hyperglycemia. Pancreas. 2006;33(1):38-44.
39. Babashah S, Sadeghizadeh M, Hajifathali A, et al. Targeting of the signal transducer Smo links microRNA-326 to the oncogenic Hedgehog pathway in CD34+ CML stem/progenitor cells. Int J Cancer. 2013;133(3):579-589.
40. 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.
41. Gialmanidis IP, Bravou V, Amanetopoulou SG, et al. Overexpression of hedgehog pathway molecules and FOXM1 in non-small cell lung carcinomas. Lung Cancer. 2009;66(1):64-74.
42. Dijkgraaf GJ, Alicke B, Weinmann L, et al. Small molecule inhibition of GDC-0449 refractory smoothened mutants and downstream mechanisms of drug resistance. Cancer Res. 2011; 71(2):435-444.
43. Bar EE, Chaudhry A, Lin A, et al. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells. 2007;25(10):2524-2533.
44. Sarangi A, Valadez JG, Rush S, et al. Targeted inhibition of the Hedgehog pathway in established malignant glioma xenografts enhances survival. Oncogene. 2009;28(39):3468-3476.
45. You M, Varona-Santos J, Singh S, et al. Targeting of the Hedgehog signal transduction pathway suppresses survival of malignant pleural mesothelioma cells in vitro. J Thorac Cardiovasc Surg. 2014;147(1):508-516.
46. Eimer S, Dugay F, Airiau K, et al. Cyclopamine cooperates with EGFR inhibition to deplete stem-like cancer cells in glioblastoma-derived spheroid cultures. Neuro Oncol. 2012; 14(12):1441-1451.
47. Takezaki T, Hide T, Takanaga H, et al. Essential role of the Hedgehog signaling pathway in human glioma-initiating cells. Cancer Sci. 2011;102(7):1306-1312.
48. Wang S, Lu S, Geng S, et al. Expression and clinical significance of microRNA-326 in human glioma miR-326 expression in glioma. Med Oncol. 2013;30(1):373.
49. Qiu S, Lin S, Hu D, et al. Interactions of miR-323/miR-326/miR-329 and miR-130a/miR-155/miR-210 as prognostic indicators for clinical outcome of glioblastoma patients. J Transl Med. 2013;11: 10.
50. Santini R, Vinci MC, Pandolfi S, et al. Hedgehog-GLI signaling drives self-renewal and tumorigenicity of human melanoma-initiating cells. Stem Cells. 2012;30(9):1808-1818.