MicroRNA-9 inhibits vasculogenic mimicry of glioma cell lines by suppressing Stathmin expression

Journal of Neuro-Oncology

Volumn 115, Issue 3, 2013, Pages 381-390

  Song, Yuwen ^a   Mu, Luyan ^a   Han, Xuezhe ^b   Li, Qingla ^a   Dong, Baijing ^a   Li, Hulun ^a,c   Liu, Xiaoqian ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c Key Laboratory of Myocardial Ischemia Mechanism   (China)

Author keywords

Glioma; MicroRNA 9; Stathmin; Vasculogenic mimicry

Indexed keywords

LUCIFERASE; MESSENGER RNA; MICRORNA 9; STATHMIN;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER SIZE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE FUNCTION; GENETIC TRANSFECTION; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROTUBULE; MOLECULAR INTERACTION; MOLECULAR MIMICRY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION; VASCULOGENIC MIMICRY;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL CYCLE; CELL PROLIFERATION; GLIOMA; HUMANS; IMMUNOENZYME TECHNIQUES; LUCIFERASES; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; NEOVASCULARIZATION, PATHOLOGIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; STATHMIN; TUMOR CELLS, CULTURED;

EID: 84890313818     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-013-1245-9     Document Type: Article

References (46)

1. Rubin CI, Atweh GF (2004) The role of Stathmin in the regulation of the cell cycle. J Cell Biochem 93:242-250
2. Bhat KM, Setaluri V (2007) Microtubule-associated proteins as targets in cancer chemotherapy. Clin Cancer Res 13:2849-2854
3. Leibl S, Zigeuner R, Hutterer G et al (2008) EGFR expression in urothelial carcinoma of the upper urinary tract is associated with disease progression and metaplastic morphology. APMIS 116:27-32
4. Cassimeris L (2002) The oncoprotein 18/Stathmin family of microtubule destabilizers. Curr Opin Cell Biol 14:18-24
5. Rana S, Maples PB, Senzer N et al (2008) Stathmin 1: a novel therapeutic target for anticancer activity. Expert Rev Anticancer Ther 8:1461-1470
6. Dong B, Mu L, Qin X et al (2012) Stathmin expression in glioma-derived microvascular endothelial cells: a novel therapeutic target. Oncol Rep 27:714-718
7. Iorio MV, Croce CM (2009) MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol 27:5848-5856
8. Omura N, Li CP, Li A, Hong SM et al (2008) Genome-wide profiling of methylated promoters in pancreatic adenocarcinoma. Cancer Biol Ther 7:1146-1156
9. Bandres E, Agirre X, Bitarte N et al (2009) Epigenetic regulation of microRNA expression in colorectal cancer. Int J Cancer 125:2737-2743
10. Hildebrandt MA, Gu J, Lin J et al (2010) Hsa-miR-9 methylation status is associated with cancer development and metastatic recurrence in patients with clear cell renal cell carcinoma. Oncogene 29:5724-5728
11. Krichevsky AM, King KS, Donachue CP et al (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9:1274-1281
12. Krichevsky AM, Sonntag KC, Isacson O et al (2006) Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24:857-864
13. Delaloy C, Gao FB (2010) A new role for microRNA-9 in human progenitor cells. Cell Cycle 15:2913-2914
14. Delaloy C, Liu L, Lee JA et al (2010) MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 4:323-335
15. Shibata M, Kurokawa D, Nakao H et al (2008) MicroRNA-9 #odulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. J Neurosci 41:10415-10421
16. Li Y, Wang F, Lee JA et al (2006) MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Gene Dev 20:2793-2805
17. Otaegi G, Pollock A, Hong J et al (2011) MicroRNA miR-9 modifies motor neuron columns by a tuning regulation of FoxP1 levels in developing spinal cords. J Neurosci 3:809-818
18. Bonev B, Pisco A, Papalopulu N (2011) MicroRNA-9 reveals regional diversity of neural progenitors along the anterior-posterior axis. Dev Cell 1:19-32
19. Holmfeldt P, Sellin ME, Gullberg M (2009) Predominant regulators of tubulin monomer-polymer partitioning and their implication for cell polarization. Cell Mol Life Sci 66:3263-3276
20. Ingber D, Prusty D, Zhengqi S et al (1995) Cell shape, cytoskeletal mechanics and cell cycle control in angiogenesis. J Biomech 28:1471-1484
21. Petrovic V, Costa RH, Lau LF et al (2008) FoxM1 regulates growth factor-induced expression of kinase-interacting stathmin to promote cell cycle progression. J Biol Chem 283:453-460
22. Kouzu Y, Uzawa K, Koike H et al (2006) Overexpression of Stathmin in oral squamous-cell carcinoma: correlation with tumour progression and poor prognosis. Br J Cancer 94:717-723
23. Yuan RH, YM J, Chen HL et al (2006) Stathmin overexpression cooperates with p53 mutation and osteopontin overexpression, and is associated with tumour progression, early recurrence, and poor prognosis in hepatocellular carcinoma. J Pathol 209:549-558
24. Ghosh R, Gu G, Tillman E et al (2007) Increased expression and differential phosphorylation of stathmin may promote prostate cancer progression. Prostate 67:1038-1052
25. Wang R, Dong K, Lin F et al (2007) Inhibiting proliferation and enhancing chemosensitivity to taxanes in osteosarcoma cells by RNA interference-mediated down- regulation of Stathmin expression. Mol Med 13:567-575
26. Alli E, Yang JM, Hait WN (2007) Silencing of Stathmin induces tumor-suppressor function in breast cancer cell lines harboring mutant p53. Oncogene 26:1003-1012
27. Johnsen JI, Aurelio ON, Kwaja Z et al (2000) p53-mediated negative regulation of Stathmin/Op18 expression is associated with G2/M cell-cycle arrest. Int J Cancer 88:685-691
28. Ngo TT, Peng T, Liang XJ et al (2007) The 1p-encoded protein stathmin and resistance of malignant gliomas to nitrosoureas. J Natl Cancer Inst 99:639-652
29. Liang XJ, Choi Y, Sackett DL et al (2008) Nitrosoureas inhibit the stathmin-mediated migration and invasion of malignant glioma cells. Cancer Res 68:5267-5272
30. Wong QW, Lung EW, Law PT et al (2008) MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin 1. Gastroenterology 135:257-269
31. Wang J, Gu Z, Ni P et al (2011) NF-kappaB P50/P65 hetero-dimer mediates differential regulation of CD166/ALCAM expression via interaction with micoRNA-9 after serum deprivation, providing evidence for a novel negative auto-regulatory loop. Nucleic Acids Res 15:6440-6455
32. Myatt S, Wang J, Monteiro L et al (2010) Definition of microRNAs that repression expression of the tumor suppressor gene FOXO1 in endometrial cancer. Cancer Res 70:367-377
33. Ma L, Young J, Prabhala H et al (2010) miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Mat cell Biol 3:247-256
34. Luo H, Zhang H, Zhang Z et al (2009) Down-regulated miR-9 and miR-433 in human gastric carcinoma. J Exp Clin Cancer Res 28:82
35. Wan H, Guo L, Liu T et al (2010) Regulation of the transcription factor NF-kB1 by micro RNA-9 in human gastric adenocarcinoma. Mole Cancer 9:16
36. Laios A, O'Toole S, Flavin R et al (2008) Potential role of miR-9 and miR-223 in recurrent ovarian cancer. Mole Cancer 7:35
37. Arora H, Qureshi R, Jin S et al (2011) miR-9 and let-7g enhance the sensitivity to ionizing radiation by suppression of NFkappaB1. Exp Mole Med 5:298-304
38. Nass D, Rosenwald S, Meiri E et al (2009) MiR-92b and miR-9/9are specifically expressed in brain primary tumors and can be used to differentiate primary from metastatic brain tumors. Brain Pathol 19:375-383
39. Jeon H, Sohn Y, Oh S et al (2011) ID4 Imparts chemoresistance and cancer stemness to glioma cells by derepressing miR-9-mediated suppression of SOX2. Cancer Res 9:3410-3421
40. Schraivogel D, Weimann L, Beier D et al (2011) CAMTA1 is a novel tumour suppressor regulated by miR-9/9in glioblastoma stem cells. EMBOJ 20:4309-4322
41. Ben-Hamo R, Efroni S (2011) Gene expression and network-based analysis reveals a novel role for hsa-miR-9 and drug control over the p38 network in glioblastoma multiforme progression. Genome Med 3(11):77
42. Chao T, Zhang Y, Yan X et al (2008) Mir-9 regulates the expression of CBX7 in Human Glioma. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 30:268-274
43. Maniotis AJ, Folberg R, Hess A et al (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155:739-752
44. Folberg R, Maniotis AJ (2004) Vasculogenic mimicry. APMIS 112:508-525
45. Wang S, Yu L, Ling G et al (2012) Vasculogenic mimicry and its clinical significance in medulloblastoma. Cancer Biol Ther 5:341-348
46. Chen Y, Jing Z, Luo C et al (2012) Vasculogenic mimicry-potential target for glioma therapy: an in vitro and in vivo study. Med Oncol 29:324-331