NF-κB induces miR-148a to sustain TGF-β/Smad signaling activation in glioblastoma

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  Wang, Hui ^a   Pan, Jian Qing ^b,c   Luo, Lun ^a   Ning, Xin jie X ^a   Ye, Zhuo Peng ^a   Yu, Zhe ^c   Li, Wen Sheng ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b The 6th Affiliated Hospital of Shenzhen University Health Science Center   (China)

^c Guangzhou Biocare Cancer Institute   (China)

Author keywords

Aggressiveness; Glioblastomas; miR 148a; NF B; QKI; TGF

Indexed keywords

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MICRORNA 148A; PROTEIN QUAKING; RNA BINDING PROTEIN; RNA INDUCED SILENCING COMPLEX; S PHASE KINASE ASSOCIATED PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 1; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; MIRN148 MICRORNA, HUMAN; QKI PROTEIN, HUMAN; SKP1 PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CELL INVASION; CONTROLLED STUDY; GENE; GENE EXPRESSION; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; MITOGEN INDUCIBLE GENE 6; MOUSE; NONHUMAN; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; BRAIN TUMOR; CARCINOGENESIS; DISEASE COURSE; GENETICS; METABOLISM; MOLECULAR GENETICS; NEOVASCULARIZATION (PATHOLOGY); NUCLEOTIDE SEQUENCE; NUDE MOUSE; PATHOLOGY; PROGNOSIS; TUMOR CELL LINE; TUMOR INVASION; UPREGULATION; VASCULARIZATION;

MUS MUSCULUS;

ANIMALS; BASE SEQUENCE; BRAIN NEOPLASMS; CARCINOGENESIS; CELL LINE, TUMOR; DISEASE PROGRESSION; GLIOBLASTOMA; HUMANS; MICE, NUDE; MICRORNAS; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B; PHENOTYPE; PROGNOSIS; RNA-BINDING PROTEINS; S-PHASE KINASE-ASSOCIATED PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 84929320152     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-14-2     Document Type: Article

References (52)

1. Kotliarova S, Fine HA: SnapShot: glioblastoma multiforme. Cancer Cell 2012,21(710-710):e711.
2. Wen PY, Kesari S: Malignant gliomas in adults. N Engl J Med 2008, 359:492-507. 10.1056/NEJMra0708126
3. Johnson DR, Leeper HE, Uhm JH: Glioblastoma survival in the United States improved after Food and Drug Administration approval of bevacizumab: a population-based analysis. Cancer 2013, 119:3489-3495.
4. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, et al.: A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 2001, 95:190-198. 10.3171/jns.2001.95.2.0190
5. Markowitz SD, Roberts AB: Tumor suppressor activity of the TGF-beta pathway in human cancers. Cytokine Growth Factor Rev 1996, 7:93-102. 10.1016/1359-6101(96)00001-9
6. Reiss M: TGF-beta and cancer. Microbes Infect 1999, 1:1327-1347. 10.1016/S1286-4579(99)00251-8
7. Akhurst RJ, Balmain A: Genetic events and the role of TGF beta in epithelial tumour progression. J Pathol 1999, 187:82-90. 10.1002/(SICI)1096-9896(199901)187:1<82::AID-PATH248>3.0.CO;2-8
8. Siegel PM, Massague J: Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003, 3:807-821. 10.1038/nrc1208
9. Pardali K, Moustakas A: Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim Biophys Acta 2007, 1775:21-62.
10. Bierie B, Moses HL: TGF-beta and cancer. Cytokine Growth Factor Rev 2006, 17:29-40. 10.1016/j.cytogfr.2005.09.006
11. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, et al.: Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007, 21:2683-2710. 10.1101/gad.1596707
12. Seoane J, Le HV, Shen L, Anderson SA, Massague J: Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 2004, 117:211-223. 10.1016/S0092-8674(04)00298-3
13. Bruna A, Darken RS, Rojo F, Ocana A, Penuelas S, Arias A, et al.: High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 2007, 11:147-160. 10.1016/j.ccr.2006.11.023
14. Ikushima H, Todo T, Ino Y, Takahashi M, Miyazawa K, Miyazono K: Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell Stem Cell 2009, 5:504-514. 10.1016/j.stem.2009.08.018
15. Penuelas S, Anido J, Prieto-Sanchez RM, Folch G, Barba I, Cuartas I, et al.: TGF-beta increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell 2009, 15:315-327. 10.1016/j.ccr.2009.02.011
16. Hong S, Lim S, Li AG, Lee C, Lee YS, Lee EK, et al.: Smad7 binds to the adaptors TAB2 and TAB3 to block recruitment of the kinase TAK1 to the adaptor TRAF2. Nat Immunol 2007, 8:504-513. 10.1038/ni1451
17. Lee YS, Kim JH, Kim ST, Kwon JY, Hong S, Kim SJ, et al.: Smad7 and Smad6 bind to discrete regions of Pellino-1 via their MH2 domains to mediate TGF-beta1-induced negative regulation of IL-1R/TLR signaling. Biochem Biophys Res Commun 2010, 393:836-843. 10.1016/j.bbrc.2010.02.094
18. Song L, Liu L, Wu Z, Li Y, Ying Z, Lin C, et al.: TGF-beta induces miR-182 to sustain NF-kappaB activation in glioma subsets. J Clin Invest 2012, 122:3563-3578. 10.1172/JCI62339
19. Vernet C, Artzt K: STAR, a gene family involved in signal transduction and activation of RNA. Trends Genet 1997, 13:479-484. 10.1016/S0168-9525(97)01269-9
20. Chen T, Richard S: Structure-function analysis of Qk1: a lethal point mutation in mouse quaking prevents homodimerization. Mol Cell Biol 1998, 18:4863-4871.
21. Wu J, Zhou L, Tonissen K, Tee R, Artzt K: The quaking I-5 protein (QKI-5) has a novel nuclear localization signal and shuttles between the nucleus and the cytoplasm. J Biol Chem 1999, 274:29202-29210. 10.1074/jbc.274.41.29202
22. Aberg K, Saetre P, Jareborg N, Jazin E: Human QKI, a potential regulator of mRNA expression of human oligodendrocyte-related genes involved in schizophrenia. Proc Natl Acad Sci U S A 2006, 103:7482-7487. 10.1073/pnas.0601213103
23. Haroutunian V, Katsel P, Dracheva S, Davis KL: The human homolog of the QKI gene affected in the severe dysmyelination "quaking" mouse phenotype: downregulated in multiple brain regions in schizophrenia. Am J Psychiatry 2006, 163:1834-1837. 10.1176/ajp.2006.163.10.1834
24. Cesari R, Martin ES, Calin GA, Pentimalli F, Bichi R, McAdams H, et al.: Parkin, a gene implicated in autosomal recessive juvenile parkinsonism, is a candidate tumor suppressor gene on chromosome 6q25-q27. Proc Natl Acad Sci U S A 2003, 100:5956-5961. 10.1073/pnas.0931262100
25. Smith DI, Zhu Y, McAvoy S, Kuhn R: Common fragile sites, extremely large genes, neural development and cancer. Cancer Lett 2006, 232:48-57. 10.1016/j.canlet.2005.06.049
26. Mulholland PJ, Fiegler H, Mazzanti C, Gorman P, Sasieni P, Adams J, et al.: Genomic profiling identifies discrete deletions associated with translocations in glioblastoma multiforme. Cell Cycle 2006, 5:783-791. 10.4161/cc.5.7.2631
27. Ichimura K, Mungall AJ, Fiegler H, Pearson DM, Dunham I, Carter NP, et al.: Small regions of overlapping deletions on 6q26 in human astrocytic tumours identified using chromosome 6 tile path array-CGH. Oncogene 2006, 25:1261-1271. 10.1038/sj.onc.1209156
28. Chen AJ, Paik JH, Zhang H, Shukla SA, Mortensen R, Hu J, et al.: STAR RNA-binding protein Quaking suppresses cancer via stabilization of specific miRNA. Genes Dev 2012, 26:1459-1472. 10.1101/gad.189001.112
29. Gavino C, Richard S: Loss of p53 in quaking viable mice leads to Purkinje cell defects and reduced survival. Sci Rep 2011, 1:84.
30. Ishii N, Maier D, Merlo A, Tada M, Sawamura Y, Diserens AC, et al.: Frequent co-alterations of TP53, p16/CDKN2A, p14ARF, PTEN tumor suppressor genes in human glioma cell lines. Brain Pathol 1999, 9:469-479. 10.1111/j.1750-3639.1999.tb00536.x
31. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szasz AM, Wang ZC, et al.: A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 2009, 137:1032-1046. 10.1016/j.cell.2009.03.047
32. Subramanyam D, Lamouille S, Judson RL, Liu JY, Bucay N, Derynck R, et al.: Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat Biotechnol 2011, 29:443-448. 10.1038/nbt.1862
33. Wang Y, Vogel G, Yu Z, Richard S: The QKI-5 and QKI-6 RNA binding proteins regulate the expression of microRNA 7 in glial cells. Mol Cell Biol 2013, 33:1233-1243. 10.1128/MCB.01604-12
34. Kim J, Zhang Y, Skalski M, Hayes J, Kefas B, Schiff D, et al.: MicroRNA-148a is a prognostic oncomiR that targets MIG6 and BIM to regulate EGFR and apoptosis in glioblastoma. Cancer Res 2014, 74:1541-1553. 10.1158/0008-5472.CAN-13-1449
35. Piek E, Heldin CH, Ten Dijke P: Specificity, diversity, and regulation in TGF-beta superfamily signaling. FASEB J 1999, 13:2105-2124.
36. Massague J, Chen YG: Controlling TGF-beta signaling. Genes Dev 2000, 14:627-644.
37. Heldin CH, Miyazono K, ten Dijke P: TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997, 390:465-471. 10.1038/37284
38. Fukuchi M, Imamura T, Chiba T, Ebisawa T, Kawabata M, Tanaka K, et al.: Ligand-dependent degradation of Smad3 by a ubiquitin ligase complex of ROC1 and associated proteins. Mol Biol Cell 2001, 12:1431-1443. 10.1091/mbc.12.5.1431
39. Lu W, Feng F, Xu J, Lu X, Wang S, Wang L, et al.: QKI impairs self-renewal and tumorigenicity of oral cancer cells via repression of SOX2. Cancer Biol Ther 2014,15(9):1174-84. 10.4161/cbt.29502
40. Zhao Y, Zhang G, Wei M, Lu X, Fu H, Feng F, et al.: The tumor suppressing effects of QKI-5 in prostate cancer: a novel diagnostic and prognostic protein. Cancer Biol Ther 2014, 15:108-118. 10.4161/cbt.26722
41. Bian Y, Wang L, Lu H, Yang G, Zhang Z, Fu H, et al.: Downregulation of tumor suppressor QKI in gastric cancer and its implication in cancer prognosis. Biochem Biophys Res Commun 2012, 422:187-193. 10.1016/j.bbrc.2012.04.138
42. Ji S, Ye G, Zhang J, Wang L, Wang T, Wang Z, et al.: miR-574-5p negatively regulates Qki6/7 to impact beta-catenin/Wnt signalling and the development of colorectal cancer. Gut 2013, 62:716-726. 10.1136/gutjnl-2011-301083
43. Galardi S, Mercatelli N, Farace MG, Ciafre SA: NF-kB and c-Jun induce the expression of the oncogenic miR-221 and miR-222 in prostate carcinoma and glioblastoma cells. Nucleic Acids Res 2011, 39:3892-3902. 10.1093/nar/gkr006
44. Song L, Lin C, Gong H, Wang C, Liu L, Wu J, et al.: miR-486 sustains NF-kappaB activity by disrupting multiple NF-kappaB-negative feedback loops. Cell Res 2013, 23:274-289. 10.1038/cr.2012.174
45. Jiang L, Wu J, Yang Y, Liu L, Song L, Li J, et al.: Bmi-1 promotes the aggressiveness of glioma via activating the NF-kappaB/MMP-9 signaling pathway. BMC Cancer 2012, 12:406. 10.1186/1471-2407-12-406
46. Liang F, Zhang S, Wang B, Qiu J, Wang Y: Overexpression of integrin-linked kinase (ILK) promotes glioma cell invasion and migration and down-regulates E-cadherin via the NF-kappaB pathway. J Mol Histol 2014, 45:141-151. 10.1007/s10735-013-9540-5
47. Holland EC: Gliomagenesis: genetic alterations and mouse models. Nat Rev Genet 2001, 2:120-129. 10.1038/35052535
48. Zhu Y, Parada LF: The molecular and genetic basis of neurological tumours. Nat Rev Cancer 2002, 2:616-626. 10.1038/nrc866
49. Joseph JV, Balasubramaniyan V, Walenkamp A, Kruyt FA: TGF-beta as a therapeutic target in high grade gliomas - promises and challenges. Biochem Pharmacol 2013, 85:478-485. 10.1016/j.bcp.2012.11.005
50. Seoane J: The TGFBeta pathway as a therapeutic target in cancer. Clin Transl Oncol 2008, 10:14-19. 10.1007/s12094-008-0148-2
51. Yingling JM, Blanchard KL, Sawyer JS: Development of TGF-beta signalling inhibitors for cancer therapy. Nat Rev Drug Discov 2004, 3:1011-1022. 10.1038/nrd1580
52. Li J, Zhang N, Song LB, Liao WT, Jiang LL, Gong LY, et al.: Astrocyte elevated gene-1 is a novel prognostic marker for breast cancer progression and overall patient survival. Clin Cancer Res 2008, 14:3319-3326. 10.1158/1078-0432.CCR-07-4054