TGF-β induces miR-182 to sustain NF-κB activation in glioma subsets

Journal of Clinical Investigation

Volumn 122, Issue 10, 2012, Pages 3563-3578

  Song, Libing ^a   Liu, Liping ^a   Wu, Zhiqiang ^b,c   Li, Yun ^b,c   Ying, Zhe ^b,c   Lin, Chuyong ^b   Wu, Jueheng ^b,c   Hu, Bo ^d   Cheng, Shi Yuan ^d   Li, Mengfeng ^b,c   Li, Jun ^b  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA 182;

ADENOID CYSTIC CARCINOMA; ARTICLE; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA; HUMAN; IN VITRO STUDY; IN VIVO STUDY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; GENES, REPORTER; GLIOMA; HUMANS; I-KAPPA B KINASE; I-KAPPA B PROTEINS; MICE; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA; RNA, NEOPLASM; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEINS; UBIQUITINATION;

EID: 84867164086     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI62339     Document Type: Article

References (63)

1. Pikarsky E, et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature. 2004;431(7007):461-466. (Pubitemid 39329586)
2. Karin M, Greten FR. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol. 2005;5(10):749-759. (Pubitemid 41400849)
3. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature. 2006; 441(7092):431-436. (Pubitemid 44050137)
4. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell. 2008;132(3):344-362.
5. Wertz IE, Dixit VM. Signaling to NF-kappaB: regulation by ubiquitination. Cold Spring Harb Perspect Biol. 2010;2(3):a003350.
6. Liu S, Chen ZJ. Expanding role of ubiquitination in NF-kappaB signaling. Cell Res. 2011;21(1):6-21.
7. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell. 2006;22(2):245-257.
8. Wang C, et al. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature. 2001;412(6844):346-351. (Pubitemid 32694385)
9. Deng L, et al. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitinconjugating enzyme complex and a unique polyubiquitin chain. Cell. 2000;103(2):351-361.
10. Ghosh S, Baltimore D. Activation in vitro of NF-kappa B by phosphorylation of its inhibitor I kappa B. Nature. 1990;344(6267):678-682.
11. Chen ZJ, Parent L, Maniatis T. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination- dependent protein kinase activity. Cell. 1996; 84(6):853-862. (Pubitemid 26106855)
12. Tokunaga F, et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat Cell Biol. 2009;11(2):123-132.
13. Xia ZP, et al. Direct activation of protein kinases by unanchored polyubiquitin chains. Nature. 2009; 461(7260):114-119.
14. Duwel M, Hadian K, Krappmann D. Ubiquitin conjugation and deconjugation in NF-kappaB signaling. Subcell Biochem. 2010;54:88-99.
15. Lee EG, et al. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science. 2000;289(5488):2350-2354.
16. Kovalenko A, et al. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature. 2003;424(6950):801-805. (Pubitemid 37021712)
17. Trompouki E, et al. CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature. 2003; 424(6950):793-796. (Pubitemid 37021710)
18. Sun SC. CYLD: a tumor suppressor deubiquitinase regulating NF-kappaB activation and diverse biological processes. Cell Death Differ. 2010;17(1):25-34.
19. Wertz IE, et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature. 2004;430(7000):694-699.
20. Evans PC, et al. Zinc-finger protein A20, a regulator of inflammation and cell survival, has de-ubiquitinating activity. Biochem J. 2004;378(pt 3):727-734. (Pubitemid 38406847)
21. Hymowitz SG, Wertz IE. A20: from ubiquitin editing to tumour suppression. Nat Rev Cancer. 2010; 10(5):332-341.
22. Huang L, et al. ABINs inhibit EGF receptor-mediated NF-kappaB activation and growth of EGF receptor- overexpressing tumour cells. Oncogene. 2008; 27(47):6131-6140.
23. Zhu G, Wu CJ, Zhao Y, Ashwell JD. Optineurin negatively regulates TNFalpha- induced NF-kappaB activation by competing with NEMO for ubiquitinated RIP. Curr Biol. 2007;17(16):1438-1443. (Pubitemid 47259388)
24. Furnari FB, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2007;21(21):2683-2710. (Pubitemid 350070717)
25. 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(2):211-223. (Pubitemid 38496241)
26. Bruna 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(2):147-160. (Pubitemid 46209848)
27. Ikushima H, et al. Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell Stem Cell. 2009;5(5):504-514.
28. Penuelas S, et al. TGF-beta increases gliomainitiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell. 2009; 15(4):315-327.
29. Park JI, et al. Transforming growth factor-beta1 activates interleukin-6 expression in prostate cancer cells through the synergistic collaboration of the Smad2, p38-NF-kappaB, JNK, and Ras signaling pathways. Oncogene. 2003;22(28):4314-4332.
30. Neil JR, Schiemann WP. Altered TAB1:I kappaB kinase interaction promotes transforming growth factor beta-mediated nuclear factor-kappaB activation during breast cancer progression. Cancer Res. 2008;68(5):1462-1470. (Pubitemid 351346854)
31. Valastyan S, et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell. 2009; 137(6):1032-1046.
32. Subramanyam D, et al. Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat Biotechnol. 2011;29(5):443-448.
33. Jiang L, et al. miR-182 as a prognostic marker for glioma progression and patient survival. Am J Pathol. 2010;177(1):29-38.
34. Lee J, et al. 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. 2006;9(5):391-403. (Pubitemid 43668737)
35. Schrock E, et al. Comparative genomic hybridization of human malignant gliomas reveals multiple amplification sites and nonrandom chromosomal gains and losses. Am J Pathol. 1994; 144(6):1203-1218. (Pubitemid 24172083)
36. Stittrich AB, et al. The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes. Nat Immunol. 2010; 11(11):1057-1062.
37. Massoumi R, et al. Down-regulation of CYLD expression by Snail promotes tumor progression in malignant melanoma. J Exp Med. 2009;206(1):221-232.
38. Espinosa L, et al. The Notch/Hes1 pathway sustains NF-kappaB activation through CYLD repression in T cell leukemia. Cancer Cell. 2010;18(3):268-281.
39. Hellerbrand C, et al. Reduced expression of CYLD in human colon and hepatocellular carcinomas. Carcinogenesis. 2007;28(1):21-27. (Pubitemid 44942623)
40. Bignell GR, et al. Identification of the familial cylindromatosis tumour-suppressor gene. Nat Genet. 2000;25(2):160-165. (Pubitemid 30394985)
41. Jono H, et al. NF-kappaB is essential for induction of CYLD, the negative regulator of NF-kappaB: evidence for a novel inducible autoregulatory feedback pathway. J Biol Chem. 2004;279(35):36171-36174. (Pubitemid 39128950)
42. Jiang L, et al. MicroRNA-30e*promotes human glioma cell invasiveness in an orthotopic xenotransplantation model by disrupting the NF-kappaB/ IkappaBalpha negative feedback loop. J Clin Invest. 2012;122(1):33-47.
43. Hjelmeland AB, et al. Targeting A20 decreases glioma stem cell survival and tumor growth. PLoS Biol. 2010;8(2):e1000319.
44. Bellail AC, Olson JJ, Yang X, Chen ZJ, Hao C. A20 ubiquitin ligase-mediated polyubiquitination of RIP1 inhibits caspase-8 cleavage and TRAIL-induced apoptosis in glioblastoma. Cancer Discov. 2012;2(2):140-155.
45. Komander D, Barford D. Structure of the A20 OTU domain and mechanistic insights into deubiquitination. Biochem J. 2008;409(1):77-85.
46. Lin SC, et al. Molecular basis for the unique deubiquitinating activity of the NF-kappaB inhibitor A20. J Mol Biol. 2008;376(2):526-540.
47. Mauro C, et al. ABIN-1 binds to NEMO/IKK-γ and co-operates with A20 in inhibiting NF-κB. J Biol Chem. 2006;281(27):18482-18488. (Pubitemid 44035507)
48. Heyninck K, Kreike MM, Beyaert R. Structure-function analysis of the A20-binding inhibitor of NF-kappa B activation, ABIN-1. FEBS Lett. 2003; 536(1-3):135-140. (Pubitemid 36206420)
49. Ghafoori P, Yoshimura T, Turpie B, Masli S. Increased IkappaB alpha expression is essential for the tolerogenic property of TGF-beta-exposed APCs. FASEB J. 2009;23(7):2226-2234.
50. Arsura M, Wu M, Sonenshein GE. TGF beta 1 inhibits NF-kappa B/Rel activity inducing apoptosis of B cells: transcriptional activation of I kappa B alpha. Immunity. 1996;5(1):31-40. (Pubitemid 26259622)
51. Hong S, 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(5):504-513. (Pubitemid 46605919)
52. Lee YS, 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(4):836-843.
53. Sorrentino A, et al. The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat Cell Biol. 2008; 10(10):1199-1207.
54. Schweitzer K, Bozko PM, Dubiel W, Naumann M. CSN controls NF-kappaB by deubiquitinylation of IkappaBalpha. EMBO J. 2007;26(6):1532-1541. (Pubitemid 46480929)
55. Eichhorn PJ, et al. USP15 stabilizes TGF-β receptor I and promotes oncogenesis through the activation of TGF-β signaling in glioblastoma. Nat Med. 2012;18(3):429-435.
56. Zhang L, et al. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc Natl Acad Sci U S A. 2008; 105(19):7004-7009. (Pubitemid 351754520)
57. Segura MF, et al. Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc Natl Acad Sci U S A. 2009;106(6):1814-1819.
58. Moskwa P, et al. miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell. 2011;41(2):210-220.
59. Holland EC. Gliomagenesis: genetic alterations and mouse models. Nat Rev Genet. 2001;2(2):120-129. (Pubitemid 33674003)
60. Zhu Y, Parada LF. The molecular and genetic basis of neurological tumours. Nat Rev Cancer. 2002; 2(8):616-626. (Pubitemid 37328928)
61. Seoane J. The TGFBeta pathway as a therapeutic target in cancer. Clin Transl Oncol. 2008;10(1):14-19.
62. Yingling JM, Blanchard KL, Sawyer JS. Development of TGF-beta signalling inhibitors for cancer therapy. Nat Rev Drug Discov. 2004;3(12):1011-1022. (Pubitemid 39642364)
63. Li J, et al. Astrocyte elevated gene-1 is a novel prognostic marker for breast cancer progression and overall patient survival. Clin Cancer Res. 2008; 14(11):3319-3326.