STAT3 upregulates miR-92a to inhibit RECK expression and to promote invasiveness of lung cancer cells

British Journal of Cancer

Volumn 109, Issue 3, 2013, Pages 731-738

  Lin, H Y ^a   Chiang, C H ^a   Hung, W C ^b  

^a NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

4 [[(4 METHYLPHENYL)SULFONYLOXY]ACETAMIDO]SALICYLIC ACID; GELATIN; MATRIX METALLOPROTEINASE; MICRORNA; MICRORNA 92A; RECK PROTEIN; S 3I 201; STAT3 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LUNG CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR INVASION; UPREGULATION; WESTERN BLOTTING; ZYMOGRAPHY;

CELL LINE, TUMOR; CELL MOVEMENT; GPI-LINKED PROTEINS; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICRORNAS; NEOPLASM INVASIVENESS; RNA, MESSENGER; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION;

EID: 84883191844     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.349     Document Type: Article

References (62)

1. Bourguignon LY, Earle C, Wong G, Spevak CC, Krueger K (2012) Stem cell marker (Nanog) and Stat-3 signaling promote MicroRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells. Oncogene 31(2): 149-160.
2. Bowman T, Garcia R, Turkson J, Jove R (2000) STATs in oncogenesis. Oncogene 19(21): 2474-2488.
3. Brock M, Trenkmann M, Gay RE, Michel BA, Gay S, Fischler M, Ulrich S, Speich R, Huber LC (2009) Interleukin-6 modulates the expression of the bone morphogenic protein receptor type II through a novel STAT3-microRNA cluster 17/92 pathway. Circ Res 104(10): 1184-1191.
4. Buettner R, Mora LB, Jove R (2002) Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin Cancer Res 8(4): 945-954.
5. Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65(14): 6029-6033.
6. Chang HC, Cho CY, Hung WC (2006) Silencing of the metastasis suppressor RECK by RAS oncogene is mediated by DNA methyltransferase 3b-induced promoter methylation. Cancer Res 66(17): 8413-8420.
7. Chang HC, Liu LT, Hung WC (2004) Involvement of histone deacetylation in ras-induced down-regulation of the metastasis suppressor RECK. Cell Signal 16(6): 675-679.
8. Cho CY, Wang JH, Chang HC, Chang CK, Hung WC (2007) Epigenetic inactivation of the metastasis suppressor RECK enhances invasion of human colon cancer cells. J Cell Physiol 213(1): 65-69.
9. Cloonan N, Brown MK, Steptoe AL, Wani S, Chan WL, Forrest AR, Kolle G, Gabrielli B, Grimmond SM (2008) The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol 9(8): R127.
10. Connolly E, Melegari M, Landgraf P, Tchaikovskaya T, Tennant BC, Slagle BL, Rogler LE, Zavolan M, Tuschl T, Rogler CE (2008) Elevated expression of the miR-17-92 polycistron and miR-21 in hepadnavirus-associated hepatocellular carcinoma contributes to the malignant phenotype. Am J Pathol 173(3): 856-864.
11. Cortas T, Eisenberg R, Fu P, Kern J, Patrick L, Dowlati A (2007) Activation state EGFR and STAT-3 as prognostic markers in resected non-small cell lung cancer. Lung Cancer 55(3): 349-355.
12. Davidson BL, McCray Jr PB (2011) Current prospects for RNA interferencebased therapies. Nat Rev Genet 12(5): 329-340.
13. Debnath B, Xu S, Neamati N (2012) Small molecule inhibitors of signal transducer and activator of transcription 3 (Stat3) protein. J Med Chem 55(15): 6645-6668.
14. Dechow TN, Pedranzini L, Leitch A, Leslie K, Gerald WL, Linkov I, Bromberg JF (2004) Requirement of matrix metalloproteinase-9 for the transformation of human mammary epithelial cells by Stat3-C. Proc Natl Acad Sci USA 101(29): 10602-10607.
15. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A (2006) Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38(9): 1060-1065.
16. Esquela-Kerscher A, Slack FJ (2006) Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6(4): 259-269.
17. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, Krichevsky AM (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28(17): 5369-5380.
18. Haug BH, Henriksen JR, Buechner J, Geerts D, Tomte E, Kogner P, Martinsson T, Flaegstad T, Sveinbjornsson B, Einvik C (2011) MYCN-regulated miRNA-92 inhibits secretion of the tumor suppressor DICKKOPF-3 (DKK3) in neuroblastoma. Carcinogenesis 32(7): 1005-1012.
19. Haura EB, Zheng Z, Song L, Cantor A, Bepler G (2005) Activated epidermal growth factor receptor-Stat-3 signaling promotes tumor survival in vivo in non-small cell lung cancer. Clin Cancer Res 11(23): 8288-8294.
20. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, Yatabe Y, Kawahara K, Sekido Y, Takahashi T (2005) A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 65(21): 9628-9632.
21. He H, Jazdzewski K, Li W, Liyanarachchi S, Nagy R, Volinia S, Calin GA, Liu CG, Franssila K, Suster S, Kloos RT, Croce CM, de la Chapelle A (2005a) The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci USA 102(52): 19075-19080.
22. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM (2005b) A microRNA polycistron as a potential human oncogene. Nature 435(7043): 828-833.
23. Hirata H, Ueno K, Shahryari V, Tanaka Y, Tabatabai ZL, Hinoda Y, Dahiya R (2012) Oncogenic miRNA-182-5p targets Smad4 and RECK in human bladder cancer. PLoS One 7(11): e51056.
24. Hoang BH, Kubo T, Healey JH, Yang R, Nathan SS, Kolb EA, Mazza B, Meyers PA, Gorlick R (2004) Dickkopf 3 inhibits invasion and motility of Saos-2 osteosarcoma cells by modulating the Wnt-beta-catenin pathway. Cancer Res 64(8): 2734-2739.
25. Hsu MC, Chang HC, Hung WC (2006) HER-2/neu represses the metastasis suppressor RECK via ERK and Sp transcription factors to promote cell invasion. J Biol Chem 281(8): 4718-4725.
26. Hsu MC, Huang CC, Chang HC, Hu TH, Hung WC (2008) Overexpression of Jab1 in hepatocellular carcinoma and its inhibition by peroxisome proliferator-activated receptor{gamma} ligands in vitro and in vivo. Clin Cancer Res 14(13): 4045-4052.
27. Hu SJ, Ren G, Liu JL, Zhao ZA, Yu YS, Su RW, Ma XH, Ni H, Lei W, Yang ZM (2008) MicroRNA expression and regulation in mouse uterus during embryo implantation. J Biol Chem 283(34): 23473-23484.
28. Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl K (2010) STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 39(4): 493-506.
29. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Menard S, Palazzo JP, Rosenberg A, Musiani P, Volinia S, Nenci I, Calin GA, Querzoli P, Negrini M, Croce CM (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65(16): 7065-7070.
30. Itoh M, Murata T, Suzuki T, Shindoh M, Nakajima K, Imai K, Yoshida K (2006) Requirement of STAT3 activation for maximal collagenase-1 (MMP-1) induction by epidermal growth factor and malignant characteristics in T24 bladder cancer cells. Oncogene 25(8): 1195-1204.
31. Jung HM, Phillips BL, Patel RS, Cohen DM, Jakymiw A, Kong WW, Cheng JQ, Chan EK (2012) Keratinization-associated miR-7 and miR-21 regulate tumor suppressor reversion-inducing cysteine-rich protein with kazal motifs (RECK) in oral cancer. J Biol Chem 287(35): 29261-29272.
32. Lee W, Swarup S, Chen J, Ishitani T, Verheyen EM (2009) Homeodomaininteracting protein kinases (Hipks) promote Wnt/Wg signaling through stabilization of beta-catenin/Arm and stimulation of target gene expression. Development 136(2): 241-251.
33. Leslie K, Lang C, Devgan G, Azare J, Berishaj M, Gerald W, Kim YB, Paz K, Darnell JE, Albanese C, Sakamaki T, Pestell R, Bromberg J (2006) Cyclin D1 is transcriptionally regulated by and required for transformation by activated signal transducer and activator of transcription 3. Cancer Res 66(5): 2544-2552.
34. Li N, Tang B, Zhu ED, Li BS, Zhuang Y, Yu S, Lu DS, Zou QM, Xiao B, Mao XH (2012) Increased miR-222 in H. pylori-associated gastric cancer correlated with tumor progression by promoting cancer cell proliferation and targeting RECK. FEBS Lett 586(6): 722-728.
35. Liu LT, Peng JP, Chang HC, Hung WC (2003) RECK is a target of Epstein-Barr virus latent membrane protein 1. Oncogene 22(51): 8263-8270.
36. Loayza-Puch F, Yoshida Y, Matsuzaki T, Takahashi C, Kitayama H, Noda M (2010) Hypoxia and RAS-signaling pathways converge on, and cooperatively downregulate, the RECK tumor-suppressor protein through microRNAs. Oncogene 29(18): 2638-2648.
37. Loffler D, Brocke-Heidrich K, Pfeifer G, Stocsits C, Hackermuller J, Kretzschmar AK, Burger R, Gramatzki M, Blumert C, Bauer K, Cvijic H, Ullmann AK, Stadler PF, Horn F (2007) Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 110(4): 1330-1333.
38. Lu Y, Thomson JM, Wong HY, Hammond SM, Hogan BL (2007) Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol 310(2): 442-453.
39. Ma L, Teruya-Feldstein J, Weinberg RA (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449(7163): 682-688.
40. Masui T, Doi R, Koshiba T, Fujimoto K, Tsuji S, Nakajima S, Koizumi M, Toyoda E, Tulachan S, Ito D, Kami K, Mori T, Wada M, Noda M, Imamura M (2003) RECK expression in pancreatic cancer: its correlation with lower invasiveness and better prognosis. Clin Cancer Res 9(5): 1779-1784.
41. Matsubara H, Takeuchi T, Nishikawa E, Yanagisawa K, Hayashita Y, Ebi H, Yamada H, Suzuki M, Nagino M, Nimura Y, Osada H, Takahashi T (2007) Apoptosis induction by antisense oligonucleotides against miR-17-5p and miR-20a in lung cancers overexpressing miR-17-92. Oncogene 26(41): 6099-6105.
42. Meng N, Li Y, Zhang H, Sun XF (2008) RECK, a novel matrix metalloproteinase regulator. Histol Histopathol 23(8): 1003-1010.
43. Mi S, Li Z, Chen P, He C, Cao D, Elkahloun A, Lu J, Pelloso LA, Wunderlich M, Huang H, Luo RT, Sun M, He M, Neilly MB, Zeleznik-Le NJ, Thirman MJ, Mulloy JC, Liu PP, Rowley JD, Chen J (2010) Aberrant overexpression and function of the miR-17-92 cluster in MLL-rearranged acute leukemia. Proc Natl Acad Sci USA 107(8): 3710-3715.
44. Nishida N, Nagahara M, Sato T, Mimori K, Sudo T, Tanaka F, Shibata K, Ishii H, Sugihara K, Doki Y, Mori M (2012) Microarray analysis of colorectal cancer stromal tissue reveals upregulation of two oncogenic miRNA clusters. Clin Cancer Res 18(11): 3054-3070.
45. Noda M, Oh J, Takahashi R, Kondo S, Kitayama H, Takahashi C (2003) RECK: a novel suppressor of malignancy linking oncogenic signaling to extracellular matrix remodeling. Cancer Metastasis Rev 22(2-3): 167-175.
46. Noda M, Takahashi C, Matsuzaki T, Kitayama H (2010) What we learn from transformation suppressor genes: lessons from RECK. Future Oncol 6(7): 1105-1116.
47. Oh J, Takahashi R, Kondo S, Mizoguchi A, Adachi E, Sasahara RM, Nishimura S, Imamura Y, Kitayama H, Alexander DB, Ide C, Horan TP, Arakawa T, Yoshida H, Nishikawa S, Itoh Y, Seiki M, Itohara S, Takahashi C, Noda M (2001) The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107(6): 789-800.
48. Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, Yoshida Y, Seto M (2004) Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res 64(9): 3087-3095.
49. Shigoka M, Tsuchida A, Matsudo T, Nagakawa Y, Saito H, Suzuki Y, Aoki T, Murakami Y, Toyoda H, Kumada T, Bartenschlager R, Kato N, Ikeda M, Takashina T, Tanaka M, Suzuki R, Oikawa K, Takanashi M, Kuroda M (2010) Deregulation of miR-92a expression is implicated in hepatocellular carcinoma development. Pathol Int 60(5): 351-357.
50. Song L, Turkson J, Karras JG, Jove R, Haura EB (2003) Activation of Stat3 by receptor tyrosine kinases and cytokines regulates survival in human non-small cell carcinoma cells. Oncogene 22(27): 4150-4165.
51. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, Ferbeyre G, Chartrand P (2007) An E2F/miR-20a autoregulatory feedback loop. J Biol Chem 282(4): 2135-2143.
52. Takahashi C, Sheng Z, Horan TP, Kitayama H, Maki M, Hitomi K, Kitaura Y, Takai S, Sasahara RM, Horimoto A, Ikawa Y, Ratzkin BJ, Arakawa T, Noda M (1998) Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc Natl Acad Sci USA 95(22): 13221-13226.
53. Takakura S, Mitsutake N, Nakashima M, Namba H, Saenko VA, Rogounovitch TI, Nakazawa Y, Hayashi T, Ohtsuru A, Yamashita S (2008) Oncogenic role of miR-17-92 cluster in anaplastic thyroid cancer cells. Cancer Sci 99(6): 1147-1154.
54. Takeuchi T, Hisanaga M, Nagao M, Ikeda N, Fujii H, Koyama F, Mukogawa T, Matsumoto H, Kondo S, Takahashi C, Noda M, Nakajima Y (2004) The membrane-anchored matrix metalloproteinase (MMP) regulator RECK in combination with MMP-9 serves as an informative prognostic indicator for colorectal cancer. Clin Cancer Res 10(16): 5572-5579.
55. Tsuchida A, Ohno S, Wu W, Borjigin N, Fujita K, Aoki T, Ueda S, Takanashi M, Kuroda M (2011) miR-92 is a key oncogenic component of the miR-17-92 cluster in colon cancer. Cancer Sci 102(12): 2264-2271.
56. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T (2008) Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132(5): 875-886.
57. Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, MuckenthalerMU, Ganser A, Eder M, Scherr M (2007) Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34\+ cells. Blood 109(10): 4399-4405.
58. Woods K, Thomson JM, Hammond SM (2007) Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 282(4): 2130-2134.
59. Wu W, Fan YH, Kemp BL, Walsh G, Mao L (1998) Overexpression of cdc25A and cdc25B is frequent in primary non-small cell lung cancer but is not associated with overexpression of c-myc. Cancer Res 58(18): 4082-4085.
60. Xie TX, Wei D, Liu M, Gao AC, Ali-Osman F, Sawaya R, Huang S (2004) Stat3 activation regulates the expression of matrix metalloproteinase-2 and tumor invasion and metastasis. Oncogene 23(20): 3550-3560.
61. Yeh HH, Lai WW, Chen HH, Liu HS, Su WC (2006) Autocrine IL-6-induced Stat3 activation contributes to the pathogenesis of lung adenocarcinoma and malignant pleural effusion. Oncogene 25(31): 4300-4309.
62. Zhang X, Chen J, Radcliffe T, Lebrun DP, Tron VA, Feilotter H (2008) An array-based analysis of microRNA expression comparing matched frozen and formalin-fixed paraffin-embedded human tissue samples. J Mol Diagn 10(6): 513-519.