MiR-93-directed downregulation of DAB2 defines a novel oncogenic pathway in lung cancer

Oncogene

Volumn 33, Issue 34, 2014, Pages 4307-4315

  Du, L ^a   Zhao, Z ^a   Ma, X ^a   Hsiao, T H ^a   Chen, Y ^a   Young, E ^a   Suraokar, M ^b   Wistuba, I ^b   Minna, J D ^c   Pertsemlidis, A ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

DAB2; lung cancer; miR 93; miRNA

Indexed keywords

DISABLED HOMOLOG 2 PROTEIN; MICRORNA; MICRORNA 93; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE;

3' UNTRANSLATED REGIONS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BASE SEQUENCE; BINDING SITES; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE-FREE SURVIVAL; FEMALE; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MICE; MICE, NUDE; MICRORNAS; NEOPLASM TRANSPLANTATION; ONCOGENES; PROMOTER REGIONS, GENETIC; PROPORTIONAL HAZARDS MODELS; RNA INTERFERENCE; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEINS;

EID: 84906937334     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.381     Document Type: Article

References (42)

1. Karam JA, Shariat SF, Huang HY, Pong RC, Ashfaq R, Shapiro E et al. Decreased DOC-2/DAB2 expression in urothelial carcinoma of the bladder. Clin Cancer Res 2007; 13(15 Pt 1): 4400-4406
2. Mok SC, Chan WY, Wong KK, Cheung KK, Lau CC, Ng SW et al. DOC-2, a candidate tumor suppressor gene in human epithelial ovarian cancer. Oncogene 1998; 16: 2381-2387
3. Fazili Z, Sun W, Mittelstaedt S, Cohen C, Xu XX. Disabled-2 inactivation is an early step in ovarian tumorigenicity. Oncogene 1999; 18: 3104-3113
4. Tseng CP, Ely BD, Li Y, Pong RC, Hsieh JT. Regulation of rat DOC-2 gene during castration-induced rat ventral prostate degeneration and its growth inhibitory function in human prostatic carcinoma cells. Endocrinology 1998; 139: 3542-3553
5. Bagadi SA, Prasad CP, Srivastava A, Prashad R, Gupta SD, Ralhan R. Frequent loss of Dab2 protein and infrequent promoter hypermethylation in breast cancer. Breast Cancer Res Treat 2007; 104: 277-286
6. Anupam K, Tusharkant C, Gupta SD, Ranju R. Loss of disabled-2 expression is an early event in esophageal squamous tumorigenesis. World J Gastroenterol 2006; 12: 6041-6045
7. Yang DH, Fazili Z, Smith ER, Cai KQ, Klein-Szanto A, Cohen C et al. Disabled-2 heterozygous mice are predisposed to endometrial and ovarian tumorigenesis and exhibit sex-biased embryonic lethality in a p53-null background. Am J Pathol 2006; 169: 258-267
8. Calvisi DF, Ladu S, Gorden A, Farina M, Lee JS, Conner EA et al. Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma. J Clin Invest 2007; 117: 2713-2722
9. Hannigan A, Smith P, Kalna G, Lo Nigro C, Orange C, O'Brien DI et al. Epigenetic downregulation of human disabled homolog 2 switches TGF-beta from a tumor suppressor to a tumor promoter. J Clin Invest 2010; 120: 2842-2857
10. Wikman H, Kettunen E, Seppanen JK, Karjalainen A, Hollmen J, Anttila S et al. Identification of differentially expressed genes in pulmonary adenocarcinoma by using cDNA array. Oncogene 2002; 21: 5804-5813
11. Xu HT, Yang LH, Li QC, Liu SL, Liu D, Xie XM et al. Disabled-2 and Axin are concurrently colocalized and underexpressed in lung cancers. Hum Pathol 2011; 42: 1491-1498
12. Xu HT, Xie XM, Li QC, Liu SL, Dai SD, Liu Y et al. Atonal homolog 1 expression in lung cancer correlates with inhibitors of the Wnt pathway as well as the differentiation and primary tumor stage. APMIS 2013; 121: 111-119
13. Chao A, Lin CY, Lee YS, Tsai CL, Wei PC, Hsueh S et al. Regulation of ovarian cancer progression by microRNA-187 through targeting Disabled homolog-2. Oncogene 2012; 31: 764-775
14. Mayorga ME, Penn MS. miR-145 is differentially regulated by TGF-beta1 and ischaemia and targets Disabled-2 expression and wnt/beta-catenin activity. J Cell Mol Med 2012; 16: 1106-1113
15. Fang L, Du WW, Yang W, Rutnam ZJ, Peng C, Li H et al. MiR-93 enhances angiogenesis and metastasis by targeting LATS2. Cell Cycle 2012; 11: 4352-4365
16. Borchert GM, Holton NW, Larson ED. Repression of human activation induced cytidine deaminase by miR-93 and miR-155. BMC Cancer 2011; 11: 347
17. Fang L, Deng Z, Shatseva T, Yang J, Peng C, Du WW et al. MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-beta8. Oncogene 2011; 30: 806-821
18. Kim K, Chadalapaka G, Lee SO, Yamada D, Sastre-Garau X, Defossez PA et al. Identification of oncogenic microRNA-17-92/ZBTB4/specificity protein axis in breast cancer. Oncogene 2012; 31: 1034-1044
19. Du L, Schageman JJ, Subauste MC, Saber B, Hammond SM, Prudkin L et al. miR-93, miR-98, and miR-197 regulate expression of tumor suppressor gene FUS1. Mol Cancer Res 2009; 7: 1234-1243
20. Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B et al. miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci USA 2010; 107: 264-269
21. Kim YK, Yu J, Han TS, Park SY, Namkoong B, Kim DH et al. Functional links between clustered microRNAs: Suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res 2009; 37: 1672-1681
22. He J, Smith ER, Xu XX. Disabled-2 exerts its tumor suppressor activity by uncoupling c-Fos expression and MAP kinase activation. J Biol Chem 2001; 276: 26814-26818
23. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19: 92-105
24. Garcia DM, Baek D, Shin C, Bell GW, Grimson A, Bartel DP. Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat Struct Mol Biol 2011; 18: 1139-1146
25. Du L, Subauste MC, DeSevo C, Zhao Z, Baker M, Borkowski R et al. miR-337-3p and its targets STAT3 and RAP1A modulate taxane sensitivity in non-small cell lung cancers. PLoS One 2012; 7: E39167
26. Wang T, Lv M, Shen S, Zhou S, Wang P, Chen Y et al. Cell-free microRNA expression profiles in malignant effusion associated with patient survival in nonsmall cell lung cancer. PLoS One 2012; 7: E43268
27. Zhoul J, Hernandez G, Tu SW, Huang CL, Tseng CP, Hsieh JT. The role of DOC-2/ DAB2 in modulating androgen receptor-mediated cell growth via the nongenomic c-Src-mediated pathway in normal prostatic epithelium and cancer. Cancer Res 2005; 65: 9906-9913
28. Long J, Wang Y, Wang W, Chang BH, Danesh FR. Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem 2010; 285: 23457-23465
29. Yeung ML, Yasunaga J, Bennasser Y, Dusetti N, Harris D, Ahmad N et al. Roles for microRNAs, miR-93 and miR-130b, and tumor protein 53-induced nuclear protein 1 tumor suppressor in cell growth dysregulation by human T-cell lymphotrophic virus 1. Cancer Res 2008; 68: 8976-8985
30. Chuang TD, Luo X, Panda H, Chegini N. miR-93/106b and their host gene, MCM7, are differentially expressed in leiomyomas and functionally target F3 and IL-8. Mol Endocrinol 2012; 26: 1028-1042
31. Smith AL, Iwanaga R, Drasin DJ, Micalizzi DS, Vartuli RL, Tan AC et al. The miR-106b-25 cluster targets Smad7, activates TGF-beta signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene 2012; 31: 5162-5171
32. Yang L, Cheng P, Chen C, He HB, Xie GQ, Zhou HD et al. miR-93/Sp7 function loop mediates osteoblast mineralization. J Bone Miner Res 2012; 27: 1598-1606
33. Fu X, Tian J, Zhang L, Chen Y, Hao Q. Involvement of microRNA-93, a new regulator of PTEN/Akt signaling pathway, in regulation of chemotherapeutic drug cisplatin chemosensitivity in ovarian cancer cells. FEBS Lett 2012; 586: 1279-1286
34. Wang Z, Liu M, Zhu H, Zhang W, He S, Hu C et al. Suppression of p21 by c-Myc through members of miR-17 family at the post-Transcriptional level. Int J Oncol 2010; 37: 1315-1321
35. Li Y, Tan W, Neo TW, Aung MO, Wasser S, Lim SG et al. Role of the miR-106b-25 microRNA cluster in hepatocellular carcinoma. Cancer Sci 2009; 100: 1234-1242
36. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, De Martino I et al. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 2008; 13: 272-286
37. Carney DN, Minna JD. Small cell cancer of the lung. Clin Chest Med 1982; 3: 389-398
38. Carney DN, Gazdar AF, Nau M, Minna JD. Biological heterogeneity of small cell lung cancer. Semin Oncol 1985; 12: 289-303
39. Prudkin L, Behrens C, Liu DD, Zhou X, Ozburn NC, Bekele BN et al. Loss and reduction of FUS1 protein expression is a frequent phenomenon in the pathogenesis of lung cancer. Clin Cancer Res 2008; 14: 41-47
40. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996; 272: 263-267
41. Kluiver J, Gibcus JH, Hettinga C, Adema A, Richter MK, Halsema N et al. Rapid generation of microRNA sponges for microRNA inhibition. PLoS One 2012; 7: E29275
42. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: Determinants beyond seed pairing. Mol Cell 2007; 27: 91-105