The miR-200 family and the miR-183∼96∼182 cluster target Foxf2 to inhibit invasion and metastasis in lung cancers

Oncogene

Volumn 35, Issue 2, 2016, Pages 173-186

  Kundu, S T ^a   Byers, L A ^a   Peng, D H ^a   Roybal, J D ^a   Diao, L ^a   Wang, J ^a   Tong, P ^a   Creighton, C J ^a,b   Gibbons, D L ^a  

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

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 183 96 182; MICRORNA 200; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXF2; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; FORKHEAD TRANSCRIPTION FACTOR; FOXF2 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MIRN182 MICRORNA, HUMAN; MIRN183 MICRORNA, HUMAN; MIRN200 MICRORNA, HUMAN; MIRN96 MICRORNA, HUMAN; ZEB1 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CANCER INHIBITION; CELL MIGRATION; ECTOPIC EXPRESSION; GENE CLUSTER; NEGATIVE FEEDBACK; NON SMALL CELL LUNG CANCER; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TUMOR INVASION; ANIMAL; CELL MOTION; DRUG SCREENING; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INBRED MOUSE STRAIN; LUNG TUMOR; METABOLISM; MULTIGENE FAMILY; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CADHERINS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; LUNG NEOPLASMS; MICE, INBRED STRAINS; MICRORNAS; MULTIGENE FAMILY; TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS; ZINC FINGER E-BOX-BINDING HOMEOBOX 1;

EID: 84954381902     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.71     Document Type: Article

References (76)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014; 64: 9-29.
2. Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005; 17: 548-558.
3. Zheng H, Kang Y. Multilayer control of the EMT master regulators. Oncogene 2014; 33: 1755-1763.
4. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009; 11: 1487-1495.
5. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004; 117: 927-939.
6. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 2008; 14: 818-829.
7. Zheng S, El-Naggar AK, Kim ES, Kurie JM, Lozano G. A genetic mouse model for metastatic lung cancer with gender differences in survival. Oncogene 2007; 26: 6896-6904.
8. Ahn YH, Gibbons DL, Chakravarti D, Creighton CJ, Rizvi ZH, Adams HP et al. ZEB1 drives prometastatic actin cytoskeletal remodeling by downregulating miR-34a expression. J Clin Inves 2012; 122: 3170-3183.
9. Gibbons DL, Lin W, Creighton CJ, Rizvi ZH, Gregory PA, Goodall GJ et al. Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev 2009; 23: 2140-2151.
10. Yang Y, Ahn YH, Gibbons DL, Zang Y, Lin W, Thilaganathan N et al. The Notch ligand Jagged2 promotes lung adenocarcinoma metastasis through a miR-200-dependent pathway in mice. J Clin Invest 2011; 121: 1373-1385.
11. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455: 64-71.
12. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-233.
13. Djuranovic S, Nahvi A, Green R. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 2012; 336: 237-240.
14. Fabian MR, Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 2012; 19: 586-593.
15. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008; 455: 58-63.
16. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 2008; 68: 7846-7854.
17. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008; 9: 582-589.
18. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593-601.
19. Li XL, Hara T, Choi Y, Subramanian M, Francis P, Bilke S et al. A p21-ZEB1 complex inhibits epithelial-mesenchymal transition through the microRNA 183-96-182 cluster. Mol Cell Biol 2014; 34: 533-550.
20. Lowery AJ, Miller N, Dwyer RM, Kerin MJ. Dysregulated miR-183 inhibits migration in breast cancer cells. BMC Cancer 2010; 10: 502.
21. Zhao H, Guo M, Zhao G, Ma Q, Ma B, Qiu X et al. miR-183 inhibits the metastasis of osteosarcoma via downregulation of the expression of Ezrin in F5M2 cells. Int J Mol Med 2012; 30: 1013-1020.
22. Sarver AL, Li L, Subramanian S. MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res 2010; 70: 9570-9580.
23. Weeraratne SD, Amani V, Teider N, Pierre-Francois J, Winter D, Kye MJ et al. Pleiotropic effects of miR-183 ∼ 96 ∼ 182 converge to regulate cell survival, proliferation and migration in medulloblastoma. Acta Neuropathol 2012; 123: 539-552.
24. Katoh M, Igarashi M, Fukuda H, Nakagama H, Katoh M. Cancer genetics and genomics of human FOX family genes. Cancer Lett 2013; 328: 198-206.
25. Lam EW, Brosens JJ, Gomes AR, Koo CY. Forkhead box proteins: tuning forks for transcriptional harmony. Nat Rev Cancer 2013; 13: 482-495.
26. Nilsson J, Helou K, Kovacs A, Bendahl PO, Bjursell G, Ferno M et al. Nuclear Janus-activated kinase 2/nuclear factor 1-C2 suppresses tumorigenesis and epithelial-to-mesenchymal transition by repressing Forkhead box F1. Cancer Res 2010; 70: 2020-2029.
27. Ormestad M, Astorga J, Landgren H, Wang T, Johansson BR, Miura N et al. Foxf1 and Foxf2 control murine gut development by limiting mesenchymal Wnt signaling and promoting extracellular matrix production. Development 2006; 133: 833-843.
28. Byers LA, Diao L, Wang J, Saintigny P, Girard L, Peyton M et al. An epithelial-mesenchymal transition gene signature predicts resistance to EGFR and PI3K inhibitors and identifies Axl as a therapeutic target for overcoming EGFR inhibitor resistance. Clin Cancer Res 2013; 19: 279-290.
29. Chen L, Gibbons DL, Goswami S, Cortez MA, Ahn YH, Byers LA et al. Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression. Nat Commun 2014; 5: 5241.
30. Betel D, Koppal A, Agius P, Sander C, Leslie C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol 2010; 11: R90.
31. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res 2008; 36: D149-D153.
32. Brabletz S, Brabletz T. The ZEB/miR-200 feedback loop - a motor of cellular plasticity in development and cancer? EMBO Rep 2010; 11: 670-677.
33. Browne G, Sayan AE, Tulchinsky E. ZEB proteins link cell motility with cell cycle control and cell survival in cancer. Cell Cycle 2010; 9: 886-891.
34. Spaderna S, Schmalhofer O, Wahlbuhl M, Dimmler A, Bauer K, Sultan A et al. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res 2008; 68: 537-544.
35. Eger A, Aigner K, Sonderegger S, Dampier B, Oehler S, Schreiber M et al. DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 2005; 24: 2375-2385.
36. Gemmill RM, Roche J, Potiron VA, Nasarre P, Mitas M, Coldren CD et al. ZEB1-responsive genes in non-small cell lung cancer. Cancer Lett 2011; 300: 66-78.
37. Hirohashi S. Inactivation of the E-cadherin-mediated cell adhesion system in human cancers. Am J Pathol 1998; 153: 333-339.
38. Tsai JH, Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev 2013; 27: 2192-2206.
39. Vincent-Salomon A, Thiery JP. Host microenvironment in breast cancer development: epithelial-mesenchymal transition in breast cancer development. Breast Cancer Res 2003; 5: 101-106.
40. Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006; 10: 437-449.
41. Husemann Y, Geigl JB, Schubert F, Musiani P, Meyer M, Burghart E et al. Systemic spread is an early step in breast cancer. Cancer Cell 2008; 13: 58-68.
42. Oft M, Peli J, Rudaz C, Schwarz H, Beug H, Reichmann E. TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev 1996; 10: 2462-2477.
43. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 1998; 392: 190-193.
44. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006; 6: 857-866.
45. Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med 2009; 60: 167-179.
46. Kasinski AL, Slack FJ. Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat Rev Cancer 2011; 11: 849-864.
47. Pencheva N, Tavazoie SF. Control of metastatic progression by microRNA regulatory networks. Nat Cell Biol 2013; 15: 546-554.
48. Korpal M, Kang Y. The emerging role of miR-200 family of microRNAs in epithelial-mesenchymal transition and cancer metastasis. RNA Biol 2008; 5: 115-119.
49. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008; 22: 894-907.
50. Adams BD, Kasinski AL, Slack FJ. Aberrant regulation and function of microRNAs in cancer. Curr Biol 2014; 24: R762-R776.
51. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006; 6: 259-269.
52. Li G, Luna C, Qiu J, Epstein DL, Gonzalez P. Targeting of integrin beta1 and kinesin 2alpha by microRNA 183. J Biol Chem 2010; 285: 5461-5471.
53. Zhu J, Feng Y, Ke Z, Yang Z, Zhou J, Huang X et al. Down-regulation of miR-183 promotes migration and invasion of osteosarcoma by targeting Ezrin. Am J Pathol 2012; 180: 2440-2451.
54. Guttilla IK, White BA. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J Biol Chem 2009; 284: 23204-23216.
55. Hirata H, Ueno K, Shahryari V, Deng G, Tanaka Y, Tabatabai ZL et al. MicroRNA-182-5p promotes cell invasion and proliferation by down regulating FOXF2, RECK and MTSS1 genes in human prostate cancer. PloS One 2013; 8: e55502.
56. Huynh C, Segura MF, Gaziel-Sovran A, Menendez S, Darvishian F, Chiriboga L et al. Efficient in vivo microRNA targeting of liver metastasis. Oncogene 2011; 30: 1481-1488.
57. Lei R, Tang J, Zhuang X, Deng R, Li G, Yu J et al. Suppression of MIM by microRNA-182 activates RhoA and promotes breast cancer metastasis. Oncogene 2014; 33: 1287-1296.
58. Segura MF, Hanniford D, Menendez S, Reavie L, Zou X, Alvarez-Diaz S et al. Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc Natl Acad Sci USA 2009; 106: 1814-1819.
59. Sun Y, Fang R, Li C, Li L, Li F, Ye X et al. Hsa-mir-182 suppresses lung tumorigenesis through down regulation of RGS17 expression in vitro. Biochem Biophys Res Commun 2010; 396: 501-507.
60. Kong PZ, Yang F, Li L, Li XQ, Feng YM. Decreased FOXF2 mRNA expression indicates early-onset metastasis and poor prognosis for breast cancer patients with histological grade II tumor. PloS One 2013; 8: e61591.
61. Wang Z, Liu P, Inuzuka H, Wei W. Roles of F-box proteins in cancer. Nat Rev Cancer 2014; 14: 233-247.
62. Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008; 68: 989-997.
63. Xia L, Huang W, Tian D, Zhu H, Qi X, Chen Z et al. Overexpression of forkhead box C1 promotes tumor metastasis and indicates poor prognosis in hepatocellular carcinoma. Hepatology 2013; 57: 610-624.
64. Lo PK, Lee JS, Chen H, Reisman D, Berger FG, Sukumar S. Cytoplasmic mislocalization of overexpressed FOXF1 is associated with the malignancy and metastasis of colorectal adenocarcinomas. Exp Mol Pathol 2013; 94: 262-269.
65. Nik AM, Reyahi A, Ponten F, Carlsson P. Foxf2 in intestinal fibroblasts reduces numbers of Lgr5(+) stem cells and adenoma formation by inhibiting Wnt signaling. Gastroenterology 2013; 144: 1001-1011.
66. Wang T, Tamakoshi T, Uezato T, Shu F, Kanzaki-Kato N, Fu Y et al. Forkhead transcription factor Foxf2 (LUN)-deficient mice exhibit abnormal development of secondary palate. Dev Biol 2003; 259: 83-94.
67. Feng X, Wang Z, Fillmore R, Xi Y. MiR-200, a new star miRNA in human cancer. Cancer Lett 2014; 344: 166-173.
68. Liu XG, Zhu WY, Huang YY, Ma LN, Zhou SQ, Wang YK et al. High expression of serum miR-21 and tumor miR-200c associated with poor prognosis in patients with lung cancer. Med Oncol 2012; 29: 618-626.
69. Pacurari M, Addison JB, Bondalapati N, Wan YW, Luo D, Qian Y et al. The microRNA-200 family targets multiple non-small cell lung cancer prognostic markers in H1299 cells and BEAS-2B cells. Int J Oncol 2013; 43: 548-560.
70. Kim T, Veronese A, Pichiorri F, Lee TJ, Jeon YJ, Volinia S et al. p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J Exp Med 2011; 208: 875-883.
71. Knouf EC, Garg K, Arroyo JD, Correa Y, Sarkar D, Parkin RK et al. An integrative genomic approach identifies p73 and p63 as activators of miR-200 microRNA family transcription. Nucleic Acids Res 2012; 40: 499-510.
72. Mizuguchi Y, Specht S, Lunz JG 3rd, Isse K, Corbitt N, Takizawa T et al. Cooperation of p300 and PCAF in the control of microRNA 200c/141 transcription and epithelial characteristics. PloS One 2012; 7: e32449.
73. Pieraccioli M, Imbastari F, Antonov A, Melino G, Raschella G. Activation of miR200 by c-Myb depends on ZEB1 expression and miR200 promoter methylation. Cell Cycle 2013; 12: 2309-2320.
74. Roy SS, Gonugunta VK, Bandyopadhyay A, Rao MK, Goodall GJ, Sun LZ et al. Significance of PELP1/HDAC2/miR-200 regulatory network in EMT and metastasis of breast cancer. Oncogene 2014; 33: 3707-3716.
75. Akbani R, Ng PK, Werner HM, Shahmoradgoli M, Zhang F, Ju Z et al. A pan-cancer proteomic perspective on The Cancer Genome Atlas. Nat Commun 2014; 5: 3887.
76. Hoadley KA, Yau C, Wolf DM, Cherniack AD, Tamborero D, Ng S et al. Multiplatform analysis of 12 cancer types reveals molecular classification within and across tissues of origin. Cell 2014; 158: 929-944.