MicroRNA-135b promotes lung cancer metastasis by regulating multiple targets in the Hippo pathway and LZTS1

Nature Communications

Volumn 4, Issue , 2013, Pages

  Lin, Ching Wen ^a   Chang, Yih Leong ^a   Chang, Yu Chiuan ^b   Lin, Jau Chen ^c   Chen, Chun Chi ^b   Pan, Szu Hua ^d   Wu, Chen Tu ^a   Chen, Hsuan Yu ^e   Yang, Shuenn Chen ^b   Hong, Tse Ming ^d   Yang, Pan Chyr ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e INSTITUTE OF STATISTICAL SCIENCE   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTAGOMIR; ANTISENSE OLIGONUCLEOTIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MICRORNA 135B; UNCLASSIFIED DRUG;

CANCER; CELL ORGANELLE; INHIBITION; MOLECULAR ANALYSIS; TUMOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER; MALE; METASTASIS; MOUSE; NONHUMAN; ONCOGENE; OUTCOME ASSESSMENT; PREDICTIVE VALUE; SIGNAL TRANSDUCTION; TUMOR INVASION; UPREGULATION;

EID: 84878703345     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2876     Document Type: Article

References (57)

1. Chen, K. & Rajewsky, N. The evolution of gene regulation by transcription factors and microRNAs. Nat. Rev. Genet. 8, 93-103 (2007) (Pubitemid 46122839)
2. Krol, J., Loedige, I. & Filipowicz, W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597-610 (2010)
3. Ebert, M. S. & Sharp, P. A. Roles for microRNAs in conferring robustness to biological processes. Cell 149, 515-524 (2012)
4. Valastyan, S., Benaich, N., Chang, A., Reinhardt, F. & Weinberg, R. A. Concomitant suppression of three target genes can explain the impact of a microRNA on metastasis. Genes Dev. 23, 2592-2597 (2009)
5. Png, K. J., Halberg, N., Yoshida, M. & Tavazoie, S. F. A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature 481, 190-194 (2012)
6. Yu, S. L. et al. MicroRNA signature predicts survival and relapse in lung cancer. Cancer Cell 13, 48-57 (2008)
7. Lin, P. Y., Yu, S. L. & Yang, P. C. MicroRNA in lung cancer. Br. J. Cancer 103, 1144-1148 (2010)
8. Hu, Z. et al. Genetic variants of miRNA sequences and non-small cell lung cancer survival. J. Clin. Invest. 118, 2600-2608 (2008) (Pubitemid 351949787)
9. Jemal, A. et al. Cancer statistics, 2009. CA Cancer J. Clin. 59, 225-249 (2009)
10. White, N. M. et al. Metastamirs: a stepping stone towards improved cancer management. Nat. Rev. Clin. Oncol. 8, 75-84 (2011)
11. Dykxhoorn, D. M. MicroRNAs and metastasis: little RNAs go a long way. Cancer Res. 70, 6401-6406 (2010)
12. Chen, J. J. et al. Global analysis of gene expression in invasion by a lung cancer model. Cancer Res. 61, 5223-5230 (2001) (Pubitemid 32681557)
13. Schaap-Oziemlak, A. M. et al. MicroRNA hsa-miR-135b regulates mineralization in osteogenic differentiation of human unrestricted somatic stem cells. Stem Cells Dev. 19, 877-885 (2010)
14. Chim, S. S. et al. Detection and characterization of placental microRNAs in maternal plasma. Clin. Chem. 54, 482-490 (2008) (Pubitemid 351348154)
15. Maccani, M. A., Padbury, J. F. & Marsit, C. J. miR-16 and miR-21 Expression in the placenta is associated with fetal growth. PLoS One 6, e21210 (2011)
16. Nagel, R. et al. Regulation of the adenomatous polyposis coli gene by the miR- 135 family in colorectal cancer. Cancer Res. 68, 5795-5802 (2008)
17. Lowery, A. J. et al. MicroRNA signatures predict oestrogen receptor, progesterone receptor and HER2/neu receptor status in breast cancer. Breast Cancer Res. 11, R27 (2009)
18. Tong, A. W. et al. MicroRNA profile analysis of human prostate cancers. Cancer Gene. Ther. 16, 206-216 (2009)
19. Matsuyama, H. et al. miR-135b mediates NPM-ALK-driven oncogenicity and renders IL-17-producing immunophenotype to anaplastic large cell lymphoma. Blood 118, 6881-6892 (2011)
20. Feng, R. et al. miR-126 functions as a tumour suppressor in human gastric cancer. Cancer Lett. 298, 50-63 (2010)
21. Liu, B., Peng, X. C., Zheng, X. L., Wang, J. & Qin, Y. W. MiR-126 restoration downregulate VEGF and inhibit the growth of lung cancer cell lines in vitro and in vivo. Lung Cancer 66, 169-175 (2009)
22. Ebert, M. S., Neilson, J. R. & Sharp, P. A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 4, 721-726 (2007) (Pubitemid 47338166)
23. Grimson, A. et al. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27, 91-105 (2007) (Pubitemid 46991392)
24. Onken, M. D., Worley, L. A. & Harbour, J. W. A metastasis modifier locus on human chromosome 8p in uveal melanoma identified by integrative genomic analysis. Clin. Cancer Res. 14, 3737-3745 (2008)
25. Chen, L. et al. Downregulation of tumour suppressor gene FEZ1/LZTS1 in breast carcinoma involves promoter methylation and associates with metastasis. Breast Cancer Res. Treat. 116, 471-478 (2009)
26. Pan, D. The hippo signaling pathway in development and cancer. Dev. Cell 19, 491-505 (2010)
27. Zhao, B., Tumaneng, K. & Guan, K. L. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 13, 877-883 (2011)
28. Bao, Y., Hata, Y., Ikeda, M. & Withanage, K. Mammalian Hippo pathway: from development to cancer and beyond. J. Biochem. 149, 361-379 (2011)
29. Hinrichs, A. S. et al. The UCSC Genome Browser Database: update 2006. Nucleic Acids Res. 34, D590-D598 (2006)
30. Ma, L. & Weinberg, R. A. Micromanagers of malignancy: role of microRNAs in regulating metastasis. Trends Genet. 24, 448-456 (2008)
31. Brabletz, S. & Brabletz, T. The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer? EMBO Rep. 11, 670-677 (2010)
32. Ma, L. et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol. 12, 247-256 (2010)
33. Bandres, E. et al. Identification by real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol. Cancer 5, 29 (2006)
34. Sarver, A. L. et al. Human colon cancer profiles show differential microRNA expression depending on mismatch repair status and are characteristic of undifferentiated proliferative states. BMC Cancer 9, 401 (2009)
35. Wang, G. et al. Transcription factor and microRNA regulation in androgen-dependent and -independent prostate cancer cells. BMC Genomics 9(Suppl 2): S22 (2008)
36. Vecchione, A. et al. FEZ1/LZTS1 is downregulated in high-grade bladder cancer, and its restoration suppresses tumorigenicity in transitional cell carcinoma cells. Am. J. Pathol. 160, 1345-1352 (2002) (Pubitemid 34411638)
37. Olson, J. E. et al. Centrosome-related genes, genetic variation, and risk of breast cancer. Breast Cancer Res. Treat. 125, 221-228 (2011)
38. Califano, D. et al. FEZ1/LZTS1 protein expression in ovarian cancer. J. Cell Physiol. 222, 382-386 (2010)
39. Nonaka, D. et al. Reduced FEZ1/LZTS1 expression and outcome prediction in lung cancer. Cancer Res. 65, 1207-1212 (2005) (Pubitemid 40270145)
40. Toyooka, S. et al. Differential expression of FEZ1/LZTS1 gene in lung cancers and their cell cultures. Clin. Cancer Res. 8, 2292-2297 (2002) (Pubitemid 34753603)
41. Vecchione, A. et al. Fez1/Lzts1 absence impairs Cdk1/Cdc25C interaction during mitosis and predisposes mice to cancer development. Cancer Cell 11, 275-289 (2007) (Pubitemid 46349844)
42. Wang, X. X. et al. Downregulation of leucine zipper putative tumour suppressor 1 is associated with poor prognosis, increased cell motility and invasion, and epithelial-to-mesenchymal transition characteristics in human breast carcinoma. Hum. Pathol. 42, 1410-1419 (2011)
43. Zhao, B., Li, L., Lei, Q. & Guan, K. L. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 24, 862-874 (2010)
44. Avruch, J., Zhou, D., Fitamant, J. & Bardeesy, N. Mst1/2 signalling to Yap: gatekeeper for liver size and tumour development. Br. J. Cancer 104, 24-32 (2011)
45. Cornils, H., Kohler, R. S., Hergovich, A. & Hemmings, B. A. Downstream of human NDR kinases: impacting on c-myc and p21 protein stability to control cell cycle progression. Cell Cycle 10, 1897-1904 (2011)
46. Dong, J. et al. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133 (2007) (Pubitemid 47410268)
47. Zhang, J. et al. YAP-dependent induction of amphiregulin identifies a non-cellautonomous component of the Hippo pathway. Nat. Cell Biol. 11, 1444-1450 (2009)
48. Huang, W. et al. The N-terminal phosphodegron targets TAZ/WWTR1 for SCFbeta-TrCP dependent degradation in response to PI3K inhibition. J. Biol. Chem. 287, 26245-26253 (2012)
49. Heallen, T. et al. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332, 458-461 (2011)
50. Varelas, X. et al. The Hippo pathway regulates Wnt/beta-catenin signaling. Dev. Cell 18, 579-591 (2010)
51. Konsavage, Jr W. M., Kyler, S. L., Rennoll, S. A., Jin, G. & Yochum, G. S. Wnt/ beta-Catenin signaling regulates Yes-associated protein (YAP) gene expression in colorectal carcinoma cells. J. Biol. Chem. 287, 11730-11739 (2012)
52. Lujambio, A. & Esteller, M. How epigenetics can explain human metastasis: a new role for microRNAs. Cell Cycle 8, 377-382 (2009)
53. Pollard, J. W. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4, 71-78 (2004) (Pubitemid 38082155)
54. Grivennikov, S. I., Greten, F. R. & Karin, M. Immunity, inflammation, and cancer. Cell 140, 883-899 (2010)
55. Necela, B. M., Carr, J. M., Asmann, Y. W. & Thompson, E. A. Differential expression of microRNAs in tumors from chronically inflamed or genetic (APC(Min/)) models of colon cancer. PLoS One 6, e18501 (2011)
56. Chu, Y.W. et al. Selection of invasive and metastatic subpopulations from a human lung adenocarcinoma cell line. Am. J. Respir. Cell Mol. Biol. 17, 353-360 (1997)
57. Chan, M. W. et al. Hypermethylation of 18S and 28S ribosomal DNAs predicts progression-free survival in patients with ovarian cancer. Clin. Cancer Res. 11, 7376-7383 (2005). (Pubitemid 41507697)