The miR-130 family promotes cell migration and invasion in bladder cancer through FAK and Akt phosphorylation by regulating PTEN

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Egawa, Hiroshi ^a   Jingushi, Kentaro ^a   Hirono, Takayuki ^a   Ueda, Yuko ^a   Kitae, Kaori ^a   Nakata, Wataru ^a   Fujita, Kazutoshi ^a   Uemura, Motohide ^a   Nonomura, Norio ^a   Tsujikawa, Kazutake ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3' UNTRANSLATED REGION; FOCAL ADHESION KINASE 1; MICRORNA; MIRN130 MICRORNA, HUMAN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PTEN PROTEIN, HUMAN; PTK2 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; AGED; BLADDER TUMOR; CELL MOTION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE; TUMOR INVASION; VERY ELDERLY;

3' UNTRANSLATED REGIONS; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICRORNAS; MIDDLE AGED; NEOPLASM INVASIVENESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; URINARY BLADDER NEOPLASMS;

EID: 84957569429     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20574     Document Type: Article

References (68)

1. Ferlay, J. et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127, 2893-2917 (2010).
2. Hautmann, R. E., de Petriconi, R. C., Pfeiffer, C. & Volkmer, B. G. Radical cystectomy for urothelial carcinoma of the bladder without neoadjuvant or adjuvant therapy: long-term results in 1100 patients. Eur Urol 61, 1039-1047 (2012).
3. Sylvester, R. J. et al. Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTC risk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol 3, discussion 475-477 (2006).
4. Nagele, U., Anastasiadis, A. G., Stenzl, A. & Kuczyk, M. Radical cystectomy with orthotopic neobladder for invasive bladder cancer: a critical analysis of long-term oncological, functional, and quality of life results. World J Urol 30, 725-732 (2011).
5. Grossman, H. B. et al. Neoadjuvant chemotherapy plus cystectomy compared with cystectomy alone for locally advanced bladder cancer. N Engl J Med 349, 859-866 (2003).
6. Soloway, M. S. Bladder cancer: Lack of progress in bladder cancer-what are the obstacles? Nat Rev Urol 10, 5-6 (2013).
7. Von der Maase, H. et al. Long-term survival results of a randomized trial comparing gemcitabine plus cisplatin, with methotrexate, vinblastine, doxorubicin, plus cisplatin in patients with bladder cancer. J Clin Oncol 23, 4602-4608 (2005).
8. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
9. Friedman, R. C., Farh, K. K.-H., Burge, C. B. & Bartel, D. P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19, 92-105 (2009).
10. Valeri, N. et al. MicroRNA-135b promotes cancer progression by acting as a downstream effector of oncogenic pathways in colon cancer. Cancer Cell 25, 469-483 (2014).
11. Gao, J. et al. miR-34a-5p suppresses colorectal cancer metastasis and predicts recurrence in patients with stage II/III colorectal cancer. Oncogene 31, 4142-4152 (2015).
12. Ma, Y. et al. Elevated oncofoetal miR-17-5p expression regulates colorectal cancer progression by repressing its target gene P130. Nat Commun 3, 1291 (2012).
13. Mogilyansky, E. & Rigoutsos, I. The miR-17/92 cluster: a comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ 20, 1603-1614 (2013).
14. Murphy, B. L. et al. Silencing of the miR-17~92 cluster family inhibits medulloblastoma progression. Cancer Res 73, 7068-7078 (2013).
15. Ell, B. et al. The microRNA-23b/27b/24 cluster promotes breast cancer lung metastasis by targeting metastasis-suppressive gene prosaposin. J Biol Chem 289, 21888-21895 (2014).
16. He, L. et al. A microRNA component of the p53 tumour suppressor network. Nature 447, 1130-1134 (2007).
17. Adam, L. et al. miR-200 expression regulates epithelial-to-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res 15, 5060-5072 (2009).
18. Ma, S. et al. miR-130b Promotes CD133(+) liver tumor-initiating cell growth and self-renewal via tumor protein 53-induced nuclear protein 1. Cell Stem Cell 7, 694-707 (2010).
19. Zhang, W. et al. MicroRNA-301a promotes migration and invasion by targeting TGFBR2 in human colorectal cancer. J Exp Clin Cancer Res 33, 113 (2014).
20. Funamizu, N. et al. MicroRNA-301b promotes cell invasiveness through targeting TP63 in pancreatic carcinoma cells. Int J Oncol 44, 725-734 (2014).
21. Czerniak, B. et al. Concurrent mutations of coding and regulatory sequences of the Ha-ras gene in urinary bladder carcinomas. Hum Pathol 23, 1199-1204 (1992).
22. Billerey, C. et al. Frequent FGFR3 mutations in papillary non-invasive bladder (pTa) tumors. Am J Pathol 158, 1955-1959 (2001).
23. Lopez-Knowles, E. PIK3CA Mutations Are an Early Genetic Alteration Associated with FGFR3 Mutations in Superficial Papillary Bladder Tumors. Cancer Res 66, 7401-7404 (2006).
24. Sarkis, A. S. et al. Nuclear overexpression of p53 protein in transitional cell bladder carcinoma: a marker for disease progression. J Natl Cancer Inst 85, 53-59 (1993).
25. Puzio-Kuter, A. M. et al. Inactivation of p53 and Pten promotes invasive bladder cancer. Genes Dev 23, 675-680 (2009).
26. The Cancer Genome Atlas Research Network. Comprehensive molecular characterization of urothelial bladder carcinoma. Nature 507, 315-322 (2014).
27. Thomas, S. et al. Src and caveolin-1 reciprocally regulate metastasis via a common downstream signaling pathway in bladder cancer. Cancer Res 71, 832-841 (2011).
28. Wang, H. et al. Phosphorylation of RalB is important for bladder cancer cell growth and metastasis. Cancer Res 70, 8760-8769 (2010).
29. Yamasaki, M. et al. α-Lipoic acid suppresses migration and invasion via downregulation of cell surface β 1-integrin expression in bladder cancer cells. J Clin Biochem Nutr 54, 18-25 (2014).
30. Tojkander, S., Gateva, G. & Lappalainen, P. Actin stress fibers-assembly, dynamics and biological roles. J Cell Sci 125, 1855-1864 (2012).
31. Nakamura, K., Yano, H., Schaefer, E. & Sabe H. Different modes and qualities of tyrosine phosphorylation of Fak and Pyk2 during epithelial-mesenchymal transdifferentiation and cell migration: analysis of specific phosphorylation events using site-directed antibodies. Oncogene 20, 2626-2635 (2001).
32. Xia, H. et al. Focal adhesion kinase is upstream of phosphatidylinositol 3-kinase/Akt in regulating fibroblast survival in response to contraction of type I collagen matrices via a beta 1 integrin viability signaling pathway. J Biol Chem 279, 33024-33034 (2004).
33. Tamura, M. et al. PTEN Interactions with Focal Adhesion Kinase and Suppression of the Extracellular Matrix-dependent Phosphatidylinositol 3-Kinase/Akt Cell Survival Pathway. J Biol Chem 274, 20693-20703 (1999).
34. Cheng, J. C.-H., Chou, C. H., Kuo, M. L. & Hsieh, C.-Y. Radiation-enhanced hepatocellular carcinoma cell invasion with MMP-9 expression through PI3K/Akt/NF-kappaB signal transduction pathway. Oncogene 25, 7009-7018 (2006).
35. Tamguney, T. & Stokoe, D. New insights into PTEN. J Cell Sci 120, 4071-4079 (2007).
36. Tsuruta, H. et al. Hyperplasia and carcinomas in Pten-deficient mice and reduced PTEN protein in human bladder cancer patients. Cancer Res 66, 8389-8396 (2006).
37. Siegel, R., Ma, J., Zou, Z. & Jemal, A. Cancer statistics, 2014. CA Cancer J Clin 64, 9-29 (2014).
38. Carneiro, B. A. et al. Emerging therapeutic targets in bladder cancer. Cancer Treat Rev 41, 170-178 (2014).
39. Hollander, M. C., Blumenthal, G. M. & Dennis, P. A. PTEN loss in the continuum of common cancers, rare syndromes and mouse models. Nat Rev Cancer 11, 289-301 (2011).
40. Aveyard, J. S., Skilleter, A., Habuchi, T. & Knowles, M. A. Somatic mutation of PTEN in bladder carcinoma. Br J Cancer 80, 904-908 (1999).
41. Ho, P. L., Kurtova, A. & Chan, K. S. Normal and neoplastic urothelial stem cells: getting to the root of the problem. Nat Rev Urol 9, 583-594 (2012).
42. Knowles, M. A. & Hurst, C. D. Molecular biology of bladder cancer : new insights into pathogenesis and clinical diversity. Nat Rev Cancer 15, 25-41 (2015).
43. Huang, J. et al. SUMO1 modification of PTEN regulates tumorigenesis by controlling its association with the plasma membrane. Nat Commun 3, 911 (2012).
44. Oinuma, I., Ito, Y., Katoh, H. & Negishi, M. Semaphorin 4D/Plexin-B1 stimulates PTEN activity through R-Ras GTPase-activating protein activity, inducing growth cone collapse in hippocampal neurons. J Biol Chem 285, 28200-28209 (2010).
45. Wu, X. et al. Evidence for regulation of the PTEN tumor suppressor by a membrane-localized multi-PDZ domain containing scaffold protein MAGI-2. Proc Natl Acad Sci 97, 4233-4238 (2000).
46. Rahdar, M. et al. A phosphorylation-dependent intramolecular interaction regulates the membrane association and activity of the tumor suppressor PTEN. Proc Natl Acad Sci USA 106, 480-485 (2009).
47. Song, P. et al. Thromboxane A2 receptor activates a Rho-associated kinase/LKB1/PTEN pathway to attenuate endothelium insulin signaling. J Biol Chem 284, 17120-17128 (2009).
48. Matsui, T. et al. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J 15, 2208-2016 (1996).
49. Schoenwaelder, S. M. et al. The protein tyrosine phosphatase Shp-2 regulates RhoA activity. Curr Biol 10, 1523-1526 (2000).
50. Zong, C., Wang, J. & Shi, T.-M. MicroRNA 130b enhances drug resistance in human ovarian cancer cells. Tumour Biol 35, 12151-12156 (2014).
51. Colangelo, T. et al. MicroRNA-130b promotes tumor development and is associated with poor prognosis in colorectal cancer. Neoplasia 15, 1218-1231 (2013).
52. Tsutsumi, A. et al. Focal adhesion kinase is a substrate and downstream effector of SHP-2 complexed with Helicobacter pylori CagA. Mol Cell Biol 26, 261-276 (2006).
53. Kodama, A. et al. Involvement of an SHP-2-Rho small G protein pathway in hepatocyte growth factor/scatter factor-induced cell scattering. Mol Biol Cell 11, 2565-2575 (2000).
54. Overall, C. M. et al. Domain interactions in the gelatinase A.TIMP-2.MT1-MMP activation complex. The ectodomain of the 44-kDa form of membrane type-1 matrix metalloproteinase does not modulate gelatinase A activation. J Biol Chem 275, 39497-39506 (2000).
55. Goebell, P. J. & Knowles, M. A. Bladder cancer or bladder cancers? Genetically distinct malignant conditions of the urothelium. Urol Oncol 28, 409-428 (2010).
56. Lai, K. W. et al. MicroRNA-130b regulates the tumour suppressor RUNX3 in gastric cancer. Eur J Cancer 46, 1456-1463 (2010).
57. Liu, L. et al. The oncogenic role of microRNA-130a/301a/454 in human colorectal cancer via targeting Smad4 expression. PLoS One 8, e55532 (2013).
58. Hall, M. C. et al. The Growth Inhibitory Effect of p21 Adenovirus on Human Bladder Cancer Cells. J Urol 163, 1033-1038 (2000).
59. Peacock, H. et al. Nucleobase and Ribose Modifications Control Immunostimulation by a MicroRNA-122-mimetic RNA. J Am Chem Soc 133, 9200-9203 (2011).
60. Didiano, D. & Hobert, O. Perfect seed pairing is not a generally reliable predictor for miRNA-target interactions. Nat Struct Mol Biol 13, 849-851 (2006).
61. Esquela-Kerscher, A. & Slack, F. J. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 6, 259-269 (2006).
62. Rottiers, V. et al. Pharmacological Inhibition of a MicroRNA Family in Nonhuman Primates by a Seed-Targeting 8-Mer AntimiR. Sci Transl Med 5, 212ra162 (2013).
63. Bertero, T. et al. Systems-level regulation of microRNA networks by miR-130/301 promotes pulmonary hypertension. J Clin Invest 124, 3514-3528 (2014).
64. Pfaff, N. et al. miRNA screening reveals a new miRNA family stimulating iPS cell generation via regulation of Meox2. EMBO Rep 12, 1153-1159 (2011).
65. Brock, M. et al. The hypoxia-induced microRNA-130a controls pulmonary smooth muscle cell proliferation by directly targeting CDKN1A. Int J Biochem Cell Biol 61, 129-137 (2015).
66. Hamilton, M. P. et al. Identification of a pan-cancer oncogenic microRNA superfamily anchored by a central core seed motif. Nat Commun 4, 2730 (2013).
67. Fogh, J. Cultivation, characterization, and identification of human tumor cells with emphasis on kidney, testis, and bladder tumors. Natl Cancer Inst Monogr 49, 5-9 (1978).
68. Grossman, H. B., Wedemeyer, G. & Ren, L. UM-UC-1 and UM-UC-2: characterization of two new human transitional cell carcinoma lines. J Urol 132, 834-837 (1984).