MicroRNA-542-3p suppresses tumor cell invasion via targeting AKT pathway in human astrocytoma

Journal of Biological Chemistry

Volumn 290, Issue 41, 2015, Pages 24678-24688

  Cai, Junchao ^a,c   Zhao, Jingjing ^c   Zhang, Nu ^c   Xu, Xiaonan ^a,c   Li, Rong ^a   Yi, Yang ^b   Fang, Lishan ^a,c   Zhang, Le ^a,c   Li, Mengfeng ^a,c   Wu, Jueheng ^c   Zhang, Heng ^c  

^a Department of Microbiology ^*  (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELLS; CHEMICAL ACTIVATION; CYTOLOGY; ENZYMES; MOLECULAR INTERACTIONS; ONCOGENIC VIRUSES; RNA; TUMORS;

GLIOBLASTOMA CELLS; INTEGRIN-LINKED KINASE; MOLECULAR MECHANISM; NEGATIVE REGULATORS; NUCLEAR TRANSLOCATIONS; THERAPEUTIC TARGETS; TRANSACTIVATION ACTIVITY; TUMOR CELL INVASION;

DIAGNOSIS;

AKT1 PROTEIN; BETA CATENIN; INTEGRIN LINKED KINASE; MICRORNA; MICRORNA 542 3P; PIK3R1 PROTEIN; PROTEIN KINASE B; REGULATOR PROTEIN; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; AKT1 PROTEIN, HUMAN; INTEGRIN-LINKED KINASE; MIRN542 MICRORNA, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PIK3R1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE;

ARTICLE; ASTROCYTOMA CELL; CANCER GRADING; CANCER INHIBITION; CANCER PATIENT; CANCER PROGNOSIS; CELL NUCLEUS; COHORT ANALYSIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME DEFECT; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE CONTROL; GENE FUNCTION; GENE OVEREXPRESSION; GENE TARGETING; GLIOBLASTOMA; GLIOMA CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR TRANSPORT; PIK3R1 GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSACTIVATION; TUMOR INVASION; 3' UNTRANSLATED REGION; DISEASE COURSE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROGNOSIS; TUMOR CELL LINE; UPREGULATION;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; BETA CATENIN; CELL LINE, TUMOR; DISEASE PROGRESSION; DOWN-REGULATION; GLIOBLASTOMA; HUMANS; MICRORNAS; NEOPLASM GRADING; NEOPLASM INVASIVENESS; PHOSPHATIDYLINOSITOL 3-KINASES; PROGNOSIS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84943800564     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.649004     Document Type: Article

References (45)

1. Arko, L., Katsyv, I., Park, G. E., Luan, W. P., and Park, J. K. (2010) Experimental approaches for the treatment of malignant gliomas. Pharmacol. Ther. 128, 1-36
2. Balmaceda, C., Peereboom, D., Pannullo, S., Cheung, Y. K., Fisher, P. G., Alavi, J., Sisti, M., Chen, J., and Fine, R. L. (2008) Multi-institutional phase II study of temozolomide administered twice daily in the treatment of recurrent high-grade gliomas. Cancer 112, 1139-1146
3. Wong, E. T., Hess, K. R., Gleason, M. J., Jaeckle, K. A., Kyritsis, A. P., Prados, M. D., Levin, V. A., and Yung, W. K. (1999) Outcomes and prognostic factors in recurrent glioma patients enrolled onto phase II clinical trials. J. Clin. Oncol. 17, 2572-2578
4. Wang, H., Wang, H., Zhang, W., Huang, H. J., Liao, W. S., and Fuller, G. N. (2004) Analysis of the activation status of Akt, NFκB, and Stat3 in human diffuse gliomas. Lab. Invest. 84, 941-951
5. Antonelli, M., Massimino, M., Morra, I., Garrè, M. L., Gardiman, M. P., Buttarelli, F. R., Arcella, A., and Giangaspero, F. (2012) Expression of pERK and pAKT in pediatric high grade astrocytomas: correlation with YKL40 and prognostic significance. Neuropathology 32, 133-138
6. Molina, J. R., Hayashi, Y., Stephens, C., and Georgescu, M. M. (2010) Invasive glioblastoma cells acquire stemness and increased Akt activation. Neoplasia 12, 453-463
7. Holland, E. C., Celestino, J., Dai, C., Schaefer, L., Sawaya, R. E., and Fuller, G. N. (2000) Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat. Genet. 25, 55-57
8. Zhang, B., Gu, F., She, C., Guo, H., Li, W., Niu, R., Fu, L., Zhang, N., and Ma, Y. (2009) Reduction of Akt2 inhibits migration and invasion of glioma cells. Int. J. Cancer 125, 585-595
9. Sonoda, Y., Ozawa, T., Aldape, K. D., Deen, D. F., Berger, M. S., and Pieper, R. O. (2001) Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. Cancer Res. 61, 6674-6678
10. Zhang, J., Han, L., Zhang, A., Wang, Y., Yue, X., You, Y., Pu, P., and Kang, C. (2010) AKT2 expression is associated with glioma malignant progression and required for cell survival and invasion. Oncol. Rep. 24, 65-72
11. Han, L., Yang, Y., Yue, X., Huang, K., Liu, X., Pu, P., Jiang, H., Yan, W., Jiang, T., and Kang, C. (2010) Inactivation of PI3K/AKT signaling inhibits glioma cell growth through modulation of β-catenin-mediated transcription. Brain Res. 1366, 9-17
12. Kwiatkowska, A., Kijewska, M., Lipko, M., Hibner, U., and Kaminska, B. (2011) Downregulation of Akt and FAK phosphorylation reduces invasion of glioblastoma cells by impairment of MT1-MMP shuttling to lamellipodia and downregulates MMPs expression. Biochim. Biophys. Acta 1813, 655-667
13. Matheny, R. W., Jr., and Adamo, M. L. (2009) Current perspectives on Akt Akt-ivation and Akt-ions. Exp. Biol. Med. 234, 1264-1270
14. Quayle, S. N., Lee, J. Y., Cheung, L. W., Ding, L., Wiedemeyer, R., Dewan, R. W., Huang-Hobbs, E., Zhuang, L., Wilson, R. K., Ligon, K. L., Mills, G. B., Cantley, L. C., and Chin, L. (2012) Somatic mutations of PIK3R1 promote gliomagenesis. PLoS One 7, e49466
15. Murga, C., Zohar, M., Teramoto, H., and Gutkind, J. S. (2002) Rac1 and RhoG promote cell survival by the activation of PI3K and Akt, independently of their ability to stimulate JNK and NF-κB. Oncogene 21, 207-216
16. Mueller, W., Mizoguchi, M., Silen, E., D'Amore, K., Nutt, C L., and Louis, D. N. (2005) Mutations of the PIK3CA gene are rare in human glioblastoma. Acta Neuropathol. 109, 654-655
17. Broderick, D. K., Di, C., Parrett, T. J., Samuels, Y. R., Cummins, J. M., McLendon, R. E., Fults, D. W., Velculescu, V. E., Bigner, D. D., and Yan, H. (2004) Mutations of PIK3CA in anaplastic oligodendrogliomas, highgrade astrocytomas, and medulloblastomas. Cancer Res. 64, 5048-5050
18. Li, J., Zhang, H., Wu, J., Guan, H., Yuan, J., Huang, Z., and Li, M. (2010) Prognostic significance of integrin-linked kinase1 overexpression in astrocytoma. Int. J. Cancer 126, 1436-1444
19. Schickel, R., Boyerinas, B., Park, S. M., and Peter, M. E. (2008) MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 27, 5959-5974
20. Calin, G. A., and Croce, C M. (2006) MicroRNA signatures in human cancers. Nat. Rev. Cancer 6, 857-866
21. Ma, L., Teruya-Feldstein, J., and Weinberg, R. A. (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682-688
22. Hayes, J., Peruzzi, P. P., and Lawler, S. (2014) MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol. Med. 20, 460-469
23. Garofalo, M., and Croce, C M. (2013) MicroRNAs as therapeutic targets in chemoresistance. Drug Resist. Updat. 16, 47-59
24. Yoon, S., Choi, Y. C., Lee, S., Jeong, Y., Yoon, J., and Baek, K. (2010) Induction of growth arrest by miR-542-3p thattargets survivin. FEBS Lett. 584, 4048-4052
25. He, T., Qi, F., Jia, L., Wang, S., Song, N., Guo, L., Fu, Y., and Luo, Y. (2014) MicroRNA-542-3p inhibits tumour angiogenesis by targeting angiopoietin-2. J. Pathol. 232, 499-508
26. Wang, Y., Jia, L., and Wu, C Y. (2008) Triptolide inhibits the differentiation of Th17 cells and suppresses collagen-induced arthritis. Scand. J. Immunol. 68, 383-390
27. Li, J., Zhang, N., Song, L. B., Liao, W. T., Jiang, L. L., Gong, L. Y., Wu, J., Yuan, J., Zhang, H. Z., Zeng, M. S., and Li, M. (2008) Astrocyte elevated gene-1 is a novel prognostic marker for breast cancer progression and overall patient survival. Clin. Cancer Res. 14, 3319-3326
28. Li, H., Du, S., Yang, L., Chen, Y., Huang, W., Zhang, R., Cui, Y., Yang, J., Chen, D., Li, Y., Zhang, S., Zhou, J., Wei, Z., and Yao, Z. (2009) Rapid pulmonary fibrosis induced by acute lung injury via a lipopolysaccharide three-hit regimen. Innate Immun. 15, 143-154
29. Manning, B. D., and Cantley, L. C. (2007) AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274
30. Bleeker, F. E., Lamba, S., Zanon, C., Van Tilborg, A. A., Leenstra, S., Troost, D., Hulsebos, T., Vandertop, W. P., and Bardelli, A. (2009) Absence of AKT1 mutations in glioblastoma. PLoS One 4, e5638
31. Cortez, V., Nair, B. C., Chakravarty, D., and Vadlamudi, R. K. (2011) Integrin-linked kinase 1: role in hormonal cancer progression. Front. Biosci. 3, 788-796
32. Troussard, A. A., McDonald, P. C., Wederell, E. D., Mawji, N. M., Filipenko, N. R., Gelmon, K. A., Kucab, J. E., Dunn, S. E., Emerman, J. T., Bally, M. B., and Dedhar, S. (2006) Preferential dependence of breast cancer cells versus normal cells on integrin-linked kinase for protein kinase B/Akt activation and cell survival. Cancer Res. 66, 393-403
33. Filipenko, N. R., Attwell, S., Roskelley, C., and Dedhar, S. (2005) Integrinlinked kinase activity regulates Rac- and Cdc42-mediated actin cytoskeleton reorganization via α-PIX. Oncogene 24, 5837-5849
34. Edwards, L. A., Woo, J., Huxham, L. A., Verreault, M., Dragowska, W. H., Chiu, G., Rajput, A., Kyle, A. H., Kalra, J., Yapp, D., Yan, H., Minchinton, A. I., Huntsman, D., Daynard, T., Waterhouse, D. N., Thiessen, B., Dedhar, S., and Bally, M. B. (2008) Suppression of VEGF secretion and changes in glioblastoma multiforme microenvironment by inhibition of integrinlinked kinase (ILK). Mol. Cancer Ther. 7, 59-70
35. Fu, Y., Zhang, Q., Kang, C., Zhang, J., Zhang, K., Pu, P., Wang, G., and Wang, T. (2009) Inhibitory effects of adenovirus mediated Akt1 and PIK3R1 shRNA on the growth of malignant tumor cells in vitro and in vivo. Cancer Biol. Ther. 8, 1002-1009
36. Weber, G. L., Parat, M. O., Binder, Z. A., Gallia, G. L., and Riggins, G. J. (2011) Abrogation of PIK3CA or PIK3R1 reduces proliferation, migration, and invasion in glioblastoma multiforme cells. Oncotarget 2, 833-849
37. Li, C., Zhou, C., Wang, S., Feng, Y., Lin, W., Lin, S., Wang, Y., Huang, H., Liu, P., Mu, Y. G., and Shen, X. (2011) Sensitization of glioma cells to tamoxifen-induced apoptosis by PI3-kinase inhibitor through the GSK-3β/β-catenin signaling pathway. PLoS One 6, e27053
38. Williams, S. P., Nowicki, M. O., Liu, F., Press, R., Godlewski, J., Abdel-Rasoul, M., Kaur, B., Fernandez, S. A., Chiocca, E. A., and Lawler, S. E. (2011) Indirubins decrease glioma invasion by blocking migratory phenotypes in both the tumor and stromal endothelial cell compartments. Cancer Res. 71, 5374-5380
39. Kahlert, U. D., Maciaczyk, D., Doostkam, S., Orr, B. A., Simons, B., Bogiel, T., Reithmeier, T., Prinz, M., Schubert, J., Niedermann, G., Brabletz, T., Eberhart, C G., Nikkhah, G., and Maciaczyk, J. (2012) Activation of canonical WNT/β-catenin signaling enhances in vitro motility of glioblastoma cells by activation of ZEB1 and other activators of epithelial-tomesenchymal transition. Cancer Lett. 325, 42-53
40. Pu, P., Zhang, Z., Kang, C., Jiang, R., Jia, Z., Wang, G., and Jiang, H. (2009) Downregulation of Wnt2 and β-catenin by siRNA suppresses malignant glioma cell growth. Cancer Gene Ther. 16, 351-361
41. MacDonald, B. T., Tamai, K., and He, X. (2009) Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26
42. Wang, K., Park, J. O., and Zhang, M. Q. (2013) Treatment of glioblastoma multiforme using a combination of small interfering RNA targeting epidermal growth factor receptor and β-catenin. J. Gene Med. 15, 42-50
43. Kahn, M. (2014) Can we safely target the WNT pathway? Nat. Rev. Drug Discov. 13, 513-532
44. Oneyama, C., Morii, E., Okuzaki, D., Takahashi, Y., Ikeda, J., Wakabayashi, N., Akamatsu, H., Tsujimoto, M., Nishida, T., Aozasa, K., and Okada, M. (2012) MicroRNA-mediated upregulation of integrin-linked kinase promotes Src-induced tumor progression. Oncogene 31, 1623-1635
45. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254