MicroRNA-182 and MicroRNA-200a control G-protein subunit α-13 (GNA13) expression and cell invasion synergistically in prostate cancer cells

Journal of Biological Chemistry

Volumn 288, Issue 11, 2013, Pages 7986-7995

  Rasheed, Suhail Ahmed Kabeer ^a   Teo, Cui Rong ^a   Beillard, Emmanuel Jean ^a   Voorhoeve, P Mathijs ^a,b   Casey, Patrick J ^a  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ECTOPIC EXPRESSIONS; EXPRESSION ANALYSIS; G PROTEIN COUPLED RECEPTORS; HETEROTRIMERIC G PROTEINS; INVERSE CORRELATION; POST-TRANSCRIPTIONAL; PROSTATE CANCER CELLS; PROTEIN EXPRESSIONS;

CELL CULTURE; DISEASES; PROTEINS; RNA;

CELLS;

CELL PROTEIN; G PROTEIN SUBUNIT ALPHA 13; MICRORNA 182; MICRORNA 200A; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CANCER INVASION; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; G PROTEIN SUBUNIT ALPHA 13 GENE; GENE EXPRESSION REGULATION; GENE LOSS; GENE REPRESSION; GENE SILENCING; IN VITRO STUDY; ONCOGENE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN PROCESSING; RNA BINDING;

CELL LINE, TUMOR; CHEMOKINE CXCL12; COLLAGEN; DRUG COMBINATIONS; GENE EXPRESSION REGULATION, NEOPLASTIC; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HEK293 CELLS; HUMANS; LAMININ; LIGANDS; MALE; MICRORNAS; MUTAGENESIS, SITE-DIRECTED; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PROGNOSIS; PROSTATIC NEOPLASMS; PROTEOGLYCANS; RNA PROCESSING, POST-TRANSCRIPTIONAL;

EID: 84875189997     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.437749     Document Type: Article

References (39)

1. Siegel, R., Naishadham, D., and Jemal, A. (2012) Cancer Statistics. Cancer J. Clin. 62, 10-29
2. Lappano, R., and Maggiolini, M. (2012) GPCRs and cancer. Acta Pharmacologica Sinica 33, 351-362
3. Spiegelberg, B. D., and Hamm, H. E. (2007) Roles of G-protein-coupled receptor signaling in cancer biology and gene transcription. Curr. Opin. Gen. Dev. 17, 40-44
4. Pi, M., and Quarles, L. D. (2012) GPRC6A regulates prostate cancer progression. The Prostate 72, 399-409
5. Kasina, S., and Macoska, J. A. (2012) The CXCL12/CXCR4 axis promotes ligand-independent activation of the androgen receptor. Mol. Cell Endocrin. 351, 249-263
6. Darash-Yahana, M., Pikarsky, E., Abramovitch, R., Zeira, E., Pal, B., Karplus, R., Beider, K., Avniel, S., Kasem, S., Galun, E., and Peled, A. (2004) Role of high expression levels of CXCR4 in tumor growth, vascularization, and metastasis. FASEB J. 18, 1240-1242
7. Li, S., Huang, S., and Peng, S. B. (2005) Overexpression of G proteincoupled receptors in cancer cells: involvement in tumor progression. Int. J. Oncol. 27, 1329-1339
8. Hains, M. D., Wing, M. R., Maddileti, S., Siderovski, D. P., and Harden, T. K. (2006) Galpha12/13- and rho-dependent activation of phospholipase Cε by lysophosphatidic acid and thrombin receptors. Mol. Pharm. 69, 2068-2075
9. Zeng, Y., Kakehi, Y., Nouh, M. A., Tsunemori, H., Sugimoto, M., and Wu, X. X. (2009) Gene expression profiles of lysophosphatidic acid-related molecules in the prostate: relevance to prostate cancer and benign hyperplasia. The Prostate 69, 283-292
10. Wettschureck, N., and Offermanns, S. (2005) Mammalian G proteins and their cell type specific functions. Physiol. Rev. 85, 1159-1204
11. Kelly, P., Casey, P. J., and Meigs, T. E. (2007) Biologic functions of the G12 subfamily of heterotrimeric g proteins: growth, migration, and metastasis. Biochemistry 46, 6677-6687
12. Kelly, P., Moeller, B. J., Juneja, J., Booden, M. A., Der, C. J., Daaka, Y., Dewhirst, M. W., Fields, T. A., and Casey, P. J. (2006) The G12 family of heterotrimeric G proteins promotes breast cancer invasion and metastasis. Proc. Natl. Acad. Sci. U.S.A. 103, 8173-8178
13. Kelly, P., Stemmle, L. N., Madden, J. F., Fields, T. A., Daaka, Y., and Casey, P. J. (2006) A role for the G12 family of heterotrimeric G proteins in prostate cancer invasion. J. Biol. Chem. 281, 26483-26490
14. Cheong, S. C., Chandramouli, G. V., Saleh, A., Zain, R. B., Lau, S. H., Sivakumaren, S., Pathmanathan, R., Prime, S. S., Teo, S. H., Patel, V., and Gutkind, J. S. (2009) Gene expression in human oral squamous cell carcinoma is influenced by risk factor exposure. Oral. Oncology 45, 712-719
15. Kozasa, T., Hajicek, N., Chow, C. R., and Suzuki, N. (2011) Signalling mechanisms of RhoGTPase regulation by the heterotrimeric G proteins G12 and G13. J. Biochem. 150, 357-369
16. Chen, Z., Guo, L., Hadas, J., Gutowski, S., Sprang, S. R., and Sternweis, P. C. (2012) Activation of p115-RhoGEF Requires Direct Association of Gα13 and the Dbl Homology Domain. J. Biol. Chem. 287, 25490-25500
17. Malchinkhuu, E., Sato, K., Maehama, T., Mogi, C., Tomura, H., Ishiuchi, S., Yoshimoto, Y., Kurose, H., and Okajima, F. (2008) S1P(2) receptors mediate inhibition of glioma cell migration through Rho signaling pathways independent of PTEN. Biochem. Biophys. Res. Comm. 366, 963-968
18. Shumay, E., Tao, J., Wang, H. Y., and Malbon, C. C. (2007) Lysophosphatidic acid regulates trafficking of α2-adrenergic receptors: the Gβ13/p115RhoGEF/JNK pathway stimulates receptor internalization. J. Biol. Chem. 282, 21529-21541
19. Kim, E. S., Lee, K. M., Noh, D. Y., and Moon, A. (2011) Regulation of matrix metalloproteinases and invasion by G(α12/13) proteins in NIH3T3 mouse fibroblast cells. Oncology Res. 19, 297-301
20. Huang, Y., Shen, X. J., Zou, Q., Wang, S. P., Tang, S. M., and Zhang, G. Z. (2011) Biological functions of microRNAs: a review. J. Physiol. Biochem. 67, 129-139
21. Rutnam, Z. J., and Yang, B. B. (2012) The involvement of microRNAs in malignant transformation. Histology Histopathol. 27, 1263-1270
22. Asangani, I. A., Rasheed, S. A., Nikolova, D. A., Leupold, J. H., Colburn, N. H., Post, S., and Allgayer, H. (2008) MicroRNA-21 (miR-21) post-transcriptionally down-regulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27, 2128-2136
23. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y., and Goodall, G. J. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593-601
24. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., and Brabletz, T. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589
25. Beillard, E., Ong, S. C., Giannakakis, A., Guccione, E., Vardy, L. A., and Voorhoeve, P. M. (2012) miR-Sens-a retroviral dual-luciferase reporter to detect microRNA activity in primary cells. RNA 18, 1091-1100
26. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
27. Rasheed, S. A., Efferth, T., Asangani, I. A., and Allgayer, H. (2010) First evidence that the antimalarial drug artesunate inhibits invasion and in vivo metastasis in lung cancer by targeting essential extracellular proteases. Int. J. Cancer 127, 1475-1485
28. Sayas, C. L., Avila, J., and Wandosell, F. (2002) Glycogen synthase kinase-3 is activated in neuronal cells by Gα12 and Gα13 by Rho-independent and Rho-dependent mechanisms. J. Neuro. 22, 6863-6875
29. Juneja, J., Cushman, I., and Casey, P. J. (2011) G12 signaling through c-Jun NH2-terminal kinase promotes breast cancer cell invasion. PloS One 6, e26085
30. Tan, W., Martin, D., and Gutkind, J. S. (2006) The Gα13-Rho signaling axis is required for SDF-1-induced migration through CXCR4. J. Biol. Chem. 281, 39542-39549
31. Shan, D., Chen, L., Wang, D., Tan, Y. C., Gu, J. L., and Huang, X. Y. (2006) The G protein Gα (13) is required for growth factor-induced cell migration. Dev. cell 10, 707-718
32. Yagi, H., Tan, W., Dillenburg-Pilla, P., Armando, S., Amornphimoltham, P., Simaan, M., Weigert, R., Molinolo, A. A., Bouvier, M., and Gutkind, J. S. (2011) A synthetic biology approach reveals a CXCR4-G13-Rho signaling axis driving transendothelial migration of metastatic breast cancer cells. Science Signal. 4, ra60
33. Zhang, Z. J., and Ma, S. L. (2012) miRNAs in breast cancer tumorigenesis (Review). Oncology Rep. 27, 903-910
34. Weeraratne, S. D., Amani, V., Teider, N., Pierre-Francois, J., Winter, D., Kye, M. J., Sengupta, S., Archer, T., Remke, M., Bai, A. H., Warren, P., Pfister, S. M., Steen, J. A., Pomeroy, S. L., and Cho, Y. J. (2012) Pleiotropic effects of miR-183 96182 converge to regulate cell survival, proliferation and migration in medulloblastoma. Acta Neuropathol. 123, 539-552
35. Xie, L., Ushmorov, A., Leithäuser, F., Guan, H., Steidl, C., Färbinger, J., Pelzer, C., Vogel, M. J., Maier, H. J., Gascoyne, R. D., Möller, P., and Wirth, T. (2012) FOXO1 is a tumor suppressor in classical Hodgkin lymphoma. Blood 119, 3503-3511
36. Segura, M. F., Hanniford, D., Menendez, S., Reavie, L., Zou, X., Alvarez- Diaz, S., Zakrzewski, J., Blochin, E., Rose, A., Bogunovic, D., Polsky, D., Wei, J., Lee, P., Belitskaya-Levy, I., Bhardwaj, N., Osman, I., and Hernando, E. (2009) Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc. Natl. Acad. Sci. U.S.A. 106, 1814-1819
37. Hu, M., Xia, M., Chen, X., Lin, Z., Xu, Y., Ma, Y., and Su, L. (2010) MicroRNA-141 regulates Smad-interacting protein 1 (SIP1) and inhibits migration and invasion of colorectal cancer cells. Dig. Dis. Sci. 55, 2365-2372
38. Saydam, O., Shen, Y., Würdinger, T., Senol, O., Boke, E., James, M. F., Tannous, B. A., Stemmer-Rachamimov, A. O., Yi, M., Stephens, R. M., Fraefel, C., Gusella, J. F., Krichevsky, A. M., and Breakefield, X. O. (2009) Downregulated microRNA-200a in meningiomas promotes tumor growth by reducing E-cadherin and activating the Wnt/beta-catenin signaling pathway. Mol. Cell Biol. 29, 5923-5940
39. Barshack, I., Lithwick-Yanai, G., Afek, A., Rosenblatt, K., Tabibian-Keissar, H., Zepeniuk, M., Cohen, L., Dan, H., Zion, O., Strenov, Y., Polak-Charcon, S., and Perelman, M. (2010) MicroRNA expression differentiates between primary lung tumors and metastases to the lung. Pathol. Res. Prac. 206, 578-584