Regulation of sodium iodide symporter gene expression by Rac1/p38β mitogen-activated protein kinase signaling pathway in MCF-7 breast cancer cells

Journal of Biological Chemistry

Volumn 287, Issue 5, 2012, Pages 3292-3300

  Kogai, Takahiko ^a,b   Liu, Yan Yun ^a,b   Mody, Kaizeen ^a,b   Shamsian, Deborah V ^a,b   Brent, Gregory A ^a,b  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALL-TRANS-RETINOIC ACID; BREAST CANCER; BREAST CANCER CELLS; DIFFERENTIAL REGULATION; DOMINANT-NEGATIVE MUTANTS; ISOFORMS; MCF-7 BREAST CANCER CELLS; MCF-7 CELLS; MITOGEN ACTIVATED PROTEIN KINASE; OVER-EXPRESSION; RT-PCR ANALYSIS; SIGNAL TRANSDUCTION PATHWAYS; SIGNALING PATHWAYS; SMALL INTERFERING RNA; SODIUM IODIDES;

CELL CULTURE; CELL PROLIFERATION; DISEASES; ENZYMES; GENE EXPRESSION; GENE EXPRESSION REGULATION; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; RNA; SIGNAL TRANSDUCTION; SODIUM;

CELLS;

MITOGEN ACTIVATED PROTEIN KINASE 11; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE 3; RAC1 PROTEIN; RETINOIC ACID; SODIUM IODIDE SYMPORTER;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG EFFECT; ENZYME PHOSPHORYLATION; GENE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; MUTANT; NIS GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; THYROID CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IODINE; ISOENZYMES; MAP KINASE SIGNALING SYSTEM; NEOPLASM PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RAC1 GTP-BINDING PROTEIN; RATS; SYMPORTERS; THYROID GLAND; TRETINOIN;

RATTUS;

EID: 84863033801     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.315523     Document Type: Article

References (37)

1. Wagner, E. F., and Nebreda, A. R. (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nat. Rev. Cancer 9, 537-549
2. Dohán, O., De la Vieja, A., Paroder, V., Riedel, C., Artani, M., Reed, M., Ginter, C. S., and Carrasco, N. (2003) The sodium/iodide symporter (NIS). Characterization, regulation, and medical significance. Endocr. Rev. 24, 48-77 (Pubitemid 36223279)
3. Trujillo, M. A., Oneal, M. J., McDonough, S., Qin, R., and Morris, J. C. (2010) A probasin promoter, conditionally replicating adenovirus that expresses the sodium iodide symporter (NIS) for radiovirotherapy of prostate cancer. Gene Ther. 17, 1325-1332
4. Penheiter, A. R., Wegman, T. R., Classic, K. L., Dingli, D., Bender, C. E., Russell, S. J., and Carlson, S. K. (2010) Sodium iodide symporter (NIS)-mediated radiovirotherapy for pancreatic cancer. AJR Am. J. Roentgenol. 195, 341-349
5. Riesco-Eizaguirre, G., De la Vieja, A., Rodríguez, I., Miranda, S., Martín-Duque, P., Vassaux, G., and Santisteban, P. (2011) Telomerase-driven expression of the sodium iodide symporter (NIS) for in vivo radioiodide treatment of cancer. A new broad-spectrum NIS-mediated antitumor approach. J. Clin. Endocrinol. Metab. 96, E1435-E1443
6. 188Re) Therapy of Liver Cancer After Transcriptionally Targeted Intratumoral in Vivo NIS Gene Delivery. Hum. Gene Ther. 22, 1403-1412
7. Tazebay, U. H., Wapnir, I. L., Levy, O., Dohan, O., Zuckier, L. S., Zhao, Q. H., Deng, H. F., Amenta, P. S., Fineberg, S., Pestell, R. G., and Carrasco, N. (2000) The mammary gland iodide transporter is expressed during lactation and in breast cancer. Nat. Med. 6, 871-878 (Pubitemid 30644744)
8. Wapnir, I. L., van de Rijn, M., Nowels, K., Amenta, P. S., Walton, K., Montgomery, K., Greco, R. S., Dohán, O., and Carrasco, N. (2003) Immunohistochemical profile of the sodium/iodide symporter in thyroid, breast, and other carcinomas using high density tissue microarrays and conventional sections. J. Clin. Endocrinol. Metab. 88, 1880-1888 (Pubitemid 36623418)
9. Welcsh, P. L., and Mankoff, D. A. (2000) Taking up iodide in breast tissue. Nature 406, 688-689
10. Boelaert, K., and Franklyn, J. A. (2003) Sodium iodide symporter. A novel strategy to target breast, prostate, and other cancers? Lancet 361, 796-797 (Pubitemid 36331838)
11. Kogai, T., Schultz, J. J., Johnson, L. S., Huang, M., and Brent, G. A. (2000) Retinoic acid induces sodium/iodide symporter gene expression and radioiodide uptake in the MCF-7 breast cancer cell line. Proc. Natl. Acad. Sci. U.S.A. 97, 8519-8524 (Pubitemid 30639705)
12. Tanosaki, S., Ikezoe, T., Heaney, A., Said, J. W., Dan, K., Akashi, M., and Koeffler, H. P. (2003) Effect of ligands of nuclear hormone receptors on sodium/iodide symporter expression and activity in breast cancer cells. Breast Cancer Res. Treat. 79, 335-345 (Pubitemid 36750941)
13. Kogai, T., Kanamoto, Y., Che, L. H., Taki, K., Moatamed, F., Schultz, J. J., and Brent, G. A. (2004) Systemic retinoic acid treatment induces sodium/iodide symporter expression and radioiodide uptake in mouse breast cancer models. Cancer Res. 64, 415-422 (Pubitemid 38114126)
14. Kogai, T., Kanamoto, Y., Li, A. I., Che, L. H., Ohashi, E., Taki, K., Chandraratna, R. A., Saito, T., and Brent, G. A. (2005) Differential regulation of sodium/iodide symporter gene expression by nuclear receptor ligands in MCF-7 breast cancer cells. Endocrinology 146, 3059-3069 (Pubitemid 41002815)
15. Kogai, T., Taki, K., and Brent, G. A. (2006) Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocr. Relat. Cancer 13, 797-826 (Pubitemid 44763258)
16. Ohashi, E., Kogai, T., Kagechika, H., and Brent, G. A. (2009) Activation of the PI3 kinase pathway by retinoic acid mediates sodium/iodide symporter induction and iodide transport in MCF-7 breast cancer cells. Cancer Res. 69, 3443-3450
17. Kogai, T., Ohashi, E., Jacobs, M. S., Sajid-Crockett, S., Fisher, M. L., Kanamoto, Y., and Brent, G. A. (2008) Retinoic acid stimulation of the sodium/iodide symporter in MCF-7 breast cancer cells is mediated by the insulin growth factor-I/phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase signaling pathways. J. Clin. Endocrinol. Metab. 93, 1884-1892 (Pubitemid 351656534)
18. Alsayed, Y., Uddin, S., Mahmud, N., Lekmine, F., Kalvakolanu, D. V., Minucci, S., Bokoch, G., and Platanias, L. C. (2001) Activation of Rac1 and the p38 mitogen-activated protein kinase pathway in response to all-trans-retinoic acid. J. Biol. Chem. 276, 4012-4019
19. Kogai, T., Endo, T., Saito, T., Miyazaki, A., Kawaguchi, A., and Onaya, T. (1997) Regulation by thyroid-stimulating hormone of sodium/iodide symporter gene expression and protein levels in FRTL-5 cells. Endocrinology 138, 2227-2232 (Pubitemid 27215219)
20. Schmutzler, C., Winzer, R., Meissner-Weigl, J., and Köhrle, J. (1997) Retinoic acid increases sodium/iodide symporter mRNA levels in human thyroid cancer cell lines and suppresses expression of functional symporter in nontransformed FRTL-5 rat thyroid cells. Biochem. Biophys. Res. Commun. 240, 832-838 (Pubitemid 28271806)
21. Pomerance, M., Abdullah, H. B., Kamerji, S., Correze, C., and Blondeau, J. P. (2000) Thyroid-stimulating hormone and cyclic AMP activate p38 mitogen-activated protein kinase cascade. Involvement of protein kinase A, rac1, and reactive oxygen species. J. Biol. Chem. 275, 40539-40546 (Pubitemid 32064691)
22. Jiang, Y., Chen, C., Li, Z., Guo, W., Gegner, J. A., Lin, S., and Han, J. (1996) Characterization of the structure and function of a new mitogen-activated protein kinase (p38β). J. Biol. Chem. 271, 17920-17926 (Pubitemid 26250772)
23. Conrad, P. W., Rust, R. T., Han, J., Millhorn, D. E., and Beitner-Johnson, D. (1999) Selective activation of p38α and p38γ by hypoxia. Role in regulation of cyclin D1 by hypoxia in PC12 cells. J. Biol. Chem. 274, 23570-23576
24. Pramanik, R., Qi, X., Borowicz, S., Choubey, D., Schultz, R. M., Han, J., and Chen, G. (2003) p38 isoforms have opposite effects on AP-1-dependent transcription through regulation of c-Jun. The determinant roles of the isoforms in the p38 MAPK signal specificity. J. Biol. Chem. 278, 4831-4839 (Pubitemid 36800988)
25. Kogai, T., Kanamoto, Y., and Brent, G. A. (2003) The modified firefly luciferase reporter gene (luc+) but not Renilla luciferase is induced by all-trans-retinoic acid in MCF-7 breast cancer cells. Breast Cancer Res. Treat. 78, 119-126 (Pubitemid 36223024)
26. Kogai, T., Sajid-Crockett, S., Newmarch, L. S., Liu, Y. Y., and Brent, G. A. (2008) Phosphoinositide 3-kinase inhibition induces sodium/iodide symporter expression in rat thyroid cells and human papillary thyroid cancer cells. J. Endocrinol. 199, 243-252
27. Weiss, S. J., Philp, N. J., and Grollman, E. F. (1984) Iodide transport in a continuous line of cultured cells from rat thyroid. Endocrinology 114, 1090-1098 (Pubitemid 14134351)
28. Barros, L. F., Young, M., Saklatvala, J., and Baldwin, S. A. (1997) Evidence of two mechanisms for the activation of the glucose transporter GLUT1 by anisomycin. p38(MAP kinase) activation and protein synthesis inhibition in mammalian cells. J. Physiol. 504, 517-525 (Pubitemid 27493851)
29. Eyers, P. A., Craxton, M., Morrice, N., Cohen, P., and Goedert, M. (1998) Conversion of SB 203580-insensitive MAP kinase family members to drug-sensitive forms by a single amino acid substitution. Chem. Biol. 5, 321-328 (Pubitemid 28309985)
30. Ju, H., Nerurkar, S., Sauermelch, C. F., Olzinski, A. R., Mirabile, R., Zimmerman, D., Lee, J. C., Adams, J., Sisko, J., Berova, M., and Willette, R. N. (2002) Sustained activation of p38 mitogen-activated protein kinase contributes to the vascular response to injury. J. Pharmacol. Exp. Ther. 301, 15-20 (Pubitemid 34250274)
31. Munoz, L., Ramsay, E. E., Manetsch, M., Ge, Q., Peifer, C., Laufer, S., and Ammit, A. J. (2010) Novel p38 MAPK inhibitor ML3403 has potent anti-inflammatory activity in airway smooth muscle. Eur. J. Pharmacol. 635, 212-218
32. Wang, X. S., Diener, K., Manthey, C. L., Wang, S., Rosenzweig, B., Bray, J., Delaney, J., Cole, C. N., Chan-Hui, P. Y., Mantlo, N., Lichenstein, H. S., Zukowski, M., and Yao, Z. (1997) Molecular cloning and characterization of a novel p38 mitogen-activated protein kinase. J. Biol. Chem. 272, 23668-23674 (Pubitemid 27410940)
33. Enslen, H., Brancho, D. M., and Davis, R. J. (2000) Molecular determinants that mediate selective activation of p38MAPkinase isoforms.EMBOJ. 19, 1301-1311 (Pubitemid 30151026)
34. Pomerance, M., Carapau, D., Chantoux, F., Mockey, M., Correze, C., Francon, J., and Blondeau, J. P. (2003) CCAAT/enhancer-binding proteinhomologous protein expression and transcriptional activity are regulated by 3′,5′-cyclic adenosine monophosphate in thyroid cells. Mol. Endocrinol. 17, 2283-2294 (Pubitemid 37352538)
35. Raingeaud, J., Gupta, S., Rogers, J. S., Dickens, M., Han, J., Ulevitch, R. J., and Davis, R. J. (1995) Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270, 7420-7426
36. Unterholzner, S., Willhauck, M. J., Cengic, N., Schütz, M., Göke, B., Morris, J. C., and Spitzweg, C. (2006) Dexamethasone stimulation of retinoic acid-induced sodium iodide symporter expression and cytotoxicity of 131I in breast cancer cells. J. Clin. Endocrinol. Metab. 91, 69-78 (Pubitemid 43069120)
37. Beardmore, V. A., Hinton, H. J., Eftychi, C., Apostolaki, M., Armaka, M., Darragh, J., McIlrath, J., Carr, J. M., Armit, L. J., Clacher, C., Malone, L., Kollias, G., and Arthur, J. S. (2005) Generation and characterization of p38β (MAPK11) gene-targeted mice. Mol. Cell Biol. 25, 10454-10464 (Pubitemid 41681967)