MicroRNA-200b suppresses arsenic-transformed cell migration by targeting protein kinase Cα and wnt5b-protein kinase Cα positive feedback loop and inhibiting Rac1 activation

Journal of Biological Chemistry

Volumn 289, Issue 26, 2014, Pages 18373-18386

  Wang, Zhishan ^a   Humphries, Brock ^a   Xiao, Hua ^a   Jiang, Yiguo ^b   Yang, Chengfeng ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; CELLS; CHEMICAL ACTIVATION; CYTOLOGY; ENZYMES; PROTEINS; RNA;

ACTIN CYTOSKELETON; BIOINFORMATICS ANALYSIS; CANCER METASTASIS; HUMAN BRONCHIAL EPITHELIAL CELLS; LUCIFERASE REPORTER ASSAYS; MECHANISTIC STUDIES; POSITIVE FEEDBACK LOOP; UNTRANSLATED REGIONS;

BIOASSAY;

ARSENIC; MICRORNA 200B; PROTEIN KINASE C ALPHA; RAC1 PROTEIN; SMALL INTERFERING RNA; WNT5B PROTEIN;

3' UNTRANSLATED REGION; ACTIN FILAMENT; ARTICLE; BIOINFORMATICS; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSFORMED CELL; UPREGULATION;

CELL MIGRATION; MICRORNA (MIRNA); PHOSPHORYLATION; RHO GTPASES; SIGNAL TRANSDUCTION; WNT PATHWAY;

ARSENIC; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; ENZYME ACTIVATION; FEEDBACK, PHYSIOLOGICAL; HUMANS; MICRORNAS; PROTEIN BINDING; PROTEIN KINASE C-ALPHA; RAC1 GTP-BINDING PROTEIN; WNT PROTEINS;

EID: 84903529396     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.554246     Document Type: Article

References (49)

1. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
2. Hobert, O. (2008) Gene regulation by transcription factors and micro-RNAs. Science 319, 1785-1786
3. 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
4. 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
5. Korpal, M., Lee, E. S., Hu, G., and Kang, Y. (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 283, 14910-14914
6. Park, S. M., Gaur, A. B., Lengyel, E., and Peter, M. E. (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22, 894-907
7. Lee, J. M., Dedhar, S., Kalluri, R., and Thompson, E. W. (2006) The epithelialmesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 172, 973-981
8. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009) Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890
9. Feng, X., Wang, Z., Fillmore, R., and Xi, Y. (2013) MiR-200, a new star miRNA in human cancer. Cancer Lett. 10.1016/j.canlet. 2013.11.004
10. Hill, L., Browne, G., and Tulchinsky, E. (2013) ZEB/miR-200 feedback loop: at the crossroads of signal transduction in cancer. Int. J. Cancer 132, 745-754
11. Howe, E. N., Cochrane, D. R., and Richer, J. K. (2012) The miR-200 and miR-221/222 microRNA families: opposing effects on epithelial identity. J. Mammary Gland Biol. Neoplasia 17, 65-77
12. Davalos, V., Moutinho, C., Villanueva, A., Boque, R., Silva, P., Carneiro, F., and Esteller, M. (2012) Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis. Oncogene 31, 2062-2074
13. Li, X., Roslan, S., Johnstone, C. N., Wright, J. A., Bracken, C. P., Anderson, M., Bert, A. G., Selth, L. A., Anderson, R. L., Goodall, G. J., Gregory, P. A., and Khew-Goodall, Y. (2013) MiR-200 can repress breast cancer metastasis through ZEB1-independent but moesin-dependent pathways. Oncogene 10.1038/onc. 2013.370
14. Yoshino, H., Enokida, H., Itesako, T., Tatarano, S., Kinoshita, T., Fuse, M., Kojima, S., Nakagawa, M., and Seki, N. (2013) Epithelial-mesenchymal transition-related microRNA-200s regulate molecular targets and pathways in renal cell carcinoma. J. Hum. Genet. 58, 508-516
15. Burridge, K., and Wennerberg, K. (2004) Rho and Rac take center stage. Cell 116, 167-179
16. Jaffe, A. B., and Hall, A. (2005) Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269
17. Disanza, A., Steffen, A., Hertzog, M., Frittoli, E., Rottner, K., and Scita, G. (2005) Actin polymerization machinery: the finish line of signaling networks, the starting point of cellular movement. Cell Mol. Life Sci. 62, 955-970
18. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science 279, 509-514
19. Ridley, A. J. (2001) Rho GTPases and cell migration. J. Cell Sci. 114, 2713-2722
20. Tapio, S., and Grosche, B. (2006) Arsenic in the aetiology of cancer. Mutat. Res. 612, 215-246
21. Wang, Z., Zhao, Y., Smith, E., Goodall, G. J., Drew, P. A., Brabletz, T., and Yang, C. (2011) Reversal and Prevention of Arsenic-Induced Human Bronchial Epithelial Cell Malignant Transformation by microRNA-200b. Toxicol. Sci. 121, 110-122
22. Jiang, R., Li, Y., Xu, Y., Zhou, Y., Pang, Y., Shen, L., Zhao, Y., Zhang, J., Zhou, J., Wang, X., and Liu, Q. (2013) EMT and CSC-like properties mediated by the IKKβ/IBα/RelA signal pathway via the transcriptional regulator, Snail, are involved in the arsenite-induced neoplastic transformation of human keratinocytes. Arch. Toxicol. 87, 991-1000
23. Xu, Y., Li, Y., Pang, Y., Ling, M., Shen, L., Yang, X., Zhang, J., Zhou, J., Wang, X., Liu, Q. (2012) EMT and stem cell-like properties associated with HIF-2α are involved in arsenite-induced transformation of human bronchial epithelial cells. PLoS One 7, e37765
24. Zhao, C. Q., Young, M. R., Diwan, B. A., Coogan, T. P., and Waalkes, M. P. (1997) Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc. Natl. Acad. Sci. U. S. A. 94, 10907-10912
25. Achanzar, W. E., Brambila, E. M., Diwan, B. A., Webber, M. M., and Waalkes, M. P. (2002) Inorganic arsenite-induced malignant transformation of human prostate epithelial cells. J. Natl. Cancer Inst. 94, 1888-1891
26. Wang, Z., Yang, J., Fisher, T., Xiao, H., Jiang, Y., and Yang, C. (2012) Akt activation is responsible for enhanced migratory and invasive behavior of arsenic-transformed human bronchial epithelial cells. Environ. Health Perspect. 120, 92-97
27. Wang, Z., Humphries, B., Xiao, H., Jiang, Y., and Yang, C. (2013) Epithelial to mesenchymal transition in arsenic-transformed cells promotes angiogenesis through activating β-catenin-vascular endothelial growth factor pathway. Toxicol. Appl. Pharmacol. 271, 20-29
28. Zhao, Y., Wang, Z., Jiang, Y., and Yang, C. (2011) Inactivation of Rac1 reduces Trastuzumab resistance in PTEN deficient and insulin-like growth factor I receptor overexpressing human breast cancer SKBR3 cells. Cancer Lett. 313, 54-63
29. Yang, C., Liu, Y., Leskow, F. C., Weaver, V. M., and Kazanietz, M. G. (2005) Rac-GAP-dependent inhibition of breast cancer cell proliferation by {β}2-chimerin. J. Biol. Chem. 280, 24363-24370
30. Yang, C., Liu, Y., Lemmon, M. A., and Kazanietz, M. G. (2006) Essential role for Rac in heregulin beta1 mitogenic signaling: a mechanism that involves epidermal growth factor receptor and is independent of ErbB4. Mol. Cell Biol. 26, 831-842
31. Luna-Ulloa, L. B., Hernández-Maqueda, J. G., Castañeda- Patlán, M. C., and Robles-Flores, M. (2011) Protein kinase C in Wnt signaling: implications in cancer initiation and progression. IUBMB Life. 63, 915-921
32. Sugimura, R., and Li, L. (2010) Noncanonical Wnt signaling in vertebrate development, stem cells, and diseases. Birth Defects Res. C Embryo. Today 90, 243-256
33. Freeley, M., Kelleher, D., and Long, A. (2011) Regulation of Protein Kinase C function by phosphorylation on conserved and non-conserved sites. Cell Signal. 23, 753-762
34. Parekh, D. B., Ziegler, W., and Parker, P. J. (2000) Multiple pathways control protein kinase C phosphorylation. EMBO J. 19, 496-503
35. Howe, E. N., Cochrane, D. R., and Richer, J. K. (2011) Targets of miR-200c mediate suppression of cell motility and anoikis resistance. Breast Cancer Res. 13, R45
36. Peng, F., Jiang, J., Yu, Y., Tian, R., Guo, X., Li, X., Shen, M., Xu, M., Zhu, F., Shi, C., Hu, J., Wang, M., and Qin, R. (2013) Direct targeting of SUZ12/ROCK2 by miR-200b/c inhibits cholangiocarcinoma tumourigenesis and metastasis. Br. J. Cancer 109, 3092-3104
37. Sossey-Alaoui, K., Bialkowska, K., and Plow, E. F. (2009) The miR200 family of microRNAs regulates WAVE3-dependent cancer cell invasion. J. Biol. Chem. 284, 33019-33029
38. Saitoh, T., and Katoh, M. (2001) Molecular cloning and characterization of human WNT5B on chromosome 12p13.3 region. Int. J. Oncol. 19, 347-351
39. Kikuchi, A., Yamamoto, H., Sato, A., and Matsumoto, S. (2012) Wnt5a: its signalling, functions and implication in diseases. Acta Physiol. 204, 17-33
40. Griner, E. M., and Kazanietz, M. G. (2007) Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer 7, 281-294
41. Jönsson, M, Smith, K., and Harris, A. L. (1998) Regulation of Wnt5a expression in human mammary cells by protein kinase C activity and the cytoskeleton. Br. J. Cancer 78, 430-438
42. Medrano, E. E. (2007) Wnt5a and PKC, a deadly partnership involved in melanoma invasion. Pigment Cell Res. 20, 258-259
43. Konopatskaya, O., and Poole, A. W. (2010) Protein kinase Calpha: disease regulator and therapeutic target. Trends Pharmacol. Sci. 31, 8-14
44. Urtreger, A. J., Kazanietz, M. G., and Bal de Kier Joffé, E. D. (2012) Contribution of individual PKC isoforms to breast cancer progression. IUBMB Life 64, 18-26
45. Mochly-Rosen, D., Das, K., and Grimes, K. V. (2012) Protein kinase C, an elusive therapeutic target? Nat. Rev. Drug Discov. 11, 937-957
46. Smith, K. R., Klei, L. R., and Barchowsky, A. (2001) Arsenite stimulates plasma membrane NADPH oxidase in vascular endothelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 280, L442-L449
47. Straub, A. C., Klei, L. R., Stolz, D. B., and Barchowsky, A. (2009) Arsenic requires sphingosine-1-phosphate type 1 receptors to induce angiogenic genes and endothelial cell remodeling. Am. J. Pathol. 174, 1949-1958
48. Waalkes, M. P., Liu, J., Germolec, D. R., Trempus, C. S., Cannon, R. E., Tokar, E. J., Tennant, R. W., Ward, J. M., and Diwan, B. A. (2008) Arsenic exposure in utero exacerbates skin cancer response in adulthood with contemporaneous distortion of tumor stem cell dynamics. Cancer Res. 68, 8278-8285
49. Mack, N. A., Whalley, H. J., Castillo-Lluva, S., and Malliri, A. (2011) The diverse roles of Rac signaling in tumorigenesis. Cell Cycle 10, 1571-1581