MicroRNA-200 is induced by thioredoxin-interacting protein and regulates Zeb1 protein signaling and beta cell

Journal of Biological Chemistry

Volumn 289, Issue 52, 2014, Pages 36275-36283

  Filios, Stephen R ^a   Xu, Guanlan ^a   Chen, Junqin ^a   Hong, Kyunghee ^a   Jing, Gu ^a   Shalev, Anath ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; PROTEINS; RNA;

BETA CELL FUNCTIONS; CELLULAR PROCESS; EPITHELIAL-MESENCHYMAL TRANSITION; KEY FACTORS; PANCREATIC BETA CELLS; PROTEIN SIGNALING; SIGNALING PATHWAYS; THIOREDOXINS;

CELL SIGNALING;

MICRORNA 200; THIOREDOXIN INTERACTING PROTEIN; TRANSCRIPTION FACTOR ZEB1; UVOMORULIN; CARRIER PROTEIN; FIZZY RELATED PROTEIN; HOMEODOMAIN PROTEIN; MICRORNA; MIRN200 MICRORNA, RAT; TCF8 PROTEIN, RAT; TRANSCRIPTION FACTOR; TXNIP PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME INHIBITION; ENZYME REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BINDING SITE; BIOSYNTHESIS; C3H MOUSE; C57BL MOUSE; CELL LINE; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RAT; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; BASE SEQUENCE; BINDING SITES; CARRIER PROTEINS; CDH1 PROTEINS; CELL LINE; DIABETES MELLITUS; HOMEODOMAIN PROTEINS; HUMANS; INSULIN-SECRETING CELLS; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; MOLECULAR SEQUENCE DATA; RATS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84919820315     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.592360     Document Type: Article

References (39)

1. Poitout, V., and Robertson, R. P. (2002) Minireview: secondary beta cell failure in type 2 diabetes-a convergence of glucotoxicity and lipotoxicity. Endocrinology 143, 339-342
2. Mathis, D., Vence, L., and Benoist, C. (2001) Beta cell death during progression to diabetes. Nature 414, 792-798
3. Shalev, A., Pise-Masison, C. A., Radonovich, M., Hoffmann, S. C., Hirshberg, B., Brady, J. N., and Harlan, D. M. (2002) Oligonucleotide microarray analysis of intact human pancreatic islets: identification of glucose-responsive genes and a highly regulated TGFβ signaling pathway. Endocrinology 143, 3695-3698
4. Minn, A. H., Hafele, C., and Shalev, A. (2005) Thioredoxin-interacting protein is stimulated by glucose through a carbohydrate response element and induces beta cell apoptosis. Endocrinology 146, 2397-2405
5. Chen, J., Saxena, G., Mungrue, I. N., Lusis, A. J., and Shalev, A. (2008) Thioredoxin-interacting protein: a critical link between glucose toxicity and beta cell apoptosis. Diabetes 57, 938-944
6. Chen, J., Fontes, G., Saxena, G., Poitout, V., and Shalev, A. (2010) Lack of TXNIP protects against mitochondria-mediated apoptosis but not against fatty acid-induced ER stress-mediated beta cell death. Diabetes 59, 440-447
7. Chen, J., Hui, S. T., Couto, F. M., Mungrue, I. N., Davis, D. B., Attie, A. D., Lusis, A. J., Davis, R. A., and Shalev, A. (2008) Thioredoxin-interacting protein deficiency induces Akt/Bcl-xL signaling and pancreatic beta cell mass and protects against diabetes. FASEB J. 22, 3581-3594
8. Xu, G., Chen, J., Jing, G., and Shalev, A. (2013) Thioredoxin-interacting protein regulates insulin transcription through microRNA-204. Nat. Med. 19, 1141-1146
9. Altuvia, Y., Landgraf, P., Lithwick, G., Elefant, N., Pfeffer, S., Aravin, A., Brownstein, M. J., Tuschl, T., and Margalit, H. (2005) Clustering and conservation patterns of human microRNAs. Nucleic Acids Res. 33, 2697-2706
10. Bracken, C. P., Gregory, P. A., Kolesnikoff, N., Bert, A. G., Wang, J., Shannon, M. F., and Goodall, G. J. (2008) A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelialmesenchymal transition. Cancer Res. 68, 7846-7854
11. 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
12. O'Day, E., and Lal, A. (2010) MicroRNAs and their target gene networks in breast cancer. Breast Cancer Res. 12, 201
13. Lim, Y. Y., Wright, J. A., Attema, J. L., Gregory, P. A., Bert, A. G., Smith, E., Thomas, D., Lopez, A. F., Drew, P. A., Khew-Goodall, Y., and Goodall, G. J. (2013) Epigenetic modulation of the miR-200 family is associated with transition to a breast cancer stem-cell-like state. J. Cell Sci. 126, 2256-2266
14. Schliekelman, M. J., Gibbons, D. L., Faca, V. M., Creighton, C. J., Rizvi, Z. H., Zhang, Q., Wong, C. H., Wang, H., Ungewiss, C., Ahn, Y. H., Shin, D. H., Kurie, J. M., and Hanash, S. M. (2011) Targets of the tumor suppressor miR-200 in regulation of the epithelial-mesenchymal transition in cancer. Cancer Res. 71, 7670-7682
15. Iliopoulos, D., Lindahl-Allen, M., Polytarchou, C., Hirsch, H. A., Tsichlis, P. N., and Struhl, K. (2010) Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol. Cell 39, 761-772
16. Uhlmann, S., Zhang, J. D., Schwäger, A., Mannsperger, H., Riazalhosseini, Y., Burmester, S., Ward, A., Korf, U., Wiemann, S., and Sahin, O. (2010) miR-200bc/429 cluster targets PLCγ1 and differentially regulates proliferation and EGF-driven invasion than miR-200a/141 in breast cancer. Oncogene 29, 4297-4306
17. Schickel, R., Park, S. M., Murmann, A. E., and Peter, M. E. (2010) miR-200c regulates induction of apoptosis through CD95 by targeting FAP-1. Mol. Cell 38, 908-915
18. Magenta, A., Cencioni, C., Fasanaro, P., Zaccagnini, G., Greco, S., Sarra-Ferraris, G., Antonini, A., Martelli, F., and Capogrossi, M. C. (2011) miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ. 18, 1628-1639
19. Yang, J., and Weinberg, R. A. (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829
20. Wiklund, E. D., Bramsen, J. B., Hulf, T., Dyrskjøt, L., Ramanathan, R., Hansen, T. B., Villadsen, S. B., Gao, S., Ostenfeld, M. S., Borre, M., Peter, M. E., Ørntoft, T. F., Kjems, J., and Clark, S. J. (2011) Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int. J. Cancer 128, 1327-1334
21. Wiklund, E. D., Gao, S., Hulf, T., Sibbritt, T., Nair, S., Costea, D. E., Villadsen, S. B., Bakholdt, V., Bramsen, J. B., Sørensen, J. A., Krogdahl, A., Clark, S. J., and Kjems, J. (2011) MicroRNA alterations and associated aberrant DNA methylation patterns across multiple sample types in oral squamous cell carcinoma. PLoS ONE 6, e27840
22. Braun, J., Hoang-Vu, C., Dralle, H., and Hüttelmaier, S. (2010) Downregulation of microRNAs directs the EMT and invasive potential of anaplastic thyroid carcinomas. Oncogene 29, 4237-4244
23. Kulkarni, R. N., Jhala, U. S., Winnay, J. N., Krajewski, S., Montminy, M., and Kahn, C. R. (2004) PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J. Clin. Invest. 114, 828-836
24. Russ, H. A., Ravassard, P., Kerr-Conte, J., Pattou, F., and Efrat, S. (2009) Epithelial-mesenchymal transition in cells expanded in vitro from lineagetraced adult human pancreatic beta cells. PLoS ONE 4, e6417
25. Russ, H. A., Sintov, E., Anker-Kitai, L., Friedman, O., Lenz, A., Toren, G., Farhy, C., Pasmanik-Chor, M., Oron-Karni, V., Ravassard, P., and Efrat, S. (2011) Insulin-producing cells generated from dedifferentiated human pancreatic beta cells expanded in vitro. PLoS ONE 6, e25566
26. Joglekar, M. V., and Hardikar, A. A. (2010) Epithelial-to-mesenchymal transition in pancreatic islet beta cells. Cell Cycle 9, 4077-4079
27. Poy, M. N., Hausser, J., Trajkovski, M., Braun, M., Collins, S., Rorsman, P., Zavolan, M., and Stoffel, M. (2009) miR-375 maintains normal pancreatic alpha and beta cell mass. Proc. Natl. Acad. Sci. U.S.A. 106, 5813-5818
28. Poy, M. N., Eliasson, L., Krutzfeldt, J., Kuwajima, S., Ma, X., Macdonald, P. E., Pfeffer, S., Tuschl, T., Rajewsky, N., Rorsman, P., and Stoffel, M. (2004) A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432, 226-230
29. Tang, H., Kong, Y., Guo, J., Tang, Y., Xie, X., Yang, L., Su, Q., and Xie, X. (2013) Diallyl disulfide suppresses proliferation and induces apoptosis in human gastric cancer through Wnt-1 signaling pathway by up-regulation of miR-200b and miR-22. Cancer Lett. 340, 72-81
30. Adam, L., Zhong, M., Choi, W., Qi, W., Nicoloso, M., Arora, A., Calin, G., Wang, H., Siefker-Radtke, A., McConkey, D., Bar-Eli, M., and Dinney, C. (2009) 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
31. 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
32. 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
33. Williams, L. V., Veliceasa, D., Vinokour, E., and Volpert, O. V. (2013) miR-200b inhibits prostate cancer EMT, growth and metastasis. PLoS ONE 8, e83991
34. 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
35. Brabletz, S., and Brabletz, T. (2010) The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer? EMBO Rep. 11, 670-677
36. Hay, E. D. (1995) An overview of epithelio-mesenchymal transformation. Acta Anat. 154, 8-20
37. Saxena, G., Chen, J., and Shalev, A. (2010) Intracellular shuttling and mitochondrial function of thioredoxin-interacting protein. J. Biol. Chem. 285, 3997-4005
38. Gershengorn, M. C., Hardikar, A. A., Wei, C., Geras-Raaka, E., Marcus-Samuels, B., and Raaka, B. M. (2004) Epithelial-to-mesenchymal transition generates proliferative human islet precursor cells. Science 306, 2261-2264
39. Atouf, F., Park, C. H., Pechhold, K., Ta, M., Choi, Y., and Lumelsky, N. L. (2007) No evidence for mouse pancreatic beta cell epithelial-mesenchymal transition in vitro. Diabetes 56, 699-702