Differential role of snail1 and snail2 zinc fingers in E-cadherin repression and epithelial to mesenchymal transition

Journal of Biological Chemistry

Volumn 289, Issue 2, 2014, Pages 930-941

  Villarejo, Ana ^a   Cortés Cabrera, Álvaro ^b   Molina Ortíz, Patricia ^a,c   Portillo, Francisco ^a   Cano, Amparo ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^c UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

E-CADHERINS; EPITHELIAL TO MESENCHYMAL TRANSITIONS; TRANSCRIPTIONAL REPRESSORS; ZINC FINGER;

BIOACTIVITY; MOLLUSCS; ZINC;

ANIMALS;

DNA; NUCLEIC ACID BINDING PROTEIN; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; UVOMORULIN; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN 1; ZINC FINGER PROTEIN 2; ZINC FINGER PROTEIN 3; ZINC FINGER PROTEIN 4;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; E BOX ELEMENT; E CADHERIN GENE; EPITHELIAL MESENCHYMAL TRANSITION; GENE LOCATION; GENE REPRESSION; HUMAN; HUMAN CELL; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DNA INTERACTION; PROTEIN FUNCTION;

DNA-BINDING PROTEIN; E-CADHERIN; EMT; REPRESSOR PROTEIN; ZINC FINGER;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CADHERINS; CELL LINE; DNA; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MICE; MICROSCOPY, CONFOCAL; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS; ZINC FINGERS;

EID: 84891956580     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.528026     Document Type: Article

References (49)

1. Nieto, M. A. (2002) The Snail superfamily of zinc finger transcription factors. Nat. Rev. Mol. Cell Biol. 3, 155-166
2. Barrallo-Gimeno, A., and Nieto M. A. (2009) Evolutionary history of the Snail/Scratch superfamily. Trends Genet. 25, 248-252
3. Grimes, H. L., Chan, T. O., Zweidler-McKay, P. A., Tong, B., and Tsichlis, P. N. (1996) The Gfi-1 proto-oncoprotein contains a novel transcriptional repressor domain, SNAG, and inhibits G1 arrest induced by interleukin-2 withdrawal. Mol. Cell Biol. 16, 6263-6272
4. Hemavathy, K., Ashraf, S. I., and Ip, Y. T. (2000) Snail/slug family of repressors: slowly going into the first lane of development and cancer. Gene. 257, 1-12
5. Batlle, E., Sancho, E., Francí, C., Domínguez, D., Monfar, M., Baulida, J., and García De Herreros, A. (2000) The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89
6. Peinado, H., Ballestar, E., Esteller, M., and Cano, A. (2004) Snail mediates E-cadherin repression by the recruitment of the Sin3A/Histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol. Cell Biol. 24, 306-319
7. Molina-Ortiz, P., Villarejo, A., MacPherson, M., Santos, V., Montes, A., Souchelnytskyi, S., Portillo, F., and Cano, A. (2012) Characterization of the SNAG and SLUG domains of Snail2 in the repression of E-cadherin and EMT induction. Modulation by serine 4 phosphorylation. PLoS ONE 7, e36132
8. Sefton, M., Sánchez, S., and Nieto, M. A. (1998) Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development. 125, 3111-3121
9. Domínguez, D., Montserrat-Sentís, B., Virgós-Soler, A., Guaita, S., Grueso, J., Porta, M., Puig, I., Baulida, J., Francí, C., and García de Herreros, A. (2003) Phosphorylation regulates the subcellular localization and activity of the snail transcriptional repressor. Mol. Cell Biol. 23, 5078-5089
10. Zhou, B. P., Deng, J., Xia, W., Xu, J., Li, Y. M., Gunduz, M., and Hung, M. C. (2004) Dual regulation of Snail by GSK-3-mediated phosphorylation in control of epithelial mesenchymal transition. Nat. Cell Biol. 6, 931-940
11. Peinado, H., Portillo, F., and Cano, A. (2005) Switching on-off Snail: LOXL2 versus GSK3-. Cell Cycle 12, 1749-1752
12. MacPherson, M. R., Molina, P., Souchelnytskyi, S., Wernstedt, C., Martin-Pérez, J., Portillo, F., and Cano, A. (2010) Phosphorylation of serine 11 and 92 as new positive regulators of human Snail1 function: potential involvement of csaein kinase-2 amd the c-AMP-activated kinase protein kinase A. Mol. Biol. Cell 21, 244-253
13. Mingot, J. M., Vega, S., Maestro, B., Sanz, J. M., and Nieto, M. A. (2009) Characterization of Snail nuclear import pathways as representatives of C2H2 zinc finger transcription factors. J. Cell Sci. 122, 1452-1460
14. Yamasaki, H., Sekimoto, T., Ohkubo, T., Douchi, T., Nagata, Y., Ozawa, M., and Yoneda, Y. (2005) Zinc finger domain of Snail functions as a nuclear localization signal for importin beta-mediated nuclear import pathway. Genes Cells. 10, 455-464
15. Miller, J., McLachlan, A. D., and Klug, A. (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 4, 1609-1614
16. Pabo, C., Peisach, E., and Grant, R. A. (2001) Design and selection of novel Cys2His2 zinc finger proteins. Annu. Rev. Biochem. 70, 313-340
17. Krishna, S., Majumdar, I., and Grishin, N. (2003) Structural classification of zinc fingers. Nucleic Acids Res. 31, 532-550
18. Pavletich, N. P., and Pabo, C. O. (1993) Crystal structure of a five finger GLI-DNA complex: new perspectives on zinc fingers. Science. 261, 1701-1707
19. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C., Yang, J., and Weinberg, R. A. (2008) The epithelial mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715
20. Nieto, M. A. (2011) The Ins and Outs of the Epithelial to Mesenchymal Transition in health and disease. Annu. Rev. Gen. Dev. Biol. 27, 347-376
21. Thiery, J. P., Acloque, H., Huang, R., and Nieto, M. A. (2009) Epitelialmesenchymal transitions in development and disease. Cell 139, 871-890
22. Moreno-Bueno, G., Portillo, F., and Cano, A. (2008) Transcriptional regulation of cell polarity in EMT and cancer. Oncogene. 27, 6958-6969
23. Nieto, M. A., and Cano, A. (2012) The epitelial-mesenchymal transition under control: global programs to regulate epithelial plasticity. Sem. Cancer Biol. 22, 361-368
24. Kalluri, R., and Weinberg, R. A. (2009) The basics of epitelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428
25. Cano, A., Pérez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F., and Nieto, M. A. (2000) The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83
26. Hajra, K. M., Chen, D. Y., and Fearon, E. R. (2002) The SLUG zinc finger protein represses E-cadherin in breast cancer. Cancer Res. 62, 1613-1618
27. Bolós, V., Peinado, H., Pérez-Moreno, M. A., Fraga, M. F., Esteller, M., and Cano, A. (2003) The transcription factor Slug represses E-cadherin and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J. Cell Sci. 116, 499-511
28. Peinado, H., Portillo, F., and Cano, A. (2004) Transcriptional regulation of cadherins during development and carcinogenesis. Int. J. Dev. Biol. 48, 365-375
29. Peinado, H., Olmeda, D., and Cano, A. (2007) Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer. 7, 415-428
30. Stanisavljevic, J., Porta-de-la-Riva, M., Batlle, R., de Herreros, A. G., and Baulida, J. (2011) The p65 subunit of NF-B and PARP1 assist Snail1 in activating fibronectin transcription. J. Cell Sci. 124, 4161-4171
31. Moreno-Bueno, G., Cubillo, E., Sarrió, D., Peinado, H., Rodríguez-Pinilla, S. M., Villa, S., Bolós, V., Jordá, M., Fabra, A., Portillo, F., Palacios, J., and Cano, A. (2006) Genetic profiling of epitelial cells expressing E-cadherin repressors reveals a distinct role for Snail, Slug, and E47 factors in epitelial mesenchymal transition. Cancer Res. 66, 9543-9556
32. del Barrio, M. G., and Nieto, M. A. (2002) Overexpression of Snail family members highlights their ability to promote chick neural crest formation. Development. 129, 1583-1593
33. Murray, S. A., and Gridley, T. (2006) Snail family genes are required for left-right asymmetry determination, but not neural crest formation, in mice. Proc. Natl. Acad. Sci. U.S.A. 103, 10300-10304
34. Martínez Álvarez, C., Blanco, M., Pérez, R., Rabadan, M., Aparicio, M., Resel, E., Martínez, T., and Nieto, M. A. (2004) Snail family members and cell survival in physiological and pathological cleft palates. Dev. Biol. 262, 207-218
35. Carver, E. A., Jiang, R., Lan, Y., Oram, K. F., and Gridley, T. (2001) The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol. Cell Biol. 21, 8184-8188
36. Jiang, R., Lan, Y., Norton, C. R., Sundberg, J. P., and Gridley, T. (1998) The Slug gene is not essential for mesoderm or neural crest development in mice. Dev. Biol. 198, 277-285
37. Olmeda, D., Moreno-Bueno, G., Flores, J. M., Fabra, A., Portillo, F., and Cano, A. (2007) Snail is required for tumor growth and lymph node metastasis of human breast carcinoma. Cancer Res. 67, 11721-11731
38. Olmeda, D., Montes, A., Moreno-Bueno, G., Flores, J. M., Portillo, F., and Cano, A. (2008) Snai1 and Snai2 collaborate on tumor growth and metastasis properties of mouse skin carcinoma cell lines. Oncogene. 27, 4690-4701
39. Zheng, L., Baumann, U., and Reymond, J. L. (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32, e115
40. Martínez-Estrada, O. M., Cullerés, A., Soriano, F. X., Peinado, H., Bolós, V., Martínez, F. O., Reina, M., Cano, A., Fabre, M., and Vilaró, S. (2006) The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem. J. 394, 449-457
41. Moreno-Bueno, G., Peinado, H., Molina, P., Olmeda, D., Cubillo, E., Santos, V., Palacios, J., Portillo, F., and Cano, A. (2009) The morphological and molecular features of the epithelial-to-mesenchymal transition. Nat. Protoc. 4, 1591-1613
42. Wolfe, S., Nekludova, L., and Pabo, C. O. (2000) DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 3, 183-212
43. Segal, D. J., Crotty, J. W., Bhakta, M. S., Barbas, C. F., 3rd, and Horton, N. C. (2006) Structure of Aart, a Designed Six-finger Zinc Finger Peptide Bound to DNA. J. Mol. Biol. 363, 405-421
44. Hemavathy, K., Guru, S. C., Harris, J., Chen, J. D., Ip, Y. T. (2000) Human slug is a repressor that localizes to sites of active transcription. Mol. Cell Biol. 20, 5087-5095
45. Manzanares, M., Locascio, A., and Nieto, M. A. (2001) The increasing complexity of the Snail gene superfamily in metazoan evolution. Trends Genet. 17, 178-181
46. Viñas-Castells, R., Beltran, M., Valls, G., Gómez, I., García, J. M., Montserrat-Sentís, B., Baulida, J., Bonilla, F., de Herreros, A. G., and Díaz, V. M. (2010) The hypoxia controlled FBX114 ubiquitin ligase targets SNAI1 for proteasome degradation. J. Biol. Chem. 285, 3794-3805
47. Elloul, S., Silins, I., Tropé, C. G., Benshushan, A., Davidson, B., and Reich, R. (2006) Expression of E-cadherin transcriptional regulators in ovarian carcinoma. Virchows Arch. 449, 520-528
48. Côme, C., Magnino, F., Bibeau, F., De Santa Barbara, P., Becker, K. F., Theillet, C., and Savagner, P. (2006) Snail and Slug play distinct roles during breast carcinoma progression. Clin. Cancer Res. 12, 5395-5402
49. Castro Alves, C., Rosivatz, E., Schott, C., Hollweck, R., Becker, I., Sarbia, M., Carneiro, F., and Becker, K. F. (2007) Slug is overexpressed in gastric carcinomas and may act synergistically with SIP1 and Snail in the downregulation of E-cadherin. J. Pathol. 211, 507-515