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

Volumn 7, Issue 5, 2012, Pages

  Molina Ortiz, Patricia ^a,c   Villarejo, Ana ^a   MacPherson, Matthew ^a,d   Santos, Vanesa ^a   Montes, Amalia ^a   Souchelnytskyi, Serhiy ^b   Portillo, Francisco ^a   Cano, Amparo ^a  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR RECEPTOR COREPRESSOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAG; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; SERINE; SNAIL FAMILY TRANSCRIPTION FACTORS;

AMINO ACID COMPOSITION; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE FUNCTION; GENE INDUCTION; GENE INTERACTION; GENE REPRESSION; GENE STRUCTURE; HUMAN; HUMAN CELL; IN VIVO STUDY; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; DOG; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOPRECIPITATION; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; WESTERN BLOTTING;

GASTROPODA;

ANIMALS; BLOTTING, WESTERN; CADHERINS; CELL LINE; DOGS; EPITHELIAL-MESENCHYMAL TRANSITION; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOPRECIPITATION; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SERINE; TRANSCRIPTION FACTORS;

EID: 84860465552     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036132     Document Type: Article

References (54)

1. Nieto MA, (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3: 155-166.
2. Barrallo-Gimeno A, Nieto MA, (2005) The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132: 3151-3161.
3. Peinado H, Olmeda D, Cano A, (2007) Snail, ZEB, and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7: 415-428.
4. Cobaleda C, Pérez-Caro M, Vicente-Dueñas C, Sánchez-García I, (2007) Function of the zinc-finger transcription factor SNAI2 in cancer and development. Annu Rev Genet 41: 41-61.
5. Manzanares M, Locascio A, Nieto MA, (2001) The increasing complexity of the Snail gene superfamily in metazoan evolution. Trends Genet 17: 78-81.
6. Grimes HL, Chan TO, Zweidler-McKay PA, Tong B, Tsichlis PN, (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.
7. Nakayama H, Scott IC, Cross JC, (1998) The transition to endoreduplication in trophoblast giant cells is regulated by the mSNA zinc finger transcription factor. Dev Biol 199: 150-163.
8. Hemavathy K, Guru SC, Harris, Chen JD, Ip YT, (2000) Human Slug is a repressor that localizes to sites of active transcription. Mol Cell Biol 20: 5087-5095.
9. Mingot JM, Vega S, Maestro B, Sanz JM, Nieto MA, (2009) Characterization of Snail nuclear import pathways as representatives of C2H2 zinc finger transcription factors. J Cell Sci 122: 1452-1460.
10. Domínguez D, Montserrat-Sentís B, Virgós-Soler A, Guaita S, Grueso J, et al. (2003) Phosphorylation regulates the subcellular location and activity of the snail transcriptional repressor. Mol Cell Biol 3: 5078-5089.
11. Zhou BP, Deng J, Xia W, Xu J, Li YM, et al. (2004) Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6: 931-840.
12. Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, et al. (2000) The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2: 76-83.
13. Batlle E, Sancho E, Francí C, Domínguez D, Monfar M, et al. (2000) The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2: 84-89.
14. Hajra KM, Chen DY, Fearon ER, (2002) The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 62: 1613-1618.
15. Bolós V, Peinado H, Pérez-Moreno MA, Fraga MF, Esteller M, et al. (2003) The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 116: 499-511.
16. del Barrio MG, Nieto MA, (2002) Overexpression of Snail family members highlights their ability to promote chick neural crest formation. Development 129: 1583-1593.
17. Martínez-Estrada OM, Cullerés A, Soriano FX, Peinado H, Bolós V, et al. (2006) The transcription factors Slug and Snail act as repressors of Claudin-expression in epithelial cells. Biochem J 394: 449-457.
18. Martin TA, Goyal A, Watkins G, Jiang WG, (2005) Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann Surg Oncol 12: 488-496.
19. Côme C, Magnino F, Bibeau F, De Santa Barbara P, Becker KF, et al. (2006) Snail and slug play distinct roles during breast carcinoma progression. Clin Cancer Res 12: 5395-5402.
20. Moreno-Bueno G, Cubillo E, Sarrio D, Peinado H, Rodriguez-Pinilla SM, et al. (2006) Genetic profiling of epithelial cells expressing E- cadherin repressors reveals a distinct role for Snail, Slug, and E47 factors in epithelial mesenchymal transition. Cancer Res 66: 9543-9556.
21. Olmeda D, Montes A, Moreno-Bueno G, Flores JM, Portillo F, et al. (2008) Snai1 and Snai2 collaborate on tumor growth and metastasis properties of mouse skin carcinoma cell lines. Oncogene 27: 4690-4701.
22. Carver EA, Jiang R, Lan Y, Oram KF, Gridley T, (2001) The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 21: 8184-8188.
23. Jiang R, Lan Y, Norton CR, Sundberg JP, Gridley T, (1998) The Slug gene is not essential for mesoderm or neural crest development in mice. Dev Biol 198: 277-285.
24. Aybar MJ, Nieto MA, Mayor R, (2003) Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development 130: 483-494.
25. Sefton M, Sánchez S, Nieto MA, (1998) Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 125: 3111-3121.
26. Vernon AE, Labonne C, (2006) Slug stability is dynamically regulated during neural crest development by the F-box protein Ppa. Development 133: 3359-3370.
27. Peinado H, Ballestar E, Esteller M, Cano A, (2004) Snai1 mediates E-cadherin repression by recruitment of the Sin3A/histone deacetylase 1 (HDAC 1)/HDAC2 complex. Mol Cell Biol 24: 306-319.
28. Herranz N, Paisini D, Diaz VM, Franci C, Gutierrez A, et al. (2008) Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor. Mol Cell Biol 28: 4772-4781.
29. Langer EM, Feng Y, Zhaoyuan H, Rauscher FJ 3rd, Kroll KL, et al. (2008) Ajuba LIM proteins are snail/slug corepressors required for neural crest development in Xenopus. Dev Cell 14: 424-436.
30. Hou Z, Peng H, Ayyanathan K, Yan KP, Langer EM, et al. (2008) The LIM protein AJUBA recruits protein arginine methyltransferase 5 to mediate SNAIL-dependent transcriptional repression. Mol Cell Biol 28: 3198-3207.
31. Lin Y, Wu Y, Li J, Dong C, Ye X, et al. (2010) The SNAG domain of Snail1 functions as a molecular hook for recruiting lysine-specific demethylase 1. EMBO J 29: 1803-1816.
32. Lin T, Ponn A, Hu X, Law BK, Lu J, (2010) Requirement of histone demethylase LSD1 in Snail1-mediated transcriptional repression during epitelial-mesenchymal transition. Oncogene 29: 4896-4904.
33. Nibu Y, Zhang H, Bajor E, Barolo S, Small S, et al. (1998) dCtBP mediates transcriptional repression by Knirps, Kruppel and Snail in the Drosophila embryo. EMBO J 17: 7009-7020.
34. Qi D, Bergman M, Aihara H, Nibu Y, Mannervik M, (2008) Drosophila Ebi mediates Snail-dependent transcriptional repression through HDAC3-induced histone deacetylation. EMBO J 27: 898-909.
35. Ayyanathan K, Peng H, Hou Z, Fredericks WJ, Goyal RK, et al. (2007) The Ajuba LIM domain protein is a corepressor for SNAG domain mediated repression and participates in nucleocytoplasmic shuttling. Cancer Res 67: 9097-9106.
36. Mittal MK, Myers JN, Misra S, Bailey CK, Chaudhuri G, (2008) In vivo binding to and functional repression of the VDR gene promoter by SLUG in human breast cells. Biochem Biophys Res Commun 372: 30-34.
37. Mittal MK, Singh K, Misra S, Chaudhuri G, (2011) SLUG-induced elevation of D1 cyclin in breast cancer cells through inhibition of its ubiquitination. J Biol Chem 286: 469-474.
38. Tripathi MK, Misra S, Khedkar SV, Hamilton N, Irvin-Wilson C, et al. (2005) Regulation of BRCA2 gene expression by the SLUG repressor protein in human breast cells. J Biol Chem 280: 17163-17171.
39. Yang Z, Rayala S, Nguyen D, Vadlamudi RK, Chen S, et al. (2005) Pak1 phosphorylation of snail, a master regulator of epithelial-to-mesenchyme transition, modulates snail's subcellular localization and functions. Cancer Res 65: 3179-3184.
40. Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ, (2005) Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem 280: 11740-11748.
41. MacPherson MR, Molina P, Souchelnytskyi S, Wernstedt C, Martin-Pérez J, et al. (2010) Phosphorylation of serine 11 and serine 92 as new positive regulators of human Snail1 function: potential involvement of casein kinase-2 and the cAMP-activated kinase protein kinase A. Mol Biol Cell 21: 244-253.
42. Du C, Zhang C, Hassan S, Biswas MH, Balaji KC, (2010) Protein kinase D1 suppresses epithelial-to-mesenchymal transition through phosphorylation of Snail. Cancer Res 70: 7810-7819.
43. Zhang K, Rodriguez-Aznar E, Yabuta N, Owen RJ, Mingot JM, et al. (2011) Lats kinase potentiates Snail1 activity by promoting nuclear retention upon phosphorylation. EMBO J 31: 29-43.
44. Wang SP, Wang WL, Chang YL, Wu CT, Chao YC, et al. (2009) p53 controls cancer cell invasion by inducing the MDM2-mediated degradation of Slug. Nat Cell Biol 11: 694-704.
45. Moreno-Bueno G, Peinado H, Molina P, Olmeda D, Cubillo E, et al. (2009) The morphological and molecular features of the epithelial-to-mesenchymal transition. Nat Protoc 4: 1591-1613.
46. Thiery JP, Acloque H, Huang RY, Nieto MA, (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
47. Nieto MA, (2011) The ins and outs of the epitelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 10: 347-376.
48. Grooteclaes ML, Frisch SM, (2000) Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene 19: 3823-3828.
49. Bailey CK, Misra S, Mittal MK, Chaudhuri G, (2007) Human SLUG does not directly bind to CtBP1. Biochem Biophys Res Commun 353: 661-664.
50. Peinado H, Portillo F, Cano A, (2004) Transcriptional regulation of cadherins during development and carcinogenesis. Int J Dev Biol 48: 365-375.
51. Viñas-Castells R, Beltran M, Valls G, Gómez I, García JM, et al. (2010) The hypoxia-controlled FBXL14 ubiquitin ligase targets SNAIL1 for proteasome degradation. J Biol Chem 285: 3794-3805.
52. Peinado H, Iglesias-de la Cruz MC, Olmeda D, Csiszar K, Fong KS, et al. (2005) A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. EMBO J 24: 3446-3458.
53. Lander R, Nordin K, Labonne C, (2011) The F-box protein Ppa is a common regulator of core EMT factors Twist, Snail, Slug and Sip1. J Cell Biol 194: 17-25.
54. Zheng L, Baumann U, Reymond JL, (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acid Res 2: e115.