Snail family members unequally trigger EMT and thereby differ in their ability to promote the neoplastic transformation of mammary epithelial cells

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Gras, Baptiste ^a,b,c,d   Jacqueroud, Laurent ^a,b,c,d   Wierinckx, Anne ^a,b,c,d,e   Lamblot, Christelle ^a,b,c,d   Fauvet, Frederique ^a,b,c,d   Lachuer, Joël ^a,b,c,d,e   Puisieux, Alain ^a,b,c,d,e,f   Ansieau, Stephane ^a,b,c,d  

^a CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^b LabEx DEVweCAN   (France)

^c UNIVERSITÉ DE LYON   (France)

^d CENTRE LÉON BÉRARD   (France)

^e ProfileXpert   (France)

^f INSTITUT UNIVERSITAIRE DE FRANCE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SNAIL1; PROTEIN SNAIL2; PROTEIN SNAIL3; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG;

ANOIKIS; ARTICLE; BREAST EPITHELIUM; CANCER CELL; CARCINOGENICITY; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALIGNANT TRANSFORMATION; NUCLEOTIDE SEQUENCE;

BREAST NEOPLASMS; CELL ADHESION; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAMMARY GLANDS, HUMAN; RNA, MESSENGER; TELOMERASE; TRANSCRIPTION FACTORS;

EID: 84898605112     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092254     Document Type: Article

References (52)

1. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939 (Pubitemid 38798858)
2. Thiery J.P., Acloque H., Huang Y., Epithelial-mesenchymal transitions in development and disease, Cell, 139, 871-890
3. Maestro R, Dei Tos AP, Hamamori Y, Krasnokutsky S, Sartorelli V, et al. (1999) Twist is a potential oncogene that inhibits apoptosis. Genes Dev 13: 2207-2217 (Pubitemid 29426726)
4. Valsesia-Wittmann S, Magdeleine M, Dupasquier S, Garin E, Jallas AC, et al. (2004) Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells. Cancer Cell 6: 625-630 (Pubitemid 40017705)
5. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, et al. (2008) Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 14: 79-89 (Pubitemid 351890463)
6. Ohashi S, Natsuizaka M, Wong GS, Michaylira CZ, Grugan KD, et al. (2010) Epidermal growth factor receptor and mutant p53 expand an esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors. Cancer Res 70: 4174-4184
7. Morel AP, Hinkal GW, Thomas C, Fauvet F, Courtois-Cox S, et al. (2012) EMT inducers catalyze malignant transformation of mammary epithelial cells and drive tumorigenesis towards claudin-low tumors in transgenic mice. PLoS Genet 8: e1002723
8. Alberga A, Boulay JL, Kempe E, Dennefeld C, Haenlin M (1991) The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers. Development 111: 983-992 (Pubitemid 21900253)
9. Nieto MA, Bennett MF, Sargent MG, Wilkinson DG (1992) Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene. Development 116: 227-237
10. Smith DE, Franco del AF, Gridley T (1992) Isolation of Sna, a mouse gene homologous to the Drosophila genes snail and escargot: its expression pattern suggests multiple roles during postimplantation development. Development 116: 1033-1039 (Pubitemid 23042443)
11. Hammerschmidt M, Nusslein-Volhard C (1993) The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation. Development 119: 1107-1118 (Pubitemid 23358580)
12. Nieto MA, Sargent MG, Wilkinson DG, Cooke J (1994) Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264: 835-839 (Pubitemid 24193449)
13. Langeland JA, Tomsa JM, Jackman WR, Jr., Kimmel CB (1998) An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo. Dev Genes Evol 208: 569-577 (Pubitemid 28542700)
14. Wada S, Saiga H (1999) Cloning and embryonic expression of Hrsna, a snail family gene of the ascidian Halocynthia roretzi: implication in the origins of mechanisms for mesoderm specification and body axis formation in chordates. Dev Growth Differ 41: 9-18 (Pubitemid 29088841)
15. Mayor R, Guerrero N, Young RM, Gomez-Skarmeta JL, Cuellar C (2000) A novel function for the Xslug gene: control of dorsal mesendoderm development by repressing BMP-4. Mech Dev 97: 47-56
16. 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 (Pubitemid 33051806)
17. Cano A, Perez-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
18. Batlle E, Sancho E, Franci C, Dominguez 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
19. Bolos V, Peinado H, Perez-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 (Pubitemid 36231290)
20. Shih JY, Tsai MF, Chang TH, Chang YL, Yuan A, et al. (2005) Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma. Clin Cancer Res 11: 8070-8078 (Pubitemid 41698750)
21. Shin NR, Jeong EH, Choi CI, Moon HJ, Kwon CH, et al. (2012) Overexpression of Snail is associated with lymph node metastasis and poor prognosis in patients with gastric cancer. BMC Cancer 12: 521
22. Kobayashi M, Huang CL, Sonobe M, Kikuchi R, Ishikawa M, et al. (2013) Snail expression is associated with a poor prognosis in malignant pleural mesotheliomas. Ann Thorac Surg 95: 1181-1188
23. Natsugoe S, Uchikado Y, Okumura H, Matsumoto M, Setoyama T, et al. (2007) Snail plays a key role in E-cadherin-preserved esophageal squamous cell carcinoma. Oncol Rep 17: 517-523
24. Cates JM, Byrd RH, Fohn LE, Tatsas AD, Washington MK, et al. (2009) Epithelial-mesenchymal transition markers in pancreatic ductal adenocarcinoma. Pancreas 38: e1-e6
25. Kataoka H, Murayama T, Yokode M, Mori S, Sano H, et al. (2000) A novel snail-related transcription factor Smuc regulates basic helix-loop-helix transcription factor activities via specific E-box motifs. Nucleic Acids Res 28: 626-633 (Pubitemid 30058005)
26. Katoh M, Katoh M (2003) Identification and characterization of human SNAIL3 (SNAI3) gene in silico. Int J Mol Med 11: 383-388
27. Zhuge X, Kataoka H, Tanaka M, Murayama T, Kawamoto T, et al. (2005) Expression of the novel Snai-related zinc-finger transcription factor gene Smuc during mouse development. Int J Mol Med 15: 945-948
28. Bradley CK, Norton CR, Chen Y, Han X, Booth CJ, et al. (2013) The snail family gene snai3 is not essential for embryogenesis in mice. PLoS ONE 8: e65344
29. Dahlem T, Cho S, Spangrude GJ, Weis JJ, Weis JH (2012) Overexpression of Snai3 suppresses lymphoid- and enhances myeloid-cell differentiation. Eur J Immunol 42: 1038-1043
30. Pioli PD, Dahlem TJ, Weis JJ, Weis JH (2013) Deletion of Snai2 and Snai3 results in impaired physical development compounded by lymphocyte deficiency. PLoS ONE 8: e69216
31. 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 (Pubitemid 28304444)
32. Come C, Arnoux V, Bibeau F, Savagner P (2004) Roles of the transcription factors snail and slug during mammary morphogenesis and breast carcinoma progression. J Mammary Gland Biol Neoplasia 9: 183-193 (Pubitemid 39177502)
33. Uchikado Y, Natsugoe S, Okumura H, Setoyama T, Matsumoto M, et al. (2005) Slug Expression in the E-cadherin preserved tumors is related to prognosis in patients with esophageal squamous cell carcinoma. Clin Cancer Res 11: 1174-1180 (Pubitemid 40175768)
34. 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 (Pubitemid 46809165)
35. Ansieau S, Hinkal G, Thomas C, Bastid J, Puisieux A (2008) Early origin of cancer metastases: dissemination and evolution of premalignant cells. Cell Cycle 7: 3659-3663
36. Cheng CW, Wu PE, Yu JC, Huang CS, Yue CT, et al. (2001) Mechanisms of inactivation of E-cadherin in breast carcinoma: modification of the two-hit hypothesis of tumor suppressor gene. Oncogene 20: 3814-3823
37. Blanco MJ, Moreno-Bueno G, Sarrio D, Locascio A, Cano A, et al. (2002) Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 21: 3241-3246 (Pubitemid 34548095)
38. Geradts J, de Herreros AG, Su Z, Burchette J, Broadwater G, et al. (2011) Nuclear Snail1 and nuclear ZEB1 protein expression in invasive and intraductal human breast carcinomas. Hum Pathol 42: 1125-1131
39. Come C, Magnino F, Bibeau F, De Santa BP, Becker KF, et al. (2006) Snail and slug play distinct roles during breast carcinoma progression. Clin Cancer Res 12: 5395-5402 (Pubitemid 44497253)
40. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, et al. (2008) Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 3: e2888
41. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715 (Pubitemid 351636299)
42. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, et al. (2010) Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci U S A 107: 15449-15454
43. Dhasarathy A, Phadke D, Mav D, Shah RR, Wade PA (2011) The transcription factors Snail and Slug activate the transforming growth factor-beta signaling pathway in breast cancer. PLoS ONE 6: e26514
44. Hugo HJ, Kokkinos MI, Blick T, Ackland ML, Thompson EW, et al. (2011) Defining the E-cadherin repressor interactome in epithelial-mesenchymal transition: the PMC42 model as a case study. Cells Tissues Organs 193: 23-40
45. Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, et al. (2006) Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10: 437-449 (Pubitemid 44693469)
46. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, et al. (2008) Loss of Ecadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68: 3645-3654
47. Smit MA, Geiger TR, Song JY, Gitelman I, Peeper DS (2009) A Twist-Snail axis critical for TrkB-induced epithelial-mesenchymal transition-like transformation, anoikis resistance, and metastasis. Mol Cell Biol 29: 3722-3737
48. Shin S, Dimitri CA, Yoon SO, Dowdle W, Blenis J (2010) ERK2 but not ERK1 induces epithelial-to-mesenchymal transformation via DEF motif-dependent signaling events. Mol Cell 38: 114-127
49. Worsham MJ, Pals G, Schouten JP, Miller F, Tiwari N, et al. (2006) Highresolution mapping of molecular events associated with immortalization, transformation, and progression to breast cancer in the MCF10 model. Breast Cancer Res Treat 96: 177-186
50. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674
51. Albagli-Curiel O, Lecluse Y, Pognonec P, Boulukos KE, Martin P (2007) A new generation of pPRIG-based retroviral vectors. BMC Biotechnol 7: 85
52. Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS (2002) The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111: 29-40