Expression of Snail is associated with myofibroblast phenotype development in oral squamous cell carcinoma

Histochemistry and Cell Biology

Volumn 131, Issue 5, 2009, Pages 651-660

  Franz, Marcus ^a   Spiegel, Karin ^a   Umbreit, Claudia ^a   Richter, Petra ^a   Codina Canet, Carolina ^a   Berndt, Angela ^b   Altendorf Hofmann, Annelore ^a   Koscielny, Sven ^a   Hyckel, Peter ^a   Kosmehl, Hartwig ^c   Virtanen, Ismo ^d   Berndt, Alexander ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^c HELIOS KLINIKUM ERFURT   (Germany)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Alpha smooth muscle actin; Metastasis; Myofibroblast; Oral squamous cell carcinoma; Snail

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CYTOKERATIN; EPIDERMAL GROWTH FACTOR; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VIMENTIN;

ADULT; AGED; ARTICLE; BASAL CELL CARCINOMA; CANCER CELL CULTURE; CANCER GRADING; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MOUTH CARCINOMA; MYOFIBROBLAST; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SQUAMOUS CELL CARCINOMA;

ACTINS; ADULT; AGED; AGED, 80 AND OVER; CADHERINS; CARCINOMA, SQUAMOUS CELL; EPIDERMAL GROWTH FACTOR; FIBROBLASTS; HUMANS; KERATINS; MIDDLE AGED; MOUTH NEOPLASMS; MYOBLASTS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1; TUMOR MARKERS, BIOLOGICAL; VIMENTIN;

GASTROPODA;

EID: 63949083631     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-009-0559-3     Document Type: Article

References (53)

1. Barnes L, Eveson JW, Reichart PA, Sidransky D (2005) Pathology and genetics of head and neck tumours (World Health Organization Classification of Tumours). IARC Press, Lyon
2. + fibrocytes in invasive ductal carcinomas, ductal carcinoma in situ, and benign breast lesions Virchows Arch 440 298 303
3. + fibrocytes, α-smooth muscle antigen-positive myofibroblasts, and CD117 expression in the stroma of invasive squamous cell carcinomas of the oral cavity, pharynx, and larynx Virchows Arch 444 231 234
4. E Batlle E Sancho C Franci D Dominguez M Monfar J Baulida A Garcia De Hereros 2000 The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells Nat Cell Biol 2 84 89
5. A Berndt P Hyckel A Könneker D Katenkamp H Kosmehl 1997 Oral squamous cell carcinoma invasion is associated with a laminin-5 matrix re-organization but independent of basement membrane hemidesmosome formation. Clues from an in vitro model Invasion Metastasis 17 251 258
6. A Berndt L Borsi P Hyckel H Kosmehl 2001 Fibrillary co-deposition of laminin-5 and large unspliced tenascin-C in the invasive front of oral squamous cell carcinoma in vivo and in vitro J Cancer Res Clin Oncol 127 286 292
7. MJ Blanco G Moreno-Bueno D Sartio A Locasicio A Cano J Palacios MA Nieto 2002 Correlation of Snail expression with histological grade and lymph node status in breast carcinomas Oncogene 21 3241 3246
8. V Bolos H Peinado MA Perez-Moreno MF Fraga M Esteller A Cano 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
9. A Boutet MA Esteban PH Maxwell MA Nieto 2007 Reactivation of Snail genes in renal fibrosis and carcinomas. A process of reversed embryogenesis? Cell Cycle 6 638 642
10. M Bryne HS Koppang R Lilleng A Kjaerheim 1992 Malignancy grading of the deep invasive margins of oral squamous cell carcinomas has high prognostic value J Pathol 166 375 381
11. A Cano MA Perez-Moreno I Rodrigo A Locascio MJ Blanco MG del Barrio F Portillo MA Nieto 2000 The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression Nat Cell Biol 2 76 83
12. AJ Daly L McIlreavey CR Irwin 2008 Regulation of HGF and SDF-1 expression by oral fibroblasts-implications for invasion of oral cancer Oral Oncol 44 646 651
13. G De Rosa E Barra M Guarino S Staibano V Donofrio A Boscaino 1994 Fibronectin, laminin, type IV collagen distribution, and myofibroblastic stromal reaction in aggressive and nonaggressive basal cell carcinoma Am J Dermatopathol 16 258 267
14. AS De Vries RG Tilton S Mortier NH Lameire 2006 Myofibroblast transdifferentiation of mesothelial cells is mediated by RAGE and contributes to peritoneal fibrosis in uraemia Nephrol Dial Transplant 21 2549 2555
15. O De Wever M Mareel 2003 Role of tissue stroma in cancer cell invasion J Pathol 200 429 447
16. C Franci M Takkunen N Dave F Alameda S Gómez R Rodríguez M Escrivà B Montserrat-Sentís T Baró M Garrido F Bonilla I Virtanen A García de Herreros 2006 Expression of Snail protein in tumor-stroma interface Oncogene 25 37 5134 5144
17. M Franz T Hansen P Richter L Borsi FD Böhmer P Hyckel P Schleier D Katenkamp L Zardi H Kosmehl A Berndt 2006 Complex formation of the laminin-5 gamma2 chain and large unspliced tenascin-C in oral squamous cell carcinoma in vitro and in situ: implications for sequential modulation of extracellular matrix in the invasive tumor front Histochem Cell Biol 126 1 125 131
18. M Franz P Richter C Geyer T Hansen LD Acuna P Hyckel FD Bohmer H Kosmehl A Berndt 2007 Mesenchymal cells contribute to the synthesis and deposition of the laminin-5 gamma 2 chain in the invasive front of oral squamous cell carcinoma J Mol Histol 38 3 183 190
19. G Giannelli C Bergamini E Fransvea C Sqarra S Antonaci 2005 Laminin-5 with transforming growth factor-beta1 induces epithelial to mesenchymal transition in hepatocellular carcinoma Gastroenterology 129 1375 1383
20. S Guaita I Puig C Franci M Garrido D Dominguez E Batlle E Sancho S Dedhar AG De Herreros J Baulida 2002 Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression J Biol Chem 277 39209 39216
21. K Higashikawa S Yoneda M Taki H Shigeishi S Ono K Tobiume N Kamata 2008 Gene expression profiling to identify genes associated with high-invasiveness in human squamous cell carcinoma with epithelial-to-mesenchymal transition Cancer Lett 264 256 264
22. SC Hung PY Kuo CF Chang TH Chen LL Ho 2006 Alpha-smooth muscle actin expression and structure integrity in chondrogenesis of human mesenchymal stem cells Cell Tissue Res 324 457 466
23. M Iwano D Plieth TM Danoff C Xue H Okada EG Neilson 2002 Evidence that fibroblasts derive from epithelium during tissue fibrosis J Clin Invest 110 341 350
24. X Jin J Li Z Li Y Li 2001 Expression of transforming growth factor beta (TGF-beta) subtypes in oral squamous cell carcinoma Hua Xi Kou Qiang Yi Xue Za Zhi 19 377 379
25. R Kalluri EG Neilson 2003 Epithelial-mesenchymal transition and its implication for fibrosis J Clin Invest 112 1776 1784
26. MG Kellermann LM Sobral SD da Silva KG Zecchin E Graner MA Lopes LP Kowalski RD Coletta 2008 Mutual paracrine effects of oral squamous cell carcinoma cells and normal oral fibroblasts: induction of fibroblast to myofibroblast transdifferentiation and modulation of tumor cell proliferation Oral Oncol 44 509 517
27. JM Lee S Dedhar R Kalluri EW Thompson 2006 The epithelial-mesenchymal transition: new insights in signalling, development, and disease J Cell Biol 172 973 981
28. MP Lewis KA Lygoe ML Nystrom WP Anderson PM Speight JF Marshall GJ Thomas 2004 Tumour-derived TGF-beta1 modulates myofibroblast differentiation and promotes HGF/SF-dependent invasion of squamous carcinoma cells Br J Cancer 90 4 822 832
29. G Maeda T Chiba M Okazaki T Satoh Y Taya T Aoba K Kato S Kawashiri K Imai 2005 Expression of SIP1 in oral squamous cell carcinomas: implications for E-cadherin expression and tumour progression Int J Oncol 27 1535 1541
30. NM Meindl-Beinker S Dooley 2008 Transforming growth factor-beta and hepatocyte transdifferentiation in liver fibrosis J Gastroenterol Hepatol 23 Suppl 1 S122 S127
31. S Natsugoe Y Uchikado H Okumura M Matsumoto T Setoyama K Tamotsu Y Kita A Sakamoto T Owaki S Ishigami T Aikou 2007 Snail plays a key role in E-cadherin-preserved esophageal squamous cell carcinoma Oncol Rep 17 517 523
32. T Onoue D Uchida NM Bequm Y Tomizuka H Yoshida M Sato 2006 Epithelial-mesenchymal transition induced by the stromal cell-derived factor-1/CXCR4 system in oral squamous cell carcinoma cells Int J Oncol 29 1133 1138
33. S Peiro M Escriva I Puig MJ Barberà N Dave N Herranz MJ Larriba M Takkunen C Francí A Muñoz I Virtanen J Baulida A García de Herreros 2006 Snail 1 transcriptional repressor binds to its own promoter and controls its expression Nucleic Acids Res 34 2077 2084
34. C Pena JM Garcia J Silva V García R Rodríguez I Alonso I Millán C Salas AG de Herreros A Muñoz F Bonilla 2005 E-cadherin and vitamin D receptor regulation by Snail and Zeb1 in colon cancer: clinicopathological correlations Hum Mol Genet 14 3361 3370
35. OW Petersen H Lind Nielsen T Gudjonsson R Villadseu L Rønnov-Jessen ML Bissell 2001 The plasticity of human breast carcinoma cells is more than epithelial to mesenchymal conversion Breast Cancer Res 3 4 213 217
36. OW Petersen H Nielsen T Gudjonsson R Villadsen F Rank E Niebuhr MJ Bissell L Rønnov-Jessen 2003 Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma Am J Pathol 162 391 402
37. G Prindull D Zipori 2004 Environmental guidance of normal and tumor cell plasticity: epithelial mesenchymal transitions as a paradigm Blood 103 2892 2899
38. DC Radisky PA Kenny MJ Bissell 2007 Fibrosis and cancer: do myofibroblasts come also from epithelial cells via EMT? J Cell Biochem 101 4 830 839
39. L Ronnov-Jessen OW Petersen VE Koteliansky MJ Bissell 1995 The origin of the myofibroblast in breast cancer: recapitulation of tumor environment in culture unreveals diversity and implicates converted fibroblasts and recruited smooth muscle cells J Clin Invest 95 859 873
40. CH Stuelten S DaCosta Byfield PR Arany TS Karpova WG Stetler-Stevenson AB Roberts 2005 Breast cancer cells induce stromal fibroblasts to express MMP-9 via secretion of TNF-alpha and TGF-beta J Cell Sci 118 2143 2153
41. L Sun ME Diamond AJ Ottaviano MJ Joseph V Ananthanarayan HG Munshi 2008 Transforming growth factor-beta 1 promotes matrix metalloproteinase-9-mediated oral cancer invasion through Snail expression Mol Cancer Res 6 10 20
42. M Taki K Higashikawa S Yoneda S Ono H Shigeishi M Nagayama N Kamata 2008 Up-regulation of stromal cell-derived factor-1alpha and its receptor CXCR4 expression accompanied with epithelial-mesenchymal transition in human oral squamous cell carcinoma Oncol Rep 19 993 998
43. M Takkunen R Grenman M Hukkanen M Korhonen A Garcia de Herreros I Virtanen 2006 Snail-dependent and -independent epithelial-mesenchymal transition in oral squamous carcinoma cells J Histochem Cytochem 54 11 1263 1275
44. M Takkunen M Ainola N Vainionpää R Grenman M Patarroyo A Garcia de Herreros YT Konttinen I Virtanen 2008 Epithelial-mesenchymal transition downregulates laminin a5 chain and upregulates a4 chain in oral squamous carcinoma cells Histochem Cell Biol 130 509 525
45. JP Thiery 2002 Epithelial-mesenchymal transition in tumour progression Nat Rev Cancer 2 442 454
46. LDR Thompson JA Wieneke M Miettinen DK Heffner 2002 Spindle cell (sarcomatoid) carcinoma of the larynx. A clinicopathologic study of 187 cases Am J Surg Pathol 26 153 170
47. CE Wilkins-Port PJ Higgins 2007 Regulation of extracellular matrix remodelling following transforming growth factor-β1/epidermal growth factor-stimulated epithelial-mesenchymal transition in human premalignant keratinocytes Cells Tissues Organs 185 116 122
48. J Yang SA Mani JL Donaher S Ramaswamy RA Itzykson C Come P Savagner I Gitelman A Richardson RA Weinberg 2004 Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis Cell 117 927 939
49. H Yanjia J Xinchun 2007 The role of epithelial-mesenchymal transition in oral squamous cell carcinoma and oral submucous fibrosis Clin Chim Acta 383 51 56
50. T Yin CY Wang T Liu G Thao YH Zha 2006 Expression of Snail and E-cadherin in pancreatic carcinoma and clinical significance thereof Zhonghua Yi Xue Za Zhi 86 2821 2925
51. K Yokoyama N Kamata R Fujimoto S Tsutsumi M Tomonari M Taki H Hosokawa M Nagayama 2003 Increased invasion and matrix metalloproteinase-2 expression by Snail-induced mesenchymal transition in squamous cell carcinoma Int J Oncol 22 891 898
52. W Zhang A Alt-Holland A Margulis Y Shamis NE Fusenig U Rodeck JA Garlick 2006 E-cadherin loss promotes the initiation of squamous cell carcinoma invasion through modulation of integrin-mediated adhesion J Cell Sci 119 283 291
53. N Zidar N Gale N Kojc M Volavsek A Cardesa L Alos H Höfler K Blechschmidt KF Becker 2008 Cadherin-catenin complex and transcription factor Snail-1 in spindle cell carcinoma of the head and neck Virchows Arch 453 267 274