Deregulation of Snai2 is associated with metastasis and poor prognosis in tongue squamous cell carcinoma

International Journal of Cancer

Volumn 130, Issue 10, 2012, Pages 2249-2258

  Wang, Cheng ^a,b   Liu, Xiqiang ^a,b   Huang, Hongzhang ^a   Ma, Huibin ^a   Cai, Weixin ^a   Hou, Jingsong ^a   Huang, Lei ^b   Dai, Yang ^b   Yu, Tianwei ^c   Zhou, Xiaofeng ^b  

^a SUN YAT SEN UNIVERSITY   (China)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

E cadherin; epithelial mesenchymal transition; Snai2; squamous cell carcinoma

Indexed keywords

TRANSCRIPTION FACTOR SLUG; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VIMENTIN;

ADULT; ARTICLE; CANCER CELL CULTURE; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; COHORT ANALYSIS; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SQUAMOUS CELL CARCINOMA; SQUAMOUS CELL CARCINOMA OF ORAL TONGUE; TONGUE CARCINOMA;

CADHERINS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALE; MIDDLE AGED; PROGNOSIS; TONGUE NEOPLASMS; TRANSCRIPTION FACTORS; VIMENTIN;

EID: 81155156590     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26226     Document Type: Article

References (46)

1. Timar J, Csuka O, Remenar E, Repassy G, Kasler M,. Progression of head and neck squamous cell cancer. Cancer Metastasis Rev 2005; 24: 107-27. (Pubitemid 40576067)
2. Franceschi D, Gupta R, Spiro RH, Shah JP,. Improved survival in the treatment of squamous carcinoma of the oral tongue. Am J Surg 1993; 166: 360-5. (Pubitemid 24240988)
3. Layland MK, Sessions DG, Lenox J,. The influence of lymph node metastasis in the treatment of squamous cell carcinoma of the oral cavity, oropharynx, larynx, and hypopharynx: N0 versus N+. Laryngoscope 2005; 115: 629-39. (Pubitemid 40530012)
4. Cunningham MJ, Johnson JT, Myers EN, Schramm VL, Jr, Thearle PB,. Cervical lymph node metastasis after local excision of early squamous cell carcinoma of the oral cavity. Am J Surg 1986; 152: 361-6. (Pubitemid 16001463)
5. Ho CM, Lam KH, Wei WI, Lau SK, Lam LK,. Occult lymph node metastasis in small oral tongue cancers. Head Neck 1992; 14: 359-63.
6. Yuen AP, Lam KY, Chan AC, Wei WI, Lam LK, Ho WK, Ho CM,. Clinicopathological analysis of elective neck dissection for N0 neck of early oral tongue carcinoma. Am J Surg 1999; 177: 90-2. (Pubitemid 29089006)
7. Sano D, Myers JN,. Metastasis of squamous cell carcinoma of the oral tongue. Cancer Metastasis Rev 2007; 26: 645-62. (Pubitemid 350115112)
8. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-15. (Pubitemid 351636299)
9. Thiery JP, Acloque H, Huang RY, Nieto MA,. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-90.
10. Kalluri R, Weinberg RA,. The basics of epithelial-mesenchymal transition. J Clin Invest 2009; 119: 1420-8.
11. Acloque H, Thiery JP, Nieto MA,. The physiology and pathology of the EMT. Meeting on the epithelial-mesenchymal transition. EMBO Rep 2008; 9: 322-6.
12. Halbleib JM, Nelson WJ,. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 2006; 20: 3199-214. (Pubitemid 44904842)
13. Liu LK, Jiang XY, Zhou XX, Wang DM, Song XL, Jiang HB,. Upregulation of vimentin and aberrant expression of E-cadherin/beta-catenin complex in oral squamous cell carcinomas: correlation with the clinicopathological features and patient outcome. Mod Pathol 2010; 23: 213-24.
14. Wang X, Zhang J, Fan M, Zhou Q, Deng H, Aisharif MJ, Chen X,. The expression of E-cadherin at the invasive tumor front of oral squamous cell carcinoma: immunohistochemical and RT-PCR analysis with clinicopathological correlation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009; 107: 547-54.
15. Barrallo-Gimeno A, Nieto MA,. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 2005; 132: 3151-61. (Pubitemid 41167144)
16. Nieto MA,. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 2002; 3: 155-66.
17. Higashikawa K, Yoneda S, Tobiume K, Taki M, Shigeishi H, Kamata N,. Snail-induced down-regulation of DeltaNp63alpha acquires invasive phenotype of human squamous cell carcinoma. Cancer Res 2007; 67: 9207-13. (Pubitemid 47535907)
18. Onoue T, Uchida D, Begum NM, Tomizuka Y, Yoshida H, Sato M,. Epithelial-mesenchymal transition induced by the stromal cell-derived factor-1/CXCR4 system in oral squamous cell carcinoma cells. Int J Oncol 2006; 29: 1133-8.
19. Bauer K, Dowejko A, Bosserhoff AK, Reichert TE, Bauer RJ,. P-cadherin induces an epithelial-like phenotype in oral squamous cell carcinoma by GSK-3beta-mediated Snail phosphorylation. Carcinogenesis 2009; 30: 1781-8.
20. Joseph MJ, Dangi-Garimella S, Shields MA, Diamond ME, Sun L, Koblinski JE, Munshi HG,. Slug is a downstream mediator of transforming growth factor-beta1-induced matrix metalloproteinase-9 expression and invasion of oral cancer cells. J Cell Biochem 2009; 108: 726-36.
21. Ye H, Yu T, Temam S, Ziober BL, Wang J, Schwartz JL, Mao L, Wong DT, Zhou X,. Transcriptomic dissection of tongue squamous cell carcinoma. BMC Genomics 2008; 9: 69.
22. O'Donnell RK, Kupferman M, Wei SJ, Singhal S, Weber R, O'Malley B, Cheng Y, Putt M, Feldman M, Ziober B, Muschel RJ,. Gene expression signature predicts lymphatic metastasis in squamous cell carcinoma of the oral cavity. Oncogene 2005; 24: 1244-51. (Pubitemid 40313925)
23. Toruner GA, Ulger C, Alkan M, Galante AT, Rinaggio J, Wilk R, Tian B, Soteropoulos P, Hameed MR, Schwalb MN, Dermody JJ,. Association between gene expression profile and tumor invasion in oral squamous cell carcinoma. Cancer Genet Cytogenet 2004; 154: 27-35. (Pubitemid 39286169)
24. Ziober AF, Patel KR, Alawi F, Gimotty P, Weber RS, Feldman MM, Chalian AA, Weinstein GS, Hunt J, Ziober BL,. Identification of a gene signature for rapid screening of oral squamous cell carcinoma. Clin Cancer Res 2006; 12: 5960-71. (Pubitemid 44703755)
25. R-Development-Core-Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, 2006.
26. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80.
27. Yu T, Ye H, Chen Z, Ziober BL, Zhou X,. Dimension reduction and mixed-effects model for microarray meta-analysis of cancer. Front Biosci 2008; 13: 2714-20. (Pubitemid 351611604)
28. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP,. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003; 31: e15.
29. Liu X, Wang A, Lo Muzio L, Kolokythas A, Sheng S, Rubini C, Ye H, Shi F, Yu T, Crowe DL, Zhou X,. Deregulation of manganese superoxide dismutase (SOD2) expression and lymph node metastasis in tongue squamous cell carcinoma. BMC Cancer 2010; 10: 365.
30. Wang A, Liu X, Sheng S, Ye H, Peng T, Shi F, Crowe DL, Zhou X,. Dysregulation of heat shock protein 27 expression in oral tongue squamous cell carcinoma. BMC Cancer 2009; 9: 167.
31. Liu X, Jiang L, Wang A, Yu J, Shi F, Zhou X,. MicroRNA-138 suppresses invasion and promotes apoptosis in head and neck squamous cell carcinoma cell lines. Cancer Lett 2009; 286: 217-22.
32. Liu X, Yu J, Jiang L, Wang A, Shi F, Ye H, Zhou X,. MicroRNA-222 regulates cell invasion by targeting matrix metalloproteinase 1 (MMP1) and manganese superoxide dismutase 2 (SOD2) in tongue squamous cell carcinoma cell lines. Cancer Genomics Proteomics 2009; 6: 131-9.
33. Sun L, Diamond ME, Ottaviano AJ, Joseph MJ, Ananthanarayan V, Munshi HG,. Transforming growth factor-beta 1 promotes matrix metalloproteinase-9-mediated oral cancer invasion through snail expression. Mol Cancer Res 2008; 6: 10-20. (Pubitemid 351378162)
34. Diamond ME, Sun L, Ottaviano AJ, Joseph MJ, Munshi HG,. Differential growth factor regulation of N-cadherin expression and motility in normal and malignant oral epithelium. J Cell Sci 2008; 121: 2197-207.
35. Jiang L, Liu X, Kolokythas A, Yu J, Wang A, Heidbreder CE, Shi F, Zhou X,. Down-regulation of the Rho GTPase signaling pathway is involved in the microRNA-138 mediated inhibition of cell migration and invasion in tongue squamous cell carcinoma. Int J Cancer 2010; 127: 505-12.
36. Gregory PA, Bracken CP, Bert AG, Goodall GJ,. MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle 2008; 7: 3112-8.
37. Schmalhofer O, Brabletz S, Brabletz T,. E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 2009; 28: 151-66.
38. Takkunen M, Ainola M, Vainionpaa N, Grenman R, Patarroyo M, Garcia de Herreros A, Konttinen YT, Virtanen I,. Epithelial-mesenchymal transition downregulates laminin alpha5 chain and upregulates laminin alpha4 chain in oral squamous carcinoma cells. Histochem Cell Biol 2008; 130: 509-25.
39. Yokoyama K, Kamata N, Hayashi E, Hoteiya T, Ueda N, Fujimoto R, Nagayama M,. Reverse correlation of E-cadherin and snail expression in oral squamous cell carcinoma cells in vitro. Oral Oncol 2001; 37: 65-71.
40. Schwock J, Bradley G, Ho JC, Perez-Ordonez B, Hedley DW, Irish JC, Geddie WR,. SNAI1 expression and the mesenchymal phenotype: an immunohistochemical study performed on 46 cases of oral squamous cell carcinoma. BMC Clin Pathol 2010; 10: 1.
41. Franz M, Spiegel K, Umbreit C, Richter P, Codina-Canet C, Berndt A, Altendorf-Hofmann A, Koscielny S, Hyckel P, Kosmehl H, Virtanen I, Berndt A,. Expression of Snail is associated with myofibroblast phenotype development in oral squamous cell carcinoma. Histochem Cell Biol 2009; 131: 651-60.
42. Haraguchi M, Okubo T, Miyashita Y, Miyamoto Y, Hayashi M, Crotti TN, McHugh KP, Ozawa M,. Snail regulates cell-matrix adhesion by regulation of the expression of integrins and basement membrane proteins. J Biol Chem 2008; 283: 23514-23.
43. Qiao B, Johnson NW, Gao J,. Epithelial-mesenchymal transition in oral squamous cell carcinoma triggered by transforming growth factor-beta1 is Snail family-dependent and correlates with matrix metalloproteinase-2 and -9 expressions. Int J Oncol 2010; 37: 663-8.
44. Hotz B, Arndt M, Dullat S, Bhargava S, Buhr HJ, Hotz HG,. Epithelial to mesenchymal transition: expression of the regulators snail, slug, and twist in pancreatic cancer. Clin Cancer Res 2007; 13: 4769-76. (Pubitemid 47294783)
45. Savagner P, Yamada KM, Thiery JP,. The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J Cell Biol 1997; 137: 1403-19. (Pubitemid 27265951)
46. Olmeda D, Montes A, Moreno-Bueno G, Flores JM, Portillo F, Cano A,. Snai1 and Snai2 collaborate on tumor growth and metastasis properties of mouse skin carcinoma cell lines. Oncogene 2008; 27: 4690-701.