E-cadherin in oral SCC: An analysis of the confusing literature and new insights related to its immunohistochemical expression

Histology and Histopathology

Volumn 27, Issue 2, 2012, Pages 141-150

  Vered, Marilena ^a   Allon, Irit ^a   Buchner, Amos ^a   Dayan, Dan ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

E cadherin; Extracellular and intracellular domain; Immunohistochemistry; Oral carcinoma; Tumor microenvironment

Indexed keywords

CADHERIN;

HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUTH TUMOR; PHYSIOLOGY; REVIEW; SQUAMOUS CELL CARCINOMA; TUMOR MICROENVIRONMENT;

CADHERINS; CARCINOMA, SQUAMOUS CELL; HUMANS; IMMUNOHISTOCHEMISTRY; MOUTH NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84857676626     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (48)

1. Araújo V.C., Demasi A.P., Furuse C., Altemani A., Alves V.A., Freitas L.L. and Araújo N.S. (2009). Collagen type I may influence the expression of E-cadherin and beta-catenin in carcinoma expleomorphic adenoma. Appl. Immunohistochem. Mol. Morphol. 17, 312-318.
2. Bankfalvi A., Kraßort M., Vegh A., Felszeghy E. and Piffko J. (2002a). Deranged expression of the E-cadherin/b-catenin complex and the epidermal growth factor receptor in the clinical evolution and progression of oral squamous cell carcinomas. J. Oral Pathol. Med. 31, 450-457.
3. Bankfalvi A., Kraßort M., Buchwalow I.B., Vegh A., Felszeghy E. and Piffko J. (2002b). Gains and losses of adhesion molecules (CD44, E-cadherin, and ß-catenin) during oral carcinogenesis and tumour progression. J. Pathol. 198, 343-351.
4. Benton G., Crooke E. and George J. (2009). Laminin-1 induces Ecadherin expression in 3-dimensional cultured breast cancer cells by inhibiting DNA methyltransferase 1 and reversing promoter methylation status. FASEB J. 23, 3884-3895.
5. Berx G. and van Roy F. (2009). Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb. Perspect. Biol. 1, a003129.
6. Céspedes M.V., Larriba M.J., Pavón M.A., Alamo P., Casanova I., Parreño M., Feliu A., Sancho F.J., Muñoz A. and Mangues R. (2010). Site-dependent E-Cadherin cleavage and nuclear translocation in a metastatic colorectal cancer model. Am. J. Pathol. 177, 2067-2079.
7. Chang H.W., Chow V., Lam K.Y., Wei W.I. and Yuen A.P. (2002). Loss of E-cadherin expression resulting from promoter hypermethylation in oral tongue carcinoma and its prognostic significance. Cancer 94, 386-392.
8. Chetty R., Serra S. and Salahshor S. (2008). Nuclear expression of Ecadherin. Am. J. Surg. Pathol. 32, 1269-1270.
9. Chow V., Yuen A.P., Lam K.Y., Tsao G.S., Ho W.K. and Wei W.I. (2001). A comparative study of the clinicopathological significance of E-cadherin and catenins (alpha, beta, gamma) expression in the surgical management of oral tongue carcinoma. J. Cancer Res. Clin. Oncol. 127, 59-63.
10. Dassen H., Punyadeera C., Delvoux B., Schulkens I., Marchetti C., Kamps R., Klomp J., Dijcks F., de Goeij A., D'Hooghe T., Kyama C., Ederveen A., Dunselman G., Groothuis P. and Romano A.(2010). Olfactomedin-4 regulation by estrogen in the human endometrium requires epidermal growth factor signaling. Am. J. Pathol. 177, 2495-2508.
11. de Moraes R.V., Oliveira D.T., Landman G., de Carvalho F., Caballero O., Nonogaki S., Nishimoto I. and Kowalski L.P. (2008). E-cadherin abnormalities resulting from CPG methylation promoter in metastatic and nonmetastatic oral cancer. Head Neck 30, 85-92.
12. Diniz-Freitas M., García-Caballero T., Antunez-Lopez J., Gandara-Rey J.M. and García-García A. (2006). Reduced E-cadherin expression is an indicator of unfavorable prognosis in oral squamous cell carcinoma. Oral Oncol. 42, 190-200.
13. Ferber E.C., Kajita M., Wadlow A., Tobiansky L., Niessen C., Ariga H., Daniel J. and Fujita Y. (2008). A role for the cleaved cytoplasmic domain of E-cadherin in the nucleus J. Biol. Chem. 283, 12691-12700.
14. Foschini M.P., Cocchi R., Morandi L., Marucci G., Pennesi M.G., Righi A., Tosi A.L., de Biase D., Pession A. and Montebugnoli L. (2008). E-cadherin loss and DNP73L expression in oral squamous cell carcinomas showing aggressive behavior. Head Neck 30, 1475-1482.
15. Franz M., Spiegel K., Umbreit C., Richter P., Codina-Canet C., Berndt A., Altendorf-Hofmann A., Koscielny S., Hyckel P., Kosmehl H., Virtanen I. and Berndt A. (2009). Expression of Snail is associated with myofibroblast phenotype development in oral squamous cell carcinoma. Histochem. Cell Biol. 131, 651-660.
16. Gaggioli C., Hooper S., Hidalgo-Carcedo C., Grosse R., Marshall J.F., Harrington K. and Sahai E. (2007). Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 9, 1392-1400.
17. Gervais M.L., Henry P.C., Saravanan A., Burry T.N., Gallie B.L., Jewett M.A., Hill R.P., Evans A.J. and Ohh M. (2007). Nuclear E-cadherin and VHL immunoreactivity are prognostic indicators of clear-cellrenal cell carcinoma. Lab. Invest. 87, 1252-1264.
18. Grover P.K., Hardingham J.E. and Cummins A.G. (2010). Stem cell marker olfactomedin 4: critical appraisal of its characteristics and role in tumorigenesis. Cancer Metastasis Rev. 29, 761-775.
19. Huber O., Kemler R. and Langosch D. (1999). Mutations affecting transmembrane segment interactions impair adhesiveness of Ecadherin. J. Cell Sci. 112, 4415-4423.
20. Hung K.F., Chang C.S., Liu C.J., Lui M.T., Cheng C.Y. and Kao S.Y. (2006). Differential expression of E-cadherin in metastatic lesions comparing to primary oral squamous cell carcinoma. J. Oral Pathol. Med. 35, 589-594.
21. Imai T., Horiuchi A., Wang C., Oka K., Ohira S., Nikaido T. and Konishi I. (2003). Hypoxia attenuates the expression of E-cadherin via upregulation of SNAIL in ovarian carcinoma cells. Am. J. Pathol. 163, 1437-1447.
22. Kudo Y., Kitajima S., Ogawa I., Hiraoka M., Sargolzaei S., Keikhaee M.R., Sato S., Miyauchi M. and Takata T. (2004). Invasion and metastasis of oral cancer cells require methylation of E-cadherin and/or degradation of membranous ß-catenin. Clin. Cancer Res. 10, 5455-5463.
23. Kurtz K.A., Hoffman H.T., Zimmerman M.B. and Robinson R.A. (2006). Decreased E-cadherin but not ß-catenin expression is associated with vascular invasion and decreased survival in head and neck squamous carcinomas. Otolaryngol. Head Neck Surg. 134, 142-146.
24. Lim S.C., Zhang S., Ishii G., Endoh Y., Kodama K., Miyamoto S., Hayashi R., Ebihara S., Cho J.S. and Ochiai A. (2004). Predictive markers for late cervical metastasis in stage I and II invasive squamous cell carcinoma of the oral tongue. Clin. Cancer Res. 10, 166-172.
25. Lim J., Kim J.H., Paeng J.Y., Kim M.J., Hong S.D., Lee J.I. and Hong S.P. (2005). Prognostic value of activated Akt expression in oral squamous cell carcinoma. J. Clin. Pathol. 58, 1199-1205.
26. Liu L.K., Jiang X.Y., Zhou X.X., Wang D.M., Song X.L. and Jiang H.B. (2010). Upregulation of vimentin and aberrant expression of Ecadherin/ b-catenin complex in oral squamous cell carcinomas: correlation with the clinicopathological features and patient outcome. Mod. Pathol. 23, 213-224.
27. Lopes F.F., da Costa Miguel M.C., Pereira A.L., da Cruz M.C., de Almeida Freitas R., Pinto L.P. and de Souza L.B. (2009). Changes in immunoexpression of E-cadherin and ß-catenin in oral squamous cell carcinoma with and without nodal metastasis. Ann. Diagn. Pathol. 13, 22-29.
28. Lyons A.J. and Jones J. (2007). Cell adhesion molecules, the extracellular matrix and oral squamous carcinoma. Int. J. Oral Maxillofac. Surg. 36, 671-679.
29. Mahomed F., Altini M. and Meer S. (2007). Altered E-cadherin/ß-catenin expression in oral squamous carcinoma with and without nodal metastasis. Oral Dis. 13, 386-392.
30. Nakanishi Y., Akimoto S., Sato Y., Kanai Y., Sakamoto M. and Hirohashi S. (2004). Prognostic significance of dysadherin expression in tongue cancer: immunohistochemical analysis of 91 cases. Appl. Immunohistochem. Mol. Morphol. 12, 323-328.
31. Nakayama S., Sasaki A., Mese H., Alcalde R.E., Tsuji T. and Matsumura T. (2001). The E-cadherin gene is silenced by CpG methylation in human oral squamous cell carcinomas. Int. J. Cancer 93, 667-673.
32. Okamoto M., Nishimine M., Kishi M., Kirita T., Sugimura M., Nakamura M. and Konishi N. (2002). Prediction of delayed neck metastasis in patients with stage I/II squamous cell carcinoma of the tongue. J. Oral Pathol. Med. 31, 227-233.
33. Onder T.T., Gupta P.B., Mani S.A., Yang J., Lander E.S. and Weinberg R.A. (2008). Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 68, 3645-3654.
34. Ozawa M. (2002). Lateral dimerization of the E-cadherin extracellular domain is necessary but not sufficient for adhesive activity. J. Biol. Chem. 277,19600-19608.
35. Pece S. and Gutkind J.S. (2002). E-cadherin and Hakai: signalling, remodeling or destruction? Nat. Cell Biol. 4, E72-E74.
36. Pugalagiri P. and Cheng Y.S. (2011). Nuclear localization of E-cadherin in oral squamous cell carcinoma. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 111, e54.
37. Pyo S.W., Hashimoto M., Kim Y.S., Kim C.H., Lee S.H., Johnson K.R., Wheelock M.J. and Park J.U. (2007). Expression of E-cadherin, Pcadherin and N-cadherin in oral squamous cell carcinoma: correlation with the clinicopathologic features and patient outcome J. Craniomaxillofac. Surg. 35, 1-9.
38. Rakha E.A., Patel A., Powe D.G., Benhasouna A., Green A.R., Lambros M.B., Reis-Filho J.S. and Ellis I.O. (2010). Clinical and biological significance of E-cadherin protein expression in invasive lobular carcinoma of the breast. Am. J. Surg. Pathol. 34, 1472-1479.
39. Saito Y., Takazawa H., Uzawa K., Tanzawa H. and Sato K. (1998). Reduced expression of E-cadherin in oral squamous cell carcinoma: relationship with DNA methylation of 5' CpG island. Int. J. Oncol. 12, 293-298.
40. Salahshor S., Naidoo R., Serra S., Shih W., Tsao M.S., Chetty R. and Woodgett J.R. (2008). Frequent accumulation of nuclear E-cadherin and alterations in the Wnt signaling pathway in esophageal squamous cell carcinomas. Mod. Pathol. 21, 271-281.
41. Schmalhofer O., Brabletz S. and Brabletz T. (2009). E-cadherin, betacatenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev. 28, 151-166.
42. Tanaka N., Odajima T., Ogi K., Ikeda T. and Satoh M. (2003). Expression of E-cadherin, a-catenin, and ß-catenin in the process of lymph node metastasis in oral squamous cell carcinoma. Br. J. Cancer 89, 557-563.
43. Ueda G., Sunakawa H., Nakamori K., Shinya T., Tsuhako W., Tamura Y., Kosugi T., Sato N., Ogi K. and Hiratsuka H. (2006). Aberrant expression of ß- and g-catenin is an independent prognostic marker in oral squamous cell carcinoma. Int. J. Oral Maxillofac. Surg. 35, 356-361.
44. Vered M., Dayan D., Yahalom R., Dobriyan A., Barshack I., Bello I.O., Kantola S. and Salo T. (2010). Cancer-associated fibroblasts and epithelial-mesenchymal transition in metastatic oral tongue squamous cell carcinoma. Int. J. Cancer 101, 274-280.
45. Viswanathan M., Tsuchida N. and Shanmugam G. (2003). Promoter hypermethylation profile of tumor-associated genes p16, p15, hMLH1, MGMT and E-cadherin in oral squamous cell carcinoma. Int. J. Cancer 105, 41-46.
46. Wang X., Zhang J., Fan M., Zhou Q., Deng H., Aisharif M.J., and Chen X. (2009).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. 107, 547-554.
47. Yeh K.T., Shih M.C., Lin T.H., Chen J.C., Chang J.Y., Kao C.F., Lin K.L. and Chang J.G. (2002). The correlation between CpG methylation on promoter and protein expression of E-cadherin in oral squamouscell carcinoma. Anticancer Res. 22, 3971-3976.
48. Zhong L.P., Li J., Zhang C.P., Zhu H.G., Sun J. and Zhang Z.Y. (2007). Expression of E-cadherin in cervical lymph nodes from primary oral squamous cell carcinoma patients. Arch. Oral Biol. 52, 740-747.