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Changed Expression of E-cadherin and Galectin-9 in Oral Squamous Cell Carcinomas but Lack of Potential as Prognostic Markers

  • Chan, Siew Wui (Department of Oro-Maxillofacial Surgical and Medical Sciences, University of Malaya) ;
  • Kallarakkal, Thomas George (Department of Oro-Maxillofacial Surgical and Medical Sciences, University of Malaya) ;
  • Abraham, Mannil Thomas (Department of Oral & Maxillofacial Surgery, Hospital Tengku Ampuan Rahimah)
  • Published : 2014.03.01

Abstract

Background: The survival rate for oral squamous cell carcinoma (OSCC) has remained generally unchanged in the past three decades, underlining the need for more biomarkers to be developed to aid prognostication and effective management. The prognostic potential of E-cadherin expression in OSCCs has been variable in previous studies while galectin-9 expression has been correlated with improved prognosis in other cancers. The aim of the present study was to investigate the expression of galectin-9 and E-cadherin in OSCC and their potential as prognostic biomarkers. Materials and Methods: E-cadherin and Galectin-9 expression was examined by immunohistochemistry in 32 cases of OSCC of the buccal mucosa (13 with and 19 without lymph node metastasis), as well as 6 samples of reactive lesions and 5 of normal buccal mucosa. Results: The expression of E-cadherin in OSCC was significantly lower than the control tissues but galectin-9 expression was conversely higher. Median E-cadherin HSCOREs between OSCCs positive and negative for nodal metastasis were not significantly different. Mean HSCOREs for galectin-9 in OSCC without lymph node metastasis ($127.7{\pm}81.8$) was higher than OSCC with lymph node metastasis ($97.9{\pm}62.9$) but this difference was not statistically significant. Conclusions: E-cadherin expression is reduced whilst galectin-9 expression is increased in OSCC. However, the present results suggest that E-cadherin and galectin-9 expression may not be useful as prognostic markers for OSCC.

References

  1. Alberts B, Johnson A, Lewis J, et al (2002). Cell-Cell Adhesion. Molecular Biology of the Cell. 4 ed. New York: Garland Science.
  2. Alves PM, Godoy GP, Gomes DQ, et al (2011). Significance of galectins-1, -3, -4 and -7 in the progression of squamous cell carcinoma of the tongue. Pathol Res Pract, 207, 236-40. https://doi.org/10.1016/j.prp.2011.02.004
  3. Balan V, Nangia-Makker P, Raz A (2010). Galectins as cancer biomarkers. Cancers, 2, 592-610. https://doi.org/10.3390/cancers2020592
  4. Berchuck A, Soisson AP, Clarke-Pearson DL, et al (1989). Immunohistochemical expression of CA 125 in endometrial adenocarcinoma: correlation of antigen expression with metastatic potential. Cancer Res, 49, 2091-5.
  5. Bosch FX, Abel U, Kartenbeck J (2005). E-cadherin is a selective and strongly dominant prognostic factor in squamous cell carcinoma: a comparison of E-cadherin with desmosomal components. Int J Cancer, 114, 779-90. https://doi.org/10.1002/ijc.20782
  6. Cada Z, Smetana K Jr, Lacina L, et al (2009). Immunohistochemical fingerprinting of the network of seven adhesion/growthregulatory lectins in human skin and detection of distinct tumour-associated alterations. Folia Biologica, 55, 145-52.
  7. Cerezo L (2011). Is loss of cadherin expression predictive of high aggressiveness in oropharyngeal squamous cell carcinoma? Oral Oncology, 47, 685. https://doi.org/10.1016/j.oraloncology.2011.02.016
  8. Chen HY, Lo CH, Li CS, Hsu DK, Liu FT (2012). Galectins and cutaneous immunity. Dermatologica Sinica, 30, 121-7. https://doi.org/10.1016/j.dsi.2012.10.002
  9. Christofori G & Semb H (1999). The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene. Trends Biochem Sci, 24, 73-6. https://doi.org/10.1016/S0968-0004(98)01343-7
  10. Cooper DN, Barondes SH (1999). God must love galectins; he made so many of them. Glycobiology, 9, 979-84. https://doi.org/10.1093/glycob/9.10.979
  11. Diniz-Freitas M, Garcia-Caballero T, Antunez-Lopez J, Gandara-Rey JM, Garcia-Garcia A (2006). Reduced E-cadherin expression is an indicator of unfavourable prognosis in oral squamous cell carcinoma. Oral Oncol, 42, 190-200.
  12. Dorta RG, Landman G, Kowalski LP, et al (2002). Tumourassociated tissue eosinophilia as a prognostic factor in oral squamous cell carcinomas. Histopathology, 41, 152-7.
  13. Edge SE, Byrd DR, Compton CC, et al (2010). AJCC Cancer Staging Manual New York, USA, Springer.
  14. Fik Z, Valach J, Chovanec M, et al (2013). Loss of adhesion/growth-regulatory galectin-9 from squamous cell epithelium in head and neck carcinomas. J Oral Pathol Med, 42, 166-73. https://doi.org/10.1111/j.1600-0714.2012.01185.x
  15. Foschini MP, Cocchi R, Morandi L, et al (2008). E-cadherin loss and Delta Np73L expression in oral squamous cell carcinomas showing aggressive behavior. Head & Neck, 30, 1475-82. https://doi.org/10.1002/hed.20908
  16. Foschini MP, Leonardi E, Eusebi LH, et al (2013). Podoplanin and E-cadherin expression in preoperative incisional biopsies of oral squamous cell carcinoma is related to lymph node metastases. Int J Surg Pathol, 21, 133-41. https://doi.org/10.1177/1066896912471851
  17. Friedrichs J, Torkko JM, Helenius J, et al (2007). Contributions of galectin-3 and -9 to epithelial cell adhesion analyzed by single cell force spectroscopy. J Biol Chem, 282, 29375-83. https://doi.org/10.1074/jbc.M701867200
  18. Hirashima M (2003). Multi-functions of Galectin-9. Mod Asp Immunobiol, 3, 6.
  19. Honjo Y, Inohara H, Akahani S, et al (2000). Expression of cytoplasmic galectin-3 as a prognostic marker in tongue carcinoma. Clin Cancer Res, 6, 4635-40.
  20. Hung KF, Chang CS, Liu CJ, et al (2006). Differential expression of E-cadherin in metastatic lesions comparing to primary oral squamous cell carcinoma. J Oral Pathol Med, 35, 589-94. https://doi.org/10.1111/j.1600-0714.2006.00474.x
  21. Irie A, Yamauchi A, Kontani K,et al (2005). Galectin-9 as a prognostic factor with antimetastatic potential in breast cancer. Clin Cancer Res, 11, 2962-8. https://doi.org/10.1158/1078-0432.CCR-04-0861
  22. Kageshita T, Kashio Y, Yamauchi A, et al (2002). Possible role of galectin-9 in cell aggregation and apoptosis of human melanoma cell lines and its clinical significance. Int J Cancer, 99, 809-16. https://doi.org/10.1002/ijc.10436
  23. Kasamatsu A, Uzawa K, Nakashima D, et al (2005). Galectin-9 as a regulator of cellular adhesion in human oral squamous cell carcinoma cell lines. Int J Mol Med, 16, 269-73.
  24. Kitawaki J, Kusuki I, Koshiba H, et al (1999). Detection of aromatase cytochrome P-450 in endometrial biopsy specimens as a diagnostic test for endometriosis. Fertil Steril, 72, 1100-6. https://doi.org/10.1016/S0015-0282(99)00424-0
  25. Leffler H, Carlsson S, Hedlund M, Qian Y, Poirier F (2004). Introduction to galectins. Glycoconj J, 19, 433-40.
  26. Li JJ, Zhang GH, Yang XM, et al (2012). Reduced E-cadherin expression is associated with lymph node metastases in laryngeal squamous cell carcinoma.
  27. Liang M, Ueno M, Oomizu S, et al (2008). Galectin-9 expression links to malignant potential of cervical squamous cell carcinoma. J Cancer Res Clin Oncol, 134, 899-907. https://doi.org/10.1007/s00432-008-0352-z
  28. Liu LK, Jiang XY, Zhou XX, et al (2010). 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, 23, 213-24. https://doi.org/10.1038/modpathol.2009.160
  29. Lopes FF, Da Costa Miguel MC, Pereira ALA, et al (2009). Changes in immunoexpression of E-cadherin and betacatenin in oral squamous cell carcinoma with and without nodal metastasis. Ann Diagn Pathol, 13, 22-9. https://doi.org/10.1016/j.anndiagpath.2008.07.006
  30. Mahomed F, Altini M, Meer S (2007). Altered E-cadherin/beta-catenin expression in oral squamous carcinoma with and without nodal metastasis. Oral Diseases, 13, 386-92. https://doi.org/10.1111/j.1601-0825.2006.01295.x
  31. Marsh R, Brackenbury R (1996). Molecules of cell adhesion and recognition: An overview. In: LEE, A. G. (ed.) Biomembranes: Receptors of cell adhesion and cellular recognition. JAI Press Inc.
  32. Matsumoto R, Matsumoto H, Seki M, et al (1998). Human ecalectin, a variant of human galectin-9, is a novel eosinophil chemoattractant produced by T lymphocytes. J Biol Chem, 273, 16976-84. https://doi.org/10.1074/jbc.273.27.16976
  33. Menezes MB, Lehn CN, Gon Alves AJ (2007). Epidemiological and histopathological data and E-cadherin-like prognostic factors in early carcinomas of the tongue and floor of mouth. Oral Oncology, 43, 656-61. https://doi.org/10.1016/j.oraloncology.2006.08.004
  34. Mostaan LV, Khorsandi MT, Sharifian SMR, et al (2011). Correlation between E-cadherin and CD44 adhesion molecules expression and cervical lymph node metastasis in oral tongue SCC: Predictive significance or not. Pathol Res Pract, 207, 448-51. https://doi.org/10.1016/j.prp.2011.04.001
  35. Murase N, Hosaka M, Takai Y, Tanimura T, Mori M (1985). Histochemical demonstration of lectinbinding sites and keratin in inflamed human gingiva. J Periodontal Res, 20, 625-36. https://doi.org/10.1111/j.1600-0765.1985.tb00847.x
  36. Nakahara S, Raz A (2008). Biological modulation by lectins and their ligands in tumor progression and metastasis. Anticancer Agents Med Chem, 8, 22-36. https://doi.org/10.2174/187152008783330833
  37. Neville BW, Day TA (2002). Oral cancer and precancerous lesions. CA Cancer J Clin, 52, 195-215 https://doi.org/10.3322/canjclin.52.4.195
  38. Nijkamp MM, Span PN, Hoogsteen IJ, et al (2011). Expression of E-cadherin and vimentin correlates with metastasis formation in head and neck squamous cell carcinoma patients. Radiother Oncol, 99, 344-8. https://doi.org/10.1016/j.radonc.2011.05.066
  39. Pioche-Durieu C, Keryer C, Souqu Re S, et al (2005). In nasopharyngeal carcinoma cells, Epstein-Barr virus LMP1 interacts with galectin 9 in membrane raft elements resistant to simvastatin. J Virol, 79, 13326-37. https://doi.org/10.1128/JVI.79.21.13326-13337.2005
  40. Rabinovich GA, Rubinstein N, Toscano MA (2002). Role of galectins in inflammatory and immunomodulatory processes. Biochim Biophys Acta, 1572, 274-84. https://doi.org/10.1016/S0304-4165(02)00314-8
  41. Rao SVK, Mejia G, Roberts-Thomson K, Logan R (2013). Epidemiology of oral cancer in Asia in the past decade- an update (2000-2012). Asian Pac J Cancer Prev, 14, 5567-77. https://doi.org/10.7314/APJCP.2013.14.10.5567
  42. Rosado P, Lequerica-Fernandez P, Fernandez S, et al 2013. E-cadherin and $\beta$-catenin expression in well-differentiated and moderately-differentiated oral squamous cell carcinoma: relations with clinical variables. Br J Oral Maxillofac Surg, 51, 149-56. https://doi.org/10.1016/j.bjoms.2012.03.018
  43. Sahu N, Grandis JR (2011). New advances in molecular approaches to head and neck squamous cell carcinoma. Anti-Cancer Drugs, 22, 656-64. https://doi.org/10.1097/CAD.0b013e32834249ba
  44. Saussez S, Camby I, Toubeau G and Kiss R (2007). Galectins as modulators of tumor progression in head and neck squamous cell carcinomas. Head & Neck, 29, 874-84. https://doi.org/10.1002/hed.20559
  45. Schipper JH, Frixen UH, Behrens J, et al (1991). E-cadherin expression in squamous cell carcinomas of head and neck: inverse correlation with tumor dedifferentiation and lymph node metastasis. Cancer Research, 51, 6328-37.
  46. Schneider PM, Baldus SE, Metzger R, et al (2005). Histomorphologic tumor regression and lymph node metastases determine prognosis following neoadjuvant radiochemotherapy for esophageal cancer: implications for response classification. Ann Surg, 242, 684-92. https://doi.org/10.1097/01.sla.0000186170.38348.7b
  47. Scully C, Bagan J (2009). Oral squamous cell carcinoma: overview of current understanding of aetiopathogenesis and clinical implications. Oral Diseases, 15, 388-99. https://doi.org/10.1111/j.1601-0825.2009.01563.x
  48. Smetana K Jr, Dvor Nkov B, Chovanec M, et al (2006). Nuclear presence of adhesion-/growth-regulatory galectins in normal/malignant cells of squamous epithelial origin. Histochem Cell Biol, 125, 171-82. https://doi.org/10.1007/s00418-005-0074-0
  49. Stewart BWW, Kleihues PI (2008). World cancer report, IARC Press.
  50. Suzuki T, Sadahiro S, Fukasawa M, et al (2004). Predictive factors of tumor shrinkage and histological regression in patients who received preoperative radiotherapy for rectal cancer. Jpn J Clin Oncol, 34, 740-6. https://doi.org/10.1093/jjco/hyh140
  51. Tanaka N, Odajima T, Ogi K, Ikeda T, Satoh M (2003). Expression of E-cadherin, alpha-catenin, and beta-catenin in the process of lymph node metastasis in oral squamous cell carcinoma. Br J Cancer, 89, 557-63. https://doi.org/10.1038/sj.bjc.6601124
  52. Ukpo OC, Thorstad WL, Zhang Q, Lewis JS Jr (2012). Lack of association of cadherin expression and histopathologic type, metastasis, or patient outcome in oropharyngeal squamous cell carcinoma: a tissue microarray study. Head Neck Pathol, 6, 38-47. https://doi.org/10.1007/s12105-011-0306-7
  53. Wang X, Zhang J, Fan M, et al (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, 547-54. https://doi.org/10.1016/j.tripleo.2008.11.021
  54. Woolgar JA (2006). Histopathological prognosticators in oral and oropharyngeal squamous cell carcinoma. Oral Oncol, 42, 229-39. https://doi.org/10.1016/j.oraloncology.2005.05.008
  55. Yamada K, Jordan R, Mori M, Speight PM (1997). The relationship between E-cadherin expression, clinical stage and tumour differentiation in oral squamous cell carcinoma. Oral Diseases, 3, 82-5.
  56. Zhao Z, Ge J, Sun Y, et al (2012). Is E-cadherin immunoexpression a prognostic factor for head and neck squamous cell carcinoma (HNSCC)? A systematic review and metaanalysis. Oral Oncol, 48, 761-7. https://doi.org/10.1016/j.oraloncology.2012.02.024
  57. Zhong LP, Li J, Zhang CP, et al (2007). Expression of E-cadherin in cervical lymph nodes from primary oral squamous cell carcinoma patients. Arch Oral Biol, 52, 740-7. https://doi.org/10.1016/j.archoralbio.2007.01.013

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