Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
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Relationships Between Clinical Behavior of Laryngeal Squamous Cell Carcinomas and Expression of VEGF, MMP-9 and E-Cadherin

  • Akdeniz, Onder (Department of Otorhinolaryngology, Bursa SevketYilmaz Training and Research Hospital) ;
  • Akduman, Davut (Department of Otorhinolaryngology, Bursa SevketYilmaz Training and Research Hospital) ;
  • Haksever, Mehmet (Department of Otorhinolaryngology, Bursa SevketYilmaz Training and Research Hospital) ;
  • Ozkarakas, Haluk (Department of Otorhinolaryngology, Acibadem University, Kadikoy Acibadem Hospital) ;
  • Muezzinoglu, Bahar (Department of Pathology, Kocaeli University, School of Medicine)
  • Published : 2013.09.30
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Abstract

The biological mechanisms of cancer and associations with behavior of tumours need to be studied to understand progression and determine appropriate treatments. Here we investigated expression of VEGF, MMP-9 and E-cadherin in laryngeal SCCs and their relations with clinical behavior. This prospective study was based on 38 surgical specimens from patients with primary laryngeal SCC and data recorded in their cards. Expression of the three factors in tumor tissue was examined using immunohistochemistry and correlations with clinical parameters of primary tumors, regional lymph node metastases, stage of disease, histopathologic differentiation, and vascular/cartilage invasion were investigated. Regarding the cases with positive MMP-9 expression, the difference between well and moderately/poorly differentiated tumors was statistically significant. However, differences between early stage (stage I and II) and late-stage (stage III and IV) tumours, and between positive and negative for pLN metastasis were not. No significant relationship between positive VEGF and tumor differentiation or stage was apparent, but E-cadherin levels significantly differed between well and moderately/poorly differentiated tumours and with the presence of pLN metastasis. E-cadherin staining did not vary between MMP-9 positive and negative cases. In conclusion, MMP-9 may be a negative predictor of differentiation in laryngeal SCC, while E-cadherin is a predictor of differentiation and nodal metastases. Even if the difference between VEGF expression and tumor stage was not statistically significant, it seems that there exists some relationship, which might be clarified with a greater number of cases.

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References

  1. Acs G, Lawton TJ, Rebbeck TR, LiVolsi VA, Zhang PJ (2001). Differential expression of E-cadherin in lobular and ductal neoplasms of the breast and its biologic and diagnostic implications. Am J ClinPathol, 115, 85-98.
  2. Andrews NA, Jones AS, Helliwell TR, Kinsella AR (1997). Expression of the E-cadherin-catenin cell adhesion complex in primary squamous cell carcinomas of the head and neck and their nodal metastases. Br J Cancer, 75, 1474-80. https://doi.org/10.1038/bjc.1997.252
  3. Bagutti C, Speight PM, Watt FM (1998). Comparison of integrin, cadherin, and catenin expression in squamous cell carcinomas of the oral cavity. J Pathol, 186, 8-16. https://doi.org/10.1002/(SICI)1096-9896(199809)186:1<8::AID-PATH156>3.0.CO;2-H
  4. Basset P, Bellocq JP, Wolf C, et al (1990). A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature, 348, 699-704. https://doi.org/10.1038/348699a0
  5. Behrens J, Mareel MM, Van Roy FM, Birchmeier W (1989). Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. J Cell Biol, 108, 2435-47. https://doi.org/10.1083/jcb.108.6.2435
  6. Behrens J (1994). Cadherins as determinants of tissue morphology and suppressors of invasion. ActaAnat (Basel), 149, 165-9. https://doi.org/10.1159/000147572
  7. Berx G, Van Roy F (2001). The E-cadherin/catenin complex: an important gatekeeper in breast cancer tumorigenesis and malignant progression. Breast Cancer Res, 3, 289-93. https://doi.org/10.1186/bcr309
  8. Borgstrom P, Hillan KJ, Sriramarao P, Ferrara N (1996). Complete inhibition of angiogenesis and growth of microtumors by anti-vascular endothelial growth factor neutralizing antibody: novel concepts of angiostatic therapy from intravital videomicroscopy. Cancer Res, 56, 4032-9.
  9. Cavallaro U, Christofori G (2004). Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer, 4, 118-32. https://doi.org/10.1038/nrc1276
  10. Charous SJ, Stricklin GP, Nanney LB, Netterville JL, Burkey BB (1997). Expression of matrix metalloproteinases and tissue inhibitor of metalloproteinases in head and neck squamous cell carcinoma. Ann Otol Rhinol Laryngol, 106, 271-8. https://doi.org/10.1177/000348949710600402
  11. Colovic Z, Pesutic-Pisac V, Poljak NK, et al (2013). Expression of matrix metalloproteinase-9 in patients with squamous cell carcinoma of the larynx. CollAntropol, 37, 151-5.
  12. Crissman JD, Zarbo RJ (1990). Squamous cell carcinoma of the upper aerodigestive tract: histologic parameters with prognostic value. In: Fee W.E. Jr, Goepfert H, Johans ME. et al (eds). Head and Neck Cancer, Vol. 2, Decker, Toronto.
  13. Dutta A, Sen T, Chatterjee A (2010). All-trans retinoic acid (ATRA) downregulates MMP-9 by modulating its regulatory molecules. Cell Adh Migr, 4, 409-18. https://doi.org/10.4161/cam.4.3.11682
  14. Eidelman S, Damsky CH, Wheelock MJ, Damjanov I (1989). Expression of the cell-cell adhesion glycoprotein cell-CAM 120/80 in normal human tissues and tumors. Am J Pathol, 135, 101-10.
  15. Eisma RJ, Spiro JD, Kreutzer DL (1999). Role of angiogenic factors: coexpression of interleukin-8 and vascular endothelial growth factor in patients with head and neck squamous carcinoma. Laryngoscope, 109, 687-93. https://doi.org/10.1097/00005537-199905000-00002
  16. Ferrara N, Davis-Smyth T (1997). The biology of vascular endothelial growth factor. Endocr Rev, 18, 4-25. https://doi.org/10.1210/edrv.18.1.0287
  17. FrigugliettI CU, Mello ES, Castro IV, Filho GB, Alves VA (2000). Metalloproteinase-9 immunoexpression and angiogenesis in thyroid follicular neoplasms: relation to clinical and histopathologic features. Head Neck, 22, 373-9. https://doi.org/10.1002/1097-0347(200007)22:4<373::AID-HED10>3.0.CO;2-H
  18. Frixen UH, Behrens J, Sachs M, et al (1991). E-cadherinmediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol, 113, 173-85. https://doi.org/10.1083/jcb.113.1.173
  19. Folkman J (1990). What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst, 82, 4-6. https://doi.org/10.1093/jnci/82.1.4
  20. Gerrow K, El-Husseini A (2006). Cell adhesion molecules at the synapse. Front Biosci, 11, 2400-19. https://doi.org/10.2741/1978
  21. Gupta K, Kshirsagar S, Li W, et al (1999). VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exp Cell Res, 247, 495-504. https://doi.org/10.1006/excr.1998.4359
  22. Haksever M, Inancli HM, Tuncel U, et al (2012). The effects of tumor size, degree of differentiation, and depth of invasion on the risk of neck node metastasis in squamous cell carcinoma of the oral cavity. Ear Nose Throat J, 91, 130-5.
  23. Hermanek P, Sobin LH (1997). UICC TNM Classification Of Malignant Tumors, 5th ed. New York, John Wiley
  24. Hiraki A, Shinohara M, Ikebe T, et al (1996). Immunohistochemical staining of desmosomal components in oral squamous cell carcinomas and its association with tumour behaviour. Br J Cancer, 73, 1491-7. https://doi.org/10.1038/bjc.1996.282
  25. Hong SD, Hong SP, Lee JI, Lim CY (2000). Expression of matrix metalloproteinase-2 and-9 in oral squamous cell carcinomas with regard to the metastatic potential. Oral Oncol, 36, 207-13. https://doi.org/10.1016/S1368-8375(99)00088-3
  26. Howlader N, Noone AM, Krapcho M, et al (2011). National Cancer Institute. Bethesda, MD. based on November 2011 SEER data submission, posted to the SEER web site, April 2012.
  27. Jakobsson PA, Eneroth CM, Killander D, Moberger G, Martensson B (1973). Histologic classification and grading of malignancy in carcinoma of the larynx. Acta Radiol Ther Phys Biol, 12, 1-8. https://doi.org/10.3109/02841867309131085
  28. Jakobsson PA (1975). Histologic grading of malignancy and prognosis in glottic carcinoma of the larynx. Can J Otolaryngol, 4, 885-92.
  29. Jawhari AU, Farthing MJ, Pignatelli M (1999). The E-cadherin/ epidermal growth factor receptor interaction: a hypothesis of reciprocal and reversible control of intercellular adhesion and cell proliferation. J Pathol, 187, 155-7. https://doi.org/10.1002/(SICI)1096-9896(199901)187:2<155::AID-PATH193>3.0.CO;2-E
  30. Kaomongkolgit R, Cheepsunthorn P, Pavasant P, Sanchavanakit N (2008). Iron increases MMP-9 expression through activation of AP-1 via ERK/Akt pathway in human head and neck squamous carcinoma cells. Oral Oncol, 44, 587-94. https://doi.org/10.1016/j.oraloncology.2007.08.005
  31. Kim KJ, Li B, Winer J, et al (1993). Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature, 362, 841-4. https://doi.org/10.1038/362841a0
  32. Klagsbrun M, Soker S (1993). VEGF/VPF: the angiogenesis factor found? Curr Biol, 3, 699-702. https://doi.org/10.1016/0960-9822(93)90073-W
  33. Klein T, Bischoff R (2011). Physiology and pathophysiology of matrix metalloproteases. Amino Acids, 41, 271-90. https://doi.org/10.1007/s00726-010-0689-x
  34. Kugler A, Hemmerlein B, Thelen P, et al (1998). Expression of metalloproteinase 2 and 9 and their inhibitors in renal cell carcinoma. J Urol, 160, 1914-8. https://doi.org/10.1016/S0022-5347(01)62443-1
  35. Kusukawa J, Sasaguri Y, Shima I, Kameyama T, Morimatsu M (1993). Expression of matrix metalloproteinase-2 related to lymph node metastasis of oral squamous cell carcinoma. A clinicopathologic study. Am J Clin Pathol, 99, 18-23. https://doi.org/10.1093/ajcp/99.1.18
  36. Kyzas PA, Stefanou D, Agnantis NJ (2004). Immunohistochemical expression of vascular endothelial growth factor correlates with positive surgical margins and recurrence in T1 and T2 squamous cell carcinoma (SCC) of the lower lip. Oral Oncol, 40, 941-7. https://doi.org/10.1016/j.oraloncology.2004.04.018
  37. Mareel M, Oliveira MJ, Madani I (2009). Cancer invasion and metastasis: interacting ecosystems. Virchows Arch, 454, 599-622. https://doi.org/10.1007/s00428-009-0784-0
  38. Mattijssen V, Peters HM, Schalkwijk L, et al (1993). E-cadherin expression in head and neck squamous-cell carcinoma is associated with clinical outcome. Int J Cancer, 55, 580-5. https://doi.org/10.1002/ijc.2910550411
  39. Mineta H, Miura K, Ogino T, et al (2000). Prognostic value of vascular endothelial growth factor (VEGF) in head and neck squamous cell carcinomas. Br J Cancer, 83, 775-81. https://doi.org/10.1054/bjoc.2000.1357
  40. Miyajima Y, Nakano R, Morimatsu M (1995). Analysis of expression of matrix metalloproteinases-2 and -9 in hypopharyngeal squamous cell carcinoma by in situ hybridization. Ann Otol Rhinol Laryngol, 104, 678-84. https://doi.org/10.1177/000348949510400902
  41. Mook ORF, Frederiks WM, Noorden CV (2004). The role of gelatinases in colorectal metastasis. Biochim Biophys Acta, 1705, 69-89.
  42. Nagafuchi A, Takeichi M (1989). Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell Regul, 1, 37-44.
  43. Navarro P, Gomez M, Pizarro A, et al (1991). A role for the E-cadherin cell-cell adhesion molecule during tumor progression of mouse epidermal carcinogenesis. J Cell Biol, 115, 517-33. https://doi.org/10.1083/jcb.115.2.517
  44. 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
  45. Nollet F, Kools P, van Roy F (2000). Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol, 299, 551-72. https://doi.org/10.1006/jmbi.2000.3777
  46. Page-McCaw A, Ewald AJ, Werb Z (2007). Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol, 8, 221-33. https://doi.org/10.1038/nrm2125
  47. Peralta Soler A, Knudsen KA, Tecson-Miguel A, et al (1997). Expression of E-cadherin and N-cadherin in surface epithelial-stromal tumors of the ovary distinguishes mucinous from serous and endometrioid tumors. Hum Pathol, 28, 734-9. https://doi.org/10.1016/S0046-8177(97)90184-2
  48. Pilch BZ, Dorfman DM, Brodsky GL (1996). Goodman M. Pathology of laryngeal malignancies. In: Fried MP. ed. The larynx; A multidisciplinary Approach. 2nd ed. St Louis, CV Mosby, 425-36
  49. Roomi MW, Monterrey JC, Kalinovsky T, Rath M, Niedzwiecki A (2009). Distinct patterns of matrix metalloproteinase-2 and -9 expression in normal human cell lines. Oncol Rep, 21, 821-6.
  50. 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
  51. Sato F, Shimada Y, Watanabe G, et al (1999). Expression of vascular endothelial growth factor, matrix metalloproteinase-9 and E-cadherin in the process of lymph node metastasis in oesophageal cancer. Br J Cancer, 80, 1366-72. https://doi.org/10.1038/sj.bjc.6690530
  52. Shima I, Sasaguri Y, Kusukawa J, et al (1992). Production of matrix metalloproteinase-2 and metalloproteinase-3 related to malignant behavior of esophageal carcinoma. A clinicopathologic study. Cancer, 70, 2747-53. https://doi.org/10.1002/1097-0142(19921215)70:12<2747::AID-CNCR2820701204>3.0.CO;2-5
  53. Shiozaki H, Tahara H, Oka H, et al (1991). Expression of immunoreactive E-cadherin adhesion molecules in human cancers. Am J Pathol, 139, 17-23.
  54. Stell PM (1990). Prognosis in laryngeal carcinoma: tumour factors. Clin Otolaryngol Allied Sci, 15, 69-81. https://doi.org/10.1111/j.1365-2273.1990.tb00436.x
  55. Takeichi M (1991). Cadherin cell adhesion receptors as a morphogenetic regulator. Science, 251, 1451-5. https://doi.org/10.1126/science.2006419
  56. Talvensaari-Mattila A, Turpeenniemi-Hujanen T. (2005). Preoperative serum MMP-9 immunoreactive protein is a prognostic indicator for relapse-free survival in breast carcinoma. Cancer Lett, 217, 237-42. https://doi.org/10.1016/j.canlet.2004.06.056
  57. Wakisaka N, Wen QH, Yoshizaki T, et al (1999). Association of vascular endothelial growth factor expression with angiogenesis and lymph node metastasis in nasopharyngeal carcinoma. Laryngoscope, 109, 810-4. https://doi.org/10.1097/00005537-199905000-00024
  58. Wang Z, Chen Y, Li X, et al (2012). Expression of VEGF-C/ VEGFR-3 in human laryngeal squamous cell carcinomas and its significance for lymphatic metastasis. Asian Pac J Cancer Prev, 13, 27-31. https://doi.org/10.7314/APJCP.2012.13.1.027
  59. Viros D, Camacho M, Zarraonandia I, et al (2013). Prognostic role of MMP-9 expression in head and neck carcinoma patients treated with radiotherapy or chemoradiotherapy. Oral Oncol, 49, 322-5. https://doi.org/10.1016/j.oraloncology.2012.10.005
  60. Zhao YG, Xiao AZ, Ni J, Man YG, Sang QX (2009). Expression of matrix metalloproteinase-26 in multiple human cancer tissues and smooth muscle cells. Ai Zheng, 28, 1168-75.
  61. Zhongliang W, Yao C, Rueixiang L (2002). Advanced in the researches for vascular endothelial growth factor (VEGF)-C and vascular endothelial growth factor receptor (VEGFR)-3. China J Cancer Prev Treat, 9, 454.

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