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01-03-2007 | Original Article

The expression of receptor for advanced glycation end products is associated with angiogenesis in human oral squamous cell carcinoma

Authors: Tomonori Sasahira, Tadaaki Kirita, Ujjal K. Bhawal, Masayuki Ikeda, Akira Nagasawa, Kazuhiko Yamamoto, Hiroki Kuniyasu

Published in: Virchows Archiv | Issue 3/2007

Abstract

The receptor for advanced glycation end products (RAGE) is associated with cancer progression in several human cancers. In this study, we examined the roles of RAGE in the angiogenesis of oral squamous cell carcinoma (OSCC). RAGE concentration was examined in 20 OSCC tumors by enzyme-linked immunosorbent assay (ELISA). The microvessel density (MVD) and lymph vessel density (LVD) were examined by immunostaining. Concentrations of vascular endothelial growth factor (VEGF) and VEGF-C were examined in tumor tissues by ELISA. Tumoral RAGE concentration was associated with higher tumor MVD (P = 0.0123) and tumor VEGF concentration (P = 0.0344), but not with LVD and VEGF-C concentration. Treatment with RAGE ligand, high-mobility group box (HMGB)-1 increased the secretion of VEGF but not that of VEGF-C in human OSCC cell lines, HSC-3 and HSC-4. The effect of HMGB-1 was abrogated by RAGE down-regulation by antisense S-oligodeoxynucleic acid. These results suggest that RAGE expression is closely associated to angiogenesis in OSCC.

Alcalde RE, Terakado N, Otsuki K, Matsumura T (1997) Angiogenesis and expression of platelet-derived endothelial cell growth factor in oral squamous cell carcinoma. Oncology 54:324–328PubMedCrossRef

Bhawal UK, Ozaki Y, Nishimura M, Sugiyama M, Sasaki N, Kuniyasu H, Kato Y (2005) Association of expression of receptors for advanced glycation end-products (RAGE) and invasive and metastatic activity of oral squamous cell carcinoma. Oncology 69:246–255PubMedCrossRef

Brownlee M (2000) Negative consequences of glycation. Metabolism 49:9–13PubMedCrossRef

Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K (1996) A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15:1751PubMed

Kaura J, Srivastava A, Ralhan R (1994) Overexpression of p53 protein in betel-and tobacco-related human oral dysplasia and squamous-cell carcinoma in India. Int J Cancer 58:340–345CrossRef

Kuniyasu H (2005) The molecular pathology of gastric cancer. In: Kuriyama S, Yoshiji H (eds) New perspectives in cancer research and therapy 2005. Research Signpost, Kerala, pp 85–98

Kuniyasu H, Chihara Y, Kondo H (2003) Differential effects between amphoterin and advanced glycation end products on colon cancer cells. Int J Cancer 104:722–727PubMedCrossRef

Kuniyasu H, Chihara Y, Kondo H, Ohmori H, Ukai R (2003) Amphoterin induction in prostatic stromal cells by androgen deprivation is associated with metastatic prostate cancer. Oncol Rep 10:1863–1868PubMed

Kuniyasu H, Chihara Y, Takahashi T (2003) Co-expression of receptor for advanced glycation end products and the ligand amphoterin associates closely with metastasis of colorectal cancer. Oncol Rep 10:445–448PubMed

10.

Kuniyasu H, Oue N, Wakikawa A, Shigeishi H, Matsutani N, Kuraoka K, Ito R, Yokozaki H, Yasui W (2002) Expression of receptors for advanced glycation end-products (RAGE) is closely associated with the invasive and metastatic activity of gastric cancer. J Pathol 196:163–170PubMedCrossRef

11.

Kuniyasu H, Tahara E (2001). Molecular pathology of esophageal cancer. In: Kelsen DP, Daly J, Kern S, Levin B, Tepper J (eds) Gastrointestinal oncology: principles and practices. Lippincott, Williams & Wilkins, Cherlottesville, pp 237–249

12.

Kuniyasu H, Yasui W, Shinohara H, Yano S, Ellis LM, Wilson MR, Bucana CD, Rikita T, Tahara E, Fidler IJ (2000) Induction of angiogenesis by hyperplastic colonic mucosa adjacent to colon cancer. Am J Pathol 157:1523–1535PubMed

13.

Li C, Shintani S, Terakado N, Klosek SK, Ishikawa T, Nakashiro K, Hamakawa H (2005) Microvessel density and expression of vascular endothelial growth factor, basic fibroblast growth factor, and platelet-derived endothelial growth factor in oral squamous cell carcinomas. Int J Oral Maxillofac Surg 34:559–565PubMedCrossRef

14.

Lopez-Graniel CM, Tamez de Leon D, Meneses-Garcia A, Gomez-Ruiz C, Frias-Mendivil M, Granados-Garcia M, Barrera-Franco JL (2001) Tumor angiogenesis as a prognostic factor in oral cavity carcinomas. J Exp Clin Cancer Res 20:463–468PubMed

15.

Melloni E, Sparatore B, Patrone M, Pessino A, Passalacqua M, Pontremoli S (1995) Identity in molecular structure between “differentiation enhancing factor” of murine erythroleukemia cells and the 30 kD heparin-binding protein of developing rat brain. Biochem Biophys Res Commun 210:82–89PubMedCrossRef

16.

Miyata Y, Kanda S, Ohba K, Nomata K, Hayashida Y, Eguchi J, Hayashi T, Kanetake H (2006) Lymphangiogenesis and angiogenesis in bladder cancer: prognostic implications and regulation by vascular endothelial growth factors-A, -C, and -D. Clin Cancer Res 12:800–806PubMedCrossRef

17.

Nagler RM (2002) Molecular aspects of oral cancer. Anticancer Res 22:2977–2980PubMed

18.

Nakazato T, Shingaki S, Kitamura N, Saito C, Kuwano R, Tachibana M (2006) Expression level of vascular endothelial growth factor-C and -A in cultured human oral squamous cell carcinoma correlates respectively with lymphatic metastasis and angiogenesis when transplanted into nude mouse oral cavity. Oncol Rep 15:825–830PubMed

19.

Okamoto T, Yamagishi S, Inagaki Y, Amano S, Koga K, Abe R, Takeuchi M, Ohno S, Yoshimura A, Makita Z (2002) Angiogenesis induced by advanced glycation end products and its prevention by cerivastatin. FASEB J 16:1928–1930PubMed

20.

Parkin DM, Bray F, Ferlay J, Pisani P (2001) Estimating the world cancer burden: Globocan 2000. Int J Cancer 94:135–156CrossRef

21.

Paterson IC, Eveson JW, Prime SS (1996) Molecular changes in oral cancer may reflect and ethnic origin. Eur J Cancer B Oral Oncol 32B:150–153PubMedCrossRef

22.

Sasahira T, Akama Y, Fujii K, Kuniyasu H (2005) Expression of receptor for advanced glycation end products and HMGB1/amphoterin in colorectal adenomas. Virchows Arch 446:411–415PubMedCrossRef

23.

Sawair FA, Irwin CR, Gordon DJ, Leonard AG, Stephenson M, Napier SS (2003) Invasive front grading: reliability and usefulness in the management of oral squamous cell carcinoma. J Oral Pathol Med 32:1–9PubMedCrossRef

24.

Schliephake H (2003) Prognostic relevance of molecular markers of oral cancer—a review. Int J Oral Maxillofac Surg 32:233–245PubMedCrossRef

25.

Schraml P, Shipman R, Colombi M, Ludwig CU (1994) Identification of genes differentially expressed in normal lung and non-small cell lung carcinoma tissue. Cancer Res 54:5236–5240PubMed

26.

Shang ZJ, Li ZB, Li JR (2005) VEGF is up-regulated by hypoxic stimulation and related to tumour angiogenesis and severity of disease in oral squamous cell carcinoma: in vitro and in vivo studies. Int J Oral Maxillofac Surg 35:533–538CrossRef

27.

Shayan R, Achen MG, Stacker SA (2006) Lymphatic vessels in cancer metastasis: bridging the gaps. Carcinogenesis 27:1729–1738PubMedCrossRef

28.

Shintani S, Li C, Ishikawa T, Mihara M, Nakashiro K, Hamakawa H (2004) Expression of vascular endothelial growth factor A, B, C, and D in oral squamous cell carcinoma. Oral Oncol 40:13–20PubMedCrossRef

29.

Sobin LH, Wittekind C (2003) UICC TNM classification of malignant tumours. Wiley, New York

30.

Treins C, Giorgetti-Peraldi S, Murdaca J, Van Obberghen E (2001) Regulation of vascular endothelial growth factor expression by advanced glycation end products. J Biol Chem 276:43836–43841PubMedCrossRef

31.

Tsai PW, Shiah SG, Lin MT, Wu CW, Kuo ML (2003) Up-regulation of vascular endothelial growth factor C in breast cancer cells by heregulin-β1. A critical role of p38/nuclear factor-κ B signaling pathway. J Biol Chem 278:5750–5759PubMedCrossRef

32.

Watanabe H, Iwase M, Ohashi M, Nagumo M (2002) Role of interleukin-8 secreted from human oral squamous cell carcinoma cell lines. Oral Oncol 38:670–679PubMedCrossRef

33.

WHO (1988) International histological classification of tumours. Springer, Berlin Heidelberg New York

34.

Yamagishi S, Takeuchi M, Inagaki Y, Nakamura K, Imaizumi T (2003) Role of advanced glycation end products (AGEs) and their receptor (RAGE) in the pathogenesis of diabetic microangiopathy. Int J Clin Pharmacol Res 23:129–134PubMed

35.

Yamamoto Y, Yamagishi S, Yonekura H, Doi T, Tsuji H, Kato I, Takasawa S, Okamoto H, Abedin J, Tanaka N, Sakurai S, Migita H, Unoki H, Wang H, Zenda T, Wu PS, Segawa Y, Higashide T, Kawasaki K, Yamamoto H (2000) Roles of the AGE–RAGE system in vascular injury in diabetes. Ann NY Acad Sci 902:163–170PubMedCrossRef

Title: The expression of receptor for advanced glycation end products is associated with angiogenesis in human oral squamous cell carcinoma
Authors: Tomonori Sasahira
Tadaaki Kirita
Ujjal K. Bhawal
Masayuki Ikeda
Akira Nagasawa
Kazuhiko Yamamoto
Hiroki Kuniyasu
Publication date: 01-03-2007
Publisher: Springer-Verlag
Published in: Virchows Archiv / Issue 3/2007
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI: https://doi.org/10.1007/s00428-006-0359-2

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The expression of receptor for advanced glycation end products is associated with angiogenesis in human oral squamous cell carcinoma

Abstract

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Abstract

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