Skip to main content
Erschienen in: Journal of Cancer Research and Clinical Oncology 7/2009

01.07.2009 | Original Paper

Down-regulation of plasma membranous Annexin A1 protein expression in premalignant and malignant lesions of the oral cavity: correlation with epithelial differentiation

verfasst von: Hitomi Nomura, Katsuhiro Uzawa, Yukio Yamano, Kazuaki Fushimi, Dai Nakashima, Yukinao Kouzu, Atsushi Kasamatsu, Katsunori Ogawara, Masashi Shiiba, Hiroki Bukawa, Hidetaka Yokoe, Hideki Tanzawa

Erschienen in: Journal of Cancer Research and Clinical Oncology | Ausgabe 7/2009

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To determine the potential involvement of ANXA1 in oral squamous-cell carcinoma (OSCC), we evaluated the ANXA1 protein expression in oral premalignant lesions (OPLs) and OSCCs and correlated the results with clinicopathologic variables.

Methods

Matched normal and tumour specimens of 44 primary OSCCs and 28 OPLs were analyzed for ANXA1 subcellular localization and protein expression level by immunohistochemistry (IHC). Correlations between ANXA1-IHC staining scores of OSCCs and clinicopathologic features were evaluated by Fisher’s exact test.

Results

Markedly down-regulation of ANXA1 protein expression was identified on the plasma membrane of epithelial cells in OSCCs (P < 0.001) and OPLs (P = 0.001) compared with normal counterparts. Moreover, loss of plasma membranous ANXA1 expression was significantly correlated with the poorly differentiated status of OSCC cells (P = 0.012).

Conclusions

Our findings suggest that loss of ANXA1 is frequent and early event during oral carcinogenesis and that ANXA1 could contribute to maintaining epithelial differentiation in OSCC.
Literatur
Zurück zum Zitat Alldridge LC, Bryant CE (2003) Annexin 1 regulates cell proliferation by disruption of cell morphology and inhibition of cyclin D1 expression through sustained activation of the ERK1/2 MAPK signal. Exp Cell Res 290:93–107. doi:10.1016/S0014-4827(03)00310-0 PubMedCrossRef Alldridge LC, Bryant CE (2003) Annexin 1 regulates cell proliferation by disruption of cell morphology and inhibition of cyclin D1 expression through sustained activation of the ERK1/2 MAPK signal. Exp Cell Res 290:93–107. doi:10.​1016/​S0014-4827(03)00310-0 PubMedCrossRef
Zurück zum Zitat Bai XF, Ni XG, Zhao P, Liu SM, Wang HX, Guo B, Zhou LP, Liu F, Zhang JS, Wang K, Xie YQ, Shao YF, Zhao XH (2004) Overexpression of annexin 1 in pancreatic cancer and its clinical significance. World J Gastroenterol 10:1466–1470PubMed Bai XF, Ni XG, Zhao P, Liu SM, Wang HX, Guo B, Zhou LP, Liu F, Zhang JS, Wang K, Xie YQ, Shao YF, Zhao XH (2004) Overexpression of annexin 1 in pancreatic cancer and its clinical significance. World J Gastroenterol 10:1466–1470PubMed
Zurück zum Zitat Bilalovic N, Sandstad B, Golouh R, Nesland JM, Selak I, Torlakovic EE (2004) CD10 protein expression in tumor and stromal cells of malignant melanoma is associated with tumor progression. Mod Pathol 17:1251–1258. doi:10.1038/modpathol.3800174 PubMedCrossRef Bilalovic N, Sandstad B, Golouh R, Nesland JM, Selak I, Torlakovic EE (2004) CD10 protein expression in tumor and stromal cells of malignant melanoma is associated with tumor progression. Mod Pathol 17:1251–1258. doi:10.​1038/​modpathol.​3800174 PubMedCrossRef
Zurück zum Zitat de Coupade C, Gillet R, Bennoun M, Briand P, Russo-Marie F, Solito E (2000) Annexin 1 expression and phosphorylation are upregulated during liver regeneration and transformation in antithrombin III SV40 T large antigen transgenic mice. Hepatology 31:371–380. doi:10.1002/hep.510310217 PubMedCrossRef de Coupade C, Gillet R, Bennoun M, Briand P, Russo-Marie F, Solito E (2000) Annexin 1 expression and phosphorylation are upregulated during liver regeneration and transformation in antithrombin III SV40 T large antigen transgenic mice. Hepatology 31:371–380. doi:10.​1002/​hep.​510310217 PubMedCrossRef
Zurück zum Zitat Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371PubMed Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371PubMed
Zurück zum Zitat Goulding NJ, Godolphin JL, Sampson MB, Maddison PJ, Flower RJ (1990) Hydrocortisone induces lipocortin 1 production by peripheral blood mononuclear cells in vivo in man. Biochem Soc Trans 18:306–307PubMed Goulding NJ, Godolphin JL, Sampson MB, Maddison PJ, Flower RJ (1990) Hydrocortisone induces lipocortin 1 production by peripheral blood mononuclear cells in vivo in man. Biochem Soc Trans 18:306–307PubMed
Zurück zum Zitat Guzmán-Aránguez A, Olmo N, Turnay J, Lecona E, Pérez-Ramos P, López de Silanes I, Lizarbe MA (2005) Differentiation of human colon adenocarcinoma cells alters the expression and intracellular localization of annexins A1, A2, and A5. J Cell Biochem 94:178–193. doi:10.1002/jcb.20293 PubMedCrossRef Guzmán-Aránguez A, Olmo N, Turnay J, Lecona E, Pérez-Ramos P, López de Silanes I, Lizarbe MA (2005) Differentiation of human colon adenocarcinoma cells alters the expression and intracellular localization of annexins A1, A2, and A5. J Cell Biochem 94:178–193. doi:10.​1002/​jcb.​20293 PubMedCrossRef
Zurück zum Zitat Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:585–587. doi:10.1093/nar/gkm259 CrossRef Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:585–587. doi:10.​1093/​nar/​gkm259 CrossRef
Zurück zum Zitat Hu N, Flaig MJ, Su H, Shou JZ, Roth MJ, Li WJ, Wang C, Goldstein AM, Li G, Emmert-Buck MR, Taylor PR (2004) Comprehensive characterization of annexin I alterations in esophageal squamous-cell carcinoma. Clin Cancer Res 10:6013–6022. doi:10.1158/1078-0432.CCR-04-0317 PubMedCrossRef Hu N, Flaig MJ, Su H, Shou JZ, Roth MJ, Li WJ, Wang C, Goldstein AM, Li G, Emmert-Buck MR, Taylor PR (2004) Comprehensive characterization of annexin I alterations in esophageal squamous-cell carcinoma. Clin Cancer Res 10:6013–6022. doi:10.​1158/​1078-0432.​CCR-04-0317 PubMedCrossRef
Zurück zum Zitat Kang SA, Cho YJ, Moon HB, Na DS (1996) Translocation of lipocortin (annexin) 1 to the membrane of U937 cells induced by phorbol ester, but not by dexamethasone. Br J Pharmacol 117:1780–1784PubMed Kang SA, Cho YJ, Moon HB, Na DS (1996) Translocation of lipocortin (annexin) 1 to the membrane of U937 cells induced by phorbol ester, but not by dexamethasone. Br J Pharmacol 117:1780–1784PubMed
Zurück zum Zitat Kang JS, Calvo BF, Maygarden SJ, Caskey LS, Mohler JL, Ornstein DK (2002) Dysregulation of annexin I protein expression in high-grade prostatic intraepithelial neoplasia and prostate cancer. Clin Cancer Res 8:117–123PubMed Kang JS, Calvo BF, Maygarden SJ, Caskey LS, Mohler JL, Ornstein DK (2002) Dysregulation of annexin I protein expression in high-grade prostatic intraepithelial neoplasia and prostate cancer. Clin Cancer Res 8:117–123PubMed
Zurück zum Zitat Koike H, Uzawa K, Nakashima D, Shimada K, Kato Y, Higo M, Kouzu Y, Endo Y, Kasamatsu A, Tanzawa H (2005) Identification of differentially expressed proteins in oral squamous cell carcinoma using a global proteomic approach. Int J Oncol 27:59–67PubMed Koike H, Uzawa K, Nakashima D, Shimada K, Kato Y, Higo M, Kouzu Y, Endo Y, Kasamatsu A, Tanzawa H (2005) Identification of differentially expressed proteins in oral squamous cell carcinoma using a global proteomic approach. Int J Oncol 27:59–67PubMed
Zurück zum Zitat Lin CY, Jeng YM, Chou HY, Hsu HC, Yuan RH, Chiang CP, Kuo MY (2008) Nuclear localization of annexin A1 is a prognostic factor in oral squamous cell carcinoma. J Surg Oncol 97:544–550. doi:10.1002/jso.20992 PubMedCrossRef Lin CY, Jeng YM, Chou HY, Hsu HC, Yuan RH, Chiang CP, Kuo MY (2008) Nuclear localization of annexin A1 is a prognostic factor in oral squamous cell carcinoma. J Surg Oncol 97:544–550. doi:10.​1002/​jso.​20992 PubMedCrossRef
Zurück zum Zitat Masaki T, Tokuda M, Ohnishi M, Watanabe S, Fujimura T, Miyamoto K, Itano T, Matsui H, Arima K, Shirai M, Maeba T, Sogawa K, Konishi R, Taniguchi K, Hatanaka Y, Hatase O, Nishioka M (1996) Enhanced expression of the protein kinase substrate annexin in human hepatocellular carcinoma. Hepatology 24:72–81PubMed Masaki T, Tokuda M, Ohnishi M, Watanabe S, Fujimura T, Miyamoto K, Itano T, Matsui H, Arima K, Shirai M, Maeba T, Sogawa K, Konishi R, Taniguchi K, Hatanaka Y, Hatase O, Nishioka M (1996) Enhanced expression of the protein kinase substrate annexin in human hepatocellular carcinoma. Hepatology 24:72–81PubMed
Zurück zum Zitat McCarty KS Jr, Szabo E, Flowers JL, Cox EB, Leight GS, Miller L, Konrath J, Soper JT, Budwit DA, Creasman WT, Seigler HF, McCarty KS Sr (1986) Use of monoclonal anti-estrogen receptor antibody in the immunohistochemical evaluation of human tumors. Cancer Res 46:4244–4248 McCarty KS Jr, Szabo E, Flowers JL, Cox EB, Leight GS, Miller L, Konrath J, Soper JT, Budwit DA, Creasman WT, Seigler HF, McCarty KS Sr (1986) Use of monoclonal anti-estrogen receptor antibody in the immunohistochemical evaluation of human tumors. Cancer Res 46:4244–4248
Zurück zum Zitat Paweletz CP, Ornstein DK, Roth MJ, Bichsel VE, Gillespie JW, Calvert VS, Vocke CD, Hewitt SM, Duray PH, Herring J, Wang QH, Hu N, Linehan WM, Taylor PR, Liotta LA, Emmert-Buck MR, Petricoin EF 3rd (2000) Loss of annexin 1 correlates with early onset of tumorigenesis in esophageal and prostate carcinoma. Cancer Res 60:6293–6297PubMed Paweletz CP, Ornstein DK, Roth MJ, Bichsel VE, Gillespie JW, Calvert VS, Vocke CD, Hewitt SM, Duray PH, Herring J, Wang QH, Hu N, Linehan WM, Taylor PR, Liotta LA, Emmert-Buck MR, Petricoin EF 3rd (2000) Loss of annexin 1 correlates with early onset of tumorigenesis in esophageal and prostate carcinoma. Cancer Res 60:6293–6297PubMed
Zurück zum Zitat Pedrero JMG, Fernandez MP, Morgan RO, Herrero Zapatero A, Gonzalez MV, Suarez Nieto C, Rodrigo JP (2004) Annexin A1 down-regulation in head and neck cancer is associated with epithelial differentiation status. Am J Pathol 164:73–79 Pedrero JMG, Fernandez MP, Morgan RO, Herrero Zapatero A, Gonzalez MV, Suarez Nieto C, Rodrigo JP (2004) Annexin A1 down-regulation in head and neck cancer is associated with epithelial differentiation status. Am J Pathol 164:73–79
Zurück zum Zitat Rodrigo JP, Garcia-Pedrero JM, Fernandez MP, Morgan RO, Suárez C, Herrero A (2005) Annexin A1 expression in nasopharyngeal carcinoma correlates with squamous differentiation. Am J Rhinol 19:483–487PubMed Rodrigo JP, Garcia-Pedrero JM, Fernandez MP, Morgan RO, Suárez C, Herrero A (2005) Annexin A1 expression in nasopharyngeal carcinoma correlates with squamous differentiation. Am J Rhinol 19:483–487PubMed
Zurück zum Zitat Shen D, Nooraie F, Elshimali Y, Lonsberry V, He J, Bose S, Chia D, Seligson D, Chang HR, Goodglick L (2006) Decreased expression of annexin A1 is correlated with breast cancer development and progression as determined by a tissue microarray analysis. Hum Pathol 37:1583–1591. doi:10.1016/j.humpath.2006.06.001 PubMedCrossRef Shen D, Nooraie F, Elshimali Y, Lonsberry V, He J, Bose S, Chia D, Seligson D, Chang HR, Goodglick L (2006) Decreased expression of annexin A1 is correlated with breast cancer development and progression as determined by a tissue microarray analysis. Hum Pathol 37:1583–1591. doi:10.​1016/​j.​humpath.​2006.​06.​001 PubMedCrossRef
Zurück zum Zitat Sinha P, Hutter G, Kottgen E, Dietel M, Schadendorf D, Lage H (1998) Increased expression of annexin I and thioredoxin detected by two-dimensional gel electrophoresis of drug resistant human stomach cancer cells. J Biochem Biophys Methods 37:105–116. doi:10.1016/S0165-022X(98)00020-7 PubMedCrossRef Sinha P, Hutter G, Kottgen E, Dietel M, Schadendorf D, Lage H (1998) Increased expression of annexin I and thioredoxin detected by two-dimensional gel electrophoresis of drug resistant human stomach cancer cells. J Biochem Biophys Methods 37:105–116. doi:10.​1016/​S0165-022X(98)00020-7 PubMedCrossRef
Zurück zum Zitat Solito E, Nuti S, Parente L (1994) Dexamethasone-induced translocation of lipocortin (annexin) 1 to the cell membrane of U-937 cells. Br J Pharmacol 112:347–348PubMed Solito E, Nuti S, Parente L (1994) Dexamethasone-induced translocation of lipocortin (annexin) 1 to the cell membrane of U-937 cells. Br J Pharmacol 112:347–348PubMed
Zurück zum Zitat Solito E, de Coupade C, Parente L, Flower RJ, Russo-Marie F (1998) Human annexin 1 is highly expressed during the differentiation of the epithelial cell line A 549: involvement of nuclear factor interleukin 6 in phorbol ester induction of annexin 1. Cell Growth Differ 9:327–336PubMed Solito E, de Coupade C, Parente L, Flower RJ, Russo-Marie F (1998) Human annexin 1 is highly expressed during the differentiation of the epithelial cell line A 549: involvement of nuclear factor interleukin 6 in phorbol ester induction of annexin 1. Cell Growth Differ 9:327–336PubMed
Zurück zum Zitat Solito E, Kamal A, Russo-Marie F, Buckingham JC, Marullo S, Perretti M (2003) A novel calcium-dependent proapoptotic effect of annexin 1 on human neutrophils. FASEB J 17:1544–1546PubMed Solito E, Kamal A, Russo-Marie F, Buckingham JC, Marullo S, Perretti M (2003) A novel calcium-dependent proapoptotic effect of annexin 1 on human neutrophils. FASEB J 17:1544–1546PubMed
Zurück zum Zitat Violette SM, King I, Browning JL, Pepinsky RB, Wallner BP, Sartorelli AC (1990) Role of lipocortin I in the glucocorticoid induction of the terminal differentiation of a human squamous carcinoma. J Cell Physiol 142:70–77. doi:10.1002/jcp.1041420110 PubMedCrossRef Violette SM, King I, Browning JL, Pepinsky RB, Wallner BP, Sartorelli AC (1990) Role of lipocortin I in the glucocorticoid induction of the terminal differentiation of a human squamous carcinoma. J Cell Physiol 142:70–77. doi:10.​1002/​jcp.​1041420110 PubMedCrossRef
Zurück zum Zitat Wang KL, Wu TT, Resetkova E, Wang H, Correa AM, Hofstetter WL, Swisher SG, Ajani JA, Rashid A, Hamilton SR, Albarracin CT (2006) Expression of annexin A1 in esophageal and esophagogastric junction adenocarcinomas: association with poor outcome. Clin Cancer Res 12:4598–4604. doi:10.1158/1078-0432.CCR-06-0483 PubMedCrossRef Wang KL, Wu TT, Resetkova E, Wang H, Correa AM, Hofstetter WL, Swisher SG, Ajani JA, Rashid A, Hamilton SR, Albarracin CT (2006) Expression of annexin A1 in esophageal and esophagogastric junction adenocarcinomas: association with poor outcome. Clin Cancer Res 12:4598–4604. doi:10.​1158/​1078-0432.​CCR-06-0483 PubMedCrossRef
Zurück zum Zitat Xia SH, Hu LP, Hu H, Ying WT, Xu X, Cai Y, Han YL, Chen BS, Wei F, Qian XH, Cai YY, Shen Y, Wu M, Wang MR (2002) Three isoforms of annexin I are preferentially expressed in normal esophageal epithelia but down-regulated in esophageal squamous cell carcinomas. Oncogene 21:6641–6648. doi:10.1038/sj.onc.1205818 PubMedCrossRef Xia SH, Hu LP, Hu H, Ying WT, Xu X, Cai Y, Han YL, Chen BS, Wei F, Qian XH, Cai YY, Shen Y, Wu M, Wang MR (2002) Three isoforms of annexin I are preferentially expressed in normal esophageal epithelia but down-regulated in esophageal squamous cell carcinomas. Oncogene 21:6641–6648. doi:10.​1038/​sj.​onc.​1205818 PubMedCrossRef
Metadaten
Titel
Down-regulation of plasma membranous Annexin A1 protein expression in premalignant and malignant lesions of the oral cavity: correlation with epithelial differentiation
verfasst von
Hitomi Nomura
Katsuhiro Uzawa
Yukio Yamano
Kazuaki Fushimi
Dai Nakashima
Yukinao Kouzu
Atsushi Kasamatsu
Katsunori Ogawara
Masashi Shiiba
Hiroki Bukawa
Hidetaka Yokoe
Hideki Tanzawa
Publikationsdatum
01.07.2009
Verlag
Springer-Verlag
Erschienen in
Journal of Cancer Research and Clinical Oncology / Ausgabe 7/2009
Print ISSN: 0171-5216
Elektronische ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-008-0530-z

Weitere Artikel der Ausgabe 7/2009

Journal of Cancer Research and Clinical Oncology 7/2009 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.