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Published in: Clinical and Translational Oncology 11/2013

01-11-2013 | Research Article

Prognostic significance of annexin II expression in non-small cell lung cancer

Authors: C.-H. Luo, Q.-Q. Liu, P.-F. Zhang, M.-Y. Li, Z.-C. Chen, Y.-F. Liu

Published in: Clinical and Translational Oncology | Issue 11/2013

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Abstract

Purpose

To discover common metastasis-related and prognostic markers in lung squamous carcinoma (LSC) and lung adenocarcinoma (AdC), two forms of non-small cell lung cancer (NSCLC).

Methods

Quantitative proteomic analysis was performed between primary cancer tissues and matched lymph node metastatic tissues in LSC and AdC, respectively. Immunohistochemistry and statistic analysis were performed to investigate prognostic significance of metastasis-related protein annexin II expression in LSC and AdC.

Results

Both in LSC and AdC, elevated expression of annexin II was identified in lymph node metastatic lung cancers compared to corresponding primary lung cancers. Furthermore, immunohistochemical analysis of a bulk of clinical specimens indicated that annexin II over-expression was more frequently observed in matched lymph node metastatic tissues than corresponding primary cancer tissues. Statistical analysis showed that annexin II over-expression was significantly associated with advanced clinical stage (P < 0.05) and lymph node metastasis (P < 0.05) and increased relapse rate (P < 0.05) and decreased overall survival (P < 0.05) in both two subtypes of NSCLC. Cox regression analysis indicated that annexin II over-expression was an important prognostic factor in both LSC and AdC.

Conclusion

Annexin II was identified as a common prognostic factor in both LSC and AdC.
Literature
1.
go back to reference Little AG, Gay EG, Gaspar LE, Stewart AK. National survey of non-small cell lung cancer in the United States: epidemiology, pathology and patterns of care. Lung Cancer. 2007;57:253–60.PubMedCrossRef Little AG, Gay EG, Gaspar LE, Stewart AK. National survey of non-small cell lung cancer in the United States: epidemiology, pathology and patterns of care. Lung Cancer. 2007;57:253–60.PubMedCrossRef
3.
go back to reference Yan JX, Devenish AT, Wait R, Stone T, Lewis S, Fowler S. Fluorescence two-dimensional difference gel electrophoresis and mass spectrometry based proteomic analysis of Escherichia coli. Proteomics. 2002;2:1682–98.PubMedCrossRef Yan JX, Devenish AT, Wait R, Stone T, Lewis S, Fowler S. Fluorescence two-dimensional difference gel electrophoresis and mass spectrometry based proteomic analysis of Escherichia coli. Proteomics. 2002;2:1682–98.PubMedCrossRef
4.
go back to reference Van den Bergh G, Arckens L. Fluorescent two-dimensional difference gel electrophoresis unveils the potential of gel-based proteomics. Curr Opin Biotechnol. 2004;15:38–43.PubMedCrossRef Van den Bergh G, Arckens L. Fluorescent two-dimensional difference gel electrophoresis unveils the potential of gel-based proteomics. Curr Opin Biotechnol. 2004;15:38–43.PubMedCrossRef
5.
go back to reference Friedman DB, Hill S, Keller JW, Merchant NB, Levy SE, Coffey RJ, et al. Proteome analysis of human colon cancer by two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics. 2004;4:793–811.PubMedCrossRef Friedman DB, Hill S, Keller JW, Merchant NB, Levy SE, Coffey RJ, et al. Proteome analysis of human colon cancer by two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics. 2004;4:793–811.PubMedCrossRef
6.
go back to reference Kakisaka T, Kondo T, Okano T, Fujii K, Honda K, Endo M, et al. Plasma proteomics of pancreatic cancer patients by multi-dimensional liquid chromatography and two-dimensional difference gel electrophoresis (2D-DIGE): up-regulation of leucine-rich alpha-2-glycoprotein in pancreatic cancer. J Chromatogr B Analyt Technol Biomed Life Sci. 2007;852:257–67.PubMedCrossRef Kakisaka T, Kondo T, Okano T, Fujii K, Honda K, Endo M, et al. Plasma proteomics of pancreatic cancer patients by multi-dimensional liquid chromatography and two-dimensional difference gel electrophoresis (2D-DIGE): up-regulation of leucine-rich alpha-2-glycoprotein in pancreatic cancer. J Chromatogr B Analyt Technol Biomed Life Sci. 2007;852:257–67.PubMedCrossRef
7.
go back to reference Fidler IJ, Kripke ML. Metastasis results from preexisting variant cells within a malignant tumor. Science. 1977;197:893–5.PubMedCrossRef Fidler IJ, Kripke ML. Metastasis results from preexisting variant cells within a malignant tumor. Science. 1977;197:893–5.PubMedCrossRef
8.
go back to reference Wallner BP, Mattaliano RJ, Hession C, Cate RL, Tizard R, Sinclair LK, et al. Cloning and expression of human lipocortin, a phospholipase A2 inhibitor with potential anti-inflammatory activity. Nature. 1986;320:77–81.PubMedCrossRef Wallner BP, Mattaliano RJ, Hession C, Cate RL, Tizard R, Sinclair LK, et al. Cloning and expression of human lipocortin, a phospholipase A2 inhibitor with potential anti-inflammatory activity. Nature. 1986;320:77–81.PubMedCrossRef
9.
go back to reference Gerke V, Moss SE. Annexins: from structure to function. Physiol Rev. 2002;82:331–71.PubMed Gerke V, Moss SE. Annexins: from structure to function. Physiol Rev. 2002;82:331–71.PubMed
10.
go back to reference Rescher U, Gerke V. Annexins—unique membrane binding proteins with diverse functions. J Cell Sci. 2004;117:2631–9.PubMedCrossRef Rescher U, Gerke V. Annexins—unique membrane binding proteins with diverse functions. J Cell Sci. 2004;117:2631–9.PubMedCrossRef
11.
12.
go back to reference Emoto K, Yamada Y, Sawada H, Fujimoto H, Ueno M, Takayama T, et al. Annexin II overexpression correlates with stromal tenascin-C overexpression: a prognostic marker in colorectal carcinoma. Cancer. 2001;92:1419–26.PubMedCrossRef Emoto K, Yamada Y, Sawada H, Fujimoto H, Ueno M, Takayama T, et al. Annexin II overexpression correlates with stromal tenascin-C overexpression: a prognostic marker in colorectal carcinoma. Cancer. 2001;92:1419–26.PubMedCrossRef
13.
go back to reference Cole SP, Pinkoski MJ, Bhardwaj G, Deeley RG. Elevated expression of annexin II (lipocortin II, p36) in a multidrug resistant small cell lung cancer cell line. Br J Cancer. 1992;65:498–502.PubMedCrossRef Cole SP, Pinkoski MJ, Bhardwaj G, Deeley RG. Elevated expression of annexin II (lipocortin II, p36) in a multidrug resistant small cell lung cancer cell line. Br J Cancer. 1992;65:498–502.PubMedCrossRef
14.
go back to reference Vishwanatha JK, Chiang Y, Kumble KD, Hollingsworth MA, Pour PM. Enhanced expression of annexin II in human pancreatic carcinoma cells and primary pancreatic cancers. Carcinogenesis. 1993;14:2575–9.PubMedCrossRef Vishwanatha JK, Chiang Y, Kumble KD, Hollingsworth MA, Pour PM. Enhanced expression of annexin II in human pancreatic carcinoma cells and primary pancreatic cancers. Carcinogenesis. 1993;14:2575–9.PubMedCrossRef
15.
go back to reference Tanaka T, Akatsuka S, Ozeki M, Shirase T, Hiai H, Toyokuni S. Redox regulation of annexin 2 and its implications for oxidative stress-induced renal carcinogenesis and metastasis. Oncogene. 2004;23:3980–9.PubMedCrossRef Tanaka T, Akatsuka S, Ozeki M, Shirase T, Hiai H, Toyokuni S. Redox regulation of annexin 2 and its implications for oxidative stress-induced renal carcinogenesis and metastasis. Oncogene. 2004;23:3980–9.PubMedCrossRef
16.
go back to reference Sharma MC, Sharma M. The role of annexin II in angiogenesis and tumor progression: a potential therapeutic target. Curr Pharm Des. 2007;13:3568–75.PubMedCrossRef Sharma MC, Sharma M. The role of annexin II in angiogenesis and tumor progression: a potential therapeutic target. Curr Pharm Des. 2007;13:3568–75.PubMedCrossRef
17.
go back to reference Mai J, Finley RL Jr, Waisman DM, Sloane BF. Human procathepsin B interacts with the annexin II tetramer on the surface of tumor cells. J Biol Chem. 2000;275:12806–12.PubMedCrossRef Mai J, Finley RL Jr, Waisman DM, Sloane BF. Human procathepsin B interacts with the annexin II tetramer on the surface of tumor cells. J Biol Chem. 2000;275:12806–12.PubMedCrossRef
18.
go back to reference Yang F, Xiao ZQ, Zhang XZ, Li C, Zhang PF, Li MY, et al. Identification of tumor antigens in human lung squamous carcinoma by serological proteome analysis. J Proteome Res. 2007;6:751–8.PubMedCrossRef Yang F, Xiao ZQ, Zhang XZ, Li C, Zhang PF, Li MY, et al. Identification of tumor antigens in human lung squamous carcinoma by serological proteome analysis. J Proteome Res. 2007;6:751–8.PubMedCrossRef
19.
go back to reference Cheng A-L, Huang W-G, Chen Z-C, Peng F, Zhang P-F, Li M-Y, et al. Identification of novel nasopharyngeal carcinoma biomarkers by laser capture microdissection and proteomic analysis. Clin Cancer Res. 2008;14:435–45.PubMedCrossRef Cheng A-L, Huang W-G, Chen Z-C, Peng F, Zhang P-F, Li M-Y, et al. Identification of novel nasopharyngeal carcinoma biomarkers by laser capture microdissection and proteomic analysis. Clin Cancer Res. 2008;14:435–45.PubMedCrossRef
20.
go back to reference Tian T, Hao J, Xu A, Hao J, Luo C, Liu C, et al. Determination of metastasis-associated proteins in non-small cell lung cancer by comparative proteomic analysis. Cancer Sci. 2007;98:1265–74.PubMedCrossRef Tian T, Hao J, Xu A, Hao J, Luo C, Liu C, et al. Determination of metastasis-associated proteins in non-small cell lung cancer by comparative proteomic analysis. Cancer Sci. 2007;98:1265–74.PubMedCrossRef
21.
go back to reference Chen ZG. Exploration of metastasis-related proteins as biomarkers and therapeutic targets in the treatment of head and neck cancer. Curr Cancer Drug Targets. 2007;7:613–22.PubMedCrossRef Chen ZG. Exploration of metastasis-related proteins as biomarkers and therapeutic targets in the treatment of head and neck cancer. Curr Cancer Drug Targets. 2007;7:613–22.PubMedCrossRef
22.
go back to reference Sakwe AM, Koumangoye R, Guillory B, Ochieng J. Annexin A6 contributes to the invasiveness of breast carcinoma cells by influencing the organization and localization of functional focal adhesions. Exp Cell Res. 2011;317:823–37.PubMedCrossRef Sakwe AM, Koumangoye R, Guillory B, Ochieng J. Annexin A6 contributes to the invasiveness of breast carcinoma cells by influencing the organization and localization of functional focal adhesions. Exp Cell Res. 2011;317:823–37.PubMedCrossRef
23.
go back to reference Wang KL, Wu T-T, Resetkova E, Wang H, Correa AM, Hofstetter WL, et al. Expression of annexin A1 in esophageal and esophagogastric junction adenocarcinomas: association with poor outcome. Clin Cancer Res. 2006;12:4598–604.PubMedCrossRef Wang KL, Wu T-T, Resetkova E, Wang H, Correa AM, Hofstetter WL, et al. Expression of annexin A1 in esophageal and esophagogastric junction adenocarcinomas: association with poor outcome. Clin Cancer Res. 2006;12:4598–604.PubMedCrossRef
24.
go back to reference Torosyan Y, Simakova O, Naga S, Mezhevaya K, Leighton X, Diaz J, et al. Annexin-A7 protects normal prostate cells and induces distinct patterns of RB-associated cytotoxicity in androgen-sensitive and -resistant prostate cancer cells. Int J Cancer. 2009;125:2528–39.PubMedCrossRef Torosyan Y, Simakova O, Naga S, Mezhevaya K, Leighton X, Diaz J, et al. Annexin-A7 protects normal prostate cells and induces distinct patterns of RB-associated cytotoxicity in androgen-sensitive and -resistant prostate cancer cells. Int J Cancer. 2009;125:2528–39.PubMedCrossRef
25.
go back to reference Shiozawa Y, Havens AM, Jung Y, Ziegler AM, Pedersen EA, Wang J, et al. Annexin II/annexin II receptor axis regulates adhesion, migration, homing, and growth of prostate cancer. J Cell Biochem. 2008;105:370–80.PubMedCrossRef Shiozawa Y, Havens AM, Jung Y, Ziegler AM, Pedersen EA, Wang J, et al. Annexin II/annexin II receptor axis regulates adhesion, migration, homing, and growth of prostate cancer. J Cell Biochem. 2008;105:370–80.PubMedCrossRef
26.
go back to reference Ohno Y, Izumi M, Kawamura T, Nishimura T, Mukai K, Tachibana M. Annexin II represents metastatic potential in clear-cell renal cell carcinoma. Br J Cancer. 2009;101:287–94.PubMedCrossRef Ohno Y, Izumi M, Kawamura T, Nishimura T, Mukai K, Tachibana M. Annexin II represents metastatic potential in clear-cell renal cell carcinoma. Br J Cancer. 2009;101:287–94.PubMedCrossRef
27.
go back to reference Singh P, Wu H, Clark C, Owlia A. Annexin II binds progastrin and gastrin-like peptides, and mediates growth factor effects of autocrine and exogenous gastrins on colon cancer and intestinal epithelial cells. Oncogene. 2007;26:425–40.PubMedCrossRef Singh P, Wu H, Clark C, Owlia A. Annexin II binds progastrin and gastrin-like peptides, and mediates growth factor effects of autocrine and exogenous gastrins on colon cancer and intestinal epithelial cells. Oncogene. 2007;26:425–40.PubMedCrossRef
28.
go back to reference Zhao P, Zhang W, Tang J, Ma XK, Dai JY, Li Y, et al. Annexin II promotes invasion and migration of human hepatocellular carcinoma cells in vitro via its interaction with HAb18G/CD147. Cancer Sci. 2010;101:387–95.PubMedCrossRef Zhao P, Zhang W, Tang J, Ma XK, Dai JY, Li Y, et al. Annexin II promotes invasion and migration of human hepatocellular carcinoma cells in vitro via its interaction with HAb18G/CD147. Cancer Sci. 2010;101:387–95.PubMedCrossRef
29.
go back to reference Takano S, Togawa A, Yoshitomi H, Shida T, Kimura F, Shimizu H, et al. Annexin II overexpression predicts rapid recurrence after surgery in pancreatic cancer patients undergoing gemcitabine-adjuvant chemotherapy. Ann Surg Oncol. 2008;15:3157–68.PubMedCrossRef Takano S, Togawa A, Yoshitomi H, Shida T, Kimura F, Shimizu H, et al. Annexin II overexpression predicts rapid recurrence after surgery in pancreatic cancer patients undergoing gemcitabine-adjuvant chemotherapy. Ann Surg Oncol. 2008;15:3157–68.PubMedCrossRef
30.
go back to reference Sharma M, Ownbey RT, Sharma MC. Breast cancer cell surface annexin II induces cell migration and neoangiogenesis via tPA dependent plasmin generation. Exp Mol Pathol. 2010;88:278–86.PubMedCrossRef Sharma M, Ownbey RT, Sharma MC. Breast cancer cell surface annexin II induces cell migration and neoangiogenesis via tPA dependent plasmin generation. Exp Mol Pathol. 2010;88:278–86.PubMedCrossRef
Metadata
Title
Prognostic significance of annexin II expression in non-small cell lung cancer
Authors
C.-H. Luo
Q.-Q. Liu
P.-F. Zhang
M.-Y. Li
Z.-C. Chen
Y.-F. Liu
Publication date
01-11-2013
Publisher
Springer Milan
Published in
Clinical and Translational Oncology / Issue 11/2013
Print ISSN: 1699-048X
Electronic ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-013-1028-y

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