Skip to main content
Top
Published in: Tumor Biology 12/2014

01-12-2014 | Research Article

Increased expression levels of S100A4 associated with hypoxia-induced invasion and metastasis in esophageal squamous cell cancer

Authors: Xiaoyan Xuan, Qianru Li, Zhongning Zhang, Ying Du, Pingping Liu

Published in: Tumor Biology | Issue 12/2014

Login to get access

Abstract

Here, we explored the expression of S100A4 in esophageal squamous cell cancer (ESCC) tissues and investigated its role in hypoxia-induced invasion and metastasis in ESCC cell lines EC-1 and EC-9706. Immunohistochemistry analysis demonstrated that S100A4 was overexpressed in human ESCC tissues especially in ESCC tissues with deep invasion and lymph node metastasis. Hypoxia-induced S100A4 overexpression was observed in EC-1 and EC-9706 cells, in which it was associated with invasion and metastasis. Furthermore, we used EC-1 and EC-9706 cells again to upregulate or knockdown the expression S100A4 to investigate the mechanism role of S100A4 in hypoxia-induced invasion and metastasis in ESCC cells. And the results showed that S100A4 played an important role in promoting the invasion and metastasis of EC-1 and EC-9706 cells under hypoxia. Therefore, S100A4 overexpression might be an important mechanism by which hypoxia induced invasion and metastasis, and S100A4 could also be a potential target for the treatment of ESCC.
Literature
1.
go back to reference Ji-Sheng L, Jian-Ming Y, Xiu-Wen W, Zhao-Hui W, Qian T, Li-Li L. Promoter methylation of tumor suppressor genes in esophageal squamous cell carcinoma. Chin J Cancer. 2013;32:3–11.CrossRef Ji-Sheng L, Jian-Ming Y, Xiu-Wen W, Zhao-Hui W, Qian T, Li-Li L. Promoter methylation of tumor suppressor genes in esophageal squamous cell carcinoma. Chin J Cancer. 2013;32:3–11.CrossRef
2.
go back to reference Yuxin H, Correa AM, Ashraful H, Baoxiang G, Fei Y, Jie H, et al. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer. 2011;128:132–43.CrossRef Yuxin H, Correa AM, Ashraful H, Baoxiang G, Fei Y, Jie H, et al. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer. 2011;128:132–43.CrossRef
3.
go back to reference Ismail TM, Zhang S, Fernig DG, Gross S, Martin-Fernandez ML, See V, et al. Self-association of calcium-binding protein S100A4 and metastasis. J Biol Chem. 2010;285:914–22.CrossRef Ismail TM, Zhang S, Fernig DG, Gross S, Martin-Fernandez ML, See V, et al. Self-association of calcium-binding protein S100A4 and metastasis. J Biol Chem. 2010;285:914–22.CrossRef
4.
go back to reference Shuangping L, Leilei L, Yingyi Z, Yiwen Z, Yu Z, Xiaona Y, et al. The oncoprotein HBXIP uses two pathways to up-regulate S100A4 in promotion of growth and migration of breast cancer cells. J Biol Chem. 2012;287:30228–39.CrossRef Shuangping L, Leilei L, Yingyi Z, Yiwen Z, Yu Z, Xiaona Y, et al. The oncoprotein HBXIP uses two pathways to up-regulate S100A4 in promotion of growth and migration of breast cancer cells. J Biol Chem. 2012;287:30228–39.CrossRef
5.
go back to reference Takenaga K, Nakanishi H, Wada K, Suzuki M, Matsuzaki O, Matsuura A, et al. Increased expression of S100A4, a metastasis-associated gene, in human colorectal adenocarcinomas. Clin Cancer Res. 1997;3:2309–16.PubMed Takenaga K, Nakanishi H, Wada K, Suzuki M, Matsuzaki O, Matsuura A, et al. Increased expression of S100A4, a metastasis-associated gene, in human colorectal adenocarcinomas. Clin Cancer Res. 1997;3:2309–16.PubMed
6.
go back to reference Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JH, Robertson L, et al. Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res. 2000;60:1595–603.PubMed Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JH, Robertson L, et al. Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res. 2000;60:1595–603.PubMed
7.
go back to reference Pedersen KB, Nesland JM, Fodstad O, Maelandsmo GM. Expression of S100A4, E-cadherin, alpha- and beta-catenin in breast cancer biopsies. Br J Cancer. 2002;87:1281–6.CrossRef Pedersen KB, Nesland JM, Fodstad O, Maelandsmo GM. Expression of S100A4, E-cadherin, alpha- and beta-catenin in breast cancer biopsies. Br J Cancer. 2002;87:1281–6.CrossRef
8.
go back to reference Schuyer M, Henzen-Logmans SC, van der Burg ME, Fieret JH, Derksen C, Look MP, et al. Genetic alterations in ovarian borderline tumours and ovarian carcinomas. Eur J Obstet Gynecol Reprod Biol. 1999;82:147–50.CrossRef Schuyer M, Henzen-Logmans SC, van der Burg ME, Fieret JH, Derksen C, Look MP, et al. Genetic alterations in ovarian borderline tumours and ovarian carcinomas. Eur J Obstet Gynecol Reprod Biol. 1999;82:147–50.CrossRef
9.
go back to reference Ito Y, Yoshida H, Tomoda C, Uruno T, Miya A, Kobayashi K, et al. S100A4 expression is an early event of papillary carcinoma of the thyroid. Oncol. 2004;67:397–402.CrossRef Ito Y, Yoshida H, Tomoda C, Uruno T, Miya A, Kobayashi K, et al. S100A4 expression is an early event of papillary carcinoma of the thyroid. Oncol. 2004;67:397–402.CrossRef
10.
go back to reference Rosty C, Ueki T, Argani P, Jansen M, Yeo CJ, Cameron JL, et al. Overexpression of S100A4 in pancreatic ductal adenocarcinomas is associated with poor differentiation and DNA hypomethylation. Am J Pathol. 2002;160:45–50.CrossRef Rosty C, Ueki T, Argani P, Jansen M, Yeo CJ, Cameron JL, et al. Overexpression of S100A4 in pancreatic ductal adenocarcinomas is associated with poor differentiation and DNA hypomethylation. Am J Pathol. 2002;160:45–50.CrossRef
11.
go back to reference Kimura K, Endo Y, Yonemura Y, Heizmann CW, Schafer BW, Watanabe Y, et al. Clinical significance of S100A4 and E-cadherin-related adhesion molecules in non-small cell lung cancer. Int J Oncol. 2000;16:1125–31.PubMed Kimura K, Endo Y, Yonemura Y, Heizmann CW, Schafer BW, Watanabe Y, et al. Clinical significance of S100A4 and E-cadherin-related adhesion molecules in non-small cell lung cancer. Int J Oncol. 2000;16:1125–31.PubMed
12.
go back to reference Takenaga K, Nakamura Y, Sakiyama S. Expression of antisense RNA to S100A4 gene encoding an S100-related calcium-binding protein suppresses metastatic potential of high-metastatic Lewis lung carcinoma cells. Oncogene. 1997;14:331–7.CrossRef Takenaga K, Nakamura Y, Sakiyama S. Expression of antisense RNA to S100A4 gene encoding an S100-related calcium-binding protein suppresses metastatic potential of high-metastatic Lewis lung carcinoma cells. Oncogene. 1997;14:331–7.CrossRef
13.
go back to reference Ninomiya I, Ohta T, Fushida S, Endo Y, Hashimoto T, Yagi M, et al. Increased expression of S100A4 and its prognostic significance in esophageal squamous cell carcinoma. Int J Oncol. 2001;18:715–20.PubMed Ninomiya I, Ohta T, Fushida S, Endo Y, Hashimoto T, Yagi M, et al. Increased expression of S100A4 and its prognostic significance in esophageal squamous cell carcinoma. Int J Oncol. 2001;18:715–20.PubMed
14.
go back to reference Gupta S, Hussain T, MacLennan GT, Fu P, Patel J, Mukhtar H. Differential expression of S100A2 and S100A4 during progression of human prostate adenocarcinoma. J Clin Oncol. 2003;21:106–12.CrossRef Gupta S, Hussain T, MacLennan GT, Fu P, Patel J, Mukhtar H. Differential expression of S100A2 and S100A4 during progression of human prostate adenocarcinoma. J Clin Oncol. 2003;21:106–12.CrossRef
15.
go back to reference Dong C, Xue-Feng Z, Ze-You Y, Dong-Xiao L, Guo-You Z, Xue-Long J, et al. S100A4 silencing blocks invasive ability of esophageal squamous cell carcinoma cells. World J Gastroenterol. 2012;18:915–22.CrossRef Dong C, Xue-Feng Z, Ze-You Y, Dong-Xiao L, Guo-You Z, Xue-Long J, et al. S100A4 silencing blocks invasive ability of esophageal squamous cell carcinoma cells. World J Gastroenterol. 2012;18:915–22.CrossRef
16.
go back to reference Hongyan C, Chengshan X, Qing’e J, Zhihua L. S100 protein family in human cancer. Am J Cancer Res. 2014;4:89–115. Hongyan C, Chengshan X, Qing’e J, Zhihua L. S100 protein family in human cancer. Am J Cancer Res. 2014;4:89–115.
17.
go back to reference Ruan K, Song G, Ouyang G. Role of hypoxia in the hallmarks of human cancer. J Cell Biochem. 2009;14(6):1053–62.CrossRef Ruan K, Song G, Ouyang G. Role of hypoxia in the hallmarks of human cancer. J Cell Biochem. 2009;14(6):1053–62.CrossRef
18.
go back to reference Iovine B, Oliviero G, Garofalo M, Orefice M, Nocella F, Borbone N, et al. The anti-proliferative effect of L-carnosine correlates with a decreased expression of hypoxia inducible factor 1 alpha in human colon cancer cells. PLoS One. 2014;9:e96755.CrossRef Iovine B, Oliviero G, Garofalo M, Orefice M, Nocella F, Borbone N, et al. The anti-proliferative effect of L-carnosine correlates with a decreased expression of hypoxia inducible factor 1 alpha in human colon cancer cells. PLoS One. 2014;9:e96755.CrossRef
19.
go back to reference Murielle M, Batra SK. Hypoxia-inducing factors as master regulators of stemness properties and altered metabolism of cancer- and metastasis-initiating cells. J Cell Mol Med. 2013;17:30–54.CrossRef Murielle M, Batra SK. Hypoxia-inducing factors as master regulators of stemness properties and altered metabolism of cancer- and metastasis-initiating cells. J Cell Mol Med. 2013;17:30–54.CrossRef
20.
go back to reference Yang-An W, Stevens PD, Gasser ML, Romina A, Tianyan G. Downregulation of PHLPP expression contributes to hypoxia-induced resistance to chemotherapy in colon cancer cells. Mol Cell Biol. 2013;33:4594–605.CrossRef Yang-An W, Stevens PD, Gasser ML, Romina A, Tianyan G. Downregulation of PHLPP expression contributes to hypoxia-induced resistance to chemotherapy in colon cancer cells. Mol Cell Biol. 2013;33:4594–605.CrossRef
21.
go back to reference Luana S, Sergio R, Marco T, Huafeng Z, Carmen Chak-Lui W, Andrea R, et al. Hypoxia-inducible factor 1-dependent expression of platelet-derived growth factor B promotes lymphatic metastasis of hypoxic breast cancer cells. Proc Natl Acad Sci U S A. 2012;109:E2707–16. Luana S, Sergio R, Marco T, Huafeng Z, Carmen Chak-Lui W, Andrea R, et al. Hypoxia-inducible factor 1-dependent expression of platelet-derived growth factor B promotes lymphatic metastasis of hypoxic breast cancer cells. Proc Natl Acad Sci U S A. 2012;109:E2707–16.
22.
go back to reference Wang S, Zhou Y, Andreyev O, Hoyt Jr RF, Singh A, Hunt T, et al. Overexpression of FABP3 inhibits human bone marrow derived mesenchymal stem cell proliferation but enhances their survival in hypoxia. Exp Cell Res. 2014;323:56–65.CrossRef Wang S, Zhou Y, Andreyev O, Hoyt Jr RF, Singh A, Hunt T, et al. Overexpression of FABP3 inhibits human bone marrow derived mesenchymal stem cell proliferation but enhances their survival in hypoxia. Exp Cell Res. 2014;323:56–65.CrossRef
23.
go back to reference Zhang W, Liu Y, Wang CW. S100A4 promotes squamous cell laryngeal cancer Hep-2 cell invasion via NF-kB/MMP-9 signal. Eur Rev Med Pharmacol Sci. 2014;18:1361–7.PubMed Zhang W, Liu Y, Wang CW. S100A4 promotes squamous cell laryngeal cancer Hep-2 cell invasion via NF-kB/MMP-9 signal. Eur Rev Med Pharmacol Sci. 2014;18:1361–7.PubMed
24.
go back to reference Bettum IJ, Vasiliauskaite K, Nygaard V, Clancy T, Pettersen SJ, Tenstad E, et al. Metastasis-associated protein S100A4 induces a network of inflammatory cytokines that activate stromal cells to acquire pro-tumorigenic properties. Cancer Lett. 2014;344:28–39.CrossRef Bettum IJ, Vasiliauskaite K, Nygaard V, Clancy T, Pettersen SJ, Tenstad E, et al. Metastasis-associated protein S100A4 induces a network of inflammatory cytokines that activate stromal cells to acquire pro-tumorigenic properties. Cancer Lett. 2014;344:28–39.CrossRef
25.
go back to reference Zhang HY, Zheng XZ, Wang XH, Xuan XY, Wang F, Li SS. S100A4 mediated cell invasion and metastasis of esophageal squamous cell carcinoma via the regulation of MMP-2 and E-cadherin activity. Mol Biol Rep. 2012;39:199–208.CrossRef Zhang HY, Zheng XZ, Wang XH, Xuan XY, Wang F, Li SS. S100A4 mediated cell invasion and metastasis of esophageal squamous cell carcinoma via the regulation of MMP-2 and E-cadherin activity. Mol Biol Rep. 2012;39:199–208.CrossRef
Metadata
Title
Increased expression levels of S100A4 associated with hypoxia-induced invasion and metastasis in esophageal squamous cell cancer
Authors
Xiaoyan Xuan
Qianru Li
Zhongning Zhang
Ying Du
Pingping Liu
Publication date
01-12-2014
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 12/2014
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-014-2573-x

Other articles of this Issue 12/2014

Tumor Biology 12/2014 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine