Skip to main content
Top
Published in: Clinical and Translational Oncology 3/2015

01-03-2015 | Research Article

MicroRNA-10b indicates a poor prognosis of non-small cell lung cancer and targets E-cadherin

Authors: J. Zhang, L. Xu, Z. Yang, H. Lu, D. Hu, W. Li, Z. Zhang, B. Liu, S. Ma

Published in: Clinical and Translational Oncology | Issue 3/2015

Login to get access

Abstract

Background

MicroRNA-10b(miR-10b) has been reported to be dysregulated in some types of cancer and to play an important role in invasion and metastasis. It was previously found to be a tumor enhancer in NSCLC; however, its clinical significance in NSCLC has not been evaluated.

Methods

We compared the expression levels of miR-10b in 73 pairs of NSCLC tissues and the corresponding noncancerous tissues, as well as in human lung cancer cell line A549 and NHBE cell line by qRT-PCR. Expression of E-cadherin (E-cad) was detected using RT-PCR and Western blot analysis. The disease-specific survival (DSS) was analyzed by log-rank test, and survival curves were plotted according to Kaplan–Meier.

Results

MiR-10b was significantly upregulated in NSCLC tissues as well as in A549 cell line. The relative miR-10b expression levels were significantly positively correlated with TNM stage (p = 0.01) and regional lymph node involvement (p < 0.001). Kaplan–Meier analysis showed that patients with higher levels of miR-10b had significantly poorer survival than those with lower expression of this miRNA in patients, with a 5-year DSS of 29.5 and 63.8 %, respectively (p = 0.003). The E-cad mRNA and protein were overexpressed in miR-10b-suppressed cells compared with controls.

Conclusion

Our results indicated that miR-10b expression was an independent prognostic factor in NSCLC patients. Furthermore, miR-10b might be necessary for driving the expression of E-cad in NSCLC.
Literature
1.
2.
go back to reference Coello MC, Luketich JD, Litle VR, Godfrey TE. Prognostic significance of micrometastasis in non-small-cell lung cancer. Clin lung cancer. 2004;5:214–25.CrossRefPubMed Coello MC, Luketich JD, Litle VR, Godfrey TE. Prognostic significance of micrometastasis in non-small-cell lung cancer. Clin lung cancer. 2004;5:214–25.CrossRefPubMed
3.
go back to reference Chen PY, Meister G. microRNA-guided posttranscriptional gene regulation. Biol Chem. 2005;386:1205–18.CrossRefPubMed Chen PY, Meister G. microRNA-guided posttranscriptional gene regulation. Biol Chem. 2005;386:1205–18.CrossRefPubMed
4.
go back to reference Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol. 2009;10:141–8.CrossRefPubMed Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol. 2009;10:141–8.CrossRefPubMed
5.
go back to reference Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology. 2007;133:647–58.PubMedCentralCrossRefPubMed Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology. 2007;133:647–58.PubMedCentralCrossRefPubMed
6.
go back to reference Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, et al. RAS is regulated by the let-7 microRNA family. Cell. 2005;120:635–47.CrossRefPubMed Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, et al. RAS is regulated by the let-7 microRNA family. Cell. 2005;120:635–47.CrossRefPubMed
7.
go back to reference Fritz HK, Lindgren D, Ljungberg B, Axelson H, Dahlback B. The miR ratio as a prognostic marker in clear cell renal cell carcinoma. Eur J Cancer. 2014; 50:1758–65. Fritz HK, Lindgren D, Ljungberg B, Axelson H, Dahlback B. The miR ratio as a prognostic marker in clear cell renal cell carcinoma. Eur J Cancer. 2014; 50:1758–65.
8.
go back to reference Xiao H, Li H, Yu G, Xiao W, Hu J, Tang K, et al. MicroRNA-10b promotes migration and invasion through KLF4 and HOXD10 in human bladder cancer. Oncol Rep. 2014;31:1832–8.PubMed Xiao H, Li H, Yu G, Xiao W, Hu J, Tang K, et al. MicroRNA-10b promotes migration and invasion through KLF4 and HOXD10 in human bladder cancer. Oncol Rep. 2014;31:1832–8.PubMed
9.
go back to reference Han X, Yan S, Weijie Z, Feng W, Liuxing W, Mengquan L, et al. Critical role of miR-10b in transforming growth factor-beta1-induced epithelial–mesenchymal transition in breast cancer. Cancer Gene Ther. 2014;21:60–7.CrossRefPubMed Han X, Yan S, Weijie Z, Feng W, Liuxing W, Mengquan L, et al. Critical role of miR-10b in transforming growth factor-beta1-induced epithelial–mesenchymal transition in breast cancer. Cancer Gene Ther. 2014;21:60–7.CrossRefPubMed
10.
go back to reference Sun XJ, Liu H, Zhang P, Zhang XD, Jiang ZW, Jiang CC. miR-10b promotes migration and invasion in nasopharyngeal carcinoma cells. APJCP. 2013;14:5533–7.PubMed Sun XJ, Liu H, Zhang P, Zhang XD, Jiang ZW, Jiang CC. miR-10b promotes migration and invasion in nasopharyngeal carcinoma cells. APJCP. 2013;14:5533–7.PubMed
11.
go back to reference Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449:682–8.CrossRefPubMed Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449:682–8.CrossRefPubMed
12.
go back to reference Liu Y, Li M, Zhang G, Pang Z. MicroRNA-10b overexpression promotes non-small cell lung cancer cell proliferation and invasion. Eur J Med Res. 2013;18:41.PubMedCentralCrossRefPubMed Liu Y, Li M, Zhang G, Pang Z. MicroRNA-10b overexpression promotes non-small cell lung cancer cell proliferation and invasion. Eur J Med Res. 2013;18:41.PubMedCentralCrossRefPubMed
13.
go back to reference Tian Y, Luo A, Cai Y, Su Q, Ding F, Chen H, et al. MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J Biol Chem. 2010;285:7986–94.PubMedCentralCrossRefPubMed Tian Y, Luo A, Cai Y, Su Q, Ding F, Chen H, et al. MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J Biol Chem. 2010;285:7986–94.PubMedCentralCrossRefPubMed
14.
go back to reference Sasayama T, Nishihara M, Kondoh T, Hosoda K, Kohmura E. MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int J cancer J Int du cancer. 2009;125:1407–13.CrossRef Sasayama T, Nishihara M, Kondoh T, Hosoda K, Kohmura E. MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int J cancer J Int du cancer. 2009;125:1407–13.CrossRef
15.
go back to reference Nakata K, Ohuchida K, Mizumoto K, Kayashima T, Ikenaga N, Sakai H, et al. MicroRNA-10b is overexpressed in pancreatic cancer, promotes its invasiveness, and correlates with a poor prognosis. Surgery. 2011;150:916–22.CrossRefPubMed Nakata K, Ohuchida K, Mizumoto K, Kayashima T, Ikenaga N, Sakai H, et al. MicroRNA-10b is overexpressed in pancreatic cancer, promotes its invasiveness, and correlates with a poor prognosis. Surgery. 2011;150:916–22.CrossRefPubMed
16.
go back to reference Li G, Wu Z, Peng Y, Liu X, Lu J, Wang L, et al. MicroRNA-10b induced by Epstein–Barr virus-encoded latent membrane protein-1 promotes the metastasis of human nasopharyngeal carcinoma cells. Cancer Lett. 2010;299:29–36.CrossRefPubMed Li G, Wu Z, Peng Y, Liu X, Lu J, Wang L, et al. MicroRNA-10b induced by Epstein–Barr virus-encoded latent membrane protein-1 promotes the metastasis of human nasopharyngeal carcinoma cells. Cancer Lett. 2010;299:29–36.CrossRefPubMed
17.
go back to reference Ouyang H, Gore J, Deitz S, Korc M. MicroRNA-10b enhances pancreatic cancer cell invasion by suppressing TIP30 expression and promoting EGF and TGF-beta actions. Oncogene 2013 [Epub ahead of print]. Ouyang H, Gore J, Deitz S, Korc M. MicroRNA-10b enhances pancreatic cancer cell invasion by suppressing TIP30 expression and promoting EGF and TGF-beta actions. Oncogene 2013 [Epub ahead of print].
18.
go back to reference Lin J, Teo S, Lam DH, Jeyaseelan K, Wang S. MicroRNA-10b pleiotropically regulates invasion, angiogenicity and apoptosis of tumor cells resembling mesenchymal subtype of glioblastoma multiforme. Cell Death Dis. 2012;3:e398.PubMedCentralCrossRefPubMed Lin J, Teo S, Lam DH, Jeyaseelan K, Wang S. MicroRNA-10b pleiotropically regulates invasion, angiogenicity and apoptosis of tumor cells resembling mesenchymal subtype of glioblastoma multiforme. Cell Death Dis. 2012;3:e398.PubMedCentralCrossRefPubMed
19.
go back to reference Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S, et al. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology. 2008;47:1955–63.CrossRefPubMed Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S, et al. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology. 2008;47:1955–63.CrossRefPubMed
20.
go back to reference Soltermann A, Tischler V, Arbogast S, Braun J, Probst-Hensch N, Weder W, et al. Prognostic significance of epithelial–mesenchymal and mesenchymal–epithelial transition protein expression in non-small cell lung cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2008;14:7430–7.CrossRef Soltermann A, Tischler V, Arbogast S, Braun J, Probst-Hensch N, Weder W, et al. Prognostic significance of epithelial–mesenchymal and mesenchymal–epithelial transition protein expression in non-small cell lung cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2008;14:7430–7.CrossRef
22.
go back to reference Wang G, Dong W, Shen H, Mu X, Li Z, Lin X, et al. A comparison of Twist and E-cadherin protein expression in primary non-small-cell lung carcinoma and corresponding metastases. Eur J Cardio Thorac Surg Off J Eur Assoc Cardio Thorac Surg. 2011;39:1028–32.CrossRef Wang G, Dong W, Shen H, Mu X, Li Z, Lin X, et al. A comparison of Twist and E-cadherin protein expression in primary non-small-cell lung carcinoma and corresponding metastases. Eur J Cardio Thorac Surg Off J Eur Assoc Cardio Thorac Surg. 2011;39:1028–32.CrossRef
23.
go back to reference Zheng G, Lyons JG, Tan TK, Wang Y, Hsu TT, Min D, et al. Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelial-mesenchymal transition downstream of transforming growth factor-beta1 in renal tubular epithelial cells. Am J Pathol. 2009;175:580–91.PubMedCentralCrossRefPubMed Zheng G, Lyons JG, Tan TK, Wang Y, Hsu TT, Min D, et al. Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelial-mesenchymal transition downstream of transforming growth factor-beta1 in renal tubular epithelial cells. Am J Pathol. 2009;175:580–91.PubMedCentralCrossRefPubMed
24.
go back to reference Thiery JP. Epithelial–mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002;2:442–54.CrossRefPubMed Thiery JP. Epithelial–mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002;2:442–54.CrossRefPubMed
25.
go back to reference Gogali A, Charalabopoulos K, Zampira I, Konstantinidis AK, Tachmazoglou F, Daskalopoulos G, et al. Soluble adhesion molecules E-cadherin, intercellular adhesion molecule-1, and E-selectin as lung cancer biomarkers. Chest. 2010;138:1173–9.CrossRefPubMed Gogali A, Charalabopoulos K, Zampira I, Konstantinidis AK, Tachmazoglou F, Daskalopoulos G, et al. Soluble adhesion molecules E-cadherin, intercellular adhesion molecule-1, and E-selectin as lung cancer biomarkers. Chest. 2010;138:1173–9.CrossRefPubMed
Metadata
Title
MicroRNA-10b indicates a poor prognosis of non-small cell lung cancer and targets E-cadherin
Authors
J. Zhang
L. Xu
Z. Yang
H. Lu
D. Hu
W. Li
Z. Zhang
B. Liu
S. Ma
Publication date
01-03-2015
Publisher
Springer Milan
Published in
Clinical and Translational Oncology / Issue 3/2015
Print ISSN: 1699-048X
Electronic ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-014-1213-7

Other articles of this Issue 3/2015

Clinical and Translational Oncology 3/2015 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