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International Journal of Oncology
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Article

Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma

  • Authors:
    • Akira Nakayama
    • Itasu Ninomiya
    • Shinichi Harada
    • Tomoya Tsukada
    • Koichi Okamoto
    • Shinichi Nakanuma
    • Seisho Sakai
    • Isamu Makino
    • Jun Kinoshita
    • Hironori Hayashi
    • Katsunobu Oyama
    • Tomoharu Miyashita
    • Hidehiro Tajima
    • Hiroyuki Takamura
    • Sachio Fushida
    • Tetsuo Ohta
  • View Affiliations / Copyright

    Affiliations: Department of Gastroenterological Surgery, Division of Cancer Medicine, Graduate School of Medical Science, Kanazawa University, Kanazawa 920-8641, Japan, Center for Biomedical Research and Education, School of Medical Science, Kanazawa University, Kanazawa 920-8641, Japan
  • Pages: 1890-1898
    |
    Published online on: August 31, 2016
       https://doi.org/10.3892/ijo.2016.3676
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Abstract

Esophageal cancer is one of the most aggressive tumor types because of its invasiveness and metastatic potential. Several reports have described an association between increased invasiveness after ionizing radiation (IR) treatment and epithelial-to-mesenchymal transition (EMT). The biguanide metformin is reported to prevent transforming growth factor-β (TGF-β)-induced EMT and proliferation of cancer. This study examined whether IR induces EMT and promotes the invasive potential of TE-9 esophageal squamous cell carcinoma cells and the effect of metformin on IR-induced EMT. After IR exposure, TE-9 cells showed a spindle-shaped morphology and lost cell-cell adhesion. Immunoblotting showed that IR induced expression of mesenchymal markers (vimentin and N-cadherin), transcription factors (Slug, Snail, and Twist), and matrix metalloproteinases. A scratch wound assay and Matrigel invasion assay showed that IR enhanced the invasive potential and migratory capacity of TE-9 cells. Expression of hypoxia-related factor-1α and TGF-β was increased after IR. IR also induced phosphorylation of Smad2 and Smad3. Metformin inhibited radiation-induced EMT-like morphological changes, and enhanced invasion and migration of TE-9 cells. Metformin inhibited IR-induced phosphorylation of Smad2 and Smad3. Although phosphorylation of AMP-activated protein kinase was enhanced by IR and metformin, phosphorylation of mammalian target of rapamycin was enhanced by IR and suppressed by metformin. These results indicated that metformin suppressed IR-induced EMT via suppression of the TGF-β-Smad phosphorylation pathway, and a part of the non-Smad pathway. Metformin might be useful to prevent IR-induced invasion and metastasis of esophageal squamous cell carcinoma.
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View References

1 

Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011. View Article : Google Scholar : PubMed/NCBI

2 

Zhang Y: Epidemiology of esophageal cancer. World J Gastroenterol. 19:5598–5606. 2013. View Article : Google Scholar : PubMed/NCBI

3 

Cooper JS, Guo MD, Herskovic A, Macdonald JS, Martenson JA Jr, Al-Sarraf M, Byhardt R, Russell AH, Beitler JJ, Spencer S, et al; Radiation Therapy Oncology Group. Chemoradiotherapy of locally advanced esophageal cancer: Long-term follow-up of a prospective randomized trial (RTOG 85-01). JAMA. 281:1623–1627. 1999. View Article : Google Scholar : PubMed/NCBI

4 

Linkous AG and Yazlovitskaya EM: Novel radiosensitizing anticancer therapeutics. Anticancer Res. 32:2487–2499. 2012.PubMed/NCBI

5 

Sjoquist KM, Burmeister BH, Smithers BM, Zalcberg JR, Simes RJ, Barbour A and Gebski V; Australasian Gastro-Intestinal Trials Group. Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: An updated meta-analysis. Lancet Oncol. 12:681–692. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Dent P, Yacoub A, Contessa J, Caron R, Amorino G, Valerie K, Hagan MP, Grant S and Schmidt-Ullrich R: Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiat Res. 159:283–300. 2003. View Article : Google Scholar : PubMed/NCBI

7 

Barcellos-Hoff MH, Park C and Wright EG: Radiation and the microenvironment - tumorigenesis and therapy. Nat Rev Cancer. 5:867–875. 2005. View Article : Google Scholar : PubMed/NCBI

8 

Tsukamoto H, Shibata K, Kajiyama H, Terauchi M, Nawa A and Kikkawa F: Irradiation-induced epithelial-mesenchymal transition (EMT) related to invasive potential in endometrial carcinoma cells. Gynecol Oncol. 107:500–504. 2007. View Article : Google Scholar : PubMed/NCBI

9 

Wild-Bode C, Weller M, Rimner A, Dichgans J and Wick W: Sublethal irradiation promotes migration and invasiveness of glioma cells: Implications for radiotherapy of human glioblastoma. Cancer Res. 61:2744–2750. 2001.PubMed/NCBI

10 

Marie-Egyptienne DT, Lohse I and Hill RP: Cancer stem cells, the epithelial to mesenchymal transition (EMT) and radioresistance: Potential role of hypoxia. Cancer Lett. 341:63–72. 2013. View Article : Google Scholar

11 

He E, Pan F, Li G and Li J: Fractionated ionizing radiation promotes epithelial-mesenchymal transition in human esophageal cancer cells through PTEN deficiency-mediated Akt activation. PLoS One. 10:e01261492015. View Article : Google Scholar : PubMed/NCBI

12 

Thiery JP, Acloque H, Huang RY and Nieto MA: Epithelial-mesenchymal transitions in development and disease. Cell. 139:871–890. 2009. View Article : Google Scholar : PubMed/NCBI

13 

Park JK, Jang SJ, Kang SW, Park S, Hwang SG, Kim WJ, Kang JH and Um HD: Establishment of animal model for the analysis of cancer cell metastasis during radiotherapy. Radiat Oncol. 7:1532012. View Article : Google Scholar : PubMed/NCBI

14 

Zhou YC, Liu JY, Li J, Zhang J, Xu YQ, Zhang HW, Qiu LB, Ding GR, Su XM, Mei-Shi, et al: Ionizing radiation promotes migration and invasion of cancer cells through transforming growth factor-beta-mediated epithelial-mesenchymal transition. Int J Radiat Oncol Biol Phys. 81:1530–1537. 2011. View Article : Google Scholar : PubMed/NCBI

15 

Bailey CJ and Turner RC: Metformin. N Engl J Med. 334:574–579. 1996. View Article : Google Scholar : PubMed/NCBI

16 

Bowker SL, Majumdar SR, Veugelers P and Johnson JA: Increased cancer-related mortality for patients with type 2 diabetes who use sulfonylureas or insulin. Diabetes Care. 29:254–258. 2006. View Article : Google Scholar : PubMed/NCBI

17 

Landman GW, Kleefstra N, van Hateren KJ, Groenier KH, Gans RO and Bilo HJ: Metformin associated with lower cancer mortality in type 2 diabetes: ZODIAC-16. Diabetes Care. 33:322–326. 2010. View Article : Google Scholar :

18 

Evans JM, Donnelly LA, Emslie-Smith AM, Alessi DR and Morris AD: Metformin and reduced risk of cancer in diabetic patients. BMJ. 330:1304–1305. 2005. View Article : Google Scholar : PubMed/NCBI

19 

Dowling RJ, Niraula S, Stambolic V and Goodwin PJ: Metformin in cancer: Translational challenges. J Mol Endocrinol. 48:R31–R43. 2012. View Article : Google Scholar : PubMed/NCBI

20 

Chaudhary SC, Kurundkar D, Elmets CA, Kopelovich L and Athar M: Metformin, an antidiabetic agent reduces growth of cutaneous squamous cell carcinoma by targeting mTOR signaling pathway. Photochem Photobiol. 88:1149–1156. 2012. View Article : Google Scholar : PubMed/NCBI

21 

Bao B, Azmi AS, Ali S, Zaiem F and Sarkar FH: Metformin may function as anti-cancer agent via targeting cancer stem cells: The potential biological significance of tumor-associated miRNAs in breast and pancreatic cancers. Ann Transl Med. 2:592014.PubMed/NCBI

22 

Dowling RJ, Zakikhani M, Fantus IG, Pollak M and Sonenberg N: Metformin inhibits mammalian target of rapamycin-dependent translation initiation in breast cancer cells. Cancer Res. 67:10804–10812. 2007. View Article : Google Scholar : PubMed/NCBI

23 

Vazquez-Martin A, Oliveras-Ferraros C, Cufí S, Del Barco S, Martin-Castillo B and Menendez JA: Metformin regulates breast cancer stem cello ntogeny by transcriptional regulation of the epithelial-mesenchymal transition (EMT) status. Cell Cycle. 9:3831–3838. 2014. View Article : Google Scholar

24 

Cufí S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Joven J and Menendez JA: Metformin against TGFβ-induced epithelial-to-mesenchymal transition (EMT): From cancer stem cells to aging-associated fibrosis. Cell Cycle. 9:4461–4468. 2010. View Article : Google Scholar

25 

Westermarck J and Kähäri VM: Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 13:781–792. 1999.PubMed/NCBI

26 

Saitoh M, Shirakihara T and Miyazono K: Regulation of the stability of cell surface E-cadherin by the proteasome. Biochem Biophys Res Commun. 381:560–565. 2009. View Article : Google Scholar : PubMed/NCBI

27 

Xu J, Lamouille S and Derynck R: TGF-beta-induced epithelial to mesenchymal transition. Cell Res. 19:156–172. 2009. View Article : Google Scholar : PubMed/NCBI

28 

Morrison CD, Parvani JG and Schiemann WP: The relevance of the TGF-β Paradox to EMT-MET programs. Cancer Lett. 341:30–40. 2013. View Article : Google Scholar : PubMed/NCBI

29 

Mimeault M and Batra SK: Hypoxia-inducing factors as master regulators of stemness properties and altered metabolism of cancer- and metastasis-initiating cells. J Cell Mol Med. 17:30–54. 2013. View Article : Google Scholar : PubMed/NCBI

30 

Lamouille S and Derynck R: Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol. 178:437–451. 2007. View Article : Google Scholar : PubMed/NCBI

31 

Chen L, Li M, Li Q, Wang CJ and Xie SQ: DKK1 promotes hepatocellular carcinoma cell migration and invasion through β-catenin/MMP7 signaling pathway. Mol Cancer. 12:1572013. View Article : Google Scholar

32 

Zhang X, Li X, Zhang N, Yang Q and Moran MS: Low doses ionizing radiation enhances the invasiveness of breast cancer cells by inducing epithelial-mesenchymal transition. Biochem Biophys Res Commun. 412:188–192. 2011. View Article : Google Scholar : PubMed/NCBI

33 

Zong H, Yin B, Zhou H, Cai D, Ma B and Xiang Y: Inhibition of mTOR pathway attenuates migration and invasion of gallbladder cancer via EMT inhibition. Mol Biol Rep. 41:4507–4512. 2014. View Article : Google Scholar : PubMed/NCBI

34 

Han B, Cui H, Kang L, Zhang X, Jin Z, Lu L and Fan Z: Metformin inhibits thyroid cancer cell growth, migration, and EMT through the mTOR pathway. Tumour Biol. 36:6295–6304. 2015. View Article : Google Scholar : PubMed/NCBI

35 

Koeck S, Amann A, Huber JM, Gamerith G, Hilbe W and Zwierzina H: The impact of metformin and salinomycin on transforming growth factor β-induced epithelial-to-mesenchymal transition in non-small cell lung cancer cell lines. Oncol Lett. 11:2946–2952. 2016.PubMed/NCBI

36 

Sanli T, Rashid A, Liu C, Harding S, Bristow RG, Cutz JC, Singh G, Wright J and Tsakiridis T: Ionizing radiation activates AMP-activated kinase (AMPK): A target for radiosensitization of human cancer cells. Int J Radiat Oncol Biol Phys. 78:221–229. 2010. View Article : Google Scholar : PubMed/NCBI

37 

Storozhuk Y, Hopmans SN, Sanli T, Barron C, Tsiani E, Cutz JC, Pond G, Wright J, Singh G and Tsakiridis T: Metformin inhibits growth and enhances radiation response of non-small cell lung cancer (NSCLC) through ATM and AMPK. Br J Cancer. 108:2021–2032. 2013. View Article : Google Scholar : PubMed/NCBI

38 

Bussink J, van der Kogel AJ and Kaanders JH: Activation of the PI3-K/AKT pathway and implications for radioresistance mechanisms in head and neck cancer. Lancet Oncol. 9:288–296. 2008. View Article : Google Scholar : PubMed/NCBI

39 

Bodmer M, Meier C, Krähenbühl S, Jick SS and Meier CR: Metformin, sulfonylureas, or other antidiabetes drugs and the risk of lactic acidosis or hypoglycemia: A nested case-control analysis. Diabetes Care. 31:2086–2091. 2008. View Article : Google Scholar : PubMed/NCBI

40 

Hadad S, Iwamoto T, Jordan L, Purdie C, Bray S, Baker L, Jellema G, Deharo S, Hardie DG, Pusztai L, et al: Evidence for biological effects of metformin in operable breast cancer: A pre-operative, window-of-opportunity, randomized trial. Breast Cancer Res Treat. 128:783–794. 2011. View Article : Google Scholar : PubMed/NCBI

41 

Goodwin PJ, Stambolic V, Lemieux J, Chen BE, Parulekar WR, Gelmon KA, Hershman DL, Hobday TJ, Ligibel JA, Mayer IA, et al: Evaluation of metformin in early breast cancer: A modification of the traditional paradigm for clinical testing of anti-cancer agents. Breast Cancer Res Treat. 126:215–220. 2011. View Article : Google Scholar

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Copy and paste a formatted citation
Spandidos Publications style
Nakayama A, Ninomiya I, Harada S, Tsukada T, Okamoto K, Nakanuma S, Sakai S, Makino I, Kinoshita J, Hayashi H, Hayashi H, et al: Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma. Int J Oncol 49: 1890-1898, 2016.
APA
Nakayama, A., Ninomiya, I., Harada, S., Tsukada, T., Okamoto, K., Nakanuma, S. ... Ohta, T. (2016). Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma. International Journal of Oncology, 49, 1890-1898. https://doi.org/10.3892/ijo.2016.3676
MLA
Nakayama, A., Ninomiya, I., Harada, S., Tsukada, T., Okamoto, K., Nakanuma, S., Sakai, S., Makino, I., Kinoshita, J., Hayashi, H., Oyama, K., Miyashita, T., Tajima, H., Takamura, H., Fushida, S., Ohta, T."Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma". International Journal of Oncology 49.5 (2016): 1890-1898.
Chicago
Nakayama, A., Ninomiya, I., Harada, S., Tsukada, T., Okamoto, K., Nakanuma, S., Sakai, S., Makino, I., Kinoshita, J., Hayashi, H., Oyama, K., Miyashita, T., Tajima, H., Takamura, H., Fushida, S., Ohta, T."Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma". International Journal of Oncology 49, no. 5 (2016): 1890-1898. https://doi.org/10.3892/ijo.2016.3676
Copy and paste a formatted citation
x
Spandidos Publications style
Nakayama A, Ninomiya I, Harada S, Tsukada T, Okamoto K, Nakanuma S, Sakai S, Makino I, Kinoshita J, Hayashi H, Hayashi H, et al: Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma. Int J Oncol 49: 1890-1898, 2016.
APA
Nakayama, A., Ninomiya, I., Harada, S., Tsukada, T., Okamoto, K., Nakanuma, S. ... Ohta, T. (2016). Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma. International Journal of Oncology, 49, 1890-1898. https://doi.org/10.3892/ijo.2016.3676
MLA
Nakayama, A., Ninomiya, I., Harada, S., Tsukada, T., Okamoto, K., Nakanuma, S., Sakai, S., Makino, I., Kinoshita, J., Hayashi, H., Oyama, K., Miyashita, T., Tajima, H., Takamura, H., Fushida, S., Ohta, T."Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma". International Journal of Oncology 49.5 (2016): 1890-1898.
Chicago
Nakayama, A., Ninomiya, I., Harada, S., Tsukada, T., Okamoto, K., Nakanuma, S., Sakai, S., Makino, I., Kinoshita, J., Hayashi, H., Oyama, K., Miyashita, T., Tajima, H., Takamura, H., Fushida, S., Ohta, T."Metformin inhibits the radiation-induced invasive phenotype of esophageal squamous cell carcinoma". International Journal of Oncology 49, no. 5 (2016): 1890-1898. https://doi.org/10.3892/ijo.2016.3676
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