Insufficient radiofrequency ablation promotes epithelial-mesenchymal transition of hepatocellular carcinoma cells through Akt and ERK signaling pathways

Journal of Translational Medicine

Volumn 11, Issue 1, 2013, Pages

  Dong, Shuying ^a   Kong, Jian ^a   Kong, Fandong ^a   Kong, Jinge ^c   Gao, Jun ^a   Ke, Shan ^a   Wang, Shaohong ^a   Ding, Xuemei ^a   Sun, Wenbing ^a   Zheng, Lemin ^b  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c PEKING UNIVERSITY   (China)

Author keywords

Epithelial mesenchymal transition; Hepatocellular carcinoma; Insufficient radiofrequency ablation; Metastasis

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; CYCLINE; GELATINASE A; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE; NERVE CELL ADHESION MOLECULE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; LUNG METASTASIS; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RADIOFREQUENCY ABLATION; SIGNAL TRANSDUCTION; TUMOR VOLUME;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CATHETER ABLATION; CELL LINE, TUMOR; CHROMONES; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FLAVONOIDS; HUMANS; LIVER NEOPLASMS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, NUDE; MORPHOLINES; NEOPLASM METASTASIS; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84886386699     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-11-273     Document Type: Article

References (36)

1. El-Serag HB. Hepatocellular carcinoma. N Engl J Med 2011, 365:1118-1127. 10.1056/NEJMra1001683, 21992124.
2. Maluccio M, Covey A. Recent progress in understanding, diagnosing, and treating hepatocellular carcinoma. CA Cancer J Clin 2012, 62:394-399. 10.3322/caac.21161, 23070690.
3. Kim KW, Lee JM, Klotz E, Kim SJ, Kim SH, Kim JY, Han JK, Choi BI. Safety margin assessment after radiofrequency ablation of the liver using registration of preprocedure and postprocedure CT images. AJR Am J Roentgenol 2011, 196:W565-W572. 10.2214/AJR.10.5122, 21512046.
4. Nijkamp MW, van der Bilt JD, de Bruijn MT, Molenaar IQ, Voest EE, van Diest PJ, Kranenburg O, Borel RI. Accelerated perinecrotic outgrowth of colorectal liver metastases following radiofrequency ablation is a hypoxia-driven phenomenon. Ann Surg 2009, 249:814-823. 10.1097/SLA.0b013e3181a38ef5, 19387320.
5. Nijkamp MW, Hoogwater FJ, Steller EJ, Westendorp BF, van der Meulen TA, Leenders MW, Borel RI, Kranenburg O. CD95 is a key mediator of invasion and accelerated outgrowth of mouse colorectal liver metastases following radiofrequency ablation. J Hepatol 2010, 53:1069-1077. 10.1016/j.jhep.2010.04.040, 20832890.
6. Nikfarjam M, Muralidharan V, Christophi C. Altered growth patterns of colorectal liver metastases after thermal ablation. Surgery 2006, 139:73-81. 10.1016/j.surg.2005.07.030, 16364720.
7. Kong J, Kong L, Kong J, Ke S, Gao J, Ding X, Zheng L, Sun H, Sun W. After insufficient radiofrequency ablation, tumor-associated endothelial cells exhibit enhanced angiogenesis and promote invasiveness of residual hepatocellular carcinoma. J Transl Med 2012, 10:230. 10.1186/1479-5876-10-230, 3543343, 23171368.
8. Kong J, Kong J, Pan B, Ke S, Dong S, Li X, Zhou A, Zheng L, Sun WB. Insufficient radiofrequency ablation promotes angiogenesis of residual hepatocellular carcinoma via HIF-1alpha/VEGFA. PLoS One 2012, 7:e37266. 10.1371/journal.pone.0037266, 3352883, 22615958.
9. Ke S, Ding XM, Kong J, Gao J, Wang SH, Cheng Y, Sun WB. Low temperature of radiofrequency ablation at the target sites can facilitate rapid progression of residual hepatic VX2 carcinoma. J Transl Med 2010, 8:73. 10.1186/1479-5876-8-73, 2917410, 20667141.
10. Obara K, Matsumoto N, Okamoto M, Kobayashi M, Ikeda H, Takahashi H, Katakura Y, Matsunaga K, Ishii T, Okuse C, et al. Insufficient radiofrequency ablation therapy may induce further malignant transformation of hepatocellular carcinoma. Hepatol Int 2008, 2:116-123. 10.1007/s12072-007-9040-3, 2716878, 19669287.
11. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147:275-292. 10.1016/j.cell.2011.09.024, 3261217, 22000009.
12. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006, 127:679-695. 10.1016/j.cell.2006.11.001, 17110329.
13. De Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013, 13:97-110. 10.1038/nrc3447, 23344542.
14. Frisch SM, Schaller M, Cieply B. Mechanisms that link the oncogenic epithelial-mesenchymal transition to suppression of anoikis. J Cell Sci 2013, 126:21-29. 10.1242/jcs.120907, 23516327.
15. Tao YM, Huang JL, Zeng S, Zhang S, Fan XG, Wang ZM, Yang HX, Yuan XH, Wang P, Wu F, et al. BTB/POZ domain-containing protein 7: epithelial-mesenchymal transition promoter and prognostic biomarker of hepatocellular carcinoma. Hepatology 2013, 57:2326-2337. 10.1002/hep.26268, 23325674.
16. Cucchetti A, Piscaglia F, Cescon M, Colecchia A, Ercolani G, Bolondi L, Pinna AD. Cost-effectiveness of hepatic resection versus percutaneous radiofrequency ablation for early hepatocellular carcinoma. J Hepatol 2013, 59:3000-3007.
17. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009, 9:239-252. 10.1038/nrc2618, 3251309, 19279573.
18. Tao ZH, Wan JL, Zeng LY, Xie L, Sun HC, Qin LX, Wang L, Zhou J, Ren ZG, Li YX, et al. miR-612 suppresses the invasive-metastatic cascade in hepatocellular carcinoma. J Exp Med 2013, 210:789-803. 10.1084/jem.20120153, 3620363, 23478189.
19. Wang XQ, Zhang W, Lui EL, Zhu Y, Lu P, Yu X, Sun J, Yang S, Poon RT, Fan ST. Notch1-Snail1-E-cadherin pathway in metastatic hepatocellular carcinoma. Int J Cancer 2012, 131:E163-E172. 10.1002/ijc.27336, 22052196.
20. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009, 9:265-273. 10.1038/nrc2620, 19262571.
21. Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R, Gray MJ, Cheng H, Hoff PM, Ellis LM. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res 2006, 12:4147-4153. 10.1158/1078-0432.CCR-06-0038, 16857785.
22. Tsukamoto H, Shibata K, Kajiyama H, Terauchi M, Nawa A, Kikkawa F. Irradiation-induced epithelial-mesenchymal transition (EMT) related to invasive potential in endometrial carcinoma cells. Gynecol Oncol 2007, 107:500-504. 10.1016/j.ygyno.2007.08.058, 17905419.
23. Xiong W, Ren ZG, Qiu SJ, Sun HC, Wang L, Liu BB, Li QS, Zhang W, Zhu XD, Liu L, et al. Residual hepatocellular carcinoma after oxaliplatin treatment has increased metastatic potential in a nude mouse model and is attenuated by Songyou Yin. BMC Cancer 2010, 10:219. 10.1186/1471-2407-10-219, 2880993, 20487542.
24. Yoshida S, Kornek M, Ikenaga N, Schmelzle M, Masuzaki R, Csizmadia E, Wu Y, Robson SC, Schuppan D. Sub-lethal heat treatment promotes epithelial-mesenchymal transition and enhances the malignant potential of hepatocellular carcinoma. Hepatology 2013, in press.
25. Brabletz T. EMT and MET in metastasis: where are the cancer stem cells?. Cancer Cell 2012, 22:699-701. 10.1016/j.ccr.2012.11.009, 23238008.
26. Lang BJ, Nguyen L, Nguyen HC, Vieusseux JL, Chai RC, Christophi C, Fifis T, Kouspou MM, Price JT. Heat stress induces epithelial plasticity and cell migration independent of heat shock factor 1. Cell Stress Chaperones 2012, 17:765-778. 10.1007/s12192-012-0349-z, 3468677, 22791010.
27. Xu X, Fan Z, Kang L, Han J, Jiang C, Zheng X, Zhu Z, Jiao H, Lin J, Jiang K, et al. Hepatitis B virus X protein represses miRNA-148a to enhance tumorigenesis. J Clin Invest 2013, 123:630-645. 3561812, 23321675.
28. Ferraro A, Mourtzoukou D, Kosmidou V, Avlonitis S, Kontogeorgos G, Zografos G, Pintzas A. EZH2 is regulated by ERK/AKT and targets integrin alpha2 gene to control Epithelial-Mesenchymal Transition and anoikis in colon cancer cells. Int J Biochem Cell Biol 2013, 45:243-254. 10.1016/j.biocel.2012.10.009, 23116973.
29. Kim S, Kang HY, Nam EH, Choi MS, Zhao XF, Hong CS, Lee JW, Lee JH, Park YK. TMPRSS4 induces invasion and epithelial-mesenchymal transition through upregulation of integrin alpha5 and its signaling pathways. Carcinogenesis 2010, 31:597-606. 10.1093/carcin/bgq024, 20118200.
30. Ha GH, Park JS, Breuer EK. TACC3 promotes epithelial-mesenchymal transition (EMT) through the activation of PI3K/Akt and ERK signaling pathways. Cancer Lett 2013, 332:63-73. 10.1016/j.canlet.2013.01.013, 23348690.
31. Tanahashi T, Osada S, Yamada A, Kato J, Yawata K, Mori R, Imai H, Sasaki Y, Saito S, Tanaka Y, et al. Extracellular signal-regulated kinase and Akt activation play a critical role in the process of hepatocyte growth factor-induced epithelial-mesenchymal transition. Int J Oncol 2013, 42:556-564.
32. Ogunwobi OO, Liu C. Hepatocyte growth factor upregulation promotes carcinogenesis and epithelial-mesenchymal transition in hepatocellular carcinoma via Akt and COX-2 pathways. Clin Exp Metastasis 2011, 28:721-731. 10.1007/s10585-011-9404-x, 3732749, 21744257.
33. Godoy P, Hengstler JG, Ilkavets I, Meyer C, Bachmann A, Muller A, Tuschl G, Mueller SO, Dooley S. Extracellular matrix modulates sensitivity of hepatocytes to fibroblastoid dedifferentiation and transforming growth factor beta-induced apoptosis. Hepatology 2009, 49:2031-2043. 10.1002/hep.22880, 19274752.
34. Katsuno Y, Lamouille S, Derynck R. TGF-beta signaling and epithelial-mesenchymal transition in cancer progression. Curr Opin Oncol 2013, 25:76-84. 10.1097/CCO.0b013e32835b6371, 23197193.
35. Zuo JH, Zhu W, Li MY, Li XH, Yi H, Zeng GQ, Wan XX, He QY, Li JH, Qu JQ, et al. Activation of EGFR promotes squamous carcinoma SCC10A cell migration and invasion via inducing EMT-like phenotype change and MMP-9-mediated degradation of E-cadherin. J Cell Biochem 2011, 112:2508-2517. 10.1002/jcb.23175, 21557297.
36. Gan Y, Shi C, Inge L, Hibner M, Balducci J, Huang Y. Differential roles of ERK and Akt pathways in regulation of EGFR-mediated signaling and motility in prostate cancer cells. Oncogene 2010, 29:4947-4958. 10.1038/onc.2010.240, 20562913.