Activated macrophages down-regulate expression of E-cadherin in hepatocellular carcinoma cells via NF–κB/Slug pathway

Tumor Biology

Volumn 35, Issue 9, 2014, Pages 8893-8901

  Wang, Xianteng ^a   Wang, Hao ^a   Li, Guosheng ^b   Song, Yonghong ^c   Wang, Shurong ^c   Zhu, Faliang ^a   Guo, Chun ^a   Zhang, Lining ^a   Shi, Yongyu ^a  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANDONG UNIVERSITY   (China)

^c Shandong Blood Center   (China)

Author keywords

E Cadherin; Hepatocellular carcinoma; NF B; Tumor associated macrophage

Indexed keywords

BETA ACTIN; I KAPPA B KINASE BETA; MESSENGER RNA; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR SLUG; UVOMORULIN; VASCULOTROPIN RECEPTOR; CADHERIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA;

ARTICLE; CANCER RECURRENCE; CELL COUNT; CELL DIFFERENTIATION; CELL INFILTRATION; CONTROLLED STUDY; DOWN REGULATION; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIVER CELL CARCINOMA; MACROPHAGE; MACROPHAGE ACTIVATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; COCULTURE; GENETICS; IMMUNOLOGY; LIVER TUMOR; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CADHERINS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELLS, CULTURED; COCULTURE TECHNIQUES; DOWN-REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MACROPHAGE ACTIVATION; MACROPHAGES; NF-KAPPA B; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS;

EID: 84919876155     PISSN: 10104283     EISSN: None     Source Type: Journal    
DOI: 10.1007/s13277-014-2159-7     Document Type: Article

References (39)

1. Qin LX, Tang ZY. Recent progress in predictive biomarkers for metastatic recurrence of human hepatocellular carcinoma: a review of the literature. J Cancer Res Clin Oncol. 2004;130:497–513.
2. Voulgari A, Pintzas A. Epithelial–mesenchymal transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim Biophys Acta. 2009;1796(2):75–90.
3. Reichl P, Haider C, Grubinger M, Mikulits W. TGF-β in epithelial to mesenchymal transition and metastasis of liver carcinoma. Curr Pharm. 2012;18:4135–47.
4. Giannelli G, Bergamini C, Fransvea E, Sgarra C, Antonaci S. Laminin-5 with transforming growthfactor-beta1 induces epithelial to mesenchymal transition in hepatocellular carcinoma. Gastroenterology. 2005;129:1375–83.
5. Kozyraki R, Scoazec JY, Flejou JF, et al. Expression of cadherins and alpha-catenin in primary epithelial tumors of the liver. Gastroenterology. 1996;110:1137–49.
6. Inayoshi J, Ichida T, Sugitani S, et al. Gross appearance of hepatocellular carcinoma reflects E-cadherin expression and risk of early recurrence after surgical treatment. J Gastroenterol Hepatol. 2003;18:673–7.
7. Zhai B, Yan HX, Liu SQ, Chen L, Wu MC, Wang HY. Reduced expression of E-cadherin/catenin complex in hepatocellular carcinomas. World J Gastroenterol. 2008;14:5665–73.
8. Wang Y, Yue B, Yu X, Wang Z, Wang M. SLUG is activated by nuclear factor kappa B and confers human alveolar epithelial A549 cells resistance to tumor necrosis factor-alpha-induced apoptosis. World J Surg Oncol. 2013;11:12.
9. Wu DW, Lee MC, Wang J, Chen CY, Cheng YW, Lee H. DDX3 loss by p53 inactivation promotes tumor malignancy via the MDM2/Slug/E-cadherin pathway and poor patient outcome in non-small-cell lung cancer. Oncogenesis. 2013. doi:10.1038/onc.
10. Wu Y, Zheng L. Dynamic education of macrophages in different areas of human tumors. Cancer Microenviron. 2012;5:195–201.
11. Zhu XD, Zhang JB, Zhuang PY, et al. High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J Clin Oncol. 2008;26:2707–16.
12. Ju MJ, Qiu SJ, Fan J, et al. Peritumoral activated hepatic stellate cells predict poor clinical outcome in hepatocellular carcinoma after curative resection. Am J Clin Pathol. 2009;131:498–510.
13. Ding T, Xu J, Wang F, et al. High tumor-infiltrating macrophage density predicts poor prognosis in patients with primary hepatocellular carcinoma after resection. Hum Pathol. 2009;40:381–9.
14. Lin CY, Lin CJ, Chen KH, Wu JC, Huang SH, Wang SM. Macrophage activation increases the invasive properties of hepatoma cells by destabilization of the adherens junction. FEBS Lett. 2006;580:3042–50.
15. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol. 2010;22:231–7.
16. Karin M. The IkappaB kinase—a bridge between inflammation and cancer. Cell Res. 2008;18:334–42.
17. Tjiu JW, Chen JS, Shun CT, et al. Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction. J Investig Dermatol. 2009;129:1016–25.
18. Gamallo C, Palacios J, Suarez A, et al. Correlation of E-cadherin expression with differentiation grade and histological type in breast carcinoma. Am J Pathol. 1993;142:987–93.
19. Sugimachi K, Tanaka S, Kameyama T, et al. Transcriptional repressor snail and progression of human hepatocellular carcinoma. Clin Cancer Res. 2003;9:2657–64.
20. Lee J, Rhee MH, Kim E, Cho JY. BAY 11-7082 is a broad-spectrum inhibitor with anti-inflammatory activity against multiple targets. Mediat Inflamm. 2012;2012:416036.
21. Juliana C, Fernandes-Alnemri T, Wu J, et al. Anti-inflammatory compounds parthenolide and Bay 11-7082 are direct inhibitors of the inflammasome. J Biol Chem. 2010;285(13):9792–802.
22. Techasen A, Namwat N, Loilome W, et al. Tumor necrosis factor-α (TNF-α) stimulates the epithelial–mesenchymal transition regulator Snail in cholangiocarcinoma. Med Oncol. 2012;29:3083–91.
23. Yamauchi Y, Kohyama T, Takizawa H, et al. Tumor necrosis factor-alpha enhances both epithelial–mesenchymal transition and cell contraction induced in A549 human alveolar epithelial cells by transforming growth factor-beta1. Exp Lung Res. 2010;36:12–24.
24. Ho MY, Tang SJ, Chuang MJ, et al. TNF-α induces epithelial–mesenchymal transition of renal cell carcinoma cells via a GSK3β-dependent mechanism. Mol Cancer Res. 2012;10:1109–19.
25. Yadav A, Kumar B, Datta J, Teknos TN, Kumar P. IL-6 promotes head and neck tumor metastasis by inducing epithelial–mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res. 2011;9:1658–67.
26. Huang C, Yang G, Jiang T, Zhu G, Li H, Qiu Z. The effects and mechanisms of blockage of STAT3 signaling pathway on IL-6 inducing EMT in human pancreatic cancer cells in vitro. Neoplasma. 2011;58:396–405.
27. Sullivan NJ, Sasser AK, Axel AE, et al. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene. 2009;28:2940–7.
28. St John MA, Dohadwala M, Luo J, et al. Proinflammatory mediators upregulate snail in head and neck squamous cell carcinoma. Clin Cancer Res. 2009;15:6018–27.
29. Mima K, Okabe H, Ishimoto T, et al. CD44s regulates the TGF-β-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res. 2012;72:3414–23.
30. Yi ZY, Feng LJ, Xiang Z, Yao H. Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in hepatocellular carcinoma cells. J Investig Surg. 2011;24:67–76.
31. Dudas PL, Sague SL, Elloso MM, Farrell FX. Proinflammatory/profibrotic effects of interleukin-17A on human proximal tubule epithelium. Nephron Exp Nephrol. 2011;117:e114–23.
32. Masuzaki R, Karp SJ, Omata M. New serum markers of hepatocellular carcinoma. Semin Oncol. 2012;39:434–9.
33. Tai DI, Tsai SL, Chang YH, et al. Constitutive activation of nuclear factor kappaB in hepatocellular carcinoma. Cancer. 2000;89:2274–81.
34. Vainer GW, Pikarsky E, Ben-Neriah Y. Contradictory functions of NF–kappaB in liver physiology and cancer. Cancer Lett. 2008;267:182–8.
35. He G, Karin M. NF–κB and STAT3—key players in liver inflammation and cancer. Cell Res. 2011;21:159–68.
36. Glauert HP. Role of NF–κB in hepatocarcinogenesis and its potential inhibition by dietary antioxidants. Curr Cancer Drug Targets. 2012;12:1160–72.
37. Arsura M, Cavin LG. Nuclear factor–kappaB and liver carcinogenesis. Cancer Lett. 2005;229:157–69.
38. Yang MH, Chen CL, Chau GY, et al. Comprehensive analysis of the independent effect of twist and snail in promoting metastasis of hepatocellular carcinoma. Hepatology. 2009;50:1464–74.
39. Sun D, Sun B, Liu T, et al. Slug promoted vasculogenic mimicry in hepatocellular carcinoma. J Cell Mol Med. 2013;17:1038–47.