TGF-β1 induces epigenetic silence of TIP30 to promote tumor metastasis in esophageal carcinoma

Oncotarget

Volumn 6, Issue 4, 2015, Pages 2120-2133

  Bu, Fangfang ^a,b,c   Liu, Xing ^d   Li, Jingjing ^a   Chen, Shukun ^a   Tong, Xin ^a,b,c   Ma, Chunsheng ^d   Mao, Hui ^a   Pan, Fei ^a   Li, Xiaoyan ^a,b   Chen, Bo ^e   Xu, Liyan ^e   Li, Enmin ^e   Kou, Geng ^a,b,f   Han, Jun ^f   Guo, Shangjing ^f   Zhao, Jian ^a,b,c   Guo, Yajun ^a,b,c,f  

^a CHINESE PLA GENERAL HOSPITAL   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c PEKING UNIVERSITY   (China)

^d The 150th Central Hospital of People's Liberation Army   (China)

^e SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^f LIAOCHENG UNIVERSITY   (China)

Author keywords

Epithelial mesenchymal transition; ESCC; Methylation; TGF 1; Tip30

Indexed keywords

30KDA HIV 1 TAT INTERACTING PROTEIN; BETA CATENIN; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR BETA ANTIBODY; TRANSFORMING GROWTH FACTOR BETA1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; ACYLTRANSFERASE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; HTATIP2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INVASION; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA METHYLATION; DOWN REGULATION; ENZYME ACTIVATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; ESOPHAGEAL CANCER CELL LINE; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; GENE TRANSLOCATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TUMOR XENOGRAFT; AGED; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; ESOPHAGUS TUMOR; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; METASTASIS; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; PROGNOSIS; RNA INTERFERENCE; SQUAMOUS CELL CARCINOMA; SURVIVAL; TUMOR CELL LINE; XENOGRAFT;

ACETYLTRANSFERASES; AGED; ANIMALS; BETA CATENIN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; EPITHELIAL-MESENCHYMAL TRANSITION; ESOPHAGEAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE, INBRED BALB C; MICE, NUDE; MIDDLE AGED; NEOPLASM METASTASIS; PROGNOSIS; RNA INTERFERENCE; SURVIVAL ANALYSIS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1; TRANSPLANTATION, HETEROLOGOUS;

EID: 84923039250     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2940     Document Type: Article

References (38)

1. Bandla, S., A. Pennathur, J.D. Luketich, D.G. Beer, L. Lin, A.J. Bass, T.E. Godfrey and V.R. Litle, Comparative genomics of esophageal adenocarcinoma and squamous cell carcinoma. Ann Thorac Surg, 2012. 93(4): p. 1101-6.
2. Hiyama, T., M. Yoshihara, S. Tanaka and K. Chayama, Genetic polymorphisms and esophageal cancer risk. Int J Cancer, 2007. 121(8): p. 1643-58.
3. Yang, J. and R.A. Weinberg, Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell, 2008. 14(6): p. 818-29.
4. Thiery, J.P. and J.P. Sleeman, Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol, 2006. 7(2): p. 131-42.
5. Hawinkels, L.J., H.W. Verspaget, W. van Duijn, J.M. van der Zon, K. Zuidwijk, F.J. Kubben, J.H. Verheijen, D.W. Hommes, C.B. Lamers and C.F. Sier, Tissue level, activation and cellular localisation of TGF-beta1 and association with survival in gastric cancer patients. Br J Cancer, 2007. 97(3): p. 398-404.
6. Langenskiold, M., L. Holmdahl, P. Falk, E. Angenete and M.L. Ivarsson, Increased TGF-beta 1 protein expression in patients with advanced colorectal cancer. J Surg Oncol, 2008. 97(5): p. 409-15.
7. von Rahden, B.H., H.J. Stein, M. Feith, F. Puhringer, J. Theisen, J.R. Siewert and M. Sarbia, Overexpression of TGF-beta1 in esophageal (Barrett's) adenocarcinoma is associated with advanced stage of disease and poor prognosis. Mol Carcinog, 2006. 45(10): p. 786-94.
8. Gholamin, M., O. Moaven, B. Memar, M. Farshchian, H. Naseh, R. Malekzadeh, M. Sotoudeh, M.T. Rajabi-Mashhadi, M.N. Forghani, F. Farrokhi and M.R. Abbaszadegan-Overexpression and interactions of interleukin-10, transforming growth factor beta, and vascular endothelial growth factor in esophageal squamous cell carcinoma. World J Surg, 2009. 33(7): p. 1439-45.
9. Lopez-Novoa, J.M. and M.A. Nieto, Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med, 2009. 1(6-7): p. 303-14.
10. Vincent, T., E.P. Neve, J.R. Johnson, A. Kukalev, F. Rojo, J. Albanell, K. Pietras, I. Virtanen, L. Philipson, P.L. Leopold, R.G. Crystal, A.G. de Herreros, et al., A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol, 2009. 11(8): p. 943-50.
11. Zhang, L., F. Zhou, Y. Drabsch, R. Gao, B.E. Snaar-Jagalska, C. Mickanin, H. Huang, K.A. Sheppard, J.A. Porter, C.X. Lu and P. Ten Dijke, USP4 is regulated by AKT phosphorylation and directly deubiquitylates TGF-beta type I receptor. Nat Cell Biol, 2012. 14(7): p. 717-26.
12. Zhang, Y.E., Non-Smad pathways in TGF-beta signaling. Cell Res, 2009. 19(1): p. 128-39.
13. Shtivelman, E., A link between metastasis and resistance to apoptosis of variant small cell lung carcinoma. Oncogene, 1997. 14(18): p. 2167-73.
14. Ito, M., C. Jiang, K. Krumm, X. Zhang, J. Pecha, J. Zhao, Y. Guo, R.G. Roeder and H. Xiao, TIP30 deficiency increases susceptibility to tumorigenesis. Cancer Res, 2003. 63(24): p. 8763-7.
15. Lu, B., Y. Ma, G. Wu, X. Tong, H. Guo, A. Liang, W. Cong, C. Liu, H. Wang, M. Wu, J. Zhao and Y. Guo, Methylation of Tip30 promoter is associated with poor prognosis in human hepatocellular carcinoma. Clin Cancer Res, 2008. 14(22): p. 7405-12.
16. Zhao, J., H. Ni, Y. Ma, L. Dong, J. Dai, F. Zhao, X. Yan, B. Lu, H. Xu and Y. Guo, TIP30/CC3 expression in breast carcinoma: relation to metastasis, clinicopathologic parameters, and P53 expression. Hum Pathol, 2007. 38(2): p. 293-8.
17. Tong, X., K. Li, Z. Luo, B. Lu, X. Liu, T. Wang, M. Pang, B. Liang, M. Tan, M. Wu, J. Zhao and Y. Guo, Decreased TIP30 expression promotes tumor metastasis in lung cancer. Am J Pathol, 2009. 174(5): p. 1931-9.
18. Guo, S., W. Jing, X. Hu, X. Zhou, L. Liu, M. Zhu, F. Yin, R. Chen, J. Zhao and Y. Guo, Decreased TIP30 expression predicts poor prognosis in pancreatic cancer patients. Int J Cancer, 2014. 134(6): p. 1369-78.
19. Zhu, M., F. Yin, X. Fan, W. Jing, R. Chen, L. Liu, L. Zhang, Y. Liu, Y. Liang, F. Bu, X. Tong, H. Zheng, et al., Decreased TIP30 promotes Snail-mediated epithelial-mesenchymal transition and tumor-initiating properties in hepatocellular carcinoma. Oncogene, 2014.
20. Zhao, J., B. Lu, H. Xu, X. Tong, G. Wu, X. Zhang, A. Liang, W. Cong, J. Dai, H. Wang, M. Wu and Y. Guo, Thirty-kilodalton Tat-interacting protein suppresses tumor metastasis by inhibition of osteopontin transcription in human hepatocellular carcinoma. Hepatology, 2008. 48(1): p. 265-75.
21. Ye, Q.H., L.X. Qin, M. Forgues, P. He, J.W. Kim, A.C. Peng, R. Simon, Y. Li, A.I. Robles, Y. Chen, Z.C. Ma, Z.Q. Wu, et al., Predicting hepatitis B virus-positive metastatic hepatocellular carcinomas using gene expression profiling and supervised machine learning. Nat Med, 2003. 9(4): p. 416-23.
22. Micalizzi, D.S., K.L. Christensen, P. Jedlicka, R.D. Coletta, A.E. Baron, J.C. Harrell, K.B. Horwitz, D. Billheimer, K.A. Heichman, A.L. Welm, W.P. Schiemann and H.L. Ford, The Six1 homeoprotein induces human mammary carcinoma cells to undergo epithelial-mesenchymal transition and metastasis in mice through increasing TGF-beta signaling. J Clin Invest, 2009. 119(9): p. 2678-90.
23. Zhao, L., W. Li, W. Zang, Z. Liu, X. Xu, H. Yu, Q. Yang and J. Jia, JMJD2B promotes epithelial-mesenchymal transition by cooperating with beta-catenin and enhances gastric cancer metastasis. Clin Cancer Res, 2013. 19(23): p. 6419-29.
24. Sanchez-Tillo, E., O. de Barrios, L. Siles, M. Cuatrecasas, A. Castells and A. Postigo, beta-catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness. Proc Natl Acad SciUSA, 2011. 108(48): p. 19204-9.
25. Zhang, C., A. Li, X. Zhang and H. Xiao, A novel TIP30 protein complex regulates EGF receptor signaling and endocytic degradation. J Biol Chem, 2011. 286(11): p. 9373-81.
26. Li, A., C. Zhang, S. Gao, F. Chen, C. Yang, R. Luo and H. Xiao, TIP30 loss enhances cytoplasmic and nuclear EGFR signaling and promotes lung adenocarcinogenesis in mice. Oncogene, 2012.
27. Zhang, W., H.C. Sun, W.Q. Wang, Q.B. Zhang, P.Y. Zhuang, Y.Q. Xiong, X.D. Zhu, H.X. Xu, L.Q. Kong, W.Z. Wu, L. Wang, T.Q. Song, et al., Sorafenib down-regulates expression of HTATIP2 to promote invasiveness and metastasis of orthotopic hepatocellular carcinoma tumors in mice. Gastroenterology, 2012. 143(6): p. 1641-1649 e5.
28. Zhang, Q., L. Chen, B.T. Helfand, T.L. Jang, V. Sharma, J. Kozlowski, T.M. Kuzel, L.J. Zhu, X.J. Yang, B. Javonovic, Y. Guo, S. Lonning, et al., TGF-beta regulates DNA methyltransferase expression in prostate cancer, correlates with aggressive capabilities, and predicts disease recurrence. PLoS One, 2011. 6(9): p. e25168.
29. Bechtel, W., S. McGoohan, E.M. Zeisberg, G.A. Muller, H. Kalbacher, D.J. Salant, C.A. Muller, R. Kalluri and M. Zeisberg, Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat Med, 2010. 16(5): p. 544-50.
30. You, H., W. Ding and C.B. Rountree, Epigenetic regulation of cancer stem cell marker CD133 by transforming growth factor-beta. Hepatology, 2010. 51(5): p. 1635-44.
31. Robertson, K.D., DNA methylation, methyltransferases, and cancer. Oncogene, 2001. 20(24): p. 3139-55.
32. Ikushima, H. and K. Miyazono, TGFbeta signalling: a complex web in cancer progression. Nat Rev Cancer, 2010. 10(6): p. 415-24.
33. Massague, J., TGFbeta in Cancer. Cell, 2008. 134(2): p. 215-30.
34. Adorno, M., M. Cordenonsi, M. Montagner, S. Dupont, C. Wong, B. Hann, A. Solari, S. Bobisse, M.B. Rondina, V. Guzzardo, A.R. Parenti, A. Rosato, et al., A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell, 2009. 137(1): p. 87-98.
35. Smith, A.P., A. Verrecchia, G. Faga, M. Doni, D. Perna, F. Martinato, E. Guccione and B. Amati, A positive role for Myc in TGFbeta-induced Snail transcription and epithelial-to-mesenchymal transition. Oncogene, 2009. 28(3): p. 422-30.
36. Tao, Q., L.J. Swinnen, J. Yang, G. Srivastava, K.D. Robertson and R.F. Ambinder, Methylation status of the Epstein-Barr virus major latent promoter C in iatrogenic B cell lymphoproliferative disease. Application of PCR-based analysis. Am J Pathol, 1999. 155(2): p. 619-25.
37. Urakami, S., H. Shiina, H. Enokida, T. Kawakami, T. Tokizane, T. Ogishima, Y. Tanaka, L.C. Li, L.A. Ribeiro-Filho, M. Terashima, N. Kikuno, H. Adachi, et al., Epigenetic inactivation of Wnt inhibitory factor-1 plays an important role in bladder cancer through aberrant canonical Wnt/beta-catenin signaling pathway. Clin Cancer Res, 2006. 12(2): p. 383-91.
38. Montserrat, N., A. Gallardo, D. Escuin, L. Catasus, J. Prat, F.J. Gutierrez-Avigno, G. Peiro, A. Barnadas and E. Lerma, Repression of E-cadherin by SNAIL, ZEB1, and TWIST in invasive ductal carcinomas of the breast: a cooperative effort? Hum Pathol, 2011. 42(1): p. 103-10.