An imbalance in TAZ and YAP expression in hepatocellular carcinoma confers cancer stem cell-like behaviors contributing to disease progression

Cancer Research

Volumn 75, Issue 22, 2015, Pages 4985-4997

  Hayashi, Hiromitsu ^a,b   Higashi, Takaaki ^a   Yokoyama, Naomi ^a   Kaida, Takayoshi ^a   Sakamoto, Keita ^a   Fukushima, Yukiko ^a   Ishimoto, Takatsugu ^c   Kuroki, Hideyuki ^a   Nitta, Hidetoshi ^a   Hashimoto, Daisuke ^a   Chikamoto, Akira ^a   Oki, Eiji ^d   Beppu, Toru ^e   Baba, Hideo ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b SAISEIKAI KUMAMOTO HOSPITAL   (Japan)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d KYUSHU UNIVERSITY   (Japan)

^e KUMAMOTO UNIVERSITY HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CURCUMIN; FLUOROURACIL; MAMMALIAN TARGET OF RAPAMYCIN; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TAZ PROTEIN; THY 1 ANTIGEN; TUMOR MARKER; UNCLASSIFIED DRUG; YAP PROTEIN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TAZ PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRANSCRIPTOME; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER STEM CELL; CELL FUNCTION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INACTIVATION; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRACELLULAR SIGNALING; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CHROMATIN IMMUNOPRECIPITATION; DISEASE COURSE; DRUG RESISTANCE; GENE SILENCING; IMMUNOHISTOCHEMISTRY; LIVER TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; NEOPLASTIC STEM CELLS; PHOSPHOPROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84955270341     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0291     Document Type: Article

References (34)

1. Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 2010;24:862-74.
2. Huang J, Wu S, Barrera J, Matthews K, Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 2005;122: 421-34.
3. Pantalacci S, Tapon N, Leopold P. The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat Cell Biol 2003;5:921-7.
4. Varelas X, Sakuma R, Samavarchi-Tehrani P, Peerani R, Rao BM, Dembowy J, et al. TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 2008;10:837-48.
5. Zhou D, Conrad C, Xia F, Park JS, Payer B, Yin Y, et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009;16:425-38.
6. Song H, Mak KK, Topol L, Yun K, Hu J, Garrett L, et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc Natl Acad Sci U S A 2010;107:1431-6.
7. Lu L, Li Y, Kim SM, Bossuyt W, Liu P, Qiu Q, et al. Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc Natl Acad Sci U S A 2010;107:1437-42.
8. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, et al. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007;130:1120-33.
9. Tschaharganeh DF, Chen X, Latzko P, Malz M, Gaida MM, Felix K, et al. Yesassociated protein up-regulates Jagged-1 and activates the Notch pathway in human hepatocellular carcinoma. Gastroenterology 2013;144:1530-42 e12.
10. Xu MZ, Yao TJ, Lee NP, Ng IO, Chan YT, Zender L, et al. Yes-associated protein is an independent prognostic marker in hepatocellular carcinoma. Cancer 2009;115:4576-85.
11. Zhang T, Zhang J, You X, Liu Q, Du Y, Gao Y, et al. Hepatitis B virus X protein modulates oncogene Yes-associated protein by CREB to promote growth of hepatoma cells. Hepatology 2012;56:2051-9.
12. Zhou D, Zhang Y, Wu H, Barry E, Yin Y, Lawrence E, et al. Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc Natl Acad Sci U S A 2011;108: E1312-20.
13. Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, et al. The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 2011;147:759-72.
14. Zhou Z, Hao Y, Liu N, Raptis L, Tsao MS, Yang X. TAZ is a novel oncogene in non-small cell lung cancer. Oncogene 2011;30:2181-6.
15. Zender L, Spector MS, Xue W, Flemming P, Cordon-Cardo C, Silke J, et al. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 2006;125:1253-67.
16. Han SX, Bai E, Jin GH, He CC, Guo XJ, Wang LJ, et al. Expression and clinical significance of YAP, TAZ, and AREG in hepatocellular carcinoma. J Immunol Res 2014;2014:261365.
17. Xiao H, Jiang N, Zhou B, Liu Q, Du C. TAZ regulates cell proliferation and epithelial-mesenchymal transition of human hepatocellular carcinoma. Cancer Sci 2015;106:151-9.
18. Hayashi H, Sakai K, Baba H, Sakai T. Thrombospondin-1 is a novel negative regulator of liver regeneration after partial hepatectomy through transforming growth factor-beta1 activation in mice. Hepatology 2012;55: 1562-73.
19. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 2011;19:387-400.
20. Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, et al. CD44s regulates the TGF-b-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res 2012;72:3414-23.
21. Hayashi H, Beppu T, Sakamoto Y, Miyamoto Y, Yokoyama N, Higashi T, et al. Prognostic value of Ki-67 expression in conversion therapy for colorectal liver-limited metastases. Am J Cancer Res 2015;5:1225-33.
22. Mao B, Hu F, Cheng J, Wang P, Xu M, Yuan F, et al. SIRT1 regulates YAP2-mediated cell proliferation and chemoresistance in hepatocellular carcinoma. Oncogene 2014;33:1468-74.
23. Touil Y, Igoudjil W, Corvaisier M, Dessein AF, Vandomme J, Monte D, et al. Colon cancer cells escape 5FU chemotherapy-induced cell death by entering stemness and quiescence associated with the c-Yes/YAP axis. Clin Cancer Res 2014;20:837-46.
24. Wendel HG, De Stanchina E, Fridman JS, Malina A, Ray S, Kogan S, et al. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 2004;428:332-7.
25. Yamashita T, Honda M, Nakamoto Y, Baba M, Nio K, Hara Y, et al. Discrete nature of EpCAM+ and CD90+ cancer stem cells in human hepatocellular carcinoma. Hepatology 2013;57:1484-97.
26. Haraguchi N, Ishii H, Mimori K, Tanaka F, Ohkuma M, Kim HM, et al. CD13 is a therapeutic target in human liver cancer stem cells. J Clin Invest 2010;120:3326-39.
27. Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008;13: 153-66.
28. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell 2007;129:465-72.
29. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 2002;298:597-600.
30. Hashimoto N, Tsunedomi R, Yoshimura K, Watanabe Y, Hazama S, Oka M. Cancer stem-like sphere cells induced from de-differentiated hepatocellular carcinoma-derived cell lines possess the resistance to anti-cancer drugs. BMC Cancer 2014;14:722.
31. Liu H, Liang Y, Wang L, Tian L, Song R, Han T, et al. In vivo and in vitro suppression of hepatocellular carcinoma by EF24, a curcumin analog. PLoS One 2012;7:e48075.
32. Darvesh AS, Aggarwal BB, Bishayee A. Curcumin and liver cancer: a review. Curr Pharm Biotechnol 2012;13:218-28.
33. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007;132:2557-76.
34. Chowdhury A, Santra A, Chakravorty R, Banerji A, Pal S, Dhali GK, et al. Community-based epidemiology of hepatitis B virus infection in West Bengal, India: prevalence of hepatitis B e antigen-negative infection and associated viral variants. J Gastroenterol Hepatol 2005;20: 1712-20.