YAP activation is an early event and a potential therapeutic target in liver cancer development

Journal of Hepatology

Volumn 61, Issue 5, 2014, Pages 1088-1096

  Perra, Andrea ^a   Kowalik, Marta Anna ^a   Ghiso, Elena ^b   Ledda Columbano, Giovanna Maria ^a   Di Tommaso, Luca ^c   Angioni, Maria Maddalena ^a   Raschioni, Carlotta ^c   Testore, Elena ^b   Roncalli, Massimo ^c   Giordano, Silvia ^b   Columbano, Amedeo ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

HCC; Hippo pathway; Preneoplastic stages; TCPOBOP; Verteporfin

Indexed keywords

1,4 BIS(3,5 DICHLORO 2 PYRIDYLOXY)BENZENE; DIETHYLNITROSAMINE; LIGASE; MICRORNA 375; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VERTEPORFIN; YES ASSOCIATED PROTEIN; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; HIPPO PROTEIN, HUMAN; MICRORNA; MIRN375 MICRORNA, HUMAN; PHOSPHOPROTEIN; PORPHYRIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; YAP PROTEIN, MOUSE; YAP PROTEIN, RAT; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

ADULT; AGED; ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL VIABILITY; CHEMICAL CARCINOGENESIS; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; HEPATOMEGALY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER ADENOMA; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; LUNG METASTASIS; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PRECANCER; PRIORITY JOURNAL; RAT; RAT MODEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WILD TYPE; YOUNG ADULT; ADENOMA, LIVER CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; DRUG EFFECTS; FISCHER 344 RAT; GENETICS; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; METABOLISM; PRECANCEROUS CONDITIONS; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOMA, LIVER CELL; ADULT; AGED; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GENE EXPRESSION; HUMANS; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICRORNAS; MIDDLE AGED; PHOSPHOPROTEINS; PORPHYRINS; PRECANCEROUS CONDITIONS; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, INBRED F344; SIGNAL TRANSDUCTION; YOUNG ADULT;

EID: 84930204654     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2014.06.033     Document Type: Article

References (34)

1. Forner A, Llovet JM, Bruix J. Hepatocellular carcinoma. Lancet 2012;379: 1245-1255.
2. Villanueva A, Minguez B, Forner A, Reig M, Llovet JM. Hepatocellular carcinoma: Novel molecular approaches for diagnosis, prognosis, and therapy. Annu Rev Med 2010;61: 317-328.
3. 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: 1120-1133.
4. Pan D. The hippo signaling pathway in development and cancer. Dev Cell 2010;19: 491-505.
5. Li H, Wolfe A, Septer S, Edwards G, Zhong X, Abdulkarim AB, et al. Deregulation of Hippo kinase signalling in human hepatic malignancies. Liver Int 2012;32: 38-47.
6. Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumourigenesis: An updated version. Genes Dev 2010;24: 862-874.
7. Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, et al. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol 2007;17: 2054-2060.
8. 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: 425-438.
9. 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: 1437-1442.
10. 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: 1431-1436.
11. Lee KP, Lee JH, Kim TS, Kim TH, Park HD, Byun JS, et al. The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis. Proc Natl Acad Sci U S A 2010;107: 8248-8253.
12. 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: 1253-1267.
13. Steinhardt AA, Gayyed MF, Klein AP, Dong J, Maitra A, Pan D, et al. Expression of Yes-Associated protein in common solid tumors. Hum Pathol 2008;39: 1582-1589.
14. 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: 4576-4585.
15. Zheng T, Wang J, Jiang H, Liu L. Hippo signaling in oval cells and hepatocarcinogenesis. Cancer Lett 2011;302: 91-99.
16. Fausto N, Campbell JS. The role of hepatocytes and oval cells in liver regeneration and repopulation. Mech Dev 2003;120: 117-130.
17. Sell S. Liver stem cells. Mod Pathol 1994;7: 105-112.
18. Shinozuka H, Lombardi B, Sell S, Iammarino RE. Early histological and functional alterations of ethionine liver carcinogenesis in rats fed a choline deficient diet. Cancer Res 1978;38: 1092-1098.
19. Solt D, Farber E. New principle for analysis of liver carcinogenesis. Am J Pathol 1976;88: 595-618.
20. Perra A, Kowalik MA, Pibiri M, Ledda-Columbano GM, Columbano A. Thyroid hormone receptor ligands induce regression of rat preneoplastic liver lesions causing their reversion to a differentiated phenotype. Hepatology 2009;49: 1287-1296.
21. Giambarresi LI, Katyal SL, Lombardi B. Promotion of liver carcinogenesis in the rat by a choline-devoid diet: Role of liver cell necrosis and regeneration. Br J Cancer 1982;46: 825-829.
22. Petrelli A, Perra A, Cora D, Sulas P, Menegon S, Manca C, et al. MicroRNA/gene profiling unveils early molecular changes and nuclear factor erythroid related factor 2 (NRF2) activation in a rat model recapitulating human hepatocellular carcinoma (HCC). Hepatology 2014;59: 228-241.
23. Migliore C, Petrelli A, Ghiso E, Corso S, Capparuccia L, Eramo A, et al. MicroRNAs impair MET-mediated invasive growth. Cancer Res 2008;68: 10128-10136.
24. Thoolen B, Ten Kate FJ, van Diest PJ, Malarkey DE, Elmore SA, Maronpot RR. Comparative histomorphological review of rat and human hepatocellular proliferative lesions. J Toxicol Pathol 2012;25: 189-199.
25. Zhao B, Li L, Tumaneng K, Wang CY, Guan KL. A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev 2010;24: 72-85.
26. Liu AM, Poon RT, Luk JM. MicroRNA-375 targets Hippo-signaling effector YAP in liver cancer and inhibits tumor properties. Biochem Biophys Res Commun 2010;394: 623-627.
27. Kowalik MA, Saliba C, Pibiri M, Perra A, Ledda-Columbano GM, Sarotto I, et al. Yes-Associated protein regulation of adaptive liver enlargement and hepatocellular carcinoma development in mice. Hepatology 2011;53: 2086-2096.
28. Devereux TR, Anna CH, Foley JF, White CM, Sills RC, Barrett JC. Mutation of beta-catenin is an early event in chemically induced mouse hepatocellular carcinogenesis. Oncogene 1999;18: 4726-4733.
29. Liu-Chittenden Y, Huang B, Shim JS, Chen Q, Lee SJ, Anders RA, et al. Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev 2012;26: 1300-1305.
30. Sawada A, Kiyonari H, Ukita K, Nishioka N, Imuta Y, Sasaki H. Redundant roles of Tead1 and Tead2 in notochord development and the regulation of cell proliferation and survival. Mol Cell Biol 2008;28: 3177-3189.
31. Komuro A, Nagai M, Navin NE, Sudol M.WWdomain-containing protein YAP associates with ErbB-4 and acts as a co-Transcriptional activator for the carboxyl-Terminal fragment of ErbB-4 that translocates to the nucleus. J Biol Chem 2003;278: 33334-33341.
32. Lujambio A, Lowe SW. The microcosmos of cancer. Nature 2012;482: 347-355.
33. 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: 1530-1542.
34. Anakk S, Bhosale M, Schmidt VA, Johnson RL, Finegold MJ, Moore DD. Bile acids activate YAP to promote liver carcinogenesis. Cell Rep 2013;27: 1060-1069.