Pro-apoptotic Sorafenib signaling in murine hepatocytes depends on malignancy and is associated with PUMA expression in vitro and in vivo

Cell Death and Disease

Volumn 5, Issue , 2014, Pages

  Sonntag, R ^a   Gassler, N ^a   Bangen, J M ^a   Trautwein, C ^a   Liedtke, C ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

hepatocellular carcinoma; liver regeneration; mitotic catastrophe; partial hepatectomy; syngeneic transplantation model

Indexed keywords

CASPASE 3; CYCLIN A2; CYCLIN B1; CYCLIN D1; CYCLIN E1; CYCLINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BCL 2; PUMA PROTEIN; RETINOBLASTOMA PROTEIN; SORAFENIB; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CARBANILAMIDE DERIVATIVE; DRUG DERIVATIVE; NICOTINAMIDE; PUMA PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; HEPATOMA CELL; IN VITRO STUDY; IN VIVO STUDY; ISOGRAFT; LIVER CELL; LIVER CELL CARCINOMA; LIVER REGENERATION; LOW DRUG DOSE; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LIVER TUMOR; MALE; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CELL CYCLE; CELLS, CULTURED; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED C57BL; NIACINAMIDE; PHENYLUREA COMPOUNDS; TUMOR SUPPRESSOR PROTEINS;

EID: 84957534864     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.557     Document Type: Article

References (33)

1. Marra M, Sordelli IM, Lombardi A, Lamberti M, Tarantino L, Giudice A et al. Molecular targets and oxidative stress biomarkers in hepatocellular carcinoma: an overview. J Transl Med 2011; 9: 171.
2. Montella L, Addeo R, Caraglia M, Del Prete S. Latest developments in targeted therapy for hepatocellular carcinoma. Exp Rev Anticancer Ther 2010; 10: 1635-1646.
3. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008; 359: 378-390.
4. Llovet JM, Bruix J. Molecular targeted therapies in hepatocellular carcinoma. Hepatology 2008; 48: 1312-1327.
5. Wilhelm S, Carter C, Lynch M, Lowinger T, Dumas J, Smith RA et al. Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat Rev Drug Discov 2006; 5: 835-844.
6. Liu L, Cao Y, Chen C, Zhang X, McNabola A, Wilkie D et al. Sorafenib blocks the RAF/MEK/ERK pathway, inhibits tumor angiogenesis, and induces tumor cell apoptosis in hepatocellular carcinoma model PLC/PRF/5. Cancer Res 2006; 66: 11851-11858.
7. Bouillet P, Purton JF, Godfrey DI, Zhang LC, Coultas L, Puthalakath H et al. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature 2002; 415: 922-926.
8. Yu C, Bruzek LM, Meng XW, Gores GJ, Carter CA, Kaufmann SH et al. The role of Mcl-1 downregulation in the proapoptotic activity of the multikinase inhibitor BAY 43-9006. Oncogene 2005; 24: 6861-6869.
9. Darlington GJ, Bernhard HP, Miller RA. Ruddle FH. Expression of liver phenotypes in cultured mouse hepatoma cells. J Natl Cancer Inst 1980; 64: 809-819.
10. Downward J. PI 3-kinase, Akt and cell survival. Semin Cell Dev Biol 2004; 15: 177-182.
11. Hu W, Nevzorova YA, Haas U, Moro N, Sicinski P, Geng Y et al. Concurrent deletion of cyclin e1 and cyclin-dependent kinase 2 in hepatocytes inhibits DNA replication and liver regeneration in mice. Hepatology 2013; e-pub ahead of print 24 December 2013; doi:10.1002/hep.26584.
12. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000; 182: 311-322.
13. Diril MK, Ratnacaram CK, Padmakumar VC, Du T, Wasser M, Coppola V et al. Cyclindependent kinase 1 (Cdk1) is essential for cell division and suppression of DNA re-replication but not for liver regeneration. Proc Natl Acad Sci USA 2012; 109: 3826-3831.
14. Miyaoka Y, Ebato K, Kato H, Arakawa S, Shimizu S, Miyajima A. Hypertrophy and unconventional cell division of hepatocytes underlie liver regeneration. Curr Biol 2012; 22: 1166-1175.
15. Dudgeon C, Peng R, Wang P, Sebastiani A, Yu J, Zhang L. Inhibiting oncogenic signaling by sorafenib activates PUMA via GSK3beta and NF-kappaB to suppress tumor cell growth. Oncogene 2012; 31: 4848-4858.
16. Xie B, Wang DH, Spechler SJ. Sorafenib for treatment of hepatocellular carcinoma: a systematic review. Digest Dis Sci 2012; 57: 1122-1129.
17. Santini D, Addeo R, Vincenzi B, Calvieri A, Montella L, Silletta M et al. Exploring the efficacy and safety of single-agent sorafenib in a cohort of Italian patients with hepatocellular carcinoma. Exp Rev Anticancer Ther 2012; 12: 1283-1288.
18. Xu M, Xie XH, Xie XY, Xu ZF, Liu GJ, Zheng YL et al. Sorafenib suppresses the rapid progress of hepatocellular carcinoma after insufficient radiofrequency ablation therapy: an experiment in vivo. Acta Radiol 2013; 54: 199-204.
19. Nevzorova YA, Bangen JM, Hu W, Haas U, Weiskirchen R, Gassler N et al. Cyclin E1 controls proliferation of hepatic stellate cells and is essential for liver fibrogenesis in mice. Hepatology 2012; 56: 1140-1149.
20. Nevzorova YA, Tschaharganeh D, Gassler N, Geng Y, Weiskirchen R, Sicinski P et al. Aberrant cell cycle progression and endoreplication in regenerating livers of mice that lack a single E-type cyclin. Gastroenterology 2009; 137: 691-703; 703 e691-696.
21. Wang Y, Gao J, Zhang D, Zhang J, Ma J, Jiang H. New insights into the antifibrotic effects of sorafenib on hepatic stellate cells and liver fibrosis. J Hepatol 2010; 53: 132-144.
22. Chen YL, Lv J, Ye XL, Sun MY, Xu Q, Liu CH et al. Sorafenib inhibits transforming growth factor beta1-mediated epithelial-mesenchymal transition and apoptosis in mouse hepatocytes. Hepatology 2011; 53: 1708-1718.
23. Vick B, Weber A, Urbanik T, Maass T, Teufel A, Krammer PH et al. Knockout of myeloid cell leukemia-1 induces liver damage and increases apoptosis susceptibility of murine hepatocytes. Hepatology 2009; 49: 627-636.
24. Cazanave SC, Gores GJ. The liver's dance with death: two Bcl-2 guardian proteins from the abyss. Hepatology 2009; 50: 1009-1013.
25. Chen S, Zheng J, Hao Q, Yang S, Wang J, Chen H et al. p53-insensitive PUMA down-regulation is essential in the early phase of liver regeneration after partial hepatectomy in mice. J Hepatol 2010; 52: 864-871.
26. Hora C, Romanque P, Dufour JF. Effect of sorafenib on murine liver regeneration. Hepatology 2011; 53: 577-586.
27. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 2004; 64: 7099-7109.
28. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ 2008; 15: 1153-1162.
29. Wustefeld T, Rakemann T, Kubicka S, Manns MP, Trautwein C. Hyperstimulation with interleukin 6 inhibits cell cycle progression after hepatectomy in mice. Hepatology 2000; 32: 514-522.
30. Pietrangelo A, Dierssen U, Valli L, Garuti C, Rump A, Corradini E et al. STAT3 is required for IL-6-gp130-dependent activation of hepcidin in vivo. Gastroenterology 2007; 132: 294-300.
31. Dierssen U, Beraza N, Lutz HH, Liedtke C, Ernst M, Wasmuth HE et al. Molecular dissection of gp130-dependent pathways in hepatocytes during liver regeneration. J Biol Chem 2008; 283: 9886-9895.
32. Zschemisch NH, Liedtke C, Dierssen U, Nevzorova YA, Wustefeld T, Borlak J et al. Expression of a cyclin E1 isoform in mice is correlated with the quiescent cell cycle status of hepatocytes in vivo. Hepatology 2006; 44: 164-173.
33. Liedtke C, Lambertz D, Schnepel N, Trautwein C. Molecular mechanism of Mitomycin C-dependent caspase-8 regulation: implications for apoptosis and synergism with interferon-alpha signaling. Apoptosis 2007; 12: 2259-2270.