Hellebrigenin induces cell cycle arrest and apoptosis in human hepatocellular carcinoma HepG2 cells through inhibition of Akt

Chemico-Biological Interactions

Volumn 219, Issue , 2014, Pages 184-194

  Deng, Li Juan ^a   Hu, Li Ping ^a   Peng, Qun Long ^a   Yang, Xiao Lin ^a   Bai, Liang Liang ^a   Yiu, Anita ^b   Li, Yong ^a   Tian, Hai Yan ^a   Ye, Wen Cai ^a   Zhang, Dong Mei ^a  

^a JINAN UNIVERSITY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Akt; Apoptosis; Cell cycle; DNA damage; Hellebrigenin; Hepatocellular carcinoma

Indexed keywords

ATM PROTEIN; BUFADIENOLIDE DERIVATIVE; CASPASE; CHECKPOINT KINASE 2; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; CYTOCHROME C; DNA; HELLEBRIGENIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE; SERINE; SMALL INTERFERING RNA; SOMATOMEDIN C; TYROSINE; UNCLASSIFIED DRUG; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN CDC25C; CCNB1 PROTEIN, HUMAN; CDC25C PROTEIN, HUMAN; CDK1 PROTEIN, HUMAN; CHEK2 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL VIABILITY; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME RELEASE; G2 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL CARCINOMA; LIVER MITOCHONDRION; MITOCHONDRIAL MEMBRANE POTENTIAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; UPREGULATION; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL STRUCTURE; COMET ASSAY; DRUG ISOLATION; FLOW CYTOMETRY; HEPG2 CELL LINE; IMMUNOFLUORESCENCE; MITOCHONDRION; MOLECULAR MECHANICS; PROTEIN PHOSPHORYLATION; ANTAGONISTS AND INHIBITORS; CARCINOMA, HEPATOCELLULAR; CELL CYCLE CHECKPOINT; CELL SURVIVAL; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; LIVER NEOPLASMS; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; BUFANOLIDES; CARCINOMA, HEPATOCELLULAR; CDC25 PHOSPHATASES; CELL CYCLE CHECKPOINTS; CELL SURVIVAL; CHECKPOINT KINASE 2; COMET ASSAY; CYCLIN B1; CYCLIN-DEPENDENT KINASES; DNA DAMAGE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MEMBRANE POTENTIAL, MITOCHONDRIAL; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84903826724     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2014.06.003     Document Type: Article

References (48)

1. G. Giannelli, A. Mazzocca, E. Fransvea, M. Lahn, and S. Antonaci Inhibiting TGF-beta signaling in hepatocellular carcinoma Biochim. Biophys. Acta 2011 1815 214 223
2. M. Thomas Molecular targeted therapy for hepatocellular carcinoma J. Gastroenterol. 44 2009 136 141
3. D.J. Newman, G.M. Cragg, S. Holbeck, and E.A. Sausville Natural products and derivatives as leads to cell cycle pathway targets in cancer chemotherapy Curr. Cancer Drug Targets 2 2002 279 308 (Pubitemid 35303466)
4. J.A. Fresno Vara, E. Casado, J. de Castro, P. Cejas, C. Belda-Iniesta, and M. Gonzalez-Baron PI3K/Akt signalling pathway and cancer Cancer Treat Rev. 30 2004 193 204
5. N.K. Saxena, D. Sharma, X.K. Ding, S.B. Lin, F. Marra, D. Merlin, and F.A. Anania Concomitant activation of the JAK/STAT, PI3K/AKT, and ERK signaling is involved in leptin-mediated promotion of invasion and migration of hepatocellular carcinoma cells Cancer Res. 67 2007 2497 2507 (Pubitemid 46548934)
6. M. Falasca PI3K/Akt signalling pathway specific inhibitors: a novel strategy to sensitize cancer cells to anti-cancer drugs Curr. Pharm. Des. 16 2010 1410 1416
7. A.G. Tempone, D.C. Pimenta, I. Lebrun, P. Sartorelli, N.N. Taniwaki, H.F. de Andrade Jr., M.M. Antoniazzi, and C. Jared Antileishmanial and antitrypanosomal activity of bufadienolides isolated from the toad Rhinella jimi parotoid macrogland secretion Toxicon 52 2008 13 21
8. +-ATPase Mol. Cancer 12 2013 33
9. Y. Kamano, A. Kotake, H. Hashima, M. Inoue, H. Morita, K. Takeya, H. Itokawa, N. Nandachi, T. Segawa, A. Yukita, K. Saitou, M. Katsuyama, and G.R. Pettit Structure-cytotoxic activity relationship for the toad poison bufadienolides Bioorg. Med. Chem. 6 1998 1103 1115 (Pubitemid 28464541)
10. G.A. Cunha, I.S. Resck, B.C. Cavalcanti, C.O. Pessoa, M.O. Moraes, J.R.O. Ferreira, F.A.R. Rodrigues, and M.L. dos Santos Cytotoxic profile of natural and some modified bufadienolides from toad Rhinella schneideri parotoid gland secretion Toxicon 56 2010 339 348
11. H.-Y. Tian, L. Wang, X.-Q. Zhang, D.-M. Zhang, Y. Wang, J.-S. Liu, R.-W. Jiang, and W.-C. Ye New bufadienolides and C23 steroids from the venom of Bufo bufo gargarizans Steroids 75 2010 884 890
12. 2/M cell cycle arrest and apoptosis Eur. J. Pharmacol. 692 2012 19 28
13. J.M. Shi, L.L. Bai, D.M. Zhang, A. Yiu, Z.Q. Yin, W.L. Han, J.S. Liu, Y. Li, D.Y. Fu, and W.C. Ye Saxifragifolin D induces the interplay between apoptosis and autophagy in breast cancer cells through ROS-dependent endoplasmic reticulum stress Biochem. Pharmacol. 85 2013 913 926
14. H. Shirai, A.R. Poetsch, A. Gunji, D. Maeda, H. Fujimori, H. Fujihara, T. Yoshida, H. Ogino, and M. Masutani PARG dysfunction enhances DNA double strand break formation in S-phase after alkylation DNA damage and augments different cell death pathways Cell Death Dis. 4 2013
15. 2/M transition Cancer Sci. 101 2010 1403 1408
16. I. Nilsson, and I. Hoffmann Cell cycle regulation by the Cdc25 phosphatase family Prog. Cell Cycle Res. 4 2000 107 114
17. M.B. Kastan, and J. Bartek Cell-cycle checkpoints and cancer Nature 432 2004 316 323 (Pubitemid 39551659)
18. J.S. Yuan, R. Adamski, and J.J. Chen Focus on histone variant H2AX: to be or not to be FEBS Lett. 584 2010 3717 3724
19. G. Kroemer, L. Galluzzi, and C. Brenner Mitochondrial membrane permeabilization in cell death Physiol. Rev. 87 2007 99 163 (Pubitemid 46209992)
20. S.W. Tait, and D.R. Green Mitochondria and cell death: outer membrane permeabilization and beyond Nat. Rev. Mol. Cell Biol. 11 2010 621 632
21. P. Li, D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade Cell 91 1997 479 489 (Pubitemid 27508237)
22. D.A. Altomare, and J.R. Testa Perturbations of the AKT signaling pathway in human cancer Oncogene 24 2005 7455 7464 (Pubitemid 41637985)
23. S.H. Zhang, Y. Zhang, Y. Zhuang, J.J. Wang, J.Q. Ye, S. Zhang, J.B. Wu, K. Yu, and Y.X. Han Matrine induces apoptosis in human acute myeloid leukemia cells via the mitochondrial pathway and Akt inactivation PLoS One 7 2012
24. F.H. Qi, A.Y. Li, Y. Inagaki, N. Kokudo, S. Tamura, M. Nakata, and W. Tang Antitumor activity of extracts and compounds from the skin of the toad Bufo bufo gargarizans Cantor Int. Immunopharmacol. 11 2011 342 349
25. K.Q. Han, G. Huang, W. Gu, Y.H. Su, X.Q. Huang, and C.Q. Ling Anti-tumor activities and apoptosis-regulated mechanisms of bufalin on the orthotopic transplantation tumor model of human hepatocellular carcinoma in nude mice World J. Gastroenterol. 13 2007 3374 3379 (Pubitemid 47062250)
26. J.S. Kim, T.Y. Jeong, C.K. Cho, Y.W. Lee, and H.S. Yoo Antitumor effect of skin of venenum bufonis in a NCI-H460 tumor regression model J. Acupunct. Meridian Stud. 3 2010 181 187
27. Y. Kamano, A. Yamashita, T. Nogawa, H. Morita, K. Takeya, H. Itokawa, T. Segawa, A. Yukita, K. Saito, M. Katsuyama, and G.R. Pettit QSAR evaluation of the Ch'an Su and related bufadienolides against the colchicine-resistant primary liver carcinoma cell line PLC/PRF/5(1) J. Med. Chem. 45 2002 5440 5447 (Pubitemid 35424962)
28. F. Qi, Y. Inagaki, B. Gao, X. Cui, H. Xu, N. Kokudo, A. Li, and W. Tang Bufalin and cinobufagin induce apoptosis of human hepatocellular carcinoma cells via Fas- and mitochondria-mediated pathways Cancer Sci. 102 2011 951 958
29. D.Z. Qiu, Z.J. Zhang, W.Z. Wu, and Y.K. Yang Bufalin, a component in Chansu, inhibits proliferation and invasion of hepatocellular carcinoma cells BMC Complement. Altern. Med. 13 2013 185
30. H.Y. Tian, L. Wang, X.Q. Zhang, Y. Wang, D.M. Zhang, R.W. Jiang, Z. Liu, J.S. Liu, Y.L. Li, and W.C. Ye Bufogargarizins A and B: two novel 19-norbufadienolides with unprecedented skeletons from the venom of Bufo bufo gargarizans Chemistry 16 2010 10989 10993
31. H.Y. Tian, S.L. Luo, J.S. Liu, L. Wang, Y. Wang, D.M. Zhang, X.Q. Zhang, R.W. Jiang, and W.C. Ye C23 steroids from the venom of Bufo bufo gargarizans J. Nat. Prod. 76 2013 1842 1847
32. L. Ma, B. Song, H. Jin, J. Pi, L. Liu, J. Jiang, and J. Cai Cinobufacini induced MDA-MB-231 cell apoptosis-associated cell cycle arrest and cytoskeleton function Bioorg. Med. Chem. Lett. 22 2012 1459 1463
33. N. Takai, T. Ueda, M. Nishida, K. Nasu, and H. Narahara Bufalin induces growth inhibition, cell cycle arrest and apoptosis in human endometrial and ovarian cancer cells Int. J. Mol. Med. 21 2008 637 643
34. J. Smith, L.M. Tho, N. Xu, and D.A. Gillespie The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer Adv. Cancer Res. 108 2010 73 112
35. A.H. Kim, G. Khursigara, X. Sun, T.F. Franke, and M.V. Chao Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1 Mol. Cell Biol. 21 2001 893 901 (Pubitemid 32104737)
36. K. Katayama, N. Fujita, and T. Tsuruo Akt/protein kinase B-dependent phosphorylation and inactivation of WEE1Hu promote cell cycle progression at G2/M transition Mol. Cell Biol. 25 2005 5725 5737 (Pubitemid 40853605)
37. E. Di Gennaro, F. Bruzzese, M. Caraglia, A. Abruzzese, and A. Budillon Acetylation of proteins as novel target for antitumor therapy: review article Amino Acids 26 2004 435 441 (Pubitemid 39093148)
38. W. Gu, and R.G. Roeder Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain Cell 90 1997 595 606 (Pubitemid 27357952)
39. J. Boyes, P. Byfield, Y. Nakatani, and V. Ogryzko Regulation of activity of the transcription factor GATA-1 by acetylation Nature 396 1998 594 598 (Pubitemid 28563723)
40. J. Makarević, N. Tawanaie, E. Juengel, M. Reiter, J. Mani, I. Tsaur, G. Bartsch, A. Haferkamp, and R.A. Blaheta Cross-communication between histone H3 and H4 acetylation and Akt-mTOR signalling in prostate cancer cells J. Cell Mol. Med. 2014
41. K.-W. Shim, G. Xi, B.-M. Farnell, D.-S. Kim, T. Tsurubuchi, T. Tomita, and C.S. Mayanil Epigenetic modification after inhibition of IGF-1R signaling in human central nervous system atypical teratoid rhabdoid tumor (AT/RT) Child's Nerv. Syst. 29 2013 1245 1251
42. +-ATPase alpha3 mediates sensitivity of hepatocellular carcinoma cells to bufalin Oncol. Rep. 25 2011 825 830
43. H. Klupp Quantitative comparison of the positively inotropic and of the toxic effect of several cardiac glycosides Naunyn-Schmiedebergs Archiv für experimentelle Pathologie und Pharmakologie 252 1966 314
44. P.S. Steyn, and F.R. van Heerden Bufadienolides of plant and animal origin Nat. Prod. Rep. 15 1998 397 413 (Pubitemid 28397881)
45. K.K. Chen, and A. Kovarikova Pharmacology and toxicology of toad venom J. Pharm. Sci. 56 1967 1535 1541
46. H.M. Gao, R. Popescu, B. Kopp, and Z.M. Wang Bufadienolides and their antitumor activity Nat. Prod. Rep. 28 2011 953 969
47. K.L. Hu, L. Zhu, H.Y. Liang, F.Q. Hu, and J.F. Feng Improved antitumor efficacy and reduced toxicity of liposomes containing bufadienolides Arch. Pharmacol. Res. 34 2011 1487 1494
48. J. Dewelle, Y.M. El, Q.E. Van, N.N. De, T. Mijatovic, L. Ingrassia, R. Kiss, V.F. Van, N. Heureux, Hellebrin and hellebrigenin derivatives, Google Patents, 2010.