Antitumour activity on extrinsic apoptotic targets of the triterpenoid maslinic acid in p53-deficient Caco-2 adenocarcinoma cells

Biochimie

Volumn 95, Issue 11, 2013, Pages 2157-2167

  Reyes Zurita, Fernando J ^a   Rufino Palomares, Eva E ^a   Medina, Pedro P ^a   Leticia Garcia Salguero E ^a   Peragón, Juan ^b   Cascante, Marta ^c   Lupiáñez, José A ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF JAÉN   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Colon cancer cells; Extrinsic apoptotic pathway; Maslinic acid; Triterpenes

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; MASLINIC ACID; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; PROTEIN P53; STRESS ACTIVATED PROTEIN KINASE;

ADENOCARCINOMA; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL STRAIN CACO 2; CONTROLLED STUDY; ENZYME ACTIVATION; FLUORESCENCE ACTIVATED CELL SORTING; GENOTOXICITY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; OLIVE; PROTEIN CLEAVAGE; PROTEIN EXPRESSION;

OLEA EUROPAEA;

2-CYANO-3,12-DIOXOOLEAN-1,9-DIEN-28-OIC ACID; 4′,6-DIAMIDINO-2-PHENYLINDOLE; CDDO; COLON CANCER CELLS; DAPI; DIMETHYL SULFOXIDE; DMEM; DMSO; DULBECCO'S MODIFIED EAGLE'S MEDIUM; EXTRINSIC APOPTOTIC PATHWAY; FACS; FCS; FLUORESCENCE-ACTIVATED CELL SORTER; FOETAL CALF SERUM; MA; MASLINIC ACID; MITOCHONDRIAL MEMBRANE POTENTIAL; MMP; PI; PROPIDIUM IODIDE; RH123; RHODAMINE; TRITERPENES;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CACO-2 CELLS; CASPASE 3; CASPASE 8; GENE EXPRESSION REGULATION, NEOPLASTIC; HT29 CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MITOCHONDRIA; SIGNAL TRANSDUCTION; TRITERPENES;

EID: 84885063950     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2013.08.017     Document Type: Article

References (41)

1. R.G. Shao, C.X. Cao, W. Nieves-Neira, M.T. Dimanche-Boitrel, E. Solary, and Y. Pommier Activation of the Fas pathway independently of Fas ligand during apoptosis induced by camptothecin in p53 mutant human colon carcinoma cells Oncogene 20 2001 1852 1859
2. O. Micheau, E. Solary, A. Hammann, F. Martin, and M.T. Dimanche-Boitrel Sensitization of cancer cells treated with cytotoxic drugs to fas-mediated cytotoxicity J. Natl. Cancer Inst. 89 1997 783 789
3. O. Micheau, E. Solary, A. Hammann, and M.T. Dimanche-Boitrel Fas ligand-independent, FADD-mediated activation of the Fas death pathway by anticancer drugs J. Biol. Chem. 274 1999 7987 7992
4. E.E. Varfolomeev, and A. Ashkenazi Tumor necrosis factor: an apoptosis JuNKie? Cell 116 2004 491 497
5. A. Lin Activation of the JNK signaling pathway: breaking the brake on apoptosis Bioassays 25 2003 17 24
6. Y. Deng, X. Ren, L. Yang, Y. Lin, and X. Wu A JNK-dependent pathway is required for TNF alpha-induced apoptosis Cell 115 2003 61 70
7. C. Tournier, P. Hess, D.D. Yang, J. Xu, T.K. Turner, A. Nimnual, D. Bar-Sagi, S.N. Jones, R.A. Flavell, and R.J. Davis Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway Science 288 2000 870 874
8. H. Wajant, K. Pfizenmaier, and P. Scheurich Tumor necrosis factor signaling Cell Death Differ. 10 2003 45 65
9. X. Deng, L. Xiao, W. Lang, F. Gao, P. Ruvolo, and W.S. May Jr. Novel role for JNK as a stress-activated Bcl2 kinase J. Biol. Chem. 276 2001 23681 23688
10. K. Lei, A. Nimnual, W.X. Zong, N.J. Kennedy, R.A. Flavell, C.B. Thompson, D. Bar-Sagi, and R.J. Davis The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase Mol. Cell Biol. 22 2002 4929 4942
11. M. Fan, M. Goodwin, T. Vu, C. Brantley-Finley, W.A. Gaarde, and T.C. Chambers Vinblastine-induced phosphorylation of Bcl-2 and Bcl-XL is mediated by JNK and occurs in parallel with inactivation of the Raf-1/MEK/ERK cascade J. Biol. Chem. 275 2000 29980 29985
12. S. Fulda Betulinic acid: a natural product with anticancer activity Mol. Nutr. Food Res. 53 2009 140 146
13. R.C. Santos, J.A. Salvador, R. Cortes, G. Pachon, S. Marin, and M. Cascante New betulinic acid derivatives induce potent and selective antiproliferative activity through cell cycle arrest at the S phase and caspase dependent apoptosis in human cancer cells Biochimie 93 2011 1065 1075
14. Y. Ito, P. Pandey, A. Place, M.B. Sporn, G.W. Gribble, T. Honda, S. Kharbanda, and D. Kufe The novel triterpenoid 2-cyano-3,12-dioxoolean-1,9-dien- 28-oic acid induces apoptosis of human myeloid leukemia cells by a caspase-8-dependent mechanism Cell Growth Differ. 11 2000 261 267
15. Y. Ito, P. Pandey, M.B. Sporn, R. Datta, S. Kharbanda, and D. Kufe The novel triterpenoid CDDO induces apoptosis and differentiation of human osteosarcoma cells by a caspase-8 dependent mechanism Mol. Pharmacol. 59 2001 1094 1099
16. T.A. Stadheim, N. Suh, N. Ganju, M.B. Sporn, and A. Eastman The novel triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid (CDDO) potently enhances apoptosis induced by tumor necrosis factor in human leukemia cells J. Biol. Chem. 277 2002 16448 16455
17. T. Ikeda, M. Sporn, T. Honda, G.W. Gribble, and D. Kufe The novel triterpenoid CDDO and its derivatives induce apoptosis by disruption of intracellular redox balance Cancer Res. 63 2003 5551 5558
18. W. Zou, X. Liu, P. Yue, Z. Zhou, M.B. Sporn, R. Lotan, F.R. Khuri, and S.Y. Sun c-Jun NH2-terminal kinase-mediated up-regulation of death receptor 5 contributes to induction of apoptosis by the novel synthetic triterpenoid methyl-2-cyano-3,12-dioxooleana-1, 9-dien-28-oate in human lung cancer cells Cancer Res. 64 2004 7570 7578
19. X. Saelens, N. Festjens, L. Vande Walle, M. van Gurp, G. van Loo, and P. Vandenabeele Toxic proteins released from mitochondria in cell death Oncogene 23 2004 2861 2874
20. Y.K. Kim, S.K. Yoon, and S.Y. Ryu Cytotoxic triterpenes from stem bark of Physocarpus intermedius Planta Med. 66 2000 485 486
21. F.J. Reyes-Zurita, E.E. Rufino-Palomares, J.A. Lupianez, and M. Cascante Maslinic acid, a natural triterpene from Olea europaea L., induces apoptosis in HT29 human colon-cancer cells via the mitochondrial apoptotic pathway Cancer Lett. 273 2009 44 54
22. E. Rufino-Palomares, F.J. Reyes-Zurita, C.A. Fuentes-Almagro, M. de la Higuera, J.A. Lupianez, and J. Peragon Proteomics in the liver of gilthead sea bream (Sparus aurata) to elucidate the cellular response induced by the intake of maslinic acid Proteomics 11 2011 3312 3325
23. R.M. Ray, S.A. McCormack, and L.R. Johnson Polyamine depletion arrests growth of IEC-6 and Caco-2 cells by different mechanisms Am. J. Physiol. Gastrointest. Liver Physiol. 281 2001 G37 G43
24. S. Djelloul, M.E. Forgue-Lafitte, B. Hermelin, M. Mareel, E. Bruyneel, A. Baldi, A. Giordano, E. Chastre, and C. Gespach Enterocyte differentiation is compatible with SV40 large T expression and loss of p53 function in human colonic Caco-2 cells. Status of the pRb1 and pRb2 tumor suppressor gene products FEBS Lett. 406 1997 234 242
25. N.R. Rodrigues, A. Rowan, M.E. Smith, I.B. Kerr, W.F. Bodmer, J.V. Gannon, and D.P. Lane p53 Mutations in colorectal cancer Proc. Natl. Acad. Sci. U. S. A. 87 1990 7555 7559
26. A. Garcia-Granados Process for the industrial recovery of oleanolic and maslinic acids contained in the olive milling byproducts Chem. Abstr. 128 1998 179706
27. F.J. Reyes, J.J. Centelles, J.A. Lupiáñez, and M. Cascante (2a,3b)-2,3-dihydroxyolean-12-en-28-oic acid, a new natural triterpene from Olea europaea, induces caspase dependent apoptosis selectively in colon adenocarcinoma cells FEBS Lett. 580 2006 6302 6310
28. N.P. Singh, M.T. McCoy, R.R. Tice, and E.L. Schneider A simple technique for quantitation of low levels of DNA damage in individual cells Exp. Cell Res. 175 1988 184 191
29. M. Borras, and J. Nadal Biomarkers of genotoxicity and other end-points in an integrated approach to environmental risk assessment Mutagenesis 19 2004 165 168
30. S. Bhushan, A. Kumar, F. Malik, S.S. Andotra, V.K. Sethi, I.P. Kaur, S.C. Taneja, G.N. Qazi, and J. Singh A triterpenediol from Boswellia serrata induces apoptosis through both the intrinsic and extrinsic apoptotic pathways in human leukemia HL-60 cells Apoptosis 12 2007 1911 1926
31. T. Rabi, L. Wang, and S. Banerjee Novel triterpenoid 25-hydroxy-3- oxoolean-12-en-28-oic acid induces growth arrest and apoptosis in breast cancer cells Breast Cancer Res. Treat 101 2007 27 36
32. H. Li, H. Zhu, C.J. Xu, and J. Yuan Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis Cell 94 1998 491 501
33. X. Luo, I. Budihardjo, H. Zou, C. Slaughter, and X. Wang Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors Cell 94 1998 481 490
34. R. Martin, J. Carvalho-Tavares, E. Ibeas, M. Hernandez, V. Ruiz-Gutierrez, and M.L. Nieto Acidic triterpenes compromise growth and survival of astrocytoma cell lines by regulating reactive oxygen species accumulation Cancer Res. 67 2007 3741 3751
35. S.J. Riedl, and G.S. Salvesen The apoptosome: signalling platform of cell death Nat. Rev. Mol. Cell Biol. 8 2007 405 413
36. A. Ashkenazi Targeting the extrinsic apoptosis pathway in cancer Cytokine Growth Factor Rev. 19 2008 325 331
37. I.C. Lin, S.L. Su, and C.D. Kuo Induction of cell death in RAW 264.7 cells by alpha-lactalbumin Food Chem. Toxicol. 46 2008 842 853
38. H.E. Kim, J.H. Oh, S.K. Lee, and Y.J. Oh Ginsenoside RH-2 induces apoptotic cell death in rat C6 glioma via a reactive oxygen- and caspase-dependent but Bcl-X(L)-independent pathway Life Sci. 65 1999 PL33 40
39. M.A. Kern, A.M. Haugg, A.F. Koch, T. Schilling, K. Breuhahn, H. Walczak, B. Fleischer, C. Trautwein, C. Michalski, H. Schulze-Bergkamen, H. Friess, W. Stremmel, P.H. Krammer, P. Schirmacher, and M. Muller Cyclooxygenase-2 inhibition induces apoptosis signaling via death receptors and mitochondria in hepatocellular carcinoma Cancer Res. 66 2006 7059 7066
40. K.B. Kim, R. Lotan, P. Yue, M.B. Sporn, N. Suh, G.W. Gribble, T. Honda, G.S. Wu, W.K. Hong, and S.Y. Sun Identification of a novel synthetic triterpenoid, methyl-2-cyano-3,12-dioxooleana-1,9-dien-28-oate, that potently induces caspase-mediated apoptosis in human lung cancer cells Mol. Cancer Ther. 1 2002 177 184
41. B. Messner, I. Zeller, C. Ploner, S. Frotschnig, T. Ringer, A. Steinacher-Nigisch, A. Ritsch, G. Laufer, C. Huck, and D. Bernhard Ursolic acid causes DNA-damage, p53-mediated, mitochondria- and caspase-dependent human endothelial cell apoptosis, and accelerates atherosclerotic plaque formation in vivo Atherosclerosis 219 2011 402 408