The natural triterpene maslinic acid induces apoptosis in HT29 colon cancer cells by a JNK-p53-dependent mechanism

BMC Cancer

Volumn 11, Issue , 2011, Pages

  Reyes Zurita, Fernando J ^a   Pachón Peña, Gisela ^b   Lizárraga, Daneida ^c   Rufino Palomares, Eva E ^a   Cascante, Marta ^b   Lupiáñez, José A ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Colon cancer cells JNK, maslinic acid, Mitochondrial apoptotic pathway, P53 mediated apoptosis; Triterpenes

Indexed keywords

CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; CYTOCHROME C; JANUS KINASE; MASLINIC ACID; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; PROTEIN P53; STRESS ACTIVATED PROTEIN KINASE; ANTINEOPLASTIC AGENT; CASPASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; TRITERPENE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; COLON CANCER; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DRUG CYTOTOXICITY; ENZYME ACTIVITY; ENZYME RELEASE; FLOW CYTOMETRY; GENOTOXICITY; HUMAN; HUMAN CELL; MITOCHONDRION; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CELL STRAIN HT29; COLON TUMOR; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; METABOLISM; PATHOLOGY;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CASPASES; COLONIC NEOPLASMS; COMET ASSAY; CYTOCHROMES C; HT29 CELLS; HUMANS; MAP KINASE KINASE 4; PROTO-ONCOGENE PROTEINS C-BCL-2; TRITERPENES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 79955139265     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-11-154     Document Type: Article

References (47)

1. Kaufmann SH, Earnshaw WC. Induction of apoptosis by cancer chemotherapy. Exp Cell Res 2000, 256(1):42-49. 10.1006/excr.2000.4838, 10739650.
2. Shishodia S, Chaturvedi MM, Aggarwal BB. Role of curcumin in cancer therapy. Curr Probl Cancer 2007, 31(4):243-305. 10.1016/j.currproblcancer.2007.04.001, 17645940.
3. Deng Y, Ren X, Yang L, Lin Y, Wu X. A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 2003, 115(1):61-70. 10.1016/S0092-8674(03)00757-8, 14532003.
4. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, Bar-Sagi D, Jones SN, Flavell RA, Davis RJ. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 2000, 288(5467):870-874. 10.1126/science.288.5467.870, 10797012.
5. Wajant H, Pfizenmaier K, Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 2003, 10(1):45-65. 10.1038/sj.cdd.4401189, 12655295.
6. Lei K, Nimnual A, Zong WX, Kennedy NJ, Flavell RA, Thompson CB, Bar-Sagi D, Davis RJ. The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase. Mol Cell Biol 2002, 22(13):4929-4942. 10.1128/MCB.22.13.4929-4942.2002, 133923, 12052897.
7. Fan M, Goodwin M, Vu T, Brantley-Finley C, Gaarde WA, Chambers TC. 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 2000, 275(39):29980-29985.
8. Lei K, Davis RJ. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 2003, 100(5):2432-2437. 10.1073/pnas.0438011100, 151358, 12591950.
9. Chang L, Karin M. Mammalian MAP kinase signaling cascades. Nature 2001, 410(6824):37-40. 10.1038/35065000, 11242034.
10. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103(2):239-252. 10.1016/S0092-8674(00)00116-1, 11057897.
11. Liu J, Lin A. Role of JNK activation in apoptosis: a double-edged sword. Cell Res 2005, 15(1):36-42. 10.1038/sj.cr.7290262, 15686625.
12. Shaulian E, Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol 2002, 4(5):E131-136. 10.1038/ncb0502-e131, 11988758.
13. Mertens-Talcott SU, Bomser JA, Romero C, Talcott ST, Percival SS. Ellagic acid potentiates the effect of quercetin on p21waf1/cip1, p53, and MAP-kinases without affecting intracellular generation of reactive oxygen species in vitro. J Nutr 2005, 135(3):609-614.
14. Yee KS, Vousden KH. Complicating the complexity of p53. Carcinogenesis 2005, 26(8):1317-1322. 10.1093/carcin/bgi122, 15888490.
15. Marchenko ND, Zaika A, Moll UM. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem 2000, 275(21):16202-16212. 10.1074/jbc.275.21.16202, 10821866.
16. Scorrano L, Korsmeyer SJ. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem Biophys Res Commun 2003, 304(3):437-444. 10.1016/S0006-291X(03)00615-6, 12729577.
17. Montilla MP, Agil A, Navarro MC, Jimenez MI, Garcia-Granados A, Parra A, Cabo MM. Antioxidant activity of maslinic acid, a triterpene derivative obtained from Olea europaea. Planta Med 2003, 69(5):472-474.
18. Reyes FJ, Centelles JJ, Lupiáñez JA, Cascante M. (2α,3β)-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 2006, 580(27):6302-6310. 10.1016/j.febslet.2006.10.038, 17083937.
19. Reyes-Zurita FJ, Rufino-Palomares EE, Lupiáñez JA, Cascante M. Maslinic acid, a natural triterpene from Olea europaea L., induces apoptosis in HT29 human colon-cancer cells via the mitochondrial apoptotic pathway. Cancer Lett 2009, 273:44-54. 10.1016/j.canlet.2008.07.033, 18790561.
20. Ikeda T, Sporn M, Honda T, Gribble GW, Kufe D. The novel triterpenoid CDDO and its derivatives induce apoptosis by disruption of intracellular redox balance. Cancer Res 2003, 63(17):5551-5558.
21. Zou W, Liu X, Yue P, Zhou Z, Sporn MB, Lotan R, Khuri FR, Sun SY. 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 2004, 64(20):7570-7578. 10.1158/0008-5472.CAN-04-1238, 15492284.
22. Ito Y, Pandey P, Sporn MB, Datta R, Kharbanda S, Kufe D. The novel triterpenoid CDDO induces apoptosis and differentiation of human osteosarcoma cells by a caspase-8 dependent mechanism. Mol Pharmacol 2001, 59(5):1094-1099.
23. Borras M, Nadal J. Biomarkers of genotoxicity and other end-points in an integrated approach to environmental risk assessment. Mutagenesis 2004, 19(3):165-168. 10.1093/mutage/geh023, 15123781.
24. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997, 88(3):323-331. 10.1016/S0092-8674(00)81871-1, 9039259.
25. Devireddy LR, Jones CJ. Activation of caspases and p53 by bovine herpesvirus 1 infection results in programmed cell death and efficient virus release. J Virol 1999, 73(5):3778-3788. 104155, 10196272.
26. Katayose D, Wersto R, Cowan K, Seth P. Consequences of p53 gene expression by adenovirus vector on cell cycle arrest and apoptosis in human aortic vascular smooth muscle cells. Biochem Biophys Res Commun 1995, 215(2):446-451. 10.1006/bbrc.1995.2485, 7487976.
27. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998, 94(4):491-501. 10.1016/S0092-8674(00)81590-1, 9727492.
28. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001, 15(22):2922-2933.
29. Sarker M, Ruiz-Ruiz C, Robledo G, Lopez-Rivas A. Stimulation of the mitogen-activated protein kinase pathway antagonizes TRAIL-induced apoptosis downstream of BID cleavage in human breast cancer MCF-7 cells. Oncogene 2002, 21(27):4323-4327. 10.1038/sj.onc.1205523, 12082620.
30. Dzubak P, Hajduch M, Vydra D, Hustova A, Kvasnica M, Biedermann D, Markova L, Urban M, Sarek J. Pharmacological activities of natural triterpenoids and their therapeutic implications. Nat Prod Rep 2006, 23(3):394-411. 10.1039/b515312n, 16741586.
31. Aoki H, Kang PM, Hampe J, Yoshimura K, Noma T, Matsuzaki M, Izumo S. Direct activation of mitochondrial apoptosis machinery by c-Jun N-terminal kinase in adult cardiac myocytes. J Biol Chem 2002, 277(12):10244-10250. 10.1074/jbc.M112355200, 11786558.
32. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004, 303(5660):1010-1014. 10.1126/science.1092734, 14963330.
33. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003, 11(3):577-590. 10.1016/S1097-2765(03)00050-9, 12667443.
34. Toledo F, Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006, 6(12):909-923. 10.1038/nrc2012, 17128209.
35. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007, 8(4):275-283. 10.1038/nrm2147, 17380161.
36. Sax JK, Fei P, Murphy ME, Bernhard E, Korsmeyer SJ, El-Deiry WS. BID regulation by p53 contributes to chemosensitivity. Nat Cell Biol 2002, 4(11):842-849. 10.1038/ncb866, 12402042.
37. Harmand PO, Duval R, Delage C, Simon A. Ursolic acid induces apoptosis through mitochondrial intrinsic pathway and caspase-3 activation in M4Beu melanoma cells. Int J Cancer 2005, 114(1):1-11. 10.1002/ijc.20588, 15523687.
38. Shishodia S, Majumdar S, Banerjee S, Aggarwal BB. Ursolic acid inhibits nuclear factor-kappaB activation induced by carcinogenic agents through suppression of IkappaBalpha kinase and p65 phosphorylation: correlation with down-regulation of cyclooxygenase 2, matrix metalloproteinase 9, and cyclin D1. Cancer Res 2003, 63(15):4375-4383.
39. Konopleva M, Tsao T, Estrov Z, Lee RM, Wang RY, Jackson CE, McQueen T, Monaco G, Munsell M, Belmont J, Kantarjian H, Sporn MB, Adreeff M. The synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid induces caspase-dependent and -independent apoptosis in acute myelogenous leukemia. Cancer Res 2004, 64(21):7927-7935. 10.1158/0008-5472.CAN-03-2402, 15520199.
40. Lapillonne H, Konopleva M, Tsao T, Gold D, McQueen T, Sutherland RL, Madden T, Andreeff M. Activation of peroxisome proliferator-activated receptor gamma by a novel synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid induces growth arrest and apoptosis in breast cancer cells. Cancer Res 2003, 63(18):5926-5939.
41. Kim KB, Lotan R, Yue P, Sporn MB, Suh N, Gribble GW, Honda T, Wu GS, Hong WK, Sun SY. 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 2002, 1(3):177-184.
42. Shishodia S, Sethi G, Konopleva M, Andreeff M, Aggarwal BB. A synthetic triterpenoid, CDDO-Me, inhibits IkappaBalpha kinase and enhances apoptosis induced by TNF and chemotherapeutic agents through down-regulation of expression of nuclear factor kappaB-regulated gene products in human leukemic cells. Clin Cancer Res 2006, 12(6):1828-1838. 10.1158/1078-0432.CCR-05-2044, 16551868.
43. Fulda S, Debatin KM. Betulinic acid induces apoptosis through a direct effect on mitochondria in neuroectodermal tumors. Med Pediatr Oncol 2000, 35(6):616-618. 10.1002/1096-911X(20001201)35:6<616::AID-MPO27>3.0.CO;2-N, 11107130.
44. Karpova MB, Sanmun D, Henter JI, Smirnov AF, Fadeel B. Betulinic acid, a natural cytotoxic agent, fails to trigger apoptosis in human Burkitt's lymphoma-derived B-cell lines. Int J Cancer 2006, 118(1):246-252. 10.1002/ijc.21311, 16003746.
45. Zuco V, Supino R, Righetti SC, Cleris L, Marchesi E, Gambacorti-Passerini C, Formelli F. Selective cytotoxicity of betulinic acid on tumor cell lines, but not on normal cells. Cancer Lett 2002, 175(1):17-25. 10.1016/S0304-3835(01)00718-2, 11734332.
46. Rabi T, Wang L, Banerjee S. Novel triterpenoid 25-hydroxy-3-oxoolean-12-en-28-oic acid induces growth arrest and apoptosis in breast cancer cells. Breast Cancer Res Treat 2007, 101(1):27-36. 10.1007/s10549-006-9275-z, 17028990.
47. Chen HW, Hsu MJ, Chien CT, Huang HC. Effect of alisol B acetate, a plant triterpene, on apoptosis in vascular smooth muscle cells and lymphocytes. Eur J Pharmacol 2001, 419(2-3):127-138. 10.1016/S0014-2999(01)00983-9, 11426834.