Oleanolic acid and ursolic acid induce apoptosis in HuH7 human hepatocellular carcinoma cells through a mitochondrial-dependent pathway and downregulation of XIAP

Journal of Agricultural and Food Chemistry

Volumn 58, Issue 10, 2010, Pages 6110-6118

  Shyu, Ming Huan ^a   Kao, Tzu Chien ^a   Yen, Gow Chin ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; HuH7 cell; Oleanolic acid; Ursolic acid and XIAP

Indexed keywords

CASPASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OLEANOLIC ACID; TRITERPENE; URSOLIC ACID; X LINKED INHIBITOR OF APOPTOSIS; XIAP PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL DIVISION; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HUMAN; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS;

APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CASPASES; CELL CYCLE; CELL DIVISION; CELL LINE, TUMOR; DOWN-REGULATION; HUMANS; LIVER NEOPLASMS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NF-KAPPA B; OLEANOLIC ACID; TRITERPENES; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 77952615172     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf100574j     Document Type: Article

References (37)

1. Somova, L. I.; Shode, F. O.; Mipando, M. Cardiotonic and antidysrhythmic effects of oleanolic and ursolic acids, methyl maslinate and uvaol Phytomedicine 2004, 11, 121-129
2. Kowalski, R. Studies of selected plant raw materials as alternative sources of triterpenes of oleanolic and ursolic acid types J. Agric. Food Chem. 2007, 55, 656-662
3. Cunha, W. R.; Martins, C.; Da Silva Ferreira, D.; Crotti, A. E.; Lopes, N. P.; Albuquerque, S. In vitro trypanocidal activity of triterpenes from Miconia species Planta Med. 2003, 69, 470-472
4. Torres-Santos, E. C.; Lopes, D.; Oliveira, R. R.; Carauta, J. P.; Falcao, C. A.; Kaplan, M. A.; Rossi-Bergmann, B. Antileishmanial activity of isolated triterpenoids from Pourouma guianensis Phytomedicine 2004, 11, 114-120
5. Gua, J. Q.; Wang, Y.; Franzblau, S. G.; Montenegro, G.; Timmermann, B. N. Constituents of Quinchamalium majus with potential antitubercular activity Z. Naturforsch. C 2004, 59, 797-802 (Pubitemid 40059818)
6. Yoshimura, H.; Sugawara, K.; Saito, M.; Murakami, S.; Miyata, N.; Kawashima, A.; Morimoto, S.; Gao, N.; Zhang, X.; Yang, J. In vitro TGF-beta1 antagonistic activity of ursolic and oleanolic acids isolated from Clerodendranthus spicatus Planta Med. 2003, 69, 673-675
7. Johnstone, R. W.; Ruefli, A. A.; Lowe, S. W. Apoptosis: A link between cancer genetics and chemotherapy Cell 2002, 108, 153-164
8. Alvarez, S.; Drane, P.; Meiller, A.; Bras, M.; Deguin-Chambon, V.; Bouvard, V.; May, E. A comprehensive study of p53 transcriptional activity in thymus and spleen of γ-irradiated mouse: High sensitivity of genes involved in the two main apoptotic pathways Int. J. Radiat. Biol. 2006, 82, 761-770
9. Cohen, G. M. Caspases: the executioners of apoptosis Biochem. J. 1997, 326, 1-16
10. Crook, N. E.; Clem, R. J.; Miller, L. K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif J. Virol. 1993, 67, 2168-2174
11. Liston, P.; Fong, W. G.; Korneluk, R. G. The inhibitors of apoptosis: there is more to life than Bcl2 Oncogene 2003, 22, 8568-8580
12. Wu, M.; Yuan, S.; Szporn, A. H.; Gan, L.; Shtilbans, V.; Burstein, D. E. Immunocytochemical detection of XIAP in body cavity effusions and washes Mod. Pathol. 2005, 18, 1618-1622
13. Berezovskaya, O.; Schimmer, A. D.; Glinskii, A. B.; Pinilla, C.; Hoffman, R. M.; Reed, J. C.; Glinsky, G. V. Increased expression of apoptosis inhibitor protein XIAP contributes to anoikis resistance of circulating human prostate cancer metastasis precursor cells Cancer Res. 2005, 65, 2378-2386
14. Stennicke, H. R.; Ryan, C. A.; Salvesen, G. S. Reprieval from execution: themolecular basis of caspase inhibition Trends Biochem. Sci. 2002, 27, 94-101
15. Shiraki, K.; Sugimoto, K.; Yamanaka, Y.; Yamaguchi, Y.; Saitou, Y.; Ito, K.; Yamamato, N.; Yamanaka, T.; Fujikawa, K.; Murata, K.; Nakano, T. Overexpression of X-linked inhibitor of apoptosis in human hepatocellular carcinoma Int. J. Mol. Med. 2003, 12, 705-708
16. Llovet, J. M.; Burroughs, A.; Bruix, J. Hepatocellular carcinoma Lancet 2003, 362, 1907-1917
17. Carr, B. I. Hepatocellular carcinoma: current management and future trends Gastroenterology 2004, 127, 218-224
18. Karin, M. Nuclear factor-kappa B in cancer development and progression Nature 2006, 441, 431-436
19. Sogno, I.; Vannini, N.; Lorusso, G.; Cammarota, R.; Noonan, D. M.; Generoso, L.; Sporn, M. B.; Albini, A. Anti-angiogenic activity of a novel class of chemopreventive compounds: oleanic acid terpenoids. Recent Results Cancer Res. 181, 209 - 212.
20. Yeh, C. T.; Wu, C. H.; Yen, G. C. Ursolic acid, a naturally occurring triterpenoid, suppresses migration and invasion of human breast cancer cells by modulating c-Jun N-terminal kinase, Akt and mammalian target of rapamycin signaling. Mol. Nutr. Food Res. 2010, DOI: 10.1002/mnfr.200900414.
21. Zhang, P.; Li, H.; Chen, D.; Ni, J.; Kang, Y.; Wang, S. Oleanolic acid induces apoptosis in human leukemia cells through caspase activation and poly(ADP-ribose) polymerase cleavage Acta. Biochim. Biophys. Sin. (Shanghai) 2007, 39, 803-809
22. Manu, K. A.; Kuttan, G. Ursolic acid induces apoptosis by activating p53 and caspase-3 gene expressions and suppressing NF-kappaB mediated activation of bcl-2 in B16F-10 melanoma cells Int. Immunopharmacol. 2008, 8, 974-981
23. Kassi, E.; Sourlingas, T. G.; Spiliotaki, M.; Papoutsi, Z.; Pratsinis, H.; Aligiannis, N.; Moutsatsou, P. Ursolic acid triggers apoptosis and Bcl-2 downregulation in MCF-7 breast cancer cells Cancer Invest. 2009, 27, 723-733
24. Zhang, Y. X.; Kong, C. Z.; Wang, H. Q.; Wang, L. H.; Xu, C. L.; Sun, Y. H. Phosphorylation of Bcl-2 and activation of caspase-3 via the c-Jun N-terminal kinase pathway in ursolic acid-induced DU145 cells apoptosis Biochimie 2009, 91, 1173-1179
25. Shyu, M. H.; Kao, T. C.; Yen, G. C. Hsian-tsao (Mesona procumbens Heml.) prevents against rat liver fibrosis induced by CCl(4) via inhibition of hepatic stellate cells activation Food. Chem. Toxicol. 2008, 46, 3707-3713
26. Liu, J. Pharmacology of oleanolic acid and ursolic acid J. Ethnopharmacol. 1995, 49, 57-68
27. Cipak, L.; Grausova, L.; Miadokva, E.; Novotny, L.; Rauko, P. Dual activity of triterpenoids: apoptotic versus antidifferentiation effects Arch. Toxicol. 2006, 80, 429-435
28. Li, J.; Guo, W. J.; Yang, Q. Y. Effects of ursolic acid and oleanolic acid on human colon carcinoma cell line HCT15 World J. Gastroenterol. 2002, 8, 493-495
29. Es-saady, D.; Najid, A.; Simon, A.; Denizot, Y.; Chulia, A. J.; De-lage, C. Effects of ursolic acid and its analogs on soybean 15-lipoxygenase activity and the proliferation rate of a human gastric tumor-cell line Mediators Inflammation 1994, 3, 181-184
30. Ovesná, Z.; Kozics, K.; Slamenová, D. Protective effects of ursolic acid and oleanolic acid in leukemia cells Mutat. Res. 2006, 600, 131-137
31. Green, D. R.; Reed, J. C. Mitochondria and apoptosis Science 1998, 281, 1309-1312
32. Raghuvar Gopal, D. V.; Narkar, A. A.; Badrinath, Y.; Mishra, K. P.; Joshi, D. S. Protection of Ewings sarcoma family tumor (ESFT) cell line SK-N-MC from betulinic acid induced apoptosis by R-DL-tocopherol Toxicol. Lett. 2004, 153, 201-212
33. Hengartner, M. O. The biochemistry of apoptosis Nature 2000, 407, 770-776
34. Andersson, D.; Liu, J. J.; Nilsson, A.; Duan, R. D. Ursolic acid inhibits proliferation and stimulates apoptosis in HT29 cells following activation of alkaline sphingomyelinase Anticancer Res. 2003, 23, 3317-3322
35. Tang, C.; Lu, Y. H.; Xie, J. H.; Wang, F.; Zou, J. N.; Yang, J. S.; Xing, Y. Y.; Xi, T. Downregulation of survivin and activation of caspase-3 through the PI3K/Akt pathway in ursolic acid-induced HepG2 cell apoptosis Anticancer Drugs 2009, 20, 249-258
36. Shishodia, S.; Majumdar, S.; Banerjee, S.; Aggarwal, B. B. Ursolic acid inhibits nuclear factor-κB activation induced by carcinogenic agents through suppression of IκBa kinase and p65 phosphorylation: correlation with down-regulation of cyclooxygenase 2, matrix metalloproteinase 9, and cyclin D1 Cancer Res. 2003, 63, 4375-4383
37. Mayo, M. W.; Baldwin, A. S. The transcription factor NF-κB: control of oncogenesis and cancer therapy resistance Biochim. Biophys. Acta 2000, 1470, M55-M62