Oleanolic acid induces metabolic adaptation in cancer cells by activating the amp-activated protein kinase pathway

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 24, 2014, Pages 5528-5537

  Liu, Jia ^a,c   Zheng, Lanhong ^b   Wu, Ning ^a   Ma, Leina ^d   Zhong, Jiateng ^e   Liu, Ge ^a,c   Lin, Xiukun ^a,f  

^a INSTITUTE OF OCEANOLOGY   (China)

^b YELLOW SEA FISHERIES RESEARCH INSTITUTE   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d OCEAN UNIVERSITY OF CHINA   (China)

^e Basic Medical College   (China)

^f CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

aerobic glycolysis; AMPK; metabolism; oleanolic acid

Indexed keywords

BIOSYNTHESIS; CARBOXYLIC ACIDS; CELL CULTURE; CELL DEATH; CELL PROLIFERATION; CHEMICAL ACTIVATION; DISEASES; ENZYME ACTIVITY; NUCLEIC ACIDS; PATHOLOGY; PHYSIOLOGY; TUMORS; CYTOLOGY; ENZYMES; METABOLISM; PROTEINS;

AEROBIC GLYCOLYSIS; AMP-ACTIVATED PROTEIN KINASE; AMPK; ANTI-TUMOR ACTIVITIES; OLEANOLIC ACIDS; PROSTATE CANCER CELLS; THERAPEUTIC STRATEGY; TUMOR SUPPRESSOR ACTIVITY; METABOLIC ADAPTATION;

METABOLISM; CELLS;

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; OLEANOLIC ACID;

ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CELL CYCLE CHECKPOINT; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; FEMALE; GENETICS; HUMAN; MALE; MCF 7 CELL LINE; METABOLISM; MOUSE; NUDE MOUSE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HUMANS; MALE; MCF-7 CELLS; MICE; MICE, INBRED BALB C; MICE, NUDE; OLEANOLIC ACID; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84902669877     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf500622p     Document Type: Article

References (27)

1. Hardie, D. G.; Alessi, D. R. LKB1 and AMPK and the cancer-metabolism link-ten years after BMC Biol. 2013, 11, 36
2. Khandekar, M. J.; Cohen, P.; Spiegelman, B. M. Molecular mechanisms of cancer development in obesity Nat. Rev. Cancer 2011, 11, 886-895
3. Faubert, B.; Boily, G.; Izreig, S.; Griss, T.; Samborska, B.; Dong, Z.; Dupuy, F.; Chambers, C.; Fuerth, B. J.; Viollet, B.; Mamer, O. A.; Avizonis, D.; DeBerardinis, R. J.; Siegel, P. M.; Jones, R. G. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo Cell Metab. 2013, 17, 113-124
4. Chung, H. H.; Moon, J. S.; Yoon, J. S.; Lee, H. W.; Won, K. C. The relationship between metformin and cancer in patients with type 2 diabetes Diabetes Metab. J. 2013, 37, 125-131
5. Wang, X.; Bai, H.; Zhang, X.; Liu, J.; Cao, P.; Liao, N.; Zhang, W.; Wang, Z.; Hai, C. Inhibitory effect of oleanolic acid on hepatocellular carcinoma via ERK-p53-mediated cell cycle arrest and mitochondrial-dependent apoptosis Carcinogenesis 2013, 34, 1323-1330
6. Mullen, A. R.; Wheaton, W. W.; Jin, E. S.; Chen, P. H.; Sullivan, L. B.; Cheng, T.; Yang, Y.; Linehan, W. M.; Chandel, N. S.; DeBerardinis, R. J. Reductive carboxylation supports growth in tumour cells with defective mitochondria Nature 2011, 481, 385-388
7. Lee, W.; Yang, E. J.; Ku, S. K.; Song, K. S.; Bae, J. S. Anticoagulant activities of oleanolic acid via inhibition of tissue factor expressions BMB Rep. 2012, 45, 390-395
8. Reisman, S. A.; Aleksunes, L. M.; Klaassen, C. D. Oleanolic acid activates Nrf2 and protects from acetaminophen hepatotoxicity via Nrf2-dependent and Nrf2-independent processes Biochem. Pharmacol. 2009, 77, 1273-1282
9. Wang, J.; Ma, H.; Zhang, X.; He, L.; Wu, J.; Gao, X.; Ren, J.; Li, J. A novel AMPK activator from Chinese herb medicine and ischemia phosphorylate the cardiac transcription factor FOXO3 Int. J. Physiol. Pathophysiol. Pharmacol. 2009, 1, 116-126
10. Pan, W.; Yang, H.; Cao, C.; Song, X.; Wallin, B.; Kivlin, R.; Lu, S.; Hu, G.; Di, W.; Wan, Y. AMPK mediates curcumin-induced cell death in CaOV3 ovarian cancer cells Oncol. Rep. 2008, 20, 1553-1559
11. Zu, X.; Zhong, J.; Luo, D.; Tan, J.; Zhang, Q.; Wu, Y.; Liu, J.; Cao, R.; Wen, G.; Cao, D. Chemical genetics of acetyl-CoA carboxylases Molecules 2013, 18, 1704-1719
12. Ha, J.; Daniel, S.; Broyles, S. S.; Kim, K. H. Critical phosphorylation sites for acetyl-CoA carboxylase activity J. Biol. Chem. 1994, 269, 22162-22168
13. Menendez, J. A.; Lupu, R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis Nat. Rev. Cancer 2007, 7, 763-777
14. Li, Y.; Xu, S.; Mihaylova, M. M.; Zheng, B.; Hou, X.; Jiang, B.; Park, O.; Luo, Z.; Lefai, E.; Shyy, J. Y.; Gao, B.; Wierzbicki, M.; Verbeuren, T. J.; Shaw, R. J.; Cohen, R. A.; Zang, M. AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice Cell Metab. 2011, 13, 376-388
15. Youn, S. H.; Lee, J. S.; Lee, M. S.; Cha, E. Y.; Thuong, P. T.; Kim, J. R.; Chang, E. S. Anticancer properties of pomolic acid-induced AMP-activated protein kinase activation in MCF7 human breast cancer cells Biol. Pharm. Bull. 2012, 35, 105-110
16. Inoki, K.; Zhu, T.; Guan, K. L. TSC2 mediates cellular energy response to control cell growth and survival Cell 2003, 115, 577-590
17. Gwinn, D. M.; Shackelford, D. B.; Egan, D. F.; Mihaylova, M. M.; Mery, A.; Vasquez, D. S.; Turk, B. E.; Shaw, R. J. AMPK phosphorylation of raptor mediates a metabolic checkpoint Mol. Cell 2008, 30, 214-226
18. Weng, Q. P.; Kozlowski, M.; Belham, C.; Zhang, A.; Comb, M. J.; Avruch, J. Regulation of the p70 S6 kinase by phosphorylation in vivo. Analysis using site-specific anti-phosphopeptide antibodies J. Biol. Chem. 1998, 273, 16621-16629
19. Gingras, A. C.; Gygi, S. P.; Raught, B.; Polakiewicz, R. D.; Abraham, R. T.; Hoekstra, M. F.; Aebersold, R.; Sonenberg, N. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism Genes Dev. 1999, 13, 1422-1437
20. Sun, Q.; Chen, X.; Ma, J.; Peng, H.; Wang, F.; Zha, X.; Wang, Y.; Jing, Y.; Yang, H.; Chen, R.; Chang, L.; Zhang, Y.; Goto, J.; Onda, H.; Chen, T.; Wang, M. R.; Lu, Y.; You, H.; Kwiatkowski, D.; Zhang, H. Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 4129-4134
21. Choi, Y. J.; Park, Y. J.; Park, J. Y.; Jeong, H. O.; Kim, D. H.; Ha, Y. M.; Kim, J. M.; Song, Y. M.; Heo, H. S.; Yu, B. P.; Chun, P.; Moon, H. R.; Chung, H. Y. Inhibitory effect of mTOR activator MHY1485 on autophagy: suppression of lysosomal fusion PLoS One 2012, 7 e43418
22. Jones, R. G.; Plas, D. R.; Kubek, S.; Buzzai, M.; Mu, J.; Xu, Y.; Birnbaum, M. J.; Thompson, C. B. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint Mol. Cell 2005, 18, 283-293
23. Imamura, K.; Ogura, T.; Kishimoto, A.; Kaminishi, M.; Esumi, H. Cell cycle regulation via p53 phosphorylation by a 5′-AMP activated protein kinase activator, 5-aminoimidazole-4-carboxamide-1-β- d -ribofuranoside, in a human hepatocellular carcinoma cell line Biochem. Biophys. Res. Commun. 2001, 287, 562-567
24. Liang, J.; Shao, S. H.; Xu, Z. X.; Hennessy, B.; Ding, Z.; Larrea, M.; Kondo, S.; Dumont, D. J.; Gutterman, J. U.; Walker, C. L.; Slingerland, J. M.; Mills, G. B. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis Nat. Cell Biol. 2007, 9, 218-224
25. Li, N.; Lu, H.; Chen, C.; Bu, X.; Huang, P. Loss of fatty acid synthase inhibits the "HER2-PI3K/Akt axis" activity and malignant phenotype of Caco-2 cells Lipids Health Dis. 2013, 12, 83
26. Fox, M. M.; Phoenix, K. N.; Kopsiaftis, S. G.; Claffey, K. P. AMP-activated protein kinase alpha 2 isoform suppression in primary breast cancer alters AMPK growth control and apoptotic signaling Genes Cancer 2013, 4, 3-14
27. Sarre, A.; Gabrielli, J.; Vial, G.; Leverve, X. M.; Assimacopoulos- Jeannet, F. Reactive oxygen species are produced at low glucose and contribute to the activation of AMPK in insulin-secreting cells Free Radical Biol. Med. 2012, 52, 142-150