Anticancer activity of pristimerin in epidermal growth factor receptor 2-positive SKBR3 human breast cancer cells

Biological and Pharmaceutical Bulletin

Volumn 36, Issue 2, 2013, Pages 316-325

  Lee, Jin Sun ^a   Yoon, In Sang ^a   Lee, Myung Sun ^a   Cha, Eun Young ^a   Thuong, Phuong Thien ^a   Diep, Trinh Thi ^a   Kim, Je Ryong ^a,b  

^a Chungnam National University College of Medicine   (South Korea)

^b Vietnam National Institute of Medicinal Materials   (Viet Nam)

Author keywords

Breast cancer; Epidermal growth factor receptor 2; Pristimerin

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FATTY ACID SYNTHASE; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PRISTIMERIN; PROTEIN KINASE B; RAPAMYCIN; S6 KINASE; STRESS ACTIVATED PROTEIN KINASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MIGRATION INHIBITION; MITOSIS INHIBITION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BREAST NEOPLASMS; CASPASES; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; FATTY ACID SYNTHETASE COMPLEX, TYPE I; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; PLANT EXTRACTS; PLANT ROOTS; POLY(ADP-RIBOSE) POLYMERASES; RECEPTOR, ERBB-2; RNA, MESSENGER; SALACIA; TOR SERINE-THREONINE KINASES; TRITERPENES; WOUND HEALING;

EID: 84874091667     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b12-00685     Document Type: Article

References (58)

1. Newman DJ, Cragg GM, Snader KM Natural products as sources of new drugs over the period 1981-2002. J. Nat. Prod., 66, 1022-1037 (2003).
2. Brinker AM, Ma J, Lipsky P.E., Raskin I. Medicinal chemistry and pharmacology of genus Tripterygium (Celastraceae). Phytochemistry, 68, 732-766 (2007).
3. Gao JM, Wu WJ, Zhang J.W., Konishi Y. The dihydro-β-agarofuran sesquiterpenoids. Nat. Prod. Rep., 24, 1153-1189 (2007).
4. Shirota O, Morita H, Takeya K., Itokawa H, Iitaka Y. Cytotoxic aromatic triterpenes from Maytenus ilicifolia and Maytenus chuchuhuasca. J. Nat. Prod., 57, 1675-1681 (1994).
5. Salminen A, Lehtonen M, Suuronen T., Kaarniranta K, Huuskonen J. Terpenoids: natural inhibitors of NF-kappaB signaling with anti-inflammatory and anticancer potential. Cell. Mol. Life Sci., 65, 2979-2999 (2008).
6. Wu CC, Chan ML, Chen W.Y., Tsai CY, Chang FR, Wu YC Pristimerin induces caspase-dependent apoptosis in MDA-MB-231 cells via direct effects on mitochondria. Mol. Cancer Ther., 4, 1277-1285 (2005).
7. Nagase M, Oto J, Sugiyama S., Yube K, Takaishi Y, Sakato N. Apoptosis induction in HL-60 cells and inhibition of topoisomerase II by triterpene celastrol. Biosci. Biotechnol. Biochem., 67, 1883-1887 (2003).
8. Yang H, Landis-Piwowar KR, Lu D., Yuan P, Li L, Reddy G.P., Yuan X., Dou QP Pristimerin induces apoptosis by targeting the proteasome in prostate cancer cells. J. Cell. Biochem., 103, 234-244 (2008).
9. Tiedemann RE, Schmidt J, Keats J.J., Shi CX, Zhu YX, Palmer SE, Mao X, Schimmer A.D., Stewart AK Identification of a potent natural triterpenoid inhibitor of proteosome chymotrypsin-like activity and NF-kappaB with antimyeloma activity in vitro and in vivo. Blood, 113, 4027-4037 (2009).
10. Byun JY, Kim MJ, Eum D.Y., Yoon CH, Seo WD, Park KH, Hyun J.W., Lee YS, Lee JS, Yoon M Y, Lee SJ Reactive oxygen species-dependent activation of Bax and poly(ADP-ribose) polymerase-1 is required for mitochondrial cell death induced by triterpenoid pristimerin in human cervical cancer cells. Mol. Pharmacol., 76, 734-744 (2009).
11. Konopleva M, Zhang W, Shi Y.X., McQueen T., Tsao T, Abdelrahim M, Munsell M.F., Johansen M., Yu D, Madden T, Safe S.H., Hung MC, Andreeff M. Synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid induces growth arrest in HER2-overexpressing breast cancer cells. Mol. Cancer Ther., 5, 317-328 (2006).
12. Slamon DJ, Clark GM, Wong S.G., Levin WJ, Ullrich A, McGuire WL Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science, 235, 177-182 (1987).
13. Hynes NE, Lane HA ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev. Cancer, 5, 341-354 (2005).
14. Klos KS, Wyszomierski SL, Sun M, Tan M., Zhou X, Li P, Yang W., Yin G, Hittelman WN, Yu D. ErbB2 increases vascular endothelial growth factor protein synthesis via activation of mammalian target of rapamycin/p70S6K leading to increased angiogenesis and spontaneous metastasis of human breast cancer cells. Cancer Res., 66, 2028-2037 (2006).
15. Yarden Y, Sliwkowski MX Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol., 2, 127-137 (2001).
16. Moasser MM. The oncogene HER2: its signaling and transforming functions and its role in human cancer pathogenesis. Oncogene, 26, 6469-6487 (2007).
17. Carter P, Presta L, Gorman C.M., Ridgway JB, Henner D, Wong WL, Rowland A.M., Kotts C., Carver ME, Shepard HM Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc. Natl. Acad. Sci. U.S.A., 89, 4285-4289 (1992).
18. Piccart-Gebhart M.J., Procter M, Leyland-Jones B, Goldhirsch A., Untch M, Smith I, Gianni L., Baselga J, Bell R, Jackisch C., Cameron D, Dowsett M, Barrios CH, Steger G, Huang CS, Andersson M, Inbar M, Lichinitser M, Láng I, Nitz U, Iwata H, Thomssen C, Lohrisch C, Suter TM, Rüschoff J, Suto T, Greatorex V, Ward C, Straehle C, McFadden E, Dolci MS, Gelber RD, Herceptin Adjuvant (HERA) Trial Study Team. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N. Engl. J. Med., 353, 1659-1672 (2005).
19. Esteva FJ, Sahin AA, Cristofanilli M, Arun B., Hortobagyi GN Molecular prognostic factors for breast cancer metastasis and survival. Semin. Radiat. Oncol., 12, 319-328 (2002).
20. Zoncu R, Efeyan A, Sabatini DM mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol., 12, 21-35 (2011).
21. Li H, Lin J, Wang X., Yao G, Wang L, Zheng H., Yang C, Jia C, Liu A., Bai X. Targeting of mTORC2 prevents cell migration and promotes apoptosis in breast cancer. Breast Cancer Res. Treat., 134, 1057-1066 (2012).
22. Morgensztern D, McLeod HL PI3K/Akt/mTOR pathway as a target for cancer therapy. Anticancer Drugs, 16, 797-803 (2005).
23. Jalving M, Gietema JA, Lefrandt J.D., de Jong S, Reyners AK, Gans R.O., de Vries EG. Metformin: taking away the candy for cancer? Eur. J. Cancer, 46, 2369-2380 (2010).
24. Tian WX, Hsu RY, Wang YS Studies on the reactivity of the essential sulfhydryl groups as a conformational probe for the fatty acid synthetase of chicken liver. Inactivation by 5, 5'-dithiobis(2-nitrobenzoic acid) and intersubunit cross-linking of the inactivated enzyme. J. Biol. Chem., 260, 11375-11387 (1985).
25. Kumar-Sinha C., Ignatoski KW, Lippman M.E., Ethier SP, Chinnaiyan AM Transcriptome analysis of HER2 reveals a molecular connection to fatty acid synthesis. Cancer Res., 63, 132-139 (2003).
26. Zhou X, Tan M, Stone Hawthorne V, Klos KS, Lan K.H., Yang Y., Yang W, Smith TL, Shi D, Yu D. Activation of the Akt/mammalian target of rapamycin/4E-BP1 pathway by ErbB2 overexpression predicts tumor progression in breast cancers. Clin. Cancer Res., 10, 6779-6788 (2004).
27. Zheng QY, Jin FS, Yao C, Zhang T., Zhang GH, Ai X. Ursolic acid-induced AMP-activated protein kinase (AMPK) activation contributes to growth inhibition and apoptosis in human bladder cancer T24 cells. Biochem. Biophys. Res. Commun., 419, 741-747 (2012).
28. Xiang X, Saha AK, Wen R, Ruderman N.B., Luo Z. AMP-activated protein kinase activators can inhibit the growth of prostate cancer cells by multiple mechanisms. Biochem. Biophys. Res. Commun., 321, 161-167 (2004).
29. Zhang WB, Wang Z, Shu F., Jin YH, Liu HY, Wang QJ, Yang Y. Activation of AMP-activated protein kinase by temozolomide contributes to apoptosis in glioblastoma cells via p53 activation and mTORC1 inhibition. J. Biol. Chem., 285, 40461-40471 (2010).
30. Costa PM, Ferreira PM, Bolzani V.S., Furlan M., de Freitas Formenton Macedo Dos Santos VA, Corsino J, de Moraes MO, CostaLotufo LV, Montenegro RC, Pessoa C. Antiproliferative activity of pristimerin isolated from Maytenus ilicifolia (Celastraceae) in human HL-60 cells. Toxicol. In Vitro, 22, 854-863 (2008).
31. Yu D, Hung MC Overexpression of ErbB2 in cancer and ErbB2-targeting strategies. Oncogene, 19, 6115-6121 (2000).
32. Little JL, Kridel SJ Fatty acid synthase activity in tumor cells. Sub-cell. Biochem., 49, 169-194 (2008).
33. Kusakabe T, Maeda M, Hoshi N., Sugino T, Watanabe K, Fukuda T., Suzuki T. Fatty acid synthase is expressed mainly in adult hormone-sensitive cells or cells with high lipid metabolism and in proliferating fetal cells. J. Histochem. Cytochem., 48, 613-622 (2000).
34. Wang Y, Kuhajda FP, Li J.N., Pizer ES, Han WF, Sokoll LJ, Chan DW Fatty acid synthase (FAS) expression in human breast cancer cell culture supernatants and in breast cancer patients. Cancer Lett., 167, 99-104 (2001).
35. Thupari JN, Pinn ML, Kuhajda FP Fatty acid synthase inhibition in human breast cancer cells leads to malonyl-CoA-induced inhibition of fatty acid oxidation and cytotoxicity. Biochem. Biophys. Res. Commun., 285, 217-223 (2001).
36. Lee JS, Lee MS, Oh W.K., Sul JY Fatty acid synthase inhibition by amentoflavone induces apoptosis and antiproliferation in human breast cancer cells. Biol. Pharm. Bull., 32, 1427-1432 (2009).
37. Bandyopadhyay S, Pai SK, Watabe M, Gross S.C., Hirota S., Hosobe S, Tsukada T, Miura K., Saito K, Markwell SJ, Wang Y, Huggenvik J., Pauza ME, Iiizumi M, Watabe K. FAS expression inversely correlates with PTEN level in prostate cancer and a PI 3-kinase inhibitor synergizes with FAS siRNA to induce apoptosis. Oncogene, 24, 5389-5395 (2005).
38. Brusselmans K, Vrolix R, Verhoeven G., Swinnen J V. Induction of cancer cell apoptosis by flavonoids is associated with their ability to inhibit fatty acid synthase activity. J. Biol. Chem., 280, 5636-5645 (2005).
39. Lee JS, Sul JY, Park J.B., Lee MS, Cha EY, Song IS, Kim J.R., Chang ES Fatty acid synthase inhibition by amentoflavone suppresses HER2/neu (erbB2) oncogene in SKBR3 human breast cancer cells. Phytother. Res., (2012), in press.
40. Zhang D, Tai LK, Wong L.L., Chiu LL, Sethi SK, Koay ES Proteomic study reveals that proteins involved in metabolic and detoxification pathways are highly expressed in HER-2/neu-positive breast cancer. Mol. Cell. Proteomics, 4, 1686-1696 (2005).
41. Scheid MP, Marignani PA, Woodgett JR Multiple phosphoinositide 3-kinase-dependent steps in activation of protein kinase B. Mol. Cell. Biol., 22, 6247-6260 (2002).
42. Bode AM, Dong Z. The functional contrariety of JNK. Mol. Carcinog., 46, 591-598 (2007).
43. Chiang CT, Way TD, Tsai S.J., Lin JK Diosgenin, a naturally occurring steroid, suppresses fatty acid synthase expression in HER2-overexpressing breast cancer cells through modulating Akt, mTOR and JNK phosphorylation. FEBS Lett., 581, 5735-5742 (2007).
44. Lu S, Archer MC Celecoxib decreases fatty acid synthase expression via down-regulation of c-Jun N-terminal kinase-1. Exp. Biol. Med. (Maywood), 232, 643-653 (2007).
45. Oliveras G, Blancafort A, Urruticoechea A., Campuzano O, Gómez-Cabello D, Brugada R, López-Rodríguez ML, Colomer R, Puig T. Novel anti-fatty acid synthase compounds with anti-cancer activity in HER2+ breast cancer. Ann. N. Y. Acad. Sci., 1210, 86-92 (2010).
46. Chiang CT, Way TD, Tsai S.J., Lin JK Diosgenin, a naturally occurring steroid, suppresses fatty acid synthase expression in HER2-overexpressing breast cancer cells through modulating Akt, mTOR and JNK phosphorylation. FEBS Lett., 581, 5735-5742 (2007).
47. Yoon S, Lee MY, Park S.W., Moon JS, Koh YK, Ahn YH, Park B.W., Kim KS Up-regulation of acetyl-CoA carboxylase alpha and fatty acid synthase by human epidermal growth factor receptor 2 at the translational level in breast cancer cells. J. Biol. Chem., 282, 26122-26131 (2007).
48. Mondesire WH, Jian W, Zhang H., Ensor J, Hung MC, Mills G.B., Meric-Bernstam F. Targeting mammalian target of rapamycin syn-ergistically enhances chemotherapy-induced cytotoxicity in breast cancer cells. Clin. Cancer Res., 10, 7031-7042 (2004).
49. Chiang CT, Way TD, Lin JK Sensitizing HER2-overexpressing cancer cells to luteolin-induced apoptosis through suppressing p21 (WAF1/CIP1) expression with rapamycin. Mol. Cancer Ther., 6, 2127-2138 (2007).
50. LoPiccolo J, Blumenthal GM, Bernstein W.B., Dennis PA Targeting the PI3K/Akt/mTOR pathway: effective combinations and clinical considerations. Drug Resist. Updat., 11, 32-50 (2008).
51. Yeh CT, Wu CH, Yen GC Ursolic acid, a naturally occurring tri-terpenoid, 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., 54, 1285-1295 (2010).
52. Ke Z, Lin H, Fan Z., Cai TQ, Kaplan RA, Ma C, Bower K.A., Shi X., Luo J. MMP-2 mediates ethanol-induced invasion of mammary epithelial cells over-expressing ErbB2. Int. J. Cancer, 119, 8-16 (2006).
53. García-García C, Ibrahim YH, Serra V, Calvo MT, Guzmán M, Grueso J, Aura C, Pérez J, Jessen K, Liu Y, Rommel C, Tabernero J, Baselga J, Scaltriti M. Dual mTORC1/2 and HER2 blockade results in antitumor activity in preclinical models of breast cancer resistant to anti-HER2 therapy. Clin. Cancer Res., 18, 2603-2612 (2012).
54. Kaufmann SH, Earnshaw WC Induction of apoptosis by cancer chemotherapy. Exp. Cell Res., 256, 42-49 (2000).
55. Kroemer G, Reed JC Mitochondrial control of cell death. Nat. Med., 6, 513-519 (2000).
56. Sharma K, Wang RX, Zhang L.Y., Yin DL, Luo XY, Solomon JC, Jiang R.F., Markos K., Davidson W, Scott DW, Shi YF Death the Fas way: regulation and pathophysiology of CD95 and its ligand. Pharmacol. Ther., 88, 333-347 (2000).
57. Lu Z, Jin Y, Chen C., Li J, Cao Q, Pan J. Pristimerin induces apoptosis in imatinib-resistant chronic myelogenous leukemia cells harboring T315I mutation by blocking NF-kappaB signaling and depleting Bcr-Abl. Mol. Cancer, 9, 112-128 (2010).
58. Seo HS, Choi HS, Kim S.R., Choi YK, Woo SM, Shin I, Woo J.K., Park SY, Shin YC, Ko SK Apigenin induces apoptosis via extrinsic pathway, inducing p53 and inhibiting STAT3 and NFκB signaling in HER2-overexpressing breast cancer cells. Mol. Cell. Biochem., 366, 319-334 (2012).