Caffeic acid Phenethyl ester and ethanol extract of Propolis induce the complementary Cytotoxic effect on triple-negative breast cancer cell lines

Molecules

Volumn 20, Issue 5, 2015, Pages 9242-9262

  Rzepecka Stojko, Anna ^a   Kabala Dzik, Agata ^a   Mozdzierz, Aleksandra ^a   Kubina, Robert ^a   Wojtyczka, Robert D ^a   Stojko, Rafal ^a   Dziedzic, Arkadiusz ^a   Jastrzebska Stojko, Zaneta ^a   Jurzak, Magdalena ^a   Buszman, Ewa ^a   Stojko, Jerzy ^a  

^a MEDICAL UNIVERSITY OF SILESIA   (Poland)

Author keywords

Breast cancer; Caffeic acid phenethyl ester; Cytotoxicity; Propolis

Indexed keywords

ANTINEOPLASTIC AGENT; CAFFEIC ACID DERIVATIVE; CAFFEIC ACID PHENETHYL ESTER; PHENETHYL ALCOHOL; PROPOLIS;

ANALOGS AND DERIVATIVES; APOPTOSIS; DRUG EFFECTS; FEMALE; HUMAN; PHYTOTHERAPY; PROCEDURES; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CAFFEIC ACIDS; CELL LINE, TUMOR; FEMALE; HUMANS; PHENYLETHYL ALCOHOL; PHYTOTHERAPY; PROPOLIS; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84983411410     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules20059242     Document Type: Article

References (56)

1. Brewster, A.M.; Chavez-MacGregor, M.; Brown, P. Epidemiology, biology, and treatment of triple-negative breast cancer in women of African ancestry. Lancet Oncol. 2014, 15, e625-e634.
2. Murtaza, G.; Karim, S.; Akram, M.R.; Khan, S.A.; Azhar, S.; Mumtaz, A.; Bin Asad, M.H. Caffeic acid phenethyl ester and therapeutic potentials. Biomed. Res. Int. 2014, 2014, 145342-145350.
3. Omene, C.; Kalac, M.; Wu. J.; Marchi, E.; Frenkel, K.; O'Connor, O.A. Propolis and its active component, caffeic acid phenethyl ester (CAPE), modulate breast cancer therapeutic targets via an epigenetically mediated mechanism of action. J. Cancer Sci. Ther. 2013, 5, 334-342.
4. Madrigal-Santillán, E.; Madrigal-Bujaidar, E.; Alvarez-González, I.; Sumaya-Martínez, M.T.; Gutiérrez-Salinas, J.; Bautista, M.; Morales-González, A.; García-Luna, Y.; González-Rubio, M.; Aguilar-Faisal, J.L.; et al. Review of natural products with hepatoprotective effects. World J. Gastroentero. 2014, 20, 14787-14804.
5. Wojtyczka, R.D.; Dziedzic, A.; Idzik, D.; Kȩpa, M.; Kubina, R.; Kabala-Dzik, A.; Smolen-Dzirba, J.; Stojko, J.; Sajewicz, M.; Wasik, T.J. Susceptibility of Staphylococcus aureus clinical isolates to propolis extract alone or in combination with antimicrobial drugs. Molecules 2013, 18, 9623-9640.
6. Dziedzic, A.; Kubina, R.; Wojtyczka, R.D.; Kabala-Dzik, A.; Tanasiewicz, M.; Morawiec, T. The antibacterial effect of ethanol extract of polish propolis on mutans streptococci and lactobacilli isolated from saliva. Evid.-Based Complement. Alternat. Med. 2013, 2013, 681891-681902.
7. Wang, K.; Zhang, J.; Ping, S.; Ma, Q.; Chen, X.; Xuan, H.; Shi, J.; Zhang, C.; Hu, F. Anti-inflammatory effects of ethanol extracts of Chinese propolis and buds from poplar (Populus × canadensis). J. Ethnopharmacol. 2014, 155, 300-311.
8. Búfalo, M.C.; Bordon-Graciani, A.P.; Conti, B.J.; de Assis Golim, M.; Sforcin, J.M. The immunomodulatory effect of propolis on receptors expression, cytokine production and fungicidal activity of human monocytes. J. Pharm. Pharmacol. 2014, 66, 1497-1504.
9. Jastrzȩbska-Stojko, Z.; Stojko, R.; Rzepecka-Stojko, A.; Kabala-Dzik, A.; Stojko, J. Biological activity of propolis-honey balm in the treatment of experimentally-evoked burn wounds. Molecules 2013, 18, 14397-14413.
10. Kurek-Górecka, A.; Rzepecka-Stojko, A.; Górecki, M.; Stojko, J.; Sosada, M.; Swierczek-Zieba, G. Structure and antioxidant activity of polyphenols derived from propolis. Molecules 2013, 19, 78-101.
11. Su, K.Y.; Hsieh, C.Y.; Chen, Y.W.; Chuang, C.T.; Chen, C.T.; Chen, Y.L. Taiwanese green propolis and propolin G protect the liver from the pathogenesis of fibrosis via eliminating TGF-β-induced smad2/3 phosphorylation. J. Agric. Food Chem. 2014, 62, 3192-3201.
12. Socha, R.; Galkowska, D.; Bugaj, M.; Juszczak, L. Phenolic composition and antioxidant activity of propolis from various regions of Poland. Nat. Prod. Res. 2014, 29, 416-422.
13. Chen, Y.J.; Shiao, M.S.; Hsu, M.L.; Tsai, T.H.; Wang, S.Y. Effect of caffeic acid phenethyl ester, an antioxidant from propolis, on inducing apoptosis in human leukemic HL-60 cells. J. Agric. Food Chem. 2001, 49, 5615-5619.
14. Kustiawan, P.M.; Puthong, S.; Arung, E.T.; Chanchao, C. In vitro cytotoxicity of indonesian stingless bee products against human cancer cell lines. Asian Pac. J. Trop. Biomed. 2014, 4, 549-556.
15. Xuan, H.; Li, Z.; Yan, H.; Sang, Q.; Wang, K.; He, Q.; Wang, Y.; Hu, F. Antitumor activity of Chinese propolis in human breast cancer MCF-7 and MDA-MB-231 cells. Evid.-Based Complement. Altern. Med. 2014, 2014, doi:10.1155/2014/280120.
16. Kamiya, T.; Nishihara, H.; Hara, H.; Adachi, T. Ethanol extract of Brazilian red propolis induces apoptosis in human breast cancer MCF-7 cells through endoplasmic reticulum stress. J. Agric. Food Chem. 2012, 60, 11065-11070.
17. Kubina, R.; Kabala-Dzik, A.; Dziedzic, A.; Bielec, B.; Wojtyczka, R.D. Buldak, R.J.; Wyszynska, M.; Stawiarska-Piȩta, B.; Szaflarska-Stojko, E. The ethanol extract of Polish propolis exhibits anti-proliferative and/or pro-Apoptotic effect on HTC 116 colon cancer and Me45 malignant melanoma cells in vitro conditions. Adv. Clin. Exp. Med. 2015, 24, 203-212.
18. Grunberger, D.; Banerjee, R.; Eisinger, K.; Oltz, E.M.; Efros, L.; Caldwell, M.; Estevez, V.; Nakanishi, K. Preferential cytotoxicity on tumor cells by caffeic acid phenethyl ester isolated from propolis. Experientia 1988, 44, 230-232.
19. Yildirim, O.; Yilmaz, A.; Oz, O.; Vatansever, H.; Cinel, L.; Aslan, G.; Tamer, L.; Adigözel, U.; Arpaci, R.; Kanik, A.; Emekdaş, G. Effect of caffeic acid phenethyl ester on treatment of experimentally induced methicillin-resistant Staphylococcus epidermidis endophthalmitis in a rabbit model. Cell Biochem. Funct. 2007, 25, 693-700.
20. Wang, P.; Liu, C.; Sanches, T.; Zhong, Y.; Liu, B.; Xiong, J.; Neamati, N.; Zhao, G. Design and synthesis of novel nitrogen-containing polyhydroxylated aromatics as HIV-1 integrase inhibitors from caffeic acid phenethyl ester. Bioorg. Med. Chem. Lett. 2009, 19, 4574-4578.
21. Cho, M.S.; Park, W.S.; Jung, W.K.; Qian, Z.J.; Lee, D.S.; Choi, J.S.; Lee, D.Y.; Park, S.G.; Seo, S.K.; Kim, H.J., et al. Caffeic acid phenethyl ester promotes anti-inflammatory effects by inhibiting MAPK and NF-κB signaling in activated HMC-1 human mast cells. Pharm. Biol. 2014, 52, 926-932.
22. Altuntaş, A.; Yilmaz, H.R.; Altuntaş, A.; Uz, E.; Demir, M.; Gökçimen, A.; Aksu, O.; Bayram, D.S.; Sezer, M.T. Caffeic acid phenethyl ester protects against amphotericin B induced nephrotoxicity in rat model. Biomed. Res. Int. 2014, 2014, 702981-702988.
23. Zhou, K.; Li, X.; Du, Q.; Li, D.; Hu, M.; Yang, X.; Jiang, Q.; Li, Z. A CAPE analogue as novel antiplatelet agent efficiently inhibits collagen-induced platelet aggregation. Pharmazie 2014, 69, 615-620.
24. Wu, J.; Omene, C.; Karkoszka, J.; Bosland, M.; Eckard, J.; Klein, C.B.; Frenkel, K. Caffeic acid phenethyl ester (CAPE), derived from a honeybee product propolis, exhibits a diversity of anti-Tumor effects in pre-clinical models of human breast cancer. Cancer Lett. 2011, 308, 43-53.
25. Akyol, S.; Ozturk, G.; Ginis, Z.; Armutcu, F.; Yigitoglu, M.R.; Akyol, O. In vivo and in vitro antineoplastic actions of caffeic acid phenethyl ester (CAPE): Therapeutic perspectives. Nutr. Cancer 2013, 65, 515-526.
26. Borrelli, F.; Izzo, A.A.; Di Carlo, G.; Maffia, P.; Russo, A.; Maiello, F.M.; Capasso, F.; Mascolo, N. Effect of a propolis extract and caffeic acid phenethyl ester on formation of aberrant crypt foci and tumors in the rat colon. Fitoterapia 2002, 73, S38-S43.
27. Xiang, D.; Wang, D.; He, Y.; Xie, J.; Zhong, Z.; Li, Z.; Xie, J. Caffeic acid phenethyl ester induces growth arrest and apoptosis of colon cancer cells via the beta-catenin/T-cell factor signaling. Anti-Cancer Drugs 2006, 17, 753-762.
28. Chen, M.F.; Wu, C.T.; Chen, Y.J.; Keng, P.C.; Chen, W.C. Cell killing and radiosensitization by caffeic acid phenethyl ester (CAPE) in lung cancer cells. J. Radiat. Res. 2004, 45, 253-260.
29. Kudugunti, S.K.; Vad, N.M.; Ekogbo, E.; Moridani, M.Y. Efficacy of caffeic acid phenethyl ester (CAPE) in skin B16-F0 melanoma tumor bearing C57BL/6 mice. Investig. New Drugs 2011, 29, 52-62.
30. Wu, C.S.; Chen, M.F.; Lee, I.L.; Tung, S.Y. Predictive role of nuclear factor-κB activity in gastric cancer: A promising adjuvant approach with caffeic acid phenethyl ester. J. Clin. Gastroenterol. 2007, 41, 894-900.
31. Chen, M.J.; Chang, W.H.; Lin, C.C.; Liu, C.Y.; Wang, T.E.; Chu, C.H.; Shih, S.C.; Chen, Y.J. Caffeic acid phenethyl ester induces apoptosis of human pancreatic cancer cells involving caspase and mitochondrial dysfunction. Pancreatology 2008, 8, 566-576.
32. Lee, K.; Kang, N.; Kim, J.; Lee, K.; Lee, D.; Hur, H.J.; Lee, H.J. Caffeic acid phenethyl ester inhibits invasion and expression of matrix metalloproteinase in SK-Hep1 human hepatocellular carcinoma cells by targeting nuclear factor κB. Genes Nutr. 2008, 2, 319-322.
33. Huang, M.T.; Ma, W.; Yen, P.; Xie, J.G.; Han, J.; Frenkel, K.; Grunberger, D.; Conney, A.H. Inhibitory effects of caffeic acid phenethyl ester (CAPE) on 12-O-Tetradecanoylphorbol-13-Acetate-induced tumor promotion in mouse skin and the synthesis of DNA, RNA and protein in HeLa cells. Carcinogenesis 1996, 17, 761-765.
34. Onori, P.; DeMorrow, S.; Gaudio, E.; Franchitto, A.; Mancinelli, R.; Venter, J.; Kopriva, S.; Ueno, Y.; Alvaro, D.; Savage, J.; et al. Caffeic acid phenethyl ester decreases cholangiocarcinoma growth by inhibition of NFκB and induction of apoptosis. Int. J. Cancer 2009, 125, 565-576.
35. Kuo, H.C.; Kuo, W.H.; Lee, Y.J.; Lin, W.L.; Chou, F.P.; Tseng, T.H. Inhibitory effect of caffeic acid phenethyl ester on the growth of C6 glioma cells in vitro and in vivo. Cancer Lett. 2006, 234, 199-208.
36. Watabe, M.; Hishikawa, K.; Takayanagi, A.; Shimizu, N.; Nakaki, T. Caffeic acid phenethyl ester induces apoptosis by inhibition of NFκB and activation of Fas in human breast cancer MCF-7 cells. J. Biol. Chem. 2004, 279, 6017-6026.
37. Eng-Wong, J.; Isaacs, C. Prediction of benefit from adjuwant treatment in patients with breast cancer. Clin. Breast Cancer 2010, 10, 32-37.
38. Omene, C.O.; Wu, J.; Frenkel, K. Caffeic acid phenethyl ester (CAPE) derived from propolis, a honeybee product, inhibits growth of breast cancer stem cells. Investig. New Drugs 2012, 30, 1279-1288.
39. Guzman, J.D. Natural cinnamic acids, synthetic derivatives and hybrids with antimicrobial activity. Molecules 2014, 19, 19292-19349.
40. Etoh, H.; Murakami, K.; Yogoh, T.; Ishikawa, H.; Fukuyama, Y.; Tanaka, H. Anti-oxidative compounds in barley tea. Biosci. Biotechnol. Biochem. 2004, 68, 2616-2618.
41. Borges, A.; Ferreira, C.; Saavedra, M.J.; Simões, M. Antioxidant and antimicrobial activities of ferulic acid esters from ochrosia oppositifolia. Microb. Drug Resist. 2013, 19, 256-265.
42. Stojković, D.; Petrović, J.; Soković, M.; Glamoclija, J.; Kukić-Marković, J.; Petrović, S. In situ antioxidant and antimicrobial activities of naturally occurring caffeic acid, p-coumaric acid and rutin, using food systems. J. Sci. Food Agric. 2013, 93, 3205-3208
43. Fernández, M.A.; Sáenz, M.T.; García, M.D. Anti-inflammatory activity in rats and mice of phenolic acids isolated from Scrophularia frutescens. J. Pharm. Pharmacol. 1998, 50, 1183-1186.
44. Boisard, S.; Le Ray, A.-M.; Landreau, A.; Kempf, M.; Cassisa, V.; Flurin, C.; Richomme, P. Antifungal and antibacterial metabolites from a French poplar type propolis. Evid.-Based Complement. Altern. Med. 2015, 2015, doi:10.1155/2015/319240.
45. Hämäläinen, M.; Nieminen, R.; Vuorela, P.; Heinonen, M.; Moilanen, E. Anti-inflammatory effects of flavonoids: Genistein, kaempferol, quercetin, and daidzein inhibit STAT-1 and NF-κB activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-κB activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediat. Inflamm. 2007, 2007, 45673, doi:10.1155/2007/45673.
46. Li, R.R.; Pang, L.L.; Du, Q.; Shi, Y.; Dai, W.J.; Yin, K.S. Apigenin inhibits allergen-induced airway inflammation and switches immune response in a murine model of asthma. Immunopharm. Immunot. 2010, 32, 364-370.
47. Lee, J.H.; Zhou, H.Y.; Cho, S.Y.; Kim, Y.S.; Lee, Y.S.; Jeong, C.S. Anti-inflammatory mechanisms of apigenin: Inhibition of cyclooxygenase-2 expression, adhesion of monocytes to human umbilical vein endothelial cells, and expression of cellular adhesion molecules. Arch. Pharm. Res. 2007, 30, 1318-1327.
48. Peng, L.; Yang, S.; Cheng, Y.J.; Chen, F.; Pan, S.; Fan, G. Antifungal activity and action mode of pinocembrin from propolis against Penicillium italicum. Food Sci. Biotechnol. 2012, 21, 1533-1539.
49. Zhang, M.; Swarts, S.G.; Yin, L.; Liu, C.; Tian, Y.; Cao, Y.; Swarts, M.; Yang, S.; Zhang, S.B.; Zhang, K., et al. Antioxidant properties of quercetin. Adv. Exp. Med. Biol. 2011, 701, 283-289.
50. Liu, Y.; Song, X.; He, J.; Zheng, X.; Wu, H. Synthetic derivatives of chrysin and their biological activities. Med. Chem. Res. 2014, 23, 555-563.
51. Paulíková, H.; Berczeliová, E. The effect of quercetin and galangin on glutathione reductase. Biomed. Pap. Med. Fac. Univ. Palacky. Olomouc. Czech Repub. 2005, 149, 497-500.
52. Lee, Y.S.; Kang, O.H.; Choi, J.G.; Oh, Y.C.; Chae, H.S.; Kim, J.H.; Park, H.; Sohn, D.H.; Wang, Z.T.; Kwon, D.Y. Synergistic effects of the combination of galangin with gentamicin against methicillin-resistant Staphylococcus aureus. J. Microbiol. 2008, 46, 283-288.
53. Carballo-Villalobos, A.I.; González-Trujano, M.E.; López-Muñoz, F.J. Evidence of mechanism of action of anti-inflammatory/antinociceptive activities of acacetin. Eur. J. Pain 2014, 18, 396-405.
54. Lee, Y.J.; Kuo, H.C.; Chu, C.Y.; Wang, C.J.; Lin, W.C.; Tseng, T.H. Involvement of tumor suppressor protein p53 and p38 MAPK in caffeic acid phenethyl ester-induced apoptosis of C6 glioma cells. Biochem. Pharmacol. 2003, 66, 2281-2289.
55. Jin, U.H.; Song, K.H.; Motomura, M.; Suzuki, I.; Gu, Y.H.; Kang, Y.J.; Moon, T.C.; Kim, C.H. Caffeic acid phenethyl ester induces mitochondriamediated apoptosis in human myeloid leukemia U937 cells. Mol. Cell Biochem. 2008, 310, 43-48.
56. Szliszka, E.; Zydowicz, G.; Janoszka, B.; Dobosz, C.; Kowalczyk-Ziomek, G.; Król, W. Ethanolic extract of Brazilian green propolis sensitizes prostate cancer cells to TRAIL induced apoptosis. Int. J. Oncol. 2011, 38, 941-953.