Synergistic effect of cucurbitacin B in combination with curcumin via enhancing apoptosis induction and reversing multidrug resistance in human hepatoma cells

European Journal of Pharmacology

Volumn 768, Issue , 2015, Pages 28-40

  Sun, Yuqi ^a,b   Zhang, Jie ^a   Zhou, Jiaying ^a   Huang, Ziyuan ^a   Hu, Haiyang ^a   Qiao, Mingxi ^a   Zhao, Xiuli ^a   Chen, Dawei ^a  

^a SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^b JINZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Cucurbitacin B; Curcumin; Enhancing apoptosis induction; Reversing multidrug resistance; Synergy

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 3; CUCURBITACIN B; CURCUMIN; FLUOROURACIL; MULTIDRUG RESISTANCE PROTEIN; UNCLASSIFIED DRUG; VERAPAMIL; ADENOSINE TRIPHOSPHATE; TRITERPENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL SURVIVAL; CELL ULTRASTRUCTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG ANTAGONISM; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG POTENTIATION; ENZYME ACTIVATION; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; S PHASE CELL CYCLE CHECKPOINT; SINGLE DRUG DOSE; TUMOR VOLUME; ANIMAL; BAGG ALBINO MOUSE; BODY WEIGHT; CELL CYCLE; CELL PROLIFERATION; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION REGULATION; INTRACELLULAR SPACE; LIVER TUMOR; METABOLISM; MULTIDRUG RESISTANCE; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; BIOLOGICAL TRANSPORT; BODY WEIGHT; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CURCUMIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; ENZYME ACTIVATION; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SPACE; LIVER NEOPLASMS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED BALB C; P-GLYCOPROTEIN; TRITERPENES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84947604465     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2015.10.003     Document Type: Article

References (42)

1. B.B. Aggarwal, I.D. Bhatt, H. Ichikawa, K.S. Ahn, G. Sethi, S.K. Sandur, C. Sundaram, N. Seeram, and S. Shishodia Curcumin-biological and medicinal properties P.N. Ravindran, K.N. Babu, K. Sivaraman, Turmeric the Genus Curcuma 2007 CRC Press NY 297 368
2. B.B. Aggarwal, A. Kumar, and A.C. Bharti Anticancer potential of curcumin: preclinical and clinical studies Anticancer Res. 23 2003 363 398
3. H.P. Ammon, and M.A. Wahl Pharmacology of curcuma longa Planta Med. 57 1991 1 7
4. D. Cerny, N. Lekic, K. Vanova, L. Muchova, A. Horinek, E. Kmonickova, Z. Zidek, L. Kamenikova, and H. Farghali Hepatoprotective effect of curcumin in lipopolysaccharide/-galactosamine model of liver injury in rats: relationship to HO-1/CO antioxidant system Fitoterapia 82 2011 786 791
5. K.T. Chan, K. Li, S.L. Liu, K.H. Chu, M. Toh, and W.D. Xie Cucurbitacin B inhibits STAT3 and the Raf/MEK/ERK pathway in leukemia cell line K562 Cancer Lett. 289 2010 46 52
6. K.T. Chan, F.Y. Meng, Q. Li, C.Y. Ho, T.S. Lam, Y. To, W.H. Lee, M. Li, K.H. Chu, and M. Toh Cucurbitacin B induces apoptosis and S phase cell cycle arrest in BEL-7402 human hepatocellular carcinoma cells and is effective via oral administration Cancer Lett. 294 2010 118 124
7. J.C. Chen, M.H. Chiu, R.L. Nie, G.A. Cordell, and S.X. Qiu Cucurbitacins and cucurbitane glycosides: structures and biological activities Nat. Prod. Rep. 22 2005 386 399
8. Z. Darzynkiewicz, J.P. Robinson, and M. Roederer Essential Cytometry Methods 2012 Science Press Beijing, China 658
9. G. Dayan, H. Baubichon-Cortay, J.M. Jault, J.C. Cortay, G. Deleage, and A. Di Pietro Recombinant N-terminal nucleotide-binding domain from mouse P-glycoprotein. Overexpression, purification, and role of cysteine 430 J. Biol. Chem. 271 1996 11652 11658
10. Y. Gao, M.S. Islam, J. Tian, V.W. Lui, and D. Xiao Inactivation of ATP citrate lyase by Cucurbitacin B: a bioactive compound from cucumber, inhibits prostate cancer growth Cancer Lett. 349 2014 15 25
11. W.R. Garcia-Nino, and J. Pedraza-Chaverri Protective effect of curcumin against heavy metals-induced liver damage Food Chem. Toxicol. 69 2014 182 201
12. W. Hong, D. Chen, X. Zhang, J. Zeng, H. Hu, X. Zhao, and M. Qiao Reversing multidrug resistance by intracellular delivery of Pluronic P85 unimers Biomaterials 34 2013 9602 9614
13. Y. Hu, S. Wang, X. Wu, J. Zhang, R. Chen, M. Chen, and Y. Wang Chinese herbal medicine-derived compounds for cancer therapy: a focus on hepatocellular carcinoma J. Ethnopharmacol. 149 2013 601 612
14. H. Kausar, R. Munagala, S.S. Bansal, F. Aqil, M.V. Vadhanam, and R.C. Gupta Cucurbitacin B potently suppresses non-small-cell lung cancer growth: identification of intracellular thiols as critical targets Cancer Lett. 332 2013 35 45
15. R. Krishna, and L.D. Mayer Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs Eur. J. Pharm. Sci. 11 2000 265 283
16. Y. Kwon Curcumin as a cancer chemotherapy sensitizing agent J. Korean Soc. Appl. Biol. Chem. 57 2014 273 280
17. D.H. Lee, G.B. Iwanski, and N.H. Thoennissen Cucurbitacin: ancient compound shedding new light on cancer treatment Sci. World J. 10 2010 413 418
18. H.I. Lee, R.A. McGregor, M.S. Choi, K.I. Seo, U.J. Jung, J. Yeo, M.J. Kim, and M.K. Lee Low doses of curcumin protect alcohol-induced liver damage by modulation of the alcohol metabolic pathway, CYP2E1 and AMPK Life Sci. 93 2013 693 699
19. C. Ling, B. Li, C. Zhang, D. Zhu, X. Huang, W. Gu, and S. Li Inhibitory effect of recombinant adenovirus carrying melittin gene on hepatocellular carcinoma Ann. Oncol. 16 2005 109 115
20. Y.L. Lo, W. Wang, and C.T. Ho 7,3′,4′-Trihydroxyisoflavone modulates multidrug resistance transporters and induces apoptosis via production of reactive oxygen species Toxicology 302 2012 221 232
21. T. Luu, C. Chung, and G. Somlo Combining emerging agents in advanced breast cancer Oncologist 16 2011 760 771
22. J. Ma, Y. Zi Jiang, H. Shi, C. Mi, J. Li, J. Xing Nan, X. Wu, J. Joon Lee, and X. Jin Cucurbitacin B inhibits the translational expression of hypoxia-inducible factor-1alpha Eur. J. Pharmacol. 723 2014 46 54
23. W.G. Nelson, A.M. De Marzo, and W.B. Isaacs Prostate cancer N Engl. J. Med. 349 2003 366 381
24. T. Nishikawa, Y. Kohjimoto, M. Nishihata, S. Ebisuno, and I. Hara Synergistic antitumor effects of fleroxacin with 5-fluorouracil in vitro and in vivo for bladder cancer cell lines Urology 74 2009 1370 1376
25. M. Notarbartolo, P. Poma, D. Perri, L. Dusonchet, M. Cervello, and N. D'Alessandro Antitumor effects of curcumin, alone or in combination with cisplatin or doxorubicin, on human hepatic cancer cells. Analysis of their possible relationship to changes in NF-kB activation levels and in IAP gene expression Cancer Lett. 224 2005 53 65
26. H.S. Park, K.I. Park, D.H. Lee, S.R. Kang, A. Nagappan, J.A. Kim, E.H. Kim, W.S. Lee, S.C. Shin, Y.S. Hah, and G.S. Kim Polyphenolic extract isolated from Korean Lonicera japonica Thunb. induce G2/M cell cycle arrest and apoptosis in HepG2 cells: involvements of PI3K/Akt and MAPKs Food Chem. Toxicol. 50 2012 2407 2416
27. R. Prasanna, H. Chinnakonda Chandramoorthy, P. Ramaiyapillai, and D. Sakthisekaran In vitro evaluation of anticancer effect of Cassia auriculata leaf extract and curcumin through induction of apoptosis in human breast and larynx cancer cell lines Biomed. Prev. Nutr. 1 2011 153 160
28. H. Qian, Y. Yang, and X. Wang Curcumin enhanced adriamycin-induced human liver-derived Hepatoma G2 cell death through activation of mitochondria-mediated apoptosis and autophagy Eur. J. Pharm. Sci. 43 2011 125 131
29. Y. Sadzuka, M. Nagamine, T. Toyooka, Y. Ibuki, and T. Sonobe Beneficial effects of curcumin on antitumor activity and adverse reactions of doxorubicin Int. J. Pharm. 432 2012 42 49
30. J. Tang, Q. Fu, Y. Wang, K. Racette, D. Wang, and F. Liu Vitamin E reverses multidrug resistance in vitro and in vivo Cancer Lett. 336 2013 149 157
31. T. Tannin-Spitz, S. Grossman, S. Dovrat, H.E. Gottlieb, and M. Bergman Growth inhibitory activity of cucurbitacin glucosides isolated from Citrullus colocynthis on human breast cancer cells Biochem. Pharmacol. 73 2007 56 67
32. N.H. Thoennissen, G.B. Iwanski, N.B. Doan, R. Okamoto, P. Lin, S. Abbassi, J.H. Song, D. Yin, M. Toh, W.D. Xie, J.W. Said, and H.P. Koeffler Cucurbitacin B induces apoptosis by inhibition of the JAK/STAT pathway and potentiates antiproliferative effects of gemcitabine on pancreatic cancer cells Cancer Res. 69 2009 5876 5884
33. I. Vermes, C. Haanen, and C. Reutelingsperger Flow cytometry of apoptotic cell death J. Immunol. Methods 243 2000 167 190
34. X.A. Wan, G.P. Sun, H. Wang, S.P. Xu, Z.G. Wang, and S.H. Liu Synergistic effect of paeonol and cisplatin on oesophageal cancer cell lines Dig. Liver Dis. 40 2008 531 539
35. W.Z. Wang, J. Cheng, J. Luo, and S.M. Zhuang Abrogation of G2/M arrest sensitizes curcumin-resistant hepatoma cells to apoptosis FEBS Lett. 582 2008 2689 2695
36. Z. Wang, S. Desmoulin, S. Banerjee, D. Kong, Y. Li, R.L. Deraniyagala, J. Abbruzzese, and F.H. Sarkar Synergistic effects of multiple natural products in pancreatic cancer cells Life Sci. 83 2008 293 300
37. M. Wink, M.L. Ashour, and M.Z. El-Readi Secondary metabolites from plants inhibiting ABC transporters and reversing resistance of cancer cells and microbes to cytotoxic and antimicrobial agents Front. Microbiol. 3 2012 130
38. Y.-Y. Xie, Z.-Z. Li, G.-J. Lin, H.-L. Huang, X.-Z. Wang, Z.-H. Liang, G.-B. Jiang, and Y.-J. Liu DNA interaction, cytotoxicity, apoptotic activity, cell cycle arrest, reactive oxygen species and mitochondrial membrane potential assay induced by ruthenium(II) polypyridyl complexes Inorg. Chim. Acta 405 2013 228 234
39. X. Xue, J.-L. Yu, D.-Q. Sun, W. Zou, F. Kong, J. Wu, H.-p Liu, X.-j Qu, and R.-M. Wang Curcumin as a multidrug resistance modulator - a quick review Biomed. Prev. Nutr. 3 2013 173 176
40. H.Y. Yang, L. Zhao, Z. Yang, Q. Zhao, L. Qiang, J. Ha, Z.Y. Li, Q.D. You, and Q.L. Guo Oroxylin A reverses multi-drug resistance of human hepatoma BEL7402/5-FU cells via downregulation of P-glycoprotein expression by inhibiting NF-kappaB signaling pathway Mol. Carcinog. 51 2012 185 195
41. H. Zhu, F. Liu, J. Guo, J. Xue, Z. Qian, and Y. Gu Folate-modified chitosan micelles with enhanced tumor targeting evaluated by near infrared imaging system Carbohydr. Polym. 86 2015 1118 1129
42. L. Zhu, L. Zhao, H. Wang, Y. Wang, D. Pan, J. Yao, Z. Li, G. Wu, and Q. Guo Oroxylin a reverses P-glycoprotein-mediated multidrug resistance of MCF7/ADR cells by G2/M arrest Toxicol. Lett. 219 2013 107 115