Induction of cell cycle arrest and apoptosis by betulinic acid-rich fraction from Dillenia suffruticosa root in MCF-7 cells involved p53/p21 and mitochondrial signalling pathway

Journal of Ethnopharmacology

Volumn 166, Issue , 2015, Pages 270-278

  Foo, Jhi Biau ^a   Saiful Yazan, Latifah ^a   Tor, Yin Sim ^a   Wibowo, Agustono ^a   Ismail, Norsharina ^a   How, Chee Wun ^a   Armania, Nurdin ^a   Loh, Su Peng ^a   Ismail, Intan Safinar ^a   Cheah, Yoke Kqueen ^a   Abdullah, Rasedee ^a  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

Author keywords

Apoptosis; Betulinic acid; Breast cancer; Dillenia suffruticosa; Triterpene

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; BETULIC ACID; CASPASE 3; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DICHLOROMETHANE; KATONIC ACID; KOETJAPIC ACID; MESSENGER RNA; PHARMACOLOGY; PLANT EXTRACT; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P21; PROTEIN P53; TRITERPENE; TRITERPENE DERIVATIVE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BREAST CANCER; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL FRACTIONATION; CHEMISTRY; COLUMN CHROMATOGRAPHY; CONTROLLED STUDY; DEGRADATION; DILLENIA SUFFRUTICOSA; DILLENIACEAE; DRUG EFFECTS; DRUG ISOLATION; DRUG STRUCTURE; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; MCF 7 CELL LINE; METABOLISM; MITOCHONDRION; MTT ASSAY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLANT ROOT; PROTEIN EXPRESSION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TUMOR CELL LINE; UPREGULATION; WESTERN BLOTTING;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; CHEMISTRY; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DILLENIACEAE; DRUG EFFECTS; G0 PHASE; G1 PHASE CELL CYCLE CHECKPOINTS; HUMANS; MCF-7 CELLS; METABOLISM; MITOCHONDRIA; PHARMACOLOGY; PLANT EXTRACTS; PLANT ROOTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRITERPENES; TUMOR SUPPRESSOR PROTEIN P53;

DILLENIA SUFFRUTICOSA; DILLENIACEAE;

EID: 84964241110     PISSN: 03788741     EISSN: 18727573     Source Type: Journal    
DOI: 10.1016/j.jep.2015.03.039     Document Type: Article

References (58)

1. S.H. Akbas, M. Timur, and T. Ozben The effect of quercetin on topotecan cytotoxicity in MCF-7 and MDA-MB 231 human breast cancer cells J. Surg. Res. 125 2005 49 55
2. M. Alkhalaf, and A.M. El-Mowafy Overexpression of wild-type p53 gene renders MCF-7 breast cancer cells more sensitive to the antiproliferative effect of progesterone J. Endocrinol. 179 2003 55 62
3. M.L. Antony, S.H. Kim, and S.V. Singh Critical role of p53 upregulated modulator of apoptosis in benzyl isothiocyanate-induced apoptotic cell death PLoS One 7 2012 e32267
4. 2/M arrest and apoptosis Molecules 18 2013 13320 13339
5. 2/M cell cycle arrest J. Ethnopharmacol. 146 2013 525 535
6. M.P. Badakhshan, S. Sreenivasan, R.N. Jegathambigai, and R. Surash Anti-leukemia activity of methanolic extracts of Lantana camara Pharmacogn. Res. 1 2009 274 279
7. J. Bartek, and J. Lukas Mammalian G1- and S-phase checkpoints in response to DNA damage Curr. Opin. Cell Biol. 13 2001 738 747
8. M.M. Bradford Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
9. M.R. Bratton, B.N. Duong, S. Elliott, C.B. Weldon, B.S. Beckman, J.A. McLachlan, and M.E. Burow Regulation of ERalpha-mediated transcription of Bcl-2 by PI3K-AKT crosstalk: implications for breast cancer cell survival Int. J. Oncol. 37 2010 541 550
10. K. Breitschopf, J. Haendeler, P. Malchow, A.M. Zeiher, and S. Dimmeler Posttranslational modification of Bcl-2 facilitates its proteasome-dependent degradation: molecular characterization of the involved signaling pathway Mol. Cell. Biol. 20 2000 1886 1896
11. P. Cao, X.T. Cai, W.G. Lu, F. Zhou, and J.G. Huo Growth inhibition and induction of apoptosis in SHG-44 glioma gells by chinese medicine formula "Pingliu Keli" Evid. Based Complement. Altern. Med. 2011 2011 (Article ID 958243, 9 pages)
12. P. Chatterjee, S.A. Kouzi, J.M. Pezzuto, and M.T. Hamann Biotransformation of the antimelanoma agent betulinic acid by Bacillus megaterium ATCC 13368 Appl. Environ. Microbiol. 66 2000 3850 3855
13. S. Cunha, Y.C. Lin, E.A. Goossen, C.I. DeVette, M.R. Albertella, S. Thomson, M.J. Mulvihill, and A.L. Welm The RON receptor tyrosine kinase promotes metastasis by triggering MBD4-dependent DNA methylation reprogramming Cell Rep. 6 2014 141 154
14. A.A. Damle, Y.P. Pawar, and A.A. Narkar Anticancer activity of betulinic acid on MCF-7 tumors in nude mice Indian J. Exp. Biol. 51 2013 485 491
15. D. Deeb, X. Gao, Y.B. Liu, K. Pindolia, and S.C. Gautam Pristimerin, a quinonemethide triterpenoid, induces apoptosis in pancreatic cancer cells through the inhibition of pro-survival Akt/NF-κB/mTOR signaling proteins and anti-apoptotic Bcl-2 Int. J. Oncol. 44 2014 1707 1715
16. C.A. Dehelean, C. Şoica, I. Ledeţi, M. Aluaş, I. Zupko, A. GC.Z.luşcan, S. Cinta-Pinzaru, and M. Munteanu Study of the betulin enriched birch bark extracts effects on human carcinoma cells and ear inflammation Chem. Cent. J. 6 2012 (Article 137, 9 pages)
17. F. Essmann, I.H. Engels, G. Totzke, K. Schulze-Osthoff, and R.U. Jänicke Apoptosis resistance of MCF-7 breast carcinoma cells to ionizing radiation is independent of p53 and cell cycle control but caused by the lack of caspase-3 and a caffeine-inhibitable event Cancer Res. 64 2004 7065 7072
18. J.B. Foo, L.S. Yazan, Y.S. Tor, N. Armania, N. Ismail, M.U. Imam, S.K. Yeap, Y.K. Cheah, R. Abdullah, and M. Ismail Induction of cell cycle arrest and apoptosis in caspase-3 deficient MCF-7 cells by Dillenia suffruticosa root extract via multiple signalling pathways BMC Complement. Altern. Med. 14 2014 (Article 197, 16 pages)
19. G. Gao, and Q.P. Dou G1 phase-dependent expression of Bcl-2 mRNA and protein correlates with chemoresistance of human cancer cells Mol. Pharmacol. 58 2000 1001 1010
20. D.X. Hou, X. Tong, N. Terahara, D. Luo, and M. Fujii Delphinidin 3-sambubioside, a Hibiscus anthocyanin, induces apoptosis in human leukemia cells through reactive oxygen species-mediated mitochondrial pathway Arch. Biochem. Biophys. 440 2005 101 109
21. K.W. Hunter, N.P. Crawford, and J. Alsarraj Mechanisms of metastasis Breast Cancer Res. 10 2008 10.1186/bcr1988 (10 pages)
22. Y. Imanishi, B. Hu, G. Xiao, X. Yao, and S.Y. Cheng Angiopoietin-2, an angiogenic regulator, promotes initial growth and survival of breast cancer metastases to the lung through the integrin-linked kinase (ILK)-AKT-B cell lymphoma 2 (Bcl-2) pathway J. Biol. Chem. 286 2011 29249 29260
23. S.R. Jada, C. Matthews, M.S. Saad, A.S. Hamzah, N.H. Lajis, M.F.G. Stevens, and J. Stanslas Benzylidene derivatives of andrographolide inhibit growth of breast and colon cancer cells in vitro by inducing G1 arrest and apoptosis Br. J. Pharmacol. 155 2008 641 654
24. N. Kaneda, J.M. Pezzuto, A.D. Kinghorn, N.R. Farnsworth, T. Santisuk, P. Tuchinda, J. Udchachon, and V. Reutrakul Plant anticancer agents, L. cytotoxic triterpenes from Sandoricum koetjape stems J. Nat. Prod. 55 1992 654 659
25. J.H. Kessler, F.B. Mullauer, G.M. de Roo, and J.P. Medema Broad in vitro efficacy of plant-derived betulinic acid against cell lines derived from the most prevalent human cancer types Cancer Lett. 251 2007 132 145
26. H. Kumar, I.-S. Kim, S.V. More, B.-W. Kim, Y.-Y. Bahk, and D.-K. Choi Gastrodin protects apoptotic dopaminergic neurons in a toxin-induced parkinsons disease model Evid. Based Complement. Altern. Med. 2013 2013 (Article ID 514095, 13 pages)
27. S.Y. Latifah, J.B. Foo, S.A.A. Ghafar, K.W. Chan, P.M. Tahir, and M. Ismail Effect of kenaf seed oil from different ways of extraction towards ovarian cancer cells Food Bioprod. Process. 89 2011 328 332
28. S.H. Liu, and Y.C. Cheng Old formula, new Rx: the journey of PHY906 as cancer adjuvant therapy J. Ethnopharmacol. 140 2012 614 623
29. Y.B. Liu, X. Gao, D. Deeb, A.S. Arbab, and S.C. Gautam Pristimerin induces apoptosis in prostate cancer cells by downregulating Bcl-2 through ROS-dependent ubiquitin-proteasomal degradation pathway J. Carcinog. Mutagen. S6 2013 005 10.4172/2157-2518.S6-005
30. E. Manchado, M. Guillamot, and M. Malumbres Killing cells by targeting mitosis Cell Death Differ. 19 2012 369 377
31. M. Mego, S.A. Mani, and M. Cristofanilli Molecular mechanisms of metastasis in breast cancer-clinical applications Nat. Rev. Clin. Oncol. 7 2010 693 701
32. S.U. Mertens-Talcott, M.C. Bertoldi, G.D. Noratto, and S. Safe Betulinic acid decreases ER-negative breast cancer cell growth in vitro and in vivo: role of sp transcription factors and microRNA-27a:ZBTB10 Mol. Carcinog. 52 2012 591 602
33. S. Mohan, S.I. Abdelwahab, B. Kamalidehghan, S. Syam, K.S. May, N.S.M. Harmal, N. Shafifiyaz, A.H.A. Hadi, N.M. Hashim, M. Rahmani, M.M.E. Taha, S.C. Cheah, and A. Zajmi Involvement of NF-κB and Bcl2/Bax signaling pathways in the apoptosis of MCF7 cells induced by a xanthone compound Pyranocycloartobiloxanthone A Phytomedicine 19 2012 1007 1015
34. S.Y. Muliawan Effect of Dillenia suffruticosa extract on dengue virus type 2 replication Universa Med. 27 2008 1 5
35. W.K. Ng, L.S. Yazan, and M. Ismail Thymoquinone from Nigella sativa was more potent than cisplatin in eliminating of SiHa cells via apoptosis with down-regulation of Bcl-2 protein Toxicol. In Vitro 25 2011 1392 1398
36. E. Pisha, H. Chai, I.S. Lee, T.E. Chagwedera, N.R. Farnsworth, G.A. Cordell, C.W. Beecher, H.H. Fong, A.D. Kinghorn, D.M. Brown, M.C. Wani, M.E. Wall, T.J. Hieken, T.K.D. Gupta, and J.M. Pezzuto Discovery of betulinic acid as a selective inhibitor of human melanoma that functions by induction of apoptosis Nat. Med. 1 1995 1046 1051
37. R. Prasad, and B. Koch Antitumor activity of ethanolic extract of Dendrobium formosum in T-cell lymphoma: an in vitro and in vivo study BioMed Res. Int. 2014 2014 (Article ID 753451, 11 pages)
38. S. Prasad, V.R. Yadav, R. Kannappan, and B.B. Aggarwal Ursolic acid, a pentacyclin triterpene, potentiates TRAIL-induced apoptosis through p53-independent up-regulation of death receptors: evidence for the role of reactive oxygen species and JNK J. Biol. Chem. 286 2011 5546 5557
39. T. Reiner, R. Parrondo, A.D.L. Pozas, D. Palenzuela, and C. Perez-Stable Betulinic acid selectively increases protein degradation and enhances prostate cancer-specific apoptosis: possible role for inhibition of deubiquitinase activity PLoS One 8 2013 e56234
40. E. Shankar, S. Krishnamurthy, R. Paranandi, and A. Basu PKCepsilon induces Bcl-2 by activating CREB Int. J. Oncol. 36 2010 883 888
41. C.M. Şoica, C.A. Dehelean, C. Peev, M. Aluas, I. Zupkó, P.J. Kása, and E. Alexa Physico-chemical comparison of betulinic acid, betulin and birch bark extract and in vitro investigation of their cytotoxic effects towards skin epidermoid carcinoma (A431), breast carcinoma (MCF7) and cervix adenocarcinoma (HeLa) cell lines Nat. Prod. Res. 26 2012 968 974
42. T. Srisawat, Y. Sukpondma, S. Chimplee, K. Kanokwiroon, A. Tedasen, and P. Graidist Extracts from Vatica diospyroides type SS fruit show low dose activity against MDA-MB-468 breast cancer cell line via apoptotic action BioMed Res. Int. 2014 2014 (Article ID 479602, 8 pages)
43. Y.F. Sun, C.K. Song, H. Viernstein, F. Unger, and Z.S. Liang Apoptosis of human breast cancer cells induced by microencapsulated betulinic acid from sour jujube fruits through the mitochondria transduction pathway Food Chem. 138 2013 1998 2007
44. G. Tadesse, P. Reneela, and A. Dekebo Isolation and characterization of natural products from Helinus mystachnus (Rhamnaceae) J. Chem. Pharm. Res. 4 2012 (Article ID 958243, 9 pages)
45. Y. Tan, R. Yu, and J.M. Pezzuto Betulinic acid-induced programmed cell death in human melanoma cells involves mitogen-activated protein kinase activation Clin. Cancer Res. 9 2003 2866 2875
46. M. Tasyriq, I.A. Najmuldeen, L.A. Lionel, K. Mohamad, K. Awang, and N. Hasima 7α-hydroxy-β-sitosterol from Chisocheton tomentosus induces apoptosis via dysregulation of cellular Bax/Bcl-2 ratio and cell cycle arrest by downregulating ERK1/2 activation Evid. Based Complement. Altern. Med. 2012 2012 (Article ID 765316, 12 pages)
47. W.R. Taylor, and A. Grabovich Targeting the cell cycle to kill cancer cells M. Hacker, K. Bachmann, W. Messer, Pharmacology: Principles and Practice 2009 Academic Press Burlington, MA 429 453
48. M. Timur, S.H. Akbas, and T. Ozben The effect of Topotecan on oxidative stress in MCF-7 human breast cancer cell line Acta Biochim. Pol. 52 2005 897 902
49. Y.S. Tor, S.Y. Latifah, J.B. Foo, N. Armania, Y.K. Cheah, R. Abdullah, M.U. Imam, N. Ismail, and M. Ismail Induction of apoptosis through oxidative stress-related pathways in MCF-7, human breast cancer cells, by ethyl acetate extract of Dillenia suffruticosa BMC Complement. Altern. Med. 14 2014 (Article 55, 12 pages)
50. M.J. Tuorkey Curcumin a potent cancer preventive agent: mechanisms of cancer cell killing Interv. Med. Appl. Sci. 6 2014 139 146
51. W.H. Wang, Y.C. Tyan, Z.S. Chen, C.G. Lin, M.H. Yang, S.S. Yuan, and W.C. Tsai Evaluation of the antioxidant activity and antiproliferative effect of the Jaboticaba (Myrciaria cauliflora) seed extracts in oral carcinoma cells BioMed Res. Int. 2014 2014 (Article ID 185946, 7 pages)
52. K.X. Wang, H. Zhang, K.Y. Zheng, J.C. Tian, Y.R. You, K. Sun, and X.F. Fei Cytotoxicity and molecule mechanism of betulinic acid J. Jilin Univ. 47 2009 622 627
53. C. Wiart, S. Mogana, S. Khalifah, M. Mahan, S. Ismail, M. Buckle, A.K. Narayana, and M. Sulaiman Antimicrobial screening of plants used for traditional medicine in the state of Perak, Peninsular Malaysia Fitoterapia 75 2004 68 73
54. G. Wu, Z. Qian, J. Guo, D. Hu, J. Bao, J. Xie, W. Xu, J. Lu, X. Chen, and Y. Wang Ganoderma lucidum extract induces G1 cell cycle arrest, and apoptosis in human breast cancer cells Am. J. Chin. Med. 40 2012 631 642
55. M. Xia, D. Knezevic, and L.T. Vassilev p21 does not protect cancer cells from apoptosis induced by nongenotoxic p53 activation Oncogene 30 2011 346 355
56. D. Xiao, V. Vogel, and S.V. Singh Benzyl isothiocyanate-induced apoptosis in human breast cancer cells is initiated by reactive oxygen species and regulated by Bax and Bak Mol. Cancer Ther. 5 2006 2931 2945
57. V. Yanamadala, H. Negoro, L. Gunaratnam, T. Kong, and B.M. Denker Galpha12 stimulates apoptosis in epithelial cells through JNK1-mediated Bcl-2 degradation and up-regulation of IkappaBalpha J. Biol. Chem. 282 2007 24352 24363
58. J. Yoon, H.S. Yoo, Y.W. Lee, and C.K. Cho An overview of current oriental medicine herbal cancer research in Korea Chin. J. Integr. Med. 17 2011 251 256