Triphala Extract Suppresses Proliferation and Induces Apoptosis in Human Colon Cancer Stem Cells via Suppressing c-Myc/Cyclin D1 and Elevation of Bax/Bcl-2 Ratio

BioMed Research International

Volumn 2015, Issue , 2015, Pages

  Vadde, Ramakrishna ^a,b   Radhakrishnan, Sridhar ^a   Reddivari, Lavanya ^a   Vanamala, Jairam K P ^a,c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b YOGI VEMANA UNIVERSITY   (India)

^c PENN STATE CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETONE; ALCOHOL; ANTIMITOTIC AGENT; ANTIOXIDANT; APOPTOSIS INDUCING FACTOR; AURANTIIN; AYURVEDIC DRUG; CYCLIN D1; FLUOROURACIL; HERBACEOUS AGENT; HEXANE; ISOORIENTIN; ISORHAMNETIN; METHANOL; MYC PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHENOL DERIVATIVE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; QUERCETIN; TRIPHALA CHURNA; UNCLASSIFIED DRUG; WATER; ONCOPROTEIN; PLANT EXTRACT; TRIPHALA;

ANALYTICAL PARAMETERS; ANTIOXIDANT ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AYURVEDA; BAX BCL 2 RATIO; CANCER STEM CELL; CELL PROLIFERATION; CELL RENEWAL; CELLS BY BODY ANATOMY; COLON; COLON CANCER STEM CELL; COLONY FORMATION; CONTROLLED STUDY; DRUG EFFICACY; ETHNOPHARMACOLOGY; HCT116 CELL LINE; HERBAL MEDICINE; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; PHYTOCHEMISTRY; PROTEIN CLEAVAGE; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; COLON TUMOR; DRUG EFFECTS; METABOLISM; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; HUMANS; NEOPLASTIC STEM CELLS; PLANT EXTRACTS; PROTO-ONCOGENE PROTEINS;

EID: 84934344062     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2015/649263     Document Type: Article

References (59)

1. R. Siegel, C. Desantis, and A. Jemal, "Colorectal cancer statistics, 2014", CA Cancer Journal for Clinicians, vol. 64, no. 2, pp. 104-117, 2014.
2. D. L. Worthley, V. L. Whitehall, K. J. Spring, and B. A. Leggett, "Colorectal carcinogenesis: road maps to cancer", World Journal of Gastroenterology, vol. 13, no. 28, pp. 3784-3791, 2007.
3. S. D. Markowitz and M. M. Bertagnolli, "Molecular origins of cancer: molecular basis of colorectal cancer", The New England Journal of Medicine, vol. 361, no. 25, pp. 2449-2460, 2009.
4. A. Bedeir and A. M. Krasinskas, "Molecular diagnostics of colorectal cancer", Archives of Pathology and Laboratory Medicine, vol. 135, no. 5, pp. 578-587, 2011.
5. X. Sui, N. Kong, X. Wang et al., "JNK confers 5-fluorouracil resistance in p53-deficient and mutant p53-expressing colon cancer cells by inducing survival autophagy", Scientific Reports, vol. 4, article 4694, 8 pages, 2014.
6. J. P. Medema, "Cancer stem cells: the challenges ahead", Nature Cell Biology, vol. 15, no. 4, pp. 338-344, 2013.
7. N. Bitarte, E. Bandres, V. Boni et al., "MicroRNA-451 is involved in the self-renewal, tumorigenicity, and chemoresistance of colorectal cancer stem cells", Stem Cells, vol. 29, no. 11, pp. 1661-1671, 2011.
8. M. Todaro, M. G. Francipane, J. P. Medema, and G. Stassi, "Colon cancer stem cells: promise of targeted therapy", Gastroenterology, vol. 138, no. 6, pp. 2151-2162, 2010.
9. M. Zhang and J. M. Rosen, "Stem cells in the etiology and treatment of cancer", Current Opinion in Genetics and Development, vol. 16, no. 1, pp. 60-64, 2006.
10. J. N. Anastas and R. T. Moon, "WNT signalling pathways as therapeutic targets in cancer", Nature Reviews Cancer, vol. 13, no. 1, pp. 11-26, 2013.
11. D. J. Liao, A. Thakur, J. Wu, H. Biliran, and F. H. Sarkar, "Perspectives on c-myc, cyclin D1, and their interaction in cancer formation, progression, and response to chemotherapy", Critical Reviews in Oncogenesis, vol. 13, no. 2, pp. 93-158, 2007.
12. J. Wang, H. Wang, Z. Li et al., "c-Myc is required for maintenance of glioma cancer stem cells", PLoS ONE, vol. 3, no. 11, Article ID e3769, 2008.
13. B. Hoffman and D. A. Liebermann, "Apoptotic signaling by cmyc", Oncogene, vol. 27, no. 50, pp. 6462-6472, 2008.
14. B. J. Chen, Y. L. Wu, Y. Tanaka, and W. Zhang, "Smallmolecules targeting c-Myc oncogene: promising anti-cancer therapeutics", International Journal of Biological Sciences, vol. 10, no. 10, pp. 1084-1096, 2014.
15. Y.-H. Deng, X.-X. Pu, M.-J. Huang et al., "5-Fluorouracil upregulates the activity of Wnt signaling pathway in CD133-positive colon cancer stem-like cells", Chinese Journal of Cancer, vol. 29, no. 9, pp. 810-815, 2010.
16. D. P. Jones, Y. Park, and T. R. Ziegler, "Nutritional metabolomics: progress in addressing complexity in diet and health", Annual Review of Nutrition, vol. 32, pp. 183-202, 2012.
17. M. Kasdagly, S. Radhakrishnan, L. Reddivari, D. R. Veeramachaneni, and J. Vanamala, "Colon carcinogenesis: influence of Western diet-induced obesity and targeting stem cells using dietary bioactive compounds", Nutrition, vol. 30, no. 11-12, pp. 1242-1256, 2014.
18. L. Reddivari, J. Vanamala, S. Chintharlapalli, S. H. Safe, and J. C. Miller Jr., "Anthocyanin fraction from potato extracts is cytotoxic to prostate cancer cells through activation of caspasedependent and caspase-independent pathways", Carcinogenesis, vol. 28, no. 10, pp. 2227-2235, 2007.
19. J. Vanamala, L. Reddivari, S. Radhakrishnan, and C. Tarver, "Resveratrol suppresses IGF-1 induced human colon cancer cell proliferation and elevates apoptosis via suppression of IGF-1R/Wnt and activation of p53 signaling pathways", BMC Cancer, vol. 10, article 238, 2010.
20. J. Vanamala, S. Radhakrishnan, L. Reddivari, V. B. Bhat, and A. Ptitsyn, "Resveratrol suppresses human colon cancer cell proliferation and induces apoptosis via targeting the pentose phosphate and the talin-FAK signaling pathways-a proteomic approach", Proteome Science, vol. 9, article 49, 2011.
21. S. Radhakrishnan, L. Reddivari, R. Sclafani, U. N. Das, and J. Vanamala, "Resveratrol potentiates grape seed extract induced human colon cancer cell apoptosis", Frontiers in Bioscience, vol. 3, no. 4, pp. 1509-1523, 2011.
22. G. P. Madiwale, L. Reddivari, M. Stone, D. G. Holm, and J. Vanamala, "Combined effects of storage and processing on the bioactive compounds and pro-apoptotic properties of color-fleshed potatoes in human colon cancer cells", Journal of Agricultural and Food Chemistry, vol. 60, no. 44, pp. 11088-11096, 2012.
23. G. Deep, M. Dhiman, A. R. Rao, and R. K. Kale, "Chemopreventive potential of Triphala (a composite Indian drug) on benzo (a) pyrene induced forestomach tumorigenesis in murine tumor model system", Journal of Experimental and Clinical Cancer Research, vol. 24, no. 4, pp. 555-563, 2005.
24. D. P. Singh, R. Govindarajan, and A. K. S. Rawat, "Highperformance liquid chromatography as a tool for the chemical standardisation of Triphala-an ayurvedic formulation", Phytochemical Analysis, vol. 19, no. 2, pp. 164-168, 2008.
25. M. S. Baliga, "Triphala, Ayurvedic formulation for treating and preventing cancer: a review", Journal of Alternative and Complementary Medicine, vol. 16, no. 12, pp. 1301-1308, 2010.
26. T. Sandhya, K. M. Lathika, B. N. Pandey, and K. P. Mishra, "Potential of traditional ayurvedic formulation, Triphala, as a novel anticancer drug", Cancer Letters, vol. 231, no. 2, pp. 206-214, 2006.
27. Y. Shi, R. P. Sahu, and S. K. Srivastava, "Triphala inhibits both in vitro and in vivo xenograft growth of pancreatic tumor cells by inducing apoptosis", BMC Cancer, vol. 8, article 294, 2008.
28. V. L. Singleton, R. Orthofer, and R. M. Lamuela-Raventós, "Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent", Methods in Enzymology, vol. 299, pp. 152-178, 1998.
29. G. P. Madiwale, L. Reddivari, D. G. Holm, and J. Vanamala, "Storage elevates phenolic content and antioxidant activity but suppresses antiproliferative and pro-apoptotic properties of colored-flesh potatoes against human colon cancer cell lines", Journal of Agricultural and Food Chemistry, vol. 59, no. 15, pp. 8155-8166, 2011.
30. J. M. Awika, L. W. Rooney, X. Wu, R. L. Prior, and L. Cisneros-Zevallos, "Screeningmethods to measure antioxidant activity of sorghum (Sorghum bicolor) and sorghum products", Journal of Agricultural and Food Chemistry, vol. 51, no. 23, pp. 6657-6662, 2003.
31. L. Reddivari, A. L. Hale, and J. C. Miller Jr., "Determination of phenolic content, composition and their contribution to antioxidant activity in specialty potato selections", American Journal of Potato Research, vol. 84, no. 4, pp. 275-282, 2007.
32. C. D. Broeckling, A. L. Heuberger, J. A. Prince, E. Ingelsson, and J. E. Prenni, "Assigning precursor-product ion relationships in indiscriminant MS/MS data from non-targeted metabolite profiling studies", Metabolomics, vol. 9, no. 1, pp. 33-43, 2013.
33. L. W. Sumner, A. Amberg, D. Barrett et al., "Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI)", Metabolomics, vol. 3, no. 3, pp. 211-221, 2007.
34. A. R. Massey, L. Reddivari, and J. Vanamala, "The dermal layer of sweet sorghum (Sorghum bicolor) stalk, a byproduct of biofuel production and source of unique 3-deoxyanthocyanidins, has more antiproliferative and proapoptotic activity than the pith in p53 variants of HCT116 and colon cancer stem cells", Journal of Agricultural and Food Chemistry, vol. 62, no. 14, pp. 3150-3159, 2014.
35. S. Ottinger, A. Klöppel, V. Rausch et al., "Targeting of pancreatic and prostate cancer stem cell characteristics by Crambe crambe marine sponge extract", International Journal of Cancer, vol. 130, no. 7, pp. 1671-1681, 2012.
36. A. Apel, I. Herr, H. Schwarz, H. P. Rodemann, and A. Mayer, "Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy", Cancer Research, vol. 68, no. 5, pp. 1485-1494, 2008.
37. R. G. Mehta, G. Murillo, R. Naithani, and X. Peng, "Cancer chemoprevention by natural products: how far have we come?" Pharmaceutical Research, vol. 27, no. 6, pp. 950-961, 2010.
38. B. Patwardhan and R. A. Mashelkar, "Traditional medicineinspired approaches to drug discovery: can Ayurveda show the way forward?" Drug Discovery Today, vol. 14, no. 15-16, pp. 804-811, 2009.
39. J. Vanamala, G. Cobb, N. D. Turner et al., "Bioactive compounds of grapefruit (Citrus paradisi cv. rio red) respond differently to postharvest irradiation, storage, and freeze drying", Journal of Agricultural and Food Chemistry, vol. 53, no. 10, pp. 3980-3985, 2005.
40. J. Vanamala, T. Leonardi, B. S. Patil et al., "Suppression of colon carcinogenesis by bioactive compounds in grapefruit", Carcinogenesis, vol. 27, no. 6, pp. 1257-1265, 2006.
41. J. Vanamala, C. C. Tarver, and P. S. Murano, "Obesity-enhanced colon cancer: functional food compounds and their mechanisms of action", Current Cancer Drug Targets, vol. 8, no. 7, pp. 611-633, 2008.
42. 3", Carcinogenesis, vol. 29, no. 4, pp. 790-796, 2008.
43. J. Vanamala, S. Radhakrishnan, L. Reddivari, and A. Massey, "Anthocyanins as apoptotic regulators", in Novel Apoptotic Regulators in Carcinogenesis, G. G. Chen and P. B. S. Lai, Eds., pp. 93-122, Springer Science+Business Media, Dordrecht, The Netherlands, 2012.
44. D. Brenner and T. W. Mak, "Mitochondrial cell death effectors", Current Opinion in Cell Biology, vol. 21, no. 6, pp. 871-877, 2009.
45. M. S. Ola, M. Nawaz, and H. Ahsan, "Role of Bcl-2 family proteins and caspases in the regulation of apoptosis", Molecular and Cellular Biochemistry, vol. 351, no. 1-2, pp. 41-58, 2011.
46. S. Elmore, "Apoptosis: a review of programmed cell death", Toxicologic Pathology, vol. 35, no. 4, pp. 495-516, 2007.
47. G. Li, T. Li, Y. Li et al., "Ulinastatin inhibits oxidant-induced endothelial hyperpermeability and apoptotic signaling", International Journal of Clinical and Experimental Pathology, vol. 7, no. 14, pp. 7342-7350, 2014.
48. K. H. Vousden and C. Prives, "Blinded by the light: the growing complexity of p53", Cell, vol. 137, no. 3, pp. 413-431, 2009.
49. S. Haupt, M. Berger, Z. Goldberg, and Y. Haupt, "Apoptosis-the p53 network", Journal of Cell Science, vol. 116, no. 20, pp. 4077-4085, 2003.
50. Y. Yu, S. S. Kanwar, B. B. Patel, J. Nautiyal, F. H. Sarkar, and A. P. N. Majumdar, "Elimination of colon cancer stem-like cells by the combination of curcumin and FOLFOX", Translational Oncology, vol. 2, no. 4, pp. 321-328, 2009.
51. Z. Niu, H. Liu, M. Zhou et al., "Knockdown of c-Myc inhibits cell proliferation by negatively regulating the Cdk/Rb/E2F pathway in nasopharyngeal carcinoma cells", Acta Biochimica et Biophysica Sinica, vol. 47, no. 3, pp. 183-191, 2015.
52. H. Li, B. Yang, J. Huang et al., "Naringin inhibits growth potential of human triple-negative breast cancer cells by targeting β-catenin signaling pathway", Toxicology Letters, vol. 220, no. 3, pp. 219-228, 2013.
53. D.-I. Kim, S.-J. Lee, S.-B. Lee, K. Park, W.-J. Kim, and S.-K. Moon, "Requirement for Ras/Raf/ERK pathway in naringininduced G1-cell-cycle arrest via p21WAF1 expression", Carcinogenesis, vol. 29, no. 9, pp. 1701-1709, 2008.
54. E.-J. Lee, G.-S. Moon, W.-S. Choi, W.-J. Kim, and S.-K. Moon, "Naringin-induced p21WAF1-mediated G1-phase cell cycle arrest via activation of the Ras/Raf/ERK signaling pathway in vascular smoothmuscle cells", Food and Chemical Toxicology, vol. 46, no. 12, pp. 3800-3807, 2008.
55. T. Leonardi, J. Vanamala, S. S. Taddeo et al., "Apigenin and naringenin suppress colon carcinogenesis through the aberrant crypt stage in azoxymethane-treated rats", Experimental Biology and Medicine, vol. 235, no. 6, pp. 710-717, 2010.
56. N. G. Amado, D. Predes, M. M. Moreno, I. O. Carvalho, F. A. Mendes, and J. G. Abreu, "Flavonoids and Wnt/β-catenin signaling: potential role in colorectal cancer therapies", International Journal of Molecular Sciences, vol. 15, no. 7, pp. 12094-12106, 2014.
57. D. Amendola, M. De Salvo, R. Marchese et al., "Myc downregulation affects cyclin D1/cdk4 activity and induces apoptosis via Smac/Diablo pathway in an astrocytoma cell line", Cell Proliferation, vol. 42, no. 1, pp. 94-109, 2009.
58. R. H. Liu, "Potential synergy of phytochemicals in cancer prevention: mechanism of action", Journal of Nutrition, vol. 134, supplement 12, pp. 3479S-3485S, 2004.
59. T. M. De Kok, S. G. Van Breda, and M. M. Manson, "Mechanisms of combined action of different chemopreventive dietary compounds: a review", European Journal of Nutrition, vol. 47, no. 2, supplement, pp. 51-59, 2008.