Bilberry extract (Antho 50) selectively induces redox-sensitive caspase 3-related apoptosis in chronic lymphocytic leukemia cells by targeting the Bcl-2/Bad pathway

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Alhosin, Mahmoud ^a   León González, Antonio J ^a   Dandache, Israa ^a   Lelay, Agnès ^a,b   Rashid, Sherzad K ^a   Kevers, Claire ^c   Pincemail, Joël ^d   Fornecker, Luc Matthieu ^a,b   Mauvieux, Laurent ^a,b   Herbrecht, Raoul ^a,b   Schini Kerth, Valérie B ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d CREDEC   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHOCYANIN; APOPTOSIS REGULATORY PROTEIN; CASPASE 3; DELPHINIDIN 3-O-GLUCOPYRANOSIDE; GLUCOSIDE; PLANT EXTRACT; PROTEIN BAD; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE;

ADULT; AGED; APOPTOSIS; BILBERRY; CHEMISTRY; CHRONIC LYMPHATIC LEUKEMIA; DRUG EFFECTS; FEMALE; HUMAN; MALE; METABOLISM; MIDDLE AGED; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTHOCYANINS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-ASSOCIATED DEATH PROTEIN; CASPASE 3; CELL LINE, TUMOR; FEMALE; GLUCOSIDES; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MIDDLE AGED; OXIDATION-REDUCTION; PHOSPHORYLATION; PLANT EXTRACTS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; VACCINIUM MYRTILLUS;

EID: 84924908487     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08996     Document Type: Article

References (47)

1. Schena, M. et al. The role of Bcl-2 in the pathogenesis of B chronic lymphocytic leukemia. Leukemia & lymphoma 11, 173-179, doi:10.3109/10428199309086993 (1993).
2. Hanada, M., Delia, D., Aiello, A., Stadtmauer, E. & Reed, J. C. bcl-2 gene hypomethylation and high-level expression in B-cell chronic lymphocytic leukemia. Blood 82, 1820-1828 (1993).
3. Cimmino, A. et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proceedings of the National Academy of Sciences of the United States of America 102, 13944-13949, doi:10.1073/pnas.0506654102 (2005).
4. Scarfo, L. & Ghia, P. Reprogramming cell death: BCL2 family inhibition in hematological malignancies. Immunology letters 155, 36-39, doi:10.1016/j.imlet.2013.09.015 (2013).
5. Wu, M., Akinleye, A. & Zhu, X. Novel agents for chronic lymphocytic leukemia. Journal of hematology & oncology 6, 36, doi:10.1186/1756-8722-6-36 (2013).
6. Mouria, M. et al. Food-derived polyphenols inhibit pancreatic cancer growth through mitochondrial cytochrome C release and apoptosis. International journal of cancer. Journal international du cancer 98, 761-769 (2002).
7. Mertens-Talcott, S. U. & Percival, S. S. Ellagic acid and quercetin interact synergistically with resveratrol in the induction of apoptosis and cause transient cell cycle arrest in human leukemia cells. Cancer letters 218, 141-151, doi:10.1016/j.canlet.2004.06.007 (2005).
8. Lee, Y. K. et al. VEGF receptor phosphorylation status and apoptosis is modulated by a green tea component, epigallocatechin-3-gallate (EGCG), in B-cell chronic lymphocytic leukemia. Blood 104, 788-794, doi:10.1182/blood-2003-08-2763 (2004).
9. Quiney, C. et al. Flavones and polyphenols inhibit the NO pathway during apoptosis of leukemia B-cells. Leukemia research 28, 851-861, doi:10.1016/j.leukres.2003.12.003 (2004).
10. Mauray, A. et al. Atheroprotective effects of bilberry extracts in apo E-deficient mice. Journal of agricultural and food chemistry 57, 11106-11111, doi:10.1021/jf9035468 (2009).
11. Cai, H. et al. Determination of anthocyanins in the urine of patients with colorectal liver metastases after administration of bilberry extract. Biomedical chromatography: BMC 25, 660-663, doi:10.1002/bmc.1499 (2011).
12. Nyman, N. A. & Kumpulainen, J. T. Determination of anthocyanidins in berries and red wine by high-performance liquid chromatography. Journal of agricultural and food chemistry 49, 4183-4187 (2001).
13. Talavera, S. et al. Anthocyanins are efficiently absorbed from the stomach in anesthetized rats. The Journal of nutrition 133, 4178-4182 (2003).
14. Tabart, J., Kevers, C., Pincemail, J., Defraigne, J. O. & Dommes, J. Evaluation of spectrophotometric methods for antioxidant compoundmeasurement in relation to total antioxidant capacity in beverages. Food chemistry 120, 607-614, doi:DOI 10.1016/j.foodchem.2009.10.031 (2010).
15. Tabart, J., Kevers, C., Evers, D. & Dommes, J. Ascorbic acid, phenolic acid, flavonoid, and carotenoid profiles of selected extracts from Ribes nigrum. Journal of agricultural and food chemistry 59, 4763-4770, doi:10.1021/jf104445c (2011).
16. Gonzalez-Rodriguez, J., Perez-Juan, P. & Luque de Castro, M. D. Method for the simultaneous determination of total polyphenol and anthocyan indexes in red wines using a flow injection approach. Talanta 56, 53-59 (2002).
17. Gokbulut, A. A., Apohan, E. & Baran, Y. Resveratrol and quercetin-induced apoptosis of human 232B4 chronic lymphocytic leukemia cells by activation of caspase-3 and cell cycle arrest. Hematology 18, 144-150, doi:10.1179/1607845412Y.0000000042 (2013).
18. Achour, M. et al. Epigallocatechin-3-gallate up-regulates tumor suppressor gene expression via a reactive oxygen species-dependent down-regulation of UHRF1. Biochemical and biophysical research communications 430, 208-212, doi:10.1016/j.bbrc.2012.11.087 (2013).
19. Sharif, T. et al. Aronia melanocarpa juice induces a redox-sensitive p73-related caspase 3-dependent apoptosis in human leukemia cells. PloS one 7, e32526, doi:10.1371/journal.pone.0032526 (2012).
20. Pan, M. H. et al. Induction of apoptosis by the oolong tea polyphenol theasinensin A through cytochrome c release and activation of caspase-9 and caspase-3 in human U937 cells. Journal of agricultural and food chemistry 48, 6337-6346 (2000).
21. Achour, M. et al. The interaction of the SRA domain of ICBP90 with a novel domain of DNMT1 is involved in the regulation of VEGF gene expression. Oncogene 27, 2187-2197 (2008).
22. Jin, W. et al. UHRF1 is associated with epigenetic silencing of BRCA1 in sporadic breast cancer. Breast cancer research and treatment 123, 359-373, doi:10.1007/s10549-009-0652-2 (2010).
23. Daskalos, A. et al. UHRF1-mediated tumor suppressor gene inactivation in nonsmall cell lung cancer. Cancer 117, 1027-1037, doi:10.1002/cncr.25531 (2011).
24. Wang, F. et al. UHRF1 promotes cell growth and metastasis through repression of p16(ink(4)a) in colorectal cancer. Annals of surgical oncology 19, 2753-2762, doi:10.1245/s10434-011-2194-1 (2012).
25. Tien, A. L. et al. UHRF1 depletion causes a G2/M arrest, activation of DNA damage response and apoptosis. The Biochemical journal 435, 175-185, doi:10.1042/BJ20100840 (2011).
26. Li, X. L., Xu, J. H., Nie, J. H. & Fan, S. J. Exogenous expression of UHRF1 promotes proliferation and metastasis of breast cancer cells. Oncology reports 28, 375-383, doi:10.3892/or.2012.1792 (2012).
27. Czabotar, P. E., Lessene, G., Strasser, A. & Adams, J. M. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nature reviews. Molecular cell biology 15, 49-63, doi:10.1038/nrm3722 (2014).
28. Balakrishnan, K. & Gandhi, V. Bcl-2 antagonists: a proof of concept for CLL therapy. Investigational new drugs 31, 1384-1394, doi:10.1007/s10637-013-0002-4 (2013).
29. Hussain, A. R. et al. Apigenin induces apoptosis via downregulation of S-phase kinase-associated protein 2-mediated induction of p27Kip1 in primary effusion lymphoma cells. Cell proliferation 43, 170-183, doi:10.1111/j.1365-2184.2009.00662.x (2010).
30. Datta, S. R. et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91, 231-241 (1997).
31. Lucas, D. M. et al. The histone deacetylase inhibitor MS-275 induces caspase-dependent apoptosis in B-cell chronic lymphocytic leukemia cells. Leukemia 18, 1207-1214, doi:10.1038/sj.leu.2403388 (2004).
32. Sharif, T. et al. Red wine polyphenols cause growth inhibition and apoptosis in acute lymphoblastic leukaemia cells by inducing a redox-sensitive up-regulation of p73 and down-regulation of UHRF1. European journal of cancer 46, 983-994, doi:10.1016/j.ejca.2009.12.029 (2010).
33. Ghia, P., Ferreri, A. M. & Caligaris-Cappio, F. Chronic lymphocytic leukemia. Critical reviews in oncology/hematology 64, 234-246, doi:10.1016/j.critrevonc.2007.04.008 (2007).
34. Forester, S. C., Choy, Y. Y., Waterhouse, A. L. & Oteiza, P. I. The anthocyanin metabolites gallic acid, 3-O-methylgallic acid, and 2,4,6-trihydroxybenzaldehyde decrease human colon cancer cell viability by regulating pro-oncogenic signals. Molecular carcinogenesis doi:10.1002/mc.21974 (2012).
35. Hsu, C. P., Shih, Y. T., Lin, B. R., Chiu, C. F. & Lin, C. C. Inhibitory effect and mechanisms of an anthocyanins- and anthocyanidins-rich extract from purple-shoot tea on colorectal carcinoma cell proliferation. Journal of agricultural and food chemistry 60, 3686-3692, doi:10.1021/jf204619n (2012).
36. Yun, J. M., Afaq, F., Khan, N. & Mukhtar, H. Delphinidin, an anthocyanidin in pigmented fruits and vegetables, induces apoptosis and cell cycle arrest in human colon cancer HCT116 cells. Molecular carcinogenesis 48, 260-270, doi:10.1002/mc.20477 (2009).
37. Hou, D. X., Tong, X., Terahara, N., Luo, D. & Fujii, M. Delphinidin 3-sambubioside, a Hibiscus anthocyanin, induces apoptosis in human leukemia cells through reactive oxygen species-mediated mitochondrial pathway. Archives of biochemistry and biophysics 440, 101-109, doi:10.1016/j.abb.2005.06.002 (2005).
38. Cheng, E. H. et al. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Molecular cell 8, 705-711 (2001).
39. Pesakhov, S., Khanin, M., Studzinski, G. P. & Danilenko, M. Distinct combinatorial effects of the plant polyphenols curcumin, carnosic acid, and silibinin on proliferation and apoptosis in acute myeloid leukemia cells. Nutrition and cancer 62, 811-824, doi:10.1080/01635581003693082 (2010).
40. Alhosin, M. et al. Down-regulation of UHRF1, associated with re-expression of tumor suppressor genes, is a common feature of natural compounds exhibiting anti-cancer properties. Journal of experimental & clinical cancer research: CR 30, 41, doi:10.1186/1756-9966-30-41 (2011).
41. Bouzar, A. B. et al. Valproate synergizes with purine nucleoside analogues to induce apoptosis of B-chronic lymphocytic leukaemia cells. British journal of haematology 144, 41-52, doi:10.1111/j.1365-2141.2008.07426.x (2009).
42. Unoki, M. Current and potential anticancer drugs targeting members of the UHRF1 complex including epigenetic modifiers. Recent patents on anti-cancer drug discovery 6, 116-130 (2011).
43. Cvorovic, J. et al. Oxidative stress-based cytotoxicity of delphinidin and cyanidin in colon cancer cells. Archives of biochemistry and biophysics 501, 151-157, doi:10.1016/j.abb.2010.05.019 (2010).
44. Feng, R. et al. Cyanidin-3-rutinoside, a natural polyphenol antioxidant, selectively kills leukemic cells by induction of oxidative stress. The Journal of biological chemistry 282, 13468-13476, doi:10.1074/jbc.M610616200 (2007).
45. Katsube, N., Iwashita, K., Tsushida, T., Yamaki, K. & Kobori, M. Induction of apoptosis in cancer cells by Bilberry (Vaccinium myrtillus) and the anthocyanins. Journal of agricultural and food chemistry 51, 68-75, doi:10.1021/jf025781x (2003).
46. Seeram, N. P., Adams, L. S., Hardy, M. L. & Heber, D. Total cranberry extract versus its phytochemical constituents: antiproliferative and synergistic effects against human tumor cell lines. Journal of agricultural and food chemistry 52, 2512-2517, doi:10.1021/jf0352778 (2004).
47. Al-Salahi, O. S. et al. Anti-tumor activity of Eurycoma longifolia root extracts against K-562 cell line: in vitro and in vivo study. PLoS ONE 9, e83818, doi:10.1371/journal.pone.0083818 (2014).