Synthetic flavanones augment the anticancer effect of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)

Molecules

Volumn 17, Issue 10, 2012, Pages 11693-11711

  Szliszka, Ewelina ^a   Kostrzewa Susłow, Edyta ^b   Bronikowska, Joanna ^a   Jaworska, Dagmara ^a   Janeczko, Tomasz ^b   Czuba, Zenon P ^a   Krol, Wojciech ^a  

^a MEDICAL UNIVERSITY OF SILESIA   (Poland)

^b WROC AW UNIVERSITY OF ENVIRONMENTAL AND LIFE SCIENCES   (Poland)

Author keywords

6 hydroxyflavanone (6 HF); 6 propionoxyflavanone (6 PF); Apoptosis; Cancer cells; Death receptor; Flavanones; Mitochondrial pathway; TRAIL

Indexed keywords

ANTINEOPLASTIC AGENT; DEATH RECEPTOR; FLAVANONE DERIVATIVE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

APOPTOSIS; ARTICLE; DRUG EFFECT; DRUG POTENTIATION; HELA CELL; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; SIGNAL TRANSDUCTION; SYNTHESIS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; DRUG SYNERGISM; FLAVANONES; HELA CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; RECEPTORS, DEATH DOMAIN; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84868091685     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules171011693     Document Type: Article

References (58)

1. Androutsopoulos, V.P.; Papakyriakou, A.; Vourloumis, D.; Tsatsakis, A.M.; Spandidos, D.A. Dietary flavonoids in cancer therapy and prevention: Substrates and inhibitors of cytochrome P450 CYP1 enzymes. Pharmacol. Ther. 2010, 126, 9-20.
2. Krol, W.; Shani, J.; Czuba, Z.; Scheller, S. Modulation luminol-dependent chemiluminescence of neutrophils by flavones. Z. Naturforsch. C 1992, 47, 889-992.
3. Vanamala, J.; Leonardi, T.; Patil, B.S.; Taddeo, S.S.; Murphy, M.E.; Pike, L.M.; Chapkin, RS.; Lupton, J.R.; Turner, N.D. Suppression of colon carcinogenesis by bioactive compounds in grapefruit. Carcinogenesis 2006, 27, 1257-1265.
4. Turner, N.D.; Paulhill, K.J.; Warren, C.A.; Davidson, L.A.; Chapkin, R.S.; Lupton, J.R.; Carroll, R.J.; Wang, N. Quercetin suppresses early colon carcinogenesis partly through inhibition of inflammatory mediators. Acta Hortic. 2009, 841, 237-242.
5. Warren, C.A.; Paulhill, K.J.; Davidson, L.A.; Lupton, J.R.; Taddeo, S.S.; Hong, M.Y.; Carroll, R.J.; Chapkin, R.S.; Turner, N.D. Quercetin may suppress rat aberrant crypt foci formation by suppressing inflammatory mediators that influence proliferation and apoptosis. J. Nutr. 2009, 139, 101-105.
6. Patil, B.S.; Jayaprakasha, G.K.; Chidambara-Murthy, K.N.; Vikram, A. Bioactive compounds: Historical perspectives, opportunities and challenges. J. Agric. Food Chem. 2009, 57, 8142-8160.
7. Leonardi, T.; Vanamala, J.; Taddeo, S.S.; Davidson, L.A.; Murphy, M.E.; Patil, B.S.; Wang, N.; Carroll, R.J.; Chapkin, R.S.; Lupton, J.R.; et al. Apigenin and naringenin suppress colon carcinogenesis through the aberrant crypt stage in azoxymethane-treated rats. Exp. Biol. Med. 2010, 235, 710-717.
8. Szliszka, E.; Skaba, D.; Czuba, Z.P.; Krol, W. Inhibition of inflammatory mediators by neobavaisoflavone in activated RAW264.7 macrophages. Molecules 2011, 16, 3701-3712.
9. Barros, L.; Duenas, M.; Carvalho, A.M.; Ferreira, I.C.; Santos-Buelga, C. Characterization of phenolic compounds in flowers of wild medicinal plants from Northeastern Portugal. Food Chem. Toxicol. 2012, 50, 1576-1582.
10. Pinela, J.; Barros, L.; Carvalho, A.M.; Ferreira, I.C. Nutritional composition and antioxidant activity of four tomato (Lycopersicon esculentum L.) farmer' varieties in Northeastern Portugal home gardens. Food Chem. Toxicol. 2012, 50, 829-834.
11. Lee, J.Y.; Huerta-Yepez, S.; Vega, M.; Baritaki, S.; Spandidos, D.A.; Bonavida, B. The NO TRAIL to YES TRAIL in cancer therapy. Int. J. Oncol. 2007, 31, 685-691.
12. Holoch, P.A.; Griffith, T.S. TNF-related apoptosis-inducing ligand (TRAIL): A new path to anti-cancer therapies. Eur. J.Pharmacol. 2009, 625, 63-72.
13. Szliszka, E.; Mazur, B.; Zydowicz, G.; Czuba, Z.P.; Krol, W. TRAIL-induced apoptosis and expression of death receptor TRAIL-R1 and TRAIL-R2 in bladder cancer cells. Folia Histochem. Cytobiol. 2009, 47, 579-585.
14. Mellier, G.; Huang, S.; Shenoy, K.; Pervaiz, S. TRAILing death in cancer. Mol. Aspects Med. 2010, 31, 93-112.
15. Russo, M.; Mupo, A.; Spagnuolo, C.; Russo, G.L. Exploring death receptor pathways as selective targets in cancer therapy. Biochem. Pharmacol. 2010, 80, 674-682.
16. Szliszka, E.; Krol, W. The role of dietary polyphenols in tumor necrosis factor-related apoptosis inducing ligand (TRAIL)-induced apoptosis for cancer chemoprevention. Eur. J. Cancer Prev. 2011, 20, 63-69.
17. Szliszka, E.; Czuba, Z.P.; Bronikowska, J.; Mertas, A.; Paradysz, A.; Krol, W. Ethanolic extract of propolis (EEP) augments TRAIL-induced apoptotic death in prostate cancer cells. Evid. Based Complement. Alternat. Med. 2011, 2011, 535172.
18. Szliszka, E.; Zydowicz, G.; Janoszka, B.; Dobosz, C.; Kowalczyk-Ziomek, G.; Krol, W. Ethanolic extract of Brazilian green propolis sensitizes prostate cancer cells to TRAIL-induced apoptosis. Int. J. Oncol. 2011, 38, 941-953.
19. Zhang, L.; Fang, B. Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther. 2005, 12, 228-237.
20. Horinanka, M.; Yoshida, T.; Shiraishi, T.; Nakata, S.; Wakada, M.; Nakanishi, R.; Nishino, H.; Sakai, T. The combination of TRAIL and luteolin enhances apoptosis in human cervival cancer HeLa cells. Biochem. Biophys. Res. Comun. 2005, 333, 833-838.
21. Horinaka, M.; Yoshida, T.; Shiraishi, T.; Nakata, S.; Wakada, M.; Sakai, T. The dietary flavonoid apigenin sensitizes malignant tumor cells to tumor necrosis factor-related apoptosis-inducing ligand. Mol. Cancer Ther. 2006, 5, 945-951.
22. Son, Y.G.; Kim, E.H.; Kim, J.Y.; Kim, S.U.; Kwon, T.K.; Yoon, A.R.; Yun, C.O.; Choi, K.S. Silibinin sensitizes human glioma cells to TRAIL-mediated apoptosis via DR5 upregulation and downregulation of cFLIP and surviving. Cancer Res. 2007, 67, 8274-8284.
23. Chen, W.; Wang, X.; Zhuang, J.; Zhang, L.; Lin, Y. Induction of death receptor 5 and suppression of surviving contribute to sensitization of TRAIL-induced cytotoxicity by quercetin in non-small lung cancer cells. Carcinogenesis 2007, 28, 2114-2121.
24. Kim, J.Y.; Kim, E.H.; Park, S.S.; Lim, J.H.; Kwon, T.K.; Choi, K.S. Quercetin sensitizes human hepatoma cells to TRAIL-induced apoptosis via Sp1-mediated DR5 upregulation and proteasome-mediated c-FLIPS downregulation. J. Cell. Biochem. 2008, 105, 1386-1398.
25. Szliszka, E.; Czuba, Z.P.; Jernas, K.; Krol, W. Dietary flavonoids sensitize HeLa cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). Int. J. Mol. Sci. 2008, 9, 56-64.
26. Yoshida, T.; Konishi, M.; Horinaka, M.; Yasuda, T.; Goda, A.E.; Taniguchi, H.; Yano, K.; Wakada, M.; Sakai, T. Kaempferol sensitizes colon cancer cells to TRAIL-induced apoptosis. Biochem. Biophys. Res. Commun. 2008, 375, 129-133.
27. Tanaguchi, H.; Yoshida, T.; Horinaka, M.; Yasuda, T.; Goda, A.E.; Konishi, M.; Wakada, M.; Kataoka, K.; Yoshikawa, T.; Sakai, T. Baicalein overcomes tumor necrosis factor-related apoptosis-inducing ligand resistance via two different cell specific pathways in cancer cells but not in normal cells. Cancer. Res. 2008, 68, 8918-8927.
28. Jung, Y.H.; Heo, J.; Lee, Y.J.; Kwon, T.K.; Kim, Y.H. Quercetin enhances TRAIL-induced apoptosis in prostate cancer cells via increased protein stability of death receptor 5. Life Sci. 2010, 86, 351-357.
29. Szliszka, E.; Gebka, J.; Bronikowska, J.; Krol, W. Dietary flavones enhance the effect of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) on bladder cancer cells. Cent. Eur. J. Urol. 2010, 63, 138-143.
30. Bronikowska, J.; Szliszka, E.; Czuba, Z.P.; Zwolinski, D.; Szmydki, B.; Krol, W. The combination of TRAIL and isoflavones enhances apoptosis in cancer cells. Molecules 2010, 15, 2000-2015.
31. Szliszka, E.; Czuba, Z.P.; Mazur, B.; Sedek, L.; Paradysz, A.; Krol, W. Chalcones enhance TRAIL-induced apoptosis in prostate cancer cells. Int. J. Mol. Sci. 2010, 11, 1-13.
32. Szliszka, E.; Czuba, Z.P.; Mazur, B.; Paradysz, A.; Krol, W. Chalcones and dihydrochalcones augment TRAIL-mediated apoptosis in prostate cancer cells. Molecules 2010, 15, 5336-5353.
33. Szliszka, E.; Bronikowska, J.; Czuba, Z.P.; Krol, W. Isoflavones augment the effect of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) on prostate cancer cells. Cent. Eur. J. Urol. 2010, 63, 182-186.
34. Szliszka, E.; Helewski, K.J.; Mizgala, E.; Krol, W. The dietary flavonol fisetin enhances the apoptosis-inducing potential of TRAIL in prostate cancer cells. Int. J. Oncol. 2011, 39, 771-779.
35. Szliszka, E.; Krol, W. Soy isoflavones augment the effect of TRAIL-mediated apoptotic death in prostate cancer cells. Oncol. Rep. 2011, 26, 533-541.
36. Jin, C.Y.; Park, C.; Hwang, H.J.; Kim, G.Y.; Choi, B.T.; Kim, W.J.; Choi, Y.H. Naringenin up-regulates the expression of death receptor 5 and enhances TRAIL-induced apoptosis in human lung cancer A549 cells. Mol. Nutr. Food Res. 2011, 55, 300-309.
37. Szliszka, E.; Czuba, Z.P.; Mertas, A.; Paradysz, A.; Krol, W. The dietary isoflavone biochanin-A sensitizes prostate cancer cells to TRAIL-induced apoptosis. Urol. Oncol. 2011, doi:10.1016/j.urolonc.2011.01.019.
38. Wudtiwai, B.; Sripanidkulchai, B.; Kongtawelert, P.; Banjerdpongchai, R. Metoxyflavone derivatives modulates the effect of TRAIL-induced apoptosis in human leukemic cell lines. J. Hematol. Oncol. 2011, 4, 52-63.
39. Ding, J.; Polier, G.; Köhler, R.; Giaisi, M.; Krammer, P.H.; Li-Weber, M. Wogonin and related natural flavones overcome tumor necrosis factor-related apoptosis inducing ligand (TRAIL) protein resistance of tumors by down-regulation of c-FLIP protein and up-regulation of TRAIL receptor 2 expression. J. Biol. Chem. 2012, 287, 641-649.
40. Graf, B.A.; Milbury, P.E.; Blumberg, J.B. Flavonols, flavones and flavanones, and human health: Epidemiological evidence. J. Med. Food 2005, 8, 281-290.
41. Park, J.H.; Jin, C.Y.; Lee, B.K.; Kim, G.Y.; Choi, Y.H.; Jeong, Y.K. Naringenin induces apoptosis through downregulation of Akt and caspase-3 activation in human leukemia THP-1 cells. Food Chem. Toxicol. 2008, 46, 3684-3690.
42. Jin, C.Y.; Park, C.; Lee, J.H.; Chung, K.T.; Kwon, T.K.; Kim, G.Y.; Choi, B.T.; Choi, Y.H. Naringenin-induced apoptosis is attenuated by Bcl-2 but restored by small molecule Bcl-2 inhibitor, HA 14-1 in human leukemia U977 cells. Toxicol. In Vitro 2009, 23, 259-265.
43. Park, H.J.; Kim, M.J.; Ha, E.; Chung, J.H. Apoptotic effect of hesperidin through caspase-3 activation in human colon cells SNU-C4. Phytomedicine 2008, 15, 147-151.
44. Ghorbani, A.; Nazari, M.; Jeddi-Tehrani, M.; Zang, H. The citrus flavonoid hesperidin induces p53 and inhibits NF-κB activation in order to trigger apoptosis in NALM-6 cells: Involvement of PPARγ-dependent mechanism. Eur. J. Nutr. 2012, 51, 39-46.
45. Zhang, S.; Zhou, Y.; Liu, Y.; Cai, Y. Effect of liquiritigenin, a flavone existed from Radix glycyrrhizae on pro-apoptotic in SMMC-7721 cells. Food Chem. Toxicol. 2009, 47, 693-701.
46. Liu, C.; Wang, Y.; Xie, S.; Zhou, Y.; Ren, X.; Li, X.; Cai, Y. Liquiritigenin induces mitochondria-mediated apoptosis via cytochrome c release and caspases activation in HeLa cells. Phytother. Res. 2011, 25, 277-283.
47. Ko, C.H.; Shen, S.; Chen, Y. Hydroxylation at C4' or C6 is essential for apoptosis-inducing activity of flavanone through activation of the casapase-3 cascade and production of reactive oxygen species. Free Radic. Biol. Med. 2004, 36, 897-910.
48. Szliszka, Ewelina. Medical University of Silesia, Katowice, ON. Unpublished work, 2012.
49. Bronikowska, J.; Szliszka, E.; Jaworska, D.; Czuba, Z.P.; Krol, W. The coumarin psoralidin enhances anticancer effect of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). Molecules 2012, 17, 6449-6464.
50. Jacquemin, G.; Granci, V.; Gallouet, A.S.; Lalaoui, N.; Morle, A.; Iessi, E.; Morizot, A.; Garrido, C.; Guillaudeux, T.; Micheau, O. Quercetin-mediated Mcl-1 and surviving downregulation restores TRAIL-induced apoptosis in non-Hodgkin's lymphoma B cells. Haematologica 2012, 97, 38-46.
51. Kostrzewa-Susłow, E.; Dmochowska-Gładysz, J.; Białonska, A.; Ciunik, Z.; Rymowicz, W. Microbial transformations of flavanone and 6-hydroxyflavanone by Aspergillus niger strains. J. Mol. Catal. B Enzym. 2006, 39, 18-23.
52. Kostrzewa-Susłow, E.; Białonska, A.; Janeczko, T. 4-Oxo-2-phenylchroman-6-yl propionate. Acta Cryst. 2010, E66, o1401, doi: 10.1107/S1600536810012298.
53. Szliszka, E.; Majcher, A.; Domino, M.; Pietsz, G.; Krol, W. Cytotoxic activity of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) against bladder cancer cells after using chemotherapeutic drugs. Urol. Pol. 2007, 60, 138-142.
54. Szliszka, E.; Bronikowska, J.; Majcher, A.; Miszkiewicz, J.; Krol, W. Enhanced sensitivity of hormone-refractory prostate cancer cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) mediated cytotoxicity by taxanes. Cent. Eur. J. Urol. 2009, 62, 29-34.
55. Szliszka, E.; Czuba, ZP.; Domino, M.; Mazur, B.; Zydowicz, G.; Krol, W. Ethanolic extract of propolis (EEP) enhances the apoptosis-inducing potential of TRAIL in cancer cells. Molecules 2009, 14, 738-754.
56. Szliszka, E.; Czuba, Z.P.; Sedek, L.; Paradysz, A.; Krol, W. Enhanced TRAIL-mediated apoptosis in prostate cancer cells by the bioactive compounds neobavaisoflavone and psoralidin isolated from Psoralea corylifolia. Pharmacol. Rep. 2011, 63, 139-148.
57. Szliszka, E.; Czuba, Z.P.; Kawczyk-Krupka, A.; Sieron-Stoltny, A.; Sieron, A.; Krol, W. Chlorin-based photodynamic therapy enhances the effect of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) in bladder cancer cells. Med. Sci. Monit. 2012, 18, BR47-53.
58. Szliszka, E.; Zydowicz, G.; Mizgala, E.; Krol, W. Artepillin C (3, 5-diprenyl-4-hydroxycinnamic acid) sensitizes prostate cancer LNCaP cells to TRAIL-induced apoptosis. Int. J. Oncol. 2012, 41, 818-828.