Flavonoids from each of the six structural groups reactivate BRM, a possible cofactor for the anticancer effects of flavonoids

Carcinogenesis

Volumn 35, Issue 10, 2014, Pages 2183-2193

  Kahali, Bhaskar ^a   Marquez, Stefanie B ^a   Thompson, Kenneth W ^a   Yu, Jinlong ^a   Gramling, Sarah J B ^a   Lu, Li ^b   Aponick, Aaron ^c   Reisman, David ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BRM PROTEIN; DELPHINIDIN; DIOSMIN; EPIGALLOCATECHIN GALLATE; FLAVONOID; GENISTEIN; HESPERIDIN; HISTONE DEACETYLASE 9; LUTEOLIN; MESSENGER RNA; QUERCETIN; RETINOBLASTOMA PROTEIN; RUTOSIDE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR GATA 3; MOLECULAR LIBRARY; SMALL INTERFERING RNA; SMARCA2 PROTEIN, HUMAN; SMARCA2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL LINE; CANCER INHIBITION; CONTROLLED STUDY; DEACETYLATION; DRUG EFFECT; DRUG MECHANISM; DRUG STRUCTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUNG ADENOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINOBLASTOMA; STRUCTURE ACTIVITY RELATION; ACETYLATION; ANIMAL; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; GENETICS; METABOLISM; MOLECULAR LIBRARY; MOLECULARLY TARGETED THERAPY; MUTANT MOUSE STRAIN; PHARMACOLOGY; PHOSPHORYLATION; PROCEDURES; TUMOR CELL LINE;

ACETYLATION; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; FLAVONOIDS; HUMANS; MICE; MICE, MUTANT STRAINS; MOLECULAR TARGETED THERAPY; PHOSPHORYLATION; RETINOBLASTOMA PROTEIN; RNA, SMALL INTERFERING; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTORS;

EID: 84922558442     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgu117     Document Type: Article

References (75)

1. Gordon, V. et al. (2010) Alteration to the SWI/SNF complex in human cancers. Oncol. Rev., 4, 89-99.
2. Reisman, D. et al. (2009) The SWI/SNF complex and cancer. Oncogene, 28, 1653-1668.
3. Wang, W. et al. (1996) Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev., 10, 2117-2130.
4. Wang, W. et al. (1996) Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J., 15, 5370-5382.
5. Xia, W. et al. (2008) BAF180 is a critical regulator of p21 induction and a tumor suppressor mutated in breast cancer. Cancer Res., 68, 1667-1674.
6. Decristofaro, M.F. et al. (2001) Characterization of SWI/SNF protein expression in human breast cancer cell lines and other malignancies. J. Cell. Physiol., 186, 136-145.
7. Wiegand, K.C. et al. (2010) ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med., 363, 1532-1543.
8. Lichner, Z. et al. (2013) The chromatin remodeling gene ARID1A is a new prognostic marker in clear cell renal cell carcinoma. Am. J. Pathol., 182, 1163-1170.
9. Guan, B. et al. (2011) ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer Res., 71, 6718-6727.
10. Cho, H., et al. (2013) Loss of ARID1A/BAF250a expression is linked to tumor progression and adverse prognosis in cervical cancer. Hum. Pathol, 44, 1365-1374.
11. Wong, A.K. et al. (2000) BRG1, a component of the SWI-SNF complex, is mutated in multiple human tumor cell lines. Cancer Res., 60, 6171-6177.
12. Medina, P.P. et al. (2008) Frequent BRG1/SMARCA4-inactivating mutations in human lung cancer cell lines. Hum. Mutat., 29, 617-622.
13. The results shown here are in whole or part based upon data generated by the TCGA Research Network: http://cancergenome.nih.gov/.
14. Oike, T. et al. (2013) A synthetic lethality-based strategy to treat cancers harboring a genetic deficiency in the chromatin remodeling factor BRG1. Cancer Res., 73, 5508-5518.
15. Fukuoka, J. et al. (2004) Chromatin remodeling factors and BRM/BRG1 expression as prognostic indicators in non-small cell lung cancer. Clin. Cancer Res., 10, 4314-4324.
16. Watanabe, T. et al. (2011) Regulation of PTEN expression by the SWI/SNF chromatin-remodelling protein BRG1 in human colorectal carcinoma cells. Br. J. Cancer, 104, 146-154.
17. Bai, J. et al. (2013) BRG1 is a prognostic marker and potential therapeutic target in human breast cancer. PLoS One, 8, e59772.
18. Bock, V.L. et al. (2011) BRM and BRG1 subunits of the SWI/SNF chromatin remodelling complex are downregulated upon progression of benign skin lesions into invasive tumours. Br. J. Dermatol., 164, 1221-1227.
19. Sun, A. et al. (2007) Aberrant expression of SWI/SNF catalytic subunits BRG1/BRM is associated with tumor development and increased invasiveness in prostate cancers. Prostate, 67, 203-213.
20. Glaros, S. et al. (2007) The reversible epigenetic silencing of BRM: implications for clinical targeted therapy. Oncogene, 26, 7058-7066.
21. Gramling, S. et al. (2011) Discovery of BRM targeted therapies: novel reactivation of an anti-cancer gene. Lett. Drug Des. Discov., 8, 93-99.
22. Reisman, D.N. et al. (2002) Concomitant down-regulation of BRM and BRG1 in human tumor cell lines: differential effects on RB-mediated growth arrest vs CD44 expression. Oncogene, 21, 1196-1207.
23. Strobeck, M.W. et al. (2002) Compensation of BRG-1 function by Brm: insight into the role of the core SWI-SNF subunits in retinoblastoma tumor suppressor signaling. J. Biol. Chem., 277, 4782-4789.
24. Betz, B.L. et al. (2002) Re-expression of hSNF5/INI1/BAF47 in pediatric tumor cells leads to G1 arrest associated with induction of p16ink4a and activation of RB. Oncogene, 21, 5193-5203.
25. DelBove, J. et al. (2011) Identification of a core member of the SWI/SNF complex, BAF155/SMARCC1, as a human tumor suppressor gene. Epigenetics, 6, 1444-1453.
26. Dunaief, J.L. et al. (1994) The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell, 79, 119-130.
27. Strober, B.E. et al. (1996) Functional interactions between the hBRM/hBRG1 transcriptional activators and the pRB family of proteins. Mol. Cell. Biol., 16, 1576-1583.
28. Yao, H. et al. (2011) Dietary flavonoids as cancer prevention agents. J. Environ. Sci. Health. C. Environ. Carcinog. Ecotoxicol. Rev., 29, 1-31.
29. Nishiumi, S. et al. (2011) Dietary flavonoids as cancer-preventive and therapeutic biofactors. Front. Biosci. (Schol. Ed)., 3, 1332-1362.
30. Clere, N. et al. (2011) Anticancer properties of flavonoids: roles in various stages of carcinogenesis. Cardiovasc. Hematol. Agents Med. Chem., 9, 62-77.
31. Sedlacek, H. et al. (1996) Flavopiridol (L86 8275; NSC 649890), a new kinase inhibitor for tumor therapy. Int. J. Oncol., 9, 1143-1168.
32. Carlson, B.A. et al. (1996) Flavopiridol induces G1 arrest with inhibition of cyclin-dependent kinase (CDK) 2 and CDK4 in human breast carcinoma cells. Cancer Res., 56, 2973-2978.
33. Lee, S.J. et al. (2011) Curcumin-induced HDAC inhibition and attenuation of medulloblastoma growth in vitro and in vivo. BMC Cancer, 11, 144.
34. Attoub, S. et al. (2011) Inhibition of cell survival, invasion, tumor growth and histone deacetylase activity by the dietary flavonoid luteolin in human epithelioid cancer cells. Eur. J. Pharmacol., 651, 18-25.
35. Wheatley, N.C. et al. (2010) Antimalarial histone deacetylase inhibitors containing cinnamate or NSAID components. Bioorg. Med. Chem. Lett., 20, 7080-7084.
36. Son, I.H. et al. (2007) Pomiferin, histone deacetylase inhibitor isolated from the fruits of Maclura pomifera. Bioorg. Med. Chem. Lett., 17, 4753-4755.
37. Bontempo, P. et al. (2007) Feijoa sellowiana derived natural Flavone exerts anti-cancer action displaying HDAC inhibitory activities. Int. J. Biochem. Cell Biol., 39, 1902-1914.
38. Gramling, S. et al. (2011) Pharmacologic reversal of epigenetic silencing of the anticancer protein BRM: a novel targeted treatment strategy. Oncogene, 30, 3289-3294.
39. Mizutani, T. et al. (2002) Maintenance of integrated proviral gene expression requires Brm, a catalytic subunit of SWI/SNF complex. J. Biol. Chem., 277, 15859-15864.
40. Bourachot, B. et al. (2003) Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation. EMBO J., 22, 6505-6515.
41. Kahali, B. et al. (2014) Identifying targets for the restoration and reactivation of BRM. Oncogene, 33, 653-664.
42. Trotter, K.W. et al. (2004) Reconstitution of glucocorticoid receptordependent transcription in vivo. Mol. Cell. Biol., 24, 3347-3358.
43. Hou, D.X. et al. (2010) Flavonoids as protein kinase inhibitors for cancer chemoprevention: direct binding and molecular modeling. Antioxid. Redox Signal., 13, 691-719.
44. Lee, S.O. et al. (2007) Silibinin suppresses PMA-induced MMP-9 expression by blocking the AP-1 activation via MAPK signaling pathways in MCF-7 human breast carcinoma cells. Biochem. Biophys. Res. Commun., 354, 165-171.
45. Reisman, D. et al. (1995) Glucocorticoid regulation of cyclin D3 gene transcription and mRNA stability in lymphoid cells. Mol. Endocrinol., 9, 1500-1509.
46. Liu, G. et al. (2011) Two novel BRM insertion promoter sequence variants are associated with loss of BRM expression and lung cancer risk. Oncogene, 30, 3295-3304.
47. Li, L. et al. (2012) Baicalin is anti-inflammatory in cigarette smoke-induced inflammatory models in vivo and in vitro: a possible role for HDAC2 activity. Int. Immunopharmacol., 13, 15-22.
48. Gilbert, E.R. et al. (2010) Flavonoids influence epigenetic-modifying enzyme activity: structure-function relationships and the therapeutic potential for cancer. Curr. Med. Chem., 17, 1756-1768.
49. Wang, Y. et al. (2006) Prevention of lung cancer progression by bexarotene in mouse models. Oncogene, 25, 1320-1329.
50. Hollman, P.C. et al. (1995) Absorption of dietary quercetin glycosides and quercetin in healthy ileostomy volunteers. Am. J. Clin. Nutr., 62, 1276-1282.
51. Hollman, P.C. et al. (1998) Bioavailability and health effects of dietary flavonols in man. Arch. Toxicol. Suppl., 20, 237-248.
52. Yang, C.S. et al. (2001) Inhibition of carcinogenesis by dietary polyphenolic compounds. Annu. Rev. Nutr., 21, 381-406.
53. Yang, K. et al. (2000) Chemoprevention studies of the flavonoids quercetin and rutin in normal and azoxymethane-treated mouse colon. Carcinogenesis, 21, 1655-1660.
54. Singh, R.P. et al. (2002) Dietary feeding of silibinin inhibits advance human prostate carcinoma growth in athymic nude mice and increases plasma insulin-like growth factor-binding protein-3 levels. Cancer Res., 62, 3063-3069.
55. Singh, R.P. et al. (2006) Effect of silibinin on the growth and progression of primary lung tumors in mice. J. Natl. Cancer Inst., 98, 846-855.
56. Lambert, J.D. et al. (2008) Effect of genistein on the bioavailability and intestinal cancer chemopreventive activity of (-)-epigallocatechin-3-gallate. Carcinogenesis, 29, 2019-2024.
57. Angst, E. et al. (2013) The flavonoid quercetin inhibits pancreatic cancer growth in vitro and in vivo. Pancreas, 42, 223-229.
58. Ni, F. et al. (2012) Flavonoid ampelopsin inhibits the growth and metastasis of prostate cancer in vitro and in mice. PLoS One, 7, e38802.
59. Manach, C. et al. (2004) Pharmacokinetics and metabolism of dietary flavonoids in humans. Free Radic. Res., 38, 771-785.
60. Birt, D.F. et al. (2001) Dietary agents in cancer prevention: flavonoids and isoflavonoids. Pharmacol. Ther., 90, 157-177.
61. Miller, Y.E. et al. (2003) Induction of a high incidence of lung tumors in C57BL/6 mice with multiple ethyl carbamate injections. Cancer Lett., 198, 139-144.
62. Thaete, L.G. et al. (1987) Cellular derivation of lung tumors in sensitive and resistant strains of mice: results at 28 and 56 weeks after urethan treatment. J. Natl. Cancer Inst., 78, 743-749.
63. Meuwissen, R. et al. (2005) Mouse models for human lung cancer. Genes Dev., 19, 643-664.
64. Lu, G. et al. (2006) Inhibition of adenoma progression to adenocarcinoma in a 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced lung tumorigenesis model in A/J mice by tea polyphenols and caffeine. Cancer Res., 66, 11494-11501.
65. Dagne, A. et al. (2011) Enhanced inhibition of lung adenocarcinoma by combinatorial treatment with indole-3-carbinol and silibinin in A/J mice. Carcinogenesis, 32, 561-567.
66. de Wet, H. et al. (2001) Sequence requirements of the ATP-binding site within the C-terminal nucleotide-binding domain of mouse P-glycoprotein: structureactivity relationships for flavonoid binding. Biochemistry, 40, 10382-10391.
67. Dahiya, A. et al. (2000) Role of the LXCXE binding site in Rb function. Mol. Cell. Biol., 20, 6799-6805.
68. Ramos, S. (2008) Cancer chemoprevention and chemotherapy: dietary polyphenols and signalling pathways. Mol. Nutr. Food Res., 52, 507-526.
69. De Azevedo, W.F. Jr et al. (1996) Structural basis for specificity and potency of a flavonoid inhibitor of human CDK2, a cell cycle kinase. Proc. Natl. Acad. Sci. USA, 93, 2735-2740.
70. Li, Y. et al. (2010) Interactions of dietary phytochemicals with ABC transporters: possible implications for drug disposition and multidrug resistance in cancer. Drug Metab. Rev., 42, 590-611.
71. Arango, D. et al. (2013) Molecular basis for the action of a dietary flavonoid revealed by the comprehensive identification of apigenin human targets. Proc. Natl. Acad. Sci. USA, 110, E2153-E2162.
72. Hostetler, G. et al. (2012) Flavone deglycosylation increases their antiinflammatory activity and absorption. Mol. Nutr. Food Res., 56, 558-569.
73. Chung, J.Y. et al. (2001) Mechanisms of inhibition of the Ras-MAP kinase signaling pathway in 30.7b Ras 12 cells by tea polyphenols (-)-epigallocatechin-3-gallate and theaflavin-3, 3'-digallate. FASEB J., 15, 2022-2024.
74. Yang, C.S. et al. (1998) Tea and tea polyphenols inhibit cell hyperproliferation, lung tumorigenesis, and tumor progression. Exp. Lung Res., 24, 629-639.
75. Yang, G. et al. (1997) Characterization of early pulmonary hyperproliferation and tumor progression and their inhibition by black tea in a 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced lung tumorigenesis model with A/J mice. Cancer Res., 57, 1889-1894.