Inhibition of MDA-MB-231 breast cancer cell proliferation and tumor growth by apigenin through induction of G2/M arrest and histone H3 acetylation-mediated p21WAF1/CIP1 expression

Environmental Toxicology

Volumn 32, Issue 2, 2017, Pages 434-444

  Tseng, Tsui Hwa ^a,b   Chien, Ming Hsien ^c,d   Lin, Wea Lung ^b   Wen, Yu Ching ^d   Chow, Jyh Ming ^d   Chen, Chi Kuan ^e   Kuo, Tsang Chih ^f   Lee, Wei Jiunn ^d,g  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e GENOMICS RESEARCH CENTER   (Taiwan)

^f NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^g TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

apigenin; breast cancer; cell cycle arrest; histone H3 acetylation; p21WAF1 CIP1

Indexed keywords

ACETYLATION; CELL CULTURE; CELL PROLIFERATION; DISEASES; ENZYME INHIBITION; TUMORS;

APIGENIN; BREAST CANCER; CELL-CYCLE ARREST; HISTONE H3; P21WAF1/CIP1;

FLAVONOIDS;

APIGENIN; CYCLIN A; CYCLIN B; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1; HISTONE DEACETYLASE; HISTONE H3; ANTINEOPLASTIC AGENT; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; HISTONE;

APOPTOSIS; BIOCHEMISTRY; CANCER; CELLS AND CELL COMPONENTS; GENE EXPRESSION; INHIBITION; ORGANIC COMPOUND; PROTEIN; TUMOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BREAST CANCER; CANCER PREVENTION; CELL CYCLE PROGRESSION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME INHIBITION; EPIGENETICS; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; M PHASE CELL CYCLE CHECKPOINT; MDA-MB-231 CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TUMOR XENOGRAFT; UPREGULATION; ACETYLATION; ANIMAL; BAGG ALBINO MOUSE; BREAST NEOPLASMS; CELL CYCLE CHECKPOINT; CELL CYCLE G2 PHASE; CELL DIVISION; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; METABOLISM; TUMOR CELL LINE;

ACETYLATION; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APIGENIN; BREAST NEOPLASMS; CELL CYCLE CHECKPOINTS; CELL DIVISION; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; EPIGENESIS, GENETIC; FEMALE; G2 PHASE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASES; HISTONES; HUMANS; MICE; MICE, INBRED BALB C; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84975778640     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.22247     Document Type: Article

References (41)

1. Beaumont T, Leadbeater M. 2011. Treatment and care of patients with metastatic breast cancer. Nurs Stand 25:49–56.
2. Birt DF, Walker B, Tibbels MG, Bresnick E. 1986. Anti-mutagenesis and anti-promotion by apigenin, robinetin and indole-3-carbinol. Carcinogenesis 7:959–963.
3. Birt DF, Hendrich S, Wang W. 2001. Dietary agents in cancer prevention: Flavonoids and isoflavonoids. Pharmacol Ther 90:157–177.
4. Blagosklonny MV, Robey R, Sackett DL, Du L, Traganos F, Darzynkiewicz Z, Fojo T, Bates SE. 2002. Histone deacetylase inhibitors all induce p21 but differentially cause tubulin acetylation, mitotic arrest, and cytotoxicity. Mol Cancer Ther 1:937–941.
5. Bolden JE, Peart MJ, Johnstone RW. 2006. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5:769–784.
6. Budman DR, Tai J, Calabro A, John V. 2011. The histone deacetylase inhibitor panobinostat demonstrates marked synergy with conventional chemotherapeutic agents in human ovarian cancer cell lines. Invest New Drugs 29:1224–1229.
7. Cao X, Liu B, Cao W, Zhang W, Zhang F, Zhao H, Meng R, Zhang L, Niu R, Hao X, Zhang B. 2013. Autophagy inhibition enhances apigenin-induced apoptosis in human breast cancer cells. Chin J Cancer Res 25:212–222.
8. Cayrol C, Knibiehler M, Ducommun B. 1998. p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells. Oncogene 16:311–320.
9. Chen D, Landis-Piwowar KR, Chen MS, Dou QP. 2007. Inhibition of proteasome activity by the dietary flavonoid apigenin is associated with growth inhibition in cultured breast cancer cells and xenografts. Breast Cancer Res 9:R80.
10. Davis CD, Ross SA. 2007. Dietary components impact histone modifications and cancer risk. Nutr Rev 65:88–94.
11. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, Lickley LA, Rawlinson E, Sun P, Narod SA. 2007. Triple-negative breast cancer: Clinical features and patterns of recurrence. Clin Cancer Res 13:4429–4434.
12. Elias AD. 2010. Triple-negative breast cancer: A short review. Am J Clin Oncol 33:637–645.
13. Ellis L, Atadja PW, Johnstone RW. 2009. Epigenetics in cancer: Targeting chromatin modifications. Mol Cancer Ther 8:1409–1420.
14. Esteller M. 2008. Epigenetics in cancer. N Engl J Med 358:1148–1159.
15. Gomathinayagam R, Sowmyalakshmi S, Mardhatillah F, Kumar R, Akbarsha MA, Damodaran C. 2008. Anticancer mechanism of plumbagin, a natural compound, on non-small cell lung cancer cells. Anticancer Res 28:785–792.
16. Ham SL, Nasrollahi S, Shah KN, Soltisz A, Paruchuri S, Yun YH, Luker GD, Bishayee A, Tavana H. 2015. Phytochemicals potently inhibit migration of metastatic breast cancer cells. Integr Biol (Camb) 7:792–800.
17. Hudis CA, Gianni L. 2011. Triple-negative breast cancer: An unmet medical need. Oncologist 1:1–11.
18. Keen JC, Yan L, Mack KM, Pettit C, Smith D, Sharma D, Davidson NE. 2003. A novel histone deacetylase inhibitor, scriptaid, enhances expression of functional estrogen receptor alpha (ER) in ER negative human breast cancer cells in combination with 5-aza 2'-deoxycytidine. Breast Cancer Res Treat 81:177–186.
19. Kikuchi H, Barman HK, Nakayama M, Takami Y, Nakayama T. 2006. Participation of histones, histone modifying enzymes and histone chaperones in vertebrate cell functions. Subcell Biochem 40:225–243.
20. Kim EJ, Shin M, Park H, Hong JE, Shin HK, Kim J, Kwon DY, Park JH. 2009. Oral administration of 3,3'-diindolylmethane inhibits lung metastasis of 4T1 murine mammary carcinoma cells in BALB/c mice. J Nutr 139:2373–2379.
21. Konstantinopoulos PA, Karamouzis MV, Papavassiliou AG. 2007. Focus on acetylation: The role of histone deacetylase inhibitors in cancer therapy and beyond. Expert Opin Investig Drugs 16:569–571.
22. Lee WJ, Chen WK, Wang CJ, Lin WL, Tseng TH. 2008. Apigenin inhibits HGF-promoted invasive growth and metastasis involving blocking PI3K/Akt pathway and beta 4 integrin function in MDA-MB-231 breast cancer cells. Toxicol Appl Pharmacol 226:178–191.
23. Lin HY, Chen CS, Lin SP, Weng JR, Chen CS. 2006. Targeting histone deacetylase in cancer therapy. Med Res Rev 26:397–413.
24. Liu T, Kuljaca S, Tee A, Marshall GM. 2006. Histone deacetylase inhibitors: Multifunctional anticancer agents. Cancer Treat Rev 32:157–165.
25. Love IM, Sekaric P, Shi D, Grossman SR, Androphy EJ. 2012. The histone acetyltransferase PCAF regulates p21 transcription through stress-induced acetylation of histone H3. Cell Cycle 11:2458–2466.
26. McDonald ER III, El-Deiry WS. 2000. Cell cycle control as a basis for cancer drug development (Review). Int J Oncol 16:871–886.
27. Meeran SM, Katiyar SK. 2008. Cell cycle control as a basis for cancer chemoprevention through dietary agents. Front Biosci 13:2191–2202.
28. Middleton E Jr, Kandaswami C, Theoharides TC. 2000. The effects of plant flavonoids on mammalian cells: Implications for inflammation, heart disease, and cancer. Pharmacol Rev 52:673–751.
29. Neumann J, Boerries M, Kohler R, Giaisi M, Krammer PH, Busch H, Li-Weber M. 2014. The natural anticancer compound rocaglamide selectively inhibits the G1-S-phase transition in cancer cells through the ATM/ATR-mediated Chk1/2 cell cycle checkpoints. Int J Cancer 134:1991–2002.
30. Paik S. 2006. Molecular profiling of breast cancer. Curr Opin Obstet Gynecol 18:59–63.
31. Patel D, Shukla S, Gupta S. 2007. Apigenin and cancer chemoprevention: Progress, potential and promise (review). Int J Oncol 30:233–245.
32. Pathiraja TN, Shetty PB, Jelinek J, He R, Hartmaier R, Margossian AL, Hilsenbeck SG, Issa JP, Oesterreich S. 2011. Progesterone receptor isoform-specific promoter methylation: Association of PRA promoter methylation with worse outcome in breast cancer patients. Clin Cancer Res 17:4177–4186.
33. Pruitt K, Zinn RL, Ohm JE, McGarvey KM, Kang SH, Watkins DN, Herman JG, Baylin SB. 2006. Inhibition of SIRT1 reactivates silenced cancer genes without loss of promoter DNA hypermethylation. PLoS Genet 2:e40.
34. Rao R, Balusu R, Fiskus W, Mudunuru U, Venkannagari S, Chauhan L, Smith JE, Hembruff SL, Ha K, Atadja P, Bhalla KN. 2012. Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells. Mol Cancer Ther 11:973–983.
35. Sharma S, Kelly TK, Jones PA. 2010. Epigenetics in cancer. Carcinogenesis 31:27–36.
36. Shukla S, Gupta S. 2007. Apigenin-induced cell cycle arrest is mediated by modulation of MAPK, PI3K-Akt, and loss of cyclin D1 associated retinoblastoma dephosphorylation in human prostate cancer cells. Cell Cycle 6:1102–1114.
37. Shukla S, Gupta S. 2010. Apigenin: A promising molecule for cancer prevention. Pharm Res 27:962–978.
38. Storch K, Eke I, Borgmann K, Krause M, Richter C, Becker K, Schrock E, Cordes N. 2010. Three-dimensional cell growth confers radioresistance by chromatin density modification. Cancer Res 70:3925–3934.
39. Tan S, Liu ZP. 2015. Natural products as zinc-dependent histone deacetylase inhibitors. Chem Med Chem 10:441–450.
40. Tate CR, Rhodes LV, Segar HC, Driver JL, Pounder FN, Burow ME, Collins-Burow BM. 2012. Targeting triple-negative breast cancer cells with the histone deacetylase inhibitor panobinostat. Breast Cancer Res 14:R79.
41. Zhou Q, Atadja P, Davidson NE. 2007. Histone deacetylase inhibitor LBH589 reactivates silenced estrogen receptor alpha (ER) gene expression without loss of DNA hypermethylation. Cancer Biol Ther 6:64–69.