Suppression of NF-?B and NF-?B-regulated gene expression by apigenin through I?Bα and IKK pathway in TRAMP mice

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Shukla, Sanjeev ^a,b   Shankar, Eswar ^c   Fu, Pingfu ^c   MacLennan, Gregory T ^d   Gupta, Sanjay ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APIGENIN; CASPASE 3; CYCLIN D1; CYCLOOXYGENASE 2; I KAPPA B KINASE; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; PROTEIN BCL XL; VASCULOTROPIN; ANTIINFLAMMATORY AGENT; ANTINEOPLASTIC AGENT; VASCULOTROPIN A;

ADENOCARCINOMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL CYCLE G0 PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; MALE; MOUSE; NONHUMAN; PROSTATE CANCER; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; TUMOR VOLUME; ANIMAL; APOPTOSIS; C57BL MOUSE; DOWN REGULATION; DRUG EFFECTS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; PROSTATIC NEOPLASMS; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTICARCINOGENIC AGENTS; APIGENIN; APOPTOSIS; CASPASE 3; CELL PROLIFERATION; DOWN-REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; I-KAPPA B KINASE; MALE; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B; PHOSPHORYLATION; PROSTATIC NEOPLASMS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84945970740     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138710     Document Type: Article

References (67)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015; 65:5-29.
2. American Cancer Society. Cancer Facts and Figures 2015 online at http://www.cancer.org/Cancer/ProstateCancer/index. (Accessed 16 June 2015).
3. Lee BH, Kibel AS, Ciezki JP, Klein EA, Reddy CA, Yu C et al. Are Biochemical Recurrence Outcomes Similar After Radical Prostatectomy and Radiation Therapy? Analysis of Prostate Cancer-Specific Mortality by Nomogram-predicted Risks of Biochemical Recurrence. Eur Urol. 2015; 67:204-209.
4. Pomerantz MM, Werner L, Xie W, Regan MM, Lee GS, Sun T et al. Association of prostate cancer risk Loci with disease aggressiveness and prostate cancer-specific mortality. Cancer Prev Res (Phila). 2011; 4:719-728.
5. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature. 2006; 441:431-436.
6. Prasad S, Ravindran J, Aggarwal BB. NF-kappaB and cancer: how intimate is this relationship. Mol Cell Biochem. 2010; 336:25-37.
7. Cortes Sempere M, Rodríguez Fanjul V, Sanchez Perez I, Perona R. The role of the NFkappaB signalling pathway in cancer. Clin Transl Oncol. 2008; 10:143-147.
8. Hoffmann A, Baltimore D. (2006) Circuitry of nuclear factor kappaB signaling. Immunol Rev. 2006; 210:171-186.
9. Chaturvedi MM, Sung B, Yadav VR, Kannappan R, Aggarwal BB. NF-kB addiction and its role in cancer: 'one size does not fit all'. Oncogene. 2011; 30:1615-1630.
10. Zhou Y, Yau C, Gray JW, Chew K, Dairkee SH, Moore DH et al. Enhanced NF kappa B and AP-1 transcriptional activity associated with antiestrogen resistant breast cancer. BMC Cancer, 2007; 7:59.
11. Cooks T, Pateras IS, Tarcic O, Solomon H, Schetter AJ, Wilder S et al. Mutant p53 prolongs NF-kB activation and promotes chronic inflammation and inflammation-Associated colorectal cancer. Cancer Cell. 2013; 23:634-646.
12. Sur I, Ulvmar M, Toftgard R. The two-faced NF-kappaB in the skin. Int Rev Immunol. 2008; 27:205-223.
13. Kumar M, Allison DF, Baranova NN, Wamsley JJ, Katz AJ, Bekiranov S et al. NF-kB regulates mesenchymal transition for the induction of non-small cell lung cancer initiating cells. PLoS One 2013; 8: e68597.
14. Liu H, Yang J, Yuan Y, Xia Z, Chen M, Xie L et al. Regulation of Mcl-1 by constitutive activation of NF-kB contributes to cell viability in human esophageal squamous cell carcinoma cells. BMC Cancer. 2014; 14:98.
15. Kuo SH, Chou CH, Cheng AL, Wang CW, Chen YH, Chen RJ. Expression of BCL10 in cervical cancer has a role in the regulation of cell growth through the activation of NF-kB-dependent cyclin D1 signaling. Gynecol Oncol. 2012; 126:245-251.
16. Yang SH, Hsu CH, Lee JC, Tien YW, Kuo SH, Cheng AL. Nuclear expression of glioma-Associated oncogene homolog 1 and nuclear factor-kB is associated with a poor prognosis of pancreatic cancer. Oncology. 2013; 85:86-94.
17. Shukla S, MacLennan GT, Fu P, Patel J, Marengo SR, Resnick MI et al. Nuclear factor-kappaB/p65 (Rel A) is constitutively activated in human prostate adenocarcinoma and correlates with disease progression. Neoplasia. 2004; 6:390-400.
18. Lessard L, Mes-Masson AM, Lamarre L, Wall L, Lattouf JB, Saad F. NF-kappa B nuclear localization and its prognostic significance in prostate cancer. BJU Int. 2003; 91:417-420.
19. Suh J, Payvandi F, Edelstein LC, Amenta PS, Zong WX, Gelinas C et al. Mechanisms of constitutive NF-kappaB activation in human prostate cancer cells. Prostate. 2002; 52:183-200.
20. Shukla S, Maclennan GT, Marengo SR, Resnick MI, Gupta S. Constitutive activation of PI3K-Akt and NF-kappaB during prostate cancer progression in autochthonous transgenic mouse model. Prostate. 2005; 64:224-239.
21. Lessard L, Karakiewicz PI, Bellon-Gagnon P, Alam-Fahmy M, Ismail HA, Mes-Masson AM et al. Nuclear localization of nuclear factor-kappaB p65 in primary prostate tumors is highly predictive of pelvic lymph node metastases. Clin Cancer Res. 2006; 12:5741-5745.
22. Domingo-Domenech J, Mellado B, Ferrer B, Truan D, Codony-Servat J, Sauleda S et al. Activation of nuclear factor-kappaB in human prostate carcinogenesis and association to biochemical relapse. Br J Cancer. 2005; 93:1285-1294.
23. Ross JS, Kallakury BV, Sheehan CE, Fisher HA, Kaufman RP Kaur P Jr, et al. Expression of nuclear factor-kappa B and I kappa B alpha proteins in prostatic adenocarcinomas: correlation of nuclear factor-kappa B immunoreactivity with disease recurrence. Clin Cancer Res. 2004; 10:2466-2472.
24. Thakur VS, Deb G, Babcook MA, Gupta S. Plant phytochemicals as epigenetic modulators: role in cancer chemoprevention. AAPS J. 2014; 16:151-163
25. Gonzalez-Vallinas M, Gonzalez-Castejon M, Rodríguez-Casado A, Ramírez de Molina A. Dietary phytochemicals in cancer prevention and therapy: a complementary approach with promising perspectives. Nutr Rev. 2013; 71:585-599
26. Shukla S, Gupta S. Apigenin: a promising molecule for cancer prevention. Pharm Res. 2010; 27:962-978.
27. Tong X, Pelling JC. Targeting the PI3K/Akt/mTOR axis by apigenin for cancer prevention. Anticancer Agents Med Chem. 2013; 13:971-978.
28. Fang J, Zhou Q, Liu LZ, Xia C, Hu X, Shi X et al. Apigenin inhibits tumor angiogenesis through decreasing HIF-1alpha and VEGF expression. Carcinogenesis. 2007; 28:858-864.
29. Liang YC, Huang YT, Tsai SH, Lin-Shiau SY, Chen CF, Lin JK. Suppression of inducible cyclooxygenase and inducible nitric oxide synthase by apigenin and related flavonoids in mouse macrophages. Carcinogenesis. 1999; 20:1945-1952.
30. Shukla S, Gupta S. Suppression of constitutive and tumor necrosis factor alpha-induced nuclear factor (NF)-kappaB activation and induction of apoptosis by apigenin in human prostate carcinoma PC-3 cells: correlation with down-regulation of NF-kappaB-responsive genes. Clin Cancer Res. 2004; 10:3169-3178.
31. Seo HS, Choi HS, Kim SR, Choi YK, Woo SM, Shin I et al. Apigenin induces apoptosis via extrinsic pathway, inducing p53 and inhibiting STAT3 and NFkB signaling in HER2-overexpressing breast cancer cells. Mol Cell Biochem. 2012; 366:319-334
32. Das S, Das J, Samadder A, Boujedaini N, Khuda-Bukhsh AR. Apigenin-induced apoptosis in A375 and A549 cells through selective action and dysfunction of mitochondria. Exp Biol Med (Maywood). 2012; 237:1433-1448.
33. Kim SH, Kang JG, Kim CS, Ihm SH, Choi MG, Yoo HJ et al. Apigenin induces c-Myc-mediated apoptosis in FRO anaplastic thyroid carcinoma cells. Mol Cell Endocrinol. 2013; 369:130-139
34. Abu-Yousif AO, Smith KA, Getsios S, Green KJ, Van Dross RT, Pelling JC. Enhancement of UVBinduced apoptosis by apigenin in human keratinocytes and organotypic keratinocyte cultures. Cancer Res. 2008; 68:3057-3065
35. Kim BR, Jeon YK, Nam MJ. A mechanism of apigenin-induced apoptosis is potentially related to antiangiogenesis and anti-migration in human hepatocellular carcinoma cells. Food Chem Toxicol. 2011; 49:1626-1632
36. Hussain AR, Khan AS, Ahmed SO, Ahmed M, Platanias LC, Al-Kuraya KS et al. Apigenin induces apoptosis via downregulation of S-phase kinase-Associated protein 2-mediated induction of p27Kip1 in primary effusion lymphoma cells. Cell Prolif. 2010; 43:170-183
37. Ruela-de-Sousa RR, Fuhler GM, Blom N, Ferreira CV, Aoyama H, Peppelenbosch MP. Cytotoxicity of apigenin on leukemia cell lines: implications for prevention and therapy. Cell Death Dis. 2010; 1:e19.
38. Shukla S, Bhaskaran N, Babcook MA, Fu P, Maclennan GT, Gupta S. Apigenin inhibits prostate cancer progression in TRAMP mice via targeting PI3K/Akt/FoxO pathway. Carcinogenesis. 2014; 35:452-460.
39. Shukla S, Gupta S. 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. 2007; 6:1102-1114.
40. Shukla S, Gupta S. Apigenin-induced prostate cancer cell death is initiated by reactive oxygen species and p53 activation. Free Radic Biol Med. 2008; 44:1833-1845
41. Shukla S, Fu P, Gupta S. Apigenin induces apoptosis by targeting inhibitor of apoptosis proteins and Ku70-Bax interaction in prostate cancer. Apoptosis. 2014; 9:883-894.
42. Hollman PC, Katan MB. Dietary flavonoids: intake, health effects and bioavailability. Food Chem Toxicol. 1999; 37:937-942.
43. Shukla S, MacLennan GT, Flask CA, Fu P, Mishra A, Resnick MI et al. Blockade of beta-catenin signaling by plant flavonoid apigenin suppresses prostate carcinogenesis in TRAMP mice. Cancer Res. 2007; 67:6925-6935.
44. Kaplan-Lefko PJ, Chen TM, Ittmann MM, Barrios RJ, Ayala GE, Huss WJ et al. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate. 2003; 55:219-237
45. Gasparian AV, Yao YJ, Kowalczyk D, Lyakh LA, Karseladze A, Slaga TJ et al. The role of IKK in constitutive activation of NF-kappaB transcription factor in prostate carcinoma cells. J Cell Sci. 2002; 115:141-151.
46. Vinall RL, Mahaffey CM, Davis RR, Luo Z, Gandour-Edwards R, Ghosh PM et al. Dual blockade of PKA and NF-kB inhibits H2 relaxin-mediated castrate-resistant growth of prostate cancer sublines and induces apoptosis. Horm Cancer. 2011; 2:224-238
47. Gasparian AV, Guryanova OA, Chebotaev DV, Shishkin AA, Yemelyanov AY, Budunova IV. Targeting transcription factor NFkappaB: comparative analysis of proteasome and IKK inhibitors. Cell Cycle. 2009; 8:1559-1566.
48. Huang S, Pettaway CA, Uehara H, Bucana CD, Fidler IJ. Blockade of NF-kappaB activity in human prostate cancer cells is associated with suppression of angiogenesis, invasion, and metastasis. Oncogene. 2001; 20:4188-4197.
49. Joyce D, Albanese C, Steer J, Fu M, Bouzahzah B, Pestell RG. NF-kappaB and cell-cycle regulation: the cyclin connection. Cytokine Growth Factor Rev. 2001; 12:73-90.
50. Hinz M, Krappmann D, Eichten A, Heder A, Scheidereit C, Strauss M. NF-kappaB function in growth control: regulation of cyclin D1 expression and G0/G1-to-S-phase transition. Mol Cell Biol. 1999; 19:2690-2698.
51. Romagnolo DF, Selmin OI. Flavonoids and cancer prevention: a review of the evidence. J Nutr Gerontol Geriatr. 2012; 31:206-238
52. Hui C, Qi X, Qianyong Z, Xiaoli P, Jundong Z, Mantian M. Flavonoids, flavonoid subclasses and breast cancer risk: a meta-Analysis of epidemiologic studies. PLoS One. 2013; 8:e54318
53. Kyle JA, Sharp L, Little J, Duthie GG, McNeill G. Dietary flavonoid intake and colorectal cancer: a casecontrol study. Br J Nutr. 2010; 103:429-436.
54. Bosetti C, Bravi F, Talamini R, Parpinel M, Gnagnarella P, Negri E et al. Flavonoids and prostate cancer risk: a study in Italy. Nutr Cancer. 2006; 56:123-127.
55. Gates MA, Vitonis AF, Tworoger SS, Rosner B, Titus-Ernstoff L, Hankinson SE et al. Flavonoid intake and ovarian cancer risk in a population-based case-control study. Int J Cancer. 2009; 124:1918-1925.
56. Leclercq G, Jacquot Y. Interactions of isoflavones and other plant derived estrogens with estrogen receptors for prevention and treatment of breast cancer-considerations concerning related efficacy and safety. J Steroid Biochem Mol Biol. 2014; 139:237-244
57. Nielsen SE, Young JF, Daneshvar B, Lauridsen ST, Knuthsen P, Sandström B et al. Effect of parsley (Petroselinum crispum) intake on urinary apigenin excretion, blood antioxidant enzymes and biomarkers for oxidative stress in human subjects. Br J Nutr. 1999; 81:447-455.
58. Janssen K, Mensink RP, Cox FJ, Harryvan JL, Hovenier R, Hollman PC et al. Effects of the flavonoids quercetin and apigenin on hemostasis in healthy volunteers: results from an in vitro and a dietary supplement study. Am J Clin Nutr. 1998; 67:255-262.
59. Moon YJ, Wang X, Morris ME. Dietary flavonoids: effects on xenobiotic and carcinogen metabolism. Toxicol In Vitro. 2006; 20:187-210.
60. Kimura Y, Ito H, Ohnishi R, Hatano T. Inhibitory effects of polyphenols on human cytochrome P450 3A4 and 2C9 activity. Food Chem Toxicol. 2010; 48:429-35
61. Si D, Wang Y, Zhou YH, Guo Y, Wang J, Zhou H et al. Mechanism of CYP2C9 inhibition by flavones and flavonols. Drug Metab Dispos. 2009; 37:629-34
62. Ross JA, Kasum CM. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr. 2002; 22:19-34.
63. Hu M, Chen J, Lin H. Metabolism of flavonoids via enteric recycling: mechanistic studies of disposition of apigenin in the Caco-2 cell culture model. J Pharmacol Exp Ther. 2003; 307:314-21
64. Gradolatto A, Basly JP, Berges R, Teyssier C, Chagnon MC, Siess MH et al. Pharmacokinetics and metabolism of apigenin in female and male rats after a single oral administration. Drug Metab Dispos. 2005; 33:49-54.
65. Meyer H, Bolarinwa A, Wolfram G, Linseisen J. Bioavailability of apigenin from apiin-rich parsley in humans. Ann Nutr Metab. 2006; 50:167-172.
66. Kallakury BV, Sheehan CE, Ambros RA, Fisher HA, Kaufman RP Jr, Ross JS. The prognostic significance of p34cdc2 and cyclin D1 protein expression in prostate adenocarcinoma. Cancer. 1997; 80:753-763.
67. Fonseca GN, Srougi M, Leite KR, Nesrallah LJ, Ortiz V. The role of HER2/neu, BCL2, p53 genes and proliferating cell nuclear protein as molecular prognostic parameters in localized prostate carcinoma. Sao Paulo Med J. 2004; 122:124-127.