Peanut arachidin-1 enhances Nrf2-mediated protective mechanisms against TNF-α-induced ICAM-1 expression and NF-κB activation in endothelial cells

Chen,Lih-Geeng; Zhang,Yu-Qi; Wu,Zhi-Zhen; Hsieh,Chia-Wen; Chu,Chi-Shih; Wung,Being-Sun

doi:10.3892/ijmm.2017.3238

Peanut arachidin-1 enhances Nrf2-mediated protective mechanisms against TNF-α-induced ICAM-1 expression and NF-κB activation in endothelial cells

Authors:
- Lih-Geeng Chen
- Yu-Qi Zhang
- Zhi-Zhen Wu
- Chia-Wen Hsieh
- Chi-Shih Chu
- Being-Sun Wung
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Affiliations: Department of Microbiology, Immunology and Biopharmaceuticals, National Chiayi University, Chiayi 600, Taiwan, R.O.C.
Published online on: November 7, 2017 https://doi.org/10.3892/ijmm.2017.3238
Pages: 541-547

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Abstract

Arachidin-1 [trans-4-(3-methyl-1-butenyl)-3,5,3',4'-tetrahydroxystilbene] is a polyphenol produced by peanut kernels during germination. The aim of the present study was to investigate the mechanism underlying the anti-inflammatory effect of arachidin-1 in endothelial cells (ECs). The results of cell adhesion and western blotting assays demonstrated that arachidin-1 attenuated tumor necrosis factor (TNF)-α-induced monocyte/EC adhesion and intercellular adhesion molecule-1 (ICAM-1) expression. Arachidin-1 was demonstrated to exert its inhibitory effects by the attenuation of TNF-α-induced nuclear factor-κB (NF-κB) nuclear translocation and inhibitor of κB-α (IκBα) degradation. Furthermore, arachidin-1 upregulated nuclear factor-E2-related factor-2 (Nrf-2), a known mediator of phase II enzyme expression, and increased the transcriptional activity of antioxidant response element. Transfection of ECs with Nrf-2 siRNA blocked the inhibitory effect of arachidin-1 on ICAM-1 expression, NF-κB nuclear translocation and IκBα degradation. In addition, arachidin-1 induced the expression of the phase II enzymes thioredoxin-1, thioredoxin reductase-1, heme oxygenase-1, glutamyl-cysteine synthetase and glutathione S-transferase. Following arachidin-1 pretreatment, the H2O2-induced generation of reactive oxygen species was reduced. Therefore, the present results indicate that arachidin-1 suppresses TNF-α-induced inflammation in ECs through the upregulation of Nrf-2-related phase II enzyme expression.

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1	Fernandes A, Miller-Fleming L and Pais TF: Microglia and inflammation: Conspiracy, controversy or control? Cell Mol Life Sci. 71:3969–3985. 2014. View Article : Google Scholar : PubMed/NCBI
2	Ross R: Atherosclerosis - an inflammatory disease. N Engl J Med. 340:115–126. 1999. View Article : Google Scholar : PubMed/NCBI
3	Glass CK and Witztum JL: Atherosclerosis. the road ahead. Cell. 104:503–516. 2001. View Article : Google Scholar : PubMed/NCBI
4	Ledebur HC and Parks TP: Transcriptional regulation of the intercellular adhesion molecule-1 gene by inflammatory cytokines in human endothelial cells. Essential roles of a variant NF-kappa B site and p65 homodimers. J Biol Chem. 270:933–943. 1995. View Article : Google Scholar : PubMed/NCBI
5	Tak PP and Firestein GS: NF-kappaB: A key role in inflammatory diseases. J Clin Invest. 107:7–11. 2001. View Article : Google Scholar : PubMed/NCBI
6	Condori J, Sivakumar G, Hubstenberger J, Dolan MC, Sobolev VS and Medina-Bolivar F: Induced biosynthesis of resveratrol and the prenylated stilbenoids arachidin-1 and arachidin-3 in hairy root cultures of peanut: Effects of culture medium and growth stage. Plant Physiol Biochem. 48:310–318. 2010. View Article : Google Scholar : PubMed/NCBI
7	Piotrowska H, Kucinska M and Murias M: Biological activity of piceatannol: Leaving the shadow of resveratrol. Mutat Res. 750:60–82. 2012. View Article : Google Scholar
8	Huang CP, Au LC, Chiou RY, Chung PC, Chen SY, Tang WC, Chang CL, Fang WH and Lin SB: Arachidin-1, a peanut stilbenoid, induces programmed cell death in human leukemia HL-60 cells. J Agric Food Chem. 58:12123–12129. 2010. View Article : Google Scholar : PubMed/NCBI
9	Ko JC, Chen HJ, Huang YC, Tseng SC, Weng SH, Wo TY, Huang YJ, Chiu HC, Tsai MS, Chiou RY, et al: HSP90 inhibition induces cytotoxicity via downregulation of Rad51 expression and DNA repair capacity in non-small cell lung cancer cells. Regul Toxicol Pharmacol. 64:415–424. 2012. View Article : Google Scholar : PubMed/NCBI
10	Ball JM, Medina-Bolivar F, Defrates K, Hambleton E, Hurlburt ME, Fang L, Yang T, Nopo-Olazabal L, Atwill RL, Ghai P, et al: Investigation of stilbenoids as potential therapeutic agents for rotavirus gastroenteritis. Adv Virol. 2015:2935242015. View Article : Google Scholar : PubMed/NCBI
11	Kang KW, Lee SJ and Kim SG: Molecular mechanism of nrf2 activation by oxidative stress. Antioxid Redox Signal. 7:1664–1673. 2005. View Article : Google Scholar : PubMed/NCBI
12	Wu CC, Hsu MC, Hsieh CW, Lin JB, Lai PH and Wung BS: Upregulation of heme oxygenase-1 by Epigallocatechin-3-gallate via the phosphatidylinositol 3-kinase/Akt and ERK pathways. Life Sci. 78:2889–2897. 2006. View Article : Google Scholar
13	Chen B, Lu Y, Chen Y and Cheng J: The role of Nrf2 in oxidative stress-induced endothelial injuries. J Endocrinol. 225:R83–R99. 2015. View Article : Google Scholar : PubMed/NCBI
14	Nguyen T, Yang CS and Pickett CB: The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic Biol Med. 37:433–441. 2004. View Article : Google Scholar : PubMed/NCBI
15	Wung BS, Hsu MC, Wu CC and Hsieh CW: Piceatannol upregulates endothelial heme oxygenase-1 expression via novel protein kinase C and tyrosine kinase pathways. Pharmacol Res. 53:113–122. 2006. View Article : Google Scholar
16	Liao BC, Hsieh CW, Liu YC, Tzeng TT, Sun YW and Wung BS: Cinnamaldehyde inhibits the tumor necrosis factor-alpha-induced expression of cell adhesion molecules in endothelial cells by suppressing NF-kappaB activation: Effects upon IkappaB and Nrf2. Toxicol Appl Pharmacol. 229:161–171. 2008. View Article : Google Scholar : PubMed/NCBI
17	Chang JC, Lai YH, Djoko B, Wu PL, Liu CD, Liu YW and Chiou RY: Biosynthesis enhancement and antioxidant and anti-inflammatory activities of peanut (Arachis hypogaea L.) arachidin-1, arachidin-3, and isopentadienylresveratrol. J Agric Food Chem. 54:10281–10287. 2006. View Article : Google Scholar : PubMed/NCBI
18	Singh A, Boldin-Adamsky S, Thimmulappa RK, Rath SK, Ashush H, Coulter J, Blackford A, Goodman SN, Bunz F, Watson WH, et al: RNAi-mediated silencing of nuclear factor erythroid-2-related factor 2 gene expression in non-small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy. Cancer Res. 68:7975–7984. 2008. View Article : Google Scholar : PubMed/NCBI
19	Kasiotis KM, Pratsinis H, Kletsas D and Haroutounian SA: Resveratrol and related stilbenes: Their anti-aging and anti-angiogenic properties. Food Chem Toxicol. 61:112–120. 2013. View Article : Google Scholar : PubMed/NCBI
20	Walle T, Hsieh F, DeLegge MH, Oatis JE Jr and Walle UK: High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab Dispos. 32:1377–1382. 2004. View Article : Google Scholar : PubMed/NCBI
21	Lee HH, Park SA, Almazari I, Kim EH, Na HK and Surh YJ: Piceatannol induces heme oxygenase-1 expression in human mammary epithelial cells through activation of ARE-driven Nrf2 signaling. Arch Biochem Biophys. 501:142–150. 2010. View Article : Google Scholar : PubMed/NCBI
22	Lin D, Dai F, Sun LD and Zhou B: Toward an understanding of the role of a catechol moiety in cancer chemoprevention: The case of copper- and o-quinone-dependent Nrf2 activation by a catechol-type resveratrol analog. Mol Nutr Food Res. 59:2395–2406. 2015. View Article : Google Scholar : PubMed/NCBI
23	Sirota R, Gibson D and Kohen R: The role of the catecholic and the electrophilic moieties of caffeic acid in Nrf2/Keap1 pathway activation in ovarian carcinoma cell lines. Redox Biol. 4:48–59. 2015. View Article : Google Scholar :
24	Surh YJ, Kundu JK and Na HK: Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med. 74:1526–1539. 2008. View Article : Google Scholar : PubMed/NCBI
25	Son Y, Byun SJ and Pae HO: Involvement of heme oxygenase-1 expression in neuroprotection by piceatannol, a natural analog and a metabolite of resveratrol, against glutamate-mediated oxidative injury in HT22 neuronal cells. Amino Acids. 45:393–401. 2013. View Article : Google Scholar : PubMed/NCBI