3,809
Views
42
CrossRef citations to date
0
Altmetric
Research Article

Kaempferol-induced GPER upregulation attenuates atherosclerosis via the PI3K/AKT/Nrf2 pathway

, , , , & ORCID Icon
Pages 1104-1114 | Received 08 Mar 2021, Accepted 26 Jul 2021, Published online: 17 Aug 2021

References

  • Alkhalidy H, Moore W, Wang Y, Luo J, McMillan RP, Zhen W, Zhou K, Liu D. 2018. The flavonoid kaempferol ameliorates streptozotocin-induced diabetes by suppressing hepatic glucose production. Molecules. 23:2338.
  • Aryan L, Younessi D, Zargari M, Banerjee S, Agopian J, Rahman S, Borna R, Ruffenach G, Umar S, Eghbali M. 2020. The role of estrogen receptors in cardiovascular disease. Int J Mol Sci. 21:4314.
  • Barton M, Prossnitz ER. 2015. Emerging roles of GPER in diabetes and atherosclerosis. Trends Endocrinol Metab. 26(4):185–192.
  • Chang W, Zhu F, Zheng H, Zhou Z, Miao P, Zhao L, Mao Z. 2019. Glucagon-like peptide-1 receptor agonist dulaglutide prevents ox-LDL-induced adhesion of monocytes to human endothelial cells: an implication in the treatment of atherosclerosis. Mol Immunol. 116:73–79.
  • Che J, Liang B, Zhang Y, Wang Y, Tang J, Shi G. 2017. Kaempferol alleviates ox-LDL-induced apoptosis by up-regulation of autophagy via inhibiting PI3K/Akt/mTOR pathway in human endothelial cells. Cardiovasc Pathol. 31:57–62.
  • Chen S, Li X, Wang Y, Mu P, Chen C, Huang P, Liu D. 2019. Ginsenoside Rb1 attenuates intestinal ischemia/reperfusion-induced inflammation and oxidative stress via activation of the PI3K/Akt/Nrf2 signaling pathway. Mol Med Rep. 19:3633–3641.
  • Cho SH, Jeong MH, Sim DS, Hong YJ, Park HW, Kim JH, Ahn Y, Cho JG, Park JC, Kang JC. 2011. Diagnostic value of nitroglycerin-induced headache as a negative predictor of coronary atherosclerosis. Chonnam Med J. 47(1):14–19.
  • Dworatzek E, Mahmoodzadeh S. 2017. Targeted basic research to highlight the role of estrogen and estrogen receptors in the cardiovascular system. Pharmacol Res. 119:27–35.
  • Fan DX, Yang XH, Li YN, Guo L. 2018. 17β-Estradiol on the expression of G-protein coupled estrogen receptor (GPER/GPR30) mitophagy, and the PI3K/Akt signaling pathway in ATDC5 chondrocytes in vitro. Med Sci Monit. 24:1936–1947.
  • Filardo EJ. 2018. A role for G-protein coupled estrogen receptor (GPER) in estrogen-induced carcinogenesis: dysregulated glandular homeostasis, survival and metastasis. J Steroid Biochem Mol Biol. 176:38–48.
  • Fredman G, Tabas I. 2017. Boosting inflammation resolution in atherosclerosis: the next frontier for therapy. Am J Pathol. 187(6):1211–1221.
  • Gencel VB, Benjamin MM, Bahou SN, Khalil RA. 2012. Vascular effects of phytoestrogens and alternative menopausal hormone therapy in cardiovascular disease. Mini Rev Med Chem. 12(2):149–174.
  • Grande F, Occhiuzzi MA, Lappano R, Cirillo F, Guzzi R, Garofalo A, Jacquot Y, Maggiolini M, Rizzuti B. 2020. Computational approaches for the discovery of GPER targeting compounds. Front Endocrinol. 11:517.
  • Gu L, Ye P, Li H, Wang Y, Xu Y, Tian Q, Lei G, Zhao C, Gao Z, Zhao W, et al. 2019. Lunasin attenuates oxidant-induced endothelial injury and inhibits atherosclerotic plaque progression in ApoE–/– mice by up-regulating heme oxygenase-1 via PI3K/Akt/Nrf2/ARE pathway. FASEB J. 33(4):4836–4850.
  • Han G, Li F, Yu X, White RE. 2013. GPER: a novel target for non-genomic estrogen action in the cardiovascular system. Pharmacol Res. 71:53–60.
  • Hu H, Wang C, Jin Y, Meng Q, Liu Q, Liu Z, Liu K, Liu X, Sun H. 2019. Catalpol inhibits homocysteine-induced oxidation and inflammation via inhibiting Nox4/NF-κB and GRP78/PERK pathways in human aorta endothelial cells. Inflammation. 42(1):64–80.
  • Huang D, Jia Z, Chang L, Zhou H, Wu X, Wei C. 2020. The role of collateral disease theory in the prevention and treatment of atherosclerosis in post-menopausal women: a narrative review. Ann Palliat Med. 9(4):2314–2322.
  • Hwang YP, Jeong HG. 2010. Ginsenoside Rb1 protects against 6-hydroxydopamine-induced oxidative stress by increasing heme oxygenase-1 expression through an estrogen receptor-related PI3K/Akt/Nrf2-dependent pathway in human dopaminergic cells. Toxicol Appl Pharmacol. 242(1):18–28.
  • Jian X, Liu Y, Zhao Z, Zhao L, Wang D, Liu Q. 2019. The role of traditional Chinese medicine in the treatment of atherosclerosis through the regulation of macrophage activity. Biomed Pharmacother. 118:109375.
  • Jing Y, Cai D, Chen Q, Xiong Q, Hu T, Yao Y, Lin C, Sun X, Lu Y, Kong X, et al. 2017. Liuwei Dihuang soft capsules attenuates endothelial cell apoptosis to prevent atherosclerosis through GPR30-mediated regulation in ovariectomized ApoE-deficient mice. J Ethnopharmacol. 208:185–198.
  • Kattoor AJ, Kanuri SH, Mehta JL. 2019. Role of Ox-LDL and LOX-1 in atherogenesis. Curr Med Chem. 26(9):1693–1700.
  • Kim TW, Lee SY, Kim M, Cheon C, Ko SG. 2018. Kaempferol induces autophagic cell death via IRE1-JNK-CHOP pathway and inhibition of G9a in gastric cancer cells. Cell Death Dis. 9(9):875.
  • Kirichenko TV, Myasoedova VA, Orekhova VA, Ravani AL, Nikitina NA, Grechko AV, Sobenin IA, Orekhov AN. 2017. Phytoestrogen-rich natural preparation for treatment of climacteric syndrome and atherosclerosis prevention in perimenopausal women. Phytother Res. 31(8):1209–1214.
  • Kiyama R. 2017. Estrogenic potentials of traditional Chinese medicine. Am J Chin Med. 45(7):1365–1399.
  • Lagari VS, Levis S. 2013. Phytoestrogens in the prevention of postmenopausal bone loss. J Clin Densitom. 16(4):445–449.
  • Langasco R, Fancello S, Rassu G, Cossu M, Cavalli R, Galleri G, Giunchedi P, Migheli R, Gavini E. 2019. Increasing protective activity of genistein by loading into transfersomes: a new potential adjuvant in the oxidative stress-related neurodegenerative diseases? Phytomedicine. 52:23–31.
  • Lee YT, Lin HY, Chan YW, Li KH, To OT, Yan BP, Liu T, Li G, Wong WT, Keung W, et al. 2017. Mouse models of atherosclerosis: a historical perspective and recent advances. Lipids Health Dis. 16(1):12.
  • Li TT, Wang ZB, Li Y, Cao F, Yang BY, Kuang HX. 2019. The mechanisms of traditional Chinese medicine underlying the prevention and treatment of atherosclerosis. Chin J Nat Med. 17(6):401–412.
  • Malekmohammad K, Sewell RDE, Rafieian-Kopaei M. 2019. Antioxidants and atherosclerosis: mechanistic aspects. Biomolecules. 9:301.
  • McClelland RL, Jorgensen NW, Budoff M, Blaha MJ, Post WS, Kronmal RA, Bild DE, Shea S, Liu K, Watson KE, et al. 2015. 10-Year coronary heart disease risk prediction using coronary artery calcium and traditional risk factors: derivation in the MESA (multi-ethnic study of atherosclerosis) with validation in the HNR (Heinz Nixdorf Recall) study and the DHS (Dallas Heart Study). J Am Coll Cardiol. 66(15):1643–1653.
  • Morselli E, Santos RS, Criollo A, Nelson MD, Palmer BF, Clegg DJ. 2017. The effects of oestrogens and their receptors on cardiometabolic health. Nat Rev Endocrinol. 13(6):352–364.
  • Morselli E, Santos RS, Gao S, Ávalos Y, Criollo A, Palmer BF, Clegg DJ. 2018. Impact of estrogens and estrogen receptor-α in brain lipid metabolism. Am J Physiol Endocrinol Metab. 315(1):E7–E14.
  • Mu PW, Jiang P, Wang MM, Chen YM, Zheng SH, Tan Z, Jiang W, Zeng LY, Wang TH. 2016. Oestrogen exerts anti-inflammation via p38 MAPK/NF-κB cascade in adipocytes. Obes Res Clin Pract. 10(6):633–641.
  • Okuyama H, Langsjoen PH, Hamazaki T, Ogushi Y, Hama R, Kobayashi T, Uchino H. 2015. Statins stimulate atherosclerosis and heart failure: pharmacological mechanisms. Expert Rev Clin Pharmacol. 8(2):189–199.
  • Peiffer DS, Ma E, Wyatt D, Albain KS, Osipo C. 2020. DAXX-inducing phytoestrogens inhibit ER + tumor initiating cells and delay tumor development. NPJ Breast Cancer. 6:37.
  • Petri MH, Laguna-Fernandez A, Arnardottir H, Wheelock CE, Perretti M, Hansson GK, Bäck M. 2017. Aspirin-triggered lipoxin A4 inhibits atherosclerosis progression in apolipoprotein E–/– mice. Br J Pharmacol. 174(22):4043–4054.
  • Pollard KJ, Daniel JM. 2019. Nuclear estrogen receptor activation by insulin-like growth factor-1 in neuro-2A neuroblastoma cells requires endogenous estrogen synthesis and is mediated by mutually repressive MAPK and PI3K cascades. Mol Cell Endocrinol. 490:68–79.
  • Reddy NM, Potteti HR, Vegiraju S, Chen HJ, Tamatam CM, Reddy SP. 2015. PI3K-AKT signaling via Nrf2 protects against hyperoxia-induced acute lung injury, but promotes inflammation post-injury independent of Nrf2 in mice. PLOS One. 10(6):e0129676.
  • Schierbeck L. 2015. Primary prevention of cardiovascular disease with hormone replacement therapy. Climacteric. 18(4):492–497.
  • Sharma D, Gondaliya P, Tiwari V, Kalia K. 2019. Kaempferol attenuates diabetic nephropathy by inhibiting RhoA/Rho-kinase mediated inflammatory signalling. Biomed Pharmacother. 109:1610–1619.
  • Thangapandiyan S, Ramesh M, Hema T, Miltonprabu S, Uddin MS, Nandhini V, Bavithra Jothi G. 2019. Sulforaphane potentially ameliorates arsenic induced hepatotoxicity in albino wistar rats: implication of PI3K/Akt/Nrf2 signaling pathway. Cell Physiol Biochem. 52:1203–1222.
  • Torres-Villarreal D, Camacho A, Castro H, Ortiz-Lopez R, de la Garza AL. 2019. Anti-obesity effects of kaempferol by inhibiting adipogenesis and increasing lipolysis in 3T3-L1 cells. J Physiol Biochem. 75(1):83–88.
  • Wang C, Niimi M, Watanabe T, Wang Y, Liang J, Fan J. 2018. Treatment of atherosclerosis by traditional Chinese medicine: questions and quandaries. Atherosclerosis. 277:136–144.
  • Wang X, Jia W, Zhao A, Wang X. 2006. Anti-influenza agents from plants and traditional Chinese medicine. Phytother Res. 20(5):335–341.
  • Wu P, Meng X, Zheng H, Zeng Q, Chen T, Wang W, Zhang X, Su J. 2018. Kaempferol attenuates ROS-induced hemolysis and the molecular mechanism of its induction of apoptosis on bladder cancer. Molecules. 23:2592.
  • Xiong Y, Zhao B, Zhang W, Jia L, Zhang Y, Xu X. 2020. Curcumin promotes osteogenic differentiation of periodontal ligament stem cells through the PI3K/AKT/Nrf2 signaling pathway. Iran J Basic Med Sci. 23(7):954–960.
  • Xu YP, Han F, Tan J. 2017. Edaravone protects the retina against ischemia/reperfusion-induced oxidative injury through the PI3K/Akt/Nrf2 pathway. Mol Med Rep. 16(6):9210–9216.
  • Yang K, Zhang H, Luo Y, Zhang J, Wang M, Liao P, Cao L, Guo P, Sun G, Sun X. 2017. Gypenoside XVII prevents atherosclerosis by attenuating endothelial apoptosis and oxidative stress: insight into the ERα-mediated PI3K/Akt pathway. Int J Mol Sci. 18:77.
  • Yang Q, Wang C, Jin Y, Ma X, Xie T, Wang J, Liu K, Sun H. 2019. Disocin prevents postmenopausal atherosclerosis in ovariectomized LDLR–/– mice through a PGC-1α/ERα pathway leading to promotion of autophagy and inhibition of oxidative stress, inflammation and apoptosis. Pharmacol Res. 148:104414.
  • Zhang G, Wang Q, Zhou Q, Wang R, Xu M, Wang H, Wang L, Wilcox CS, Liu R, Lai EY. 2016. Protective effect of tempol on acute kidney injury through PI3K/Akt/Nrf2 signaling pathway. Kidney Blood Press Res. 41(2):129–138.
  • Zhang K, Zhang Y, Zhang M, Gu L, Liu Z, Jia J, Chen X. 2016. Effects of phospholipid complexes of total flavonoids from persimmon (Diospyros kaki L.) leaves on experimental atherosclerosis rats. J Ethnopharmacol. 191:245–253.
  • Zhong X, Zhang L, Li Y, Li P, Li J, Cheng G. 2018. Kaempferol alleviates ox-LDL-induced apoptosis by up-regulation of miR-26a-5p via inhibiting TLR4/NF-κB pathway in human endothelial cells. Biomed Pharmacother. 108:1783–1789.
  • Zhu Q, Kang J, Xu G, Li J, Zhou H, Liu Y. 2020. Traditional Chinese medicine Shenqi compound to improve lower extremity atherosclerosis of patients with type 2 diabetes by affecting blood glucose fluctuation: study protocol for a randomized controlled multicenter trial. Medicine. 99(11):e19501.