Chicoric acid attenuates hyperglycemia-induced endothelial dysfunction through AMPK-dependent inhibition of oxidative/nitrative stresses

References

• Mancini GBJ, Cheng AY, Connelly K, et al. CardioDiabetes: core competencies for cardiovascular clinicians in a rapidly evolving era of type 2 diabetes management. Can J Cardiol. 2018;34(10):1350–1361.
   PubMed Web of Science ®Google Scholar
• Mancini GB, Cheng AY, Connelly K, et al. Diabetes for cardiologists: practical issues in diagnosis and management. Can J Cardiol. 2017;33(3):366–377.
   PubMed Web of Science ®Google Scholar
• Ovalle F. Cardiovascular implications of antihyperglycemic therapies for type 2 diabetes. Clin Ther. 2011;33(4):393–407.
   PubMed Web of Science ®Google Scholar
• Fitchett D, Cheng A, Connelly K, et al. A practical guide to the use of glucose-lowering agents with cardiovascular benefit or proven safety. Can J Cardiol. 2017;33(7):940–942.
   PubMed Web of Science ®Google Scholar
• Sun HJ, Wu ZY, Nie XW, et al. Role of endothelial dysfunction in cardiovascular diseases: the link between inflammation and hydrogen sulfide. Front Pharmacol. 2019;10:1568.
   PubMed Web of Science ®Google Scholar
• Gliemann L, Nyberg M, Hellsten Y. Nitric oxide and reactive oxygen species in limb vascular function: what is the effect of physical activity? Free Radic Res. 2014;48(1):71–83.
   PubMed Web of Science ®Google Scholar
• Schulman IH, Zhou MS, Raij L. Interaction between nitric oxide and angiotensin II in the endothelium: role in atherosclerosis and hypertension. J Hypertension Suppl. 2006;24(1):S45–S50.
   PubMedGoogle Scholar
• Sena CM, Pereira AM, Seiça R. Endothelial dysfunction - a major mediator of diabetic vascular disease. Biochim Biophys Acta. 2013;1832(12):2216–2231.
   PubMed Web of Science ®Google Scholar
• Paneni F, Beckman JA, Creager MA, et al. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J. 2013;34(31):2436–2443.
   PubMed Web of Science ®Google Scholar
• Tsai KL, Kao CL, Hung CH, et al. Chicoric acid is a potent anti-atherosclerotic ingredient by anti-oxidant action and anti-inflammation capacity. Oncotarget. 2017;8(18):29600–29612.
   PubMedGoogle Scholar
• Schlernitzauer A, Oiry C, Hamad R, et al. Chicoric acid is an antioxidant molecule that stimulates AMP kinase pathway in L6 myotubes and extends lifespan in Caenorhabditis elegans. PloS One. 2013;8(11):e78788.
   PubMed Web of Science ®Google Scholar
• Lu QB, Wan MY, Wang PY, et al. Chicoric acid prevents PDGF-BB-induced VSMC dedifferentiation, proliferation and migration by suppressing ROS/NFκB/mTOR/P70S6K signaling cascade. Redox Biol. 2018;14:656–668.
   PubMed Web of Science ®Google Scholar
• Landmann M, Kanuri G, Spruss A, et al. Oral intake of chicoric acid reduces acute alcohol-induced hepatic steatosis in mice. Nutrition. 2014;30(7–8):882–889.
   PubMed Web of Science ®Google Scholar
• Liu Q, Chen Y, Shen C, et al. Chicoric acid supplementation prevents systemic inflammation-induced memory impairment and amyloidogenesis via inhibition of NF-κB. FASEB J. 2017;31(4):1494–1507.
   PubMed Web of Science ®Google Scholar
• Azay-Milhau J, Ferrare K, Leroy J, et al. Antihyperglycemic effect of a natural chicoric acid extract of chicory (Cichorium intybus L.): a comparative in vitro study with the effects of caffeic and ferulic acids. J Ethnopharmacol. 2013;150(2):755–760.
   PubMed Web of Science ®Google Scholar
• Lu QB, Du Q, Wang HP, et al. Salusin-β mediates tubular cell apoptosis in acute kidney injury: involvement of the PKC/ROS signaling pathway. Redox Biol. 2020;30:101411.
   PubMed Web of Science ®Google Scholar
• Zhang M, Wang S, Pan Z, et al. AMPK/NF-κB signaling pathway regulated by ghrelin participates in the regulation of HUVEC and THP1 Inflammation. Mol Cell Biochem. 2018;437(1–2):45–53.
   PubMed Web of Science ®Google Scholar
• Garcia-Morales V, Luaces-Regueira M, Campos-Toimil M. The cAMP effectors PKA and Epac activate endothelial NO synthase through PI3K/Akt pathway in human endothelial cells. Biochem Pharmacol. 2017;145:94–101.
   PubMed Web of Science ®Google Scholar
• Zhu D, Wang H, Zhang J, et al. Irisin improves endothelial function in type 2 diabetes through reducing oxidative/nitrative stresses. J Mol Cell Cardiol. 2015;87:138–147.
   PubMed Web of Science ®Google Scholar
• Sun HJ, Chen D, Wang PY, et al. Salusin-β is involved in diabetes mellitus-induced endothelial dysfunction via degradation of peroxisome proliferator-activated receptor gamma. Oxid Med Cell Longev. 2017;2017:6905217.
   PubMed Web of Science ®Google Scholar
• Hao Y, Liu HM, Wei X, et al. Diallyl trisulfide attenuates hyperglycemia-induced endothelial apoptosis by inhibition of Drp1-mediated mitochondrial fission. Acta Diabetol. 2019;56(11):1177–1189.
   PubMed Web of Science ®Google Scholar
• Cui J, Li Z, Zhuang S, et al. Melatonin alleviates inflammation-induced apoptosis in human umbilical vein endothelial cells via suppression of Ca2+-XO-ROS-Drp1-mitochondrial fission axis by activation of AMPK/SERCA2a pathway. Cell Stress Chaperones. 2018;23(2):281–293.
   PubMed Web of Science ®Google Scholar
• Sun HJ, Zhao MX, Ren XS, et al. Salusin-β promotes vascular smooth muscle cell migration and intimal hyperplasia after vascular injury via ROS/NFκB/MMP-9 pathway. Antioxid Redox Signal. 2016;24(18):1045–1057.
   PubMed Web of Science ®Google Scholar
• Sun H, Zhang F, Xu Y, et al. Salusin-β promotes vascular calcification via nicotinamide adenine dinucleotide phosphate/reactive oxygen species-mediated klotho downregulation. Antioxid Redox Signal. 2019;31(18):1352–1370.
   PubMed Web of Science ®Google Scholar
• Haarmann A, Nehen M, Deiß A, et al. Fumaric acid esters do not reduce inflammatory NF-κB/p65 nuclear translocation, ICAM-1 expression and T-cell adhesiveness of human brain microvascular endothelial cells. Int J Mol Sci. 2015;16(8):19086–19095.
   PubMed Web of Science ®Google Scholar
• Wang L, Cao Y, Gorshkov B, et al. Ablation of endothelial Pfkfb3 protects mice from acute lung injury in LPS-induced endotoxemia. Pharmacol Res. 2019;146:104292.
   PubMed Web of Science ®Google Scholar
• Sun HJ, Xiong SP, Wu ZY, et al. Induction of caveolin-3/eNOS complex by nitroxyl (HNO) ameliorates diabetic cardiomyopathy. Redox Biol. 2020;32:101493.
   PubMed Web of Science ®Google Scholar
• Jiang X, Wang X. Cytochrome C-mediated apoptosis. Annu Rev Biochem. 2004;73:87–106.
   PubMed Web of Science ®Google Scholar
• Uthman L, Baartscheer A, Schumacher CA, et al. Direct cardiac actions of sodium glucose cotransporter 2 inhibitors target pathogenic mechanisms underlying heart failure in diabetic patients. Front Physiol. 2018;9:1575.
   PubMed Web of Science ®Google Scholar
• Atawia RT, Bunch KL, Toque HA, et al. Mechanisms of obesity-induced metabolic and vascular dysfunctions. Front Biosci. 2019;24:890–934.
   Web of Science ®Google Scholar
• Lindsey KQ, Caughman SW, Olerud JE, et al. Neural regulation of endothelial cell-mediated inflammation. J Investig Dermatol Symp Proc. 2000;5(1):74–78.
   PubMedGoogle Scholar
• Hsu CP, Lin CH, Kuo CY. Endothelial-cell inflammation and damage by reactive oxygen species are prevented by propofol via ABCA1-mediated cholesterol efflux. Int J Med Sci. 2018;15(10):978–985.
   PubMed Web of Science ®Google Scholar
• Huang W, Huang M, Ouyang H, et al. Oridonin inhibits vascular inflammation by blocking NF-κB and MAPK activation. Eur J Pharmacol. 2018;826:133–139.
   PubMed Web of Science ®Google Scholar
• Li R, Wang WQ, Zhang H, et al. Adiponectin improves endothelial function in hyperlipidemic rats by reducing oxidative/nitrative stress and differential regulation of eNOS/iNOS activity. Am J Physiol Endocrinol Metabol. 2007;293(6):E1703–E1708.
   PubMed Web of Science ®Google Scholar
• Konior A, Schramm A, Czesnikiewicz-Guzik M, et al. NADPH oxidases in vascular pathology. Antioxid Redox Signal. 2014;20(17):2794–2814.
   PubMed Web of Science ®Google Scholar
• Creager MA, Lüscher TF, Cosentino F, et al. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Circulation. 2003;108(12):1527–1532.
   PubMed Web of Science ®Google Scholar
• Lerman A, Zeiher AM. Endothelial function: cardiac events. Circulation. 2005;111(3):363–368.
   PubMed Web of Science ®Google Scholar
• Vanhoutte PM, Shimokawa H, Feletou M, et al. Endothelial dysfunction and vascular disease - a 30th anniversary update. Acta Physiol. 2017;219(1):22–96.
   PubMed Web of Science ®Google Scholar
• Xie L, Feng H, Li S, et al. SIRT3 mediates the antioxidant effect of hydrogen sulfide in endothelial cells. Antioxid Redox Signal. 2016;24(6):329–343.
   PubMed Web of Science ®Google Scholar
• Tao L, Liu HR, Gao E, et al. Antioxidative, antinitrative, and vasculoprotective effects of a peroxisome proliferator-activated receptor-gamma agonist in hypercholesterolemia. Circulation. 2003;108(22):2805–2811.
   PubMed Web of Science ®Google Scholar
• Wang D, Luo P, Wang Y, et al. Glucagon-like peptide-1 protects against cardiac microvascular injury in diabetes via a cAMP/PKA/Rho-dependent mechanism. Diabetes. 2013;62(5):1697–1708.
   PubMed Web of Science ®Google Scholar
• Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87(1):245–313.
   PubMed Web of Science ®Google Scholar
• Lu Q, Li X, Liu J, et al. AMPK is associated with the beneficial effects of antidiabetic agents on cardiovascular diseases. Bioscience Reports. 2019;39(2):BSR20181995.
   PubMedGoogle Scholar
• Li Z, Feng H, Han L, et al. Chicoric acid ameliorate inflammation and oxidative stress in Lipopolysaccharide and d-galactosamine induced acute liver injury. J Cell Mol Med. 2020;24(5):3022–3033.
   PubMed Web of Science ®Google Scholar
• Sadeghabadi ZA, Ziamajidi N, Abbasalipourkabir R, et al. Palmitate-induced IL6 expression ameliorated by chicoric acid through AMPK and SIRT1-mediated pathway in the PBMCs of newly diagnosed type 2 diabetes patients and healthy subjects. Cytokine. 2019;116:106–114.
   PubMed Web of Science ®Google Scholar
• Zhu X, Zhou Y, Cai W, et al. Salusin-β mediates high glucose-induced endothelial injury via disruption of AMPK signaling pathway. Biochem Biophys Res Commun. 2017;491(2):515–521.
   PubMed Web of Science ®Google Scholar
• Dong Y, Fernandes C, Liu Y, et al. Role of endoplasmic reticulum stress signalling in diabetic endothelial dysfunction and atherosclerosis. Diab Vasc Dis Res. 2017;14(1):14–23.
   PubMed Web of Science ®Google Scholar
• Roy S. Caspases at the heart of the apoptotic cell death pathway. Chem Res Toxicol. 2000;13(10):961–962.
   PubMed Web of Science ®Google Scholar
• Cai L, Li W, Wang G, et al. Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes. 2002;51(6):1938–1948.
   PubMed Web of Science ®Google Scholar
• Han X, Wang B, Sun Y, et al. Metformin modulates high glucose-incubated human umbilical vein endothelial cells proliferation and apoptosis through AMPK/CREB/BDNF pathway. Front Pharmacol. 2018;9:1266.
   PubMed Web of Science ®Google Scholar
• Song H, Wu F, Zhang Y, et al. Irisin promotes human umbilical vein endothelial cell proliferation through the ERK signaling pathway and partly suppresses high glucose-induced apoptosis. PloS One. 2014;9(10):e110273.
   PubMed Web of Science ®Google Scholar
• Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281(5381):1309–1312.
   PubMed Web of Science ®Google Scholar
• Baynes JW, Thorpe SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes. 1999;48(1):1–9.
   PubMed Web of Science ®Google Scholar
• Wang GW, Kang YJ. Inhibition of doxorubicin toxicity in cultured neonatal mouse cardiomyocytes with elevated metallothionein levels. J Pharmacol Exper Ther. 1999;288(3):938–944.
   PubMed Web of Science ®Google Scholar
• Wang GW, Klein JB, Kang YJ. Metallothionein inhibits doxorubicin-induced mitochondrial cytochrome c release and caspase-3 activation in cardiomyocytes. J Pharmacol Exp Ther. 2001;298(2):461–468.
   PubMed Web of Science ®Google Scholar
• Wu M-Y, Yiang G-T, Lai T-T, et al. The oxidative stress and mitochondrial dysfunction during the pathogenesis of diabetic retinopathy. Oxid Med Cell Longev. 2018;2018:3420187.
   PubMed Web of Science ®Google Scholar
• Knapp M, Tu X, Wu R. Vascular endothelial dysfunction, a major mediator in diabetic cardiomyopathy. Acta Pharmacol Sin. 2019;40(1):1–8.
   PubMed Web of Science ®Google Scholar
• Widlansky ME, Hill RB. Mitochondrial regulation of diabetic vascular disease: an emerging opportunity. Transl Res. 2018;202:83–98.
   PubMed Web of Science ®Google Scholar
• Yu L, Liang Q, Zhang W, et al. HSP22 suppresses diabetes-induced endothelial injury by inhibiting mitochondrial reactive oxygen species formation. Redox Biol. 2019;21:101095.
   PubMed Web of Science ®Google Scholar
• Sun HJ, Hou B, Wang X, et al. Endothelial dysfunction and cardiometabolic diseases: role of long non-coding RNAs. Life Sci. 2016;167:6–11.
   PubMed Web of Science ®Google Scholar
• Zhang HN, Xu QQ, Thakur A, et al. Endothelial dysfunction in diabetes and hypertension: role of microRNAs and long non-coding RNAs. Life Sci. 2018;213:258–268.
   PubMed Web of Science ®Google Scholar
• Quintela AM, Jiménez R, Gómez-Guzmán M, et al. Activation of peroxisome proliferator-activated receptor-β/-δ (PPARβ/δ) prevents endothelial dysfunction in type 1 diabetic rats. Free Radic Biol Med. 2012;53(4):730–741.
   PubMed Web of Science ®Google Scholar
• Leonard A, Rahman A, Fazal F. Importins α and β signaling mediates endothelial cell inflammation and barrier disruption. Cell Signal. 2018;44:103–117.
   PubMed Web of Science ®Google Scholar
• Wang F, Zou Z, Gong Y, et al. Regulation of human brain microvascular endothelial cell adhesion and barrier functions by memantine. J Mol Neurosci. 2017;62(1):123–129.
   PubMed Web of Science ®Google Scholar
• Langouche L, Vanhorebeek I, Vlasselaers D, et al. Intensive insulin therapy protects the endothelium of critically ill patients. J Clin Invest. 2005;115(8):2277–2286.
   PubMed Web of Science ®Google Scholar
• Shrikanth CB, Nandini CD. AMPK in microvascular complications of diabetes and the beneficial effects of AMPK activators from plants. Phytomed: Int J Phytother Phytopharmacol. 2020;73:152808.
   PubMed Web of Science ®Google Scholar
• Joshi T, Singh AK, Haratipour P, et al. Targeting AMPK signaling pathway by natural products for treatment of diabetes mellitus and its complications. J Cell Physiol. 2019;234(10):17212–17231.
   PubMed Web of Science ®Google Scholar
• Liu Q, Fang J, Chen P, et al. Chicoric acid improves neuron survival against inflammation by promoting mitochondrial function and energy metabolism. Food Funct. 2019;10(9):6157–6169.
   PubMed Web of Science ®Google Scholar
• Gao P, Li L, Wei X, et al. Activation of transient receptor potential channel vanilloid 4 by DPP-4 (dipeptidyl peptidase-4) inhibitor vildagliptin protects against diabetic endothelial dysfunction. Hypertension. 2020;75(1):150–162.
   PubMed Web of Science ®Google Scholar
• Taguchi K, Tano I, Kaneko N, et al. Plant polyphenols morin and quercetin rescue nitric oxide production in diabetic mouse aorta through distinct pathways. Biomed Pharmacother. 2020;129:110463.
   PubMed Web of Science ®Google Scholar
• Hu R, Wang MQ, Ni SH, et al. Salidroside ameliorates endothelial inflammation and oxidative stress by regulating the AMPK/NF-κB/NLRP3 signaling pathway in AGEs-induced HUVECs. Eur J Pharmacol. 2020;867:172797.
   PubMed Web of Science ®Google Scholar
• Xu F, Liu Y, Zhu X, et al. Protective effects and mechanisms of vaccarin on vascular endothelial dysfunction in diabetic angiopathy. IJMS. 2019;20(18):4587.
   Google Scholar