High-density lipoprotein protects vascular endothelial cells from indoxyl sulfate insults through its antioxidant ability

References

• Foley RN, Parfrey PS, Sarnak MJ. Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J Kidney Dis. 1998 Nov;32(5 Suppl 3):S112–9. PubMed PMID: 9820470. doi: 10.1053/ajkd.1998.v32.pm9820470
   PubMed Web of Science ®Google Scholar
• Subbiah AK, Chhabra YK, Mahajan S. Cardiovascular disease in patients with chronic kidney disease: a neglected subgroup. Heart Asia. 2016;8(2):56–61. PubMed PMID: 27933104; PubMed Central PMCID: PMCPMC5133395. doi: 10.1136/heartasia-2016-010809
   PubMed Web of Science ®Google Scholar
• Tornavaca O, Chia M, Dufton N, et al. ZO-1 controls endothelial adherens junctions, cell-cell tension, angiogenesis, and barrier formation. J Cell Bio. 2015 Mar 16;208(6): 821–838. PubMed PMID: 25753039; PubMed Central PMCID: PMCPMC4362456. doi: 10.1083/jcb.201404140
   PubMed Web of Science ®Google Scholar
• Wakamatsu T, Yamamoto S, Ito T, et al. Indoxyl sulfate promotes macrophage IL-1β production by activating Aryl hydrocarbon receptor/NF-κ/MAPK cascades, but the NLRP3 inflammasome was not activated. Toxins (Basel). 2018 Mar 15;10(3): 124. PubMed PMID: 29543732; PubMed Central PMCID: PMCPMC5869412. eng. doi: 10.3390/toxins10030124
   PubMed Web of Science ®Google Scholar
• Barreto FC, Barreto DV, Liabeuf S, et al. Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin J Am Soc Nephrol. 2009 Oct;4(10):1551–8. PubMed PMID: 19696217; PubMed Central PMCID: PMCPMC2758258. doi: 10.2215/CJN.03980609
   PubMed Web of Science ®Google Scholar
• Duranton F, Cohen G, De Smet R, et al. Normal and pathologic concentrations of uremic toxins. J Am Soc Nephrol. 2012 Jul;23(7):1258–70. PubMed PMID: 22626821; PubMed Central PMCID: PMCPMC3380651. doi: 10.1681/ASN.2011121175
   PubMed Web of Science ®Google Scholar
• Niwa T, Nomura T, Sugiyama S, et al. The protein metabolite hypothesis, a model for the progression of renal failure: an oral adsorbent lowers indoxyl sulfate levels in undialyzed uremic patients. Kidney Int Suppl. 1997 Nov;62:S23–8. PubMed PMID: 9350673
   PubMed Web of Science ®Google Scholar
• Six I, Gross P, Rémond MC, et al. Deleterious vascular effects of indoxyl sulfate and reversal by oral adsorbent AST-120. Atherosclerosis. 2015 Nov;243(1):248–56. PubMed PMID: 26408929; eng. doi: 10.1016/j.atherosclerosis.2015.09.019
   PubMed Web of Science ®Google Scholar
• Dou L, Bertrand E, Cerini C, et al. The uremic solutes p-cresol and indoxyl sulfate inhibit endothelial proliferation and wound repair. Kidney Int. 2004 Feb;65(2):442–51. PubMed PMID: 14717914. doi: 10.1111/j.1523-1755.2004.00399.x
   PubMed Web of Science ®Google Scholar
• Wu VC, Young GH, Huang PH, et al. In acute kidney injury, indoxyl sulfate impairs human endothelial progenitor cells: modulation by statin. Angiogenesis. 2013 Jul;16(3):609–24. PubMed PMID: 23408148; eng. doi: 10.1007/s10456-013-9339-8
   PubMed Web of Science ®Google Scholar
• Hung SC, Kuo KL, Huang HL, et al. Indoxyl sulfate suppresses endothelial progenitor cell-mediated neovascularization. Kidney Int. 2016 Mar;89(3):574–585. PubMed PMID: 26880454; eng. doi: 10.1016/j.kint.2015.11.020
   PubMed Web of Science ®Google Scholar
• Carmona A, Guerrero F, Buendia P, et al. Microvesicles derived from indoxyl sulfate treated endothelial cells induce endothelial progenitor cells dysfunction. Front Physiol. 2017;8:666. PubMed PMID: 28951723; PubMed Central PMCID: PMCPMC5599774. doi: 10.3389/fphys.2017.00666
   PubMed Web of Science ®Google Scholar
• Assmann G, Gotto AM Jr. HDL cholesterol and protective factors in atherosclerosis. Circulation. 2004 Jun 15; 109(23 Suppl 1): PubMed PMID: 15198960:III8–14. doi: 10.1161/01.CIR.0000131512.50667.46
   PubMed Web of Science ®Google 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 PMID: 30013438; PubMed Central PMCID: PMCPMC6036153. doi: 10.7150/ijms.24659
   PubMed Web of Science ®Google Scholar
• Besler C, Heinrich K, Rohrer L, et al. Mechanisms underlying adverse effects of HDL on eNOS-activating pathways in patients with coronary artery disease. J Clin Invest. 2011 Jul;121(7):2693–708. PubMed PMID: 21701070; PubMed Central PMCID: PMCPMC3223817. doi: 10.1172/JCI42946
   PubMed Web of Science ®Google Scholar
• Huang CY, Lin FY, Shih CM, et al. Moderate to high concentrations of high-density lipoprotein from healthy subjects paradoxically impair human endothelial progenitor cells and related angiogenesis by activating Rho-associated kinase pathways. Arterioscler Thromb Vasc Biol. 2012 Oct;32(10):2405–17. PubMed PMID: 22904272; eng. doi: 10.1161/atvbaha.112.248617
   PubMed Web of Science ®Google Scholar
• Smith JD. Dysfunctional HDL as a diagnostic and therapeutic target. Arterioscler Thromb Vas Biol. 2010 Feb;30(2):151–155. PubMed PMID: 19679832; PubMed Central PMCID: PMCPMC2809786. eng. doi: 10.1161/atvbaha.108.179226
   PubMed Web of Science ®Google Scholar
• Rosenson RS, Brewer HB Jr., Ansell BJ, et al. Dysfunctional HDL and atherosclerotic cardiovascular disease. Nat Rev Cardiol. 2016 Jan;13(1):48–60. PubMed PMID: 26323267; PubMed Central PMCID: PMCPMC6245940. eng. doi: 10.1038/nrcardio.2015.124
   PubMed Web of Science ®Google Scholar
• Holy EW, Besler C, Reiner MF, et al. High-density lipoprotein from patients with coronary heart disease loses anti-thrombotic effects on endothelial cells: impact on arterial thrombus formation. Thromb Haemost. 2014 Nov;52(11):1024–1035. PubMed PMID: 25056722; eng. doi: 10.1160/th13-09-0775
   Google Scholar
• Taki K, Tsuruta Y, Niwa T. Indoxyl sulfate and atherosclerotic risk factors in hemodialysis patients. Am J Nephrol. 2007;27(1):30–35. PubMed PMID: 17215572; eng. doi: 10.1159/000098542
   PubMed Web of Science ®Google Scholar
• Kronenberg F. HDL in CKD-The devil is in the detail. J Am Soc Nephrol. 2018 May;29(5):1356–1371. PubMed PMID: 29472417; PubMed Central PMCID: PMCPMC5967756. eng. doi: 10.1681/asn.2017070798
   PubMed Web of Science ®Google Scholar
• Rysz J, Gluba-Brzózka A, Rysz-Górzyńska M, et al. The role and function of HDL in patients with chronic kidney disease and the risk of cardiovascular disease. Int J Mol Sci. 2020 Jan 17;21(2): PubMed PMID: 31963445; PubMed Central PMCID: PMCPMC7014265. eng. doi: 10.3390/ijms21020601
   Web of Science ®Google Scholar
• Nieuwdorp M, Vergeer M, Bisoendial RJ, et al. Reconstituted HDL infusion restores endothelial function in patients with type 2 diabetes mellitus. Diabetologia. 2008 Jun;51(6):1081–4. PubMed PMID: 18389214; PubMed Central PMCID: PMCPMC2362135. eng. doi: 10.1007/s00125-008-0975-2
   PubMed Web of Science ®Google Scholar
• Nicholls SJ, Dusting GJ, Cutri B, et al. Reconstituted high-density lipoproteins inhibit the acute pro-oxidant and proinflammatory vascular changes induced by a periarterial collar in normocholesterolemic rabbits. Circulation. 2005 Mar 29;111(12):1543–50. PubMed PMID: 15781735; eng. doi: 10.1161/01.Cir.0000159351.95399.50
   PubMed Web of Science ®Google Scholar
• Levkau B, Hermann S, Theilmeier G, et al. High-density lipoprotein stimulates myocardial perfusion in vivo. Circulation. 2004 Nov 23;110(21):3355–9. PubMed PMID: 15545521; eng. doi: 10.1161/01.Cir.0000147827.43912.Ae
   PubMed Web of Science ®Google Scholar
• Chang TT, Chen JW. Hydralazine improves ischemia-induced neovasculogenesis via xanthine-oxidase inhibition in chronic renal insufficiency. Pharmacol Res. 2020 Jan;151:104509. PubMed PMID: 31678640: doi: 10.1016/j.phrs.2019.104509
   PubMed Web of Science ®Google Scholar
• Lin CJ, Chen HH, Pan CF, et al. P-cresylsulfate and indoxyl sulfate level at different stages of chronic kidney disease. J Clin Lab Analysis. 2011;25(3):191–7. PubMed PMID: 21567467; PubMed Central PMCID: PMCPMC6647585. eng. doi: 10.1002/jcla.20456
   PubMed Web of Science ®Google Scholar
• Stinghen AE, Chillon JM, Massy ZA, et al. Differential effects of indoxyl sulfate and inorganic phosphate in a murine cerebral endothelial cell line (bEnd.3). Toxins (Basel). 2014 Jun 4;6(6):1742–60. PubMed PMID: 24902077; PubMed Central PMCID: PMCPMC4073127. eng. doi: 10.3390/toxins6061742
   PubMed Web of Science ®Google Scholar
• de Giorgis T, Marcovecchio ML, Di Giovanni I, et al. Triglycerides-to-HDL ratio as a new marker of endothelial dysfunction in obese prepubertal children. Eur J Endocrinol. 2014 Feb;170(2):173–180. PubMed PMID: 24165018. doi: 10.1530/EJE-13-0452
   PubMed Web of Science ®Google Scholar
• Hedrick CC, Thorpe SR, Fu MX, et al. Glycation impairs high-density lipoprotein function. Diabetologia. 2000 Mar;43(3):312–20. PubMed PMID: 10768092; eng. doi: 10.1007/s001250050049
   PubMed Web of Science ®Google Scholar
• Femlak M, Gluba-Brzózka A, Ciałkowska-Rysz A, et al. The role and function of HDL in patients with diabetes mellitus and the related cardiovascular risk. 2017 Oct 30; 16(1):207. PubMed PMID: 29084567; PubMed Central PMCID: PMCPMC5663054. eng. doi: 10.1186/s12944-017-0594-3
   Google Scholar
• Zewinger S, Speer T, Kleber ME, et al. HDL cholesterol is not associated with lower mortality in patients with kidney dysfunction. J Am Soc Nephrol. 2014 May;25(5):1073–82. PubMed PMID: 24610925; PubMed Central PMCID: PMCPMC4005298. eng. doi: 10.1681/asn.2013050482
   PubMed Web of Science ®Google Scholar
• Shroff R, Speer T, Colin S, et al. HDL in children with CKD promotes endothelial dysfunction and an abnormal vascular phenotype. J Am Soc Nephrol. 2014 Nov;25(11):2658–68. PubMed PMID: 24854267; PubMed Central PMCID: PMCPMC4214534. eng. doi: 10.1681/asn.2013111212
   PubMed Web of Science ®Google Scholar
• Zewinger S, Kleber ME, Rohrer L, et al. Symmetric dimethylarginine, high-density lipoproteins and cardiovascular disease. Eur Heart J. 2017 May 21;38(20):1597–1607. PubMed PMID: 28379378; eng. doi: 10.1093/eurheartj/ehx118
   PubMed Web of Science ®Google Scholar
• Shao B, Afshinnia F, Mathew AV, et al. Low concentrations of medium-sized HDL particles predict incident CVD in chronic kidney disease patients. J Lipid Res. 2023 Jun;64(6):100381. PubMed PMID: 37100172; PubMed Central PMCID: PMCPMC10323925. eng. doi: 10.1016/j.jlr.2023.100381
   PubMed Web of Science ®Google Scholar
• Terasaka N, Yu S, Yvan-Charvet L, et al. ABCG1 and HDL protect against endothelial dysfunction in mice fed a high-cholesterol diet. J Clin Invest. 2008 Nov;118(11):3701–13. PubMed PMID: 18924609; PubMed Central PMCID: PMCPMC2567835. doi: 10.1172/JCI35470
   PubMed Web of Science ®Google Scholar
• Nofer JR, Levkau B, Wolinska I, et al. Suppression of endothelial cell apoptosis by high density lipoproteins (HDL) and HDL-associated lysosphingolipids. J Biol Chem. 2001 Sep 14;276(37): 34480–5. PubMed PMID: 11432865. doi: 10.1074/jbc.M103782200
   PubMed Web of Science ®Google Scholar
• Mineo C, Yuhanna IS, Quon MJ, et al. High density lipoprotein-induced endothelial nitric-oxide synthase activation is mediated by Akt and MAP kinases. J Biol Chem. 2003 Mar 14;278(11): 9142–9. PubMed PMID: 12511559. doi: 10.1074/jbc.M211394200
   PubMed Web of Science ®Google Scholar
• Kimura T, Tomura H, Sato K, et al. Mechanism and role of high density lipoprotein-induced activation of AMP-activated protein kinase in endothelial cells. J Biol Chem. 2010 Feb 12;285(7): 4387–97. PubMed PMID: 20018878; PubMed Central PMCID: PMCPMC2836043. doi: 10.1074/jbc.M109.043869
   PubMed Web of Science ®Google Scholar
• Wu BJ, Shrestha S, Ong KL, et al. Increasing HDL levels by inhibiting cholesteryl ester transfer protein activity in rabbits with hindlimb ischemia is associated with increased angiogenesis. Int J Cardiol. 2015 Nov 15;199:204–12. PubMed PMID: 26204569. doi: 10.1016/j.ijcard.2015.07.014
   PubMed Web of Science ®Google Scholar
• Prosser HC, Tan JT, Dunn LL, et al. Multifunctional regulation of angiogenesis by high-density lipoproteins. Cardiovasc Res. 2014 Jan 1;101(1): 145–154. PubMed PMID: 24130189. doi: 10.1093/cvr/cvt234
   PubMed Web of Science ®Google Scholar
• Calabresi L, Franceschini G, Sirtori CR, et al. Inhibition of VCAM-1 expression in endothelial cells by reconstituted high density lipoproteins. Biochem Biophys Res Commun. 1997 Sep 8;238(1): 61–5. PubMed PMID: 9299452. doi: 10.1006/bbrc.1997.7236
   PubMed Web of Science ®Google Scholar
• Park SH, Park JH, Kang JS, et al. Involvement of transcription factors in plasma HDL protection against TNF-alpha-induced vascular cell adhesion molecule-1 expression. Int J Biochem Cell Biol. 2003 Feb;35(2):168–182. PubMed PMID: 12479867. doi: 10.1016/s1357-2725(02)00173-5
   PubMed Web of Science ®Google Scholar
• Breitenstein A, Wyss CA, Spescha RD, et al. Peripheral blood monocyte Sirt1 expression is reduced in patients with coronary artery disease. PLoS One. 2013;8(1):e53106. PubMed PMID: 23382833; PubMed Central PMCID: PMCPMC3558418. doi: 10.1371/journal.pone.0053106
   PubMed Web of Science ®Google Scholar
• Lin TY, Chou HH, Huang HL, et al. Indoxyl sulfate and incident peripheral artery disease in hemodialysis patients. Toxins (Basel). 2020 Nov 2;12(11): 696. PubMed PMID: 33147880; PubMed Central PMCID: PMCPMC7693838. doi: 10.3390/toxins12110696
   PubMed Web of Science ®Google Scholar
• Wang CH, Lai YH, Kuo CH, et al. Association between serum indoxyl sulfate levels and endothelial function in non-dialysis chronic kidney disease. Toxins (Basel). 2019 Oct 11;11(10): 589. PubMed PMID: 31614554; PubMed Central PMCID: PMCPMC6832597. doi: 10.3390/toxins11100589
   PubMed Web of Science ®Google Scholar
• Hsu CC, Lu YC, Chiu CA, et al. Levels of indoxyl sulfate are associated with severity of coronary atherosclerosis. Clin Invest Med. 2013 Feb 1;36(1): E42–9. PubMed PMID: 23374599. doi: 10.25011/cim.v36i1.19404
   PubMed Web of Science ®Google Scholar
• Dou L, Jourde-Chiche N, Faure V, et al. The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells. J Thromb Haemost. 2007 Jun;5(6):1302–8. PubMed PMID: 17403109; eng. doi: 10.1111/j.1538-7836.2007.02540.x
   PubMed Web of Science ®Google Scholar
• Tumur Z, Niwa T. Indoxyl sulfate inhibits nitric oxide production and cell viability by inducing oxidative stress in vascular endothelial cells. Am J Nephrol. 2009;29(6):551–7. PubMed PMID: 19129694; eng. doi: 10.1159/000191468
   PubMed Web of Science ®Google Scholar
• Yu M, Kim YJ, Kang DH. Indoxyl sulfate-induced endothelial dysfunction in patients with chronic kidney disease via an induction of oxidative stress. Clin J Am Soc Nephrol. 2011 Jan;6(1):30–39. PubMed PMID: 20876676; PubMed Central PMCID: PMC3022246. eng. doi: 10.2215/cjn.05340610
   PubMed Web of Science ®Google Scholar
• Ito S, Osaka M, Edamatsu T, et al. Crucial Role of the Aryl Hydrocarbon Receptor (AhR) in Indoxyl Sulfate-Induced Vascular Inflammation. J Atheroscler Thromb. 2016 Aug 1;23(8):960–75. PubMed PMID: 26860885; PubMed Central PMCID: PMCPMC7399298. doi: 10.5551/jat.34462
   PubMed Web of Science ®Google Scholar
• Shen WC, Liang CJ, Huang TM, et al. Indoxyl sulfate enhances IL-1beta-induced E-selectin expression in endothelial cells in acute kidney injury by the ROS/MAPKs/NFkappaB/AP-1 pathway. Arch Toxicol. 2016 Nov;90(11):2779–2792. PubMed PMID: 26659566. doi: 10.1007/s00204-015-1652-0
   PubMed Web of Science ®Google Scholar
• Adelibieke Y, Shimizu H, Muteliefu G, et al. Indoxyl sulfate induces endothelial cell senescence by increasing reactive oxygen species production and p53 activity. J Ren Nutr. 2012 Jan;22(1):86–9. PubMed PMID: 22200421. doi: 10.1053/j.jrn.2011.10.027
   PubMed Web of Science ®Google Scholar
• Koizumi M, Tatebe J, Watanabe I, et al. Aryl hydrocarbon receptor mediates indoxyl sulfate-induced cellular senescence in human umbilical vein endothelial cells. J Atheroscler Thromb. 2014;21(9):904–16. PubMed PMID: 24727683. doi: 10.5551/jat.23663
   PubMed Web of Science ®Google Scholar
• Xu W, Liang M, Zhang Y, et al. Endothelial FAM3A positively regulates post-ischaemic angiogenesis. EBioMedicine. 2019 May;43:32–42. PubMed PMID: 31000420; PubMed Central PMCID: PMCPMC6562148. eng. doi: 10.1016/j.ebiom.2019.03.038
   PubMed Web of Science ®Google Scholar
• Xu H, Czerwinski P, Hortmann M, et al. Protein kinase C alpha promotes angiogenic activity of human endothelial cells via induction of vascular endothelial growth factor. Cardiovasc Res. 2008 May 1;78(2): 349–355. PubMed PMID: 18056764; eng. doi: 10.1093/cvr/cvm085
   PubMed Web of Science ®Google Scholar