The Korean journal of internal medicine

The Korean Association of Internal Medicine (대한내과학회)
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Correlation between NADPH oxidase-mediated oxidative stress and dysfunction of endothelial progenitor cell in hyperlipidemic patients

  • Li, Ting-Bo (Department of Laboratory Medicine, Xiangya School of Medicine) ;
  • Zhang, Yin-Zhuang (Department of Cardiovascular Medicine, Xiangya Hospital, Central South University) ;
  • Liu, Wei-Qi (Department of Cardiovascular Medicine, Xiangya Hospital, Central South University) ;
  • Zhang, Jie-Jie (Department of Pharmacology, School of Pharmaceutical Sciences, Central South University) ;
  • Peng, Jun (Department of Pharmacology, School of Pharmaceutical Sciences, Central South University) ;
  • Luo, Xiu-Ju (Department of Laboratory Medicine, Xiangya School of Medicine) ;
  • Ma, Qi-Lin (Department of Cardiovascular Medicine, Xiangya Hospital, Central South University)
  • Received : 2016.04.23
  • Accepted : 2016.10.13
  • Published : 2018.03.01
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Abstract

Background/Aims: NADPH (nicotinamide adenine dinucleotide phosphate) oxidase (NOX)-mediated oxidative stress plays a key role in promotion of oxidative injury in the cardiovascular system. The aim of this study is to evaluate the status of NOX in endothelial progenitor cells (EPCs) of hyperlipidemic patients and to assess the correlation between NOX activity and the functions EPCs. Methods: A total of 30 hyperlipidemic patients were enrolled for this study and 30 age-matched volunteers with normal level of plasma lipids served as controls. After the circulating EPCs were isolated, the EPC functions (migration, adhesion and tube formation) were evaluated and the status of NOX (expression and activity) was examined. Results: Compared to the controls, hyperlipidemic patients showed an increase in plasma lipids and a reduction in EPC functions including the attenuated abilities in adhesion, migration and tube formation, concomitant with an increase in NOX expression ($NOX_2$ and $NOX_4$), NOX activity, and reactive oxygen species production. The data analysis showed negative correlations between NOX activity and EPC functions. Conclusions: There is a positive correlation between the NOX-mediated oxidative stress and the dysfunctions of circulating EPCs in hyperlipidemic patients, and suppression of NOX might offer a novel strategy to improve EPCs functions in hyperlipidemia.

Keywords

Acknowledgement

Supported by : National Natural Science Foundation of China

References

  1. Hermida N, Balligand JL. Low-density lipoproteincholesterol- induced endothelial dysfunction and oxidative stress: the role of statins. Antioxid Redox Signal 2014;20:1216-1237. https://doi.org/10.1089/ars.2013.5537
  2. Liu YH, Liu Y, Chen JY, et al. LDL cholesterol as a novel risk factor for contrast-induced acute kidney injury in patients undergoing percutaneous coronary intervention. Atherosclerosis 2014;237:453-459. https://doi.org/10.1016/j.atherosclerosis.2014.10.022
  3. Messner B, Bernhard D. Smoking and cardiovascular disease: mechanisms of endothelial dysfunction and early atherogenesis. Arterioscler Thromb Vasc Biol 2014;34:509-515. https://doi.org/10.1161/ATVBAHA.113.300156
  4. George AL, Bangalore-Prakash P, Rajoria S, et al. Endothelial progenitor cell biology in disease and tissue regeneration. J Hematol Oncol 2011;4:24. https://doi.org/10.1186/1756-8722-4-24
  5. Peng J, Liu B, Ma QL, Luo XJ. Dysfunctional endothelial progenitor cells in cardiovascular diseases: role of NADPH oxidase. J Cardiovasc Pharmacol 2015;65:80-87. https://doi.org/10.1097/FJC.0000000000000166
  6. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 2004;95:343-353. https://doi.org/10.1161/01.RES.0000137877.89448.78
  7. Alexandru N, Popov D, Dragan E, Andrei E, Georgescu A. Circulating endothelial progenitor cell and platelet microparticle impact on platelet activation in hypertension associated with hypercholesterolemia. PLoS One 2013;8:e52058. https://doi.org/10.1371/journal.pone.0052058
  8. Imanishi T, Hano T, Matsuo Y, Nishio I. Oxidized lowdensity lipoprotein inhibits vascular endothelial growth factor-induced endothelial progenitor cell differentiation. Clin Exp Pharmacol Physiol 2003;30:665-670. https://doi.org/10.1046/j.1440-1681.2003.03894.x
  9. Rossi F, Bertone C, Michelon E, Bianco MJ, Santiemma V. High-density lipoprotein cholesterol affects early endothelial progenitor cell number and endothelial function in obese women. Obesity (Silver Spring) 2013;21:2356-2361. https://doi.org/10.1002/oby.20367
  10. Custodis F, Baumhakel M, Schlimmer N, et al. Heart rate reduction by ivabradine reduces oxidative stress, improves endothelial function, and prevents atherosclerosis in apolipoprotein E-deficient mice. Circulation 2008;117:2377-2387. https://doi.org/10.1161/CIRCULATIONAHA.107.746537
  11. Haddad P, Dussault S, Groleau J, Turgeon J, Maingrette F, Rivard A. Nox2-derived reactive oxygen species contribute to hypercholesterolemia-induced inhibition of neovascularization: effects on endothelial progenitor cells and mature endothelial cells. Atherosclerosis 2011;217:340-349. https://doi.org/10.1016/j.atherosclerosis.2011.03.038
  12. Lam YT. Critical roles of reactive oxygen species in age-related impairment in ischemia-induced neovascularization by regulating stem and progenitor cell function. Oxid Med Cell Longev 2015;2015:7095901.
  13. Drummond GR, Sobey CG. Endothelial NADPH oxidases: which NOX to target in vascular disease? Trends Endocrinol Metab 2014;25:452-463. https://doi.org/10.1016/j.tem.2014.06.012
  14. Jiang F, Zhang Y, Dusting GJ. NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol Rev 2011;63:218-242. https://doi.org/10.1124/pr.110.002980
  15. Ushio-Fukai M, Urao N. Novel role of NADPH oxidase in angiogenesis and stem/progenitor cell function. Antioxid Redox Signal 2009;11:2517-2533. https://doi.org/10.1089/ars.2009.2582
  16. Fenyo IM, Florea IC, Raicu M, Manea A. Tyrphostin AG490 reduces NAPDH oxidase activity and expression in the aorta of hypercholesterolemic apolipoprotein E-deficient mice. Vascul Pharmacol 2011;54:100-106. https://doi.org/10.1016/j.vph.2011.03.006
  17. Du F, Zhou J, Gong R, et al. Endothelial progenitor cells in atherosclerosis. Front Biosci (Landmark Ed) 2012;17:2327-2349. https://doi.org/10.2741/4055
  18. Madonna R, De Caterina R. Circulating endothelial progenitor cells: do they live up to their name? Vascul Pharmacol 2015;67-69:2-5. https://doi.org/10.1016/j.vph.2015.02.018
  19. Huang Q, Qin L, Dai S, et al. AIP1 suppresses atherosclerosis by limiting hyperlipidemia-induced inflammation and vascular endothelial dysfunction. Arterioscler Thromb Vasc Biol 2013;33:795-804. https://doi.org/10.1161/ATVBAHA.113.301220
  20. Yoder MC. Human endothelial progenitor cells. Cold Spring Harb Perspect Med 2012;2:a006692.
  21. Kawahara T, Lambeth JD. Molecular evolution of Phoxrelated regulatory subunits for NADPH oxidase enzymes. BMC Evol Biol 2007;7:178. https://doi.org/10.1186/1471-2148-7-178
  22. Lassegue B, San Martin A, Griendling KK. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res 2012;110:1364-1390. https://doi.org/10.1161/CIRCRESAHA.111.243972
  23. Chen DD, Dong YG, Yuan H, Chen AF. Endothelin 1 activation of endothelin A receptor/NADPH oxidase pathway and diminished antioxidants critically contribute to endothelial progenitor cell reduction and dysfunction in salt-sensitive hypertension. Hypertension 2012;59:1037-1043. https://doi.org/10.1161/HYPERTENSIONAHA.111.183368
  24. Lou Z, Ren KD, Tan B, et al. Salviaolate protects rat brain from ischemia-reperfusion injury through inhibition of NADPH oxidase. Planta Med 2015;81:1361-1369. https://doi.org/10.1055/s-0035-1557774
  25. Shao B, Bayraktutan U. Hyperglycaemia promotes human brain microvascular endothelial cell apoptosis via induction of protein kinase C-${\beta}I$ and prooxidant enzyme NADPH oxidase. Redox Biol 2014;2:694-701. https://doi.org/10.1016/j.redox.2014.05.005
  26. Urao N, Inomata H, Razvi M, et al. Role of $NOX_2$-based NADPH oxidase in bone marrow and progenitor cell function involved in neovascularization induced by hindlimb ischemia. Circ Res 2008;103:212-220. https://doi.org/10.1161/CIRCRESAHA.108.176230
  27. Zhang YS, Liu B, Luo XJ, et al. Nuclear cardiac myosin light chain 2 modulates NADPH oxidase 2 expression in myocardium: a novel function beyond muscle contraction. Basic Res Cardiol 2015;110:38. https://doi.org/10.1007/s00395-015-0494-5
  28. Zhu K, Kakehi T, Matsumoto M, et al. NADPH oxidase NOX1 is involved in activation of protein kinase C and premature senescence in early stage diabetic kidney. Free Radic Biol Med 2015;83:21-30. https://doi.org/10.1016/j.freeradbiomed.2015.02.009
  29. Liu B, Li T, Peng JJ, et al. Non-muscle myosin light chain promotes endothelial progenitor cells senescence and dysfunction in pulmonary hypertensive rats through up-regulation of NADPH oxidase. Eur J Pharmacol 2016;775:67-77. https://doi.org/10.1016/j.ejphar.2016.02.022

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