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N‑acetyl cysteine prevents ambient fine particulate matter‑potentiated atherosclerosis via inhibition of reactive oxygen species‑induced oxidized low density lipoprotein elevation and decreased circulating endothelial progenitor cell
- Authors:
- Yixin Xu
- Haoran Bu
- Yufan Jiang
- Xiaoqing Zhuo
- Ke Hu
- Zhihua Si
- Yong Chen
- Qiwei Liu
- Xianwei Gong
- Haihui Sun
- Qingyi Zhu
- Lianqun Cui
- Xiaochun Ma
- Yuqi Cui
-
Affiliations: Department of Cardiology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, Shandong 250021, P.R. China, Department of Cardiology, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250021, P.R. China, Department of Emergency, Qianfoshan Hospital, Shandong First Medical University, Jinan, Shandong 250014, P.R. China, Department of Pharmacy, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, Shandong 250021, P.R. China, Department of Cardiovascular Medicine, Second Xiangya Hospital, Central South University, Changsha, Hunan 410008, P.R. China, Department of Cardiovascular Surgery, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, Shandong 250021, P.R. China - Published online on: May 27, 2022 https://doi.org/10.3892/mmr.2022.12752
- Article Number: 236
-
Copyright: © Xu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
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Cui Y, Sun Q and Liu Z: Ambient particulate matter exposure and cardiovascular diseases: A focus on progenitor and stem cells. J Cell Mol Med. 20:782–793. 2016. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Pan J, Fan C, Xu R, Wang Y, Xu C, Xie S, Zhang H, Cui X, Peng Z, et al: Short-term exposure to ambient air pollution and mortality from myocardial infarction. J Am Coll Cardiol. 77:271–281. 2021. View Article : Google Scholar : PubMed/NCBI | |
Shah AS, Lee KK, McAllister DA, Hunter A, Nair H, Whiteley W, Langrish JP, Newby DE and Mills NL: Short term exposure to air pollution and stroke: Systematic review and meta-analysis. BMJ. 350:h12952015. View Article : Google Scholar : PubMed/NCBI | |
Rajagopalan S, Al-Kindi SG and Brook RD: Air pollution and cardiovascular disease: JACC state-of-the-art review. J Am Coll Cardiol. 72:2054–2070. 2018. View Article : Google Scholar : PubMed/NCBI | |
Sun Q, Wang A, Jin X, Natanzon A, Duquaine D, Brook RD, Aguinaldo JG, Fayad ZA, Fuster V, Lippmann M, et al: Long-term air pollution exposure and acceleration of atherosclerosis and vascular inflammation in an animal model. JAMA. 294:3003–3010. 2005. View Article : Google Scholar : PubMed/NCBI | |
Davignon J and Ganz P: Role of endothelial dysfunction in atherosclerosis. Circulation. 109 (23 Suppl 1):III27–III32. 2004. View Article : Google Scholar : PubMed/NCBI | |
Heitzer T, Schlinzig T, Krohn K, Meinertz T and Munzel T: Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease. Circulation. 104:2673–2678. 2001. View Article : Google Scholar : PubMed/NCBI | |
Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, Wang T, Gregg D, Ramaswami P, Pippen AM, Annex BH, Dong C and Taylor DA: Aging, progenitor cell exhaustion, and atherosclerosis. Circulation. 108:457–463. 2003. View Article : Google Scholar : PubMed/NCBI | |
Strehlow K, Werner N, Berweiler J, Link A, Dirnagl U, Priller J, Laufs K, Ghaeni L, Milosevic M, Böhm M and Nickenig G: Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation. 107:3059–3065. 2003. View Article : Google Scholar : PubMed/NCBI | |
Urbich C and Dimmeler S: Endothelial progenitor cells: Characterization and role in vascular biology. Circ Res. 95:343–353. 2004. View Article : Google Scholar : PubMed/NCBI | |
Werner N, Junk S, Laufs U, Link A, Walenta K, Bohm M and Nickenig G: Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res. 93:e17–e24. 2003. View Article : Google Scholar : PubMed/NCBI | |
Chen JZ, Zhang FR, Tao QM, Wang XX and Zhu JH and Zhu JH: Number and activity of endothelial progenitor cells from peripheral blood in patients with hypercholesterolaemia. Clin Sci (Lond). 107:273–280. 2004. View Article : Google Scholar : PubMed/NCBI | |
Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM and Dimmeler S: Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 89:E1–E7. 2001. View Article : Google Scholar : PubMed/NCBI | |
Kattoor AJ, Pothineni NVK, Palagiri D and Mehta JL: Oxidative stress in atherosclerosis. Curr Atheroscler Rep. 19:422017. View Article : Google Scholar : PubMed/NCBI | |
Cui Y, Narasimhulu CA, Liu L, Li X, Xiao Y, Zhang J, Xie X, Hao H, Liu JZ, He G, et al: Oxidized low-density lipoprotein alters endothelial progenitor cell populations. Front Biosci (Landmark Ed). 20:975–988. 2015. View Article : Google Scholar : PubMed/NCBI | |
Auten RL and Davis JM: Oxygen toxicity and reactive oxygen species: The devil is in the details. Pediatr Res. 66:121–127. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ogasawara MA and Zhang H: Redox regulation and its emerging roles in stem cells and stem-like cancer cells. Antioxid Redox Signal. 11:1107–1122. 2009. View Article : Google Scholar : PubMed/NCBI | |
Pervaiz S, Taneja R and Ghaffari S: Oxidative stress regulation of stem and progenitor cells. Antioxid Redox Signal. 11:2777–2789. 2009. View Article : Google Scholar : PubMed/NCBI | |
Cominacini L, Garbin U, Pasini AF, Davoli A, Campagnola M, Pastorino AM, Gaviraghi G and Lo Cascio V: Oxidized low-density lipoprotein increases the production of intracellular reactive oxygen species in endothelial cells: Inhibitory effect of lacidipine. J Hypertens. 16:1913–1919. 1998. View Article : Google Scholar : PubMed/NCBI | |
Vasconcelos EM, Degasperi GR, de Oliveira HC, Vercesi AE, de Faria EC and Castilho LN: Reactive oxygen species generation in peripheral blood monocytes and oxidized LDL are increased in hyperlipidemic patients. Clin Biochem. 42:1222–1227. 2009. View Article : Google Scholar : PubMed/NCBI | |
Cui Y, Xie X, Jia F, He J, Li Z, Fu M, Hao H, Liu Y, Liu JZ, Cowan PJ, et al: Ambient fine particulate matter induces apoptosis of endothelial progenitor cells through reactive oxygen species formation. Cell Physiol Biochem. 35:353–363. 2015. View Article : Google Scholar : PubMed/NCBI | |
Dludla PV, Dias SC, Obonye N, Johnson R, Louw J and Nkambule BB: A systematic review on the protective effect of N-Acetyl cysteine against diabetes-associated cardiovascular complications. Am J Cardiovasc Drugs. 18:283–298. 2018. View Article : Google Scholar : PubMed/NCBI | |
Cui Y, Narasimhulu CA, Liu L, Zhang Q, Liu PZ, Li X, Xiao Y, Zhang J, Hao H, Xie X, et al: N-acetylcysteine inhibits in vivo oxidation of native low-density lipoprotein. Sci Rep. 5:163392015. View Article : Google Scholar : PubMed/NCBI | |
Mutlu GM, Green D, Bellmeyer A, Baker CM, Burgess Z, Rajamannan N, Christman JW, Foiles N, Kamp DW, Ghio AJ, et al: Ambient particulate matter accelerates coagulation via an IL-6-dependent pathway. J Clin Invest. 117:2952–2961. 2007. View Article : Google Scholar : PubMed/NCBI | |
Gavett SH, Haykal-Coates N, Highfill JW, Ledbetter AD, Chen LC, Cohen MD, Harkema JR, Wagner JG and Costa DL: World Trade Center fine particulate matter causes respiratory tract hyperresponsiveness in mice. Environ Health Perspect. 111:981–991. 2003. View Article : Google Scholar : PubMed/NCBI | |
Shadie AM, Herbert C and Kumar RK: Ambient particulate matter induces an exacerbation of airway inflammation in experimental asthma: Role of interleukin-33. Clin Exp Immunol. 177:491–499. 2014. View Article : Google Scholar : PubMed/NCBI | |
Holt GR: Effects of air pollution on the upper aerodigestive tract. Otolaryngol Head Neck Surg. 114:201–204. 1996. View Article : Google Scholar : PubMed/NCBI | |
Aggarwal DJ, Kathariya MG and Verma DPK: LDL-C, NON-HDL-C and APO-B for cardiovascular risk assessment: Looking for the ideal marker. Indian Heart J. 73:544–548. 2021. View Article : Google Scholar : PubMed/NCBI | |
Zhuo X, Bu H, Hu K, Si Z, Chen L, Chen Y, Yang L, Jiang Y, Xu Y, Zhao P, et al: Differences in the reaction of hyperlipidemia on different endothelial progenitor cells based on sex. Biomed Rep. 15:642021. View Article : Google Scholar : PubMed/NCBI | |
Cui Y, Liu L, Xiao Y, Li X, Zhang J, Xie X, Tian J, Sen CK, He X, Hao H and Liu Z: N-acetylcysteine differentially regulates the populations of bone marrow and circulating endothelial progenitor cells in mice with limb ischemia. Eur J Pharmacol. 881:1732332020. View Article : Google Scholar : PubMed/NCBI | |
Rosenkranz AR, Schmaldienst S, Stuhlmeier KM, Chen W, Knapp W and Zlabinger GJ: A microplate assay for the detection of oxidative products using 2′,7′-dichlorofluorescin-diacetate. J Immunol Methods. 156:39–45. 1992. View Article : Google Scholar : PubMed/NCBI | |
Eggermann J, Kliche S, Jarmy G, Hoffmann K, Mayr-Beyrle U, Debatin KM, Waltenberger J and Beltinger C: Endothelial progenitor cell culture and differentiation in vitro: A methodological comparison using human umbilical cord blood. Cardiovasc Res. 58:478–486. 2003. View Article : Google Scholar : PubMed/NCBI | |
Ii M, Takenaka H, Asai J, Ibusuki K, Mizukami Y, Maruyama K, Yoon YS, Wecker A, Luedemann C, Eaton E, et al: Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circ Res. 98:697–704. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kinnaird T, Stabile E, Zbinden S, Burnett MS and Epstein SE: Cardiovascular risk factors impair native collateral development and may impair efficacy of therapeutic interventions. Cardiovasc Res. 78:257–264. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sodha NR, Clements RT, Boodhwani M, Xu SH, Laham RJ, Bianchi C and Sellke FW: Endostatin and angiostatin are increased in diabetic patients with coronary artery disease and associated with impaired coronary collateral formation. Am J Physiol Heart Circ Physiol. 296:H428–H434. 2009. View Article : Google Scholar : PubMed/NCBI | |
Panahi Y, Ahmadi Y, Teymouri M, Johnston TP and Sahebkar A: Curcumin as a potential candidate for treating hyperlipidemia: A review of cellular and metabolic mechanisms. J Cell Physiol. 233:141–152. 2016. View Article : Google Scholar : PubMed/NCBI | |
Krauzova E, Kracmerova J, Rossmeislova L, Mališová L, Tencerová M, Koc M, Štich V and Šiklová M: Acute hyperlipidemia initiates proinflammatory and proatherogenic changes in circulation and adipose tissue in obese women. Atherosclerosis. 250:151–157. 2016. View Article : Google Scholar : PubMed/NCBI | |
He L, Hao L, Fu X, Huang M and Li R: Severe hypertriglyceridemia and hypercholesterolemia accelerating renal injury: A novel model of type 1 diabetic hamsters induced by short-term high-fat/high-cholesterol diet and low-dose streptozotocin. BMC Nephrol. 16:512015. View Article : Google Scholar : PubMed/NCBI | |
Krysiak R, Zmuda W, Marek B and Okopien B: Comparison of the effects of short-term hypolipidaemic treatment on plasma adipokine levels in men and women with isolated hypercholesterolaemia. Endokrynol Pol. 66:114–120. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bevan GH, Al-Kindi SG, Brook R and Rajagopalan S: Ambient air pollution and atherosclerosis: Recent updates. Curr Atheroscler Rep. 23:632021. View Article : Google Scholar : PubMed/NCBI | |
Kander MC, Cui Y and Liu Z: Gender difference in oxidative stress: A new look at the mechanisms for cardiovascular diseases. J Cell Mol Med. 21:1024–1032. 2017. View Article : Google Scholar : PubMed/NCBI | |
Liu X, Xiao Y, Zhu Q, Cui Y, Hao H, Wang M, Cowan PJ, Korthuis RJ, Li G, Sun Q and Liu Z: Circulating endothelial progenitor cells are preserved in female mice exposed to ambient fine particulate matter independent of estrogen. Int J Mol Sci. 22:72002021. View Article : Google Scholar : PubMed/NCBI | |
Liu X, Wang A, Chen Z, Cui Y, Hao H, Domeier TL, Sun Q and Liu Z: Tempol preserves endothelial progenitor cells in male mice with ambient fine particulate matter exposure. Biomedicines. 10:3272022. View Article : Google Scholar : PubMed/NCBI | |
Zafarullah M, Li WQ, Sylvester J and Ahmad M: Molecular mechanisms of N-acetylcysteine actions. Cell Mol Life Sci. 60:6–20. 2003. View Article : Google Scholar : PubMed/NCBI | |
Bartekova M, Barancik M, Ferenczyova K and Dhalla NS: Beneficial effects of N-acetylcysteine and N-mercaptopropionylglycine on ischemia reperfusion injury in the heart. Curr Med Chem. 25:355–366. 2018. View Article : Google Scholar : PubMed/NCBI | |
Marian AJ: Experimental therapies in hypertrophic cardiomyopathy. J Cardiovasc Transl Res. 2:483–492. 2009. View Article : Google Scholar : PubMed/NCBI | |
Nikbakht M, Ahmadi F, Vaseghi G, Talasaz AH, Eshraghi A, Naderi J and Daneshmehr MA: The role of N-acetylcysteine in platelet aggregation and reperfusion injury in recent years. Curr Clin Pharmacol. 12:83–91. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lin CP, Huang PH, Lai CF, Chen JW, Lin SJ and Chen JS: Simvastatin attenuates oxidative stress, NF-κB activation, and artery calcification in LDLR-/-mice fed with high fat diet via down-regulation of tumor necrosis factor-α and TNF receptor 1. PLoS One. 10:e01436862015. View Article : Google Scholar : PubMed/NCBI | |
Subrahmanian S, Varshney R, Subramani K, Murphy B, Woolington S and Ahamed J: N-Acetylcysteine inhibits aortic stenosis progression in a murine model by blocking Shear-induced activation of platelet latent transforming growth factor beta 1. Antioxid Redox Signal. Dec 7–2021.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Spartalis M, Siasos G, Mastrogeorgiou M, Spartalis E, Kaminiotis VV, Mylonas KS, Kapelouzou A, Kontogiannis C, Doulamis IP, Toutouzas K, et al: The effect of per os colchicine administration in combination with fenofibrate and N-acetylcysteine on triglyceride levels and the development of atherosclerotic lesions in cholesterol-fed rabbits. Eur Rev Med Pharmacol Sci. 25:7765–7776. 2021.PubMed/NCBI | |
Korou LM, Agrogiannis G, Pantopoulou A, Vlachos IS, Iliopoulos D, Karatzas T and Perrea DN: Comparative antilipidemic effect of N-acetylcysteine and sesame oil administration in diet-induced hypercholesterolemic mice. Lipids Health Dis. 9:232010. View Article : Google Scholar : PubMed/NCBI | |
Meng XP, Yin CS, Cui JH, Li ZX, Wang L, Wang YW and Li YL: Inhibitory effect of N-acetylcysteine upon atherosclerotic processes in rabbit carotid. Zhonghua Yi Xue Za Zhi. 89:1850–1853. 2009.(In Chinese). PubMed/NCBI | |
Sung HJ, Kim J, Kim Y, Jang SW and Ko J: N-acetyl cysteine suppresses the foam cell formation that is induced by oxidized low density lipoprotein via regulation of gene expression. Mol Biol Rep. 39:3001–3007. 2012. View Article : Google Scholar : PubMed/NCBI | |
Thiele H, Hildebrand L, Schirdewahn C, Eitel I, Adams V, Fuernau G, Erbs S, Linke A, Diederich KW, Nowak M, et al: Impact of high-dose N-acetylcysteine versus placebo on contrast-induced nephropathy and myocardial reperfusion injury in unselected patients with ST-segment elevation myocardial infarction undergoing primary percutaneous coronary intervention. The LIPSIA-N-ACC (Prospective, Single-Blind, Placebo-Controlled, Randomized Leipzig Immediate PercutaneouS Coronary Intervention Acute Myocardial Infarction N-ACC) Trial. J Am Coll Cardiol. 55:2201–2209. 2010. View Article : Google Scholar : PubMed/NCBI | |
Poitevin S, Garnotel R, Antonicelli F, Gillery P and Nguyen P: Type I collagen induces tissue factor expression and matrix metalloproteinase 9 production in human primary monocytes through a redox-sensitive pathway. J Thromb Haemost. 6:1586–1594. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wiklund O, Fager G, Andersson A, Lundstam U, Masson P and Hultberg B: N-acetylcysteine treatment lowers plasma homocysteine but not serum lipoprotein(a) levels. Atherosclerosis. 119:99–106. 1996. View Article : Google Scholar : PubMed/NCBI | |
Zhu Q, Hao H, Xu H, Fichman Y, Cui Y, Yang C, Wang M, Mittler R, Hill MA, Cowan PJ, et al: Combination of antioxidant enzyme overexpression and N-acetylcysteine treatment enhances the survival of bone marrow mesenchymal stromal cells in ischemic limb in mice with type 2 diabetes. Am Heart Assoc. 10:e0234912021. View Article : Google Scholar : PubMed/NCBI | |
Omara FO, Fournier M, Vincent R and Blakley BR: Suppression of rat and mouse lymphocyte function by urban air particulates (Ottawa dust) is reversed by N-acetylcysteine. J Toxicol Environ Health A. 59:67–85. 2000. View Article : Google Scholar : PubMed/NCBI | |
Rhoden CR, Lawrence J, Godleski JJ and Gonzalez-Flecha B: N-acetylcysteine prevents lung inflammation after short-term inhalation exposure to concentrated ambient particles. Toxicol Sci. 79:296–303. 2004. View Article : Google Scholar : PubMed/NCBI | |
Wang T, Wang L, Moreno-Vinasco L, Lang GD, Siegler JH, Mathew B, Usatyuk PV, Samet JM, Geyh AS, Breysse PN, et al: Particulate matter air pollution disrupts endothelial cell barrier via calpain-mediated tight junction protein degradation. Part Fibre Toxicol. 9:352012. View Article : Google Scholar : PubMed/NCBI | |
Sharma K, Lee HH, Gong DS, Park SH, Yi E, Schini-Kerth V and Oak MH: Fine air pollution particles induce endothelial senescence via redox-sensitive activation of local angiotensin system. Environ Pollut. 252((Pt A)): 317–329. 2019. View Article : Google Scholar : PubMed/NCBI | |
Reboul C, Boissiere J, Andre L, Meyer G, Bideaux P, Fouret G, Feillet-Coudray C, Obert P, Lacampagne A, Thireau J, et al: Carbon monoxide pollution aggravates ischemic heart failure through oxidative stress pathway. Sci Rep. 7:397152017. View Article : Google Scholar : PubMed/NCBI | |
Kim JB, Kim C, Choi E, Park S, Park H, Pak HN, Lee MH, Shin DC, Hwang KC and Joung B: Particulate air pollution induces arrhythmia via oxidative stress and calcium calmodulin kinase II activation. Toxicol Appl Pharmacol. 259:66–73. 2012. View Article : Google Scholar : PubMed/NCBI | |
Tzeng HP, Yang RS, Ueng TH and Liu SH: Upregulation of cyclooxygenase-2 by motorcycle exhaust particulate-induced reactive oxygen species enhances rat vascular smooth muscle cell proliferation. Chem Res Toxicol. 20:1170–1176. 2007. View Article : Google Scholar : PubMed/NCBI | |
Rhoden CR, Wellenius GA, Ghelfi E, Lawrence J and Gonzalez-Flecha B: PM-induced cardiac oxidative stress and dysfunction are mediated by autonomic stimulation. Biochim Biophys Acta. 1725:305–313. 2005. View Article : Google Scholar : PubMed/NCBI | |
Cui Y, Jia F, He J, Xie X, Li Z, Fu M, Hao H, Liu Y, Liu DZ, Cowan PJ, et al: Ambient fine particulate matter suppresses in vivo proliferation of bone marrow stem cells through reactive oxygen species formation. PLoS One. 10:e01273092015. View Article : Google Scholar : PubMed/NCBI |