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Published in: Inflammation Research 6/2019

01-06-2019 | Atorvastatin | Review

Roles of eNOS in atherosclerosis treatment

Authors: Fen-fang Hong, Xiao-yu Liang, Wei Liu, Sha Lv, Shu-jin He, Hai-bin Kuang, Shu-long Yang

Published in: Inflammation Research | Issue 6/2019

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Abstract

Background

Atherosclerosis (AS) is the main pathogeny of coronary heart disease, cerebral infarction and peripheral vascular disease. Endothelial dysfunction is one of the important pathogenesis of AS. As an important endothelium-derived relaxation factor, nitric oxide (NO) plays a role in cardiovascular protection and anti-AS function; but in the pathological state, endothelial nitric oxide synthase (eNOS) disorder causes an abnormal production of NO, which may damage endothelial function and trigger AS. This review summarized the research progresses in the treatment strategies for AS based on correcting the disordered eNOS/ NO signaling pathway.

Main body

According to the topic, select the search terms ‘atherosclerosis,’ ‘nitric oxide,’ ‘eNOS,’ ‘treatment,’ ‘management,’ ‘medication,’ ‘maintenance,’ ‘remission’. Using these terms, a structured literature search via multiple electronic databases was performed for the most recent trial evidence in recent years. We read and analyze these literatures carefully, classified these literatures according to their content, and then summarized and outlined the common main points in these classified literatures. Finally, literature data were organized to discuss these main points logically. We found that both aberrant expression and dysfunction of eNOS are closely related to AS development, and some new treatment strategies aimed at eNOS have been proposed, including upregulation of eNOS expression and inhibition of eNOS uncoupling. The former one is mainly related to inflammatory inhibition and protection of the PKB-eNOS signaling pathway; whereas the latter one is associated with the addition of the L-arginine substrate of eNOS, arginase inhibition, and the supplement of tetrahydrobiopterin, which can elevate no level.

Conclusions

eNOS can be an important target for prevention and treatment of AS, and eNOS drugs may be another potent class of effective therapeutic treatment for AS following traditional lipid-lowering, anti-platelet, vasodilator drugs. But applying these experimental results to clinic treatment still requires further studies and development of biotechnology.
Literature
1.
go back to reference Ke YN, Liu Y. Cholesterol depressing and atherosclerosis prevention. Health Care Elder. 2016;1:8–9. Ke YN, Liu Y. Cholesterol depressing and atherosclerosis prevention. Health Care Elder. 2016;1:8–9.
2.
go back to reference Younk LM, Lamos EM, Davis SN. The cardiovascular effects of insulin. Expert Opin Drug Saf. 2014;13:955–66.CrossRefPubMed Younk LM, Lamos EM, Davis SN. The cardiovascular effects of insulin. Expert Opin Drug Saf. 2014;13:955–66.CrossRefPubMed
3.
go back to reference Lurie A. Endothelial dysfunction in adults with obstructive sleep apnea. Adv Cardiol. 2011;46:139–70.CrossRef Lurie A. Endothelial dysfunction in adults with obstructive sleep apnea. Adv Cardiol. 2011;46:139–70.CrossRef
4.
go back to reference Zhang HP, Tang N, Ka B. Endothelial nitric oxide synthase uncoupling and oxidative stress. Traditional Chinese Medicine J Liaoning Univ. 2009;11:36–40. Zhang HP, Tang N, Ka B. Endothelial nitric oxide synthase uncoupling and oxidative stress. Traditional Chinese Medicine J Liaoning Univ. 2009;11:36–40.
5.
go back to reference Sukhovershin RA, Yepuri G, Ghebremariam YT. endothelium-derived nitric oxide as an antiatherogenic mechanism: implications for therapy. Methodist Debakey Cardiovasc J. 1900;11:166–71.CrossRef Sukhovershin RA, Yepuri G, Ghebremariam YT. endothelium-derived nitric oxide as an antiatherogenic mechanism: implications for therapy. Methodist Debakey Cardiovasc J. 1900;11:166–71.CrossRef
6.
go back to reference Saini V, Bhatnagar MK, Bhattacharjee J. Endothelial nitric oxide synthase Glu298Asp (G894T) gene polymorphism in coronary artery disease patients with type 2 diabetes mellitus. Diabetes Metab Syndr. 2012;6:106–9.CrossRefPubMed Saini V, Bhatnagar MK, Bhattacharjee J. Endothelial nitric oxide synthase Glu298Asp (G894T) gene polymorphism in coronary artery disease patients with type 2 diabetes mellitus. Diabetes Metab Syndr. 2012;6:106–9.CrossRefPubMed
7.
go back to reference Xin G, Li S, Fu YM, Yong Z. Effects of olmesartan on endothelial progenitor cell mobilization and function in carotid atherosclerosis. Med Sci Monit Int Med J Exp Clin Res. 2015;21:1189–93. Xin G, Li S, Fu YM, Yong Z. Effects of olmesartan on endothelial progenitor cell mobilization and function in carotid atherosclerosis. Med Sci Monit Int Med J Exp Clin Res. 2015;21:1189–93.
8.
go back to reference Scalia R, Stalker TJ. Microcirculation as a target for the anti-inflammatory properties of statins. Microcirculation. 2002;9:431–42.CrossRefPubMed Scalia R, Stalker TJ. Microcirculation as a target for the anti-inflammatory properties of statins. Microcirculation. 2002;9:431–42.CrossRefPubMed
9.
go back to reference Xu L, Wang S, Li B, Sun A, Zou Y, Ge J. A protective role of ciglitazone in ox-LDL-induced rat microvascular endothelial cells via modulating PPARgamma-dependent AMPK/eNOS pathway. J Cell Mol Med. 2015;19:92–102.CrossRefPubMed Xu L, Wang S, Li B, Sun A, Zou Y, Ge J. A protective role of ciglitazone in ox-LDL-induced rat microvascular endothelial cells via modulating PPARgamma-dependent AMPK/eNOS pathway. J Cell Mol Med. 2015;19:92–102.CrossRefPubMed
10.
go back to reference Yin J, Huang F, Yi Y, Yin L, Peng D. EGCG attenuates atherosclerosis through the Jagged-1/Notch pathway. Int J Mol Med. 2016;37:398–406.CrossRefPubMed Yin J, Huang F, Yi Y, Yin L, Peng D. EGCG attenuates atherosclerosis through the Jagged-1/Notch pathway. Int J Mol Med. 2016;37:398–406.CrossRefPubMed
11.
go back to reference Bao MH, Zhang YW, Lou XY, Xiao Y, Cheng Y, Zhou HH. Puerarin protects endothelial cells from oxidized low density lipoprotein induced injuries via the suppression of LOX-1 and induction of eNOS. Can J Physiol Pharmacol. 2014;92:299–306.CrossRefPubMed Bao MH, Zhang YW, Lou XY, Xiao Y, Cheng Y, Zhou HH. Puerarin protects endothelial cells from oxidized low density lipoprotein induced injuries via the suppression of LOX-1 and induction of eNOS. Can J Physiol Pharmacol. 2014;92:299–306.CrossRefPubMed
12.
go back to reference Yu S, Wong SL, Lau CW, Huang Y, Yu CM. Oxidized LDL at low concentration promotes in-vitro angiogenesis and activates nitric oxide synthase through PI3K/Akt/eNOS pathway in human coronary artery endothelial cells. Biochem Biophys Res Commun. 2011;407:44–8.CrossRefPubMed Yu S, Wong SL, Lau CW, Huang Y, Yu CM. Oxidized LDL at low concentration promotes in-vitro angiogenesis and activates nitric oxide synthase through PI3K/Akt/eNOS pathway in human coronary artery endothelial cells. Biochem Biophys Res Commun. 2011;407:44–8.CrossRefPubMed
13.
go back to reference Tsai KL, Huang YH, Kao CL, Yang DM, Lee HC, Chou HY, et al. A novel mechanism of coenzyme Q10 protects against human endothelial cells from oxidative stress-induced injury by modulating NO-related pathways. J Nutr Biochem. 2012;23:458–68.CrossRefPubMed Tsai KL, Huang YH, Kao CL, Yang DM, Lee HC, Chou HY, et al. A novel mechanism of coenzyme Q10 protects against human endothelial cells from oxidative stress-induced injury by modulating NO-related pathways. J Nutr Biochem. 2012;23:458–68.CrossRefPubMed
14.
go back to reference Imachi H, Murao K. HDL metabolism in lifestyle-related illnesses. Rinsho Byori. 2012;60:1081–6.PubMed Imachi H, Murao K. HDL metabolism in lifestyle-related illnesses. Rinsho Byori. 2012;60:1081–6.PubMed
15.
go back to reference Durante A, Peretto G, Laricchia A, Ancona F, Spartera M, Mangieri A, et al. Role of the renin–angiotensin–aldosterone system in the pathogenesis of atherosclerosis. Curr Pharm Des. 2012;18:981–1004.CrossRefPubMed Durante A, Peretto G, Laricchia A, Ancona F, Spartera M, Mangieri A, et al. Role of the renin–angiotensin–aldosterone system in the pathogenesis of atherosclerosis. Curr Pharm Des. 2012;18:981–1004.CrossRefPubMed
16.
go back to reference Qaradakhi T, Apostolopoulos V, Zulli A. Angiotensin (1–7) and Alamandine: Similarities and differences. Pharmacol Res. 2016;111:820–6.CrossRefPubMed Qaradakhi T, Apostolopoulos V, Zulli A. Angiotensin (1–7) and Alamandine: Similarities and differences. Pharmacol Res. 2016;111:820–6.CrossRefPubMed
17.
go back to reference Aoyama T, Minatoguchi S. The effect of ARB on prevention of atherosclerosis. Nihon Rinsho. 2011;69:92–9.PubMed Aoyama T, Minatoguchi S. The effect of ARB on prevention of atherosclerosis. Nihon Rinsho. 2011;69:92–9.PubMed
18.
go back to reference Fu R, Chen Z, Wang Q, Guo Q, Xu J, Wu X. XJP-1, a novel ACEI, with anti-inflammatory properties in HUVECs. Atherosclerosis. 2011;219:40–8.CrossRefPubMed Fu R, Chen Z, Wang Q, Guo Q, Xu J, Wu X. XJP-1, a novel ACEI, with anti-inflammatory properties in HUVECs. Atherosclerosis. 2011;219:40–8.CrossRefPubMed
19.
go back to reference Stegbauer J, Potthoff SA, Quack I, Mergia E, Clasen T, Friedrich S, et al. Chronic treatment with angiotensin-(1–7) improves renal endothelial dysfunction in apolipoproteinE-deficient mice. Br J Pharmacol. 2011;163:974–83.CrossRefPubMedPubMedCentral Stegbauer J, Potthoff SA, Quack I, Mergia E, Clasen T, Friedrich S, et al. Chronic treatment with angiotensin-(1–7) improves renal endothelial dysfunction in apolipoproteinE-deficient mice. Br J Pharmacol. 2011;163:974–83.CrossRefPubMedPubMedCentral
20.
go back to reference Kljajic ST, Widdop RE, Vinh A, Welungoda I, Bosnyak S, Jones ES, et al. Direct AT(2) receptor stimulation is athero-protective and stabilizes plaque in apolipoprotein E-deficient mice. Int J Cardiol. 2013;169:281–7.CrossRefPubMed Kljajic ST, Widdop RE, Vinh A, Welungoda I, Bosnyak S, Jones ES, et al. Direct AT(2) receptor stimulation is athero-protective and stabilizes plaque in apolipoprotein E-deficient mice. Int J Cardiol. 2013;169:281–7.CrossRefPubMed
21.
go back to reference Kilic U, Gok O, Elibol-Can B, Uysal O, Bacaksiz A. Efficacy of statins on sirtuin 1 and endothelial nitric oxide synthase expression: the role of sirtuin 1 gene variants in human coronary atherosclerosis. Clin Exp Pharmacol Physiol. 2015;42:321–30.CrossRefPubMed Kilic U, Gok O, Elibol-Can B, Uysal O, Bacaksiz A. Efficacy of statins on sirtuin 1 and endothelial nitric oxide synthase expression: the role of sirtuin 1 gene variants in human coronary atherosclerosis. Clin Exp Pharmacol Physiol. 2015;42:321–30.CrossRefPubMed
22.
go back to reference Balakumar P, Kathuria S, Taneja G, Kalra S, Mahadevan N. Is targeting eNOS a key mechanistic insight of cardiovascular defensive potentials of statins? J Mol Cell Cardiol. 2012;52:83–92.CrossRefPubMed Balakumar P, Kathuria S, Taneja G, Kalra S, Mahadevan N. Is targeting eNOS a key mechanistic insight of cardiovascular defensive potentials of statins? J Mol Cell Cardiol. 2012;52:83–92.CrossRefPubMed
23.
go back to reference Berthe MC, Bernard M, Rasmusen C, Darquy S, Cynober L, Couderc R. Arginine or citrulline associated with a statin stimulates nitric oxide production in bovine aortic endothelial cells. Eur J Pharmacol. 2011;670:566–70.CrossRefPubMed Berthe MC, Bernard M, Rasmusen C, Darquy S, Cynober L, Couderc R. Arginine or citrulline associated with a statin stimulates nitric oxide production in bovine aortic endothelial cells. Eur J Pharmacol. 2011;670:566–70.CrossRefPubMed
24.
go back to reference Ota H, Eto M, Ogawa S, Iijima K, Akishita M, Ouchi Y. SIRT1/eNOS axis as a potential target against vascular senescence, dysfunction and atherosclerosis. J Atheroscler Thromb. 2010;17:431–5.CrossRefPubMed Ota H, Eto M, Ogawa S, Iijima K, Akishita M, Ouchi Y. SIRT1/eNOS axis as a potential target against vascular senescence, dysfunction and atherosclerosis. J Atheroscler Thromb. 2010;17:431–5.CrossRefPubMed
25.
go back to reference Mattagajasingh I, Kim CS, Naqvi A, Yamamori T, Hoffman TA, Jung SB, et al. SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase. Proc Natl Acad Sci USA. 2007;104:14855–60.CrossRefPubMedPubMedCentral Mattagajasingh I, Kim CS, Naqvi A, Yamamori T, Hoffman TA, Jung SB, et al. SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase. Proc Natl Acad Sci USA. 2007;104:14855–60.CrossRefPubMedPubMedCentral
26.
go back to reference Ota H, Akishita M, Eto M, Iijima K, Kaneki M, Ouchi Y. Sirt1 modulates premature senescence-like phenotype in human endothelial cells. J Mol Cell Cardiol. 2007;43:571–9.CrossRefPubMed Ota H, Akishita M, Eto M, Iijima K, Kaneki M, Ouchi Y. Sirt1 modulates premature senescence-like phenotype in human endothelial cells. J Mol Cell Cardiol. 2007;43:571–9.CrossRefPubMed
27.
go back to reference Liu X, Ma D, Zheng S, Zha K, Feng J, Cai Y, et al. The roles of nitric oxide and hydrogen sulfide in the anti-atherosclerotic effect of atorvastatin. J Cardiovasc Med (Hagerstown). 2015;16:22–8.CrossRef Liu X, Ma D, Zheng S, Zha K, Feng J, Cai Y, et al. The roles of nitric oxide and hydrogen sulfide in the anti-atherosclerotic effect of atorvastatin. J Cardiovasc Med (Hagerstown). 2015;16:22–8.CrossRef
28.
go back to reference Li T, Li D, Xu H, Zhang H, Tang D, Cao H. Wen-Xin Decoction ameliorates vascular endothelium dysfunction via the PI3K/AKT/eNOS pathway in experimental atherosclerosis in rats. BMC Complement Altern Med. 2016;16:27.CrossRefPubMedPubMedCentral Li T, Li D, Xu H, Zhang H, Tang D, Cao H. Wen-Xin Decoction ameliorates vascular endothelium dysfunction via the PI3K/AKT/eNOS pathway in experimental atherosclerosis in rats. BMC Complement Altern Med. 2016;16:27.CrossRefPubMedPubMedCentral
29.
go back to reference Ren Y, Tao S, Zheng S, Zhao M, Zhu Y, Yang J, et al. Salvianolic acid B improves vascular endothelial function in diabetic rats with blood glucose fluctuations via suppression of endothelial cell apoptosis. Eur J Pharmacol. 2016;791:308–15.CrossRefPubMed Ren Y, Tao S, Zheng S, Zhao M, Zhu Y, Yang J, et al. Salvianolic acid B improves vascular endothelial function in diabetic rats with blood glucose fluctuations via suppression of endothelial cell apoptosis. Eur J Pharmacol. 2016;791:308–15.CrossRefPubMed
30.
go back to reference Hong SH, Kim M, Noh JS, Song YO. Perilla oil reduces fatty streak formation at aortic sinus via attenuation of plasma lipids and regulation of nitric oxide synthase in ApoE KO mice. Lipids. 2016;51:1161–70.CrossRefPubMed Hong SH, Kim M, Noh JS, Song YO. Perilla oil reduces fatty streak formation at aortic sinus via attenuation of plasma lipids and regulation of nitric oxide synthase in ApoE KO mice. Lipids. 2016;51:1161–70.CrossRefPubMed
31.
go back to reference Horigome S, Yoshida I, Ito S, Inohana S, Fushimi K, Nagai T, et al. Inhibitory effects of Kaempferia parviflora extract on monocyte adhesion and cellular reactive oxygen species production in human umbilical vein endothelial cells. Eur J Nutr. 2017;56:949–64.CrossRefPubMed Horigome S, Yoshida I, Ito S, Inohana S, Fushimi K, Nagai T, et al. Inhibitory effects of Kaempferia parviflora extract on monocyte adhesion and cellular reactive oxygen species production in human umbilical vein endothelial cells. Eur J Nutr. 2017;56:949–64.CrossRefPubMed
32.
go back to reference Ichimura M, Kato S, Tsuneyama K, Matsutake S, Kamogawa M, Hirao E, et al. Phycocyanin prevents hypertension and low serum adiponectin level in a rat model of metabolic syndrome. Nutr Res. 2013;33:397–405.CrossRefPubMed Ichimura M, Kato S, Tsuneyama K, Matsutake S, Kamogawa M, Hirao E, et al. Phycocyanin prevents hypertension and low serum adiponectin level in a rat model of metabolic syndrome. Nutr Res. 2013;33:397–405.CrossRefPubMed
33.
go back to reference Xiang W, He XJ, Ma YL, Yi ZW, Cao Y, Zhao SP, et al. [1,25(OH)(2)D(3) influences endothelial cell proliferation, apoptosis and endothelial nitric oxide synthase expression of aorta in apolipoprotein E-deficient mice]. Zhonghua Er Ke Za Zhi. 2011;49:829–33.PubMed Xiang W, He XJ, Ma YL, Yi ZW, Cao Y, Zhao SP, et al. [1,25(OH)(2)D(3) influences endothelial cell proliferation, apoptosis and endothelial nitric oxide synthase expression of aorta in apolipoprotein E-deficient mice]. Zhonghua Er Ke Za Zhi. 2011;49:829–33.PubMed
34.
go back to reference Porto ML, Lima LC, Pereira TM, Nogueira BV, Tonini CL, Campagnaro BP, et al. Mononuclear cell therapy attenuates atherosclerosis in apoE KO mice. Lipids Health Dis. 2011;10:155.CrossRefPubMedPubMedCentral Porto ML, Lima LC, Pereira TM, Nogueira BV, Tonini CL, Campagnaro BP, et al. Mononuclear cell therapy attenuates atherosclerosis in apoE KO mice. Lipids Health Dis. 2011;10:155.CrossRefPubMedPubMedCentral
35.
go back to reference Xu S, Ha CH, Wang W, Xu X, Yin M, Jin FQ, et al. PECAM1 regulates flow-mediated Gab1 tyrosine phosphorylation and signaling. Cell Signal. 2016;28:117–24.CrossRefPubMed Xu S, Ha CH, Wang W, Xu X, Yin M, Jin FQ, et al. PECAM1 regulates flow-mediated Gab1 tyrosine phosphorylation and signaling. Cell Signal. 2016;28:117–24.CrossRefPubMed
36.
go back to reference Dai Y, Mehta JL, Chen M. Glucagon-like peptide-1 receptor agonist liraglutide inhibits endothelin-1 in endothelial cell by repressing nuclear factor-kappa B activation. Cardiovasc Drugs Ther. 2013;27:371–80.CrossRefPubMed Dai Y, Mehta JL, Chen M. Glucagon-like peptide-1 receptor agonist liraglutide inhibits endothelin-1 in endothelial cell by repressing nuclear factor-kappa B activation. Cardiovasc Drugs Ther. 2013;27:371–80.CrossRefPubMed
37.
go back to reference Margaritis M, Antonopoulos AS, Digby J, Lee R, Reilly S, Coutinho P, et al. Interactions between vascular wall and perivascular adipose tissue reveal novel roles for adiponectin in the regulation of endothelial nitric oxide synthase function in human vessels. Circulation. 2013;127:2209–21.CrossRefPubMed Margaritis M, Antonopoulos AS, Digby J, Lee R, Reilly S, Coutinho P, et al. Interactions between vascular wall and perivascular adipose tissue reveal novel roles for adiponectin in the regulation of endothelial nitric oxide synthase function in human vessels. Circulation. 2013;127:2209–21.CrossRefPubMed
38.
go back to reference Notsu Y, Yano S, Shibata H, Nagai A, Nabika T. Plasma arginine/ADMA ratio as a sensitive risk marker for atherosclerosis: Shimane CoHRE study. Atherosclerosis. 2015;239:61–6.CrossRefPubMed Notsu Y, Yano S, Shibata H, Nagai A, Nabika T. Plasma arginine/ADMA ratio as a sensitive risk marker for atherosclerosis: Shimane CoHRE study. Atherosclerosis. 2015;239:61–6.CrossRefPubMed
39.
40.
go back to reference Xie L, Talukder MA, Sun J, Varadharaj S, Zweier JL. Liposomal tetrahydrobiopterin preserves eNOS coupling in the post-ischemic heart conferring in vivo cardioprotection. J Mol Cell Cardiol. 2015;86:14–22.CrossRefPubMedPubMedCentral Xie L, Talukder MA, Sun J, Varadharaj S, Zweier JL. Liposomal tetrahydrobiopterin preserves eNOS coupling in the post-ischemic heart conferring in vivo cardioprotection. J Mol Cell Cardiol. 2015;86:14–22.CrossRefPubMedPubMedCentral
41.
go back to reference Vasquez-Vivar J, Kalyanaraman B, Martasek P. The role of tetrahydrobiopterin in superoxide generation from eNOS: enzymology and physiological implications. Free Radic Res. 2003;37:121–7.CrossRefPubMed Vasquez-Vivar J, Kalyanaraman B, Martasek P. The role of tetrahydrobiopterin in superoxide generation from eNOS: enzymology and physiological implications. Free Radic Res. 2003;37:121–7.CrossRefPubMed
42.
go back to reference Sugiyama T, Levy BD, Michel T. Tetrahydrobiopterin recycling, a key determinant of endothelial nitric-oxide synthase-dependent signaling pathways in cultured vascular endothelial cells. J Biol Chem. 2009;284:12691–700.CrossRefPubMedPubMedCentral Sugiyama T, Levy BD, Michel T. Tetrahydrobiopterin recycling, a key determinant of endothelial nitric-oxide synthase-dependent signaling pathways in cultured vascular endothelial cells. J Biol Chem. 2009;284:12691–700.CrossRefPubMedPubMedCentral
43.
go back to reference Kim HJ, Son J, Jin E, Lee J, Park S. Effects of exercise and l-arginine intake on inflammation in aorta of high-fat diet induced obese rats. J Exerc Nutr Biochem. 2016;20:36–40. Kim HJ, Son J, Jin E, Lee J, Park S. Effects of exercise and l-arginine intake on inflammation in aorta of high-fat diet induced obese rats. J Exerc Nutr Biochem. 2016;20:36–40.
44.
go back to reference Nguyen MC, Park JT, Jeon YG, Jeon BH, Hoe KL, Kim YM, et al. Arginase inhibition restores peroxynitrite-induced endothelial dysfunction via l-arginine-dependent endothelial nitric oxide synthase phosphorylation. Yonsei Med J. 2016;57:1329–38.CrossRefPubMedPubMedCentral Nguyen MC, Park JT, Jeon YG, Jeon BH, Hoe KL, Kim YM, et al. Arginase inhibition restores peroxynitrite-induced endothelial dysfunction via l-arginine-dependent endothelial nitric oxide synthase phosphorylation. Yonsei Med J. 2016;57:1329–38.CrossRefPubMedPubMedCentral
45.
go back to reference Bahadoran Z, Mirmiran P, Tahmasebinejad Z, Azizi F. Dietary l-arginine intake and the incidence of coronary heart disease: Tehran lipid and glucose study. Nutr Metab (Lond). 2016;13:23.CrossRef Bahadoran Z, Mirmiran P, Tahmasebinejad Z, Azizi F. Dietary l-arginine intake and the incidence of coronary heart disease: Tehran lipid and glucose study. Nutr Metab (Lond). 2016;13:23.CrossRef
46.
47.
go back to reference You H, Gao T, Cooper TK, Morris SM Jr, Awad AS. Arginase inhibition: a new treatment for preventing progression of established diabetic nephropathy. Am J Physiol Renal Physiol. 2015;309:F447-55.CrossRefPubMed You H, Gao T, Cooper TK, Morris SM Jr, Awad AS. Arginase inhibition: a new treatment for preventing progression of established diabetic nephropathy. Am J Physiol Renal Physiol. 2015;309:F447-55.CrossRefPubMed
50.
go back to reference Pham TN, Bordage S, Pudlo M, Demougeot C, Thai KM, Girard-Thernier C. Cinnamide derivatives as mammalian arginase inhibitors: synthesis, biological evaluation and molecular docking. Int J Mol Sci 2016;17:1656CrossRefPubMedCentral Pham TN, Bordage S, Pudlo M, Demougeot C, Thai KM, Girard-Thernier C. Cinnamide derivatives as mammalian arginase inhibitors: synthesis, biological evaluation and molecular docking. Int J Mol Sci 2016;17:1656CrossRefPubMedCentral
51.
go back to reference Shin W, Cuong TD, Lee JH, Min B, Jeon BH, Lim HK, et al. Arginase inhibition by ethylacetate extract of Caesalpinia sappan lignum contributes to activation of endothelial nitric oxide synthase. Korean J Physiol Pharmacol. 2011;15:123–8.CrossRefPubMedPubMedCentral Shin W, Cuong TD, Lee JH, Min B, Jeon BH, Lim HK, et al. Arginase inhibition by ethylacetate extract of Caesalpinia sappan lignum contributes to activation of endothelial nitric oxide synthase. Korean J Physiol Pharmacol. 2011;15:123–8.CrossRefPubMedPubMedCentral
52.
go back to reference JS Z. L L, FY C. Tetrahydrobiopterin and vascular endothelial dysfunction. Prog Physiol Sci. 2004;35:155–8. JS Z. L L, FY C. Tetrahydrobiopterin and vascular endothelial dysfunction. Prog Physiol Sci. 2004;35:155–8.
53.
go back to reference Antoniades C, Bakogiannis C, Leeson P, Guzik TJ, Zhang MH, Tousoulis D, et al. Rapid, direct effects of statin treatment on arterial redox state and nitric oxide bioavailability in human atherosclerosis via tetrahydrobiopterin-mediated endothelial nitric oxide synthase coupling. Circulation. 2011;124:335–45.CrossRefPubMedPubMedCentral Antoniades C, Bakogiannis C, Leeson P, Guzik TJ, Zhang MH, Tousoulis D, et al. Rapid, direct effects of statin treatment on arterial redox state and nitric oxide bioavailability in human atherosclerosis via tetrahydrobiopterin-mediated endothelial nitric oxide synthase coupling. Circulation. 2011;124:335–45.CrossRefPubMedPubMedCentral
54.
go back to reference Herranz B, Marquez S, Guijarro B, Aracil E, Aicart-Ramos C, Rodriguez-Crespo I, et al. Integrin-linked kinase regulates vasomotor function by preventing endothelial nitric oxide synthase uncoupling: role in atherosclerosis. Circ Res. 2012;110:439–49.CrossRefPubMed Herranz B, Marquez S, Guijarro B, Aracil E, Aicart-Ramos C, Rodriguez-Crespo I, et al. Integrin-linked kinase regulates vasomotor function by preventing endothelial nitric oxide synthase uncoupling: role in atherosclerosis. Circ Res. 2012;110:439–49.CrossRefPubMed
55.
go back to reference Zhou MM. Protective effect and mechanism of propofol on endothelial injury induced by high glucose. Shanghai: Fudan University; 2012. Zhou MM. Protective effect and mechanism of propofol on endothelial injury induced by high glucose. Shanghai: Fudan University; 2012.
56.
go back to reference Liu JB, Wang G, Hong TP. Fenofibrate promotes endothelial nitric oxide synthase coupling by up regulating the level of four hydrogen biopterin. In: Annual meeting of endocrinology and diabetes branch of Beijing Medical Association. 2011. Liu JB, Wang G, Hong TP. Fenofibrate promotes endothelial nitric oxide synthase coupling by up regulating the level of four hydrogen biopterin. In: Annual meeting of endocrinology and diabetes branch of Beijing Medical Association. 2011.
57.
go back to reference Zhang HP. Vasodilatation effect and anti eNOS coupling mechanism of 7 Chinese herbal extracts. Thesis, Shanghai university of Chinese medicine. 2010. Zhang HP. Vasodilatation effect and anti eNOS coupling mechanism of 7 Chinese herbal extracts. Thesis, Shanghai university of Chinese medicine. 2010.
58.
go back to reference Hofmeister LH, Lee SH, Norlander AE, Montaniel KR, Chen W, Harrison DG, et al. Phage-display-guided nanocarrier targeting to atheroprone vasculature. ACS Nano. 2015;9:4435–46.CrossRefPubMedPubMedCentral Hofmeister LH, Lee SH, Norlander AE, Montaniel KR, Chen W, Harrison DG, et al. Phage-display-guided nanocarrier targeting to atheroprone vasculature. ACS Nano. 2015;9:4435–46.CrossRefPubMedPubMedCentral
59.
go back to reference Li H, Forstermann U. Uncoupling of endothelial NO synthase in atherosclerosis and vascular disease. Curr Opin Pharmacol. 2013;13:161–7.CrossRefPubMed Li H, Forstermann U. Uncoupling of endothelial NO synthase in atherosclerosis and vascular disease. Curr Opin Pharmacol. 2013;13:161–7.CrossRefPubMed
60.
go back to reference Bhardwaj P, Khanna D, Balakumar P. Catechin averts experimental diabetes mellitus-induced vascular endothelial structural and functional abnormalities. Cardiovasc Toxicol. 2014;14:41–51.CrossRefPubMed Bhardwaj P, Khanna D, Balakumar P. Catechin averts experimental diabetes mellitus-induced vascular endothelial structural and functional abnormalities. Cardiovasc Toxicol. 2014;14:41–51.CrossRefPubMed
61.
go back to reference Jung CH, Lee WJ, Hwang JY, Lee MJ, Seol SM, Kim YM, et al. The preventive effect of uncarboxylated osteocalcin against free fatty acid-induced endothelial apoptosis through the activation of phosphatidylinositol 3-kinase/Akt signaling pathway. Metabolism. 2013;62:1250–7.CrossRefPubMed Jung CH, Lee WJ, Hwang JY, Lee MJ, Seol SM, Kim YM, et al. The preventive effect of uncarboxylated osteocalcin against free fatty acid-induced endothelial apoptosis through the activation of phosphatidylinositol 3-kinase/Akt signaling pathway. Metabolism. 2013;62:1250–7.CrossRefPubMed
62.
go back to reference CM W. H L, JY W. The mechanism of berberine regulating eNOS/NO to protect HUVECs damage induced by palmitic acid. J Beihua Univ (Nat Sci). 2014;15:743–6. CM W. H L, JY W. The mechanism of berberine regulating eNOS/NO to protect HUVECs damage induced by palmitic acid. J Beihua Univ (Nat Sci). 2014;15:743–6.
63.
go back to reference Go YM, Lee HR, Park H. H(2)S inhibits oscillatory shear stress-induced monocyte binding to endothelial cells via nitric oxide production. Mol Cells. 2012;34:449–55.CrossRefPubMedPubMedCentral Go YM, Lee HR, Park H. H(2)S inhibits oscillatory shear stress-induced monocyte binding to endothelial cells via nitric oxide production. Mol Cells. 2012;34:449–55.CrossRefPubMedPubMedCentral
64.
go back to reference LJ LL. Z. Hydrogen sulfide: a new target for atherosclerosis research Chinese. J Arterioscler. 2015;23:201–6. LJ LL. Z. Hydrogen sulfide: a new target for atherosclerosis research Chinese. J Arterioscler. 2015;23:201–6.
65.
go back to reference Li W, Tang C, Jin H, Du J. Effects of onion extract on endogenous vascular H2S and adrenomedulin in rat atherosclerosis. Curr Pharm Biotechnol. 2011;12:1427–39.CrossRefPubMed Li W, Tang C, Jin H, Du J. Effects of onion extract on endogenous vascular H2S and adrenomedulin in rat atherosclerosis. Curr Pharm Biotechnol. 2011;12:1427–39.CrossRefPubMed
66.
go back to reference Hayashi T, Yamaguchi T, Sakakibara Y, Taguchi K, Maeda M, Kuzuya M, et al. eNOS-dependent antisenscence effect of a calcium channel blocker in human endothelial cells. PLoS One. 2014;9:e88391.CrossRefPubMedPubMedCentral Hayashi T, Yamaguchi T, Sakakibara Y, Taguchi K, Maeda M, Kuzuya M, et al. eNOS-dependent antisenscence effect of a calcium channel blocker in human endothelial cells. PLoS One. 2014;9:e88391.CrossRefPubMedPubMedCentral
67.
go back to reference Liu SJ, Liu WH, Zhong Y, Liu SM. Glycogen synthase kinase-3beta is involved in C-reactive protein-induced endothelial cell activation. Biochemistry. 2013;78:915–9.PubMed Liu SJ, Liu WH, Zhong Y, Liu SM. Glycogen synthase kinase-3beta is involved in C-reactive protein-induced endothelial cell activation. Biochemistry. 2013;78:915–9.PubMed
68.
go back to reference da Motta NA, Kummerle AE, Marostica E, Dos Santos CF, Fraga CA, Barreiro EJ, et al. Anti-atherogenic effects of a new thienylacylhydrazone derivative, LASSBio-788, in rats fed a hypercholesterolemic diet. J Pharmacol Sci. 2013;123:47–57.CrossRefPubMed da Motta NA, Kummerle AE, Marostica E, Dos Santos CF, Fraga CA, Barreiro EJ, et al. Anti-atherogenic effects of a new thienylacylhydrazone derivative, LASSBio-788, in rats fed a hypercholesterolemic diet. J Pharmacol Sci. 2013;123:47–57.CrossRefPubMed
Metadata
Title
Roles of eNOS in atherosclerosis treatment
Authors
Fen-fang Hong
Xiao-yu Liang
Wei Liu
Sha Lv
Shu-jin He
Hai-bin Kuang
Shu-long Yang
Publication date
01-06-2019
Publisher
Springer International Publishing
Published in
Inflammation Research / Issue 6/2019
Print ISSN: 1023-3830
Electronic ISSN: 1420-908X
DOI
https://doi.org/10.1007/s00011-019-01229-9

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