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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Mitochondrion as a Selective Target for the Treatment of Atherosclerosis: Role of Mitochondrial DNA Mutations and Defective Mitophagy in the Pathogenesis of Atherosclerosis and Chronic Inflammation

Author(s): Alexander N. Orekhov*, Anastasia V. Poznyak, Igor A. Sobenin, Nikita N. Nikifirov and Ekaterina A. Ivanova

Volume 18, Issue 11, 2020

Page: [1064 - 1075] Pages: 12

DOI: 10.2174/1570159X17666191118125018

Price: $65

Abstract

Background: Atherosclerosis is a chronic inflammatory condition that affects different arteries in the human body and often leads to severe neurological complications, such as stroke and its sequelae. Affected blood vessels develop atherosclerotic lesions in the form of focal thickening of the intimal layer, so called atherosclerotic plaques.

Objectives: Despite the high priority of atherosclerosis research for global health and the numerous preclinical and clinical studies conducted, currently, there is no effective pharmacological treatment that directly impacts atherosclerotic plaques. Many knowledge gaps exist in our understanding of the mechanisms of plaque formation. In this review, we discuss the role of mitochondria in different cell types involved in atherogenesis and provide information about mtDNA mutations associated with the disease.

Results: Mitochondria of blood and arterial wall cells appear to be one of the important factors in disease initiation and development. Significant experimental evidence connects oxidative stress associated with mitochondrial dysfunction and vascular disease. Moreover, mitochondrial DNA (mtDNA) deletions and mutations are being considered as potential disease markers. Further study of mtDNA damage and associated dysfunction may open new perspectives for atherosclerosis treatment.

Conclusion: Mitochondria can be considered as important disease-modifying factors in several chronic pathologies. Deletions and mutations of mtDNA may be used as potential disease markers. Mitochondria-targeting antioxidant therapies appear to be promising for the development of treatment of atherosclerosis and other diseases associated with oxidative stress and chronic inflammation.

Keywords: Atherosclerosis, mitochondrion, inflammation, mtDNA, oxidative stress, LDL metabolism.

Graphical Abstract

[1]
Herrington, W; Lacey, B; Sherliker, P; Armitage, J; Lewington, S Epidemiology of Atherosclerosis and the Potential to Reduce the Global Burden of Atherothrombotic Disease. Circ. Res., 2016, 118(4), 535-46.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.307611]
[2]
Marulanda-Londoño, E; Chaturvedi, S Stroke due to large vessel atherosclerosis: Five new things. Neurol Clin Pract., 2016, 6(3), 252-258.
[http://dx.doi.org/10.1212/CPJ.0000000000000247]
[3]
Dima-Cozma, C. Atherosclerosis in the young adult: Fewer hypotheses, more facts. Rev. Med. Chir. Soc. Med. Nat. Iasi., 2016, 120(4), 768-76.
[4]
Orekhov, A.N.; Ivanova, E.A. Introduction of the special issue “Atherosclerosis and related diseases”. Vessel Plus, 2017, 1, 163-165.
[http://dx.doi.org/10.20517/2574-1209.2017.33]
[5]
Katsouras, C.S.; Baltogiannis, G.G.; Naka, K.K.; Roukos, D.H.; Michalis, L.K. Decoding coronary artery disease: somatic mosaicism and genomics for personal and population risk prediction. Biomarkers Med., 2013, 7(2), 189-192.
[http://dx.doi.org/10.2217/bmm.13.4] [PMID: 23547811]
[6]
Sazonova, M.A.; Sinyov, V.V.; Barinova, V.A.; Ryzhkova, A.I.; Zhelankin, A.V.; Postnov, A.Y.; Sobenin, I.A.; Bobryshev, Y.V.; Orekhov, A.N. Mosaicism of mitochondrial genetic variation in atherosclerotic lesions of the human aorta. BioMed Res. Int., 2015, 2015825468
[http://dx.doi.org/10.1155/2015/825468] [PMID: 25834827]
[7]
van der Bliek, A.M.; Sedensky, M.M.; Morgan, P.G. Cell Biology of the Mitochondrion. Genetics, 2017, 207(3), 843-871. Review. Erratum in: Genetics. 2018, 208. [4] :1673. PubMed Genetics,
[http://dx.doi.org/10.1534/genetics.117.300262] [PMID: 29097398]
[8]
Aliev, G.; Obrenovich, ME; Tabrez, S; Jabir, NR; Reddy, VP; Li, Y; Burnstock, G; Cacabelos, R; Kamal, MA Link between cancer and Alzheimer disease via oxidative stress induced by nitric oxide-dependent mitochondrial DNA over proliferation and deletion. Oxid Med Cell Longev., 2013.
[http://dx.doi.org/10.1155/2013/962984]
[9]
Truban, D; Hou, X; Caulfield, TR; Fiesel, FC; Springer, W PINK1, Parkin, and Mitochondrial Quality Control: What can we Learn about Parkinson’s Disease pathobiology? J. Parkinsons Dis., 2017, 7(1), 13-29.
[http://dx.doi.org/10.3233/JPD-160989]
[10]
Gowdar, S.; Syal, S.; Chhabra, L. Probable protective role of diabetes mellitus in takotsubo cardiomyopathy: a review. Vessel Plus, 2017, 1, 129-136.
[http://dx.doi.org/10.20517/2574-1209.2017.12]
[11]
Stefano, G.B.; Bjenning, C.; Wang, F.; Wang, N.; Kream, R.M. mitochondrial heteroplasmy. Adv. Exp. Med. Biol., 2017, 982, 577-594.
[http://dx.doi.org/10.1007/978-3-319-55330-6_30]
[12]
Sazonova, M.A.; Sinyov, V.V.; Ryzhkova, A.I.; Galitsyna, E.V.; Melnichenko, AA; Postnov, AY; Orekhov, A.N.; Sobenin, I.A. Cybrid models of pathological cell processes in different diseases. Oxid. Med. Cell Longev., 2018, eCollection.,
[http://dx.doi.org/10.1155/2018/4647214]
[13]
Ruparelia, N.; Chai, J.T.; Fisher, E.A.; Choudhury, R.P. Inflammatory processes in cardiovascular disease: a route to targeted therapies. Nat. Rev. Cardiol., 2017, 14(3), 133-144.
[http://dx.doi.org/10.1038/nrcardio.2016.185] [PMID: 27905474]
[14]
Caja, S.; Enríquez, J.A. Mitochondria in endothelial cells: Sensors and integrators of environmental cues. Redox Biol., 2017, 821-827.
[http://dx.doi.org/10.1016/j.redox.2017.04.021]
[15]
Gimbrone, M.A. Jr.; García-Cardeña, G. Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ. Res., 2016, 118(4), 620-636.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.306301]
[16]
Kroemer, G.; Galluzzi, L.; Brenner, C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev., 2007, 87(1), 99-163.
[http://dx.doi.org/10.1152/physrev.00013.2006]
[17]
De Bock, K.; Georgiadou, M.; Carmeliet, P. Role of endothelial cell metabolism in vessel sprouting. Cell Metab., 2013, 18(5), 634-47.
[http://dx.doi.org/10.1016/j.cmet.2013.08.001]
[18]
Golub, A.S.; Song, B.K.; Pittman, R.N. The rate of O loss from mesenteric arterioles is not unusually high. Am. J. Physiol. Heart Circ. Physiol., 2011, 301(3), H737-H745.
[http://dx.doi.org/10.1152/ajpheart.00353.2011] [PMID: 21685269]
[19]
Haslip, M.; Dostanic, I.; Huang, Y.; Zhang, Y.; Russell, K.S.; Jurczak, M.J.; Mannam, P.; Giordano, F.; Erzurum, S.C.; Lee, P.J. Endothelial uncoupling protein 2 regulates mitophagy and pulmonary hypertension during intermittent hypoxia. Arterioscler. Thromb. Vasc. Biol., 2015, 35(5), 1166-1178.
[http://dx.doi.org/10.1161/ATVBAHA.114.304865] [PMID: 25814675]
[20]
Widlansky, M.E.; Gutterman, D.D. Regulation of endothelial function by mitochondrial reactive oxygen species. Antioxid. Redox Signal., 2011, 15(6), 1517-30.
[http://dx.doi.org/10.1089/ars.2010.3642]
[21]
Chen, F.; Haigh, S.; Barman, S.; Fulton, D.J. From form to function: the role of Nox4 in the cardiovascular system. Front. Physiol., 2012, 3, 412.
[http://dx.doi.org/10.3389/fphys.2012.00412]
[22]
Chistiakov, DA; Melnichenko, AA; Myasoedova, V.A.; Grechko, AV; Orekhov, A.N. Mechanisms of foam cell formation in atherosclerosis. J. Mol. Med. (Berl), 2017, 95(11), 1153-1165.
[23]
Kieser, K.J.; Kagan, J.C. Multi-receptor detection of individual bacterial products by the innate immune system. Nat. Rev. Immunol., 2017, 17(6), 376-390.
[http://dx.doi.org/10.1038/nri.2017.25]
[24]
Tur, J.; Vico, T.; Lloberas, J.; Zorzano, A.; Celada, A. Macrophages and mitochondria: A critical interplay between metabolism, signaling, and the functional activity. Adv. Immunol., 2017, 1-36.
[25]
Liu, P.S.; Ho, P.C. Mitochondria: A master regulator in macrophage and T cell immunity. Mitochondrion, 2018.
[http://dx.doi.org/10.1016/j.mito.2017.11.002]
[26]
Sinyov, V.V.; Sazonova, M.A.; Ryzhkova, A.I.; Galitsyna, E.V.; Melnichenko, A.A.; Postnov, A.Y.; Orekhov, A.N.; Grechko, A.V.; Sobenin, I.A. Potential use of buccal epithelium for genetic diagnosis of atherosclerosis using mtDNA mutations. Vessel Plus, 2017, 1, 145-150.
[http://dx.doi.org/10.20517/2574-1209.2016.04]
[27]
Zhong, Z.; Umemura, A.; Sanchez-Lopez, E.; Liang, S.; Shalapour, S.; Wong, J.; He, F.; Boassa, D.; Perkins, G.; Ali, S.R.; McGeough, M.D.; Ellisman, M.H.; Seki, E.; Gustafsson, A.B.; Hoffman, H.M.; Diaz-Meco, M.T.; Moscat, J.; Karin, M. NF-κB restricts inflammasome activation via elimination of damaged mitochondria. Cell, 2016, 164(5), 896-910.
[http://dx.doi.org/10.1016/j.cell.2015.12.057] [PMID: 26919428]
[28]
Finucane, O.M.; Sugrue, J.; Rubio-Araiz, A.; Guillot-Sestier, M.V.; Lynch, M.A. The NLRP3 inflammasome modulates glycolysis by increasing PFKFB3 in an IL-1β-dependent manner in macrophages. Sci. Rep., 2019, 9(1), 4034.
[http://dx.doi.org/10.1038/s41598-019-40619-1] [PMID: 30858427]
[29]
O'Neill, L.A.; Pearce, E.J. Immunometabolism governs dendritic cell and macrophage function. J. Exp. Med., 2016, 213(1), 15-23.
[30]
Nonnenmacher, Y.; Hiller, K. Biochemistry of proinflammatory macrophage activation. Cell. Mol. Life Sci., 2018, 75(12), 2093-2109.
[http://dx.doi.org/10.1007/s00018-018-2784-1] [PMID: 29502308]
[31]
Huang, S.C.; Smith, A.M.; Everts, B.; Colonna, M.; Pearce, E.L.; Schilling, J.D.; Pearce, E.J. Metabolic reprogramming mediated by the mtorc2-irf4 signaling axis is essential for macrophage alternative activation. Immunity, 2016, 45(4), 817-830.
[http://dx.doi.org/10.1016/j.immuni.2016.09.016] [PMID: 27760338]
[32]
Bories, G.F.P.; Leitinger, N. Macrophage metabolism in atherosclerosis. FEBS Lett., 2017, 591(19), 3042-3060.
[http://dx.doi.org/10.1002/1873-3468.12786] [PMID: 28796886]
[33]
Andreeva, E.R.; Pugach, I.M.; Gordon, D.; Orekhov, A.N. Continuous subendothelial network formed by pericyte-like cells in human vascular bed. Tissue Cell, 1998, 30(1), 127-135.
[http://dx.doi.org/10.1016/S0040-8166(98)80014-1] [PMID: 9569686]
[34]
Orekhov, A.N.; Bobryshev, Y.V.; Chistiakov, D.A. The complexity of cell composition of the intima of large arteries: focus on pericyte-like cells. Cardiovasc. Res., 2014, 103(4), 438-451.
[http://dx.doi.org/10.1093/cvr/cvu168]
[35]
Vásquez-Trincado, C.; García-Carvajal, I.; Pennanen, C.; Parra, V.; Hill, J.A.; Rothermel, B.A.; Lavandero, S. Mitochondrial dynamics, mitophagy and cardiovascular disease. J. Physiol., 2016, 594(3), 509-25.
[36]
Summerhill, V.; Orekhov, A. Pericytes in Atherosclerosis. Adv. Exp. Med. Biol., 2019, 1147, 279-297.
[http://dx.doi.org/10.1007/978-3-030-16908-4_13] [PMID: 31147883]
[37]
Price, T.O.; Sheibani, N.; Shah, G.N. Regulation of high glucose-induced apoptosis of brain pericytes by mitochondrial CA VA: A specific target for prevention of diabetic cerebrovascular pathology. Biochim. Biophys. Acta Mol. Basis Dis., 2017, 1863(4), 929-935.
[http://dx.doi.org/10.1016/j.bbadis.2017.01.025] [PMID: 28131914]
[38]
Chalmers, S.; Saunter, C.D.; Girkin, J.M.; McCarron, J.G. Age decreases mitochondrial motility and increases mitochondrial size in vascular smooth muscle. J. Physiol., 2016, 594(15), 4283-4295.
[http://dx.doi.org/10.1113/JP271942] [PMID: 26959407]
[39]
Marsboom, G.; Toth, P.T.; Ryan, J.J.; Hong, Z.; Wu, X.; Fang, Y.H.; Thenappan, T.; Piao, L.; Zhang, H.J.; Pogoriler, J.; Chen, Y.; Morrow, E.; Weir, E.K.; Rehman, J.; Archer, S.L. Dynamin-related protein 1-mediated mitochondrial mitotic fission permits hyperproliferation of vascular smooth muscle cells and offers a novel therapeutic target in pulmonary hypertension. Circ. Res., 2012, 110(11), 1484-1497.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.263848] [PMID: 22511751]
[40]
Salabei, J.K.; Hill, B.G. Mitochondrial fission induced by platelet-derived growth factor regulates vascular smooth muscle cell bioenergetics and cell proliferation. Redox Biol., 2013, 1(1), 542-51.
[http://dx.doi.org/10.1016/j.redox.2013.10.011]
[41]
Pisoschi, A.M.; Pop, A. The role of antioxidants in the chemistry of oxidative stress: A review. Eur. J. Med. Chem., 2015, 55-74.
[http://dx.doi.org/10.1016/j.ejmech.2015.04.040]
[42]
Kattoor, A.J.; Pothineni, N.V.K.; Palagiri, D.; Mehta, J.L. Oxidative Stress in Atherosclerosis. Curr. Atheroscler. Rep., 2017, 19(11), 42.
[http://dx.doi.org/10.1007/s11883-017-0678-6]]
[43]
Förstermann, U.; Xia, N.; Li, H. Roles of vascular oxidative stress and nitric oxide in the pathogenesis of atherosclerosis. Circ. Res., 2017, 120(4.)
[http://dx.doi.org/10.1161/CIRCRESAHA.116.309326]]
[44]
Aliev, G.; Gasimov, E.; Obrenovich, M.E.; Fischbach, K.; Shenk, J.C.; Smith, M.A.; Perry, G. Atherosclerotic lesions and mitochondria DNA deletions in brain microvessels: implication in the pathogenesis of Alzheimer’s disease. Vasc. Health Risk Manag., 2008, 4(3), 721-730.
[http://dx.doi.org/10.2147/VHRM.S2608] [PMID: 18827923]
[45]
Aliev, G.; Smith, M.A.; de la Torre, J.C.; Perry, G. Discuss how the oxidative stress indices and initiates mtDNA overproliferation that when become as a de compensatory stages mtDNA deletion is occurs. Mitochondrion, 2004, 4(5-6), 649-663.
[http://dx.doi.org/10.1016/j.mito.2004.07.018] [PMID: 16120422]
[46]
Nicolson, G.L. Mitochondrial Dysfunction and chronic disease: treatment with natural supplements. Integr. Med. (Encinitas), 2014, 13(4), 35-43.
[PMID: 26770107]
[47]
Twig, G; Shirihai, OS The interplay between mitochondrial dynamics and mitophagy. Antioxid. Redox Signal., 2011, 14(10), 1939-51.
[http://dx.doi.org/10.1089/ars.2010.3779]
[48]
Chistiakov, DA; Shkurat, TP; Melnichenko, AA; Grechko, AV; Orekhov, AN The role of mitochondrial dysfunction in cardiovascular disease: a brief review. Ann. Med., 2018, 20(2), 121-127.
[http://dx.doi.org/10.1080/07853890.2017.1417631]
[49]
Ballinger, S.W.; Patterson, C.; Knight-Lozano, C.A.; Burow, D.L.; Conklin, C.A.; Hu, Z.; Reuf, J.; Horaist, C.; Lebovitz, R.; Hunter, G.C.; McIntyre, K.; Runge, M.S. Mitochondrial integrity and function in atherogenesis. Circulation, 2002, 106(5), 544-549.
[http://dx.doi.org/10.1161/01.CIR.0000023921.93743.89] [PMID: 12147534]
[50]
Yu, E.; Calvert, P.A.; Mercer, J.R.; Harrison, J.; Baker, L.; Figg, N.L.; Kumar, S.; Wang, J.C.; Hurst, L.A.; Obaid, D.R.; Logan, A.; West, N.E.; Clarke, M.C.; Vidal-Puig, A.; Murphy, M.P.; Bennett, M.R. Mitochondrial DNA damage can promote atherosclerosis independently of reactive oxygen species through effects on smooth muscle cells and monocytes and correlates with higher-risk plaques in humans. Circulation, 2013, 128(7), 702-712.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.113.002271] [PMID: 23841983]
[51]
Alipov, V.I.; Sukhorukov, V.N.; Karagodin, V.P.; Grechko, A.V.; Orekhov, A.N. Chemical composition of circulating native and desialylated low density lipoprotein: what is the difference? Vessel Plus, 2017, 1, 107-115.
[http://dx.doi.org/10.20517/2574-1209.2017.20]
[52]
Chistiakov, DA The complexity of cell composition of the intima of large arteries: focus on pericyte-like cells. Cardiovasc. Res., 2014, 103(4), 438-51.
[53]
Xu, Q; Yuan, F; Shen, X; Wen, H; Li, W; Cheng, B; Wu, J Polymorphisms of C242T and A640G in CYBA gene and the risk of coronary artery disease: a meta-analysis. PLoS One., 2014.
[54]
Fujimoto, H.; Taguchi, J.; Imai, Y.; Ayabe, S.; Hashimoto, H.; Kobayashi, H.; Ogasawara, K.; Aizawa, T.; Yamakado, M.; Nagai, R.; Ohno, M. Manganese superoxide dismutase polymorphism affects the oxidized low-density lipoprotein-induced apoptosis of macrophages and coronary artery disease. Eur. Heart J., 2008, 29(10), 1267-1274.
[http://dx.doi.org/10.1093/eurheartj/ehm500] [PMID: 17967822]
[55]
Zhang, J.X.; Wang, Z.M.; Zhang, J.J.; Zhu, L.L.; Gao, X.F.; Chen, S.L. Association of glutathione peroxidase-1 (GPx-1) rs1050450 Pro198Leu and Pro197Leu polymorphisms with cardiovascular risk: a meta-analysis of observational studies. J. Geriatr. Cardiol., 2014, 11(2), 141-150.
[http://dx.doi.org/10.3969/j.issn.1671-5411.2014.02.003] [PMID: 25009565]
[56]
Boya, P.; Reggiori, F.; Codogno, P. Emerging regulation and functions of autophagy. Nat. Cell Biol., 2013, 15(7), 713-720.
[http://dx.doi.org/10.1038/ncb2788] [PMID: 23817233]
[57]
Narendra, D.; Tanaka, A.; Suen, D.F.; Youle, R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol., 2008, 183(5), 795-803.
[http://dx.doi.org/10.1083/jcb.200809125] [PMID: 19029340]
[58]
Swiader, A.; Nahapetyan, H.; Faccini, J.; D’Angelo, R.; Mucher, E.; Elbaz, M.; Boya, P.; Vindis, C. Mitophagy acts as a safeguard mechanism against human vascular smooth muscle cell apoptosis induced by atherogenic lipids. Oncotarget, 2016, 7(20), 28821-28835.
[http://dx.doi.org/10.18632/oncotarget.8936] [PMID: 27119505]
[59]
Grootaert, M.O.J.; Roth, L.; Schrijvers, D.M.; De Meyer, G.R.Y.; Martinet, W. Defective autophagy in atherosclerosis: To die or to senesce? Oxid. Med. Cell. Longev., 2018, 2018,7687083.
[60]
Liao, X.; Sluimer, J.C.; Wang, Y.; Subramanian, M.; Brown, K.; Pattison, J.S.; Robbins, J.; Martinez, J.; Tabas, I. Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab., 2012, 15(4), 545-553.
[http://dx.doi.org/10.1016/j.cmet.2012.01.022] [PMID: 22445600]
[61]
Peng, W.; Cai, G.; Xia, Y.; Chen, J.; Wu, P.; Wang, Z.; Li, G.; Wei, D. Mitochondrial Dysfunction in Atherosclerosis. DNA Cell Biol., 2019, 38(7), 597-606.
[http://dx.doi.org/10.1089/dna.2018.4552]
[62]
Zhang, Z.; Meng, P.; Han, Y.; Shen, C.; Li, B.; Hakim, M.A.; Zhang, X.; Lu, Q.; Rong, M.; Lai, R. Mitochondrial DNA-LL-37 Complex promotes atherosclerosis by escaping from autophagic recognition. Immunity, 2015, 43(6), 1137-1147.
[http://dx.doi.org/10.1016/j.immuni.2015.10.018] [PMID: 26680206]
[63]
Sazonova, M.A.; Sinyov, V.V.; Ryzhkova, A.I.; Galitsyna, E.V.; Khasanova, Z.B.; Postnov, A.Y.; Yarygina, E.I.; Orekhov, A.N.; Sobenin, I.A. Role of mitochondrial genome mutations in pathogenesis of carotid atherosclerosis. Oxid. Med. Cell. Longev., 2017, 2017,6934394.
[http://dx.doi.org/10.1155/2017/6934394]] [PMID: 28951770]
[64]
Sobenin, I.A.; Zhelankin, A.V.; Mitrofanov, K.Y.; Sinyov, V.V.; Sazonova, M.A.; Postnov, A.Y.; Orekhov, A.N. Mutations of mitochondrial DNA in atherosclerosis and atherosclerosis-related diseases. Curr. Pharm. Des., 2015, 21(9), 1158-63.
[http://dx.doi.org/10.2174/1381612820666141013133000]
[65]
Sobenin, I.A.; Sazonova, M.A.; Postnov, A.Y.; Salonen, J.T.; Bobryshev, Y.V.; Orekhov, A.N. Association of mitochondrial genetic variation with carotid atherosclerosis. PLoS One, 2013, 8(7),e68070.
[66]
Orekhov, A.N.; Zhelankin, A.V.; Kolmychkova, K.I.; Mitrofanov, K.Y.; Kubekina, M.V.; Ivanova, E.A.; Sobenin, I.A. Susceptibility of monocytes to activation correlates with atherogenic mitochondrial DNA mutations. Exp. Mol. Pathol., 2015, 99(3), 672-676.
[http://dx.doi.org/10.1016/j.yexmp.2015.11.006] [PMID: 26551079]
[67]
Warren, L.; Bryder, D.; Weissman, I.L.; Quake, S.R. Transcription factor profiling in individual hematopoietic progenitors by digital RT-PCR. Proc. Natl. Acad. Sci. USA, 2006, 103(47), 17807-17812.
[http://dx.doi.org/10.1073/pnas.0608512103] [PMID: 17098862]
[68]
Tertov, V.V.; Sobenin, I.A.; Gabbasov, Z.A.; Popov, E.G.; Jaakkola, O.; Solakivi, T.; Nikkari, T.; Smirnov, V.N.; Orekhov, A.N. Multiple-modified desialylated low density lipoproteins that cause intracellular lipid accumulation. Isolation, fractionation and characterization. Lab. Invest., 1992, 67(5), 665-675.
[PMID: 1434544]
[69]
Tertov, V.V.; Sobenin, I.A.; Gabbasov, Z.A.; Popov, E.G.; Orekhov, A.N. Lipoprotein aggregation as an essential condition of intracellular lipid accumulation caused by modified low density lipoproteins. Biochem. Biophys. Res. Commun., 1989, 163(1), 489-494.
[http://dx.doi.org/10.1016/0006-291X(89)92163-3] [PMID: 2775281]
[70]
Orekhov, A.N.; Nikiforov, N.G.; Elizova, N.V.; Korobov, G.A.; Aladinskaya, A.V.; Sobenin, I.A.; Bobryshev, Y.V. Tumor necrosis factor-α and c-c motif chemokine ligand 18 associate with atherosclerotic lipid accumulation In situ and In vitro. Curr. Pharm. Des., 2018, 24(24), 2883-2889.
[http://dx.doi.org/10.2174/1381612824666180911120726] [PMID: 30205791]
[71]
Meyer, A; Laverny, G; Bernardi, L; Charles, AL; Alsaleh, G; Pottecher, J; Sibilia, J; Geny, B Mitochondria: An organelle of bacterial origin controlling inflammation. Front. Immunol., 2018, 9, 536.
[http://dx.doi.org/10.3389/fimmu.2018.00536]
[72]
Dominic, E.A.; Ramezani, A.; Anker, S.D.; Verma, M.; Mehta, N.; Rao, M. Mitochondrial cytopathies and cardiovascular disease. Heart, 2014, 100(8), 611-8.
[http://dx.doi.org/10.1136/heartjnl-2013-304657]
[73]
Tousoulis, D.; Antoniades, C.; Vasiliadou, C.; Kourtellaris, P.; Koniari, K.; Marinou, K.; Charakida, M.; Ntarladimas, I.; Siasos, G.; Stefanadis, C. Effects of atorvastatin and vitamin C on forearm hyperaemic blood flow, asymmentrical dimethylarginine levels and the inflammatory process in patients with type 2 diabetes mellitus. Heart, 2007, 93(2), 244-246.
[http://dx.doi.org/10.1136/hrt.2006.093112] [PMID: 16914485]
[74]
Michels, A.J.; Frei, B. Myths, artifacts, and fatal flaws: identifying limitations and opportunities in vitamin C research. Nutrients, 2013, 5(12), 5161-92.
[http://dx.doi.org/10.3390/nu5125161]
[75]
Pepe, S.; Marasco, S.F.; Haas, S.J.; Sheeran, F.L.; Krum, H.; Rosenfeldt, F.L. Coenzyme Q10 in cardiovascular disease. Mitochondrion, 2007.
[http://dx.doi.org/10.1016/j.mito.2007.02.005]
[76]
Chen, S; Wang, Y; Zhang, H; Chen, R; Lv, F; Li, Z; Jiang, T; Lin, D; Zhang, H; Yang, L; Kong, X The antioxidant mitoq protects against cse-induced endothelial barrier injury and inflammation by inhibiting ros and autophagy in human umbilical vein endothelial cells. Int. J. Biol. Sci., 2019, 15(7), 1440-1451.
[77]
Graham, D.; Huynh, N.N.; Hamilton, C.A.; Beattie, E.; Smith, R.A.; Cochemé, H.M.; Murphy, M.P.; Dominiczak, A.F. Mitochondria-targeted antioxidant MitoQ10 improves endothelial function and attenuates cardiac hypertrophy. Hypertension, 2009, 54(2), 322-328.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.109.130351] [PMID: 19581509]
[78]
Siasos, G.; Tsigkou, V.; Kosmopoulos, M.; Theodosiadis, D.; Simantiris, S.; Tagkou, NM; Tsimpiktsioglou, A.; Stampouloglou, P.K.; Oikonomou, E.; Mourouzis, K.; Philippou, A.; Vavuranakis, M.; Stefanadis, C.; Tousoulis, D.; Papavassiliou, A.G. Mitochondria and cardiovascular diseases-from pathophysiology to treatment. Ann. Transl. Med., 2018, 6(12), 256.
[http://dx.doi.org/10.21037/atm.2018.06.21]
[79]
Isaev, N.K.; Stelmashook, E.V.; Genrikhs, E.E.; Korshunova, G.A.; Sumbatyan, N.V. Kapkaeva –M.R.; Skulachev. V.P. Neuroprotective properties of mitochondria-targeted antioxidants of the SkQ-type. Rev. Neurosci., 2016, 27(8), 849-855.
[80]
Ng, K.K.; Zheng, G. Molecular interactions in organic nanoparticles for phototheranostic applications. Chem. Rev., 2015, 115(19), 11012-11042.
[http://dx.doi.org/10.1021/acs.chemrev.5b00140] [PMID: 26244706]
[81]
Maytin, E.V.; Anand, S.; Riha, M.; Lohser, S.; Tellez, A.; Ishak, R.; Karpinski, L.; Sot, J.; Hu, B.; Denisyuk, A.; Davis, S.C.; Kyei, A.; Vidimos, A. 5-Fluoruracil enhances protoporphyrin IX accumulation and lesion clearance during photodynamic therapy of actinic keratoses: A mechanism-based clinical trial. Clin. Cancer Res., 2018, 24(13), 3026-3035.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-2020] [PMID: 29593028]
[82]
Ryabova, A.V.; Romanishkin, I.D.; Skobeltsin, A.S.; Moskalev, A.S.; Makarov, V.I.; Loschenov, V.B.; Nikiforov, N.G.; Sobenin, I.A.; Orekhov, A.N. Subcellular anti-atherosclerotic therapy. Vessel Plus, 2019, 3, 17.

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