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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Mutations of mtDNA in some Vascular and Metabolic Diseases

Author(s): Margarita A. Sazonova*, Anastasia I. Ryzhkova, Vasily V. Sinyov, Marina D. Sazonova, Tatiana V. Kirichenko, Natalya A. Doroschuk, Vasily P. Karagodin, Alexander N. Orekhov and Igor A. Sobenin

Volume 27, Issue 2, 2021

Published on: 20 August, 2020

Page: [177 - 184] Pages: 8

DOI: 10.2174/1381612826999200820162154

Price: $65

Abstract

Background: The present review article considers some chronic diseases of vascular and metabolic genesis, the causes of which may be mitochondrial dysfunction. Very often, in the long course of the disease, complications may occur, leading to myocardial infarction or ischemic stroke and, as a result, death. In particular, a large percentage of human deaths nowadays belongs to cardiovascular diseases, such as coronary heart disease (CHD), arterial hypertension, cardiomyopathies, and type 2 diabetes mellitus.

Objective: The aim of the present review was the analysis of literature sources, devoted to an investigation of a link of mitochondrial DNA mutations with chronic diseases of vascular and metabolic genesis.

Results: The analysis of literature indicates the association of the mitochondrial genome mutations with coronary heart disease, type 2 diabetes mellitus, hypertension, and various types of cardiomyopathies.

Conclusion: The detected mutations can be used to analyze the predisposition to chronic diseases of vascular and metabolic genesis. They can also be used to create molecular-cell models necessary to evaluate the effectiveness of drugs developed for the treatment of these pathologies. MtDNA mutations associated with the absence of diseases of vascular and metabolic genesis could be potential candidates for gene therapy of the said diseases.

Keywords: Mitochondrial genome mutation, vascular diseases, metabolic diseases, coronary heart disease, type 2 diabetes mellitus, arterial hypertension, cardiomyopathies.

[1]
Lozano R, Naghavi M, Foreman K, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380(9859): 2095-128.
[http://dx.doi.org/10.1016/S0140-6736(12)61728-0]] [PMID: 23245604]
[2]
Rankinen T, Sarzynski MA, Ghosh S, Bouchard C. Are there genetic paths common to obesity, cardiovascular disease outcomes, and cardiovascular risk factors? Circ Res 2015; 116(5): 909-22. [http://dx.doi.org/10.1161/CIRCRESAHA.116.302888]. [PMID: 25722444].
[3]
Roger VL, Go AS, Lloyd-Jones DM, et al. American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 2012; 125(1): e2-e220. [http://dx.doi.org/10.1161/CIR.0b013e31823ac046]. [PMID: 22179539].
[4]
Reinehr T. Type 2 diabetes mellitus in children and adolescents. World J Diabetes 2013; 4(6): 270-81. [http://dx.doi.org/10.4239/wjd.v4.i6.270]. [PMID: 24379917].
[5]
van der Kooi AL, Snijder MB, Peters RJ, van Valkengoed IG. The Association of Handgrip Strength and Type 2 Diabetes Mellitus in Six Ethnic Groups: An Analysis of the HELIUS Study. PLoS One 2015; 10(9)e0137739 [http://dx.doi.org/10.1371/journal.pone.0137739]. [PMID: 26368020].
[6]
Lipshultz SE, Cochran TR, Briston DA, et al. Pediatric cardiomyopathies: causes, epidemiology, clinical course, preventive strategies and therapies. Future Cardiol 2013; 9(6): 817-48. [http://dx.doi.org/10.2217/fca.13.66]. [PMID: 24180540].
[7]
Sazonova M, Budnikov E, Khasanova Z, Sobenin I, Postnov A, Orekhov A. Studies of the human aortic intima by a direct quantitative assay of mutant alleles in the mitochondrial genome. Atherosclerosis 2009; 204(1): 184-90. [http://dx.doi.org/10.1016/j.atherosclerosis.2008.09.001].
[8]
Sazonova MA, Sinyov VV, Ryzhkova AI, et al. Role of Mitochondrial Genome Mutations in Pathogenesis of Carotid Atherosclerosis. Oxid Med Cell Longev 2017; 20176934394 [http://dx.doi.org/10.1155/2017/6934394]. [PMID: 28951770].
[9]
Sazonova MA, Ryzhkova AI, Sinyov VV, et al. Mitochondrial Genome Mutations Associated with Myocardial Infarction. Dis Markers 2018; 20189749457 [http://dx.doi.org/10.1155/2018/9749457]. [PMID: 29670672].
[10]
Sazonova MA, Ryzhkova AI, Sinyov VV, et al. Mitochondrial mutations associated with cardiac angina. Vessel Plus 2019; 3: 8. [http://dx.doi.org/10.20517/25741209.2019.01].
[11]
Sazonova MA, Sinyov VV, Ryzhkova AI, Sazonova MD, Khasanova ZB, Sobenin IA. MtDNA mutations linked with left ventricular hypertrophy. Vessel Plus 2019; 3: 5. [http://dx.doi.org/10.20517/2574-1209.2018.56].
[12]
Sazonova MA, Sinyov VV, Ryzhkova AI, et al. Creation of Cybrid Cultures Containing mtDNA Mutations m.12315G>A and m.1555G>A, Associated with Atherosclerosis. Biomolecules 2019; 9(9)E499 [http://dx.doi.org/10.3390/biom9090499]. [PMID: 31540444].
[13]
Sazonova MA, Sinyov VV, Ryzhkova AI, et al. Cybrid Models of Pathological Cell Processes in Different Diseases. Oxid Med Cell Longev 2018; 104647214 [http://dx.doi.org/10.1155/2018/4647214].
[14]
Wallace DC, Chalkia D. Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold Spring Harb Perspect Biol 2013; 5(11)a021220 [http://dx.doi.org/10.1101/cshperspect.a021220]. [PMID: 24186072].
[15]
Fetterman JL, Holbrook M, Westbrook DG, et al. Mitochondrial DNA damage and vascular function in patients with diabetes mellitus and atherosclerotic cardiovascular disease. Cardiovasc Diabetol 2016; 15: 53. [http://dx.doi.org/10.1186/s12933-016-0372-y]. [PMID: 27036979].
[16]
Bratic A, Larsson NG. The role of mitochondria in aging. J Clin Invest 2013; 123(3): 951-7. [http://dx.doi.org/10.1172/JCI64125]. [PMID: 23454757].
[17]
Chinnery PF, Thorburn DR, Samuels DC, et al. The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both? Trends Genet 2000; 16(11): 500-5. [http://dx.doi.org/10.1016/S0168-9525(00)02120-X]. [PMID: 11074292].
[18]
Souren NY, Gerdes LA, Kümpfel T, et al. Mitochondrial DNA Variation and Heteroplasmy in Monozygotic Twins Clinically Discordant for Multiple Sclerosis. Hum Mutat 2016; 37(8): 765-75. [http://dx.doi.org/10.1002/humu.23003].
[19]
Xie S, Zhang J, Sun J, et al. Mitochondrial haplogroup D4j specific variant m.11696G> a(MT-ND4) may increase the penetrance and expressivity of the LHON-associated m.11778G;a mutation in Chinese pedigrees. MappSeq Anal 2016; 22: 1-8.
[20]
Chen S, Xie X, Wang Y, et al. Association between leukocyte mitochondrial DNA content and risk of coronary heart disease: a case-control study. Atherosclerosis 2014; 237(1): 220-6. [http://dx.doi.org/10.1016/j.atherosclerosis.2014.08.051]. [PMID: 25244506].
[21]
Catteruccia M, Sauchelli D, Della Marca G, et al. “Myo-cardiomyopathy” is commonly associated with the A8344G “MERRF” mutation. J Neurol 2015; 262(3): 701-10. [http://dx.doi.org/10.1007/s00415-014-7632-0]. [PMID: 25559684].
[22]
Saric A, Andreau K, Armand AS, Møller IM, Petit PX. Barth Syndrome: From Mitochondrial Dysfunctions Associated with Aberrant Production of Reactive Oxygen Species to Pluripotent Stem Cell Studies. Front Genet 2016; 6: 359. [http://dx.doi.org/10.3389/fgene.2015.00359]. [PMID: 26834781].
[23]
Szalardy L, Molnar M, Torok R, et al. Histopathological comparison of Kearns-Sayre syndrome and PGC-1α-deficient mice suggests a novel concept for vacuole formation in mitochondrial encephalopathy. Folia Neuropathol 2016; 54(1): 9-22. [http://dx.doi.org/10.5114/fn.2016.58911]. [PMID: 27179217].
[24]
Chen XY, Zhao SY, Wang Y, et al. A novel mitochondrial DNA deletion in a patient with Pearson syndrome and neonatal diabetes mellitus provides insight into disease etiology, severity and progression. Mitochondrial DNA A DNA Mapp Seq Anal 2016; 27(4): 2492-5. [http://dx.doi.org/10.3109/19401736.2015.1033712]. [PMID: 26016877].
[25]
Liu LP, Cheng K, Ning MA, et al. Association between peripheral blood cells mitochondrial DNA content and severity of coronary heart disease. Atherosclerosis 2017; 261: 105-10. [http://dx.doi.org/10.1016/j.atherosclerosis.2017.02.013]. [PMID: 28242046].
[26]
Mitrofanov KY, Zhelankin AV, Shiganova GM, et al. Analysis of mitochondrial DNA heteroplasmic mutations A1555G, C3256T, T3336C, C5178A, G12315A, G13513A, G14459A, G14846A and G15059A in CHD patients with the history of myocardial infarction. Exp Mol Pathol 2016; 100(1): 87-91. [http://dx.doi.org/10.1016/j.yexmp.2015.12.003]. [PMID: 26654794].
[27]
Albert CM, Oh K, Whang W, et al. Dietary alpha-linolenic acid intake and risk of sudden cardiac death and coronary heart disease. Circulation 2005; 112(21): 3232-8. [http://dx.doi.org/10.1161/CIRCULATIONAHA.105.572008]. [PMID: 16301356].
[28]
Masic I, Rahimic M, Dilic M, Kadribasic R, Toromanovic S. Socio-medical Characteristics of Coronary Disease in Bosnia and Herzegovina and the World. Mater Sociomed 2011; 23(3): 171-83. [http://dx.doi.org/10.5455/msm.2011.23.171-183]. [PMID: 23922510].
[29]
Shahzadi S. Shabana, Chaudhry M, Arooj I, Hasnain S. Polymorphism in C12orf43 Region is Associated with the Risk of Coronary Artery Disease in a Pakistani Cohort. Biochem Genet 2016; 54(5): 676-84.
[30]
Yayan J. Emerging families of biomarkers for coronary artery disease: inflammatory mediators. Vasc Health Risk Manag 2013; 9: 435-56. [http://dx.doi.org/10.2147/VHRM.S45704]. [PMID: 23983474].
[31]
Sobenin IA, Sazonova MA, Ivanova MM, et al. Mutation C3256T of mitochondrial genome in white blood cells: novel genetic marker of atherosclerosis and coronary heart disease. PLoS One 2012; 7(10)e46573 [http://dx.doi.org/10.1371/journal.pone.0046573]. [PMID: 23056349].
[32]
Sinyov VV, Sazonova MA, Ryzhkova AI, et al. Potential use of buccal epithelium for genetic diagnosis of atherosclerosis using mtDNA mutations. Vessel Plus 2017; 1: 145-50. [http://dx.doi.org/10.20517/2574-1209.2016.04].
[33]
Yu P, Yu DM, Liu DM, Wang K, Tang XZ. Relationship between mutations of mitochondrial DNA ND1 gene and type 2 diabetes. Chin Med J (Engl) 2004; 117(7): 985-9.
[PMID: 15265369]
[34]
Yang T, Lam CW, Tsang MW, et al. Novel mitochondrial 16S rRNA mutation, 3200T->C, associated with adult-onset type 2 diabetes. Chin Med J (Engl) 2002; 115(5): 753-8.
[PMID: 12133550]
[35]
Sazonova MA, Zhelankin AV, Barinova VA, et al. Dataset of mitochondrial genome variants associated with asymptomatic atherosclerosis. Data Brief 2016; 7(7): 1570-5. [http://dx.doi.org/10.1016/j.dib.2016.04.055]. [PMID: 27222855].
[36]
Böttger EC. Mutant A1555G mitochondrial 12S rRNA and aminoglycoside susceptibility. Antimicrob Agents Chemother 2010; 54(7): 3073-4. [http://dx.doi.org/10.1128/AAC.01819-09]. [PMID: 20554968].
[37]
Kolovou V, Lagou E, Mihas C, et al. Angiotensinogen (AGT) M235T, AGT T174M and Angiotensin-1-Converting Enzyme (ACE) I/D Gene Polymorphisms in Essential Hypertension: Effects on Ramipril Efficacy. Open Cardiovasc Med J 2015; 9: 118-26. [http://dx.doi.org/10.2174/1874192401509010118]. [PMID: 27006715].
[38]
Echem C, Costa TJD, Oliveira V, et al. Mitochondrial DNA: A new driver for sex differences in spontaneous hypertension. Pharmacol Res 2019; 144: 142-50. [http://dx.doi.org/10.1016/j.phrs.2019.04.008]. [PMID: 30965087].
[39]
Govindaraj P, Rani B, Sundaravadivel P, et al. Mitochondrial genome variations in idiopathic dilated cardiomyopathy. Mitochondrion 2019; 48: 51-9. [http://dx.doi.org/10.1016/j.mito.2019.03.003]. [PMID: 30910572].
[40]
Zaragoza MV, Brandon MC, Diegoli M, Arbustini E, Wallace DC. Mitochondrial cardiomyopathies: how to identify candidate pathogenic mutations by mitochondrial DNA sequencing, MITOMASTER and phylogeny. Eur J Hum Genet 2011; 19(2): 200-7. [http://dx.doi.org/10.1038/ejhg.2010.169]. [PMID: 20978534].
[41]
Sazonova MA, Ryzhkova AI, Sinyov VV, et al. New markers of atherosclerosis: a threshold level of heteroplasmy in mtDNA mutations. Vessel Plus Vessel Plus 2017; 1: 182-91. [http://dx.doi.org/10.20517/2574-1209.2017.16].
[42]
Ryzhkova AI, Sazonova MA, Sinyov VV, et al. Mitochondrial diseases caused by mtDNA mutations: a mini-review. Ther Clin Risk Manag 2018; 14: 1933-42. [http://dx.doi.org/10.2147/TCRM.S154863]. [PMID: 30349272].
[43]
Sobenin IA. Role of Mitochondrial Genome Mutations in Pathogenesis of Carotid Atherosclerosis Oxidative Medicine and Cellular Longevity 2018; 7620234: 3.
[44]
Sazonova MA, Sinyov VV, Barinova VA, et al. Association of mitochondrial mutations with the age of patients having atherosclerotic lesions. Exp Mol Pathol 2015; 99(3): 717-9. [http://dx.doi.org/10.1016/j.yexmp.2015.11.019]. [PMID: 26586456].
[45]
Staiger H, Schaeffeler E, Schwab M, Häring HU. Pharmacogenetics: Implications for Modern Type 2 Diabetes Therapy. Rev Diabet Stud 2015; 12(3-4): 363-76. [http://dx.doi.org/10.1900/RDS.2015.12.363]. [PMID: 27111121].
[46]
Sazonova MA, Chicheva MM, Zhelankin AV, Sobenin IA, Bobryshev YV, Orekhov AN. Association of mutations in the mitochondrial genome with the subclinical carotid atherosclerosis in women. Exp Mol Pathol 2015; 99(1): 25-32. [http://dx.doi.org/10.1016/j.yexmp.2015.04.003]. [PMID: 25910413].
[47]
Luizon MR, Palei ACT, Belo VA, et al. Gene-gene interactions in the NAMPT pathway, plasma visfatin/NAMPT levels, and antihypertensive therapy responsiveness in hypertensive disorders of pregnancy. Pharmacogenomics J 2016; 17(5): 427-34.
[48]
Sobenin IA, Zhelankin AV, Mitrofanov KY, et al. 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]. [PMID: 25312735].
[49]
Hodgkinson KA, Howes AJ, Boland P, et al. Long-Term Clinical Outcome of Arrhythmogenic Right Ventricular Cardiomyopathy in Individuals With a p.S358L Mutation in TMEM43 Following Implantable Cardioverter Defibrillator Therapy. Circ Arrhythm Electrophysiol 2016; 9(3)e003589 [http://dx.doi.org/10.1161/CIRCEP.115.003589]. [PMID: 26966288].
[50]
Naing A, Kenchaiah M, Krishnan B, et al. Maternally inherited diabetes and deafness (MIDD): diagnosis and management. J Diabetes Complications 2014; 28(4): 542-6. [http://dx.doi.org/10.1016/j.jdiacomp.2014.03.006]. [PMID: 24746802].
[51]
Skou AS, Tranebjærg L, Jensen T, Hasle H. Mitochondrial 12S ribosomal RNA A1555G mutation associated with cardiomyopathy and hearing loss following high-dose chemotherapy and repeated aminoglycoside exposure. J Pediatr 2014; 164(2): 413-5. [http://dx.doi.org/10.1016/j.jpeds.2013.10.024]. [PMID: 24252789].
[52]
Sazonova MA, Sinyov VV, Barinova VA, et al. 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].
[53]
Sazonova MA, Zhelankin AV, Barinova VA, et al. Mutations of mitochondrial genome in carotid atherosclerosis. Front Genet 2015; 6: 111. [http://dx.doi.org/10.3389/fgene.2015.00111]. [PMID: 25852749].
[54]
Meng X, Yang J, Dong M, et al. Regulatory T cells in cardiovascular diseases. Nat Rev Cardiol 2016; 13(3): 167-79. [http://dx.doi.org/10.1038/nrcardio.2015.169]. [PMID: 26525543].
[55]
Wolf DP, Mitalipov PA, Mitalipov SM. Principles of and strategies for germline gene therapy. Nat Med 2019; 25(6): 890-7. [http://dx.doi.org/10.1038/s41591-019-0473-8]. [PMID: 31160821].
[56]
Kirichenko TV, Ragino YI, Voevoda MI, et al. Data on association of mitochondrial heteroplasmy with carotid intima-media thickness in subjects from Russian and Kazakh populations. Data Brief 2020; 29105136 [http://dx.doi.org/10.1016/j.dib.2020.105136].
[57]
Calvo MJ, Martínez MS, Torres W, et al. Omega-3 polyunsaturated fatty acids and cardiovascular health: a molecular view into structure and function. Vessel Plus 2017; 1: 116-28.
[58]
Schiffrin EL. Mechanisms of remodelling of small arteries, antihypertensive therapy and the immune system in hypertension. Clin Invest Med 2015; 38(6): E394-402. [http://dx.doi.org/10.25011/cim.v38i6.26202]. [PMID: 26654522].
[59]
Sazonova MA. [Association of mitochondrial genome mutations with lipofibrous plaques in human aortic intima]. Patol Fiziol Eksp Ter 2015; 59(1): 17-28. PMID: 26226685
[60]
Nandeesha H, Bobby Z, Selvaraj N, Rajappa M. Pre-hypertension: Is it an inflammatory state? Clin Chim Acta 2015; 451(Pt. B): 338-42.
[61]
Zhelankin A, Khasanova Z, Barinova L, Sazonova M, Postnov A, Sobenin I. 1A.06: Mitochondrial DNA haplogroup h is associated with subclinical carotid atherosclerosis in russian population. J Hypertens 2015; 33(Suppl. 1)e2 [http://dx.doi.org/10.1097/01.hjh.0000467356.04711.50].
[62]
Balta S, Mikhailidis DP, Demirkol S, Ozturk C, Celik T, Iyisoy A. Endocan: A novel inflammatory indicator in cardiovascular disease? Atherosclerosis 2015; 243(1): 339-43. [http://dx.doi.org/10.1016/j.atherosclerosis.2015.09.030]. [PMID: 26448266].
[63]
Domingueti CP, Dusse LM. Carvalho Md, de Sousa LP, Gomes KB, Fernandes AP. Diabetes mellitus: The linkage between oxidative stress, inflammation, hypercoagulability and vascular complications. J Diabetes Complications 2016; 30(4): 738-45. [http://dx.doi.org/10.1016/j.jdiacomp.2015.12.018]. [PMID: 26781070].
[64]
Verdile G, Keane KN, Cruzat VF, et al. Inflammation and Oxidative Stress: The Molecular Connectivity between Insulin Resistance, Obesity, and Alzheimer’s Disease. Mediators Inflamm 2015; 2015105828 [http://dx.doi.org/10.1155/2015/105828]. [PMID: 26693205].
[65]
Coope A, Torsoni AS, Velloso LA. MECHANISMS IN ENDOCRINOLOGY: Metabolic and inflammatory pathways on the pathogenesis of type 2 diabetes. Eur J Endocrinol 2016; 174(5): R175-87. [http://dx.doi.org/10.1530/EJE-15-1065]. [PMID: 26646937].
[66]
Gowdar S, Syal S, Chhabra L. Probable protective role of diabetes mellitus in takotsubo cardiomyopathy: a review. Vessel Plus 2017; 1: 129-36. [http://dx.doi.org/10.20517/2574-1209.2017.12].
[67]
Chistiakov DA, Bobryshev YV, Orekhov AN. Macrophage-mediated cholesterol handling in atherosclerosis. J Cell Mol Med 2016; 20(1): 17-28. [http://dx.doi.org/10.1111/jcmm.12689]. [PMID: 26493158].
[68]
Tertov VV, Sobenin IA, Gabbasov ZA, Popov EG, Orekhov AN. Lipoprotein aggregation as an essential condition of intracellular lipid accumulation caused by modified low density lipoproteins. Biochem Biophys Res Commun 1989; 163(1): 489-94. [http://dx.doi.org/10.1016/0006-291X(89)92163-3]. [PMID: 2775281].
[69]
Sobenin IA, Tertov VV, Orekhov AN. Atherogenic modified LDL in diabetes. Diabetes 1996; 45(Suppl. 3): S35-9. [http://dx.doi.org/10.2337/diab.45.3.S35]. [PMID: 8674887].
[70]
Panasenko OM, Mel’nichenko AA, Aksenov DV, et al. Oxidation-induced aggregation of LDL increases their uptake by smooth muscle cells from human aorta. Bull Exp Biol Med 2007; 143(2): 200-3. [http://dx.doi.org/10.1007/s10517-007-0050-x]. [PMID: 17970201].
[71]
Orekhov AN, Bobryshev YV, Sobenin IA, Melnichenko AA, Chistiakov DA. Modified low density lipoprotein and lipoprotein-containing circulating immune complexes as diagnostic and prognostic biomarkers of atherosclerosis and type 1 diabetes macrovascular disease. Int J Mol Sci 2014; 15(7): 12807-41. [http://dx.doi.org/10.3390/ijms150712807]. [PMID: 25050779].
[72]
Sobenin IA, Salonen JT, Zhelankin AV, et al. Low density lipoprotein-containing circulating immune complexes: role in atherosclerosis and diagnostic value. BioMed Res Int 2014; 2014205697 [http://dx.doi.org/10.1155/2014/205697]. [PMID: 25054132].
[73]
Sobenin IA, Orekhov AN. Mechanistic Biomarkers: The Field for the Development of Non-Pharmaceutical and Pharmaceutical Approaches to Diagnostics, Prevention and Treatment of Chronic Diseases. Curr Pharm Des 2016; 22(3): 265-7. [http://dx.doi.org/10.2174/138161282203151221144210]. [PMID: 26719154].
[74]
Sazonova MA, Budnikov YY, Khazanova ZB, Postnov AY, Sobenin IA, Orekhov AN. Direct quantitative assessment of mutant allele in mitochondrial genome in atherosclerotic lesion of human aorta. Atheroscler Suppl 2007; 8(1): 45-6. [http://dx.doi.org/10.1016/S1567-5688(07)71125-X].
[75]
Postnov AY, Sazonova MA, Budnikov YY, Khazanova ZB, Sobenin IA, Orekhov AN. Association of somatic mitochondrial mutations with atherosclerosis. Atheroscler Suppl 2007; 8(1): 46. [http://dx.doi.org/10.1016/S1567-5688(07)71126-1].
[76]
Sazonova M, Andrianova I, Khasanova Z, Sobenin I, Postnov A. Quantitative mitochondrial genome mutation investigation and possible role of the somatic mutations in development of atherosclerotic lesion of human aorta. Atheroscler Suppl 2008; 9(1): 113. [http://dx.doi.org/10.1016/S1567-5688(08)70454-9].

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