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

Volumn 128, Issue 7, 2013, Pages 702-712

  Yu, Emma ^a   Calvert, Patrick A ^a,c   Mercer, John R ^a   Harrison, James ^a   Baker, Lauren ^a   Figg, Nichola L ^a   Kumar, Sheetal ^a   Wang, Julie C ^a   Hurst, Liam A ^a   Obaid, Daniel R ^a,c   Logan, Angela ^d   West, Nick E J ^c   Clarke, Murray C H ^a   Vidal Puig, Antonio ^b   Murphy, Michael P ^d   Bennett, Martin R ^a,b,c  

^a Department of Medicine   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c PAPWORTH HOSPITAL   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Apoptosis; Atherosclerosis; Free radicals

Indexed keywords

APOLIPOPROTEIN E; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; CONTROLLED STUDY; CYTOKINE RELEASE; DNA DAMAGE; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; HYPERLIPIDEMIA; INTRAVASCULAR ULTRASOUND; MALE; MONOCYTE; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

APOPTOSIS; ATHEROSCLEROSIS; FREE RADICALS;

ADIPOSITY; ADULT; AGED; ANIMALS; APOLIPOPROTEINS E; APOPTOSIS; ATHEROSCLEROSIS; CELLS, CULTURED; CYTOKINES; DNA ADDUCTS; DNA DAMAGE; DNA, MITOCHONDRIAL; DNA-DIRECTED DNA POLYMERASE; ELECTRON TRANSPORT; FEMALE; HUMANS; HYPERLIPIDEMIAS; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MITOCHONDRIA; MONOCYTES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; OXYGEN CONSUMPTION; PLAQUE, ATHEROSCLEROTIC; RADIATION CHIMERA; REACTIVE OXYGEN SPECIES; RISK;

EID: 84882287053     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.002271     Document Type: Article

References (48)

1. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc). 2005;70:200-214.
2. Ballinger SW, Patterson C, Yan CN, Doan R, Burow DL, Young CG, Yakes FM, Van Houten B, Ballinger CA, Freeman BA, Runge MS. Hydrogen peroxide-and peroxynitrite-induced mitochondrial DNA damage and dysfunction in vascular endothelial and smooth muscle cells. Circ Res. 2000;86:960-966.
3. Clayton DA, Doda JN, Friedberg EC. The absence of a pyrimidine dimer repair mechanism in mammalian mitochondria. Proc Natl Acad Sci U S A. 1974;71:2777-2781.
4. Croteau DL, Stierum RH, Bohr VA. Mitochondrial DNA repair pathways. Mutat Res. 1999;434:137-148.
5. Yakes FM, Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A. 1997;94:514-519.
6. Chomyn A, Attardi G. MtDNA mutations in aging and apoptosis. Biochem Biophys Res Commun. 2003;304:519-529.
7. Pitkanen S, Robinson BH. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J Clin Invest. 1996;98:345-351.
8. Salminen A, Ojala J, Kaarniranta K, Kauppinen A. Mitochondrial dysfunction and oxidative stress activate inflammasomes: Impact on the aging process and age-related diseases. Cell Mol Life Sci. 2012;69:2999-3013.
9. James AM, Murphy MP. How mitochondrial damage affects cell function. J Biomed Sci. 2002;9(pt 1):475-487.
10. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12:1075-1080.
11. Clarke MC, Littlewood TD, Figg N, Maguire JJ, Davenport AP, Goddard M, Bennett MR. Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res. 2008;102:1529-1538.
12. Ballinger SW, Patterson C, Knight-Lozano CA, Burow DL, Conklin CA, Hu Z, Reuf J, Horaist C, Lebovitz R, Hunter GC, McIntyre K, Runge MS. Mitochondrial integrity and function in atherogenesis. Circulation. 2002;106:544-549.
13. Botto N, Berti S, Manfredi S, Al-Jabri A, Federici C, Clerico A, Ciofini E, Biagini A, Andreassi MG. Detection of mtDNA with 4977 bp deletion in blood cells and atherosclerotic lesions of patients with coronary artery disease. Mutat Res. 2005;570:81-88.
14. Corral-Debrinski M, Shoffner JM, Lott MT, Wallace DC. Association of mitochondrial DNA damage with aging and coronary atherosclerotic heart disease. Mutat Res. 1992;275:169-180.
15. Mercer J, Figg N, Stoneman V, Braganza D, Bennett MR. Endogenous p53 protects vascular smooth muscle cells from apoptosis and reduces atherosclerosis in ApoE knockout mice. Circ Res. 2005;96:667-674.
16. Mercer JR, Cheng KK, Figg N, Gorenne I, Mahmoudi M, Griffin J, Vidal-Puig A, Logan A, Murphy MP, Bennett M. DNA damage links mitochondrial dysfunction to atherosclerosis and the metabolic syndrome. Circ Res. 2010;107:1021-1031.
17. Cochemé HM, Logan A, Prime TA, Abakumova I, Quin C, McQuaker SJ, Patel JV, Fearnley IM, James AM, Porteous CM, Smith RA, Hartley RC, Partridge L, Murphy MP. Using the mitochondria-targeted ratiometric mass spectrometry probe MitoB to measure H2O2 in living Drosophila. Nat Protoc. 2012;7:946-958.
18. Mercer JR, Yu E, Figg N, Cheng KK, Prime TA, Griffin JL, Masoodi M, Vidal-Puig A, Murphy MP, Bennett MR. The mitochondria-targeted antioxidant MitoQ decreases features of the metabolic syndrome in ATM+//ApoE/mice. Free Radic Biol Med. 2012;52:841-849.
19. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc. 2008;3:965-976.
20. Calvert PA, Liew TV, Gorenne I, Clarke M, Costopoulos C, Obaid DR, O'Sullivan M, Shapiro LM, McNab DC, Densem CG, Schofield PM, Braganza D, Clarke SC, Ray KK, West NE, Bennett MR. Leukocyte telomere length is associated with high-risk plaques on virtual histology intravascular ultrasound and increased proinflammatory activity. Arterioscler Thromb Vasc Biol. 2011;31:2157-2164.
21. Calvert PA, Obaid DR, O'Sullivan M, Shapiro LM, McNab D, Densem CG, Schofield PM, Braganza D, Clarke SC, Ray KK, West NE, Bennett MR. Association between IVUS findings and adverse outcomes in patients with coronary artery disease: The VIVA (VH-IVUS in Vulnerable Atherosclerosis) Study. JACC Cardiovasc Imaging. 2011;4:894-901.
22. Moraes CT, Ciacci F, Bonilla E, Jansen C, Hirano M, Rao N, Lovelace RE, Rowland LP, Schon EA, DiMauro S. Two novel pathogenic mitochondrial DNA mutations affecting organelle number and protein synthesis: Is the tRNA(Leu(UUR)) gene an etiologic hot spot? J Clin Invest. 1993;92:2906-2915.
23. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, Bohlooly-Y M, Gidlöf S, Oldfors A, Wibom R, Törnell J, Jacobs HT, Larsson NG. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature. 2004;429:417-423.
24. Trifunovic A, Hansson A, Wredenberg A, Rovio AT, Dufour E, Khvorostov I, Spelbrink JN, Wibom R, Jacobs HT, Larsson NG. Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc Natl Acad Sci U S A. 2005;102:17993-17998.
25. Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, Morrow JD, Van Remmen H, Sedivy JM, Yamasoba T, Tanokura M, Weindruch R, Leeuwenburgh C, Prolla TA. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science. 2005;309:481-484.
26. Schaar JA, Muller JE, Falk E, Virmani R, Fuster V, Serruys PW, Colombo A, Stefanadis C, Ward Casscells S, Moreno PR, Maseri A, van der Steen AF. Terminology for high-risk and vulnerable coronary artery plaques: Report of a meeting on the vulnerable plaque. Eur Heart J. 2004;25:1077-1082.
27. Huang-Doran I, Sleigh A, Rochford JJ, O'Rahilly S, Savage DB. Lipodystrophy: Metabolic insights from a rare disorder. J Endocrinol. 2010;207:245-255.
28. Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristea E, Mintz GS, Mehran R, McPherson J, Farhat N, Marso SP, Parise H, Templin B, White R, Zhang Z, Serruys PW; PROSPECT Investigators. A prospective natural-history study of coronary atherosclerosis. N Engl J Med. 2011;364:226-235.
29. Madamanchi NR, Vendrov A, Runge MS. Oxidative stress and vascular disease. Arterioscler Thromb Vasc Biol. 2005;25:29-38.
30. Harman D. The biologic clock: The mitochondria? J Am Geriatr Soc. 1972;20:145-147.
31. Gredilla R. DNA damage and base excision repair in mitochondria and their role in aging. J Aging Res. 2010;2011:257093.
32. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: A dawn for evolutionary medicine. Annu Rev Genet. 2005;39:359-407.
33. Hiona A, Sanz A, Kujoth GC, Pamplona R, Seo AY, Hofer T, Someya S, Miyakawa T, Nakayama C, Samhan-Arias AK, Servais S, Barger JL, Portero-Otín M, Tanokura M, Prolla TA, Leeuwenburgh C. Mitochondrial DNA mutations induce mitochondrial dysfunction, apoptosis and sarcopenia in skeletal muscle of mitochondrial DNA mutator mice. PLoS One. 2010;5:e11468.
34. Dai DF, Chen T, Wanagat J, Laflamme M, Marcinek DJ, Emond MJ, Ngo CP, Prolla TA, Rabinovitch PS. Age-dependent cardiomyopathy in mitochondrial mutator mice is attenuated by overexpression of catalase targeted to mitochondria. Aging Cell. 2010;9:536-544.
35. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: The importance of lesion stage and phagocytic efficiency. Arterioscler Thromb Vasc Biol. 2005;25:2255-2264.
36. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 1999;397:441-446.
37. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. Cell. 1996;86:147-157.
38. Zoratti M, Szabò I. The mitochondrial permeability transition. Biochim Biophys Acta. 1995;1241:139-176.
39. Wang W, Yang X, López de Silanes I, Carling D, Gorospe M. Increased AMP:ATP ratio and AMP-activated protein kinase activity during cellular senescence linked to reduced HuR function. J Biol Chem. 2003;278:27016-27023.
40. Wang W, Fan J, Yang X, Fürer-Galban S, Lopez de Silanes I, von Kobbe C, Guo J, Georas SN, Foufelle F, Hardie DG, Carling D, Gorospe M. AMP-activated kinase regulates cytoplasmic HuR. Mol Cell Biol. 2002;22:3425-3436.
41. Hardie DG, Carling D. The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur J Biochem. 1997;246:259-273.
42. Cossarizza A, Mussini C, Viganò A. Mitochondria in the pathogenesis of lipodystrophy induced by anti-HIV antiretroviral drugs: Actors or bystanders? Bioessays. 2001;23:1070-1080.
43. Brinkman K, Smeitink JA, Romijn JA, Reiss P. Mitochondrial toxicity induced by nucleoside-analogue reverse-transcriptase inhibitors is a key factor in the pathogenesis of antiretroviral-therapy-related lipodystrophy. Lancet. 1999;354:1112-1115.
44. Thorp E, Li Y, Bao L, Yao PM, Kuriakose G, Rong J, Fisher EA, Tabas I. Brief report: Increased apoptosis in advanced atherosclerotic lesions of Apoe-/-mice lacking macrophage Bcl-2. Arterioscler Thromb Vasc Biol. 2009;29:169-172.
45. Schrijvers DM, De Meyer GR, Kockx MM, Herman AG, Martinet W. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol. 2005;25:1256-1261.
46. Tabas I, Seimon T, Timmins J, Li G, Lim W. Macrophage apoptosis in advanced atherosclerosis. Ann N Y Acad Sci. 2009;1173(suppl 1):E40-E45.
47. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol. 2011;12:222-230.
48. Shimada K, Crother TR, Karlin J, Dagvadorj J, Chiba N, Chen S, Ramanujan VK, Wolf AJ, Vergnes L, Ojcius DM, Rentsendorj A, Vargas M, Guerrero C, Wang Y, Fitzgerald KA, Underhill DM, Town T, Arditi M. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity. 2012;36:401-414.