Mitochondria-targeted antioxidant (MitoQ) ameliorates age-related arterial endothelial dysfunction in mice

Journal of Physiology

Volumn 592, Issue 12, 2014, Pages 2549-2561

  Gioscia Ryan, Rachel A ^a   LaRocca, Thomas J ^a   Sindler, Amy L ^a   Zigler, Melanie C ^a   Murphy, Michael P ^b   Seals, Douglas R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ANTIOXIDANT; MITOCHONDRIA TARGETED ANTIOXIDANT; MITOQ; NITRIC OXIDE SYNTHASE; NITROPRUSSIDE SODIUM; SUPEROXIDE; UNCLASSIFIED DRUG; 10-(6'-UBIQUINONYL)DECYLTRIPHENYLPHOSPHONIUM BROMIDE; NITRIC OXIDE; ORGANOPHOSPHORUS COMPOUND; UBIQUINONE;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; EX VIVO STUDY; FLUID INTAKE; HEART MITOCHONDRION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TREATMENT RESPONSE; AGING; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DRUG EFFECTS; METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; PHYSIOLOGY; THORACIC AORTA; VASCULAR DISEASES; VASCULAR ENDOTHELIUM; VASODILATATION;

AGING; ANIMALS; ANTIOXIDANTS; AORTA, THORACIC; ENDOTHELIUM, VASCULAR; MALE; MICE, INBRED C57BL; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; ORGANOPHOSPHORUS COMPOUNDS; OXIDATIVE STRESS; SUPEROXIDES; UBIQUINONE; VASCULAR DISEASES; VASODILATION;

EID: 84902303333     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.268680     Document Type: Article

References (58)

1. Adlam VJ, Harrison JC, Porteous CM, James AM, Smith RAJ, Murphy MP & Sammut IA (2005). Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J 19, 1088-1095.
2. Anderson R & Prolla T (2009). PGC-1α and anti-aging interventions. Biochim Biophys Acta 1790, 1059-1066.
3. Bachschmid MM, Schildknecht S, Matsui R, Zee R, Haeussler D, Cohen RA, Pimental D & van der Loo B (2013). Vascular aging: chronic oxidative stress and impairment of redox signaling-consequences for vascular homeostasis and disease. Ann Med 45, 17-36.
4. Balaban RS, Nemoto S & Finkel T (2005). Mitochondria, oxidants, and aging. Cell 120, 483-495.
5. Ballinger SW (2002). Mitochondrial integrity and function in atherogenesis. Circulation 106, 544-549.
6. Blouin A, Bolender RP & Weibel ER (1977). Distribution of organelles and membranes between hepatocytes and non-hepatocytes in the rat liver parenchyma: a stereological study. J Cell Biol 72, 441-455.
7. Brandes RP, Fleming I & Busse R (2005). Endothelial aging. Cardiovasc Res 66, 286-294.
8. Brown KA, Didion SP, Andresen JJ & Faraci FM (2007). Effect of aging, MnSOD deficiency, and genetic background on endothelial function: evidence for MnSOD haploinsufficiency. Arterioscler Thromb Vasc Biol 27, 1941-1946.
9. shc adaptor protein prevents hyperglycemia-induced endothelial dysfunction and oxidative stress. Proc Natl Acad Sci U S A 104, 5217-5222.
10. Cochemé HM, Kelso GF, James AM, Ross MF, Trnka J, Mahendiran T, Asin-Cayuela J, Blaikie FH, Manas ARB, Porteous CM, Adlam VJ, Smith RAJ & Murphy MP (2007). Mitochondrial targeting of quinones: therapeutic implications. Mitochondrion 7, S94-S102.
11. Csiszar A, Labinskyy N, Orosz Z & Ungvari Z (2006). Altered mitochondrial energy metabolism may play a role in vascular aging. Med Hypotheses 67, 904-908.
12. Dai DF, Rabinovitch PS & Ungvari Z (2012). Mitochondria and cardiovascular aging. Circ Res 110, 1109-1124.
13. Dikalov SI, Kirilyuk IA, Voinov M & Grigor'ev IA (2011). EPR detection of cellular and mitochondrial superoxide using cyclic hydroxylamines. Free Radic Res 45, 417-430.
14. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG & Dikalov SI (2010). Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 107, 106-116.
15. Donato AJ, Walker AE, Magerko KA, Bramwell RC, Black AD, Henson GD, Lawson BR, Lesniewski LA & Seals DR (2013). Life-long caloric restriction reduces oxidative stress and preserves nitric oxide bioavailability and function in arteries of old mice. Aging Cell 12, 772-783.
16. Dromparis P & Michelakis ED (2013). Mitochondria in vascular health and disease. Annu Rev Physiol 75, 95-126.
17. Fleenor BS, Sindler AL, Marvi NK, Howell KL, Zigler ML, Yoshizawa M & Seals DR (2013). Curcumin ameliorates arterial dysfunction and oxidative stress with aging. Exp Gerontol 48, 269-276.
18. Fleenor BS, Sindler AL, Eng JS, Nair DP, Dodson RB & Seals DR (2012). Sodium nitrite de-stiffening of large elastic arteries with aging: role of normalization of advanced glycation end-products. Exp Gerontol 47, 588-594.
19. Galluzzi L, Kepp O, Trojel-Hansen C & Kroemer G (2012). Mitochondrial control of cellular life, stress, and death. Circ Res 111, 1198-1207.
20. Gane EJ, Weilert F, Orr DW, Keogh GF, Gibson M, Lockhart MM, Frampton CM, Taylor KM, Smith RAJ & Murphy MP (2010). The mitochondria-targeted anti-oxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients. Liver Int 30, 1019-1026.
21. Gertz M & Steegborn C (2010). The lifespan-regulator p66Shc in mitochondria: redox enzyme or redox sensor? Antioxid Redox Signal 13, 1417-1428.
22. Graham D, Huynh NN, Hamilton CA, Beattie E, Smith RAJ, Cochemé HM, Murphy MP & Dominiczak AF (2009). Mitochondria-targeted antioxidant MitoQ10 improves endothelial function and attenuates cardiac hypertrophy. Hypertension 54, 322-328.
23. Griffith TM, Edwards DH, Newby AC, Lewis MJ & Henderson AH (1986). Production of endothelium derived relaxant factor is dependent on oxidative phosphorylation and extracellular calcium. Cardiovasc Res 20, 7-12.
24. Herrera MD, Mingorance C, Rodríguez-Rodríguez R & Alvarez de Sotomayor M (2010). Endothelial dysfunction and aging: an update. Ageing Res Rev 9, 142-152.
25. Kluge MA, Fetterman JL & Vita JA (2013). Mitochondria and endothelial function. Circ Res 112, 1171-1188.
26. Kris-Etherton PM, Lichtenstein AH, Howard BV, Steinberg D & Witztum JL (2004). Antioxidant vitamin supplements and cardiovascular disease. Circulation 110, 637-641.
27. Lakatta EG (2003). Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part III: cellular and molecular clues to heart and arterial aging. Circulation 107, 490-497.
28. Lakshminarasimhan M & Steegborn C (2011). Emerging mitochondrial signaling mechanisms in physiology, aging processes, and as drug targets. Exp Gerontol 46, 174-177.
29. LaRocca TJ, Gioscia-Ryan RA, Hearon CM & Seals DR (2013). The autophagy enhancer spermidine reverses arterial aging. Mech Ageing Dev 134, 314-320.
30. LaRocca TJ, Henson GD, Thorburn A, Sindler AL, Pierce GL & Seals DR (2012). Translational evidence that impaired autophagy contributes to arterial ageing. J Physiol 590, 3305-3316.
31. Li N, Ragheb K, Lawler G, Sturgis J, Rajwa B, Melendez JA & Robinson JP (2003). Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem 278, 8516-8525.
32. López-Armada MJ, Riveiro-Naveira RR, Vaamonde-García C & Valcárcel-Ares MN (2013). Mitochondrial dysfunction and the inflammatory response. Mitochondrion 13, 106-118.
33. Murphy MP (2009). How mitochondria produce reactive oxygen species. Biochem J 417, 1-13.
34. Murphy MP & Smith RAJ (2007). Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu Rev Pharmacol Toxicol 47, 629-656.
35. Nunnari J & Suomalainen A (2012). Mitochondria: in sickness and in health. Cell 148, 1145-1159.
36. Quintero M, Colombo SL, Godfrey A & Moncada S (2006). Mitochondria as signaling organelles in the vascular endothelium. Proc Natl Acad Sci U S A 103, 5379-5384.
37. Radi R (2013). Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Acc Chem Res 46, 550-559.
38. Radi R (2004). Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci U S A 101, 4003-4008.
39. Rippe C, Lesniewski L, Connell M, LaRocca T, Donato A & Seals D (2010). Short-term calorie restriction reverses vascular endothelial dysfunction in old mice by increasing nitric oxide and reducing oxidative stress. Aging Cell 9, 304-312.
40. Rodman DM, Mallet J & McMurty IF (1991). Difference in effect of inhibitors on energy metabolism on endothelium-dependent relaxation of rat pulmonary artery and aorta. Am J Respir Cell Mol Biol 4, 237-242.
41. Rodriguez-Cuenca S, Cochemé HM, Logan A, Abakumova I, Prime TA, Rose C, Vidal-Puig A, Smith AC, Rubinsztein DC, Fearnley AM, Jones BA, Pope S, Heales SJR, Lam BYH, Neogi SG, McFarlane I, James AM, Smith RAJ & Murphy MP (2010). Consequences of long-term oral administration of the mitochondria-targeted antioxidant MitoQ to wild-type mice. Free Radic Biol Med 48, 161-172.
42. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, Moy CS, Mozaffarian D, Mussolino ME, Nicol G, Paynter NP, Soliman EZ, Sorlie PD, Sotoodehnia N, Turan TN, Virani SS, Wong ND, Woo D & Turner MB (2012). Heart disease and stroke statistics - 2012 update: a report from the American Heart Association. Circulation 125, e2-e220.
43. Ross MF, Prime TA, Abakumova I, James AM, Porteous CM, Smith RAJ & Murphy MP (2008). Rapid and extensive uptake and activation of hydrophobic triphenylphosphonium cations within cells. Biochem J 411, 633-645.
44. Sastre J (2003). The role of mitochondrial oxidative stress in aging. Free Radic Biol Med 35, 1-8.
45. Shenouda SM, Widlansky ME, Chen K, Xu G, Holbrook M, Tabit CE, Hamburg NM, Frame AA, Caiana TL, Kluge MA, Duess MA, Levit A, Kim B, Harman ML, Joseph L, Shirihai OS, Vita JA (2011). Altered mitochondrial dynamics contributes to endothelial dysfunction in diabetes mellitus. Circulation 124, 444-453.
46. Sindler AL, Fleenor BS, Calvert JW, Marshall KD, Zigler ML, Lefer DJ & Seals DR (2011). Nitrite supplementation reverses vascular endothelial dysfunction and large elastic artery stiffness with aging. Aging Cell 10, 429-437.
47. Smith RAJ & Murphy MP (2010). Animal and human studies with the mitochondria-targeted antioxidant MitoQ. Ann N Y Acad Sci 1201, 96-103.
48. Smith RAJ, Hartley RC, Cochemé HM & Murphy MP (2012). Mitochondrial pharmacology. Trends Pharmacol Sci 33, 341-352.
49. Snow BJ, Rolfe FL, Lockhart MM, Frampton CM, O'Sullivan JD, Fung V, Smith RAJ, Murphy MP & Taylor KM (2010). A double-blind, placebo-controlled study to assess the mitochondria-targeted antioxidant MitoQ as a disease-modifying therapy in Parkinson's disease. Mov Dis 25, 1670-1674.
50. Sprott RL & Ramirez I (1997). Current inbred and hybrid rat and mouse models. ILAR J 38, 104-109.
51. Ungvari Z, Labinskyy N, Gupte S, Chander PN, Edwards JG & Csiszar A (2008). Dysregulation of mitochondrial biogenesis in vascular endothelial and smooth muscle cells of aged rats. Am J Physiol Heart Circ Physiol 294, H2121-H2128.
52. 2 production promotes endothelial NF-κB activation in aged rat arteries. Am J Physiol Heart Circ Physiol 293, H37-H47.
53. van der Loo B, Labugger R, Skepper JN, Bachschmid M, Kilo J, Powell JM, Palacios-Callender M, Erusalimsky JD, Quaschning T, Malinski T, Gygi D, Ullrich V & Lüscher TF (2000). Enhanced peroxynitrite formation is associated with vascular aging. J Exp Med 192, 1731-1744.
54. Weber TA & Reichert AS (2010). Impaired quality control of mitochondria: aging from a new perspective. Exp Gerontol 45, 503-511.
55. Weir CJ, Gibson IF & Martin W (1991). Effects of metabolic inhibitors on endothelium-dependent and endothelium-independent vasodilatation of rat and rabbit aorta. Br J Pharmacol 102, 162-166.
56. Wenzel P, Schuhmacher S, Kienhöfer J, Müller J, Hortmann M, Oelze M, Schulz E, Treiber N, Kawamoto T, Scharffetter-Kochanek K, Münzel T, Bürkle A, Bachschmid MM & Daiber A (2008). Manganese superoxide dismutase and aldehyde dehydrogenase deficiency increase mitochondrial oxidative stress and aggravate age-dependent vascular dysfunction. Cardiovasc Res 80, 280-289.
57. Yeboah J, Crouse JR, Hsu FC, Burke GL & Herrington DM (2007). Brachial flow-mediated dilation predicts incident cardiovascular events in older adults: the Cardiovascular Health Study. Circulation 115, 2390-2397.
58. Zhang DX & Gutterman DD (2007). Mitochondrial reactive oxygen species-mediated signaling in endothelial cells. Am J Physiol Heart Circ Physiol 292, H2023-H2031.