Mitochondrial cyclophilin D in vascular oxidative stress and hypertension

Hypertension

Volumn 67, Issue 6, 2016, Pages 1218-1227

  Itani, Hana A ^a   Dikalova, Anna E ^a   Mcmaster, William G ^a   Nazarewicz, Rafal R ^a   Bikineyeva, Alfiya T ^a   Harrison, David G ^a   Dikalov, Sergey I ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

angiotensin II; cyclophilin D; endothelial oxidative stress; hypertension; inflammatory cytokines; mitochondria; vasorelaxation

Indexed keywords

CATALASE; CYCLOPHILIN D; HYDROGEN PEROXIDE; SANGLIFEHRIN A; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; ANGIOTENSIN II; BIOLOGICAL MARKER; CYCLOPHILIN; LACTONE; SPIRO COMPOUND; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HYPERTENSION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; VASODILATATION; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DISEASE MODEL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; RANDOMIZATION; VASCULAR ENDOTHELIUM;

ANALYSIS OF VARIANCE; ANGIOTENSIN II; ANIMALS; BIOMARKERS; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYCLOPHILINS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HYPERTENSION; LACTONES; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OXIDATIVE STRESS; RANDOM ALLOCATION; SPIRO COMPOUNDS; SUPEROXIDES; VASODILATION;

EID: 84963682574     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.07085     Document Type: Article

References (45)

1. Harrison DG, Marvar PJ, Titze JM, Vascular inflammatory cells in hypertension. Front Physiol 2012 3 128. doi: 10.3389/fphys.2012.00128
2. Sacco RL, Benjamin EJ, Broderick JP, Dyken M, Easton JD, Feinberg WM, Goldstein LB, Gorelick PB, Howard G, Kittner SJ, Manolio TA, Whisnant JP, Wolf PA, American Heart Association Prevention Conference. IV. Prevention and rehabilitation of stroke. Risk factors. Stroke 1997 28 1507 1517
3. Fletcher RD, Amdur RL, Kolodner R, McManus C, Jones R, Faselis C, Kokkinos P, Singh S, Papademetriou V, Blood pressure control among US veterans: a large multiyear analysis of blood pressure data from the Veterans Administration health data repository. Circulation 2012 125 2462 2468. doi: 10.1161/CIRCULATIONAHA.111.029983
4. Harrison DG, Gongora MC, Guzik TJ, Widder J, Oxidative stress and hypertension. J Am Soc Hypertens 2007 1 30 44. doi: 10.1016/j.jash.2006.11.006
5. Lee MY, Griendling KK, Redox signaling, vascular function, and hypertension. Antioxid Redox Signal 2008 10 1045 1059. doi: 10.1089/ars.2007.1986
6. Ghiadoni L, Taddei S, Virdis A, Hypertension and endothelial dysfunction: therapeutic approach. Curr Vasc Pharmacol 2012 10 42 60
7. Rubattu S, Pagliaro B, Pierelli G, Santolamazza C, Castro SD, Mennuni S, Volpe M, Pathogenesis of target organ damage in hypertension: role of mitochondrial oxidative stress. Int J Mol Sci 2015 16 823 839. doi: 10.3390/ijms16010823
8. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, Dikalov SI, Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 2010 107 106 116. doi: 10.1161/CIRCRESAHA.109.214601
9. Dikalov SI, Nazarewicz RR, Bikineyeva A, Hilenski L, Lassègue B, Griendling KK, Harrison DG, Dikalova AE, Nox2-induced production of mitochondrial superoxide in angiotensin II-mediated endothelial oxidative stress and hypertension. Antioxid Redox Signal 2014 20 281 294. doi: 10.1089/ars.2012.4918
10. Eirin A, Lerman A, Lerman LO, Mitochondria: a pathogenic paradigm in hypertensive renal disease. Hypertension 2015 65 264 270. doi: 10.1161/HYPERTENSIONAHA.114.04598
11. Doughan AK, Harrison DG, Dikalov SI, Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 2008 102 488 496. doi: 10.1161/CIRCRESAHA.107.162800
12. Kröller-Schön S, Steven S, Kossmann S, Molecular mechanisms of the crosstalk between mitochondria and NADPH oxidase through reactive oxygen species-studies in white blood cells and in animal models. Antioxid Redox Signal 2014 20 247 266. doi: 10.1089/ars.2012.4953
13. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T, Tsujimoto Y, Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005 434 652 658. doi: 10.1038/nature03317
14. Kinnally KW, Peixoto PM, Ryu SY, Dejean LM, Is mPTP the gatekeeper for necrosis, apoptosis, or both? Biochim Biophys Acta 2011 1813 616 622. doi: 10.1016/j.bbamcr.2010.09.013
15. Tavecchio M, Lisanti S, Lam A, Ghosh JC, Martin NM, O'Connell M, Weeraratna AT, Kossenkov AV, Showe LC, Altieri DC, Cyclophilin D extramitochondrial signaling controls cell cycle progression and chemokine-directed cell motility. J Biol Chem 2013 288 5553 5561. doi: 10.1074/jbc.M112.433045
16. Di Lisa F, Carpi A, Giorgio V, Bernardi P, The mitochondrial permeability transition pore and cyclophilin D in cardioprotection. Biochim Biophys Acta 2011 1813 1316 1322. doi: 10.1016/j.bbamcr.2011.01.031
17. Ponticelli C, Cucchiari D, Graziani G, Hypertension in kidney transplant recipients. Transpl Int 2011 24 523 533. doi: 10.1111/j.1432-2277.2011.01242.x
18. Bautista LE, Vera LM, Arenas IA, Gamarra G, Independent association between inflammatory markers (C-reactive protein, interleukin-6, and TNF-Alpha) and essential hypertension. J Hum Hypertens 2005 19 149 154. doi: 10.1038/sj.jhh.1001785
19. Madhur MS, Lob HE, McCann LA, Iwakura Y, Blinder Y, Guzik TJ, Harrison DG, Interleukin 17 promotes angiotensin II-induced hypertension and vascular dysfunction. Hypertension 2010 55 500 507. doi: 10.1161/HYPERTENSIONAHA.109.145094
20. Nguyen H, Chiasson VL, Chatterjee P, Kopriva SE, Young KJ, Mitchell BM, Interleukin-17 causes Rho-kinase-mediated endothelial dysfunction and hypertension. Cardiovasc Res 2013 97 696 704. doi: 10.1093/cvr/cvs422
21. Clarke SJ, McStay GP, Halestrap AP, Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J Biol Chem 2002 277 34793 34799. doi: 10.1074/jbc.M202191200
22. Dikalova A, Clempus R, Lassègue B, Cheng G, McCoy J, Dikalov S, San Martin A, Lyle A, Weber DS, Weiss D, Taylor WR, Schmidt HH, Owens GK, Lambeth JD, Griendling KK, Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 2005 112 2668 2676. doi: 10.1161/CIRCULATIONAHA.105.538934
23. Kowluru RA, Kowluru V, Xiong Y, Ho YS, Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress. Free Radic Biol Med 2006 41 1191 1196. doi: 10.1016/j.freeradbiomed.2006.01.012
24. Krege JH, Hodgin JB, Hagaman JR, Smithies O, A noninvasive computerized tail-cuff system for measuring blood pressure in mice. Hypertension 1995 25 1111 1115
25. Widder JD, Guzik TJ, Mueller CF, Clempus RE, Schmidt HH, Dikalov SI, Griendling KK, Jones DP, Harrison DG, Role of the multidrug resistance protein-1 in hypertension and vascular dysfunction caused by angiotensin II. Arterioscler Thromb Vasc Biol 2007 27 762 768. doi: 10.1161/01.ATV.0000259298.11129.a2
26. Dikalov S, Griendling KK, Harrison DG, Measurement of reactive oxygen species in cardiovascular studies. Hypertension 2007 49 717 727. doi: 10.1161/01.HYP.0000258594.87211.6b
27. Dikalov S, Fink B, ESR techniques for the detection of nitric oxide in vivo and in tissues. Methods Enzymol 2005 396 597 610. doi: 10.1016/S0076-6879(05)96052-7
28. Linard D, Kandlbinder A, Degand H, Morsomme P, Dietz KJ, Knoops B, Redox characterization of human cyclophilin D: identification of a new mammalian mitochondrial redox sensor? Arch Biochem Biophys 2009 491 39 45. doi: 10.1016/j.abb.2009.09.002
29. Shagdarsuren E, Wellner M, Braesen JH, Park JK, Fiebeler A, Henke N, Dechend R, Gratze P, Luft FC, Muller DN, Complement activation in angiotensin II-induced organ damage. Circ Res 2005 97 716 724. doi: 10.1161/01.RES.0000182677.89816.38
30. McMaster WG, Kirabo A, Madhur MS, Harrison DG, Inflammation, immunity, and hypertensive end-organ damage. Circ Res 2015 116 1022 1033. doi: 10.1161/CIRCRESAHA.116.303697
31. Saleh MA, McMaster WG, Wu J, Lymphocyte adaptor protein LNK deficiency exacerbates hypertension and end-organ inflammation. J Clin Invest 2015 125 1189 1202. doi: 10.1172/JCI76327
32. Zielonka J, Kalyanaraman B, Hydroethidine- And MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation: another inconvenient truth. Free Radic Biol Med 2010 48 983 1001. doi: 10.1016/j.freeradbiomed.2010.01.028
33. Kirabo A, Fontana V, de Faria AP, DC isoketal-modified proteins activate T cells and promote hypertension. J Clin Invest 2014 124 4642 4656. doi: 10.1172/JCI74084
34. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG, Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 2007 204 2449 2460. doi: 10.1084/jem.20070657
35. Boos CJ, Lip GY, Is hypertension an inflammatory process? Curr Pharm Des 2006 12 1623 1635
36. Panov A, Schonfeld P, Dikalov S, Hemendinger R, Bonkovsky HL, Brooks BR, The neuromediator glutamate, through specific substrate interactions, enhances mitochondrial ATP production and reactive oxygen species generation in nonsynaptic brain mitochondria. J Biol Chem 2009 284 14448 14456. doi: 10.1074/jbc.M900985200
37. Nazarewicz RR, Dikalova AE, Bikineyeva A, Dikalov SI, Nox2 as a potential target of mitochondrial superoxide and its role in endothelial oxidative stress. Am J Physiol Heart Circ Physiol 2013 305 H1131 H1140. doi: 10.1152/ajpheart.00063.2013
38. Coble JP, Grobe JL, Johnson AK, Sigmund CD, Mechanisms of brain renin angiotensin system-induced drinking and blood pressure: importance of the subfornical organ. Am J Physiol Regul Integr Comp Physiol 2015 308 R238 R249. doi: 10.1152/ajpregu.00486.2014
39. Hall JE, The kidney, hypertension, and obesity. Hypertension 2003 41 3 pt 2 625 633. doi: 10.1161/01.HYP.0000052314.95497.78
40. Harrison DG, Widder J, Grumbach I, Chen W, Weber M, Searles C, Endothelial mechanotransduction, nitric oxide and vascular inflammation. J Intern Med 2006 259 351 363. doi: 10.1111/j.1365-2796.2006.01621.x
41. Dikalov SI, Ungvari Z, Role of mitochondrial oxidative stress in hypertension. Am J Physiol Heart Circ Physiol 2013 305 H1417 H1427. doi: 10.1152/ajpheart.00089.2013
42. de Cavanagh EM, Inserra F, Ferder M, Ferder L, From mitochondria to disease: role of the renin-Angiotensin system. Am J Nephrol 2007 27 545 553. doi: 10.1159/000107757
43. Fridovich I, Mitochondria: are they the seat of senescence? Aging Cell 2004 3 13 16
44. Song Y, Cook NR, Albert CM, Van Denburgh M, Manson JE, Effects of vitamins C and E and beta-carotene on the risk of type 2 diabetes in women at high risk of cardiovascular disease: a randomized controlled trial. Am J Clin Nutr 2009 90 429 437. doi: 10.3945/ajcn.2009.27491
45. Sesso HD, Buring JE, Christen WG, Kurth T, Belanger C, MacFadyen J, Bubes V, Manson JE, Glynn RJ, Gaziano JM, Vitamins E and C in the prevention of cardiovascular disease in men: the Physicians' Health Study II randomized controlled trial. JAMA 2008 300 2123 2133. doi: 10.1001/jama.2008.600