Molecular mechanisms of the crosstalk between mitochondria and NADPH oxidase through reactive oxygen species - Studies in white blood cells and in animal models

Antioxidants and Redox Signaling

Volumn 20, Issue 2, 2014, Pages 247-266

  Kröller Schön, Swenja ^a   Steven, Sebastian ^a   Kossmann, Sabine ^a   Scholz, Alexander ^a   Daub, Steffen ^a   Oelze, Matthias ^a   Xia, Ning ^a   Hausding, Michael ^a   Mikhed, Yuliya ^a   Zinßius, Elena ^a   Mader, Michael ^a   Stamm, Paul ^a   Treiber, Nicolai ^b   Scharffetter Kochanek, Karin ^b   Li, Huige ^a   Schulz, Eberhard ^a   Wenzel, Philip ^a   Münzel, Thomas ^a   Daiber, Andreas ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; CYCLOPHILIN D; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN PEROXIDE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PROTEIN KINASE C; PROTEIN P47; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE CSRC; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CALCIUM CELL LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LEUKOCYTE; MITOCHONDRION; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL;

ANGIOTENSIN II; ANIMALS; BIOLOGICAL TRANSPORT; CYCLOPHILINS; ENZYME ACTIVATION; HUMANS; LEUKOCYTES; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MODELS, BIOLOGICAL; NADPH OXIDASE; NEUTROPHILS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXIDES; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; SUPEROXIDE DISMUTASE;

EID: 84890307737     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4953     Document Type: Article

References (69)

1. Ago T, Kuroda J, Pain J, Fu C, Li H, and Sadoshima J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res 106: 1253-1264, 2010.
2. Ahmad M, Kelly MR, Zhao X, Kandhi S, and Wolin MS. Roles for Nox4 in the contractile response of bovine pulmonary arteries to hypoxia. Am J Physiol Heart Circ Physiol 298: H1879-H1888, 2010.
3. Balsari A, Marolda R, Gambacorti-Passerini C, Sciorelli G, Tona G, Cosulich E, Taramelli D, Fossati G, Parmiani G, and Cascinelli N. Systemic administration of autologous, alloactivated helper-enriched lymphocytes to patients with metastatic melanoma of the lung. A phase I study. Cancer Immunol Immunother 21: 148-155, 1986.
4. Basso E, Fante L, Fowlkes J, Petronilli V, Forte MA, and Bernardi P. Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D. J Biol Chem 280: 18558-18561, 2005.
5. Block K, Gorin Y, and Abboud HE. Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci U S A 106: 14385-14390, 2009.
6. Brandes RP. Triggering mitochondrial radical release: a new function for NADPH oxidases. Hypertension 45: 847-848, 2005.
7. Byrne JA, Grieve DJ, Bendall JK, Li JM, Gove C, Lambeth JD, Cave AC, and Shah AM. Contrasting roles of NADPH oxidase isoforms in pressure-overload versus angiotensin IIinduced cardiac hypertrophy. Circ Res 93: 802-805, 2003.
8. Castor LR, Locatelli KA, and Ximenes VF. Pro-oxidant activity of apocynin radical. Free Radic Biol Med 48: 1636-1643, 2010.
9. Chen CA, Wang TY, Varadharaj S, Reyes LA, Hemann C, Talukder MA, Chen YR, Druhan LJ, and Zweier JL. Sglutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 468: 1115-1118, 2010.
10. Chen Z, Zhang J, and Stamler JS. Identification of the enzymatic mechanism of nitroglycerin bioactivation. Proc Natl Acad Sci U S A 99: 8306-8311, 2002.
11. Daiber A. Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim Biophys Acta 1797: 897-906, 2010.
12. Daiber A, August M, Baldus S, Wendt M, Oelze M, Sydow K, Kleschyov AL, and Munzel T. Measurement of NAD(P)H oxidase-derived superoxide with the luminol analogue L-012. Free Radic Biol Med 36: 101-111, 2004.
13. Daiber A, Oelze M, August M, Wendt M, Sydow K, Wieboldt H, Kleschyov AL, and Munzel T. Detection of superoxide and peroxynitrite in model systems and mitochondria by the luminol analogue L-012. Free Radic Res 38: 259-269, 2004.
14. Daiber A, Oelze M, Coldewey M, Bachschmid M, Wenzel P, Sydow K, Wendt M, Kleschyov AL, Stalleicken D, Ullrich V, Mulsch A, and Munzel T. Oxidative stress and mitochondrial aldehyde dehydrogenase activity: a comparison of pentaerythritol tetranitrate with other organic nitrates. Mol Pharmacol 66: 1372-1382, 2004.
15. Daiber A, Oelze M, Sulyok S, Coldewey M, Schulz E, Treiber N, Hink U, Mulsch A, Scharffetter-Kochanek K, and Munzel T. Heterozygous deficiency of manganese superoxide dismutase in mice (Mn-SOD + / -): a novel approach to assess the role of oxidative stress for the development of nitrate tolerance. Mol Pharmacol 68: 579-588, 2005.
16. Dehne N and Brune B. Sensors, transmitters, and targets in mitochondrial oxygen shortage-A hypoxia-inducible factor relay story. Antioxid Redox Signal 20: 339-352, 2014.
17. Di Lisa F and Bernardi P. Mitochondria and ischemia-reperfusion injury of the heart: fixing a hole. Cardiovasc Res 70: 191-199, 2006.
18. Di Lisa F, Canton M, Carpi A, Kaludercic N, Menabo R, Menazza S, and Semenzato M. Mitochondrial injury and protection in ischemic pre-And postconditioning. Antioxid Redox Signal 14: 881-891, 2011.
19. Dikalov S, Griendling KK, and Harrison DG. Measurement of reactive oxygen species in cardiovascular studies. Hypertension 49: 717-727, 2007.
20. Dikalov SI and Harrison DG. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid Redox Signal 20: 372-382, 2014.
21. Dikalov SI, Li W, Doughan AK, Blanco RR, and Zafari AM. Mitochondrial reactive oxygen species and calcium uptake regulate activation of phagocytic NADPH oxidase. Am J Physiol Regul Integr Comp Physiol 302: R1134-R1142, 2012.
22. Dikalova A, Clempus R, Lassegue B, Cheng G, McCoy J, Dikalov S, San Martin A, Lyle A, Weber DS, Weiss D, Taylor WR, Schmidt HH, Owens GK, Lambeth JD, and Griendling KK. Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 112: 2668-2676, 2005.
23. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, and Dikalov SI. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 107: 106-116, 2010.
24. Doughan AK, Harrison DG, and Dikalov SI. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 102: 488-496, 2008.
25. Graham KA, Kulawiec M, Owens KM, Li X, Desouki MM, Chandra D, and Singh KK. NADPH oxidase 4 is an oncoprotein localized to mitochondria. Cancer Biol Ther 10: 223-231, 2010.
26. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, and Harrison DG. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204: 2449-2460, 2007.
27. Hausenloy D, Wynne A, Duchen M, and Yellon D. Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection. Circulation 109: 1714-1717, 2004.
28. Heumuller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schroder K, and Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51: 211-217, 2008.
29. Jamieson D, Chance B, Cadenas E, and Boveris A. The relation of free radical production to hyperoxia. Annu Rev Physiol 48: 703-719, 1986.
30. Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, Mann GE, Moore K, Roberts LJ, 2nd, and Ischiropoulos H. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 52: 1-6, 2012.
31. Kimura S, Zhang GX, Nishiyama A, Shokoji T, Yao L, Fan YY, Rahman M, and Abe Y. Mitochondria-derived reactive oxygen species and vascular MAP kinases: comparison of angiotensin II and diazoxide. Hypertension 45: 438-444, 2005.
32. Kleschyov AL and Munzel T. Advanced spin trapping of vascular nitric oxide using colloid iron diethyldithiocarbamate. Methods Enzymol 359: 42-51, 2002.
33. Knorr M, Hausding M, Kroller-Schuhmacher S, Steven S, Oelze M, Heeren T, Scholz A, Gori T, Wenzel P, Schulz E, Daiber A, and Munzel T. Nitroglycerin-induced endothelial dysfunction and tolerance involve adverse phosphorylation and s-glutathionylation of endothelial nitric oxide synthase: beneficial effects of therapy with the AT1 receptor blocker telmisartan. Arterioscler Thromb Vasc Biol 31: 2223-2231, 2011.
34. Kossmann S, Schwenk M, Hausding M, Karbach SH, Schmidgen MI, Brandt M, Knorr M, Hu H, Kroller-Schon S, Schonfelder T, Grabbe S, Oelze M, Daiber A, Munze T, Becker C, and Wenzel P. Angiotensin II-induced vascular dysfunction depends on interferon-gamma-driven immune cell recruitment and mutual activation of monocytes and NK-cells. Arterioscler Thromb Vasc Biol 33: 1313-1319, 2013.
35. Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, and Sadoshima J. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci U S A 107: 15565-15570, 2010.
36. Landmesser U, Cai H, Dikalov S, McCann L, Hwang J, Jo H, Holland SM, and Harrison DG. Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension 40: 511-515, 2002.
37. Madhur MS, Lob HE, McCann LA, Iwakura Y, Blinder Y, Guzik TJ, and Harrison DG. Interleukin 17 promotes angiotensin II-induced hypertension and vascular dysfunction. Hypertension 55: 500-507, 2010.
38. Maghzal GJ, Krause KH, Stocker R, and Jaquet V. Detection of reactive oxygen species derived from the family of NOX NADPH oxidases. Free Radic Biol Med 53: 1903-1918, 2012.
39. Matsuno K, Yamada H, Iwata K, Jin D, Katsuyama M, Matsuki M, Takai S, Yamanishi K, Miyazaki M, Matsubara H, and Yabe-Nishimura C. Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation 112: 2677-2685, 2005.
40. Mollnau H, Wenzel P, Oelze M, Treiber N, Pautz A, Schulz E, Schuhmacher S, Reifenberg K, Stalleicken D, Scharffetter-Kochanek K, Kleinert H, Munzel T, and Daiber A. Mitochondrial oxidative stress and nitrate tolerance-comparison of nitroglycerin and pentaerithrityl tetranitrate in Mn-SOD + / -mice. BMC Cardiovasc Disord 6: 44, 2006.
41. Munzel T, Li H, Mollnau H, Hink U, Matheis E, Hartmann M, Oelze M, Skatchkov M, Warnholtz A, Duncker L, Meinertz T, and Forstermann U. Effects of long-term nitroglycerin treatment on endothelial nitric oxide synthase (NOS III) gene expression, NOS III-mediated superoxide production, and vascular NO bioavailability. Circ Res 86: E7-E12, 2000.
42. Oelze M, Daiber A, Brandes RP, Hortmann M, Wenzel P, Hink U, Schulz E, Mollnau H, von Sandersleben A, Kleschyov AL, Mulsch A, Li H, Forstermann U, and Munzel T. Nebivolol inhibits superoxide formation by NADPH oxidase and endothelial dysfunction in angiotensin II-treated rats. Hypertension 48: 677-684, 2006.
43. Oelze M, Knorr M, Schuhmacher S, Heeren T, Otto C, Schulz E, Reifenberg K, Wenzel P, Munzel T, and Daiber A. Vascular Dysfunction in Streptozotocin-Induced Experimental Diabetes Strictly Depends on Insulin Deficiency. J Vasc Res 48: 275-284, 2011.
44. Oelze M, Warnholtz A, Faulhaber J, Wenzel P, Kleschyov AL, Coldewey M, Hink U, Pongs O, Fleming I, Wassmann S, Meinertz T, Ehmke H, Daiber A, and Munzel T. NADPH oxidase accounts for enhanced superoxide production and impaired endothelium-dependent smooth muscle relaxation in BKbeta1 -/ -mice. Arterioscler Thromb Vasc Biol 26: 1753-1759, 2006.
45. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N, Elbelghiti R, Cung TT, Bonnefoy E, Angoulvant D, Macia C, Raczka F, Sportouch C, Gahide G, Finet G, Andre-Fouet X, Revel D, Kirkorian G, Monassier JP, Derumeaux G, and Ovize M. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 359: 473-481, 2008.
46. Radi R, Cassina A, Hodara R, Quijano C, and Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33: 1451-1464, 2002.
47. Rathore R, Zheng YM, Niu CF, Liu QH, Korde A, Ho YS, and Wang YX. Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca2 + ]i through the mitochondrial ROSPKCepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic Biol Med 45: 1223-1231, 2008.
48. Reinehr R, Becker S, Eberle A, Grether-Beck S, and Haussinger D. Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J Biol Chem 280: 27179-27194, 2005.
49. Rossi F, Grzeskowiak M, Della Bianca V, Calzetti F, and Gandini G. Phosphatidic acid and not diacylglycerol generated by phospholipase D is functionally linked to the activation of the NADPH oxidase by FMLP in human neutrophils. Biochem Biophys Res Commun 168: 320-327, 1990.
50. Schluter T, Steinbach AC, Steffen A, Rettig R, and Grisk O. Apocynin-induced vasodilation involves Rho kinase inhibition but not NADPH oxidase inhibition. Cardiovasc Res 80: 271-279, 2008.
51. Schuhmacher S, Oelze M, Bollmann F, Kleinert H, Otto C, Heeren T, Steven S, Hausding M, Knorr M, Pautz A, Reifenberg K, Schulz E, Gori T, Wenzel P, Munzel T, and Daiber A. Vascular Dysfunction in experimental diabetes is improved by pentaerithrityl tetranitrate but not isosorbide-5-mononitrate therapy. Diabetes 60: 2608-2616, 2011.
52. Schuhmacher S, Schulz E, Oelze M, Konig A, Roegler C, Lange K, Sydow L, Kawamoto T, Wenzel P, Munzel T, Lehmann J, and Daiber A. A new class of organic nitrates: investigations on bioactivation, tolerance and cross-tolerance phenomena. Br J Pharmacol 158: 510-520, 2009.
53. Schuhmacher S, Wenzel P, Schulz E, Oelze M, Mang C, Kamuf J, Gori T, Jansen T, Knorr M, Karbach S, Hortmann M, Mathner F, Bhatnagar A, Forstermann U, Li H, Munzel T, and Daiber A. Pentaerythritol tetranitrate improves angiotensin II-induced vascular dysfunction via induction of heme oxygenase-1. Hypertension 55: 897-904, 2010.
54. Schulz E, Wenzel P, Munzel T, and Daiber A. Mitochondrial redox signaling: interaction of mitochondrial reactive oxygen species with other sources of oxidative stress. Antioxid Redox Signal 20: 308-324, 2014.
55. Strassburger M, Bloch W, Sulyok S, Schuller J, Keist AF, Schmidt A, Wenk J, Peters T, Wlaschek M, Krieg T, Hafner M, Kumin A, Werner S, Muller W, and Scharffetter-Kochanek K. Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radic Biol Med 38: 1458-1470, 2005.
56. Sydow K, Daiber A, Oelze M, Chen Z, August M, Wendt M,Ullrich V, Mulsch A, Schulz E, Keaney JF, Jr., Stamler JS, and Munzel T. Central role of mitochondrial aldehyde dehydrogenase and reactive oxygen species in nitroglycerin tolerance and cross-tolerance. J Clin Invest 113: 482-489, 2004.
57. Touyz RM, Yao G, and Schiffrin EL. c-Src induces phosphorylation and translocation of p47phox: role in superoxide generation by angiotensin II in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 23: 981-987, 2003.
58. Ullrich V and Kissner R. Redox signaling: bioinorganic chemistry at its best. J Inorg Biochem 100: 2079-2086, 2006.
59. Ullrich V and Schildknecht S. Sensing hypoxia by mitochondria: a unifying hypothesis involving S-nitrosation. Antioxid Redox Signal 20: 325-338, 2014.
60. Wenzel P, Knorr M, Kossmann S, Stratmann J, Hausding M, Schuhmacher S, Karbach SH, Schwenk M, Yogev N, Schulz E, Oelze M, Grabbe S, Jonuleit H, Becker C, Daiber A, Waisman A, and Munzel T. Lysozyme M-positive monocytes mediate angiotensin II-induced arterial hypertension and vascular dysfunction. Circulation 124: 1370-1381, 2011.
61. Wenzel P, Mollnau H, Oelze M, Schulz E, Wickramanayake JM, Muller J, Schuhmacher S, Hortmann M, Baldus S, Gori T, Brandes RP, Munzel T, and Daiber A. First evidence for a crosstalk between mitochondrial and NADPH oxidasederived reactive oxygen species in nitroglycerin-triggered vascular dysfunction. Antioxid Redox Signal 10: 1435-1447, 2008.
62. Wenzel P, Schuhmacher S, Kienhofer J, Muller J, Hortmann M, Oelze M, Schulz E, Treiber N, Kawamoto T, Scharffetter-Kochanek K, Munzel T, Burkle A, Bachschmid MM, and Daiber A. Manganese superoxide dismutase and aldehyde dehydrogenase deficiency increase mitochondrial oxidative stress and aggravate age-dependent vascular dysfunction. Cardiovasc Res 80: 280-289, 2008.
63. Wenzel P, Schulz E, Gori T, Ostad MA, Mathner F, Schildknecht S, Gobel S, Oelze M, Stalleicken D, Warnholtz A, Munzel T, and Daiber A. Monitoring white blood cell mitochondrial aldehyde dehydrogenase activity: implications for nitrate therapy in humans. J Pharmacol Exp Ther 330: 63-71, 2009.
64. Wenzel P, Schulz E, Oelze M, Muller J, Schuhmacher S, Alhamdani MS, Debrezion J, Hortmann M, Reifenberg K, Fleming I, Munzel T, and Daiber A. AT1-receptor blockade by telmisartan upregulates GTP-cyclohydrolase I and protects eNOS in diabetic rats. Free Radic Biol Med 45: 619-626, 2008.
65. Wind S, Beuerlein K, Eucker T, Muller H, Scheurer P, Armitage ME, Ho H, Schmidt HH, and Wingler K. Comparative pharmacology of chemically distinct NADPH oxidase inhibitors. Br J Pharmacol 161: 885-898, 2010.
66. Yin F, Boveris A, and Cadenas E. Mitochondrial energy metabolism and redox signaling in brain aging and neurodegeneration. Antioxid Redox Signal 20: 353-371, 2014.
67. Yoo SK, Freisinger CM, LeBert DC, and Huttenlocher A. Early redox, Src family kinase, and calcium signaling integrate wound responses and tissue regeneration in zebrafish. J Cell Biol 199: 225-234, 2012.
68. Yoo SK, Starnes TW, Deng Q, and Huttenlocher A. Lyn is a redox sensor that mediates leukocyte wound attraction in vivo. Nature 480: 109-112, 2011.
69. Zenke G, Strittmatter U, Fuchs S, Quesniaux VF, Brinkmann V, Schuler W, Zurini M, Enz A, Billich A, Sanglier JJ, and Fehr T. Sanglifehrin A, a novel cyclophilin-binding compound showing immunosuppressive activity with a new mechanism of action. J Immunol 166: 7165-7171, 2001.