Depleted energy charge and increased pulmonary endothelial permeability induced by mitochondrial complex i inhibition are mitigated by coenzyme Q 1 in the isolated perfused rat lung

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 1455-1463

  Bongard, Robert D ^a   Yan, Ke ^a   Hoffmann, Raymond G ^a   Audi, Said H ^b   Zhang, Xiao ^b   Lindemer, Brian J ^a   Townsley, Mary I ^c   Merker, Marilyn P ^a,d  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Medical College of Wisconsin and Marquette University   (United States)

^c UNIVERSITY OF SOUTH ALABAMA   (United States)

^d CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Free radicals; Mitochondrial electron transport complex I; Perfused lung; Pulmonary endothelial filtration coefficient; Pulmonary endothelial permeability; Pulmonary endothelium; Quinone

Indexed keywords

2,3 DIMETHOXY 5 METHYL 6 (3 METHYL 2 BUTENYL) 1,4 BENZOQUINONE; ADENINE NUCLEOTIDE; ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; LACTIC ACID; OXIDOREDUCTASE INHIBITOR; PIERICIDIN A; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; SODIUM CHLORIDE; UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOENERGY; CELL MEMBRANE PERMEABILITY; CELL SEPARATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRY WEIGHT; GLYCOLYSIS; ISOLATED LUNG; LUNG ALVEOLUS CELL; LUNG PARENCHYMA; LUNG PERFUSION; MALE; MICROVASCULAR ENDOTHELIAL CELL; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; RAT; SCANNING ELECTRON MICROSCOPY;

RATTUS;

FREE RADICALS; MITOCHONDRIAL ELECTRON TRANSPORT COMPLEX I; PERFUSED LUNG; PULMONARY ENDOTHELIAL FILTRATION COEFFICIENT; PULMONARY ENDOTHELIAL PERMEABILITY; PULMONARY ENDOTHELIUM; QUINONE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTI-BACTERIAL AGENTS; BLOOD-AIR BARRIER; CAPILLARY PERMEABILITY; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX III; ENDOTHELIUM, VASCULAR; ENERGY METABOLISM; GLYCOLYSIS; LACTIC ACID; LUNG; LUNG INJURY; MALE; MITOCHONDRIA; NAD(P)H DEHYDROGENASE (QUINONE); OXIDATION-REDUCTION; PYRIDINES; PYRUVIC ACID; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION; ROTENONE; UBIQUINONE; UNCOUPLING AGENTS;

EID: 84890437171     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.07.040     Document Type: Article

References (68)

1. A.B. Fisher Intermediary metabolism of the lung Environ. Health Perspect. 55 1984 149 158
2. 1 redox metabolism during passage through the rat pulmonary circulation and the effect of hyperoxia J. Appl. Physiol. 105 2008 1114 1126
3. P.R. Gardner, D.D. Nguyen, and C.W. White Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs Proc. Natl. Acad. Sci. USA 91 1994 12248 12252
4. M. Hashizume, M. Mouner, J.M. Chouteau, O.M. Gorodnya, M.V. Ruchko, B.J. Potter, G.L. Wilson, M.N. Gillespie, and J.C. Parker Mitochondrial targeted DNA repair enzyme 8-oxoguanine DNA glycosylase 1 protects against ventilator induced lung injury in intact mice Am. J. Physiol. Lung Cell. Mol. Physiol. 304 2012 L287 L297
5. 1 as a probe for mitochondrial complex I activity in the intact perfused hyperoxia-exposed wild-type and Nqo1-null mouse lung Am. J. Physiol. Lung Cell. Mol. Physiol. 302 2012 L949 L958
6. G.C. Chuang, Z. Yang, D.G. Westbrook, M. Pompilius, C.A. Ballinger, C.R. White, D.M. Krzywanski, E.M. Postlethwait, and S.W. Ballinger Pulmonary ozone exposure induces vascular dysfunction, mitochondrial damage, and atherogenesis Am. J. Physiol. Lung Cell. Mol. Physiol. 297 2009 L209 L216
7. W. Xu, T. Koeck, A.R. Lara, D. Neumann, F.P. DiFilippo, M. Koo, A.J. Janocha, F.A. Masri, A.C. Arroliga, C. Jennings, R.A. Dweik, R.M. Tuder, D.J. Stuehr, and S.C. Erzurum Alterations of cellular bioenergetics in pulmonary artery endothelial cells Proc. Natl. Acad. Sci. USA 104 2007 1342 1347
8. W. Qiu, H. Gu, L. Zheng, J. Zhou, D. Chen, and Y. Chen Pretreatment with edaravone reduces lung mitochondrial damage in an infant rabbit ischemia-reperfusion model J. Pediatr. Surg. 43 2008 2053 2060
9. P.R. De Leyn, T.E. Lerut, H.H. Schreinemakers, D.E. Van Raemdonck, K. Mubagwa, and W. Flameng Effect of inflation on adenosine triphosphate catabolism and lactate production during normothermic lung ischemia Ann. Thorac. Surg. 55 1993 1073 1078
10. S.P. Sommer, S. Sommer, B. Sinha, J. Wiedemann, C. Otto, I. Aleksic, C. Schimmer, and R.G. Leyh Ischemia-reperfusion injury-induced pulmonary mitochondrial damage J. Heart Lung Transplant. 30 2011 811 818
11. T. Fukushima, T. Gao, T. Tawara, N. Hojo, A. Isobe, and Y. Yamane Inhibitory effect of nicotinamide to paraquat toxicity and the reaction site on complex I Arch. Toxicol. 71 1997 633 637
12. N. Soulitzis, E. Neofytou, M. Psarrou, A. Anagnostis, N. Tavernarakis, N. Siafakas, and E.G. Tzortzaki Downregulation of lung mitochondrial prohibitin in COPD Respir. Med. 106 2012 954 961
13. S.P. Sommer, S. Sommer, B. Sinha, and R.G. Leyh Glycine preconditioning to ameliorate pulmonary ischemia reperfusion injury in rats Interact. Cardiovasc. Thorac. Surg. 14 2012 521 525
14. A.M. D'Armini, E.J. Tom, C.S. Roberts, D.C. Henke, J.J. Lemasters, and T.M. Egan When does the lung die? Time course of high energy phosphate depletion and relationship to lung viability after death J. Surg. Res. 59 1995 468 474
15. X.J. Qin, Y.N. Li, X. Liang, P. Wang, and C.X. Hai The dysfunction of ATPases due to impaired mitochondrial respiration in phosgene-induced pulmonary edema Biochem. Biophys. Res. Commun. 367 2008 150 155
16. T. Fukuse, T. Hirata, M. Ueda, T. Nakamura, M. Kawashima, S. Hitomi, and H. Wada Energy metabolism and mitochondrial damage during pulmonary preservation Transplant. Proc. 31 1999 1937 1938
17. T. Hirata, T. Fukuse, T. Nakamura, M. Ueda, M. Kawashima, S. Hitomi, and H. Wada Reperfusion lung injury after cold preservation correlates with decreased levels of intrapulmonary high-energy phosphates Transplantation 69 2000 1793 1801
18. S. Aggarwal, C. Dimitropoulou, Q. Lu, S.M. Black, and S. Sharma Glutathione supplementation attenuates lipopolysaccharide-induced mitochondrial dysfunction and apoptosis in a mouse model of acute lung injury Front. Physiol. 3 2012 161
19. M. Akai, T. Ishizaki, S. Matsukawa, K. Shigemori, and I. Miyamori Leukotoxin (9,10-epoxy-12-octadecenoate) impairs energy and redox state of isolated perfused rat lung Free Radic. Biol. Med. 25 1998 596 604
20. M.N. Islam, S.R. Das, M.T. Emin, M. Wei, L. Sun, K. Westphalen, D.J. Rowlands, S.K. Quadri, S. Bhattacharya, and J. Bhattacharya Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury Nat. Med. 18 2012 759 765
21. A.B. Fisher, C. Dodia, and A. Chander Energy dependence of lung phosphatidylcholine biosynthesis studied with CO hypoxia Am. J. Physiol. 249 1985 E89 93
22. J.C. Parker, and M.I. Townsley Evaluation of lung injury in rats and mice Am. J. Physiol. Lung Cell. Mol. Physiol. 286 2004 L231 L246
23. D.J. Bassett, and A.B. Fisher Metabolic response to carbon monoxide by isolated rat lungs Am. J. Physiol. 230 1976 658 663
24. D.J. Bassett, and A.B. Fisher Stimulation of rat lung metabolism with 2,4-dinitrophenol and phenazine methosulfate Am. J. Physiol. 231 1976 898 902
25. S. Matalon, and M.A. Cesar Effects of 100% oxygen breathing on the capillary filtration coefficient in rabbit lungs Microvasc. Res. 29 1985 70 80
26. L. Ernster, G. Dallner, and G.F. Azzone Differential effects of rotenone and amytal on mitochondrial electron and energy transfer J. Biol. Chem. 238 1963 1124 1131
27. S.H. Audi, R.D. Bongard, C.A. Dawson, D. Siegel, D.L. Roerig, and M.P. Merker Duroquinone reduction during passage through the pulmonary circulation Am. J. Physiol. Lung Cell. Mol. Physiol. 285 2003 L1116 L1131
28. T.S. Chan, S. Teng, J.X. Wilson, G. Galati, S. Khan, and P.J. O'Brien Coenzyme Q cytoprotective mechanisms for mitochondrial complex I cytopathies involves NAD(P)H:quinone oxidoreductase 1 (NQO1) Free Radic. Res. 36 2002 421 427
29. M. Erb, B. Hoffmann-Enger, H. Deppe, M. Soeberdt, R.H. Haefeli, C. Rummey, A. Feurer, and N. Gueven Features of idebenone and related short-chain quinones that rescue ATP levels under conditions of impaired mitochondrial complex I. PLoS One 7 2012 e36153
30. V. Giorgio, V. Petronilli, A. Ghelli, V. Carelli, M. Rugolo, G. Lenaz, and P. Bernardi The effects of idebenone on mitochondrial bioenergetics Biochim. Biophys. Acta Bioenerg. 1817 2012 363 369
31. D.S. Kerr Review of clinical trials for mitochondrial disorders: 1997-2012 Neurotherapeutics 10 2013 307 319
32. 10 deficient fibroblasts with ubiquinone, CoQ analogs, and vitamin C: time- and compound-dependent effects PLoS One 5 2010 e11897
33. R.D. Bongard, B.J. Lindemer, G.S. Krenz, and M.P. Merker Preferential utilization of NADPH as the endogenous electron donor for NAD(P)H:quinone oxidoreductase 1 (NQO1) in intact pulmonary arterial endothelial cells Free Radic. Biol. Med. 46 2009 25 32
34. D.E. Atkinson Energy charge of the adenylate pool as a regulatory parameter: interaction with feedback modifiers Biochemistry 7 1968 4030 4034
35. F.J. Ballard Adenine nucleotides and the adenylate kinase equilibrium in livers of foetal and newborn rats Biochem. J 117 1970 231 235
36. C. Owens, and R. Belcher A colorimetric micro-method for the determination of glutathione Biochem. J. 94 1965 705 711
37. F. Tietze Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues Anal. Biochem. 27 1969 502 522
38. O.W. Griffith Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine Anal. Biochem. 106 1980 207 212
39. R.A. Waller, and D.B. Duncan A Bayes rule for the symmetric multiple comparison problem J. Am. Statist. Assoc. 64 1969 1484 1504
40. R. Bolin, R.J. Guest, and R.K. Albert Glycolysis is not required for fluid homeostasis in isolated rabbit lungs J. Appl. Physiol. 64 1988 2517 2521
41. P. De Leyn, T. Lerut, H. Schreinemakers, H. van Belle, J. Lauwerijns, F. van Lommel, E. Verbeken, and W. Flameng Adenine nucleotide degradation in ischemic rabbit lung tissue Am. J. Physiol. Lung Cell. Mol. Physiol. 264 1993 L329 L337
42. E. Janssen, A. Terzic, B. Wieringa, and P.P. Dzeja Impaired intracellular energetic communication in muscles from creatine kinase and adenylate kinase (M-CK/AK1) double knock-out mice J. Biol. Chem. 278 2003 30441 30449
43. + transport in isolated perfused rat lungs Am. J. Respir. Cell Mol. Biol. 9 1993 157 165
44. D.B. Hinshaw, J.M. Burger, M.T. Miller, J.A. Adams, T.F. Beals, and G.M. Omann ATP depletion induces an increase in the assembly of a labile pool of polymerized actin in endothelial cells Am. J. Physiol. 264 1993 C1171 C1179
45. V. Adam-Vizi Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources Antioxid. Redox Signaling 7 2005 1140 1149
46. K. Radad, W.D. Rausch, and G. Gille Rotenone induces cell death in primary dopaminergic culture by increasing ROS production and inhibiting mitochondrial respiration Neurochem. Int. 49 2006 379 386
47. A. Barrientos, and C.T. Moraes Titrating the effects of mitochondrial complex I impairment in the cell physiology J. Biol. Chem. 274 1999 16188 16197
48. R. Fato, C. Bergamini, M. Bortolus, A.L. Maniero, S. Leoni, T. Ohnishi, and G. Lenaz Differential effects of mitochondrial complex I inhibitors on production of reactive oxygen species Biochim. Biophys. Acta. 1787 2009 384 392
49. S.P. Sanders, J.L. Zweier, P. Kuppusamy, S.J. Harrison, D.J. Bassett, E.W. Gabrielson, and J.T. Sylvester Hyperoxic sheep pulmonary microvascular endothelial cells generate free radicals via mitochondrial electron transport J. Clin. Invest. 91 1993 46 52
50. C. Brueckl, S. Kaestle, A. Kerem, H. Habazettl, F. Krombach, H. Kuppe, and W.M. Kuebler Hyperoxia-induced reactive oxygen species formation in pulmonary capillary endothelial cells in situ Am. J. Respir. Cell Mol. Biol. 34 2006 453 463
51. J.J. Zulueta, F.S. Yu, I.A. Hertig, V.J. Thannickal, and P.M. Hassoun Release of hydrogen peroxide in response to hypoxia-reoxygenation: role of and NAD(P)H oxidase-like enzyme in endothelial cell plasma membrane Am. J. Respir. Cell Mol. Biol. 12 1995 41 49
52. + channel signaling pathway regulated secretion of human pulmonary artery endothelial cells Free Radic. Res. 46 2012 1437 1445
53. H. Ichimura, K. Parthasarathi, S. Quadri, A.C. Issekutz, and J. Bhattacharya Mechano-oxidative coupling by mitochondria induces proinflammatory responses in lung venular capillaries J. Clin. Invest. 111 2003 691 699
54. 2-activated TRPM2 calcium channel in oxidant-induced endothelial injury J. Thromb. Haemostasis 101 2009 619 625
55. C.D. Ochoa, M. Alexeyev, V. Pastukh, R. Balczon, and T. Stevens Pseudomonas aeruginosa exotoxin Y is a promiscuous cyclase that increases endothelial tau phosphorylation and permeability J. Biol. Chem. 287 2012 25407 25418
56. A.D. Verin, A. Birukova, P. Wang, F. Liu, P. Becker, K. Birukov, and J.G.N. Garcia Microtubule disassembly increases endothelial cell barrier dysfunction: role of MLC phosphorylation Am. J. Physiol. Lung Cell. Mol. Physiol. 281 2001 L565 L574
57. W.S. Choi, R.D. Palmiter, and Z. Xia Loss of mitochondrial complex I activity potentiates dopamine neuron death induced by microtubule dysfunction in a Parkinson's disease model J. Cell Biol. 192 2011 873 882
58. X. Tian, Y. Tian, N. Sarich, T. Wu, and A.A. Birukova Novel role of stathmin in microtubule-dependent control of endothelial permeability FASEB J. 26 2012 3862 3874
59. A. Das, S. Chakrabarty, D. Choudhury, and G. Chakrabarti 1,4-Benzoquinone (PBQ) induced toxicity in lung epithelial cells is mediated by the disruption of the microtubule network and activation of caspase-3 Chem. Res. Toxicol. 23 2010 1054 1066
60. G and TRPV4 channels differentially regulates surface expression of P-selectin and barrier integrity in pulmonary capillary endothelium Am. J. Physiol. Lung Cell. Mol. Physiol. 297 2009 L650 L657
61. G. Parra-Bonilla, D.F. Alvarez, A.B. Al-Mehdi, M. Alexeyev, and T. Stevens Critical role for lactate dehydrogenase A in aerobic glycolysis that sustains pulmonary microvascular endothelial cell proliferation Am. J. Physiol. Lung Cell. Mol. Physiol. 299 2010 L513 L522
62. 2+ channels and pulmonary endothelial permeability: insights from study of intact lung and chronic pulmonary hypertension Microcirculation 13 2006 725 739
63. N. Demaurex, D. Poburko, and M. Frieden Regulation of plasma membrane calcium fluxes by mitochondria Biochim. Biophys. Acta. 1787 2009 1383 1394
64. 2+ homeostasis in human NADH:ubiquinone oxidoreductase deficiency Cell Calcium 44 2008 123 133
65. K.J. Cavanaugh Jr, J. Oswari, and S.S. Margulies Role of stretch on tight junction structure in alveolar epithelial cells Am. J. Respir. Cell Mol. Biol. 25 2001 584 591
66. +)-ATPase and E-cadherin J. Cell Sci. 107 1994 3315 3324
67. P.L. Khimenko, J.W. Barnard, T.M. Moore, P.S. Wilson, S.T. Ballard, and A.E. Taylor Vascular permeability and epithelial transport effects on lung edema formation in ischemia and reperfusion J. Appl. Physiol. 77 1994 1116 1121
68. G. Yue, and S. Matalon Mechanisms and sequelae of increased alveolar fluid clearance in hyperoxic rats Am. J. Physiol. 272 1997 L407 L412 Sciences