The Effect of Mitochondrial Complex I-Linked Respiration by Isoflurane Is Independent of Mitochondrial Nitric Oxide Production

Overview

Journal Cardiorenal Med

Publisher Karger

Specialties Cardiology & Vascular Diseases
Endocrinology
Nephrology

Date 2018 Apr 5

PMID 29617003

Citations 5

Authors

Fuqi Xu

Shigang Qiao

Hua Li

Yanjun Deng

Chen Wang

Jianzhong An

Affiliations

Soon will be listed here.

Abstract

Background: Anesthetic preconditioning (APC) of the myocardium is mediated in part by reversible alteration of mitochondrial function. Nitric oxide (NO) inhibits mitochondrial respiration and may mediate APC-induced cardioprotection. In this study, the effects of isoflurane on different states of mitochondrial respiration during the oxidation of complex I-linked substrates and the role of NO were investigated.

Methods: Mitochondria were isolated from Sprague-Dawley rat hearts. Respiration rates were measured polarographically at 28ºC with a computer-controlled Clark-type O2 electrode in the mitochondria (0.5 mg/mL) with complex I substrates glutamate/malate (5 mM). Isoflurane (0.25 mM) was administered before or after adenosine diphosphate (ADP)-initiated state 3 respiration. The NO synthase (NOS) inhibitor L-N5-(1-iminoethyl)-ornithine (L-NIO, 10 μM) and the NO donor S-nitroso-N-acetylpenicillamine (SNAP, 1 μM) were added before or after the addition of ADP.

Results: Isoflurane administered in state 2 increased state 2 respiration and decreased state 3 respiration. This attenuation of state 3 respiration by isoflurane was similar when it was given during state 3. L-NIO did not alter mitochondrial respiration or the effect of isoflurane. SNAP only, added in state 3, decreased state 3 respiration and enhanced the isoflurane-induced attenuation of state 3 respiration.

Conclusion: Isoflurane has clearly distinguishable effects on different states of mitochondrial respiration during the oxidation of complex I substrates. The uncoupling effect during state 2 respiration and the attenuation of state 3 respiration may contribute to the mechanism of APC-induced cardioprotection. These effects of isoflurane do not depend on endogenous mitochondrial NO, as the NOS inhibitor L-NIO did not alter the effects of isoflurane on mitochondrial respiration.

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References

Cleeter M, Cooper J, Darley-Usmar V, Moncada S, Schapira A . Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett. 1994; 345(1):50-4. DOI: 10.1016/0014-5793(94)00424-2. View

Lenaz G . The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life. 2002; 52(3-5):159-64. DOI: 10.1080/15216540152845957. View

Bolli R . Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J Mol Cell Cardiol. 2001; 33(11):1897-918. DOI: 10.1006/jmcc.2001.1462. View

Zaobornyj T, Ghafourifar P . Strategic localization of heart mitochondrial NOS: a review of the evidence. Am J Physiol Heart Circ Physiol. 2012; 303(11):H1283-93. DOI: 10.1152/ajpheart.00674.2011. View

Pannala V, Camara A, Dash R . Modeling the detailed kinetics of mitochondrial cytochrome c oxidase: Catalytic mechanism and nitric oxide inhibition. J Appl Physiol (1985). 2016; 121(5):1196-1207. PMC: 5142251. DOI: 10.1152/japplphysiol.00524.2016. View

Lores-Arnaiz S, DAmico G, Czerniczyniec A, Bustamante J, Boveris A . Brain mitochondrial nitric oxide synthase: in vitro and in vivo inhibition by chlorpromazine. Arch Biochem Biophys. 2004; 430(2):170-7. DOI: 10.1016/j.abb.2004.07.012. View

Ludwig L, Tanaka K, Eells J, Weihrauch D, Pagel P, Kersten J . Preconditioning by isoflurane is mediated by reactive oxygen species generated from mitochondrial electron transport chain complex III. Anesth Analg. 2004; 99(5):1308-1315. DOI: 10.1213/01.ANE.0000134804.09484.5D. View

Tengan C, Moraes C . NO control of mitochondrial function in normal and transformed cells. Biochim Biophys Acta Bioenerg. 2017; 1858(8):573-581. PMC: 5487294. DOI: 10.1016/j.bbabio.2017.02.009. View

Sanz A, Caro P, Gomez J, Barja G . Testing the vicious cycle theory of mitochondrial ROS production: effects of H2O2 and cumene hydroperoxide treatment on heart mitochondria. J Bioenerg Biomembr. 2006; 38(2):121-7. DOI: 10.1007/s10863-006-9011-8. View

10.

Shiva S, Oh J, Landar A, Ulasova E, Venkatraman A, Bailey S . Nitroxia: the pathological consequence of dysfunction in the nitric oxide-cytochrome c oxidase signaling pathway. Free Radic Biol Med. 2005; 38(3):297-306. DOI: 10.1016/j.freeradbiomed.2004.10.037. View

11.

Swyers T, Redford D, Larson D . Volatile anesthetic-induced preconditioning. Perfusion. 2013; 29(1):10-5. DOI: 10.1177/0267659113503975. View

12.

Kato K, Giulivi C . Critical overview of mitochondrial nitric-oxide synthase. Front Biosci. 2006; 11:2725-38. DOI: 10.2741/2002. View

13.

Ge Z, Pravdic D, Bienengraeber M, Pratt Jr P, Auchampach J, Gross G . Isoflurane postconditioning protects against reperfusion injury by preventing mitochondrial permeability transition by an endothelial nitric oxide synthase-dependent mechanism. Anesthesiology. 2009; 112(1):73-85. PMC: 4374483. DOI: 10.1097/ALN.0b013e3181c4a607. View

14.

Brookes P, Kraus D, Shiva S, Doeller J, Barone M, Patel R . Control of mitochondrial respiration by NO*, effects of low oxygen and respiratory state. J Biol Chem. 2003; 278(34):31603-9. DOI: 10.1074/jbc.M211784200. View

15.

An J, Varadarajan S, Novalija E, Stowe D . Ischemic and anesthetic preconditioning reduces cytosolic [Ca2+] and improves Ca(2+) responses in intact hearts. Am J Physiol Heart Circ Physiol. 2001; 281(4):H1508-23. DOI: 10.1152/ajpheart.2001.281.4.H1508. View

16.

Tian Y, Li H, Liu P, Xu J, Irwin M, Xia Z . Captopril Pretreatment Produces an Additive Cardioprotection to Isoflurane Preconditioning in Attenuating Myocardial Ischemia Reperfusion Injury in Rabbits and in Humans. Mediators Inflamm. 2015; 2015:819232. PMC: 4530291. DOI: 10.1155/2015/819232. View

17.

Chiari P, Bienengraeber M, Weihrauch D, Krolikowski J, Kersten J, Warltier D . Role of endothelial nitric oxide synthase as a trigger and mediator of isoflurane-induced delayed preconditioning in rabbit myocardium. Anesthesiology. 2005; 103(1):74-83. DOI: 10.1097/00000542-200507000-00014. View

18.

Andrukhiv A, Costa A, West I, Garlid K . Opening mitoKATP increases superoxide generation from complex I of the electron transport chain. Am J Physiol Heart Circ Physiol. 2006; 291(5):H2067-74. DOI: 10.1152/ajpheart.00272.2006. View

19.

Wojtovich A, Smith C, Urciuoli W, Wang Y, Xia X, Brookes P . Cardiac Slo2.1 Is Required for Volatile Anesthetic Stimulation of K+ Transport and Anesthetic Preconditioning. Anesthesiology. 2016; 124(5):1065-76. PMC: 4837053. DOI: 10.1097/ALN.0000000000001046. View

20.

Zaobornyj T, Valdez L . Heart mitochondrial nitric oxide synthase: a strategic enzyme in the regulation of cellular bioenergetics. Vitam Horm. 2014; 96:29-58. DOI: 10.1016/B978-0-12-800254-4.00003-9. View