In vivo desflurane preconditioning evokes dynamic alterations of metabolic proteins in the heart - Proteomic insights strengthen the link between bioenergetics and cardioprotection

Cellular Physiology and Biochemistry

Volumn 33, Issue 4, 2014, Pages 967-981

  Dyballa Rukes, Nadine ^a   Schuh, Christian ^a   Vogt, Hendrik ^a   Toma, Octavian ^b   Schlack, Wolfgang S ^b   Weber, Nina C ^b   Metzger, Sabine ^a,c  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Desflurane; Preconditioning; Protein remodelling; Proteomics; Volatile anaesthetics

Indexed keywords

DESFLURANE; ACONITASE 2; ACONITATE HYDRATASE; ALBUMIN; ASPARTATE AMINOTRANSFERASE ISOENZYME 1; ASPARTATE AMINOTRANSFERASE ISOENZYME 2; CARBONATE DEHYDRATASE I; CARBONATE DEHYDRATASE II; INORGANIC PYROPHOSPHATASE; ISOPROTEIN; LACTATE DEHYDROGENASE; METHYLMALONATE SEMIALDEHYDE DEHYDROGENASE (ACYLATING); MITOCHONDRIAL PROTEIN; NADH DEHYDROGENASE UBIQUINONE FLAVOPROTEIN 1; PROTEOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE CORE PROTEIN 1; UNCLASSIFIED DRUG; INHALATION ANESTHETIC AGENT; ISOFLURANE;

ACIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENERGY; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FRACTIONATION; HEART; HEART PROTECTION; IN VIVO STUDY; ISCHEMIC PRECONDITIONING; MALE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; RAT; REPEATED DRUG DOSE; TWO DIMENSIONAL GEL ELECTROPHORESIS; CALCIUM BALANCE; PROTEIN ANALYSIS; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; HEART INFARCTION PREVENTION; HEART MUSCLE; HEART VENTRICLE REMODELING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM;

RATTUS;

ANESTHETICS, INHALATION; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HEART; ISCHEMIC PRECONDITIONING, MYOCARDIAL; ISOFLURANE; MYOCARDIUM; PROTEIN ISOFORMS; PROTEOME; RATS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; VENTRICULAR REMODELING;

EID: 84897362280     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000358668     Document Type: Article

References (53)

1. Lu X, Moore PG, Liu H, Schaefer S: Phosphorylation of ARC is a critical element in the antiapoptotic effect of anesthetic preconditioning. Anesth Analg 2011;112:525-531.
2. Sedlic F, Pravdic D, Ljubkovic M, Marinovic J, Stadnicka A, Bosnjak ZJ: Differences in production of reactive oxygen species and mitochondrial uncoupling as events in the preconditioning signaling cascade between desflurane and sevoflurane. Anesth Analg 2009;109:405-411.
3. Redel A, Lange M, Jazbutyte V, Lotz C, Smul TM, Roewer N, Kehl F: Activation of mitochondrial large-conductance calcium-activated K+ channels via protein kinase A mediates desflurane-induced preconditioning. Anesth Analg 2008;106:384-391.
4. Smul TM, Lange M, Redel A, Burkhard N, Roewer N, Kehl F: Desflurane-induced preconditioning against myocardial infarction is mediated by nitric oxide. Anesthesiology 2006;105:719-725.
5. Toma O, Weber NC, Wolter JI, Obal D, Preckel B, Schlack W: Desflurane preconditioning induces time-dependent activation of protein kinase C epsilon and extracellular signal-regulated kinase 1 and 2 in the rat heart in vivo. Anesthesiology 2004;101:1372-1380.
6. Ebel D, Müllenheim J, Südkamp H, Bohlen T, Ferrari J, Huhn R, Preckel B, Schlack W: Role of tyrosine kinase in desflurane-induced preconditioning. Anesthesiology 2004;100:555-561.
7. Bein B, Renner J, Caliebe D, Hanss R, Bauer M, Fraund S, Scholz J: The effects of interrupted or continuous administration of sevoflurane on preconditioning before cardio-pulmonary bypass in coronary artery surgery: comparison with continuous propofol. Anaesthesia 2008;63:1046-1055.
8. Frässdorf J, Borowski A, Ebel D, Feindt P, Hermes M, Meemann T, Weber R, Müllenheim J, Weber NC, Preckel B, Schlack W: Impact of preconditioning protocol on anesthetic-induced cardioprotection in patients having coronary artery bypass surgery. J Thorac Cardiovasc Surg 2009;137:1436-1442.
9. Meco M, Cirri S, Gallazzi C, Magnani G, Cosseta D: Desflurane preconditioning in coronary artery bypass graft surgery: a double-blinded, randomised and placebo-controlled study. Eur J Cardio-Thorac Surg 2007;32:319-325.
10. Piriou V, Chiari P, Lhuillier F, Bastien O, Loufoua J, Raisky O, David JS, Ovize M, Lehot JJ: Pharmacological preconditioning: comparison of desflurane, sevoflurane, isoflurane and halothane in rabbit myocardium. Br J Anaesth 2002;89:486-491.
11. Lotz C, Fisslthaler B, Redel A, Smul TM, Stumpner J, Pociej J, Roewer N, Fleming I, Kehl F, Lange M: Activation of adenosine-monophosphate-activated protein kinase abolishes desflurane-induced preconditioning against myocardial infarction in vivo. J Cardiothorac Vasc Anesth 2011;25:66-71.
12. Lange M, Smul TM, Redel A, Lotz C, Jazbutyte V, Schnupp V, Roewer N, Kehl F: Differential role of calcium/calmodulin-dependent protein kinase II in desflurane-induced preconditioning and cardioprotection by metoprolol: metoprolol blocks desflurane-induced preconditioning. Anesthesiology 2008;109:72-80.
13. Stumpner J, Redel A, Kellermann A, Lotz CA, Blomeyer CA, Smul TM, Kehl F, Roewer N, Lange M: Differential role of Pim-1 kinase in anesthetic-induced and ischemic preconditioning against myocardial infarction. Anesthesiology 2009;111:1257-1264.
14. Feng J, Zhu M, Schaub MC, Gehrig P, Roschitzki B, Lucchinetti E, Zaugg M: Phosphoproteome analysis of isoflurane-protected heart mitochondria: phosphorylation of adenine nucleotide translocator-1 on Tyr194 regulates mitochondrial function. Cardiovasc Res 2008;80:20-29.
15. Xiao Y-Y, Chang Y-T, Ran K, Liu J-P: Delayed preconditioning by sevoflurane elicits changes in the mitochondrial proteome in ischemia-reperfused rat hearts. Anesth Analg 2011;113:224-232.
16. Bienengraeber M, Pellitteri-Hahn M, Hirata N, Baye TM, Bosnjak ZJ, Olivier M: Quantitative characterization of changes in the cardiac mitochondrial proteome during anesthetic preconditioning and ischemia. Physiol Genomics 2013;45:163-170.
17. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
18. Kang D, Gho YS, Suh M, Kang C: Highly sensitive and fast protein detection with Coomassie Brilliant Blue in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Bull Korean Chem Soc 2002;23:1511-1512.
19. Dyballa N, Metzger S: Fast and sensitive colloidal coomassie G-250 staining for proteins in polyacrylamide gels. J Vis Exp. 2009;(30). pii: 1431. doi: 10.3791/1431
20. 2 species formation and preserved mitochondrial NADH and [Ca2+] levels during short-term 17 degrees C ischemia in intact hearts. Cardiovasc Res 2004;61:580-590.
21. Riess ML, Camara AKS, Chen Q, Novalija E, Rhodes SS, Stowe DF: Altered NADH and improved function by anesthetic and ischemic preconditioning in guinea pig intact hearts. Am J Physiol Heart Circ Physiol 2002;283:H53-60.
22. Nishimura M, Takami H, Kaneko M, Nakano S, Matsuda H, Kurosawa K, Inoue T, Tagawa K: Mechanism of mitochondrial enzyme leakage during reoxygenation of the rat heart. Cardiovasc Res 1993;27:1116-1122.
23. Ouyang Y-B, Kuroda S, Kristián T, Siesjö BK: Release of mitochondrial aspartate aminotransferase (mAST) following transient focal cerebral ischemia suggests the opening of a mitochondrial permeability transition pore. Neurosci Res Commun 1997;20:167-173.
24. Bulteau A-L, Lundberg KC, Ikeda-Saito M, Isaya G, Szweda LI: Reversible redox-dependent modulation of mitochondrial aconitase and proteolytic activity during in vivo cardiac ischemia/reperfusion. Proc Natl Acad Sci 2005;102:5987-5991.
25. Hunzinger C, Wozny W, Schwall GP, Poznanović S, Stegmann W, Zengerling H, Schoepf R, Groebe K, Cahill MA, Osiewacz HD, Jägemann N, Bloch M, Dencher NA, Krause F, Schrattenholz A: Comparative profiling of the mammalian mitochondrial proteome: multiple aconitase-2 isoforms including N-formylkynurenine modifications as part of a protein biomarker signature for reactive oxidative species. J Proteome Res 2006;5:625-633.
26. Yarian CS, Rebrin I, Sohal RS: Aconitase and ATP synthase are targets of malondialdehyde modification and undergo an age-related decrease in activity in mouse heart mitochondria. Biochem Biophys Res Commun 2005;330:151-156.
27. Yarian CS, Sohal RS: In the aging housefly aconitase is the only citric acid cycle enzyme to decline significantly. J Bioenerg Biomembr 2005;37:91-96.
28. Hanouz J-L, Zhu L, Lemoine S, Durand C, Lepage O, Massetti M, Khayat A, Plaud B, Gérard J-L: Reactive oxygen species mediate sevoflurane-and desflurane-induced preconditioning in isolated human right atria in vitro. Anesth Analg 2007;105:1534-1539, table of contents.
29. Müllenheim J, Ebel D, Frässdorf J, Preckel B, Thämer V, Schlack W: Isoflurane preconditions myocardium against infarction via release of free radicals. Anesthesiology 2002;96:934-940.
30. Riess ML, Kevin LG, McCormick J, Jiang MT, Rhodes SS, Stowe DF: Anesthetic preconditioning: the role of free radicals in sevoflurane-induced attenuation of mitochondrial electron transport in Guinea pig isolated hearts. Anesth Analg 2005;100:46-53.
31. Tanaka K, Weihrauch D, Kehl F, Ludwig LM, LaDisa JF, Kersten JR, Pagel PS, Warltier DC: Mechanism of preconditioning by isoflurane in rabbits: a direct role for reactive oxygen species. Anesthesiology 2002;97:1485-1490.
32. Novalija E, Varadarajan SG, Camara AKS, An J, Chen Q, Riess ML, Hogg N, Stowe DF: Anesthetic preconditioning: triggering role of reactive oxygen and nitrogen species in isolated hearts. Am J Physiol Heart Circ Physiol 2002;283:H44-52.
33. Tanaka K, Kehl F, Gu W, Krolikowski JG, Pagel PS, Warltier DC, Kersten JR: Isoflurane-induced preconditioning is attenuated by diabetes. Am J Physiol Heart Circ Physiol 2002;282:H2018-2023.
34. Dean RT, Fu S, Stocker R, Davies MJ: Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 1997;324:1-18.
35. Wen J-J, Garg N: Oxidative modification of mitochondrial respiratory complexes in response to the stress of Trypanosoma cruzi infection. Free Radic Biol Med 2004;37:2072-2081.
36. Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH: The impact of oxidative stress on Arabidopsis mitochondria. Plant J Cell Mol Biol 2002;32:891-904.
37. Møller IM, Kristensen BK: Protein oxidation in plant mitochondria detected as oxidized tryptophan. Free Radic Biol Med 2006;40:430-435.
38. Iuso A, Scacco S, Piccoli C, Bellomo F, Petruzzella V, Trentadue R, Minuto M, Ripoli M, Capitanio N, Zeviani M, Papa S: Dysfunctions of Cellular Oxidative Metabolism in Patients with Mutations in the NDUFS1 and NDUFS4 Genes of Complex I. J Biol Chem 2006;281:10374-10380.
39. Falk MJ, Kayser E-B, Morgan PG, Sedensky MM: Mitochondrial Complex I Function Modulates Volatile Anesthetic Sensitivity in C. elegans. Curr Biol 2006;16:1641-1645.
40. Mayr M, Liem D, Zhang J, Li X, Avliyakulov NK, Yang JI, Young G, Vondriska TM, Ladroue C, Madhu B, Griffiths JR, Gomes A, Xu Q, Ping P: Proteomic and metabolomic analysis of cardioprotection: Interplay between protein kinase C epsilon and delta in regulating glucose metabolism of murine hearts. J Mol Cell Cardiol 2009;46:268-277.
41. Perrelli M-G, Pagliaro P, Penna C: Ischemia/reperfusion injury and cardioprotective mechanisms: Role of mitochondria and reactive oxygen species. World J Cardiol 2011;3:186-200.
42. Wong R, Aponte AM, Steenbergen C, Murphy E: Cardioprotection leads to novel changes in the mitochondrial proteome. Am J Physiol Heart Circ Physiol 2010;298:H75-91.
43. Arrell DK, Elliott ST, Kane LA, Guo Y, Ko YH, Pedersen PL, Robinson J, Murata M, Murphy AM, Marbán E, Van Eyk JE: Proteomic analysis of pharmacological preconditioning: novel protein targets converge to mitochondrial metabolism pathways. Circ Res 2006;99:706-714.
44. Wang L, Ko KWS, Lucchinetti E, Zhang L, Troxler H, Hersberger M, Omar MA, Posse de Chaves EI, Lopaschuk GD, Clanachan AS, Zaugg M: Metabolic profiling of hearts exposed to sevoflurane and propofol reveals distinct regulation of fatty acid and glucose oxidation: CD36 and pyruvate dehydrogenase as key regulators in anesthetic-induced fuel shift. Anesthesiology 2010;113:541-551.
45. Shen Y-T, Depre C, Yan L, Park JY, Tian B, Jain K, Chen L, Zhang Y, Kudej RK, Zhao X, Sadoshima J, Vatner DE, Vatner SF: Repetitive ischemia by coronary stenosis induces a novel window of ischemic preconditioning. Circulation 2008;118:1961-1969.
46. De Hert SG, Preckel B, Hollmann MW, Schlack WS: Drugs mediating myocardial protection. Eur J Anaesthesiol 2009;26:985-995.
47. Hu Z-Y, Liu J: Mechanism of cardiac preconditioning with volatile anaesthetics. Anaesth Intensive Care 2009;37:532-538.
48. Przyklenk K: Reduction of myocardial infarct size with ischemic "conditioning": physiologic and technical considerations. Anesth Analg 2013;117:891-901.
49. Frässdorf J, De Hert S, Schlack W: Anaesthesia and myocardial ischaemia/reperfusion injury. Br J Anaesth 2009;103:89-98.
50. Landoni G, Fochi O, Tritapepe L, Guarracino F, Belloni I, Bignami E, Zangrillo A: Cardiac protection by volatile anesthetics. A review. Minerva Anestesiol 2009;75:269-273.
51. Burwell LS, Nadtochiy SM, Brookes PS: Cardioprotection by metabolic shut-down and gradual wake-up. J Mol Cell Cardiol 2009;46:804-810.
52. Petrak J, Ivanek R, Toman O, Cmejla R, Cmejlova J, Vyoral D, Zivny J, Vulpe CD: Déjà vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins. Proteomics 2008;8:1744-1749.
53. Kalenka A, Maurer MH, Feldmann RE, Kuschinsky W, Waschke KF: Volatile anesthetics evoke prolonged changes in the proteome of the left ventricule myocardium: defining a molecular basis of cardioprotection? Acta Anaesthesiol Scand 2006;50:414-427.