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Heat shock protein expression and change of cytochrome c oxidase activity: presence of two phylogenic old systems to protect tissues in ischemia and reperfusion

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Abstract

Induction of heat shock proteins (hsp) has been shown to protect cells from ischemia by providing transient tolerance against myocardial injury and improving postischemic functional recovery. Attenuation of ATP depletion and earlier restoration of ATP content on reperfusion are thought to play a role in this scenario. Hsp induction is accompanied by altered enzyme activity of the respiratory chain, the major generator of ATP under physiological conditions. This report addresses the question whether processing and final assembly of the active holoenzyme cytochrome c oxidase (CcO, complex IV), member of the respiratory chain, is compromised under hypoxic conditions unless protected by stress proteins. Special focus is laid on function of the enzyme’s subunits and importance of cellular energy availability and maintenance.

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References

  • Arnold S, Kadenbach B (1997) Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome-c oxidase. Eur J Biochem 249:350–354

    Article  CAS  Google Scholar 

  • Arnold S, Goglia F, Kadenbach B (1998) 3,5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur J Biochem 252:325–330

    Google Scholar 

  • Arnold S, Kadenbach B (1999) The intramitochondrial ATP/ADP-ratio controls cytochrome c oxidase activity allosterically. FEBS Lett 443:105–108

    Article  CAS  Google Scholar 

  • Ashburner M, Bonner JJ (1979) The induction of gene activity in drosophilia by heat shock. Cell 17:241–254

    Article  CAS  Google Scholar 

  • Boengler K, Gres P, Cabestrero A, Ruiz-Meana M, Garcia-Dorado D, Heusch G, Schulz R (2006) Prevention of the ischemia-induced decrease in mitochondrial Tom20 content by ischemic preconditioning. J Mol Cell Cardiol 41:426–430

    Article  CAS  Google Scholar 

  • Borger DR, Essig DA (1998) Induction of HSP 32 gene in hypoxic cardiomyocytes is attenuated by treatment with N-acetyl-L-cysteine. Am J Physiol 274:H965–H973

    CAS  Google Scholar 

  • Bowers M, Ardehali H (2006) TOM20 and the heartbreakers: evidence for the role of mitochondrial transport proteins in cardioprotection. J Mol Cell Cardiol 41:406–409

    Article  CAS  Google Scholar 

  • Brunori M, Giuffrè A, Forte E, Mastronicola D, Barone MC, Sarti P (2004) Control of cytochrome c oxidase activity by nitric oxide. Biochim Biophys Acta 1655:365–371

    Google Scholar 

  • Calderwood SK, Mambula SS, Gray PJ Jr (2007) Extracellular heat shock proteins in cell signaling and immunity. Ann N Y Acad Sci 1113:28–39

    Article  CAS  Google Scholar 

  • Carr HS, Winge DR (2003) Assembly of cytochrome c oxidase within the mitochondrion. Acc Chem Res 36:309–316

    Article  CAS  Google Scholar 

  • Chang J, Knowlton AA, Xu F, Wasser JS (2001) Activation of the heat shock response: relationship to energy metabolites. A (31)P NMR study in rat hearts. Am J Physiol Heart Circ Physiol 280:H426–H433

    CAS  Google Scholar 

  • Chen HS, Shan YX, Yang TL, Lin HD, Chen JW, Lin SJ, Wang PH (2005) Insulin deficiency downregulated heat shock protein 60 and IGF-1 receptor signaling in diabetic myocardium. Diabetes 54:175–181

    Article  CAS  Google Scholar 

  • Converso DP, Taillé C, Carreras MC, Jaitovich A, Poderoso JJ, Boczkowski J (2006) HO-1 is located in liver mitochondria and modulates mitochondrial heme content and metabolism. FASEB J 20:1236–1238

    Article  CAS  Google Scholar 

  • Cooper CE, Giulivi C (2007) Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology. Am J Physiol Cell Physiol 292:C 1993–C 2003

    Article  CAS  Google Scholar 

  • Cronje FJ, Carraway MS, Freiberger JJ, Suliman HB, Piantadosi CA (2004) Carbon monoxide actuates O(2)-limited heme degradation in the rat brain. Free Radic Biol Med 37:1802–1812

    Article  CAS  Google Scholar 

  • Currie RW, Karmazyn M, Kloc M, Mailer K (1988) Heat-shock response is associated with enhanced postischemic ventricular recovery. Circ Res 63:543–549

    CAS  Google Scholar 

  • D'Amico G, Lam F, Hagen T, Moncada S (2006) Inhibition of cellular respiration by endogenously produced carbon monoxide. J Cell Sci 119:2291–2298

    Article  Google Scholar 

  • Das DK, Maulik N (2006) Cardiac genomic response following preconditioning stimulus. Cardiovasc Res 70:254–263

    Article  CAS  Google Scholar 

  • de Marcos-Lousa C, Sideris DP, Tokatlidis K (2006) Translocation of mitochondrial inner-membrane proteins: conformation matters. Trends Biochem Sci 31:259–267

    Article  Google Scholar 

  • Dedio J, König P, Wohlfart P, Schroeder C, Kummer W, Müller-Esterl W (2001) NOSIP, a novel modulator of endothelial nitric oxide synthase activity. FASEB J 15:79–89

    Article  CAS  Google Scholar 

  • Di Noia MA, Van Driesche S, Palmieri F, Yang LM, Quan S, Goodman AI, Abraham NG (2006) Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome C oxidase activity in experimental diabetes. J Biol Chem 281:15687–15693

    Article  Google Scholar 

  • D'Souza SM, Brown IR (1998) Constitutive expression of heat shock proteins Hsp90, Hsc70, Hsp70 and Hsp60 in neural and non-neural tissues of the rat during postnatal development. Cell Stress Chaperones 3:188–199

    Article  Google Scholar 

  • Dudley R (1998) Atmospheric oxygen, giant Paleozoic insects and the evolution of aerial locomotor performance. J Exp Biol 201:1043–1050

    CAS  Google Scholar 

  • Endo T (1991) Co-operative binding of hsp60 may promote transfer from hsp70 and correct folding of imported proteins in mitochondria. FEBS Lett 293:1–3

    Article  CAS  Google Scholar 

  • Fang JK, Prabu SK, Sepuri NB, Raza H, Anandatheerthavarada HK, Galati D, Spear J, Avadhani NG (2007) Site specific phosphorylation of cytochrome c oxidase subunits I, IVi1 and Vb in rabbit hearts subjected to ischemia/reperfusion. FEBS Lett 581:1302–1310

    Article  CAS  Google Scholar 

  • Fontanesi F, Soto IC, Horn D, Barrientos A (2006) Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am J Physiol Cell Physiol 29:C1129–C1147

    Article  Google Scholar 

  • Fontanesi F, Soto IC, Barrientos A (2008) Cytochrome c oxidase biogenesis: new levels of regulation. IUBMB Life 60:557–568

    Article  CAS  Google Scholar 

  • Frazier AE, Chacinska A, Truscott KN, Guiard B, Pfanner N, Rehling P (2003) Mitochondria use different mechanisms for transport of multispanning membrane proteins through the intermembrane space. Mol Cell Biol 23:7818–7828

    Article  CAS  Google Scholar 

  • Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, Semenza GL (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129:111–122

    Article  CAS  Google Scholar 

  • Genth-Zotz S, Bolger AP, Kalra PR, von Haehling S, Doehner W, Coats AJ, Volk HD, Anker SD (2004) Heat shock protein 70 in patients with chronic heart failure: relation to disease severity and survival. Int J Cardiol 96:397–401

    Article  Google Scholar 

  • Giulivi C, Kato K, Cooper CE (2006) Nitric oxide regulation of mitochondrial oxygen consumption I: cellular physiology. Am J Physiol Cell Physiol 291:C1225–C1231

    Article  CAS  Google Scholar 

  • Glembotski CC (2008) The role of the unfolded protein response in the heart. J Mol Cell Cardiol 44:453–459

    Article  CAS  Google Scholar 

  • Grossman LI, Lomax MI (1997) Nuclear genes for cytochrome c oxidase. Biochim Biophys Acta 1352:174–192

    Google Scholar 

  • Hampton CR, Shimamoto A, Rothnie CL, Griscavage-Ennis J, Chong A, Dix DJ, Verrier ED, Pohlman TH (2003) HSP70.1 and −70.3 are required for late-phase protection induced by ischemic preconditioning of mouse hearts. Am J Physiol Heart Circ Physiol 285:H866–H874

    CAS  Google Scholar 

  • Hooper PL, Hooper PL (2009) Inflammation, heat shock proteins, and type 2 diabetes. Cell Stress Chaperones 14:113–115

    Article  CAS  Google Scholar 

  • Horvat S, Beyer C, Arnold S (2006) Effect of hypoxia on the transcription pattern of subunit isoforms and the kinetics of cytochrome c oxidase in cortical astrocytes and cerebellar neurons. J Neurochem 99:937–951

    Article  CAS  Google Scholar 

  • Hüttemann M, Kadenbach B, Grossman LI (2001) Mammalian subunit IV isoforms of cytochrome c oxidase. Gene 267:111–123

    Google Scholar 

  • Hüttemann M, Lee I, Pecinova A, Pecina P, Przyklenk K, Doan JW (2008) Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease. J Bioenerg Biomembr 40:445–456

    Article  Google Scholar 

  • Jayakumar J, Suzuki K, Khan M, Smolenski RT, Farrell A, Latif N, Raisky O, Abunasra H, Sammut IA, Murtuza B, Amrani M, Yacoub MH (2000) Gene therapy for myocardial protection: transfection of donor hearts with heat shock protein 70 gene protects cardiac function against ischemia-reperfusion injury. Circulation 102(Suppl 3):III302–III306

    CAS  Google Scholar 

  • Jayakumar J, Suzuki K, Sammut IA, Smolenski RT, Khan M, Latif N, Abunasra H, Murtuza B, Amrani M, Yacoub MH (2001) Heat shock protein 70 gene transfection protects mitochondrial and ventricular function against ischemia-reperfusion injury. Circulation 104(Suppl 1):I303–I307

    CAS  Google Scholar 

  • Jeneson JA, Wiseman RW, Westerhoff HV, Kushmerick MJ (1996) The signal transduction function for oxidative phosphorylation is at least second order in ADP. J Biol Chem 271:27995–27998

    Article  CAS  Google Scholar 

  • Jérôme V, Léger J, Devin J, Baulieu EE, Catelli MG (1991) Growth factors acting via tyrosine kinase receptors induce HSP90 alpha gene expression. Growth Factors 4:317–327

    Article  Google Scholar 

  • Kadenbach B, Napiwotzki J, Frank V, Arnold S, Exner S, Hüttemann M (1998) Regulation of energy transduction and electron transfer in cytochrome c oxidase by adenine nucleotides. J Bioenerg Biomembr 30:25–33

    Article  CAS  Google Scholar 

  • Kadenbach B, Hüttemann M, Arnold S, Lee I, Bender E (2000) Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic Biol Med 29:211–221

    Article  CAS  Google Scholar 

  • Kadenbach B, Ramzan R, Vogt S (2009) Degenerative diseases, oxidative stress and cytochrome c oxidase function. Trends Mol Med 15:139–147

    Article  CAS  Google Scholar 

  • Kawana K, Miyamoto Y, Tanonaka K, Han-no Y, Yoshida H, Takahashi M, Takeo S (2000) Cytoprotective mechanism of heat shock protein 70 against hypoxia/reoxygenation injury. J Mol Cell Cardiol 32:2229–2237

    Article  CAS  Google Scholar 

  • Koehler CM, Tienson HL (2009) Redox regulation of protein folding in the mitochondrial intermembrane space. Biochim Biophys Acta 1793:139–145

    Article  CAS  Google Scholar 

  • Kunz W, Bohnensack R, Böhme G, Küster U, Letko G, Schönfeld P (1981) Relations between extramitochondrial and intramitochondrial adenine nucleotide systems. Arch Biochem Biophys 209:219–229

    Article  CAS  Google Scholar 

  • Lee I, Salomon AR, Ficarro S, Mathes I, Lottspeich F, Grossman LI, Hüttemann M (2005) cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J Biol Chem 280:6094–6100

    Article  CAS  Google Scholar 

  • Lemma-Gray P, Weintraub ST, Carroll CA, Musatov A, Robinson NC (2007) Tryptophan 334 oxidation in bovine cytochrome c oxidase subunit I involves free radical migration. FEBS Lett 581:437–442

    Article  CAS  Google Scholar 

  • Li G, Ali IS, Currie RW (2006) Insulin induces myocardial protection and Hsp70 localization to plasma membranes in rat hearts. Am J Physiol Heart Circ Physiol 291:H1709–H1721

    Article  CAS  Google Scholar 

  • Lin KM, Lin B, Lian IY, Mestril R, Scheffler IE, Dillmann WH (2001) Combined and individual mitochondrial HSP60 and HSP10 expression in cardiac myocytes protects mitochodnrial function and prevents apoptotic cell deaths induced by simulated ischemia-reoxygenation. Circulation 103:1787–1792

    Google Scholar 

  • Louapre P, Grongnet JF, Tanguay RM, David JC (2005) Effects of hypoxia on stress proteins in the piglet heart at birth. Cell Stress Chaperones 10(1):17–23

    Article  CAS  Google Scholar 

  • Ludwig B, Bender E, Arnold S, Hüttemann M, Lee I, Kadenbach B (2001) Cytochrome C oxidase and the regulation of oxidative phosphorylation. Chembiochem 2:392–403

    Google Scholar 

  • Meares GP, Zmijewska AA, Jope RS (2004) Heat shock protein-90 dampens and directs signaling stimulated by insulin-like growth factor-1 and insulin. FEBS Lett 574:181–186

    Article  CAS  Google Scholar 

  • Melling CW, Thorp DB, Noble EG (2004) Regulation of myocardial heat shock protein 70 gene expression following exercise. J Mol Cell Cardiol 37:847–855

    Article  CAS  Google Scholar 

  • Melling CW, Thorp DB, Milne KJ, Krause MP, Noble EG (2007) Exercise-mediated regulation of Hsp70 expression following aerobic exercise training. Am J Physiol Heart Circ Physiol 293:H3692–H3698

    Article  CAS  Google Scholar 

  • Niizeki T, Takeishi Y, Watanabe T, Nitobe J, Miyashita T, Miyamoto T, Kitahara T, Suzuki S, Sasaki T, Bilim O, Ishino M, Kubota I (2008) Relation of serum heat shock protein 60 level to severity and prognosis in chronic heart failure secondary to ischemic or idiopathic dilated cardiomyopathy. Am J Cardiol 102:606–610

    Article  CAS  Google Scholar 

  • Nijtmans LG, Taanman JW, Muijsers AO, Speijer D, Van den Bogert C (1998) Assembly of cytochrome-c oxidase in cultured human cells. Eur J Biochem 254:389–394

    Article  CAS  Google Scholar 

  • Ou J, Fontana JT, Ou Z, Jones DW, Ackerman AW, Oldham KT, Yu J, Sessa WC, Pritchard KA Jr (2004) Heat shock protein 90 and tyrosine kinase regulate eNOS NO* generation but not NO* bioactivity. Am J Physiol Heart Circ Physiol 286:H561–H569

    Article  CAS  Google Scholar 

  • Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E (1997) Age-dependent decline in the cytochrome c oxidase activity in rat heart. mitochondria: role of cardiolipin. FEBS Lett 406:136–138

    Google Scholar 

  • Pfanner N, Söllner T, Neupert W (1991) Mitochondrial import receptors for precursor proteins. Trends Biochem Sci 16:63–67

    Article  Google Scholar 

  • Prabhakar NR (1998) Endogenous carbon monoxide in control of respiration. Respir Physiol 114:57–64

    Article  CAS  Google Scholar 

  • Prabu SK, Anandatheerthavarada HK, Raza H, Srinivasan S, Spear JF, Avadhani NG (2006) Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J Biol Chem 281:2061–2070

    Article  CAS  Google Scholar 

  • Racay P, Tatarkova Z, Drgova A, Kaplan P, Dobrota D (2009) Ischemia-reperfusion induces inhibition of mitochondrial protein synthesis and cytochrome c oxidase activity in rat hippocampus. Physiol Res 58:127–138

    CAS  Google Scholar 

  • Sammut IA, Harrison JC (2003) Cardiac mitochondrial complex activity is enhanced by heat shock proteins. Clin Exp Pharmacol Physiol 30:110–115

    Article  CAS  Google Scholar 

  • Sammut IA, Jayakumar J, Latif N, Rothery S, Severs NJ, Smolenski RT, Bates TE, Yacoub MH (2001) Heat stress contributes to the enhancement of cardiac mitochondrial complex activity. Am J Pathol 158:1821–1831

    Article  CAS  Google Scholar 

  • Schmitt JP, Schunkert H, Birnbaum DE, Aebert H (2002) Kinetics of heat shock protein 70 synthesis in the human heart after cold cardioplegic arrest. Eur J Cardiothorac Surg 22:415–420

    Article  CAS  Google Scholar 

  • Sheehan TE, Kumar PA, Hood DA (2004) Tissue-specific regulation of cytochrome c oxidase subunit expression by thyroid hormone. Am J Physiol Endocrinol Metab 286:E968–E974

    Article  CAS  Google Scholar 

  • Simkhovich BZ, Marjoram P, Poizat C, Kedes L, Kloner RA (2003) Brief episode of ischemia activates protective genetic program in rat heart: a gene chip study. Cardiovasc Res 59:450–459

    Article  CAS  Google Scholar 

  • Sin YT (1975) Induction of puffs in drosophila salivary gland cells by mitochondrial factors. Nature 258:159–160

    Article  CAS  Google Scholar 

  • Tamura Y, Harada Y, Shiota T, Yamano K, Watanabe K, Yokota M, Yamamoto H, Sesaki H, Endo T (2009) Tim23-Tim50 pair coordinates functions of translocators and motor proteins in mitochondrial protein import. J Cell Biol 184:129–141

    Article  CAS  Google Scholar 

  • Terui K, Haga S, Enosawa S, Ohnuma N, Ozaki M (2004) Hypoxia/re-oxygenation-induced, redox-dependent activation of STAT1 (signal transducer and activator of transcription 1) confers resistance to apoptotic cell death via hsp70 induction. Biochem J 380(Pt 1):203–209

    Article  CAS  Google Scholar 

  • Truscott KN, Pfanner N, Voos W (2001) Transport of proteins into mitochondria. Rev Physiol Biochem Pharmacol 143:81–136

    Article  CAS  Google Scholar 

  • Valen G, Hansson GK, Dumitrescu A, Vaage J (2000) Unstable angina activates myocardial heat shock protein 72, endothelial nitric oxide synthase, and transcription factors NFkappaB and AP-1. Cardiovasc Res 47:49–56

    Article  CAS  Google Scholar 

  • Vijayasarathy C, Biunno I, Lenka N, Yang M, Basu A, Hall IP, Avadhani NG (1998) Variations in the subunit content and catalytic activity of the cytochrome c oxidase complex from different tissues and different cardiac compartments. Biochim Biophys Acta 1371:71–82

    Article  CAS  Google Scholar 

  • Vijayasarathy C, Damle S, Prabu SK, Otto CM, Avadhani NG (2003) Adaptive changes in the expression of nuclear and mitochondrial encoded subunits of cytochrome c oxidase and the catalytic activity during hypoxia. Eur J Biochem 270:871–879

    Article  CAS  Google Scholar 

  • Vittorini S, Storti S, Andreani G, Giusti L, Murzi B, Furfori P, Baroni A, De Lucia V, Luisi VS, Clerico A (2007) Heat shock protein 70–1 gene expression in pediatric heart surgery using blood cardioplegia. Clin Chem Lab Med 45:244–248

    Article  CAS  Google Scholar 

  • Vogt S, Troitzsch D, Abdul-Khaliq H, Böttcher W, Lange PE, Moosdorf R (2000) Improved myocardial preservation with short hyperthermia prior to cold cardioplegic ischemia in immature rabbit hearts. Eur J Cardiothorac Surg 18:233–240

    Article  CAS  Google Scholar 

  • Vogt S, Rhiel A, Koch V, Kadenbach B (2007a) Regulation of oxidative phosphorylation by inhibition of its enzyme complexes via reversible phosphorylation. Curr Enzym Inhib 3:189–206

    Article  CAS  Google Scholar 

  • Vogt S, Troitzsch D, Abdul-Khaliq H, Moosdorf R (2007b) Heat stress attenuates ATP-depletion and pH-decrease during cardioplegic arrest. J Surg Res 139:176–181

    Article  CAS  Google Scholar 

  • Wagner K, Mick DU, Rehling P (2009) Protein transport machineries for precursor translocation across the inner mitochondrial membrane. Biochim Biophys Acta 1793:52–59

    Article  CAS  Google Scholar 

  • Williamson CL, Dabkowski ER, Dillmann WH, Hollander JM (2008) Mitochondria protection from hypoxia/reoxygenation injury with mitochondria heat shock protein 70 overexpression. Am J Physiol Heart Circ Physiol 294:H249–H256

    Article  CAS  Google Scholar 

  • Wilson N, McArdle A, Guerin D, Tasker H, Wareing P, Foster CS, Jackson MJ, Rhodes LE (2000) Hyperthermia to normal human skin in vivo upregulates heat shock proteins 27, 60, 72i and 90. J Cutan Pathol 27:176–182

    Article  CAS  Google Scholar 

  • Yu Q, Nguyen T, Ogbi M, Caldwell RW, Johnson JA (2008) Differential loss of cytochrome-c oxidase subunits in ischemia-reperfusion injury: exacerbation of COI subunit loss by PKC-epsilon inhibition. Am J Physiol Heart Circ Physiol 294:H2637–H2645

    Article  CAS  Google Scholar 

  • Zhao Y, Wang W, Qian L (2007) Hsp70 may protect cardiomyocytes from stress-induced injury by inhibiting Fas-mediated apoptosis. Cell Stress Chaperones 12:83–95

    Article  CAS  Google Scholar 

  • Zimmermann K, Opitz N, Dedio J, Renne C, Muller-Esterl W, Oess S (2002) NOSTRIN: a protein modulating nitric oxide release and subcellular distribution of endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 99:17167–17172

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Cardiovascular Research Lab, Biomedical Research Center, Philipps- University Marburg, Hans Meerwein Str. 2, 35043, Marburg, Germany

    Sebastian Vogt, Petra Weber & Rabia Ramzan

  2. Center for Internal Medicine- Cardiology, Marburg, Germany

    Irene Portig & Volker Ruppert

  3. Cardiovascular Surgery, Universitätsklinikum Marburg und Giessen GmbH, Marburg, Germany

    Sebastian Vogt & Mark Irqsusi

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  1. Sebastian Vogt
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Vogt, S., Portig, I., Irqsusi, M. et al. Heat shock protein expression and change of cytochrome c oxidase activity: presence of two phylogenic old systems to protect tissues in ischemia and reperfusion. J Bioenerg Biomembr 43, 425–435 (2011). https://doi.org/10.1007/s10863-011-9367-2

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