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Regulation of mitochondrial energy production in cardiac cells of rainbow trout (Oncorhynchus mykiss)

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Abstract

In skinned rat cardiac fibres, mitochondrial affinity for endogenous ADP generated by creatine kinase and Ca2+-activated ATPases is higher than for exogenous ADP added to the surrounding medium, suggesting that mitochondria are functionally coupled to creatine kinase and ATPases. Such a coupling may be weaker or absent in ectothermic vertebrate cardiac cells, because they typically have less elaborate intracellular membrane structures, higher glycolytic capacity and lower working temperature. Therefore, we examined skinned cardiac fibres from rainbow trout at 10 °C. The apparent mitochondrial affinity for endogenous ADP was obtained by stimulation with ATP and recording of the release of ADP into the surrounding medium. The apparent affinity for endogenous ADP was much higher than for exogenous ADP suggesting a functional coupling between mitochondria and ATPases. The apparent affinity for exogenous ADP and ATP was increased by creatine or an increase in Ca2+-activity, which should increase intrafibrillar turnover of ATP to ADP. In conclusion, ADP seems to be channelled from creatine kinase and ATPases to mitochondria without being released to the surrounding medium. Thus, despite difference in structure, temperature and metabolic capacity, trout myocardium resembles that of rat with regard to the regulation of mitochondrial respiration.

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Abbreviations

ACR :

acceptor control ratio

ANT :

adenine nucleotide translocase

K M ADP :

apparent mitochondrial affinity for ADP

K M ATP :

apparent mitochondrial affinity for ATP

LDH :

lactate dehydrogenase

V ADP :

ADP-stimulated respiration rate

V ADP max :

maximal ADP-stimulated respiration rate

V ATP :

ATP-stimulated respiration rate

V ATP max :

maximal ATP-stimulated respiration rate

V 0 :

basal respiration rate in the absence of ADP

References

  • Andrienko T, Kuznetzov AV, Kaanbre T, Usson Y, Orosco A, Appaix F, Tiivel T, Sikk P, Vendelin M, Margreiter R, Saks VA (2003) Metabolic consequences of functional complexes of mitochondria, myofibrils and sarcoplasmic reticulum in muscle cells. J Exp Biol 206:2059–2072

    Google Scholar 

  • Ban K, Handa S, Chapman RA (1999) On the mechanism of the failure of mitochondrial function in isolated guinea-pig myocytes subjected to a Ca2+ overload. Cardiovasc Res 44:556–567

    Google Scholar 

  • Bers DM, Patton CW, Nuccitelli R (1994) A practical guide to the preparation of Ca2+ buffers. Methods Cell Biol 40:3–29

    Google Scholar 

  • Birkedal R, Gesser H (2003) Creatine kinase and mitochondrial respiration in hearts of trout, cod and freshwater turtle. J Comp Physiol B 173:493–499

    Article  CAS  PubMed  Google Scholar 

  • Brand MD (1990) The proton leak across the mitochondrial inner membrane. Biochim Biophys Acta 1018:128–133

    CAS  PubMed  Google Scholar 

  • Brown GC (1992) Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem J 284:1–13

    CAS  PubMed  Google Scholar 

  • Brown GC, Brand MD (1991) On the nature of the mitochondrial proton leak. Biochim Biophys Acta 1059:55–62

    CAS  PubMed  Google Scholar 

  • Christensen M, Hartmund T, Gesser H (1994) Creatine kinase, energy-rich phosphates and energy metabolism in heart muscle of different vertebrates. J Comp Physiol B 164:118–123

    CAS  Google Scholar 

  • Degn P, Gesser H (1997) Ca2+ activated myosin-ATPase in cardiac myofibrils of rainbow trout, freshwater turtle, and rat. J Exp Zool 278:381–390

    Article  CAS  PubMed  Google Scholar 

  • Dixon M, Webb EC (1979) Enzymes, 3rd edn. Academic Press, New York

  • Gesser H, Poupa O (1973) The lactate dehydrogenase system in the heart and skeletal muscle of fish: a comparative study. Comp Biochem Physiol B 46:683–690

    Article  CAS  PubMed  Google Scholar 

  • Hill RW, Wyse GA (1989) Animal Physiology, 2nd edn. Harper–Collins, New York

  • Hubley MJ, Locke BR, Moerland TS (1997) Reaction-diffusion analysis of the effects of temperature on high-energy phosphate dynamics in goldfish skeletal muscle. J Exp Biol 200:975–988

    CAS  PubMed  Google Scholar 

  • Kaasik A, Veksler V, Boehm E, Novotova M, Minajeva A, Ventura-Clapier R (2001) Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ Res 89:153–159

    CAS  PubMed  Google Scholar 

  • Kinsey ST, Moerland TS (2002) Metabolite diffusion in giant muscle fibers of the spiny lobster Panulirus argus. J Exp Biol 205:3377–3386

    CAS  PubMed  Google Scholar 

  • Lowry OH, Passonneau JV (1972) A flexible system of enzymatic analysis. Academic Press

  • Saks VA, Veksler VI, Kuznetsov AV, Kay L, Sikk P, Tiivel T, Tranqui L, Olivares J, Winkler K, Wiedemann F, Kunz WS (1998) Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 184:81–100

    Article  CAS  PubMed  Google Scholar 

  • Saks VA, Kaambre T, Sikk P, Eimre M, Orlova E, Paju K, Piirsoo A, Appaix F, Kay L, Regitz-Zagrosek V, Fleck E, Seppet E (2001) Intracellular energetic units in red muscle cells. Biochem J 356:643–657

    Article  CAS  PubMed  Google Scholar 

  • Santer RM (1974) The organization of the sarcoplasmic reticulum in teleost ventricular myocardial cells. Cell Tissue Res 151:395–402

    PubMed  Google Scholar 

  • Seppet EK, Kaambre T, Sikk P, Tiivel T, Vija H, Tonkonogi M, Sahlin K, Kay L, Appaix F, Braun U, Eimre M, Saks VA (2001) Functional complexes of mitochondria with Ca, MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells. Biochim Biophys Acta 1504:379–395

    Article  CAS  PubMed  Google Scholar 

  • Tibbits GF, Kashihara H, Thomas MJ, Keen JE, Farrell AP (1990) Ca2+ transport in myocardial sarcolemma from rainbow trout. Am J Physiol 259:R453–R460

    PubMed  Google Scholar 

  • Tibbits GF, Hove-Madsen L, Bers DM (1991) Calcium transport and the regulation of cardiac contractility in teleosts: a comparison with higher vertebrates. Can J Zool 69:2014–2019

    CAS  Google Scholar 

  • Ventura-Clapier R, Kuznetsov A, Veksler V, Boehm E, Anflous K (1998) Functional coupling of creatine kinases in muscles: species and tissue specificity. Mol Cell Biochem 184:231–247

    Article  CAS  PubMed  Google Scholar 

  • Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the ‘phosphocreatine circuit’ for cellular energy homeostasis. Biochem J 281:21–40

    CAS  PubMed  Google Scholar 

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Acknowledgements

We wish to acknowledge the support of this study by the Danish Research Council and engineer Einer Larsen for the construction of the computer program used for collection of data.

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Correspondence to R. Birkedal.

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Communicated by G. Heldmaier

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Birkedal, R., Gesser, H. Regulation of mitochondrial energy production in cardiac cells of rainbow trout (Oncorhynchus mykiss). J Comp Physiol B 174, 255–262 (2004). https://doi.org/10.1007/s00360-003-0410-4

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