Circulation Research. 2001
Published online before print July 5, 2001, doi: 10.1161/hh1401.093440
Published online before print July 5, 2001, doi: 10.1161/hh1401.093440
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© 2001 American Heart Association, Inc.
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Energetic Crosstalk Between Organelles
Architectural Integration of Energy Production and Utilization
From the Cardiologie Cellulaire et Moléculaire U-446 INSERM (A.K., V.V., E.B., A.M., R.V.-C.), Université Paris-Sud, Châtenay-Malabry, France; Molecular Physiology and Genetics (M.N.), Slovak Academy of Sciences, Bratislava, Slovak Republic. Present address for A.K. is Department of Pharmacology, University of Tartu, Tartu, Estonia; present address for E.B. is Wellcome Trust Centre for Human Genetics, Oxford, UK.
Correspondence to Renée Ventura-Clapier, U-446 INSERM, Faculté de Pharmacie, 92 296 Châtenay-Malabry, France. E-mail Renee.Ventura{at}cep.u-psud.fr
Abstract
Abstract—Cells with high and fluctuating energy demands such as cardiomyocytes need efficient systems to link energy production to energy utilization. This is achieved in part by compartmentalized energy transfer enzymes such as creatine kinase (CK). However, hearts from CK-deficient mice develop normal cardiac function under conditions of moderate workload. We have therefore investigated whether a direct functional interplay exists between mitochondria and sarcoplasmic reticulum or between mitochondria and myofilaments in cardiac cells that catalyzes direct energy and signal channeling between organelles. We used the selective permeabilization of sarcolemmal membranes with saponin to study the functional interactions between organelles within the cellular architecture. We measured contractile kinetics, oxygen consumption, and caffeine-induced tension transients. The results show that in hearts of normal mice, ATP produced by mitochondria (supplied with substrates, oxygen, and adenine nucleotides) was able to sustain calcium uptake and contractile speed. Moreover, direct mitochondrially supplied ATP was nearly as effective as CK-supplied ATP and much more effective than externally supplied ATP, suggesting that a direct ATP/ADP channeling exists between the sites of energy production (mitochondria) and energy utilization (sarcoplasmic reticulum and myofilaments). On the other hand, in cardiac cells of mice deficient in mitochondrial and cytosolic CK, marked cytoarchitectural modifications were observed, and direct adenine nucleotide channeling between mitochondria and organelles was still effective for sarcoplasmic reticulum and myofilaments. Such direct crosstalk between organelles may explain the preserved cardiac function of CK-deficient mice under moderate workloads.
Key Words: mitochondria • sarcoplasmic reticulum • myofibrils • creatine kinase • knockout mice
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