Modular organization of cardiac energy metabolism: energy conversion, transfer and feedback regulation

R. Guzun, T. Kaambre, R. Bagur, A. Grichine, Y. Usson, M. Varikmaa, T. Anmann, K. Tepp, N. Timohhina, I. Shevchuk, V. Chekulayev, F. Boucher, P. Dos Santos, U. Schlattner, T. Wallimann, A. V. Kuznetsov, Petras P Dzeja, M. Aliev, V. Saks

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

To meet high cellular demands, the energy metabolism of cardiac muscles is organized by precise and coordinated functioning of intracellular energetic units (ICEUs). ICEUs represent structural and functional modules integrating multiple fluxes at sites of ATP generation in mitochondria and ATP utilization by myofibrillar, sarcoplasmic reticulum and sarcolemma ion-pump ATPases. The role of ICEUs is to enhance the efficiency of vectorial intracellular energy transfer and fine tuning of oxidative ATP synthesis maintaining stable metabolite levels to adjust to intracellular energy needs through the dynamic system of compartmentalized phosphoryl transfer networks. One of the key elements in regulation of energy flux distribution and feedback communication is the selective permeability of mitochondrial outer membrane (MOM) which represents a bottleneck in adenine nucleotide and other energy metabolite transfer and microcompartmentalization. Based on the experimental and theoretical (mathematical modelling) arguments, we describe regulation of mitochondrial ATP synthesis within ICEUs allowing heart workload to be linearly correlated with oxygen consumption ensuring conditions of metabolic stability, signal communication and synchronization. Particular attention was paid to the structure-function relationship in the development of ICEU, and the role of mitochondria interaction with cytoskeletal proteins, like tubulin, in the regulation of MOM permeability in response to energy metabolic signals providing regulation of mitochondrial respiration. Emphasis was given to the importance of creatine metabolism for the cardiac energy homoeostasis.

Original languageEnglish (US)
Pages (from-to)84-106
Number of pages23
JournalActa Physiologica
Volume213
Issue number1
DOIs
StatePublished - Jan 1 2015

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Energy Transfer
Energy Metabolism
Adenosine Triphosphate
Mitochondrial Membranes
Permeability
Mitochondria
Ion Pumps
Sarcolemma
Cytoskeletal Proteins
Adenine Nucleotides
Creatine
Sarcoplasmic Reticulum
Tubulin
Workload
Oxygen Consumption
Adenosine Triphosphatases
Myocardium
Respiration
Homeostasis

Keywords

  • cardiac metabolism
  • creatine kinase
  • mitochondria
  • respiration regulation

ASJC Scopus subject areas

  • Medicine(all)

Cite this

Guzun, R., Kaambre, T., Bagur, R., Grichine, A., Usson, Y., Varikmaa, M., ... Saks, V. (2015). Modular organization of cardiac energy metabolism: energy conversion, transfer and feedback regulation. Acta Physiologica, 213(1), 84-106. https://doi.org/10.1111/apha.12287

Modular organization of cardiac energy metabolism : energy conversion, transfer and feedback regulation. / Guzun, R.; Kaambre, T.; Bagur, R.; Grichine, A.; Usson, Y.; Varikmaa, M.; Anmann, T.; Tepp, K.; Timohhina, N.; Shevchuk, I.; Chekulayev, V.; Boucher, F.; Dos Santos, P.; Schlattner, U.; Wallimann, T.; Kuznetsov, A. V.; Dzeja, Petras P; Aliev, M.; Saks, V.

In: Acta Physiologica, Vol. 213, No. 1, 01.01.2015, p. 84-106.

Research output: Contribution to journalArticle

Guzun, R, Kaambre, T, Bagur, R, Grichine, A, Usson, Y, Varikmaa, M, Anmann, T, Tepp, K, Timohhina, N, Shevchuk, I, Chekulayev, V, Boucher, F, Dos Santos, P, Schlattner, U, Wallimann, T, Kuznetsov, AV, Dzeja, PP, Aliev, M & Saks, V 2015, 'Modular organization of cardiac energy metabolism: energy conversion, transfer and feedback regulation', Acta Physiologica, vol. 213, no. 1, pp. 84-106. https://doi.org/10.1111/apha.12287
Guzun, R. ; Kaambre, T. ; Bagur, R. ; Grichine, A. ; Usson, Y. ; Varikmaa, M. ; Anmann, T. ; Tepp, K. ; Timohhina, N. ; Shevchuk, I. ; Chekulayev, V. ; Boucher, F. ; Dos Santos, P. ; Schlattner, U. ; Wallimann, T. ; Kuznetsov, A. V. ; Dzeja, Petras P ; Aliev, M. ; Saks, V. / Modular organization of cardiac energy metabolism : energy conversion, transfer and feedback regulation. In: Acta Physiologica. 2015 ; Vol. 213, No. 1. pp. 84-106.
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