Formation of highly organized intracellular structure and energy metabolism in cardiac muscle cells during postnatal development of rat heart.
Adult cardiomyocytes have highly organized intracellular structure and energy metabolism whose formation during postnatal development is still largely unclear. Our previous results together with the data from the literature suggest that cytoskeletal proteins, particularly βII-tubulin, are involved in the formation of complexes between mitochondria and energy consumption sites. The aim of this study was to examine the arrangement of intracellular architecture parallel to the alterations in regulation of mitochondrial respiration in rat cardiomyocytes during postnatal development, from 1 day to 6 months. Respirometric measurements were performed to study the developmental alterations of mitochondrial function. Changes in the mitochondrial arrangement and cytoarchitecture of βII- and αIV-tubulin were examined by confocal microscopy. Our results show that functional maturation of oxidative phosphorylation in mitochondria is completed much earlier than efficient feedback regulation is established between mitochondria and ATPases via creatine kinase system. These changes are accompanied by significant remodeling of regular intermyofibrillar mitochondrial arrays aligned along the bundles of βII-tubulin. Additionally, we demonstrate that formation of regular arrangement of mitochondria is not sufficient per se to provide adult-like efficiency in metabolic feed-back regulation, but organized tubulin networks and reduction in mitochondrial outer membrane permeability for ADP are necessary as well. In conclusion, cardiomyocytes in rat heart become mature on the level of intracellular architecture and energy metabolism at the age of 3 months.
Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia. Electronic address: tiia.anmann@kbfi.ee.
Tiia
T
Anmann
Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia; Faculty of Science, Department of Chemistry, Tallinn University of Technology, Tallinn, Estonia.
Minna
M
Varikmaa
Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia.
Natalja
N
Timohhina
Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia.
Kersti
K
Tepp
Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia.
Igor
I
Shevchuk
Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia.
Vladimir
V
Chekulayev
Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia; Laboratory of Fundamental and Applied Bioenergetics, Joseph Fourier University, Grenoble, France.
Valdur
V
Saks
Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia; Institute of Mathematics and Natural Sciences, Tallinn University, Tallinn, Estonia.
Tuuli
T
Kaambre
D000244:Adenosine Diphosphate / Q000378:metabolism; D000818:Animals; D003599:Cytoskeleton; D004622:Embryo, Mammalian / Q000648:ultrastructure; D047108:Embryonic Development / Q000235:genetics*; D004734:Energy Metabolism; D006801:Humans; D008929:Mitochondria, Heart / Q000378:metabolism / Q000648:ultrastructure; D051336:Mitochondrial Membranes / Q000378:metabolism / Q000648:ultrastructure; D009206:Myocardium / Q000378:metabolism / Q000648:ultrastructure; D032383:Myocytes, Cardiac / Q000378:metabolism / Q000648:ultrastructure*; D051381:Rats; D014404:Tubulin / Q000737:chemistry / Q000378:metabolism*
D014404:Tubulin; D000244:Adenosine Diphosphate
Bioenergetics; Cardiomyocyte; Development; Intracellular architecture; Mitochondria; Tubulin