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Journal of Comparative Physiology B

, Volume 187, Issue 1, pp 103–116 | Cite as

Metabolic compartmentation in rainbow trout cardiomyocytes: coupling of hexokinase but not creatine kinase to mitochondrial respiration

  • Niina Karro
  • Mervi Sepp
  • Svetlana Jugai
  • Martin Laasmaa
  • Marko Vendelin
  • Rikke BirkedalEmail author
Original Paper

Abstract

Rainbow trout (Oncorhynchus mykiss) cardiomyocytes have a simple morphology with fewer membrane structures such as sarcoplasmic reticulum and t-tubules penetrating the cytosol. Despite this, intracellular ADP diffusion is restricted. Intriguingly, although diffusion is restricted, trout cardiomyocytes seem to lack the coupling between mitochondrial creatine kinase (CK) and respiration. Our aim was to study the distribution of diffusion restrictions in permeabilized trout cardiomyocytes and verify the role of CK. We found a high activity of hexokinase (HK), which led us to reassess the situation in trout cardiomyocytes. We show that diffusion restrictions are more prominent than previously thought. In the presence of a competitive ADP-trapping system, ADP produced by HK, but not CK, was channeled to the mitochondria. In agreement with this, we found no positively charged mitochondrial CK in trout heart homogenate. The results were best fit by a simple mathematical model suggesting that trout cardiomyocytes lack a functional coupling between ATPases and pyruvate kinase. The model simulations show that diffusion is restricted to almost the same extent in the cytosol and by the outer mitochondrial membrane. Furthermore, they confirm that HK, but not CK, is functionally coupled to respiration. In perspective, our results suggest that across a range of species, cardiomyocyte morphology and metabolism go hand in hand with cardiac performance, which is adapted to the circumstances. Mitochondrial CK is coupled to respiration in adult mammalian hearts, which are specialized to high, sustained performance. HK associates with mitochondria in hearts of trout and neonatal mammals, which are more hypoxia-tolerant.

Keywords

ADP diffusion restriction Creatine kinase Heart Hexokinase Metabolic compartmentation Rainbow trout 

Notes

Acknowledgments

We wish to acknowledge Ms. Merle Mandel for her assistance with the spectrophotometric recordings. We also thank Dr. Erkki Truve and Dr. Cecilia Sarmiento for letting us use their gel electrophoresis system. This study was funded by the Estonian Science Foundation (Grant No. ETF8041), the European Union through the European Regional Development Fund (CENS Estonian Center of Excellence in Research) and the Estonian Research Council (IUT 33-7).

Supplementary material

360_2016_1025_MOESM1_ESM.pdf (147 kb)
Supplementary material 1 (PDF 147 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Niina Karro
    • 1
  • Mervi Sepp
    • 1
  • Svetlana Jugai
    • 1
  • Martin Laasmaa
    • 1
  • Marko Vendelin
    • 1
  • Rikke Birkedal
    • 1
    Email author
  1. 1.Institute of CyberneticsTallinn University of TechnologyTallinnEstonia

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