Analysis of mitochondrial 3D-deformation in cardiomyocytes during active contraction reveals passive structural anisotropy of orthogonal short axes

Yael Yaniv, Magdalena Juhaszova, Su Wang, Kenneth W. Fishbein, Dmitry B. Zorov, Steven J. Sollott

Research output: Contribution to journalArticle

Abstract

The cardiomyocyte cytoskeleton, composed of rigid and elastic elements, maintains the isolated cell in an elongated cylindrical shape with an elliptical cross-section, even during contraction-relaxation cycles. Cardiomyocyte mitochondria are micron-sized, fluid-filled passive spheres distributed throughout the cell in a crystal-like lattice, arranged in pairs sandwiched between the sarcomere contractile machinery, both longitudinally and radially. Their shape represents the extant 3-dimensional (3D) force-balance. We developed a novel method to examine mitochondrial 3D-deformation in response to contraction and relaxation to understand how dynamic forces are balanced inside cardiomyocytes. The variation in transmitted light intensity induced by the periodic lattice of myofilaments alternating with mitochondrial rows can be analyzed by Fourier transformation along a given cardiomyocyte axis to measure mitochondrial deformation along that axis. This technique enables precise detection of changes in dimension of ~1% in ~1 μm (long-axis) structures with 8 ms time-resolution. During active contraction (1 Hz stimulation), mitochondria deform along the length- and width-axes of the cell with similar deformation kinetics in both sarcomere and mitochondrial structures. However, significant deformation anisotropy (without hysteresis) was observed between the orthogonal short-axes (i.e., width and depth) of mitochondria during electrical stimulation. The same degree of deformation anisotropy was also found between the myocyte orthogonal short-axes during electrical stimulation. Therefore, the deformation of the mitochondria reflects the overall deformation of the cell, and the apparent stiffness and stress/strain characteristics of the cytoskeleton differ appreciably between the two cardiomyocyte orthogonal short-axes. This method may be applied to obtaining a better understanding of the dynamic force-balance inside cardiomyocytes and of changes in the spatial stiffness characteristics of the cytoskeleton that may accompany aging or pathological conditions.

Original languageEnglish (US)
Article numbere21985
JournalPLoS One
Volume6
Issue number7
DOIs
StatePublished - 2011
Externally publishedYes

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Anisotropy
Cardiac Myocytes
Mitochondria
Cytoskeleton
mitochondria
cytoskeleton
Sarcomeres
sarcomeres
Electric Stimulation
Stiffness
cells
Myofibrils
myofibrils
hysteresis
Muscle Cells
cardiomyocytes
Crystal lattices
myocytes
Machinery
crystals

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Analysis of mitochondrial 3D-deformation in cardiomyocytes during active contraction reveals passive structural anisotropy of orthogonal short axes. / Yaniv, Yael; Juhaszova, Magdalena; Wang, Su; Fishbein, Kenneth W.; Zorov, Dmitry B.; Sollott, Steven J.

In: PLoS One, Vol. 6, No. 7, e21985, 2011.

Research output: Contribution to journalArticle

Yaniv, Yael ; Juhaszova, Magdalena ; Wang, Su ; Fishbein, Kenneth W. ; Zorov, Dmitry B. ; Sollott, Steven J. / Analysis of mitochondrial 3D-deformation in cardiomyocytes during active contraction reveals passive structural anisotropy of orthogonal short axes. In: PLoS One. 2011 ; Vol. 6, No. 7.
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