Abstract
ABSTRACTCardiomyocytes both cause and experience continual cyclic deformation. The exact effects of this deformation on the properties of intracellular organelles are not well characterized, although they are likely to be relevant for cardiomyocyte responses to active and passive changes in their mechanical environment. In the present study we provide three‐dimensional ultrastructural evidence for mechanically induced mitochondrial deformation in rabbit ventricular cardiomyocytes over a range of sarcomere lengths representing myocardial tissue stretch, an unloaded “slack” state, and contracture. We also show structural indications for interaction of mitochondria with one another, as well as with other intracellular elements such as microtubules, sarcoplasmic reticulum and T‐tubules. The data presented here help to contextualize recent reports on the mechanosensitivity and cell‐wide connectivity of the mitochondrial network and provide a structural framework that may aide interpretation of mechanically‐regulated molecular signaling in cardiac cells. Anat Rec, 302:146–152, 2019. © 2018 The Authors. The Anatomical Record published by Wiley Periodicals, Inc. on behalf of American Association of Anatomists.
Highlights
As the heart beats, cardiomyocytes undergo significant phasic deformations with up to Æ10% changes in length, compared to their resting state
Organelles are influenced by deformations resulting from passive cardiomyocyte stretch and active shortening, a process aided by cytoskeletal filaments that bear and transmit mechanical loads throughout the cell (BartolakSuki et al, 2017; Ingber, 2008; Robison et al, 2016)
Mitochondria become elongated with their major axis aligned near-parallel to the contractile filament bundles (Fig. 1D)
Summary
Cardiomyocytes undergo significant phasic deformations with up to Æ10% changes in length, compared to their resting state. Cardiomyocytes are enclosed by a deformable but nondistensible lipid bilayer that contains numerous surface folds and invaginations that unfold during strain (Kohl et al, 2003). This “spare membrane” addresses the otherwise problematic change in surface-tovolume ratio that would occur upon stretching an isovolumic “cylinder” (McNary et al, 2012; Pfeiffer et al, 2014). As shown for the surface sarcolemma (Kohl et al, 2003; Pfeiffer et al, 2014), some intracellular membranous structures, such as T-tubules, contain “spare membrane” in the shape of caveolae (Burton et al, 2017)
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