Atomic force and electron microscopic-based study of sarcolemmal surface of living cardiomyocytes unveils unexpected mitochondrial shift in heart failure

Dague, Étienne; Genet, Gaël; Lachaize, Véronique; Guilbeau‐Frugier, Céline; Fauconnier, Jérémy; Mias, Céline; Payré, Bruno; Chopinet, Louise; Alsteens, David; Kasas, Sandor; Severac, Childérick; Thireau, Jérôme; Heymes, Christophe; Honton, Benjamin; Lacampagne, Alain; Pathak, Atul; Sénard, Jean-Michel; Galès, Céline

doi:10.1016/j.yjmcc.2014.05.006

Cited by 30 publications

(62 citation statements)

References 40 publications

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“…Isolated SSM mitochondria from male Sprague Dawley rats also exhibit lower oxidative phosphorylation and reduced NADH oxidation after a 40 minutes hypoxia/reoxygenation insult thereby indicating the unique properties of mitochondrial subtypes 21 . Likewise and in partial agreement with our data, myocardial infarction via left coronary artery ligation of male Sprague Dawley rats has been shown to specifically alter the topography 29 . In parallel, IPC has been shown to induce its cardioprotective effects by increasing the S-nitrosylation, promoting the complex I respiration and preserving the activity of electron transport chain enzymes of SSM mitochondria 30,31 .…”

Section: Resultssupporting

confidence: 91%

Unique morphological characteristics of mitochondrial subtypes in the heart: the effect of ischemia and ischemic preconditioning

Kalkhoran

Munro

Fan

et al. 2017

Discoveries (Craiova)

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Rationale Three subsets of mitochondria have been described in adult cardiomyocytes - intermyofibrillar (IMF), subsarcolemmal (SSM), and perinuclear (PN). They have been shown to differ in physiology, but whether they also vary in morphological characteristics is unknown. Ischemic preconditioning (IPC) is known to prevent mitochondrial dysfunction induced by acute myocardial ischemia/reperfusion injury (IRI), but whether IPC can also modulate mitochondrial morphology is not known. Aims Morphological characteristics of three different subsets of adult cardiac mitochondria along with the effect of ischemia and IPC on mitochondrial morphology will be investigated. Methods Mouse hearts were subjected to the following treatments (N=6 for each group): stabilization only, IPC (3x5 min cycles of global ischemia and reperfusion), ischemia only (20 min global ischemia); and IPC and ischemia. Hearts were then processed for electron microscopy and mitochondrial morphology was assessed subsequently. Results In adult cardiomyocytes, IMF mitochondria were found to be more elongated and less spherical than PN and SSM mitochondria. PN mitochondria were smaller in size when compared to the other two subsets. SSM mitochondria had similar area to IMF mitochondria but their sphericity measures were similar to PN mitochondria. Ischemia was shown to increase the sphericity parameters of all 3 subsets of mitochondria; reduce the length of IMF mitochondria, and increase the size of PN mitochondria. IPC had no effect on mitochondrial morphology either at baseline or after ischemia. Conclusion The three subsets of mitochondria in the adult heart are morphologically different. IPC does not appear to modulate mitochondrial morphology in adult cardiomyocytes.

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Section: Resultssupporting

confidence: 91%

Unique morphological characteristics of mitochondrial subtypes in the heart: the effect of ischemia and ischemic preconditioning

Kalkhoran

Munro

Fan

et al. 2017

Discoveries (Craiova)

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“…In the field of cardiology, it is also known that erythrocytes interactions with fibrogen, as probed by AFM, are modified in ischemia and that red blood cells stiffness is altered 13 . As for the cardiology area for example cardiomyocytes are difficult to handle, and then works have reported the characterization of 1 to 30 cardiomyocytes [14][15][16][17][18][19][20] in about 6-8 h. which is a too small amount of cells to make a statistically relevant information in the context of human diseases and therefore will never be reliable enough for clinicians. Mechanical properties have also help understanding the effects of antimicrobial molecules on bacteria or yeast cell's walls 21 .…”

Section: Introductionmentioning

confidence: 99%

Beyond the paradigm of nanomechanical measurements on cells using AFM: an automated methodology to rapidly analyse thousands of cells

et al. 2020

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“…Recently, sarcolemmal surface topography and physical properties were directly examined using Atomic Force Microscopy in living cardiomyocytes, from healthy and failing mouse hearts [56] . The presence of highly organized crests and hollows along myofilaments in isolated healthy cardiomyocytes was observed.…”

Section: Nanomechanical Change In Living Cardiomyocytes In Heart Failmentioning

confidence: 99%

Intrinsic nanomechanical changes in live diabetic cardiomyocytes

Benech

Benech²,

Zambrana³

et al. 2015

Cardiovasc Regen Med

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Patients with diabetes develop a cardiomyopathy that is independent of both coronary artery disease and hypertension and contributes to mortality and morbidity caused by diabetes. The mechanisms underlying the development of diabetic cardiomyopathy are poorly understood. Several reports showed that an early manifestation of diabetic myocardial dysfunction is an increased diastolic left ventricular (LV) stiffness. This increase is usually attributed to myocardial fibrosis or to myocardial deposition of advanced glycation end products. Alteration of the stiffness (resting tension) of the diabetic cardiomyocyte was also proposed to be an important factor contributing to increased LV stiffness. Some of these data were obtained from isolated cardiomyocytes from human frozen biopsy samples that had been thawed, mechanically disrupted, and incubated with Triton X-100, disrupting sarcolemmal and sarcoplasmic membranes. We therefore determined the stiffness of live isolated cardiomyocytes from control and streptozotocin-treated mice using atomic force microscopy (AFM) nanoindentation. We show that 3 months of type 1 diabetes provoked fragmentation and disorder of myocardial fibers, interstitial collagen deposition, reduction in SERCA2a calcium pump expression and changes in F-actin organization. Moreover, we show that live isolated diabetic cardiomyocytes are stiffer than control cardiomyocytes when tested in Tyrode buffer with different ionic compositions. Hence, it is very likely that intrinsic mechanical changes of cardiomyocytes are an important factor in increasing myocardial stiffness in vivo.

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Atomic force and electron microscopic-based study of sarcolemmal surface of living cardiomyocytes unveils unexpected mitochondrial shift in heart failure

Cited by 30 publications

References 40 publications

Unique morphological characteristics of mitochondrial subtypes in the heart: the effect of ischemia and ischemic preconditioning

Unique morphological characteristics of mitochondrial subtypes in the heart: the effect of ischemia and ischemic preconditioning

Beyond the paradigm of nanomechanical measurements on cells using AFM: an automated methodology to rapidly analyse thousands of cells

Intrinsic nanomechanical changes in live diabetic cardiomyocytes

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