Role of mitochondria–cytoskeleton interactions in respiration regulation and mitochondrial organization in striated muscles

Varikmaa, Minna; Bagur, Rafaela; Käämbre, Tuuli; Grichine, Alexeï; Timohhina, Natalja; Tepp, Kersti; Shevchuk, Igor; Chekulayev, Vladimir; Metsis, Madis; Boucher, François; Saks, Valdur; Kuznetsov, Andrey V.; Guzun, Rita

doi:10.1016/j.bbabio.2013.10.011

Cited by 43 publications

(59 citation statements)

References 68 publications

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“…Further, tethering to tubulin, actin [64], and intermediate filaments [65] is required for mitochondrion cristae to acquire their characteristics invaginated morphology. Tubulin tethering to mitochondria has been shown to play both structural and functional roles in striated muscle homeostasis [66] and disease [10]. Specifically, by physically and chemically interacting with the mitochondrial outer membrane, tubulin modulates the function of the permeability transition pore [67] and of voltage-dependent anion channels [68].…”

Section: Intracellular Energetic Units In Healthy Heartsmentioning

confidence: 99%

Mechanotransduction and Metabolism in Cardiomyocyte Microdomains

Pasqualini

Nesmith

Horton

et al. 2016

BioMed Research International

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Efficient contractions of the left ventricle are ensured by the continuous transfer of adenosine triphosphate (ATP) from energy production sites, the mitochondria, to energy utilization sites, such as ionic pumps and the force-generating sarcomeres. To minimize the impact of intracellular ATP trafficking, sarcomeres and mitochondria are closely packed together and in proximity with other ultrastructures involved in excitation-contraction coupling, such as t-tubules and sarcoplasmic reticulum junctions. This complex microdomain has been referred to as the intracellular energetic unit. Here, we review the literature in support of the notion that cardiac homeostasis and disease are emergent properties of the hierarchical organization of these units. Specifically, we will focus on pathological alterations of this microdomain that result in cardiac diseases through energy imbalance and posttranslational modifications of the cytoskeletal proteins involved in mechanosensing and transduction.

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Section: Intracellular Energetic Units In Healthy Heartsmentioning

confidence: 99%

Mechanotransduction and Metabolism in Cardiomyocyte Microdomains

Pasqualini

Nesmith

Horton

et al. 2016

BioMed Research International

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“…More specifically, because we did not have significant alterations due to DHA on isolated mitochondrial function but major changes on permeabilized myofibers, we can conclude that DHA may exert its effects through the mitochondrial environment. Among hypothetic mechanisms proposed to explain such an importance, components of the cytoskeleton, such as tubulin isoforms, have been suggested to play a role in the regulation of the mitochondrial metabolism (60). Further experiments are needed to precisely measure that contribution and the potential modulating action of polyunsaturated fatty acids.…”

Section: E219mentioning

confidence: 99%

A 9-wk docosahexaenoic acid-enriched supplementation improves endurance exercise capacity and skeletal muscle mitochondrial function in adult rats

Guen

Chaté

Hininger‐Favier

et al. 2016

American Journal of Physiology-Endocrinology and Metabolism

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Among the causes, modifications of the mitochondrial function could be of major importance. Polyunsaturated fatty (-3) acids have been shown to play a role in intracellular functions. We hypothesize that docosahexaenoic acid (DHA) supplementation could improve muscle mitochondrial function that could contribute to limit the early consequences of aging on adult muscle. Twelve-month-old male Wistar rats were fed a low-polyunsaturated fat diet and were given DHA (DHA group) or placebo (control group) for 9 wk. Rats from the DHA group showed a higher endurance capacity (ϩ56%, P Ͻ 0.05) compared with control animals. Permeabilized myofibers from soleus muscle showed higher O2 consumptions (P Ͻ 0.05) in the DHA group compared with the control group, with glutamate-malate as substrates, both in basal conditions (i.e., state 2) and under maximal conditions (i.e., state 3, using ADP), along with a higher apparent Km for ADP (P Ͻ 0.05). Calcium retention capacity of isolated mitochondria was lower in DHA group compared with the control group (P Ͻ 0.05). Phospho-AMPK/AMPK ratio and PPAR␦ mRNA content were higher in the DHA group compared with the control group (P Ͻ 0.05). Results showed that DHA enhanced endurance capacity in adult animals, a beneficial effect potentially resulting from improvement in mitochondrial function, as suggested by our results on permeabilized fibers. DHA supplementation could be of potential interest for the muscle function in adults and for fighting the decline in exercise tolerance with age that could imply energy-sensing pathway, as suggested by changes in phospho-AMPK/AMPK ratio. polyunsaturated fatty acids; isolated mitochondria; permeabilized myofibers; muscle bioenergetics AGING IS ASSOCIATED WITH A PROGRESSIVE DECREASE in muscle mass and alterations in muscle function leading to reduced physical abilities, exercise performance and quality of life, and ultimately disabilities (21,26,36). Among the causes of such sarcopenia, inadequate protein synthesis matching protein degradations is of major importance (4, 12). Also, changes in metabolism could be part of the muscle mass decrease with age.

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“…Additionally, the low apparent ADP-affinity is specific for oxidative muscles (Kuznetsov et al, 1996; Ventura-Clapier et al, 1998). The difference between muscles might be explained by distinct expression of tubulin that regulate VDAC gating (Varikmaa et al, 2014). Another explanation involves SR-mitochondria interaction that seems to be more prominent in muscles that are rich in mitochondria (Franzini-Armstrong, 2007).…”

Section: Energetic Compartments Affect Energetic Communication—but How?mentioning

confidence: 99%

The location of energetic compartments affects energetic communication in cardiomyocytes

2014

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The heart relies on accurate regulation of mitochondrial energy supply to match energy demand. The main regulators are Ca2+ and feedback of ADP and Pi. Regulation via feedback has intrigued for decades. First, the heart exhibits a remarkable metabolic stability. Second, diffusion of ADP and other molecules is restricted specifically in heart and red muscle, where a fast feedback is needed the most. To explain the regulation by feedback, compartmentalization must be taken into account. Experiments and theoretical approaches suggest that cardiomyocyte energetic compartmentalization is elaborate with barriers obstructing diffusion in the cytosol and at the level of the mitochondrial outer membrane (MOM). A recent study suggests the barriers are organized in a lattice with dimensions in agreement with those of intracellular structures. Here, we discuss the possible location of these barriers. The more plausible scenario includes a barrier at the level of MOM. Much research has focused on how the permeability of MOM itself is regulated, and the importance of the creatine kinase system to facilitate energetic communication. We hypothesize that at least part of the diffusion restriction at the MOM level is not by MOM itself, but due to the close physical association between the sarcoplasmic reticulum (SR) and mitochondria. This will explain why animals with a disabled creatine kinase system exhibit rather mild phenotype modifications. Mitochondria are hubs of energetics, but also ROS production and signaling. The close association between SR and mitochondria may form a diffusion barrier to ADP added outside a permeabilized cardiomyocyte. But in vivo, it is the structural basis for the mitochondrial-SR coupling that is crucial for the regulation of mitochondrial Ca2+-transients to regulate energetics, and for avoiding Ca2+-overload and irreversible opening of the mitochondrial permeability transition pore.

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Role of mitochondria–cytoskeleton interactions in respiration regulation and mitochondrial organization in striated muscles

Cited by 43 publications

References 68 publications

Mechanotransduction and Metabolism in Cardiomyocyte Microdomains

Mechanotransduction and Metabolism in Cardiomyocyte Microdomains

A 9-wk docosahexaenoic acid-enriched supplementation improves endurance exercise capacity and skeletal muscle mitochondrial function in adult rats

The location of energetic compartments affects energetic communication in cardiomyocytes

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