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We tested the hypothesis that physical linkage of SR and mitochondria via Mfn2 is essential for IP 3 R-mediated signal transduction to mitochondria to maintain ATP levels in cardiac myocytes under physiological conditions i.

In our previous study Seidlmayer et al. In contrast, under basal conditions, beta-adrenergic stimulation with ISO was not able to induce measurable ATP production.

Furthermore, another study demonstrated that beta-adrenergic stimulation with ISO induced only a transient MCU-dependent increase in oxygen consumption, suggesting that MCU only plays a role in acute matching of the mitochondrial energy output with increase in cardiac metabolic demand Kwong et al.

The disruption of Mfn2-mediated intact ER-mitochondrial contacts exists in conditions of heart failure induced by transverse aortic constriction TAC , which is associated with a decreased excitability and force generation in cardiac myocytes Goh et al.

ET-1 levels are typically increased in chronic stress as in the setting of congestive heart failure CHF Wei et al.

To determine if this increase in the ET-1 axis is pathologic, a mouse model was developed to conditionally overexpress ET-1 in the myocardium that led to nearly fold increase in ET-1 concentration in the heart, without any significant increase in circulating ET-1 levels Yang et al.

Mice with elevated cardiac ET-1 expression presented with severe heart inflammation, hypertrophy leading to dilated cardiomyopathy, CHF, and death within 5 weeks of induction.

These observations suggest that while fold elevation in ET-1 levels in cardiac myocytes is clearly pathological, basal levels of ET-1 are required for maintaining normal physiological function in cardiac myocytes.

Indeed, myocardial ET-1 depicts beneficial effects depending on the physiological situation. In the myocardium, ET-1 prevents excessive apoptosis after cardiac overload induced by aortic banding Zhao et al.

It has been reported that ET-1 prevents the early phase of doxorubicin-induced cytotoxicity via the upregulation of the antioxidant manganese superoxide dismutase through the ET A receptor in cultured cardiomyocytes Suzuki and Miyauchi, Preconditioning infusion of ET-1 can reduce infarct size in rats subjected to ischemia-reperfusion Gourine et al.

The transgenic expression of ET-1 in mice lacking a functional gene for eNOS restores diastolic function presumably through modulation of oxidative stress and a change of metabolic substrate from fatty acid oxidation toward enhanced glycolysis Vignon-Zellweger et al.

The significance of a physical linkage of SR and mitochondria in cardiac myocytes is still debated. As shown by our group before Seidlmayer et al.

Here, we were able to demonstrate that this metabolic feedback is severely disturbed in Mfn2-deficient mice.

This finding is supported by several studies providing evidence for not only structural differences of IFM Fawcett and McNutt, ; Shimada et al.

Since ET-1 has a positive inotropic effect and activates pathological gene transcription in the nucleus, a preferential effect of ET-1 on IFM and PNM is in agreement with these findings.

Interestingly, the basal mitochondrial membrane potential measured with TMRM was not different between the two genotypes, which is in accordance with the results of Chen et al.

Taken together, these results indicate a crucial role of physical tethering of SR and mitochondria by Mfn2 for adaptation of energy production to chronic stress.

These data suggest that tethering between SR and mitochondria is heterogeneous within ventricular myocytes to support the privileged SR-mitochondrial communication between IR3 receptors and mRyR1.

Our study demonstrates that in ventricular myocytes, basal ET-1 signaling is required for maintaining normal cardiac function and bioenergetics Figure 6.

These findings could explain the impaired cardiac function observed in aged mice and young mice following TAC Goh et al. LS and ED designed the study and wrote the manuscript.

BG and SF provided financial support. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

National Center for Biotechnology Information , U. Journal List Front Physiol v. Front Physiol. Published online Jul Lea K. Dorn, II.

Elena N. Author information Article notes Copyright and License information Disclaimer. Seidlmayer, ed. Dedkova, ude. This article was submitted to Mitochondrial Research, a section of the journal Frontiers in Physiology.

Received Nov 4; Accepted May The use, distribution or reproduction in other forums is permitted, provided the original author s and the copyright owner s are credited and that the original publication in this journal is cited, in accordance with accepted academic practice.

No use, distribution or reproduction is permitted which does not comply with these terms. This article has been cited by other articles in PMC.

PDF K. Introduction Heart failure HF is one of the most common chronic conditions associated with aging. Cell Isolation Adult left ventricular myocytes were isolated from to week-old Mfn2 KO mice and their healthy littermates.

Immunoblot Analysis Left ventricular tissue was homogenized in ice-cold lysis buffer 50 mM Tris pH 7. Statistics The data are normalized to untreated control and background corrected.

Open in a separate window. Figure 1. Figure 2. Figure 3. Figure 4. Figure 5. Figure 6. Conclusions Our study demonstrates that in ventricular myocytes, basal ET-1 signaling is required for maintaining normal cardiac function and bioenergetics Figure 6.

Conflict of Interest Statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Footnotes Funding. References Balaban R. Acta , — Type 1 ryanodine receptor in cardiac mitochondria: transducer of excitation-metabolism coupling.

Acta , 1—

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References Balaban R. Acta , — Type 1 ryanodine receptor in cardiac mitochondria: transducer of excitation-metabolism coupling. Acta , 1— Cell , — Mitochondrial fusion is essential for organelle function and cardiac homeostasis.

OPA1 requires mitofusin 1 to promote mitochondrial fusion. USA , — Structural and functional features and significance of the physical linkage between ER and mitochondria.

Cell Biol. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature , — Cell Death Differ. Cell Calcium 44 , 77— Measuring mitochondrial function in intact cardiac myocytes.

Mitochondria-mediated cardioprotection by trimetazidine in rabbit heart failure. SR and mitochondria: calcium cross-talk between kissing cousins.

The ultrastructure of the cat myocardium. Ventricular papillary muscle. Mitofusin 2 ablation increases endoplasmic reticulum-mitochondria coupling.

USA , E—E Calcium binding and translocation by the voltage-dependent anion channel: a possible regulatory mechanism in mitochondrial function.

Impaired mitochondrial network excitability in failing Guinea-pig cardiomyocytes. Endothelin-1 regulates cardiac sympathetic innervation in the rodent heart by controlling nerve growth factor expression.

Intracellular signaling pathways for norepinephrine- and endothelinmediated regulation of myocardial cell apoptosis.

Molecular and functional identification of a mitochondrial ryanodine receptor in neurons. Novel molecular mechanism of increased myocardial endothelin-1 expression in the failing heart involving the transcriptional factor hypoxia-inducible factor-1alpha induced for impaired myocardial energy metabolism.

Circulation , — Impaired development of the thyroid and thymus in endothelin-1 knockout mice. Aortic arch malformations and ventricular septal defect in mice deficient in endothelin Elevated blood pressure and craniofacial abnormalities in mice deficient in endothelin The mitochondrial calcium uniporter selectively matches metabolic output to acute contractile stress in the heart.

Cell Rep. Lifetime risk for developing congestive heart failure: the Framingham heart study. On the existence of two populations of mitochondria in a single organ.

Respiration, calcium transport and enzyme activities. Calcium uptake by two preparations of mitochondria from heart.

Subsarcolemmal mitochondria and capillarization of soleus muscle fibers in young rats subjected to an endurance training.

A morphometric study of semithin sections. Cell Tissue Res. Critical reappraisal confirms that mitofusin 2 is an endoplasmic reticulum-mitochondria tether.

Heart J. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle.

The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter.

Coordinated upregulation of the cardiac endothelin system in a rat model of heart failure. Functional effects of endothelin and regulation of endothelin receptors in isolated human nonfailing and failing myocardium.

Circulation 99 , — Inositol 1,4,5-trisphosphate supports the arrhythmogenic action of endothelin-1 on ventricular cardiac myocytes. Cell Sci.

Mitochondrial dysfunction in heart failure. Heart Fail. Mitofusins, from mitochondria to metabolism. Cell 61 , — Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies.

Morphological studies of different mitochondrial populations in monkey myocardial cells. Uncovering the role of VDAC in the regulation of cell life and death.

VDAC1 at the crossroads of cell metabolism, apoptosis and cell stress. Cell Stress 1 , 11— A novel pharmacological action of ET-1 to prevent the cytotoxicity of doxorubicin in cardiomyocytes.

Calcium signal transmission between ryanodine receptors and mitochondria. Cardiac-specific conditional knockout of the kDa mitochondrial translocator protein protects from pressure overload induced heart failure.

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