A unique micromechanocalorimeter for simultaneous measurement of heat rate and force production of cardiac trabeculae carneae

Han, June‐Chiew; Taberner, Andrew J.; Kirton, Robert; Nielsen, Poul M. F.; Smith, Nicholas P.; Loiselle, Denis S.

doi:10.1152/japplphysiol.00549.2009

Cited by 38 publications

(43 citation statements)

References 25 publications

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“…The micromechanocalorimeter was capable of a noise-equivalent temperature of 4.1 K/ ͙ Hz and a noise-equivalent power of 37.1 nW/ ͙ Hz at 22°C (37), but our thermoelectric module-based calorimeter, at 22°C, has resolutions of 0.4 K/ ͙ Hz and 2.6 nW/ ͙ Hz, respectively. These values are an order of magnitude better than any previous calorimeter systems (8,12,16,22,27,33,39).…”

Section: Discussionmentioning

confidence: 66%

“…In the 1990s, Schramm et al (35) and Loiselle et al (29) used the thermopile-based calorimeter of Daut and Elzinga (7) to measure the heat output of trabeculae at 37°C, in the complete absence of force measurement. About two decades later, Han et al (16) constructed a thermopile-based micromechanocalorimeter that was capable of the first simultaneous measurements of force and heat output of isolated trabeculae. However, comparatively low-resolution temperature sensors were used and the inclusion of a mechanical testing apparatus prevented the use of a thermal control system similar to that of Daut and Elzinga.…”

Section: Discussionmentioning

confidence: 99%

“…The use of thermoelectric modules offers several advantages. First, it yields a 10-fold improvement in temperature resolution over our previous micromechanocalorimeter (16,37) and provides sufficiently low electrical and thermal noise to allow measurements of the extremely small heat output of trabeculae at 37°C, while retaining the ability to measure muscle force. Second, it is mechanically robust, which simplifies device construction and reduces the risk of damage to both the preparation and the instrument when mounting a trabecula.…”

Section: Discussionmentioning

confidence: 99%

“…We have overcome these limitations by constructing a temperature-controlled flow-through muscle calorimeter with exceptionally high thermal resolution. In contrast to previous muscle calorimeter designs (16,36,37), we have used solid-state thermoelectric modules as both temperature sensors and temperature controllers. …”

mentioning

confidence: 99%

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A high-resolution thermoelectric module-based calorimeter for measuring the energetics of isolated ventricular trabeculae at body temperature

Johnston

Han

Ruddy

et al. 2015

American Journal of Physiology-Heart and Circulatory Physiology

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Johnston CM, Han JC, Ruddy BP, Nielsen PM, Taberner AJ. A high-resolution thermoelectric module-based calorimeter for measuring the energetics of isolated ventricular trabeculae at body temperature. Am J Physiol Heart Circ Physiol 309: H318 -H324, 2015. First published May 22, 2015; doi:10.1152/ajpheart.00194.2015.-Isolated ventricular trabeculae are the most common experimental preparations used in the study of cardiac energetics. However, the experiments have been conducted at subphysiological temperatures. We have overcome this limitation by designing and constructing a novel calorimeter with sufficiently high thermal resolution for simultaneously measuring the heat output and force production of isolated, contracting, ventricular trabeculae at body temperature. This development was largely motivated by the need to better understand cardiac energetics by performing such measurements at body temperature to relate tissue performance to whole heart behavior in vivo. Our approach uses solid-state thermoelectric modules, tailored for both temperature sensing and temperature control. The thermoelectric modules have high sensitivity and low noise, which, when coupled with a multilevel temperature control system, enable an exceptionally high temperature resolution with a noise-equivalent power an order of magnitude greater than those of other existing muscle calorimeters. Our system allows us to rapidly and easily change the experimental temperature without disturbing the state of the muscle. Our calorimeter is useful in many experiments that explore the energetics of normal physiology as well as pathophysiology of cardiac muscle. muscle energetics; microcalorimetry; heat production NEW & NOTEWORTHY We have developed a new muscle calorimeter, which has enabled the first simultaneous measurements of the force and heat output of isolated, actively contracting, cardiac trabeculae at body temperature. This was achieved by the use of thermoelectric modules for high-resolution temperature sensing and precise temperature control.MEASUREMENTS OF THE ENERGETICS of cardiac muscle under controlled experimental conditions, and in particular at body temperature, enable better understanding of cardiac muscle function in health and disease. Studies of force production simultaneous with heat output of cardiac muscle require the use of isolated tissue preparations such as small papillary muscles (2-4, 12, 26, 34) or trabeculae carneae (17-21) as they are sufficiently small to avoid muscle anoxia (14). The use of these tissue preparations, which have approximately one-dimensional arrangements of myocytes, simplifies the interpretation of measurements. Although these tissue studies have improved our understanding of myocardial energetics, previous experiments have been performed only at subphysiological temperatures, typically 10°C below that of body temperature (3,5,10,11,13,23,25,26,28,30,31). One exception is the study by Widén (39), who made simultaneous force and heat measurements in mouse papillary muscles at body temperature. H...

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Section: Discussionmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

A high-resolution thermoelectric module-based calorimeter for measuring the energetics of isolated ventricular trabeculae at body temperature

Johnston

Han

Ruddy

et al. 2015

American Journal of Physiology-Heart and Circulatory Physiology

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“…The first version (Fig. 8) used thin-film infra-red thermopile sensors in "conduction mode" (64) and allowed the heat output of rat right-ventricular trabeculae undergoing fixed-end contractions to be made (65). Subsequent modifications to both hardware and software (132) achieved both truly isometric contractions as well as isotonic "workloop" contractions at various afterloads.…”

Section: Cardiac Muscle Myometrymentioning

confidence: 99%

Muscle heat: a window into the thermodynamics of a molecular machine

Loiselle

Johnston

Han

et al. 2016

American Journal of Physiology-Heart and Circulatory Physiology

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contraction of muscle is characterized by the development of force and movement (mechanics) together with the generation of heat (metabolism). Heat represents that component of the enthalpy of ATP hydrolysis that is not captured by the microscopic machinery of the cell for the performance of work. It arises from two conceptually and temporally distinct sources: initial metabolism and recovery metabolism. Initial metabolism comprises the hydrolysis of ATP and its rapid regeneration by hydrolysis of phosphocreatine (PCr) in the processes underlying excitation-contraction coupling and subsequent cross-bridge cycling and sliding of the contractile filaments. Recovery metabolism describes those process, both aerobic (mitochondrial) and anaerobic (cytoplasmic), that produce ATP, thereby allowing the regeneration of PCr from its hydrolysis products. An equivalent partitioning of muscle heat production is often invoked by muscle physiologists. In this formulation, total enthalpy expenditure is separated into external mechanical work (W) and heat (Q). Heat is again partitioned into three conceptually distinct components: basal, activation, and force dependent. In the following mini-review, we trace the development of these ideas in parallel with the development of measurement techniques for separating the various thermal components.Microcalorimetry; muscle heat production; myothermy; thermopiles MUSCLE IS A MOLECULAR machine. It operates isothermally, isobarically, and isovolumetrically. At the microscopic level, it directly converts the Free Energy component of the enthalpy of ATP hydrolysis into cyclic attachment and detachment of actomyosin cross bridges, together with transportation of ions up their electrochemical potential gradients. At the macroscopic level, two consequences result: the generation of force and the evolution of heat. Of these two entities, heat is by far the more difficult to quantify and to interpret. In this brief review, we trace the development of techniques to measure muscle heat production from the mid-19th century to the present, providing parallel commentary on the progressive understanding of muscle function. We give particular consideration to the development of techniques of separating the metabolic cost of cross-bridge cycling from the purely "overhead" cost of its activation.

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Mitochondrial Bioenergetics During Ischemia and Reperfusion

Consolini

Ragone

Bonazzola

et al. 2017

Advances in Experimental Medicine and Biology

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During ischemia and reperfusion (I/R) mitochondria suffer a deficiency to supply the cardiomyocyte with chemical energy, but also contribute to the cytosolic ionic alterations especially of Ca. Their free calcium concentration ([Ca]m) mainly depends on mitochondrial entrance through the uniporter (UCam) and extrusion in exchange with Na (mNCX) driven by the electrochemical gradient (ΔΨm). Cardiac energetic is frequently estimated by the oxygen consumption, which determines metabolism coupled to ATP production and to the maintaining of ΔΨm. Nevertheless, a better estimation of heart energy consumption is the total heat release associated to ATP hydrolysis, metabolism, and binding reactions, which is measurable either in the presence or the absence of oxygenation or perfusion. Consequently, a mechano-calorimetrical approach on isolated hearts gives a tool to evaluate muscle economy. The mitochondrial role during I/R depends on the injury degree. We investigated the role of the mitochondrial Ca transporters in the energetic of hearts stunned by a model of no-flow I/R in rat hearts. This chapter explores an integrated view of previous and new results which give evidences to the mitochondrial role in cardiac stunning by ischemia o hypoxia, and the influence of thyroid alterations and cardioprotective strategies, such as cardioplegic solutions (high K-low Ca, pyruvate) and the phytoestrogen genistein in both sex. Rat ventricles were perfused in a flow-calorimeter at either 30 °C or 37 °C to continuously measure the left ventricular pressure (LVP) and total heat rate (Ht). A pharmacological treatment was done before exposing to no-flow I and R. The post-ischemic contractile (PICR as %) and energetical (Ht) recovery and muscle economy (Eco: P/Ht) were determined during stunning. The functional interaction between mitochondria (Mit) and sarcoplasmic reticulum (SR) was evaluated with selective mitochondrial inhibitors in hearts reperfused with Krebs-10 mM caffeine-36 mM Na. The caffeine induced contracture (CIC) was due to SR Ca release, while relaxation mainly depends on mitochondrial Ca uptake since neither SL-NCX nor SERCA are functional under this media. The ratio of area-under-curves over ischemic values (AUC-ΔHt/AUC-ΔLVP) estimates the energetical consumption (EC) to maintain CIC. Relaxation of CIC was accelerated by inhibition of mNCX or by adding the aerobic substrate pyruvate, while both increased EC. Contrarily, relaxation was slowed by cardioplegia (high K-low Ca Krebs) and by inhibition of UCam. Thus, Mit regulate the cytosolic [Ca] and SR Ca content. Both, hyperthyroidism (HpT) and hypothyroidism (HypoT) reduced the peak of CIC but increased EC, in spite of improving PICR. Both, CIC and PICR in HpT were also sensitive to inhibition of mNCX or UCam, suggesting that Mit contribute to regulate the SR store and Ca release. The interaction between mitochondria and SR and the energetic consequences were also analyzed for the effects of genistein in hearts exposed to I/R, and for the hypoxia/reoxygenation process. Ou...

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A unique micromechanocalorimeter for simultaneous measurement of heat rate and force production of cardiac trabeculae carneae

Cited by 38 publications

References 25 publications

A high-resolution thermoelectric module-based calorimeter for measuring the energetics of isolated ventricular trabeculae at body temperature

A high-resolution thermoelectric module-based calorimeter for measuring the energetics of isolated ventricular trabeculae at body temperature

Muscle heat: a window into the thermodynamics of a molecular machine

Mitochondrial Bioenergetics During Ischemia and Reperfusion

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