Carbonic anhydrase in skeletal and cardiac muscle from rabbit and rat

Geers, Cornelia; D, Krüger; Siffert, Winfried; Schmid, Andreas; Bruns, W.; Gro, G

doi:10.1042/bj2820165

Cited by 25 publications

(25 citation statements)

References 33 publications

(39 reference statements)

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“…The animal's right hind limb was extended, and the surface coil was placed over the belly of the gastrocnemius muscle. A one-turn standard 1 H coil was placed underneath the hind limb to permit localized shimming. The homogeneity of the magnetic field was optimized by using the proton signal from skeletal muscle (Ϸ50 Hz).…”

Section: Methodsmentioning

confidence: 99%

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A quantitative study of bioenergetics in skeletal muscle lacking carbonic anhydrase III using ³¹ P magnetic resonance spectroscopy

Liu

Walter

Pathare

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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Oxidative slow skeletal muscle contains carbonic anhydrase III in high concentration, but its primary function remains unknown. To determine whether its lack handicaps energy metabolism and/or acid elimination, we measured the intracellular pH and energy phosphates by 31 P magnetic resonance spectroscopy in hind limb muscles of wild-type and CA III knockout mice during and after ischemia and intense exercise (electrical stimulation). Thirty minutes of ischemia caused phosphocreatine (PCr) to fall and Pi to rise while pH and ATP remained constant in both strains of mice. PCr and Pi kinetics during ischemia and recovery were not significantly different between the two genotypes. From this we conclude that under neutral pH conditions resting muscle anaerobic metabolism, the rate of the creatine kinase reaction, intracellular buffering of protons, and phosphorylation of creatine by mitochondrial oxygen metabolism are not influenced by the lack of CA III. Two minutes of intense stimulation of the mouse gastrocnemius caused PCr, ATP, and pH to fall and ADP and P i to rise, and these changes, with the exception of ATP, were all significantly larger in the CA III knockouts. The rate of return of pH and ADP to control values was the same in wild-type and mutant mice, but in the mutants PCr and Pi recovery were delayed in the first minute after stimulation. Because the tension decrease during fatigue is known to be the same in the two genotypes, we conclude that a lack of CA III impairs mitochondrial ATP synthesis.mitochondrial ATP synthesis S keletal muscle contains at least four isozymes of carbonic anhydrase (EC 4.2.1.1): CA II, CA III, CA IV, and CA V (1). CA II, the high-activity enzyme found in erythrocytes, is present in the sarcoplasm available to accelerate the removal of acid as CO 2 . CA IV is bound to the sarcolemma and facilitates lactate transport across the sarcolemma. CA V, in the mitochondria, accelerates the metabolism of pyruvate (2). CA III is present in the highest concentration of any of the carbonic anhydrases, as much as 2% of wet weight in slow oxidative muscle (type 1) (3), but its function is unknown. It is only minimally present in fast glycolytic (type 2) muscle (4). Changes in CA III levels have been reported when skeletal muscle is undergoing remodeling due to training (5) or inactivity (6, 7). CA III has a molecular weight of Ϸ30,000, similar to that of isozymes CA II, CA IV, and CA V, but accelerates CO 2 hydration at only 1/60th as much as human erythrocyte CA II and is 30,000 times less sensitive to acetazolamide (a widely used sulfonamide inhibitor) (8). It has two reactive surface cysteines, whereas the other muscle isozymes have none, indicating that it may have a role in the regulation of oxidative stress (9). In addition, CA III itself interacts directly with glutathione and is highly modified during lipid peroxidation (10, 11). Despite many experimental studies, no convincing rationale for the presence, preservation, and production of the large concentration of CA III in oxidative ...

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Section: Methodsmentioning

confidence: 99%

“…keletal muscle contains at least four isozymes of carbonic anhydrase (EC 4.2.1.1): CA II, CA III, CA IV, and CA V (1). CA II, the high-activity enzyme found in erythrocytes, is present in the sarcoplasm available to accelerate the removal of acid as CO 2 .…”

mentioning

confidence: 99%

A quantitative study of bioenergetics in skeletal muscle lacking carbonic anhydrase III using ³¹ P magnetic resonance spectroscopy

Liu

Walter

Pathare

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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“…CA activities were measured using the barbital system in Maren's micromethod as described by Bruns and Gros (11). CA III activity was determined in the presence of 5 ϫ 10 Ϫ6 M of the CA inhibitor acetazolamide, and CA II activity was obtained by subtracting CA III activity from the total activity measured in the absence of inhibitor (12).…”

Section: Methodsmentioning

confidence: 99%

Adult fast myosin pattern and Ca ²⁺ -induced slow myosin pattern in primary skeletal muscle culture

Kubis

Haller

Wetzel

et al. 1997

Proc. Natl. Acad. Sci. U.S.A.

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A primary muscle cell culture derived from newborn rabbit muscle and growing on microcarriers in suspension was established. When cultured for several weeks, the myotubes in this model develop the completely adult pattern of fast myosin light and heavy chains. When Ca 2؉ ionophore is added to the culture medium on day 11, raising intracellular [Ca 2؉ ] about 10-fold, the myotubes develop to exhibit properties of an adult slow muscle by day 30, expressing slow myosin light as well as heavy chains, elevated citrate synthase, and reduced lactate dehydrogenase. The remarkable plasticity of these myotubes becomes apparent, when 8 days after withdrawal of the ionophore a marked slow-to-fast transition, as judged from the expression of isomyosins and metabolic enzymes, occurs.While the alterations that occur in mammalian muscle during fast-to-slow transition in vivo are known in great detail, mostly from chronic electrostimulation experiments with fast hindlimb muscles (1), the information on the mechanism initiating this process is sparse. A reduced intracellular phosphorylation potential and an elevated intracellular Ca 2ϩ concentration ([Ca 2ϩ ] i ), as they occur during sustained contractile activity, have been discussed as possible trigger events (2-5). It was our aim to test whether an increase in [Ca 2ϩ ] i imposed on the muscle cell is indeed able to induce a fast-to-slow transition. Because such an experiment cannot be performed in vivo, we were searching for a suitable myogenic cell culture system in which this would become feasible.Thus, this paper has two goals: (i) to report how a primary muscle culture can be grown that develops into an adult-like state, expressing adult myosin of the fast type only, and (ii) to study whether manipulation of [Ca 2ϩ ] i induces a shift between ''fast'' and ''slow'' fiber properties in the cultured myotubes. We show, first, that myotubes derived from newborn rabbit muscles and grown for 4 weeks on microcarriers in suspension possess a purely adult fast myosin pattern. Second, we show that these myotubes exhibit a similarly remarkable plasticity as it is known for adult rabbit muscles (1). This plasticity becomes apparent during exposure of the myotubes to high [Ca 2ϩ ] i , which causes development of the slow isoforms of myosin light chains (MLCs) and myosin heavy chains (MHCs) instead of their fast counterparts, of an increased aerobic metabolic capacity accompanied by a decreased anaerobic capacity as evidenced from elevated citrate synthase (CS) and reduced lactate dehydrogenase (LDH) levels, and of an increased activity ratio of the carbonic anhydrases CA III/CA II. Lowering [Ca 2ϩ ] i back to normal levels is followed by a reversal of all these changes within a few days. EXPERIMENTAL PROCEDURESCulture and Harvesting of Muscle Cells. Newborn White New Zealand rabbits were killed by decapitation. Hindlimb muscles were cut in small pieces and incubated in BSS, pH 7.0 (4.56 mM KCl͞0.44 mM KH 2 PO 4 ͞0.42 mM Na 2 HPO 4 ͞25 mM NaHCO 3 ͞ 119.8 mM NaCl͞50 mg/...

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“…These insights cannot be obtained by studying isolated plasma membranes because of the high CA activity in the microsomal fraction Geers et al, 1992), as CA4 is present on both endothelial cell and cardiomyocyte membranes (Knüppel-Ruppert et al, 2000; Sender et al, 1998), as well as potential contamination from intracellular CA4 activity (Schneider et al, 2013). Nonetheless, limitations to our method include the inability to measure the true uncatalyzed reaction rate and a lack of mixing of the reaction volume, which prevent quantification of absolute CA activity.…”

Section: Discussionmentioning

confidence: 97%

Evidence for a plasma-accessible carbonic anhydrase in the lumen of salmon heart that may enhance oxygen delivery to the myocardium

Alderman

Harter

Wilson

et al. 2016

Journal of Experimental Biology

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Oxygen supply to the heart of most teleosts, including salmonids, relies in part or in whole on oxygen-depleted venous blood. Given that plasma-accessible carbonic anhydrase (CA) in red muscle of rainbow trout has recently been shown to facilitate oxygen unloading from arterial blood under certain physiological conditions, we tested the hypothesis that plasma-accessible CA is present in the lumen of coho salmon (Oncorhynchus kisutch) hearts, and may therefore assist in the luminal oxygen supply to the spongy myocardium, which has no coronary circulation. We demonstrate a widespread distribution of CA throughout the heart chambers, including lumen-facing cells in the atrium, and confirm that the membrane-bound isoform ca4 is expressed in the atrium and ventricle of the heart. Further, we confirm that CA catalytic activity is available to blood in the atrial lumen using a modified electrometric ΔpH assay in intact atria in combination with either a membrane-impermeable CA inhibitor or specific cleavage of the Ca4 membrane anchor. Combined, these results support our hypothesis of the presence of an enhanced oxygen delivery system in the lumen of a salmonid heart, which could help support oxygen delivery when the oxygen content of venous blood becomes greatly reduced, such as after burst exercise and during environmental hypoxia.

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Carbonic anhydrase in skeletal and cardiac muscle from rabbit and rat

Cited by 25 publications

References 33 publications

A quantitative study of bioenergetics in skeletal muscle lacking carbonic anhydrase III using ³¹ P magnetic resonance spectroscopy

A quantitative study of bioenergetics in skeletal muscle lacking carbonic anhydrase III using ³¹ P magnetic resonance spectroscopy

Adult fast myosin pattern and Ca ²⁺ -induced slow myosin pattern in primary skeletal muscle culture

Evidence for a plasma-accessible carbonic anhydrase in the lumen of salmon heart that may enhance oxygen delivery to the myocardium

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Carbonic anhydrase in skeletal and cardiac muscle from rabbit and rat

Cited by 25 publications

References 33 publications

A quantitative study of bioenergetics in skeletal muscle lacking carbonic anhydrase III using 31 P magnetic resonance spectroscopy

A quantitative study of bioenergetics in skeletal muscle lacking carbonic anhydrase III using 31 P magnetic resonance spectroscopy

Adult fast myosin pattern and Ca 2+ -induced slow myosin pattern in primary skeletal muscle culture

Evidence for a plasma-accessible carbonic anhydrase in the lumen of salmon heart that may enhance oxygen delivery to the myocardium

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A quantitative study of bioenergetics in skeletal muscle lacking carbonic anhydrase III using ³¹ P magnetic resonance spectroscopy

A quantitative study of bioenergetics in skeletal muscle lacking carbonic anhydrase III using ³¹ P magnetic resonance spectroscopy

Adult fast myosin pattern and Ca ²⁺ -induced slow myosin pattern in primary skeletal muscle culture