pH control in rat skeletal muscle during exercise, recovery from exercise, and acute respiratory acidosis

Kemp, Graham J.; Thompson, C.; Sanderson, A. L.; Radda, GK

doi:10.1002/mrm.1910310203

Cited by 50 publications

(55 citation statements)

References 27 publications

(45 reference statements)

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“…After acidifying exercise, pH recovers, despite net H ϩ generation by PCr resynthesis (16), because of acid efflux, due partly to the Na ϩ /H ϩ antiporter and to lactate-H ϩ cotransport (18). In the absence of acid pH change or lactate accumulation (as here), there is no driving force for H ϩ efflux, and so the return of pH from alkaline to basal is, to a first approximation, the consequence of PCr resynthesis H ϩ generation alone, as in the dogfish muscle study (8).…”

Section: Discussionmentioning

confidence: 99%

“…We will argue that lactate production is negligible, so that H ϩ load ϭ Ϫ͐␥d[PCr], which is negative and results in alkalinization. During recovery from acidifying exercise, pH returns to basal, despite net H ϩ generation by PCr resynthesis, because of net H ϩ (acid) efflux from the cell by various means (18). Here, where muscle alkalinizes during exercise, we will argue that H ϩ efflux during recovery is negligible, so that H ϩ load ϭ Ϫ ͐␥d [PCr], which is positive and results in acidification (8).…”

Section: Subjectsmentioning

confidence: 99%

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ATP synthesis and proton handling in muscle during short periods of exercise and subsequent recovery

Bendahan

Kemp

Roussel

et al. 2003

Journal of Applied Physiology

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. Cozzone. ATP synthesis and proton handling in muscle during short periods of exercise and subsequent recovery. J Appl Physiol 94: 2391-2397, 2003.. First published February 28, 2003 10.1152 10. /japplphysiol.00589.2002 31 P-magnetic resonance spectroscopy to study proton buffering in finger flexor muscles of eight healthy men (25-45 yr), during brief (18-s) voluntary finger flexion exercise (0.67-Hz contraction at 10% maximum voluntary contraction; 50/50 duty cycle) and 180-s recovery. Phosphocreatine (PCr) concentration fell 19 Ϯ 2% during exercise and then recovered with half time ϭ 0.24 Ϯ 0.01 min. Cell pH rose by 0.058 Ϯ 0.003 units during exercise as a result of H ϩ consumption by PCr splitting, which (assuming no lactate production or H ϩ efflux) implies a plausible non-Pi buffer capacity of 20 Ϯ 3 mmol ⅐ l intracellular water Ϫ1 ⅐ pH unit Ϫ1 . There was thus no evidence of significant glycogenolysis to lactate during exercise. Analysis of PCr kinetics as a classic linear response suggests that oxidative ATP synthesis reached 48 Ϯ 2% of ATP demand by the end of exercise; the rest was met by PCr splitting. Postexercise pH recovery was faster than predicted, suggesting "excess proton" production, with a peak value of 0.6 Ϯ 0.2 mmol/l intracellular water at 0.45 min of recovery, which might be due to, e.g., proton influx driven by cellular alkalinization, or a small glycolytic contribution to PCr resynthesis in recovery.bioenergetics; buffer capacity; glycogenolysis; phosphorus-31 magnetic resonance spectroscopy; skeletal muscle ALTHOUGH THE NONINVASIVE TECHNIQUE of 31 P-magnetic resonance spectroscopy (MRS) of muscle can measure far fewer metabolites than biopsy-based methods, time-resolved 31 P-MRS measurements of exercise and recovery changes in phosphocreatine (PCr), P i , and cytosolic pH offer a window into important aspects of ATP turnover and cellular acid-base physiology ("H ϩ handling") (15). There are two basic approaches: assume cytosolic buffer capacity (␤) and so estimate lactate synthesis (4); or assume a constant contractile efficiency and so estimate, for example, glycolytic ATP synthesis in ischemic exercise (13) and oxidative ATP synthesis in pure "aerobic" exercise (24). The ␤ (13) is difficult to measure in vivo, except indirectly by using 31 P-MRS (1). We earlier used an analysis of ischemic exercise (13) to estimate ␤ in human muscle, which was complicated by its pH dependence. Here we set out to minimize such complications by studying the early phase of the rest-exercise and exercise-rest transitions by using 31 P-MRS. Because of their bearing on the analysis of ATP turnover, we also consider some quantitative implications of recent proposals that rapid cycles of PCr splitting and resynthesis (3), fueled by anaerobic glycogenolysis (29), operate during muscle contraction, unobservable by conventional 31 P-MRS or biopsy methods. Part of this work has been presented in preliminary form (12). METHODS Subjects.The study was conducted on the dominant forearm of eight male volunteers, age...

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Section: Discussionmentioning

confidence: 99%

Section: Subjectsmentioning

confidence: 99%

ATP synthesis and proton handling in muscle during short periods of exercise and subsequent recovery

Bendahan

Kemp

Roussel

et al. 2003

Journal of Applied Physiology

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“…The clearance rate of protons can be quite large and variable, and buffer capacity also is subject to change (92). These issues are extensively discussed elsewhere, including interpretation of lactic acidosis (93,94).…”

Section: Anaerobic Glycolysismentioning

confidence: 99%

Skeletal muscle energetics with PNMR: personal views and historic perspectives

Chance

Nioka

et al. 2006

NMR in Biomedicine

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This article reviews historical and current NMR approaches to describing in vivo bioenergetics of skeletal muscles in normal and diseased populations. It draws upon the first author's more than 70 years of personal experience in enzyme kinetics and the last author's physiological approaches. The development of in vivo PNMR jointly with researchers around the world is described. It is explained how non-invasive PNMR has advanced human exercise biochemistry, physiology and pathology. Further, after a brief explanation of bioenergetics with PNMR on creatine kinase, anerobic glycolysis and mitochondrial oxidative phosphorylation, some basic and controversial subjects are focused upon, and the authors' view of the subjects are offered, with questions and answers. Some of the research has been introduced in exercise physiology. Future directions of NMR on bioenergetics, as a part of system biological approaches, are indicated.

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“…In other words, it is not excluded that the expected higher non-oxidative glycolysis-related H + production has been compensated by the greater H + removal due to the faster PCr hydrolysis, explaining why no difference was recorded concerning pH despite a potential ischemia in M1. In the same line, considering PCr resynthesis as a protons source [21], the slower PCr recovery kinetics observed in M1 ( figure 1A) can be considered as a reduced H + source during the recovery period thereby limiting intracellular acidosis, potentially counteracting the direct effects of ischemia. In addition, it is also possible that intracellular H + removal was increased in M1 mouse.…”

Section: Accepted Manuscriptmentioning

confidence: 94%

Exacerbated in vivo metabolic changes suggestive of a spontaneous muscular vaso-occlusive crisis in exercising muscle of a sickle cell mouse

Chatel

Messonnier

Bendahan

2017

Blood Cells, Molecules, and Diseases

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, Exacerbated in vivo metabolic changes suggestive of a spontaneous muscular vasoocclusive crisis in exercising muscle of a sickle cell mouse, Blood Cells, Molecules and Diseases (2017), doi: 10.1016/j.bcmd.2017 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPTA C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT A C C E P T E D M A N U S C R I P TMuscular vaso-occlusive crisis in a sickle mouse 3 AbstractWhile sickle cell disease (SCD) is characterized by frequent vaso-occlusive crisis (VOC), no direct observation of such an event in skeletal muscle has been performed in vivo. The present study reported exacerbated in vivo metabolic changes suggestive of a spontaneous muscular VOC in exercising muscle of a sickle cell mouse. Using magnetic resonance spectroscopy of phosphorus 31, phosphocreatine and inorganic phosphate concentrations and intramuscular pH were measured throughout two standardized protocols of restexercise -recovery at two different intensities in ten SCD mice. Among these mice, one single mouse presented divergent responses. A statistical analysis (based on confidence intervals) revealed that this single mouse presented slower phosphocreatine resynthesis and inorganic phosphate disappearance during the post-stimulation recovery of one of the protocols, what could suggest an ischemia. This study described, for the first time in a sickle cell mouse in vivo, exacerbated metabolic changes triggered by an exercise session that would be suggestive of a live observation of a muscular VOC. However, no evidence of a direct cause-effect relationship between exercise and VOC has been put forth. Key wordsPhysical activity, red blood cell sickling, HbS polymerization, magnetic resonance spectroscopy of phosphorus 31. ACCEPTED MANUSCRIPT A C C E P T E D M A N U S C R I P TMuscular vaso-occlusive crisis in a sickle mouse 4 Introduction Sickle cell disease (SCD) is a genetic hemoglobinopathy related to the production of abnormal hemoglobin (HbS). In its deoxygenated form, HbS tends to polymerize, leading to the sickling of red blood cells (RBC) [1]. Owing to their poor deformability and elevated adhesion, sickle RBCs tend to obstruct the microcirculation thereby leading to vaso-occlusive crises (VOC) that represent the most severe clinical complications of SCD [2]. If this type of crisis has been acknowledged in many tissues [2], the potential occurrence of such an event in skeletal muscle has rarely been documented [3; 4; 5; 6]. To the best of our knowledge, no direct observation of a skeletal muscle VOC has been performed in real time.In a pr...

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pH control in rat skeletal muscle during exercise, recovery from exercise, and acute respiratory acidosis

Cited by 50 publications

References 27 publications

ATP synthesis and proton handling in muscle during short periods of exercise and subsequent recovery

ATP synthesis and proton handling in muscle during short periods of exercise and subsequent recovery

Skeletal muscle energetics with PNMR: personal views and historic perspectives

Exacerbated in vivo metabolic changes suggestive of a spontaneous muscular vaso-occlusive crisis in exercising muscle of a sickle cell mouse

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