Talk:Boushel 2011 Mitochondrion

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Faculty of 1000

This paper - "Muscle mitochondrial capacity exceeds maximal oxygen delivery in humans (2011)" - has been selected and evaluated by Max Gassmann, a Member of the Faculty of 1000. More information for subscribers:
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Sections: Chemical Biology of the Cell,Integrative Physiology,Muscle & Connective Tissue
This work details our current understanding of oxygen transport and utilization while also contributing novel insight into mitochondrial physiology. Comparisons and references relating ex vivo measurements of mitochondrial respiration to various functional in vivo assessments of oxygen flux are greatly needed and this study provides just that. The study by Boushel et al. provides direct evidence advocating a mitochondrial respiratory reserve; a capacity for cellular respiration in skeletal muscle that can exceed the capacity for oxygen transport during maximal exercise. These results substantiate and extend upon findings of earlier, classic studies {1, 2}. The ability to examine mitochondrial function ex vivo via small intact tissue samples, such as permeabilized skeletal muscle fibers, has dramatically improved over the last decade {3} and is becoming commonplace in studies that vary greatly in topic. It is not, however, completely understood how representative or reflective these measurements are of in vivo mitochondrial function. This specific study found that ex vivo measurements of maximal oxidative phosphorylation (malate + octanoyl carnitine + glutamate + succinate + ADP-stimulated state 3 respiration) from a vastus lateralis tissue sample exceeded in vivo skeletal muscle oxygen consumption during lower-body maximal exercise consisting of 26% body mass (6.9 and 5.0 mmol O2 per kg & min, respectively) although respiratory capacities from deltoid muscle samples did not exceed oxygen consumption during upper-body maximal exercise, engaging only 8% body mass (4.3 and 4.7 mmol O2 per kg & min, respectively). The caveat being, however, that the respiratory capacities being compared, both of which were normalized to mass, were from different muscles. There is evidence demonstrating greater mitochondrial content per gram of skeletal muscle obtained from the vastus lateralis versus the deltoid {4}. Taking this into account, with the assumption that mitochondrial content of the deltoid is approximately 67% of that in the vastus lateralis {4}, differences in ex vivo respiratory capacities between lower- and upper-body muscle samples disappear. Moreover, while in vivo measurements of oxygen consumption in the leg during cycle ergometry remain lower than ex vivo respiratory measurements in the vastus lateralis, oxygen consumption during maximal arm crank ergometry may actually exceed OXPHOS capacity (maximal State 3 respiration) in the deltoid. An earlier study examining lower limb oxygen consumption during knee extensor exercise, involving only 3% body mass, reported in vivo oxygen consumption of approximately 13.3 mmol O2 per kg & min {2}. This dramatically exceeds the current study's reported maximal State 3 respiration measured from vastus lateralis samples, which would only account for 52% of in vivo oxygen consumption.
These measurements correspond with previous in vitro measurements of isolated mitochondrial respiration that accounted for, at most, 60% of measured in vivo oxygen consumption {2}. Electron transport capacity, or maximal non-coupled respiration, does exceed maximal oxidative phosphorylation capacity in human skeletal muscle {5}; however, the physiologic relevance of this phenomenon is unknown. Are in vivo measurements of oxygen consumption above those of ex vivo maximal State 3 respiration a result of mitochondrial uncoupling? Or rather, an aberration of ex vivo respiratory measurements? Future studies should compare in vivo oxygen consumption during maximal exercise engaging only a small muscle mass to ex vivo measurements of maximal, non-coupled, electron transport capacity to help clarify these questions.
{1} Andersen, Saltin (1985) J. Physiol. 366: 233-249 [PMID:4057091].
{2} Rasmussen et al (2001) Am. J. Physiol. Endocrinol. Metab. 280: E301-307 [PMID:11158934].
{3} Kuznetsov et al (2008) Nat. Protoc. 3: 965-976 [PMID:18536644].
{4} Larsen et al. (2009) Diabetologia 52: 1400-1408 [PMID:19396425].
{5} Gnaiger E (2009) Int. J. Biochem. Cell Biol. 41: 1837-1845 [PMID:19467914].
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