Analysis of intracellular oxygenation of isolated adult cardiac myocytes

Jones, Dean P.; Kennedy, F. G.

doi:10.1152/ajpcell.1986.250.3.c384

Cited by 38 publications

(21 citation statements)

References 29 publications

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“…The value used here was based on in vivo measures of oxygen diffusion using phosphorescence quenching microscopy (32). Although this estimate is considerably lower than Krogh's original estimate (33), it is within two-to threefold of many current estimates from various tissues-particularly those using in vivo methods (34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46). The diffusion constant was adjusted for temperature to 38°C in our analysis of endotherms and to 25°C for ectotherms, based on a reported Q10 of 1.1 (47).…”

Section: Methodsmentioning

confidence: 95%

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Gillooly

Gómez

Mavrodiev

et al. 2016

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

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The area and thickness of respiratory surfaces, and the constraints they impose on passive oxygen diffusion, have been linked to differences in oxygen consumption rates and/or aerobic activity levels in vertebrates. However, it remains unclear how respiratory surfaces and associated diffusion rates vary with body mass across vertebrates, particularly in relation to the body mass scaling of oxygen consumption rates. Here we address these issues by first quantifying the body mass dependence of respiratory surface area and respiratory barrier thickness for a diversity of endotherms (birds and mammals) and ectotherms (fishes, amphibians, and reptiles). Based on these findings, we then use Fick's law to predict the body mass scaling of oxygen diffusion for each group. Finally, we compare the predicted body mass dependence of oxygen diffusion to that of oxygen consumption in endotherms and ectotherms. We find that the slopes and intercepts of the relationships describing the body mass dependence of passive oxygen diffusion in these two groups are statistically indistinguishable from those describing the body mass dependence of oxygen consumption. Thus, the area and thickness of respiratory surfaces combine to match oxygen diffusion capacity to oxygen consumption rates in both air-and water-breathing vertebrates. In particular, the substantially lower oxygen consumption rates of ectotherms of a given body mass relative to those of endotherms correspond to differences in oxygen diffusion capacity. These results provide insights into the long-standing effort to understand the structural attributes of organisms that underlie the body mass scaling of oxygen consumption.allometry | metabolic theory | respiration rate | metabolism | oxygen consumption S ince the classic debates of Krogh and Bohr (1), the relationship of passive oxygen diffusion to oxygen consumption has remained the focus of considerable research (2). Still, we have much to learn about how oxygen diffusion across respiratory surfaces relates to whole-organism oxygen consumption (3). In particular, we have much to learn about how the structural constraints on oxygen diffusion capacity, namely the thickness and area of respiratory surfaces, relate to the body mass scaling of oxygen consumption in vertebrates-a pattern that reflects the scaling of species' energy use (3).Studies on the body mass dependence of oxygen diffusion have been undertaken over the last century in all major classes of vertebrates, typically using respiratory surface area as a metric of diffusion capacity (2, 3). Less commonly, studies have also considered potentially relevant changes in respiratory barrier thickness with mass (4). In many cases, these studies have concluded that the body mass scaling of oxygen diffusion relative to that of oxygen consumption differs between endotherms and ectotherms (3,5,6). This has led to very different conclusions regarding the structure and function of respiratory systems among classes of vertebrates, as explained below.Among endotherms, particularly...

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Section: Methodsmentioning

confidence: 95%

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Gillooly

Gómez

Mavrodiev

et al. 2016

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

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“…By considering the available experimental information (Evans et al 1981, Jones 1984, Jones & Kennedy 1986, Rumsey et al 1990, Lango et al 1996, as well as theoretical determinations (Tai & Chang 1974), a feasible range for the diffusion coefficient of oxygen in pure granulosa cells (D g ) is estimated to range from 1 to 5!10 K10 m 2 /s. Therefore, the nominal value of D g is taken as 3!10 K10 m 2 /s (mid range).…”

Section: Estimation Of the Diffusion Coefficient Of Oxygen In The Gramentioning

confidence: 99%

Mathematical modelling of oxygen transport-limited follicle growth

Redding¹,

Bronlund²,

Hart³

2007

Reproduction

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Mathematical modelling was used to investigate oxygen transport in the developing ovarian follicle. In contrast to previous findings, the results show that oxygen can reach the oocyte in large preantral follicles. This is largely due to the inclusion of fluid voidage in the model and improved estimates of oxygen diffusion coefficients through the granulosa. The results also demonstrate that preantral follicles will eventually reach a size beyond which further growth will result in the follicle becoming increasingly anoxic. The predicted size range at which this occurs is consistent with the size range at which antrum formation is observed in many mammals. This suggests that the antrum formation stage of follicular growth may be pivotal to the further development and ultimate fate of the follicle, and that antrum formation itself may represent a mechanism by which the follicle can overcome oxygen limitations. This was supported through extension of the model to the antral follicle, which showed that antrum formation can provide a way in which the follicle can continue to grow and yet avoid becoming hypoxic. The results of the model were consistent with observed follicle development.

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“…The present study indicates that the maximal mitochondrial oxygen consumption in isolated cat muscles is somewhat lower than values obtained during voluntary exercise (range in the present study 0O81 to 2-29 ml 02 cm-3 min-'). In vitro, the oxygen consumption rates of mitochondria in isolated cardiac myocytes under control and uncoupled conditions are reported to be 2-1 and 4-2 ml 02 cm-3 min-', respectively (calculated from Jones & Kennedy, 1986, assuming a volume density of 33 % for mitochondria in rat heart cells). Further, Schwerzmann et al (1986) reported isolated liver mitochondria to consume from 0-48 to 3 40 ml 02 cm-3 min-' depending on substrate.…”

Section: Oxygen Consumptionmentioning

confidence: 99%

Relationship between mitochondria and oxygen consumption in isolated cat muscles.

Hoppeler

Hudlická

Uhlmann

1987

The Journal of Physiology

106

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SUMMARY1. Oxygen consumption, mitochondrial content and composition, intracellular lipid stores and fibre size were studied in isolated cat muscles: predominantly glycolytic gracilis, purely oxidative soleus and gracilis transformed into an oxidative muscle by chronic low-frequency (10 Hz) electrical stimulation.2. Oxygen consumption in control gracilis at rest (0 303 + 0 050 ml 02 min-' 100 g-'; mean + S.E. of mean) was three to five times lower than in either stimulated gracilis (1-16+0-40) or soleus (1-57+0056); it was about two times lower during maximal contractions in control gracilis (5 15 + 0 24) than in either stimulated gracilis (11-6 +2'0) or soleus (9-34 + 0-78).3. The volume density of mitochondria in control gracilis (2-75 + 012 %) was half that of soleus (6-23 + 0 76) and only one-third that of stimulated gracilis (8-35 + 0-7 1). Subsarcolemmal mitochondria represented a significantly smaller fraction of the total mitochondrial volume in control gracilis than in either soleus or stimulated gracilis.4. The surface area of inner and outer mitochondrial membranes per unit volume of mitochondria ranged from 23-4 to 26'1 and from 14-0 to 16-5 m2 cm-3, respectively.Mean values of these variables were not significantly different among experimental groups. 5. The volume density of the intracellular lipid stores in control gracilis (0-232 + 0-041 %) was one-fourth of that in stimulated gracilis (0-860 +0-12) and one-fifth of that in soleus (1-17 + 0 27).6. The fibre cross-sectional area was 1670 + 260,m2 in control gracilis, 2250 + 280 in stimulated gracilis and 2390+110 in soleus. The difference was statistically significant only between control gracilis and soleus.7. There was a significant correlation between the volume density of mitochondria and maximal oxygen consumption for all three muscles combined.8. It was found that mitochondrial structure was similar in muscles with different oxidative capacities and that equal amounts of mitochondria consumed equal amounts of oxygen under limiting conditions of maximal in vivo respiration.

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Analysis of intracellular oxygenation of isolated adult cardiac myocytes

Cited by 38 publications

References 29 publications

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Mathematical modelling of oxygen transport-limited follicle growth

Relationship between mitochondria and oxygen consumption in isolated cat muscles.

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