scispace - formally typeset
Search or ask a question
Journal Article•DOI•

Does intracellular metabolite diffusion limit post-contractile recovery in burst locomotor muscle?

Stephen T. Kinsey1, Pragyansri Pathi2, Kristin M. Hardy1, Amanda Jordan2, Bruce R. Locke2 •
University of North Carolina at Wilmington1, Florida A&M University – Florida State University College of Engineering2
15 Jul 2005-The Journal of Experimental Biology (J Exp Biol)-Vol. 208, Iss: 14, pp 2641-2652
TL;DR: It is concluded that fiber SA:V and O2 flux exert more control than intracellular metabolite diffusive flux over the developmental changes in metabolic organization and metabolic fluxes that characterize these muscles.
Abstract: Post-metamorphic growth in the blue crab entails an increase in body mass that spans several orders of magnitude. The muscles that power burst swimming in these animals grow hypertrophically, such that small crabs have fiber diameters that are typical of most cells ( 600·µm). Thus, as the animals grow, their muscle fibers cross and greatly exceed the surface area to volume ratio (SA:V) and intracellular diffusion distance threshold that is adhered to by most cells. Large fiber size should not impact burst contractile function, but post-contractile recovery may be limited by low SA:V and excessive intracellular diffusion distances. A number of changes occur in muscle structure, metabolic organization and metabolic flux during development to compensate for the effects of increasing fiber size. In the present study, we examined the impact of intracellular metabolite diffusive flux on the rate of postcontractile arginine phosphate (AP) resynthesis in burst locomotor muscle from small and large animals. AP recovery was measured following burst exercise, and these data were compared to a mathematical reaction‐diffusion model of aerobic metabolism. The measured rates of AP resynthesis were independent of fiber size, while simulations of aerobic AP resynthesis yielded lower rates in large fibers. These contradictory findings are consistent with previous observations that there is an increased reliance on anaerobic metabolism for post-contractile metabolic recovery in large fibers. However, the model results suggest that the interaction between mitochondrial ATP production rates, ATP consumption rates and diffusion distances yield a system that is not particularly close to being limited by intracellular metabolite diffusion. We conclude that fiber SA:V and O2 flux exert more control than intracellular metabolite diffusive flux over the developmental changes in metabolic organization and metabolic fluxes that characterize these muscles.

Content maybe subject to copyright    Report

Citations
More filters
Journal Article•DOI•
Do we underestimate the importance of water in cell biology

[...]

Martin F. Chaplin1•
London South Bank University1
01 Nov 2006-Nature Reviews Molecular Cell Biology
TL;DR: Water can generate small active clusters and macroscopic assemblies, which can both transmit information on different scales and allow water to execute an intricate three-dimensional 'ballet' while retaining complex order and enduring effects.
Abstract: Liquid water is a highly versatile material. Although it is formed from the tiniest of molecules, it can shape and control biomolecules. The hydrogen-bonding properties of water are crucial to this versatility, as they allow water to execute an intricate three-dimensional 'ballet', exchanging partners while retaining complex order and enduring effects. Water can generate small active clusters and macroscopic assemblies, which can both transmit information on different scales.

566 citations

Journal Article•DOI•
Molecules in motion: influences of diffusion on metabolic structure and function in skeletal muscle

[...]

Stephen T. Kinsey1, Bruce R. Locke2, Richard M. Dillaman1•
University of North Carolina at Wilmington1, Florida A&M University – Florida State University College of Engineering2
15 Jan 2011-The Journal of Experimental Biology
TL;DR: Experimental measurements of metabolic fluxes, diffusion distances and diffusion coefficients, coupled with reaction–diffusion mathematical models in a range of muscle types has started to reveal some general principles guiding muscle structure and metabolic function.
Abstract: Metabolic processes are often represented as a group of metabolites that interact through enzymatic reactions, thus forming a network of linked biochemical pathways. Implicit in this view is that diffusion of metabolites to and from enzymes is very fast compared with reaction rates, and metabolic fluxes are therefore almost exclusively dictated by catalytic properties. However, diffusion may exert greater control over the rates of reactions through: (1) an increase in reaction rates; (2) an increase in diffusion distances; or (3) a decrease in the relevant diffusion coefficients. It is therefore not surprising that skeletal muscle fibers have long been the focus of reaction–diffusion analyses because they have high and variable rates of ATP turnover, long diffusion distances, and hindered metabolite diffusion due to an abundance of intracellular barriers. Examination of the diversity of skeletal muscle fiber designs found in animals provides insights into the role that diffusion plays in governing both rates of metabolic fluxes and cellular organization. Experimental measurements of metabolic fluxes, diffusion distances and diffusion coefficients, coupled with reaction–diffusion mathematical models in a range of muscle types has started to reveal some general principles guiding muscle structure and metabolic function. Foremost among these is that metabolic processes in muscles do, in fact, appear to be largely reaction controlled and are not greatly limited by diffusion. However, the influence of diffusion is apparent in patterns of fiber growth and metabolic organization that appear to result from selective pressure to maintain reaction control of metabolism in muscle.

71 citations

Cites background from "Does intracellular metabolite diffu..."

  • ...…density (Kinsey et al., 2007; Locke and Kinsey, 2008), from respiration rates of isolated mitochondria (Burpee et al., 2010), or from direct measurements of ATP turnover using NMR in isolated muscles or in vivo (Kinsey et al., 2005; Hardy et al., 2006; Nyack et al., 2007; Jimenez et al., 2008)....

    [...]

  • ...This allows phosphagen resynthesis to occur faster than our reaction–diffusion model predicted that it should in the large fibers (Kinsey et al., 2005)....

    [...]

  • ...THE JOURNAL OF EXPERIMENTAL BIOLOGY 264 can be <0.1mol ATPg–1min–1 (Kinsey et al., 2005; Nyack et al., 2007), whereas in insect flight muscle it can exceed 2000mol ATPg–1min–1 (Suarez, 1998)....

    [...]

Journal Article•DOI•
Fishes of southern South America: a story driven by temperature

[...]

Victor E. Cussac1, Daniel Alfredo Fernández2, Sergio Enrique Gómez2, Hugo Luis López3•
National University of Comahue1, National Scientific and Technical Research Council2, National University of La Plata3
01 Mar 2009-Fish Physiology and Biochemistry
TL;DR: Biological and ecological data of marine and freshwater fishes from the southern Neotropics, including Patagonia, are reviewed, and several examples of dependence on temperature are reported, from glacial times to today’s climate change.
Abstract: The latitudinal extension of southern South America imposes a thermal gradient that affects the structure of marine and freshwater fish assemblages and the biology of the species through direct exposure to the temperature gradients or by means of a web of historical and ecological relationships. We have reviewed biological and ecological data of marine and freshwater fishes from the southern Neotropics, including Patagonia, and report several examples of dependence on temperature, from glacial times to today’s climate change. We were able to identify historic and present effects on the diversity of fish assemblages, isolation, southern limits for the distribution of species, and morphological variation among populations. There is a wide range of characteristics that exemplify an adaptation to low temperatures, including biochemical peculiarities, physiological adjustments, and alternative life history patterns, and these appear in both freshwater and marine, and native and exotic fishes. The consequences of stable temperature regimes in both the ocean and thermal streams deserve special mention as these shape specialists under conditions of low selective pressure. At present, habitat use and interactions among species are being subject to changes as consequences of water temperature, and some of these are already evident in the northern and southern hemispheres.

69 citations

Cites methods from "Does intracellular metabolite diffu..."

  • ...This idea, called the ‘optimal fiber size hypothesis’, was proposed by Johnston et al. (2003, 2004) for notothenioids and Arctic char evolution and by Kinsey et al. (2005) for blue crabs....

    [...]

Journal Article•DOI•
The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle.

[...]

Stephen T. Kinsey1, Kristin M. Hardy1, Bruce R. Locke2•
University of North Carolina at Wilmington1, Florida A&M University – Florida State University College of Engineering2
15 Oct 2007-The Journal of Experimental Biology
TL;DR: The effect of diffusion distance on O(2) flux in muscle has been the subject of quantitative analyses for a century, but the influence of ATP diffusion from mitochondria to cellular ATPases on aerobic metabolism has received much less attention as discussed by the authors.
Abstract: A fundamental principle of physiology is that cells are small in order to minimize diffusion distances for O(2) and intracellular metabolites. In skeletal muscle, it has long been recognized that aerobic fibers that are used for steady state locomotion tend to be smaller than anaerobic fibers that are used for burst movements. This tendency reflects the interaction between diffusion distances and aerobic ATP turnover rates, since maximal intracellular diffusion distances are ultimately limited by fiber size. The effect of diffusion distance on O(2) flux in muscle has been the subject of quantitative analyses for a century, but the influence of ATP diffusion from mitochondria to cellular ATPases on aerobic metabolism has received much less attention. The application of reaction-diffusion mathematical models to experimental measurements of aerobic metabolic processes has revealed that the extreme diffusion distances between mitochondria found in some muscle fibers do not necessarily limit the rates of aerobic processes per se, as long as the metabolic process is sufficiently slow. However, skeletal muscle fibers from a variety of animals appear to have intracellular diffusion distances and/or fiber sizes that put them on the brink of diffusion limitation. Thus, intracellular metabolite diffusion likely influences the evolution of muscle design and places limits on muscle function.

57 citations

Cites background or methods from "Does intracellular metabolite diffu..."

  • ...Coupling experimental data with a reaction–diffusion mathematical model, however, we found that the observed rate of AP resynthesis following burst contraction in the anaerobic locomotor fibers of small and large blue crabs was not dramatically limited by intracellular metabolite diffusion (Kinsey et al., 2005)....

    [...]

  • ...…data with a reaction–diffusion mathematical model, however, we found that the observed rate of AP resynthesis following burst contraction in the anaerobic locomotor fibers of small and large blue crabs was not dramatically limited by intracellular metabolite diffusion (Kinsey et al., 2005)....

    [...]

  • ...…during fiber growth can be demonstrated by rearranging the equation described above for displacement, , to solve for diffusion time, t, using time-dependent diffusion coefficients and mitochondrial spacing data from a crustacean muscle example (Kinsey and Moerland, 2002; Kinsey et al., 2005)....

    [...]

  • ...Quantitative analyses of some skeletal muscle types indicate that the extent to which metabolite diffusion limits aerobic flux is variable (e.g. Mainwood and Rakusan, 1982; Meyer et al., 1984; Tyler and Sidell, 1984; Egginton and Sidell, 1989; Hubley et al., 1997; Kemp et al., 1998; Kinsey et al., 2005; Hardy et al., 2006; Nyack et al., 2007), but a broad analysis that encompasses diffusion effects over the full spectrum of muscle fiber designs is lacking....

    [...]

  • ...…variable (e.g. Mainwood and Rakusan, 1982; Meyer et al., 1984; Tyler and Sidell, 1984; Egginton and Sidell, 1989; Hubley et al., 1997; Kemp et al., 1998; Kinsey et al., 2005; Hardy et al., 2006; Nyack et al., 2007), but a broad analysis that encompasses diffusion effects over the full spectrum of…...

    [...]

Journal Article•DOI•
The influence of oxygen and high-energy phosphate diffusion on metabolic scaling in three species of tail-flipping crustaceans

[...]

Ana Gabriela Jimenez1, Bruce R. Locke2, Stephen T. Kinsey1•
University of North Carolina at Wilmington1, Florida A&M University – Florida State University College of Engineering2
15 Oct 2008-The Journal of Experimental Biology
TL;DR: An examination of the influence of O2 and HEP diffusion on the observed rate of aerobic flux in muscle revealed that diffusion limitation was minimal under most conditions, suggesting that diffusion might act on the evolution of fiber design but usually does not directly limit aerobic flux.
Abstract: We examined the influence of intracellular diffusion of O(2) and high-energy phosphate (HEP) molecules on the scaling with body mass of the post-exercise whole-animal rate of O(2) consumption (V(O(2))) and muscle arginine phosphate (AP) resynthesis rate, as well as muscle citrate synthase (CS) activity, in three groups of tail-flipping crustaceans. Two size classes in each of three taxa (Palaemonetes pugio, Penaeus spp. and Panulirus argus) were examined that together encompassed a 27,000-fold range in mean body mass. In all species, muscle fiber size increased with body mass and ranged in diameter from 70+/-1.5 to 210+/-8.8 microm. Thus, intracellular diffusive path lengths for O(2) and HEP molecules were greater in larger animals. The body mass scaling exponent, b, for post-tail flipping V(O(2)) (b=-0.21) was not similar to that for the initial rate of AP resynthesis (b=-0.12), which in turn was different from that of CS activity (b=0.09). We developed a mathematical reaction-diffusion model that allowed an examination of the influence of O(2) and HEP diffusion on the observed rate of aerobic flux in muscle. These analyses revealed that diffusion limitation was minimal under most conditions, suggesting that diffusion might act on the evolution of fiber design but usually does not directly limit aerobic flux. However, both within and between species, fibers were more diffusion limited as they grew larger, particularly when hemolymph P(O(2)) was low, which might explain some of the divergence in the scaling exponents of muscle aerobic capacity and muscle aerobic flux.

42 citations

Cites background or methods or result from "Does intracellular metabolite diffu..."

  • ...…ADP, Pi, AP/PCr and arginine/creatine) does not lead to sizable intracellular concentration gradients in the very large anaerobic fibers of crustacean or fish muscle, despite the fact that diffusion might occur over hundreds of microns (Kinsey et al., 2005; Hardy et al., 2006; Nyack et al., 2007)....

    [...]

  • ...The area under each peak was integrated using Xwin-NMR software to yield the relative concentrations of each metabolite, and these values were converted to concentration by assuming a total HEP concentration of 50mmol l–1, which is characteristic of crustacean white muscle (see Kinsey et al., 2005)....

    [...]

  • ...This is consistent with prior suggestions that O2 delivery is a greater constraint on muscle design and function than is HEP diffusion (Kinsey et al., 2005; Hardy et al., 2006; Nyack et al., 2007)....

    [...]

  • ...Exceeding this maximum size might therefore compromise aerobic metabolism, which relies on oxygen flux from the blood to the mitochondria and ATP-equivalent diffusion within the cytoplasm (Mainwood and Rakusan, 1982; Meyer, 1988; Hubley et al., 1997; Boyle et al., 2003; Johnson et al., 2004; Kinsey et al., 2005; Hardy et al., 2006)....

    [...]

  • ...Presumably, adult crabs are exploiting anaerobic metabolism to accelerate certain key phases of recovery such as AP resynthesis, the rate of which would otherwise be restricted by large fiber size (Kinsey and Moerland, 2002; Boyle et al., 2003; Johnson et al., 2004; Kinsey et al., 2005)....

    [...]

References
More filters
Journal Article•DOI•
Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective.

[...]

Ian A. Johnston1, Daniel Alfredo Fernández1, Jorge Calvo2, Vera L. A. Vieira1, Anthony W. North3, Marguerite Abercromby1, Theodore Garland4 •
University of St Andrews1, National Scientific and Technical Research Council2, British Antarctic Survey3, University of California, Riverside4
01 Aug 2003-The Journal of Experimental Biology
TL;DR: Estimates of trait values at nodes of the maximum likelihood phylogenetic tree were consistent with a progressive reduction in fibre number during part of the notothenioid radiation, perhaps serving to reduce basal energy requirements to compensate for the additional energetic costs of antifreeze production.
Abstract: The fish fauna of the continental shelf of the Southern Ocean is dominated by a single sub-order of Perciformes, the Notothenioidei, which have unusually large diameter skeletal muscle fibres. We tested the hypothesis that in fast myotomal muscle a high maximum fibre diameter (FDmax) was related to a reduction in the number of muscle fibres present at the end of the recruitment phase of growth. We also hypothesized that the maximum fibre number (FNmax) would be negatively related to body size, and that both body size and size-corrected FNmax would show phylogenetic signal (tendency for related species to resemble each other). Finally, we estimated ancestral values for body size and FNmax. A molecular phylogeny was constructed using 12S mitochondrial rRNA sequences. A total of 16 species were studied from the Beagle Channel, Tierra del Fuego (5–11°C), Shag Rocks, South Georgia (0.5–4°C), and Adelaide Island, Antarctic Peninsula (–1.5 to 0.5°C). The absence of muscle fibres of less than 10·mm diameter was used as the criterion for the cessation of fibre recruitment. FDmax increased linearly with standard length (SL), reaching 500–650·mm in most species. Maximum body size was a highly significant predictor of species variation in FNmax, and both body size and size-corrected FNmax showed highly significant phylogenetic signal (P<0.001). Estimates of trait values atnodes of the maximum likelihood phylogenetic tree were consistent with a progressive reduction in fibre number during part of the notothenioid radiation, perhaps serving to reduce basal energy requirements to compensate for the additional energetic costs of antifreeze production. For example, FNmax in Chaenocephalus aceratus (12·700±300, mean ± S.E.M., N=18) was only 7.7% of the value found in Eleginops maclovinus (164·000±4100, N=17), which reaches a similar maximum length (85·cm). Postembryonic muscle fibre recruitment in teleost fish normally involves stratified followed by mosaic hyperplasia. No evidence for this final phase of growth was found in two of the most derived families (Channichthyidae and Harpagiferidae). The divergence of the notothenioids in Antarctica after the formation of the Antarctic Polar Front and more recent dispersal north would explain the high maximum diameter and low fibre number in the derived sub-Antarctic notothenioids. These characteristics of notothenioids may well restrict their upper thermal tolerance, particularly for Champsocephalus esox and similar Channichthyids that lack respiratory pigments.

127 citations

"Does intracellular metabolite diffu..." refers background in this paper

  • ...Johnston et al. (2003, 2004) proposed that in certain cold-water fishes white muscle fibers attain a size that is just below that which would be diffusionlimited in order to minimize sarcolemmal surface area over which ionic gradients must be maintained, thus lowering metabolic rates....

    [...]

Journal Article•DOI•
Changes in mitochondrial distribution and diffusion distances in muscle of goldfish upon acclimation to warm and cold temperatures

[...]

Seth Tyler1, Bruce D. Sidell1•
University of Maine1
01 Oct 1984-Journal of Experimental Zoology
TL;DR: It appears reasonable to assume that cold-induced rises in the concentration of enzymes in fish muscle reflect changes in organellar densities–changes which may serve primarily to ameliorate the effect of temperature on diffusive exchange between mitochondria and cytoplasm rather than solely to overcome catalytic limitation as is widely assumed.
Abstract: Transmission electron microscopy of myotomal muscle from goldfish (Carassius auratus L.) reveals significant differences in distribution and density of mitochondria in animals acclimated to cold temperature (5°C) as compared to those acclimated to warm temperature (25°C). Micrographs of red and white muscle from these animals have been analyzed quantitatively for the stereological parameters Vv (volume density), Sv (surface density), and S/V (specific surface); and diffusion distances between mitochondria have been calculated as the harmonic mean of spacings between clusters of mitochondria (τh). The most dramatic differences occur in Vv, Sv, and τh of red muscle, Vv and Sv being significantly greater in cold-acclimated animals and τh being smaller. In white muscle, Vv is significantly greater for cold-acclimated animals than warm-acclimated animals, but other parameters are not significantly different. Using our values of Sv as estimates of the surface area through which exchange of metabolites occurs and our values of τh as estimates of the distance over which diffusion occurs, we calculate that the diffusivity constant in the one-dimensional diffusion equation for metabolites may be reduced in cold-acclimated animals to as low as 0.29 that of warm-acclimated animals while still maintaining absolute rates of diffusive flux between cytoplasm and mitochondria. It appears reasonable to assume that cold-induced rises in the concentration of enzymes in fish muscle reflect changes in organellar densities–changes which may serve primarily to ameliorate the effect of temperature on diffusive exchange between mitochondria and cytoplasm rather than solely to overcome catalytic limitation as is widely assumed.

119 citations

"Does intracellular metabolite diffu..." refers background in this paper

  • ...…reasoning that cellular dimensions tend to be modest (muscle fibers generally range from 10 to 100·µm in diameter; Russell et al., 2000) and intracellular diffusion distances between mitochondria are typically very short in both aerobic and anaerobic skeletal muscle (e.g. Tyler and Sidell, 1984)....

    [...]

Journal Article•DOI•
In vivo 31P-NMR diffusion spectroscopy of ATP and phosphocreatine in rat skeletal muscle

[...]

Robin A. de Graaf1, Arnaud van Kranenburg1, Klaas Nicolay1•
Utrecht University1
01 Apr 2000-Biophysical Journal
TL;DR: The modelling suggests that the in vivo restriction of ATP and PCr diffusion is not imposed by the sarcolemma but by other, intracellular structures with an overall cylindrical orientation.

119 citations

Journal Article•DOI•
Compartmentalized energy transfer in cardiomyocytes: use of mathematical modeling for analysis of in vivo regulation of respiration.

[...]

M.K. Aliev, V.A. Saks
01 Jul 1997-Biophysical Journal
TL;DR: The mathematical model developed can be used as a basis for further quantitative analyses of energy fluxes in the cell and their regulation, particularly by adding modules for adenylate kinase, the glycolytic system, and other reactions of energy metabolism of the cell.

108 citations

"Does intracellular metabolite diffu..." refers background in this paper

  • ...aerobic metabolism found theoretical evidence for concentration gradients in high-energy phosphate molecules during steady-state contraction in muscle (Mainwood and Rakusan, 1982; Meyer et al., 1984; Hubley et al., 1997; Aliev and Saks, 1997; Kemp et al., 1998; Vendelin et al., 2000; Saks et al., 2003)....

    [...]

  • ...…metabolism found theoretical evidence for concentration gradients in high-energy phosphate molecules during steady-state contraction in muscle (Mainwood and Rakusan, 1982; Meyer et al., 1984; Hubley et al., 1997; Aliev and Saks, 1997; Kemp et al., 1998; Vendelin et al., 2000; Saks et al., 2003)....

    [...]

Journal Article•DOI•
Calculated intra- and extracellular PO2 gradients in heavily working red muscle.

[...]

K. Groebe1, G. Thews1•
University of Rochester1
01 Jul 1990-American Journal of Physiology-heart and Circulatory Physiology
TL;DR: A recently introduced three-dimensional analytical model of O 2 diffusion to heavily working muscle that considers myoglobin-facilitated O2 diffusion inside the muscle fiber and a carrier-free layer separating erythrocytes and fiber is able to furnish the following new insights in O2 supply to red muscle at high performance.
Abstract: A recently introduced three-dimensional analytical model of O2 diffusion to heavily working muscle that considers myoglobin-facilitated O2 diffusion inside the muscle fiber and a carrier-free layer...

98 citations

"Does intracellular metabolite diffu..." refers background in this paper

  • ...The lack of myoglobin (Mb) in the light levator muscle amplifies this effect, since Mb-less fibers require a higher extracellular PO∑ to support a given rate of O2 consumption compared with muscles with Mb (Groebe and Thews, 1990)....

    [...]

Related Papers (5)
A model for intracellular energy transport.

[...]

01 Jan 1982-Canadian Journal of Physiology and Pharmacology
G. W. Mainwood, K. Rakusan
The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle.

[...]

15 Oct 2007-The Journal of Experimental Biology
Stephen T. Kinsey, Kristin M. Hardy, Bruce R. Locke
A simple analysis of the "phosphocreatine shuttle"

[...]

01 May 1984-American Journal of Physiology-cell Physiology
R. A. Meyer, H. L. Sweeney, Martin J. Kushmerick
Diffusional anisotropy is induced by subcellular barriers in skeletal muscle.

[...]

01 Feb 1999-NMR in Biomedicine
Stephen T. Kinsey, Bruce R. Locke, Bruce R. Locke, Brigita Penke, Timothy S. Moerland 
Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective.

[...]

01 Aug 2003-The Journal of Experimental Biology
Ian A. Johnston, Daniel Alfredo Fernández, Jorge Calvo, Vera L. A. Vieira, Anthony W. North, Marguerite Abercromby, Theodore Garland