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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.

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Citations
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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

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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)....

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

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  • ...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)....

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

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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....

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

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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)....

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  • ...…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)....

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  • ...…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)....

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  • ...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....

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  • ...…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…...

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

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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)....

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  • ...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)....

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  • ...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)....

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  • ...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)....

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  • ...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)....

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Journal Article•DOI•
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Journal Article•DOI•
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Marko Vendelin, Olav Kongas, Valdur Saks1•
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Abstract: The purpose of this study is to investigate theoretically which intracellular factors may be important for regulation of mitochondrial respiration in working heart cells in vivo. We have developed ...

160 citations

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

  • ...…of ATP utilization, such as in some muscle fibers with a higher aerobic capacity than examined here (Meyer et al., 1984; Stokes and Josephson, 1992; Vendelin et al., 2000; Saks et al., 2003; Suarez, 2003) or in the flagellum of spermatozoa, which has been the subject of many reaction–diffusion…...

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  • ...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)....

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  • ...These are likely to include systems with relatively high rates of ATP production/consumption and distant sites of ATP utilization, such as in some muscle fibers with a higher aerobic capacity than examined here (Meyer et al., 1984; Stokes and Josephson, 1992; Vendelin et al., 2000; Saks et al., 2003; Suarez, 2003) or in the flagellum of spermatozoa, which has been the subject of many reaction–diffusion analyses (e....

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  • ...…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)....

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Journal Article•DOI•
The Quest for Speed: Muscles Built for High-Frequency Contractions

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Lawrence C. Rome1, Stan L. Lindstedt•
University of Pennsylvania1
01 Dec 1998-Physiology
TL;DR: Vertebrate sound-producing muscles can contract at frequencies greater than 100 Hz, a feat impossible in locomotory muscles, not accomplished by unique proteins or structures but by qualitative shifts in isoforms and quantitative reapportionment of structures.
Abstract: Vertebrate sound-producing muscles can contract at frequencies greater than 100 Hz, a feat impossible in locomotory muscles. This is not accomplished by unique proteins or structures but by qualitative shifts in isoforms and quantitative reapportionment of structures. Speed comes with costs and trade-offs, however, that restrict how a muscle can be used.

158 citations

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

  • ...Rome and Lindstedt (1998) have characterized the manner in which muscle fiber volume is devoted to metabolic or contractile machinery in relation to muscle function....

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Journal Article•DOI•
Design of the mammalian respiratory system. IX. Functional and structural limits for oxygen flow

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E R Weibel1, E R Weibel2, C. R. Taylor2, C. R. Taylor1, Peter Gehr1, Peter Gehr2, H Hoppeler2, H Hoppeler1, O. Mathieu1, O. Mathieu2, Gmo Maloiy1, Gmo Maloiy2 •
University of Bern1, Harvard University2
01 Apr 1981-Respiration Physiology
TL;DR: The accumulated evidence supports the principle of symmorphosis, i.e. of morphogenesis adapted to functional needs at all organizational levels considered, although the models used for structure-function correlation need further refinement.

155 citations

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