Functional and Evolutionary Implications of the Distribution of Phosphagens in Primitive-Type Spermatozoa

Ellington, W. Ross; Kinsey, Stephen T.

doi:10.2307/1543138

Cited by 19 publications

(10 citation statements)

References 46 publications

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“…It was therefore surprising that the model results did not indicate a limitation of aerobic flux by intracellular metabolite diffusion, considering that AP and arginine, which are the key diffusing species (Ellington and Kinsey, 1998), can traverse the λ/2 distance in small fibers in <30·ms, while needing 16·000 times longer (nearly 8·min) to cover the distance modeled in large fibers (Kinsey and Moerland, 2002). Implicit in this finding is that kinetic expressions alone (no diffusion component) would have been nearly sufficient to simulate the differences between small and large fibers in Fig.·3.…”

Section: Discussionmentioning

confidence: 99%

“…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.g. Nevo and Rikmenspoel, 1969;Tombes and Shapiro, 1985;Van Dorsten et al, 1997;Ellington and Kinsey, 1998). However, it is possible that in most cases neither intracellular metabolite diffusion nor sarcolemmal O 2 flux limit aerobic metabolism per se, but even if this is true it is still likely that the interaction between diffusive processes and ATP demand has shaped the evolution of cellular design.…”

Section: Discussionmentioning

confidence: 99%

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

Kinsey

Pathi

Hardy

et al. 2005

Journal of Experimental Biology

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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

Kinsey

Pathi

Hardy

et al. 2005

Journal of Experimental Biology

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“…That is, since the high-energy phosphate on PCr or AP is rapidly exchanged with that on ATP, these phosphagens can be thought of as carriers of high energy phosphates that supplement the direct diffusion of ATP (Fig.·2). In fact, since PCr and AP occur in higher concentrations and have higher diffusion coefficients than ATP, the vast majority of high-energy phosphate transport from mitochondria to cellular ATPases in muscle occurs by the diffusion of phosphagen, rather than directly as ATP (Fig.·2) (Meyer et al, 1984;Ellington and Kinsey, 1998).…”

Section: Energy Transport In Muscle Fibersmentioning

confidence: 99%

“…Short diffusion distances are necessary to facilitate both rapid O 2 flux to mitochondria and ATP flux from mitochondria to sites of ATP demand. Thus, a likely functional consequence of excessive cell size is a reduced capacity for critical oxidative metabolic processes (Egginton and Sidell, 1989;Egginton et al, 2000;Boyle et al, 2003;Johnston et al, 2003a;Johnston et al, 2004;Kinsey et al, 2005; (Ellington and Kinsey, 1998), and declines to a steady state value that is lower for radial diffusion, due to the presence of intracellular barriers such as the sarcoplasmic reticulum [data from Kinsey et al (Kinsey et al, 1999) ©1999, John Wiley and Sons, Ltd, reproduced with permission]. (C) Hindered radial diffusion in muscle (red line) increases the time required for PCr to diffuse a given distance compared to diffusion in water (broken black line).…”

Section: Muscle Fiber Size Diversitymentioning

confidence: 99%

The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle

Kinsey

Hardy

Locke

2007

Journal of Experimental Biology

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SUMMARY A fundamental principle of physiology is that cells are small in order to minimize diffusion distances for O2 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 O2 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.

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“…The reaction is central to short-term temporal energy buffering (1,2) as well as in spatial shuttling of energy from production to consumption sites (3)(4)(5). A wide array of endergonic processes is driven by nucleotide hydrolysis, from motion in molecular motors, active transport, and synthetic metabolism to signal transduction.…”

mentioning

confidence: 99%

The Structure of Lombricine Kinase

Bush

Kirillova

Clark

et al. 2011

Journal of Biological Chemistry

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Lombricine kinase is a member of the phosphagen kinase family and a homolog of creatine and arginine kinases, enzymes responsible for buffering cellular ATP levels. Structures of lombricine kinase from the marine worm Urechis caupo were determined by x-ray crystallography. One form was crystallized as a nucleotide complex, and the other was substrate-free. The two structures are similar to each other and more similar to the substrate-free forms of homologs than to the substrate-bound forms of the other phosphagen kinases. Active site specificity loop 309 -317, which is disordered in substrate-free structures of homologs and is known from the NMR of arginine kinase to be inherently dynamic, is resolved in both lombricine kinase structures, providing an improved basis for understanding the loop dynamics. Phosphagen kinases undergo a segmented closing on substrate binding, but the lombricine kinase ADP complex is in the open form more typical of substrate-free homologs. Through a comparison with prior complexes of intermediate structure, a correlation was revealed between the overall enzyme conformation and the substrate interactions of His 178 . Comparative modeling provides a rationale for the more relaxed specificity of these kinases, of which the natural substrates are among the largest of the phosphagen substrates.Lombricine, arginine, and creatine kinases (EC 2.7.3) are homologous phosphagen kinases that catalyze the buffering of cellular ATP levels through phosphoryl transfer to/from their respective guanidino-containing substrates. The reaction is central to short-term temporal energy buffering (1, 2) as well as in spatial shuttling of energy from production to consumption sites (3-5). A wide array of endergonic processes is driven by nucleotide hydrolysis, from motion in molecular motors, active transport, and synthetic metabolism to signal transduction. Thus, the maintenance of a constant ATP/ADP ratio, displaced far from thermodynamic equilibrium in the face of high and variable rates of ATP turnover, is crucial for cellular homeostasis (2).Different organisms use different phosphagen substrates, usually only one and each with its own specific phosphagen kinase ( Fig. 1) (2). Lombricine kinase, as well as taurocyamine kinase and glycocyamine kinase, is found exclusively in annelids and allied groups (2). Phylogenetic analyses and studies of the intron/exon organization of the genes of these phosphagen kinases unique to annelids have shown that they are more closely related to creatine kinases (with which they share 50 -60% sequence identity) than typical monomeric arginine kinases such as that from the horseshoe crab (6) (40% sequence identity). Annelids are more diverse in their choice of phosphagen, and the substrate specificities of the corresponding kinases are often lower (6).Structural work has concentrated on the presumptive ancestral arginine kinase and the vertebrate creatine kinase (7, 8), but sequence alignment suggests that subunit fold, if not quaternary structure, is conserved across the fa...

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Functional and Evolutionary Implications of the Distribution of Phosphagens in Primitive-Type Spermatozoa

Cited by 19 publications

References 46 publications

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

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

The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle

The Structure of Lombricine Kinase

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