Allometric scaling in centrarchid fish: origins of intra- and inter-specific variation in oxidative and glycolytic enzyme levels in muscle

Davies, Rhiannon; Moyes, Christopher D.

doi:10.1242/jeb.003897

Cited by 43 publications

(38 citation statements)

References 33 publications

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“…Somero and Childress (36) were the first to note the reciprocal pattern in scaling of mitochondrial and glycolytic enzymes, the same relationship observed in our study and others (10,15). It is unclear whether this pattern arises as a result of independent regulatory pathways or a single pathway with reciprocal effects.…”

Section: Reciprocal Regulation Of Oxphos and Glycolytic Genessupporting

confidence: 80%

“…Thus, consideration of myonuclear content reduced the differences between muscles of a species, but not differences between species. Previous studies with fish reached the same conclusion: expressing mitochondrial enzyme activities relative to DNA content largely negated differences in mitochondrial enzymes in relation to size (10) and between fibers (8) but did not affect differences between species (8).…”

Section: Scaling Of Metabolic Enzyme Activitiesmentioning

confidence: 60%

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Origins of interspecies variation in mammalian muscle metabolic enzymes

Kocha

Genge

Moyes

2011

Physiological Genomics

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Kocha KM, Genge CE, Moyes CD. Origins of interspecies variation in mammalian muscle metabolic enzymes. Physiol Genomics 43: 873-883, 2011. First published May 17, 2011 doi:10.1152/physiolgenomics.00025.2011.-Do the transcriptional mechanisms that control an individual's mitochondrial content, PGC1␣ (peroxisome proliferator-activated receptor ␥ coactivator-1␣) and NRF1 (nuclear respiratory factor-1), also cause differences between species? We explored the determinants of cytochrome c oxidase (COX) activities in muscles from 12 rodents differing 1,000-fold in mass. Hindlimb muscles differed in scaling patterns from isometric (soleus, gastrocnemius) to allometric (tibialis anterior, scaling coefficient ϭ Ϫ0.16). Consideration of myonuclear domain reduced the differences within species, but interspecies differences remained. For tibialis anterior, there was no significant scaling relationship in mRNA/g for COX4-1, PGC1␣, or NRF1, yet COX4-1 mRNA/g was a good predictor of COX activity (r 2 ϭ 0.55), PGC1␣ and NRF1 mRNA correlated with each other (r 2 ϭ 0.42), and both could predict COX4-1 mRNA (r 2 ϭ 0.48 and 0.52) and COX activity (r 2 ϭ 0.55 and 0.49). This paradox was resolved by multivariate analysis, which explained 90% of interspecies variation, about equally partitioned between mass effects and PGC1␣ (or NRF1) mRNA levels, independent of mass. To explore the determinants of PGC1␣ mRNA, we analyzed 52 mammalian PGC1␣ proximal promoters and found no size dependence in regulatory element distribution. Likewise, the activity of PGC1␣ promoter reporter genes from 30 mammals showed no significant relationship with body mass. Collectively, these studies suggest that not all muscles scale equivalently, but for those that show allometric scaling, transcriptional regulation of the master regulators, PGC1␣ and NRF1, does not account for scaling patterns, though it does contribute to interspecies differences in COX activities independent of mass.scaling; cytochrome c oxidase; peroxisome proliferator-activated receptor ␥ coactivator-1␣; nuclear respiratory factor-1; mitochondria; lactate dehydrogenase ALL ANIMALS HAVE THE NEED to alter muscle mitochondrial content during development and in response to physiological and environmental challenges. Central to this remodeling process are transcriptional master regulators, namely peroxisome proliferator-activated receptor ␥ coactivator-1␣ (PGC1␣) and nuclear respiratory factor-1 (NRF1) (20,33,34). Mitochondrial biogenesis requires the coordination of hundreds of nuclear genes encoding mitochondrial structural and enzymatic proteins, including the proteins that control replication, transcription, and translation of mitochondrial DNA. This onerous task is mediated by the coactivator PGC1␣, which regulates suites of nuclear-encoded metabolic genes through direct and indirect association with DNA-binding transcription factors. Central to control of genes in oxidative phosphorylation are NRF1, NRF2, and nuclear hormone receptors [e.g., peroxisome proliferator-activated receptor (PPAR...

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Section: Reciprocal Regulation Of Oxphos and Glycolytic Genessupporting

confidence: 80%

Section: Scaling Of Metabolic Enzyme Activitiesmentioning

confidence: 60%

Origins of interspecies variation in mammalian muscle metabolic enzymes

Kocha

Genge

Moyes

2011

Physiological Genomics

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“…Subsequent studies have confirmed this general pattern, although interspecific differences are influenced by life history, activity levels and Integrated muscle response to growth phylogenetic relationships (Childress and Somero, 1990). Hence, LDH and PK showed positive allometry (b>0) in white muscle of many fishes (Burness et al, 1999;Davies and Moyes, 2007;Ewart et al, 1988;Martinez et al, 2000;Sullivan and Somero, 1983;Torres and Somero, 1988), whereas in striped bass positive scaling was found in small and medium, but not large (>1000g) fish (Norton et al, 2000). The same trend was also demonstrated in the present study in which LDH scaled with a similar exponent (b0.342) to that previously reported (b0.31) (Norton et al, 2000), although PK had weaker positive allometry (b0.110 and b0.56, respectively).…”

Section: Metabolismmentioning

confidence: 83%

“…Importantly, CPK also displayed positive allometry in trout white muscle (Burness et al, 1999) and in the present study, where the scaling exponent showed the strongest positive allometry (P<0.0001). By contrast, the oxidative enzymes COX and CS displayed negative allometry in fish white muscle (Davies and Moyes, 2007;Martinez et al, 2000;Torres and Somero, 1988;Tripathi and Verma, 2004). However, CS displayed no size dependence in other species (Burness et al, 1999;Torres and Somero, 1988).…”

Section: Metabolismmentioning

confidence: 90%

Allometry of skeletal muscle fine structure allows maintenance of aerobic capacity during ontogenetic growth

Young

Egginton

2009

Journal of Experimental Biology

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SUMMARYControversy exists over the scaling of oxygen consumption with body mass in vertebrates. A combination of biochemical and structural analyses were used to examine whether individual elements influencing oxygen delivery and demand within locomotory muscle respond similarly during ontogenetic growth of striped bass. Mass-specific metabolic enzyme activity confirmed that glycolytic capacity scaled positively in deep white muscle (regression slope, b0.1 to 0.8) over a body mass range of ~20-1500g, but only creatine phosphokinase showed positive scaling in lateral red muscle (b0.5). Although oxidative enzymes showed negative allometry in red muscle (b-0.01 to -0.02), mass-specific myoglobin content scaled positively (b0.7). Capillary to fibre ratio of red muscle was higher in larger (1.42±0.

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“…Thus, standard ANCOVAs are still commonly used in scaling studies (e.g. Niven and Scharlemann, 2005;Davies and Moyes, 2007;Snelling et al, 2011;Xu et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Differences in scaling and morphology between lumbricid earthworm ecotypes

Kurth¹,

Kier

2015

Journal of Experimental Biology

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Many soft-bodied invertebrates use a flexible, fluid-filled hydrostatic skeleton for burrowing. The aim of our study was to compare the scaling and morphology between surface-dwelling and burrowing earthworm ecotypes to explore the specializations of non-rigid musculoskeletal systems for burrowing locomotion. We compared the scaling of adult lumbricid earthworms across species and ecotypes to determine whether linear dimensions were significantly associated with ecotype. We also compared the ontogenetic scaling of a burrowing species, Lumbricus terrestris, and a surface-dwelling species, Eisenia fetida, using glycol methacrylate histology. We show that burrowing species are longer, thinner and have higher length-todiameter ratios than non-burrowers, and that L. terrestris is thinner for any given body mass compared with E. fetida. We also found differences in the size of the musculature between the two species that may correlate with surface crawling or burrowing. Our results suggest that adaptations to burrowing for soft-bodied animals include a disproportionately thin body and strong longitudinal muscles.

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Allometric scaling in centrarchid fish: origins of intra- and inter-specific variation in oxidative and glycolytic enzyme levels in muscle

Cited by 43 publications

References 33 publications

Origins of interspecies variation in mammalian muscle metabolic enzymes

Origins of interspecies variation in mammalian muscle metabolic enzymes

Allometry of skeletal muscle fine structure allows maintenance of aerobic capacity during ontogenetic growth

Differences in scaling and morphology between lumbricid earthworm ecotypes

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