Light microscopy and image analysis of thin filament lengths utilizing dual probes on beef, chicken, and rabbit myofibrils1

Ringkob, T.P.; Swartz, Darl R.; Greaser, Marion L.

doi:10.2527/2004.8251445x

Cited by 34 publications

(16 citation statements)

References 11 publications

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“…Given the mean sarcomere length of 1.97μm reported by Mathieu-Costello et al (Mathieu-Costello et al, 1992a), we conclude that the thin filament length in their report likely represents the combined I-band length from two adjacent sarcomeres and the intervening Z-band length (I-Z-I length). Reported thin filament lengths in other vertebrate muscles are longer: they average ~1.31μm in several bovine muscles, 1.16μm in rabbit psoas muscle and 1.05μm in chicken pectoralis muscle (Ringkob et al, 2004), and ~1.03μm in frog leg and chicken pectoralis muscle [half of the I-Z-I length reported by Page and Huxley (Page and Huxley, 1963)]. The short thin filament length in hummingbird pectoralis fibers correlates well with the very short SL null values in bird pectoralis fibers in the present study.…”

Section: Discussionmentioning

confidence: 99%

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Reiser

Welch

Suarez

et al. 2013

Journal of Experimental Biology

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SUMMARYHummingbird flight muscle is estimated to have among the highest mass-specific power output among vertebrates, based on aerodynamic models. However, little is known about the fundamental contractile properties of their remarkable flight muscles. We hypothesized that hummingbird pectoralis fibers generate relatively low force when activated in a tradeoff for high shortening speeds associated with the characteristic high wingbeat frequencies that are required for sustained hovering. Our objective was to measure maximal force-generating ability (maximal force/cross-sectional area, P o /CSA) in single, skinned fibers from the pectoralis and supracoracoideus muscles, which power the wing downstroke and upstroke, respectively, in hummingbirds (Calypte anna) and in another similarly sized species, zebra finch (Taeniopygia guttata), which also has a very high wingbeat frequency during flight but does not perform a sustained hover. Mean P o /CSA in hummingbird pectoralis fibers was very low -1.6, 6.1 and 12.2kNm -2 , at 10, 15 and 20°C, respectively. P o /CSA in finch pectoralis fibers was also very low (for both species, ~5% of the reported P o /CSA of chicken pectoralis fast fibers at 15°C). Q 10-force (force generated at 20°C/force generated at 10°C) was very high for hummingbird and finch pectoralis fibers (mean=15.3 and 11.5, respectively) compared with rat slow and fast fibers (1.8 and 1.9, respectively). P o /CSA in hummingbird leg fibers was much higher than in pectoralis fibers at each temperature, and the mean Q 10-force was much lower. Thus, hummingbird and finch pectoralis fibers have an extremely low force-generating ability compared with other bird and mammalian limb fibers, and an extremely high temperature dependence of force generation. However, the extrapolated maximum force-generating ability of hummingbird pectoralis fibers in vivo (~48kNm -2 ) is substantially higher than the estimated requirements for hovering flight of C. anna. The unusually low P o /CSA of hummingbird and zebra finch pectoralis fibers may reflect a constraint imposed by a need for extremely high contraction frequencies, especially during hummingbird hovering. Supplementary material available online at

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Section: Discussionmentioning

confidence: 99%

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Reiser

Welch

Suarez

et al. 2013

Journal of Experimental Biology

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“…Whereas thick filament lengths are essentially constant in all skeletal muscles and species examined (∼1.65 µm), thin filament lengths vary substantially across muscles and vertebrate species (0.95-1.40 µm) (Castillo et al, 2009;Gokhin et al, 2012Gokhin et al, , 2010Granzier et al, 1991;Ringkob et al, 2004). Thin filament lengths are remarkably plastic during normal postnatal skeletal muscle development and aging (Gokhin et al, 2014a) but can become misspecified in some congenital myopathies.…”

Section: Introductionmentioning

confidence: 99%

Tropomodulin1 directly controls thin filament length in both wild-type and tropomodulin4-deficient skeletal muscle

et al. 2015

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The sarcomeric tropomodulin (Tmod) isoforms Tmod1 and Tmod4 cap thin filament pointed ends and functionally interact with the leiomodin (Lmod) isoforms Lmod2 and Lmod3 to control myofibril organization, thin filament lengths, and actomyosin crossbridge formation in skeletal muscle fibers. Here, we show that Tmod4 is more abundant than Tmod1 at both the transcript and protein level in a variety of muscle types, but the relative abundances of sarcomeric Tmods are muscle specific. We then generate Tmod4 −/− mice, which exhibit normal thin filament lengths, myofibril organization, and skeletal muscle contractile function owing to compensatory upregulation of Tmod1, together with an Lmod isoform switch wherein Lmod3 is downregulated and Lmod2 is upregulated. However, RNAi depletion of Tmod1 from either wild-type or Tmod4 −/− muscle fibers leads to thin filament elongation by ∼15%. Thus, Tmod1 per se, rather than total sarcomeric Tmod levels, controls thin filament lengths in mouse skeletal muscle, whereas Tmod4 appears to be dispensable for thin filament length regulation. These findings identify Tmod1 as the key direct regulator of thin filament length in skeletal muscle, in both adult muscle homeostasis and in developmentally compensated contexts.

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“…10). Values for sarcomere number (S n ) and normalized fiber length (L fn ) were then calculated for the isolated bundles according to the following equations: and where L so represents optimal sarcomere length for each particular species, obtained from the literature where available or estimated based on values from similar species (Bang et al, 2006;Burkholder and Lieber, 2001;Ringkob et al, 2004). Normalized muscle length (L mn ) was derived similarly to normalized muscle fiber length.…”

Section: Research Articlementioning

confidence: 99%

Comparison of rotator cuff muscle architecture among humans and selected vertebrate species

Mathewson

Kwan

Eng

et al. 2013

Journal of Experimental Biology

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In this study, we compare rotator cuff muscle architecture of typically used animal models with that of humans and quantify the scaling relationships of these muscles across mammals. The four muscles that correspond to the human rotator cuff -supraspinatus, infraspinatus, subscapularis and teres minor -of 10 commonly studied animals were excised and subjected to a series of comparative measurements. When body mass among animals was regressed against physiological cross-sectional area, muscle mass and normalized fiber length, the confidence intervals suggested geometric scaling but did not exclude other scaling relationships. Based on the architectural difference index (ADI), a combined measure of fiber length-to-moment arm ratio, fiber length-to-muscle length ratio and the fraction of the total rotator cuff physiological cross-sectional area contributed by each muscle, chimpanzees were found to be the most similar to humans (ADI=2.15), followed closely by capuchins (ADI=2.16). Interestingly, of the eight non-primates studied, smaller mammals such as mice, rats and dogs were more similar to humans in architectural parameters compared with larger mammals such as sheep, pigs or cows. The force production versus velocity trade-off (indicated by fiber length-to-moment arm ratio) and the excursion ability (indicated by fiber length-to-muscle length ratio) of humans were also most similar to those of primates, followed by the small mammals. Overall, primates provide the best architectural representation of human muscle architecture. However, based on the muscle architectural parameters of non-primates, smaller rather than larger mammals may be better models for studying muscles related to the human rotator cuff.

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Light microscopy and image analysis of thin filament lengths utilizing dual probes on beef, chicken, and rabbit myofibrils1

Cited by 34 publications

References 11 publications

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Tropomodulin1 directly controls thin filament length in both wild-type and tropomodulin4-deficient skeletal muscle

Comparison of rotator cuff muscle architecture among humans and selected vertebrate species

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