Abstract
Introduction: The passive mechanical behavior of skeletal muscle represents both important and generally underappreciated biomechanical properties with little attention paid to their trainability. These experiments were designed to gain insight into the trainability of muscle passive mechanical properties in both single fibers and fiber bundles. Methods: Rats were trained in two groups: 4 weeks of either uphill (UH) or downhill (DH) treadmill running; with a third group as sedentary control. After sacrifice, the soleus (SOL), extensor digitorum longus (EDL), and vastus intermedius (VI) were harvested. One hundred seventy-nine bundles and 185 fibers were tested and analyzed using a cumulative stretch-relaxation protocol to determine the passive stress and elastic modulus. Titin isoform expression was analyzed using sodium dodecyl sulfate vertical agarose gel electrophoresis (SDS-VAGE). Results: Single fibers: passive modulus and stress were greater for the EDL at sarcomere lengths (SLs) ≥ 3.7 μm (modulus) and 4.0 μm (stress) with DH training compared to UH training and lesser for the SOL (SLs ≥ 3.3 μm) with DH training compared with control; there was no effect of UH training. Vastus intermedius was not affected by either training protocol. Fiber bundles: passive modulus and stress were greater for the EDL at SLs ≥ 2.5 μm (modulus) and 3.3 μm (stress) in the DH training group as compared with control, while no affects were observed in either the SOL or VI for either training group. No effects on titin isoform size were detected with training. Conclusion: This study demonstrated that a trainability of passive muscle properties at both the single fiber and fiber bundle levels was not accompanied by any detectable changes to titin isoform size.
Highlights
The passive mechanical behavior of skeletal muscle represents both important and generally underappreciated biomechanical properties with little attention paid to their trainability
At the whole muscle level, it is generally recognized that the extracellular matrix has a large role in dictating muscle passive properties (Prado et al, 2005; Gillies and Lieber, 2011; Meyer and Lieber, 2018; Ward et al, 2020); others have argued that the intracellular protein titin is predominantly responsible for whole muscle passive stiffness at short (2.4–2.7 μm) sarcomere lengths (SLs; Brynnel et al, 2019)
There was an effect of training group on the extensor digitorum longus (EDL) and SOL but not the vastus intermedius (VI) (Figure 2)
Summary
The passive mechanical behavior of skeletal muscle represents both important and generally underappreciated biomechanical properties with little attention paid to their trainability. At the single fiber level, it is generally thought that titin is primarily responsible for passive stiffness and tension (Wang et al, 1979; Horowits et al, 1986; Trombitás et al, 1995; Granzier et al, 1996, 2003; Linke et al, 1996; Kontrogianni-Konstantopoulos et al, 2009); the contribution of other intra/extra cellular proteins should not be excluded (Ramsey and Street, 1940; Rapoport, 1973; Tidball, 1986; Shah et al, 2004; Noonan et al, 2020a) While these mechanistic studies have aimed to elucidate the relative roles of the intracellular and extracellular matrix proteins in dictating passive muscle properties, little attention has been paid to the trainability of skeletal muscle passive properties at both the single fiber and fiber bundle levels
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