Muscle fibers bear a larger fraction of passive muscle tension in frogs compared with mice

Abstract

Differences in passive muscle mechanical properties between amphibians and mammals have led to differing hypotheses on the functional role of titin in skeletal muscle. Early studies of frog muscle clearly demonstrated intracellular load bearing by titin, but more recent structural and biological studies in mice have shown that titin may serve other functions. Here, we present biomechanical studies of isolated frog and mouse fibers, and fiber bundles to compare the relative importance of intracellular versus extracellular load bearing in these species. Mouse bundles exhibited increased modulus compared with fibers on the descending limb of the length-tension curve, reaching a 2.4-fold elevation at the longest sarcomere lengths. By contrast, frog fibers and bundles had approximately the same modulus at all sarcomere lengths tested. These findings suggest that in the mouse, both muscle fibers and the ECM are involved in bearing whole muscle passive tension, which is distinct from the load bearing process in frog muscle, where titin bears the majority of whole muscle passive tension.

Keywords: Comparative biomechanics; Muscle mechanics; Passive stiffness; Titin.

Fig. 1.

Raw stress–sarcomere length curves from frog and mouse muscle. Stress versus length curves for frog and mouse single muscle fibers (A) and fiber bundles (B). Representative data from one experiment. Data are plotted in terms of sarcomere length to enable comparison across species and on different portions of the sarcomere length–tension curves.

Fig. 2.

Tangent modulus for frog and mouse fibers and bundles as a function of sarcomere length. Tangent modulus for fibers and bundles in frog (A) and mouse (B) as a function of sarcomere length. Tangent moduli were calculated at sarcomere lengths across the plateau and descending limb of the length-tension curve for each species in 0.25 µm increments (means±s.e.m., n=9–17 per group). Vertical dotted line is placed at the species-specific 75% point on the descending limb and this value is plotted in C. (C) Modulus values from frog and mouse single fibers and fiber bundles at the sarcomere length denoted by vertical dotted lines in A and B. Two-way ANOVA found a significant species×size scale interaction (P<0.01) explicitly demonstrating a species-dependent effect on scaling of passive tension (means±s.e.m., n=9–17 per group).

Fig. 3.

Fraction of passive load borne by frog and mouse muscle fibers. Values are predicted by the rule of mixtures assuming these muscles are a continuous composite of 90% unidirectional fibers and 10% extracellular matrix (Meyer and Lieber, 2012) using the fiber and bundle moduli presented in this report.