Effect of exercise training on passive stiffness in locomotor skeletal muscle: role of extracellular matrix

Abstract

The purpose of this study was to evaluate the effect of endurance exercise training on both locomotor skeletal muscle collagen characteristics and passive stiffness properties in the young adult and old rat. Young (3-mo-old) and senescent (23-mo-old) male Fischer 344 rats were randomly assigned to either a control or exercise training group [young control (YC), old control (OC), young trained (YT), old trained (OT)]. Exercise training consisted of treadmill running at approximately 70% of maximal oxygen consumption (45 min/day, 5 days/wk, for 10 wk). Passive stiffness (stress/strain) of the soleus (Sol) muscle from all four groups was subsequently measured in vitro at 26 degreesC. Stiffness was significantly greater for Sol muscles in OC rats compared with YC rats, but in OT rats exercise training resulted in muscles with stiffness characteristics not different from those in YC rats. Sol muscle collagen concentration and the level of the nonreducible collagen cross-link hydroxylysylpyridinoline (HP) significantly increased from young adulthood to senescence. Although training had no effect on Sol muscle collagen concentration in either age group, it resulted in a significant reduction in the level of Sol muscle HP in OT rats. In contrast, exercise had no effect on HP in the YT animals. These findings indicate that 10 wk of endurance exercise significantly alter the passive viscoelastic properties of Sol muscle in old but not in young adult rats. The coincidental reduction in the principal collagen cross-link HP also observed in response to training in OT muscle highlights the potential role of collagen in influencing passive muscle viscoelastic properties.

Effects of early-stage aging on locomotor dynamics and hindlimb muscle force production in the rat

“…Across all gaits, stride lengths are significantly shorter in aged mammals (Bassey et al, 1992;Brown et al, 2003), and these shorter stride lengths are indicative of reduced ranges of joint motion with age (Shaffer and Harrison, 2007). Whether this is caused by age-related increases in muscle stiffness or joint capsule stiffness could not be assessed in this study, but both factors are likely to be influential in reducing the stride lengths (Gosselin et al, 1998). Additionally, the increased kyphosis of the spines in the aged rats would reduce the functional trunk length -and thus stride lengthif immobilized by stiffened ligaments and joint capsules.…”

Diving into old age: muscular senescence in a large-bodied, long-lived mammal, the Weddell seal (Leptonychotes weddellii)

“…Muscle stiffening due to heightened collagen content or stability has been widely reported in terrestrial mammals (Mohan and Radha, 1980;Kovanen and Suominen, 1989;Gosselin et al, 1998). Such collagen remodeling in aged muscle (mediated by transforming growth factor-beta) has also been documented subsequent to mechanical, cytokine or oxidative tissue stress (Border and Noble, 1994;Cannon and St Pierre, 1998).…”

“…The mechanical properties of this ECM affect those of muscle as well, because the force generated by contractile tissue must overcome internal work created by connective tissue components in order to generate movement (Kjaer, 2004). Importantly, collagen content and collagen cross-linking increase with advancing age in rodents and humans (Mays et al, 1988;Kovanen and Suominen, 1989;Gosselin et al, 1998).…”

“…Exercise training, injury, disease and aging are all associated with some degree of ECM remodeling (Mohan and Radha, 1980;Marshall et al, 1989;Williams et al, 1999;Miller et al, 2001;Mackey et al, 2004). Detectable signs of normal aging in skeletal muscle include increased deposition of total collagen (Mays et al, 1988;Kovanen and Suominen, 1989;Gosselin et al, 1998) resulting from increased resistance to collagen degradation and turnover (Mohan and Radha, 1980), as well as a relatively greater contribution of type I, at the expense of type III, to the collagen pool (Mays et al, 1988;Kovanen and Suominen, 1989). Both developments are expected to compromise the internal work capability of skeletal muscle with age.…”

Life-long endurance running is associated with reduced glycation and mechanical stress in connective tissue

“…However, if long-term physical activity can modify the accumulation of enzymatic and AGE cross-links in human tendon with aging has never been investigated. It appears that endurance training in aging animals yield a stronger and more compliant tendon (Gosselin et al 1998;Viidik et al 1996;Simonsen et al 1995;LaCroix et al 2013;Nielsen et al 1998), but this remains to be confirmed in a human model. Furthermore, at the microstructural level, the size and/or density of tendon collagen fibrils seems to be reduced with aging (Curwin et al 1994;Nakagawa et al 1994;Partington and Wood 1963;Patterson-Kane et al 1997), but if these age-related adaptations are influenced by physical activity remains unknown (Edwards et al 2005).…”