Regulation of energy liberation during steady sarcomere shortening

Oren Tchaicheeyan, Amir Landesberg
2005 American Journal of Physiology. Heart and Circulatory Physiology  
Tchaicheeyan, Oren, and Amir Landesberg. Regulation of energy liberation during steady sarcomere shortening. Energy liberation rate (Ė ) during steady muscle shortening is a monotonic increasing or biphasic function of the shortening velocity (V). The study examines three plausible hypotheses for explaining the biphasic Ė -V relationship (EVR): 1) the cross-bridge (XB) turnover rate from non-force-generating (weak) to force-generating (strong) conformation decreases as V increases; 2) XB
more » ... s is determined by the number of strong XBs (XB-XB cooperativity); and 3) the affinity of troponin for calcium is modulated by the number of strong XBs (XB-Ca cooperativity). The relative role of the various energy-regulating mechanisms is not well defined. The hypotheses were tested by coupling calcium kinetics with XB cycling. All three hypotheses yield identical steady-state characteristics: 1) hyperbolic force-velocity relationship; 2) quasi-linear stiffness-force relationship; and 3) biphasic EVR, where Ė declines at high V due to decrease in the number of cycling XBs or in the weak-to-strong transition rate. The hypotheses differ in the ability to describe the existence of both monotonic and biphasic EVRs and in the effect of intracellular free calcium concentration ([Ca 2ϩ ]i) on the EVR peak. Monotonic and biphasic EVRs with a shift in EVR peak to higher velocity at higher [Ca 2ϩ ]i are obtained only by XB-Ca cooperativity. XB-XB cooperativity provides only biphasic EVRs. A direct effect of V on XB kinetics predicts that EVR peak is obtained at the same velocity independently of [Ca 2ϩ ]i. The study predicts that measuring the dependence of the EVR on [Ca 2ϩ ]i allows us to test the hypotheses and to identify the dominant energy-regulating mechanism. The established XB-XB and XB-Ca mechanisms provide alternative explanations to the various reported EVRs. muscle energetics; cross bridge; excitation-contraction coupling; cardiac mechanics; cooperativity THE DOMINANT MECHANISM underlying the modulation of energy liberation from muscle by the loading conditions is not well defined (12, 29). The rate of energy liberation (Ė ), i.e., mechanical power plus heat production rate, is higher in steady shortening than in isometric contraction (Ė 0 ) (29). Hill's original study (17) has demonstrated that Ė increased monotonically with shortening velocity (V). Later studies by Hill (16) and others (1, 29) have established the existence also of a biphasic Ė -V relationship (EVR) with a decrease of Ė as V approaches the unloaded shortening velocity (V u ). This biphasic phenomenon and an apparent plateau at velocities about one-half the maximal velocity were reported in fast-twitch [frog sartorius (16), mouse extensor digitorum longus (2, 3), and dogfish white myotomal fibers (8)] and slow-twitch [tortoise rectus femoris (28) and mouse soleus (1)] muscles of various vertebrates. There is a lot of evidence suggesting that Address for reprint requests and other correspondence: A. Landesberg,
doi:10.1152/ajpheart.00124.2005 pmid:16006550 fatcat:audznmdlvbdc3legjmb6eldzvm