Changes in contractile properties of skeletal muscle during developmentally programmed atrophy and death

Abstract

Schwartz, Lawrence M., and Robert L. Ruff. Changes in contractile properties of skeletal muscle during developmentally programmed atrophy and death. Am J Physiol Cell Physiol 282: C1270-C1277, 2002. First published January 16, 2002 10.1152/ajpcell.01275.2000.-Skeletal muscle atrophy and death are protracted processes that accompany aging and pathological insults in mammals. The intersegmental muscles (ISMs) from the tobacco hawkmoth Manduca sexta are composed of giant fibers that undergo distinct hormonally-regulated programs of atrophy and death at the end of metamorphosis. Atrophy occurs during the 3 days preceding adult emergence and results in a 40% reduction of mass, whereas death takes place during the subsequent 30 h and results in the complete loss of the fibers. There are no significant changes in tetanic force or calcium sensitivity in skinned fiber preparations during atrophy. However, the size of caffeine-induced contractions fell by about 50%. With the onset of the death phase, dramatic reductions occur in ISM: tetanic force, twitch amplitude, resting potential, caffeineinduced contractions, calcium sensitivity, and Hill coefficients. Several lines of evidence suggest that ISM atrophy is caused by an increase in protein turnover without significant modification of fiber organization. In contrast, ISM death is accompanied by disorganization of the contractile apparatus and concomitant loss of contractile function.

Programmed cell death in flight muscle histolysis of the house cricket

“…Alterations in contractile potential of involuting insect muscles have been reported in ISMs of the blood-sucking bug, Rhodnius prolixus (Wigglesworth, 1956) and moth, Manduca sexta (Lockshin and Beaulaton, 1979). More recently, electrophysiologic studies have revealed dramatic declines in muscle contractility accompany PCD in insect muscle (Schwartz and Ruff, 2002). Changes in length of the DLMs of the cricket observed when muscles are cut as in our procedures probably do not represent normal in vivo contraction.…”

Atrophy and programmed cell death of skeletal muscle

“…Muscle fibers can also be induced to die via necrosis, autophagy and apoptosis, depending on the stimulus and developmental programming of the cell Atrophy is not accompanied by changes in muscle physiological parameters such as: resting potential, force/ cross-sectional area, tentanic contracture, or sensitivity to intracellular calcium in skinned fiber preparations. 33 There is also no overt change in the stochiometric levels of the major contractile proteins. 34,35 These data support the hypothesis that atrophy involves a general increase in protein catabolism rather than the selective loss-specific contractile proteins as has been been shown in mammals.…”

“…29,31,43 Coincident with eclosion, the resting potential declines at a rate of about 2.5 mV/h and the mass at a rate of B4%/h. 33 While the muscles are no longer contractile 15 h later, they still maintain a modest resting potential (BÀ30 mV), suggesting that there has been no membrane rupture or necrosis. By 30 h post-eclosion, almost all the muscle mass is gone and the fibers are composed of whorls of internalized membranes and connective tissue.…”

“…By 5 h posteclosion the muscles have lost significant mass and physiological function. 33 Most genes are constitutively expressed, like the ubiquitin fusion 80 (Ubf-80) gene, which plays a role in ribosome biogenesis. 37 A small number of genes are induced or repressed with the commitment to die.…”

Skeletal Muscles Do not Undergo Apoptosis During Either Atrophy or Programmed Cell Death

“…This dramatic atrophy is equivalent to the loss of muscle mass that is seen in 80 year olds with sarcopenia, but takes place in three days rather than 30 years. While the ISMs lose mass, they retain normal physiological properties such as resting potential and force/ cross-sectional area [46]. The ISMs are used for the eclosion behavior and then initiate programmed cell death (PCD), both of which are triggered by a specific peptide hormone, the eclosion hormone [45,47].…”