Endocrine regulation of terminal muscle differentiation: Atrophy and degeneration of the intersegmental muscles of Lepidoptera

Abstract

The intersegmental muscles of the Lepidoptera pass through three separate, sequential differentiated states during pharate adult development: status quo; atrophy; degeneration. Each of these developmental programs is characterized by a distinct morphology, physiology and endocrine responsiveness. The factors responsible for regulating these differentiative changes are ecdysteroids. In Manduca sexta, the haemolymph ecdysteroid titre declines in a circadian-modified fashion during the last three days of adult development, which parallels the maturation of the intersegmental muscles. Abdomen-ligation, which causes a precipitous decline in the ecdysteroid titre, causes the precocious atrophy and degeneration of these muscles, whereas injection of, or infusion with, 20-hydroxyecdysone greatly delays such changes. While the terminal differentiation of the epidermis and nervous system is also regulated by ecdysteroids, endocrine manipulations have suggested that the development of the intersegmental muscles is independent of these tissues. In the silkmoth Antheraea polyphemus, ecdysteroids are also responsible for regulating intersegmental muscle differentiation, but eclosion hormone (a peptide) acts as the proximal trigger for the activation of the degeneration program. The declining ecdysteroid titre initiates the atrophy program and subsequently determines the timing of both release of eclosion hormone and intersegmental muscle sensitivity to the peptide. Eclosion hormone then acts directly on the muscles, via cGMP, to activate the degeneration program. Ecdysteroids appear to prevent premature muscle degeneration by regulating a biochemical step distal to both the eclosion hormone receptor and the rise in cGMP.