Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. II. Hormonal control of imaginal nest cell degeneration and differentiation during metamorphosis

Abstract

The nervous system of an adult moth is comprised of retained larval neurons that are remodeled during metamorphosis and a set of new adult specific neurons. The new neurons arise from a stereotyped array of stem cells (neuroblasts) that divide during larval life to generate nests of up to 100 arrested postmitotic immature neurons, the imaginal nest (IN) cells. At the onset of metamorphosis, some of the IN cells die while the remainder differentiate into mature functional neurons. Metamorphosis in insects is regulated by 2 classes of hormones, the ecdysteroids and the juvenile hormones. The transition from larva to pupa requires the disappearance of juvenile hormones followed by 2 releases of ecdysteroids: a small “commitment peak” and a larger “prepupal peak.” Through a series of endocrine manipulations, we demonstrate that the death and differentiation observed among the abdominal IN cells at metamorphosis are both influenced by these hormonal cues. If the abdomen was isolated from the hormonal sources in the anterior half of the larva before the onset of metamorphosis, death and differentiation of the IN cells were prevented. Infusion of ecdysteroids into such abdomens, to mimic the prepupal peak, resulted in the IN cells showing the same fate as seen in control animals during the early phases of metamorphosis. The response of the IN cells to the small commitment peak of ecdysteroids was heterogeneous. Exposure to this small peak of steroids caused some cells to become committed to resume their development, making them resistant to juvenile hormone application.

Postembryonic neurogenesis in the central nervous system of the tobacco hornworm,Manduca sexta. III. Spatial and temporal patterns of proliferation

“…The IN cells resumed their development in response to the same hormonal cues that trigger metamorphosis (Booker and Truman, 1987b). The results presented here reveal that within 24 h of their birth a substantial number of the IN cells initiate a program of cell death.…”

“…The cell deaths that occur at the onset of metamorphosis are triggered by a surge in the titer of the ecdysteroid hormones in the absence of juvenile hormones (Booker and Truman, 1987b). Many of the doomed I N cells are rescued by the application of juvenile hormone prior to the appearance of the large peak of ecdysteroids that drives the formation of the pupal stage.…”

“…The resumption of IN cell development is triggered by the same hormonal signals responsible for triggering metamorphosis ( Booker and Truman, 1987b). Some of the IN cells respond to these hormonal signals by degenerating, whereas the survivors enter terminal differentiation, developing into functional adult neurons.…”

Mechanisms of Dendritic Elaboration of Sensory Neurons inDrosophila: Insights fromIn VivoTime Lapse

“…However, it is interesting that another group of neurons, the arrested adultspecific neurons, begin soma enlargement and adult outgrowth during the larval-pupal transition, a time when JH transiently reappears. Experimental manipulation of JH levels demonstrates that JH controls the amount of early growth shown by these cells in response to 20E (Booker and Truman, 1987). Consequently, the JH sensitivity shown by the adult-specific cells may also be shared by remodeling neurons during their outgrowth phase despite the fact that the latter neurons normally do not see JH at that time.…”

A juvenile hormone agonist reveals distinct developmental pathways mediated by Ecdysone-inducible broad complex transcription factors

“…(The term juvenoids includes endogenous compounds and chemical analogs with JH-like activity.) Studies in several insect species indicate that juvenoids can modulate cellular responses to 20E [Chihara and Fristrom, 1973;Wyss, 1976;Mitsui and Riddiford, 1978;Levine et al, 1986;Booker and Truman, 1987;Truman and Reiss, 1988;Cherbas et al, 1989;Jacobs and Weeks, 1990;Prugh et al, 1992]. We tested the hypothesis that juvenoid-induced lethality results from interfering with the function of the Broad Complex (BRC), a gene essential for transducing 20E signals into the metamorphic development of larval and imaginal tissues, including the epidermis, salivary glands, central nervous system (CNS), gut, and musculature [Kiss et al, 1988;White, 1991, 1992].…”