The hormonal pathway controlling cell death during metamorphosis in a hemimetabolous insect

Abstract

Metamorphosis in holometabolous insects is mainly based on the destruction of larval tissues. Intensive research in Drosophila melanogaster, a model of holometabolan metamorphosis, has shown that the steroid hormone 20-hydroxyecdysone (20E) signals cell death of larval tissues during metamorphosis. However, D. melanogaster shows a highly derived type of development and the mechanisms regulating apoptosis may not be representative in the insect class context. Unfortunately, no functional studies have been carried out to address whether the mechanisms controlling cell death are present in more basal hemimetabolous species. To address this, we have analyzed the apoptosis of the prothoracic gland of the cockroach Blattella germanica, which undergoes stage-specific degeneration just after the imaginal molt. Here, we first show that B. germanica has two inhibitor of apoptosis (IAP) proteins and that one of them, BgIAP1, is continuously required to ensure tissue viability, including that of the prothoracic gland, during nymphal development. Moreover, we demonstrate that the degeneration of the prothoracic gland is controlled by a complex 20E-triggered hierarchy of nuclear receptors converging in the strong activation of the death-inducer Fushi tarazu-factor 1 (BgFTZ-F1) during the nymphal-adult transition. Finally, we have also shown that prothoracic gland degeneration is effectively prevented by the presence of juvenile hormone (JH). Given the relevance of cell death in the metamorphic process, the characterization of the molecular mechanisms regulating apoptosis in hemimetabolous insects would allow to help elucidate how metamorphosis has evolved from less to more derived insect species.

Transcription factor E93 specifies adult metamorphosis in hemimetabolous and holometabolous insects

“…S1 I-N). Recently, we have shown that a complex 20E-triggered hierarchy of nuclear receptors controls these metamorphic transformations in B. germanica (11,12). The same gene cascade, however, is also present during the previous nymphal-nymphal transitions (12), implying that stage-specific factors modify the responsiveness of target genes during the metamorphic transition.…”

“…S1 A-H). During this transition, the prothoracic gland, which is responsible for the synthesis of ecdysteroids, degenerates, and the corpora allata cells switch from the proliferative phase to the adult-specific nonproliferative state (11) (Fig. S1 I-N).…”

Juvenile hormone biosynthesis in adult Blattella germanica requires nuclear receptors Seven-up and FTZ-F1

“…In this case, BgFTZ-F1 induces the degeneration of the prothoracic gland immediately after the imaginal molt, a critical event required for proper adult development in B. germanica 54. BgFTZ-F1 acts, therefore, as a critical adult-specific factor in the two main endocrine glands, the prothoracic gland where induces its degeneration, and the CA where promotes the synthesis of high levels of JH.…”

Conserved repressive function of Krüppel homolog 1 on insect metamorphosis in hemimetabolous and holometabolous species

“…Most of the reported data on this cascade of transcription factors refer to Drosophila melanogaster , the fruit fly, a holometabolous insect that shows many highly derived characters, which has been the most thoroughly studied species from the point of view of molecular endocrinology89. From this point of view, the most widely studied hemimetabolous model is the German cockroach Blattella germanica , and results indicate that the transcription factors involved in 20-hydroxyecdysone signalling are generally conserved, although the functions of some of them and the precise epistatic relationships between them may differ with respect to D. melanogaster 1011121314.…”