The ecdysone regulatory cascade and ovarian development in lepidopteran insects: insights from the silkmoth paradigm

Abstract

The developing ovariole of the silkmoth Bombyx mori represents an excellent model for studies on the changes that occur in gene expression during the execution of long-term developmental programs. All stages of follicle development, which differ from each other by 2-2.5 h of developmental time, are organized in a single array and can be isolated simultaneously for physiological, biochemical and gene expression studies from a single animal. Recently, significant progress has been made toward the understanding of the hormonal regulation and autonomous implementation of the developmental program that governs follicular cell differentiation during oogenesis in Bombyx. In this review, the developmental career of the ovarian follicle during pharate adult development is discussed in view of the new physiological, biochemical and gene expression data that have recently accumulated. An overview is presented of the changes in expression of structural and regulatory genes and their hormonal regulation in the developing follicle during the transitions among the broad developmental periods of previtellogenesis, vitellogenesis and choriogenesis. Ovarian development in silkmoth pharate adults is induced by 20-hydroxy-ecdysone (20E) through the activation of a regulatory cascade similar to the one observed during Drosophila development. The transition from previtellogenesis to vitellogenesis corresponds to a late response to the hormone and is characterized by the induction of the expression of a unique isoform of the nuclear receptor BmHR3 and the follicular cell-specific yolk protein ESP. The transition from early to middle and late vitellogenesis and choriogenesis, on the other hand, is regulated by positively and negatively acting intra- and extra-ovarian factors. In vitro cultures of developing ovarioles reveal the requirement for the presence of an as yet unidentified growth factor(s) in the hemolymph, while the follicle developmental arrest that is observed after treatment with the ecdysone agonist tebufenozide indicates the requirement for a decline in the level of 20E. The initiation of choriogenesis is characterized by the transcriptional activation of the gene BmGATAbeta that encodes GATA transcription factors, and the chorion genes in the follicular cells. Furthermore, modulation of the activity of BmGATAbeta at the posttranscriptional level is crucial for the stage-specific activation of chorion genes during late choriogenesis. The developing ovariole of the silkmoth is, therefore, emerging as an important model for the study of insect oogenesis and the action of the steroid hormone 20E at the molecular level.