Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary

Abstract

It has been suggested that insulin signaling mutations of Drosophila melanogaster are sterile and long-lived because of juvenile hormone (JH) and ecdysteroid deficiency. However, female sterility of an insulin/IGF-like signaling mutant (chico(1)) of D. melanogaster is not mediated by downstream systemic signaling in terms of major alterations in JH or ecdysteroid levels. chico(1) is a null mutation in the insulin substrate protein (CHICO) gene of D. melanogaster. Homozygous chico(1) females are sterile and their oocytes do not mature beyond the last previtellogenic stage. Homozygous chico(1) females exhibit approximately wild-type rates of JH biosynthesis, ovarian release of ecdysteroids and haemolymph ecdysteroid levels, suggesting that these two major hormone systems play no role in producing the sterility. Previtellogenic wild-type ovaries transplanted into homozygous chico(1) females underwent vitellogenesis, showing that systemic factors present in mutant females are sufficient to support normal vitellogenesis. chico(1) ovaries transplanted into wild-type females did not undergo vitellogenesis indicating that CHICO is necessary in the ovary for vitellogenic maturation. The ovary transplant experiments corroborate the endocrine results and demonstrate that insulin/insulin-like signaling (IIS) is necessary for vitellogenesis even when sufficient levels of JH, ecdysteroids or other factors are present.

The cost of reproduction: the devil in the details

“…17) could be due either to the specifi c gene that was mutated in the insulin signaling pathway (DInR versus chico) or to genetic background. However, the only functional test in this series of studies (reciprocal ovarian transplants between wild-type and chico 1 females) showed that wild-type ovaries produced mature eggs in chico 1 females, whereas chico 1 ovaries did not mature in wild-type individuals [17]. Thus, the systemic factors necessary for egg production are present in homozygous chico 1 individuals.…”

“…Low levels of JH biosynthesis in vitro were also observed in individuals with a mutation in chico, a gene-encoding an insulin substrate protein [16]. However, in a different study [17], fl ies with the same mutation exhibited neither reduced JH biosynthesis nor lowered levels of ecdysteroids [17]. The differences between these studies (Refs 13 and 16 versus Ref.…”

Role of the insulin/Tor signaling network in starvation-induced programmed cell death in Drosophila oogenesis

“…Flies were well-fed, but mutant GLCs did not progress into mid oogenesis (Supplementary Figure 1), consistent with previous studies. 7,14,20 To determine the stage of oogenesis in which growth arrested, the last healthy egg chamber at the end of an ovariole was scored (Supplementary Figure 1m). Stage 4 of oogenesis was the predominant stage at which oogenesis arrested for InR 339 (38%), chico 1 (50%), Tor DP (59%), and S6k lÀ1 (54%) GLCs.…”

Reproductive protein protects functionally sterile honey bee workers from oxidative stress

“…In general terms, yolk precursor-encoding genes are downstream of signaling cascades that shorten lifespan in solitary model organisms (4,28,54). IIS is necessary for vitellogenesis in Drosophila (29), and negative effects on longevity have been shown directly for vitellogeninencoding genes that are controlled by IIS in C. elegans (3).…”

“…JH is part of the IIS pathway in Drosophila (5) that coregulates yolk peptide expression and somatic maintenance antagonistically (1,4,(28)(29)(30). In C. elegans, reduced activity of the vitellogenin-encoding genes vit-2 and vit-5 (which are downstream of the IIS receptor Daf-2) lengthens lifespan (3).…”