Insulin receptor-mediated nutritional signalling regulates juvenile hormone biosynthesis and vitellogenin production in the German cockroach

Abstract

Female reproductive processes, which comprise, amongst others, the synthesis of yolk proteins and the endocrine mechanisms which regulate this synthesis, need a considerable amount of energy and resources. The role of communicating that the required nutritional status has been attained is carried out by nutritional signalling pathways and, in particular, by the insulin receptor (InR) pathway. In the present study, using the German cockroach, Blattella germanica, as a model, we analysed the role of InR in different processes, but mainly those related to juvenile hormone (JH) synthesis and vitellogenin production. We first cloned the InR cDNA from B. germanica (BgInR) and then determined that its expression levels were constant in corpora allata and fat body during the first female gonadotrophic cycle. Results showed that the observed increase in BgInR mRNA in fat body from starved compared to fed females was abolished in those females treated with systemic RNAi in vivo against the transcription factor BgFoxO. RNAi-mediated BgInR knockdown during the final two nymphal stages produced significant delays in the moults, together with smaller adult females which could not spread the fore- and hindwings properly. In addition, BgInR knockdown led to a severe inhibition of juvenile hormone synthesis in adult female corpora allata, with a concomitant reduction of mRNA levels corresponding to 3-hydroxy-3-methylglutaryl coenzyme A (HMG-CoA) synthase-1, HMG-CoA synthase-2, HMG-CoA reductase and methyl farnesoate epoxidase. BgInR RNAi treatment also reduced fat body vitellogenin mRNA and oocyte growth. Our results show that BgInR knockdown produces similar phenotypes to those obtained in starved females in terms of corpora allata activity and vitellogenin synthesis, and indicate that the InR pathway mediates the activation of JH biosynthesis and vitellogenin production elicited by nutrition signalling.

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

“…In B. germanica , BgHMG-S1 and BgHMG-R have been identified as key enzymes in the mevalonate pathway leading to JH synthesis282930. B. germanica has a second HMG synthase gene, BgHMG-S2 , although its expression and regulation is identical to BgHMG-S1 3031. Paralleling the rate of JH synthesis, mRNAs of BgHMG-S1 and BgHMG-R are significantly upregulated in the CA during the nymphal-to-adult transition and are maintained high during the first gonadotrophic cycle (Fig.…”

Silencing of Two Insulin Receptor Genes Disrupts Nymph-Adult Transition of Alate Brown Citrus Aphid

“…Silencing of AcInR1 and AcInR2 disrupted the development (including wing development) of the aphids during the nymph–adult transition and this might indicate that decreased capability for food intake reduced nutrient transport. Other studies have demonstrated that high expression levels of BdInR , BmInR , and BgInR were induced by starvation of B. dorsalis , B. mori , and B. germanica , respectively [3,16,45]. In T. castaneum , knockdown of TcInR1 decreased food intake through the sulfakinin signal pathway in the larval stages [21].…”

“…In some insects, only one insulin receptor gene occurs. These insects include the Diptera: Drosophila melanogaster [13], Bactrocera dorsalis [3], and Aedes aegypti [14]; Lepidoptera: Bombyx mori [15], Blattoidea: Blattella germanica [16]; and Coleoptera: Onthophagus nigriventris [17]. Both insulin receptor genes have been identified in polymorphic insects, such as Aphis mellifera [18], Solenopsis invicta [19], Nilaparvata lugens [6], Acyrthosiphon pisum [2], and the non-polymorphic insect Tribolium castaneum [7].…”

Reproduction–Immunity Trade-Offs in Insects

“…D. melanogaster insulin receptor ( dInR ) mutants exhibit low JH titers (135), indicating that IIS promotes JH synthesis. Nuclear FOXO—an indication of low IIS activity—also increases JH titers and vitellogenin production in the German cockroach ( B. germanica ) (1, 130). Moreover, JH and 20E can regulate IIS activity.…”