A coordinated expression of biosynthetic enzymes controls the flux of juvenile hormone precursors in the corpora allata of mosquitoes

Abstract

Juvenile hormone (JH) is a key regulator of metamorphosis and ovarian development in mosquitoes. Adult female Aedes aegypti mosquitoes show developmental and dynamically regulated changes of JH synthesis. Newly emerged females have corpora allata (CA) with low biosynthetic activity, but they produce high amounts of JH a day later; blood feeding results in a striking decrease in JH synthesis, but the CA returns to a high level of JH synthesis three days later. To understand the molecular bases of these dynamic changes we combined transcriptional studies of 11 of the 13 enzymes of the JH pathway with a functional analysis of JH synthesis. We detected up to a 1000-fold difference in the levels of mRNA in the CA among the JH biosynthetic enzymes studied. There was a coordinated expression of the 11 JH biosynthetic enzymes in female pupae and adult mosquito. Increases or decreases in transcript levels for all the enzymes resulted in increases or decreases of JH synthesis; suggesting that transcript changes are at least partially responsible for the dynamic changes of JH biosynthesis observed. JH synthesis by the CA was progressively increased in vitro by addition of exogenous precursors such as geranyl-diphosphate, farnesyl-diphosphate, farnesol, farnesal and farnesoic acid. These results suggest that the supply of these precursors and not the activity of the last 6 pathway enzymes is rate limiting in these glands. Nutrient reserves play a key role in the regulation of JH synthesis. Nutritional deficient females had reduced transcript levels for the genes encoding JH biosynthetic enzymes and reduced JH synthesis. Our studies suggest that JH synthesis is controlled by the rate of flux of isoprenoids, which is the outcome of a complex interplay of changes in precursor pools, enzyme levels and external regulators such as nutrients and brain factors. Enzyme levels might need to surpass a minimum threshold to achieve a net flux of precursors through the biosynthetic pathway. In glands with low synthetic activity, the flux of isoprenoids might be limited by the activity of enzymes with low levels of expression

Allatotropin inhibits juvenile hormone biosynthesis by the corpora allata of adult Bombyx mori

“…Through the combinatorial actions of these stimulatory and inhibitory factors, a large JH peak appears in the hemolymph at the appropriate developmental stage necessary for reproduction. A similar regulation was observed in A. aegypti where AST-C and AT induced a proper surge in JH synthesis during the adult stage (Li et al, 2003;Nouzova et al, 2011).…”

“…The regulatory mechanisms of JH biosynthesis in the adult stage have also been well studied in several insect species, in particular, cockroaches (reviewed by Stay and Tobe, 2007;Marchal et al, 2013) and mosquitoes (Noriega, 2004;Mayoral et al, 2009;Nouzova et al, 2011Nouzova et al, , 2012Pérez-Hedo et al, 2013;Nyati et al, 2013;Rivera-Perez et al, 2013). Allatotropin (AT) and allatostatin (AST) are two major neuropeptide hormones that control JH synthesis during the adult stage (Weaver and Audsley, 2009;Goodman and Granger, 2005).…”

Interplay between insulin signaling, juvenile hormone, and vitellogenin regulates maternal effects on polyphenism in ants

“…Changes in IIS usually result in the release of neuropeptides (e.g., allatostatin, allatotropin) that influence the production of JH by the corpus allatum (59,64). Accordingly, the exposure to cold also up-regulated the expression of the JHepox gene, which encodes JH epoxidase, the enzyme that catalyzes the oxidation of methyl farnesoate into JH III (86,87), the last step in the JH biosynthesis in most insects (88)(89)(90)(91).…”

Peptidergic control of food intake and digestion in insects1This review is part of a virtual symposium on recent advances in understanding a variety of complex regulatory processes in insect physiology and endocrinology, including development, metabolism, cold hardiness, food intake and digestion, and diuresis, through the use of omics technologies in the postgenomic era.

“…ATs exert their effects on their cellular targets by binding to high-affinity receptors, which are members of the GPCR superfamily Horodyski et al 2011;Nouzova et al 2011;Vuerinckx et al 2011). In A. aegypti, an AT receptor was characterized and found to be expressed in the CC, but also in the heart, hindgut, accessory glands, and testes (Nouzova et al 2011).…”

“…In A. aegypti, an AT receptor was characterized and found to be expressed in the CC, but also in the heart, hindgut, accessory glands, and testes (Nouzova et al 2011). Blood feeding resulted in a decrease in transcript levels.…”