Abstract
Although the regulation of vitellogenesis in insects has been mainly discussed in terms of ‘classical’ lipid hormones, juvenile hormone (JH), and 20-hydroxyecdysone (20E), recent data support the notion that this process must be adjusted in harmony with a nutritional input/reservoir and involvement of certain indoleamines and neuropeptides in regulation of such process. This study focuses on crosstalks among these axes, lipid hormones, monoamines, and neuropeptides in regulation of vitellogenesis in the American cockroach Periplaneta americana with novel aspects in the roles of arylalkylamine N-acetyltransferase (aaNAT), a key enzyme in indoleamine metabolism, and the enteroendocrine peptides; crustacean cardioactive peptide (CCAP) and short neuropeptide F (sNPF). Double-stranded RNA against aaNAT (dsRNAaaNAT) was injected into designated-aged females and the effects were monitored including the expressions of aaNAT itself, vitellogenin 1 and 2 (Vg1 and Vg2) and the vitellogenin receptor (VgR) mRNAs, oocyte maturation and changes in the hemolymph peptide concentrations. Effects of peptides application and 20E were also investigated. Injection of dsRNAaaNAT strongly suppressed oocyte maturation, transcription of Vg1, Vg2, VgR, and genes encoding JH acid- and farnesoate O-methyltransferases (JHAMT and FAMeT, respectively) acting in the JH biosynthetic pathway. However, it did not affect hemolymph concentrations of CCAP and sNPF. Injection of CCAP stimulated, while sNPF suppressed oocyte maturation and Vgs/VgR transcription, i.e., acting as allatomedins. Injection of CCAP promoted, while sNPF repressed ecdysteroid (20E) synthesis, particularly at the second step of Vg uptake. 20E also affected the JH biosynthetic pathway and Vg/VgR synthesis. The results revealed that on the course of vitellogenesis, JH- and 20E-mediated regulation occurs downstream to indoleamines- and peptides-mediated regulations. Intricate mutual interactions of these regulatory routes must orchestrate reproduction in this species at the highest potency.
Highlights
Oocytes maturation follows massive biosynthesis of vitellogenins (Vgs), the yolk protein precursors, in the fat body
juvenile hormone (JH) directly influences transcription of Vg genes and the subsequent control of Vg biosynthesis in P. americana [23] with two Vg gene isoforms, Vg1 and Previously we showed that crustacean cardioactive peptide (CCAP) and short neuropeptide F (sNPF) regulate digestive physiology in the alimentary canal, in both positive and negative feedback loops, and food searching behavior in P. americana [16,17]
We focused on potential interactions among arylalkylamine N-acetyltransferase (aaNAT), indoleamines, neuropeptides (CCAP and sNPF) and JH/20E on vitellogenesis and maturation of oocytes in P. americana to address whether these routes may form a hierarchy or at least a network of crosstalks with each other or otherwise each may represent an independent pathway from independent input signal(s)
Summary
Oocytes maturation follows massive biosynthesis of vitellogenins (Vgs), the yolk protein precursors, in the fat body. Vgs bind to the Vg receptor (VgR), which belongs to the low-density lipoprotein receptor (LDLR) family, located on the oocyte membrane. After Vgs binding to VgR, they are co-endocytosed from the hemolymph into oocytes via clathrin and Ras-like GTPase Rab protein mechanisms [1,2,3]. JH is a widespread gonadotropin [5], while 20E plays a more important role in evolved insect orders [6]. This simplified view of the process, overlooks some important aspects in Vg synthesis and its uptake by oocytes, neuropeptides and monoamines functions. Environmental input may reach the brain, corpus cardiacum (CC), corpus allatum (CA), fat body and follicle cells or oocytes membrane from a variety of origins such as nutritional, seasonal, social and thermal stress conditions
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