The Role of Peptide Hormones in Insect Lipid Metabolism

Abstract

Lipids are the primary storage molecules and an essential source of energy in insects during reproduction, prolonged periods of flight, starvation, and diapause. The coordination center for insect lipid metabolism is the fat body, which is analogous to the vertebrate adipose tissue and liver. The fat body is primarily composed of adipocytes, which accumulate triacylglycerols in intracellular lipid droplets. Genomics and proteomics, together with functional analyses, such as RNA interference and CRISPR/Cas9-targeted genome editing, identified various genes involved in lipid metabolism and elucidated their functions. However, the endocrine control of insect lipid metabolism, in particular the roles of peptide hormones in lipogenesis and lipolysis are relatively less-known topics. In the current review, the neuropeptides that directly or indirectly affect insect lipid metabolism are introduced. The primary lipolytic and lipogenic peptide hormones are adipokinetic hormone and the brain insulinlike peptides (ILP2, ILP3, ILP5). Other neuropeptides, such as insulin-growth factor ILP6, neuropeptide F, allatostatin-A, corazonin, leucokinin, tachykinins and limostatin, might stimulate lipolysis, while diapause hormone-pheromone biosynthesis activating neuropeptide, short neuropeptide F, CCHamide-2, and the cytokines Unpaired 1 and Unpaired 2 might induce lipogenesis. Most of these peptides interact with one another, but mostly with insulin signaling, and therefore affect lipid metabolism indirectly. Peptide hormones are also involved in lipid metabolism during reproduction, flight, diapause, starvation, infections and immunity; these are also highlighted. The review concludes with a discussion of the potential of lipid metabolism-related peptide hormones in pest management.

Endocrine regulation of immunity in insects

“…Cytokines are a vast group of evolutionarily conserved peptide hormones that affect several biological processes, including inflammation and immunity [41,169]. Similarly to humans, insect cytokines are the major players in the coordination between the different components of the immune system [169].…”

“…Tachykinins (TKs) are ancient widespread neuropeptides of which the best characterized to date is the vertebrate substance P, known to be involved for example in inflammation, immune responses, gut function and haematopoiesis [186]. In D. melanogaster, TKs were shown to be produced in enteroendocrine cells of the midgut and have been implicated in several aspects of metabolic stress regulation and hormone release [41,187,188]. More recently, it was also demonstrated that activation of the Imd pathway in the midgut leads to the expression and release of TK, which ultimately results in reduced IIS and lipid storage [189].…”

Drosophila melanogaster Mitochondrial Carriers: Similarities and Differences with the Human Carriers

“…Nevertheless, when starvation was prolonged, the UCP5KO flies depleted their reserves more rapidly and died faster than controls [ 142 ]. Consistently with these findings, and considering that ectopic neuronal Dm UCP5 expression was able restore starvation resistance in UCP5KO flies, this carrier could be involved in the control of metabolic homeostasis at the brain level, by uncoupling mitochondria in brain neurosecretory cells and affecting their secretion of adipokinetic hormone (the fruit fly equivalent of glucagone) and insulin-like peptides [ 143 ]. In this light, Dm UCP5 could interfere with hormonal metabolic homeostasis, as observed for mammalian UCP2 [ 103 , 104 ].…”

Two calcium‐binding chaperones from the fat body of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) involved in diapause

“…LdCrT and LdCnX expression was unaffected or downregulated in the fat body by post‐diapause, a phase requiring energy supply and lipolytic activity (Lehmann et al, 2016; May, 1989; Sinclair & Marshall, 2018; Toprak et al, 2014). As was also discussed in the context of starvation, fat body‐specific downregulation of both genes by post‐diapause might lead to a reduction in ER Ca 2+ levels (Brandt et al, 2019; W. A. Wang et al, 2017) and hydrolysis of lipids in adipocytes (Baumbach et al, 2014; Subramanian et al, 2013; Toprak, 2020), therefore, contributing to the supply of energy required for emergence from diapause. However, the fat body is not a primary site of expression for either gene in adults.…”

“…As was also discussed in the context of starvation, fat body-specific downregulation of both genes by post-diapause might lead to a reduction in ER Ca 2+ levels (Brandt et al, 2019;W. A. Wang et al, 2017) and hydrolysis of lipids in adipocytes (Baumbach et al, 2014;Subramanian et al, 2013;Toprak, 2020), therefore, contributing to the supply of energy required for emergence from diapause. However, the fat body is not a primary site of expression for either gene in adults.…”