Roles of Insect Oenocytes in Physiology and Their Relevance to Human Metabolic Diseases

Abstract

Oenocytes are large secretory cells present in the abdomen of insects known to synthesize very-long-chain fatty acids to produce hydrocarbons and pheromones that mediate courtship behavior in adult flies. In recent years, oenocytes have been implicated in the regulation of energy metabolism. These hepatocyte-like cells accumulate lipid droplets under starvation and can non-autonomously regulate tracheal waterproofing and adipocyte lipid composition. Here, we summarize evidence, mostly from Drosophila, establishing that oenocytes perform liver-like functions. We also compare the functional differences in oenocytes and the fat body, another lipid storage tissue which also performs liver-like functions. Lastly, we examine signaling pathways that regulate oenocyte metabolism derived from other metabolic tissues, as well as oenocyte-derived signals that regulate energy homeostasis.

Keywords: Drosophila; adipocyte; fat body cells; hepatocyte; hydrocarbon; lipid metabolism; oenocytes; tissue communication.

Figure 1

Roles of oenocytes in modulating metabolism and responding to nutritional signal. Muscle derived PDGF- and VEGF-related factor 1 (Pvf1) signals to PDGF- and VEGF-receptor related (PvR) in oenocytes to inhibit lipid accumulation and lipogenesis in adult flies (27). Elevated levels of circulating fats can promote oenocyte steatosis and inhibit very long chain fatty acid biosynthesis (28). Knockdown of target of rapamycin (TOR) or slimfast (slif) in the larval fat body increase steatosis in oenocytes (6). During fasting, the adult fat body produces Insulin-like peptide 6 (Ilp6) which activates the Insulin-like receptor (InR) in oenocytes to promote lipid accumulation and mobilization (13). The nuclear receptors Hepatocyte nuclear factor 4 (Hnf4) and seven up (svp) in adult oenocytes regulate very long chain fatty acid (VLCFA) biosynthesis (26, 29). Knockdown of svp in oenocytes impairs vitellogenesis in ovaries, possibly by reducing hydrocarbon production (30). Spidey in oenocytes can metabolize 20-hydroxyecdysone (20HE) and promotes oenocyte proliferation (26). Larval oenocyte-derived hydrocarbon can waterproof the trachea (31). The VLCFA biosynthesis pathway is depicted with Drosophila genes (in blue) (29). Abbreviations in the pathway: ACC, Acetyl-CoA carboxylase; FASN1-3, Fatty acid synthase 1-3; TER, HACD and Elongase are each encoded by multiple genes; FarO, Fatty acyl-CoA reductase in oenocytes; Cyp4g1, cytochrome P450 4g1; Cpr, Cytochrome P450 reductase. Figure is created with BioRender.com.