Specialized hepatocyte-like cells regulate Drosophila lipid metabolism

Abstract

Lipid metabolism is essential for growth and generates much of the energy needed during periods of starvation. In Drosophila, fasting larvae release large quantities of lipid from the fat body but it is unclear how and where this is processed. Here we identify the oenocyte as the principal cell type accumulating lipid droplets during starvation. Tissue-specific manipulations of the Slimfast amino-acid channel, the Lsd2 fat-storage regulator and the Brummer lipase indicate that oenocytes act downstream of the fat body. In turn, oenocytes are required for depleting stored lipid from the fat body during fasting. Hence, lipid-metabolic coupling between the fat body and oenocytes is bidirectional. When food is plentiful, oenocytes have critical roles in regulating growth, development and feeding behaviour. In addition, they specifically express many different lipid-metabolizing proteins, including Cyp4g1, an omega-hydroxylase regulating triacylglycerol composition. These findings provide evidence that some lipid-processing functions of the mammalian liver are performed in insects by oenocytes.

Insights into the transcriptome of oenocytes from Aedes aegypti pupae

“…Previous data have also suggested that oenocytes are able to produce integument hydrocarbons (Fan et al 2003). This lipid processing role was demonstrated in D. melanogaster by Gutierrez et al (2007) with the identification of 51 genes related to lipid metabolism that were expressed exclusively in the oenocytes of the fruit fly. Interestingly, 40% of those genes were homologous to human genes related to lipid metabolism/processing.…”

“…In addition to their role in steroid metabolism and in analogy to mammalian hepatocytes, insect oenocytes participate in detoxification processes specifically related to xenobiotics (Sundseth et al 1990, Gutierrez et al 2007). In insects, increased transcription of P450s is frequently associated with resistance to insecticides (Scott & Wen 2001).…”

“…In addition, some of these transcripts also coded the following proteins: a catalase (corresponding to Ae. aegypti whole genome sequence AAEL013407), whose role is possibly linked to the removal of excessive reactive oxygen intermediates that allows the cells to maintain homeostasis following oxidative bursts (Gutierrez et al 2007), a NA-DPH CPR (corresponding to Ae. aegypti whole genome sequence AAEL003349), that is known to be involved with insecticide clearance in An.…”

“…Since then, their function has remained unclear and they have been investigated in largely descriptive studies implicating larval oenocytes in processes such as cuticle synthesis and the regulation of hemolymph composition (reviewed by Dean et al 1985). Gutierrez et al (2007) demonstrated that oenocytes from Drosophila melanogaster larva store lipid as cytoplasm droplets and appear to play a crucial role in insect development. Additionally, D. melanogaster oenocytes and the mammalian liver share several homologous genes coding for lipid metabolism/processing.…”

“…Of the 51 transcripts that were identified to be exclusive to D. melanogaster larvae oenocytes, 40% of the transcripts have human homologues that are associated with lipid metabolism and protein processing. Thus, in Drosophila, oenocytes can be considered analogous to mammalian hepatocytes (Gutierrez et al 2007 pression profile (transcriptome) in mosquito oenocytes is currently unknown. One role assigned to An.…”