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

Overview

Journal Front Insect Sci

Date 2024 Mar 12

PMID 38468774

Authors

Kerui Huang

Ying Liu

Norbert Perrimon

Affiliations

Soon will be listed here.

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 , 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.

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References

Palm W, Sampaio J, Brankatschk M, Carvalho M, Mahmoud A, Shevchenko A . Lipoproteins in Drosophila melanogaster--assembly, function, and influence on tissue lipid composition. PLoS Genet. 2012; 8(7):e1002828. PMC: 3406001. DOI: 10.1371/journal.pgen.1002828. View

Krupp J, Levine J . Dissection of oenocytes from adult Drosophila melanogaster. J Vis Exp. 2010; (41). PMC: 3156075. DOI: 10.3791/2242. View

Flatt T, Heyland A, Rus F, Porpiglia E, Sherlock C, Yamamoto R . Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. J Exp Biol. 2008; 211(Pt 16):2712-24. PMC: 2522372. DOI: 10.1242/jeb.014878. View

Tew K, Ronai Z . GST function in drug and stress response. Drug Resist Updat. 2001; 2(3):143-147. DOI: 10.1054/drup.1999.0086. View

Parvy J, Napal L, Rubin T, Poidevin M, Perrin L, Wicker-Thomas C . Drosophila melanogaster Acetyl-CoA-carboxylase sustains a fatty acid-dependent remote signal to waterproof the respiratory system. PLoS Genet. 2012; 8(8):e1002925. PMC: 3431307. DOI: 10.1371/journal.pgen.1002925. View

Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Leopold P . A nutrient sensor mechanism controls Drosophila growth. Cell. 2003; 114(6):739-49. DOI: 10.1016/s0092-8674(03)00713-x. View

Reiter L, Potocki L, Chien S, Gribskov M, Bier E . A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res. 2001; 11(6):1114-25. PMC: 311089. DOI: 10.1101/gr.169101. View

Hoffmann J, Reichhart J . Drosophila innate immunity: an evolutionary perspective. Nat Immunol. 2002; 3(2):121-6. DOI: 10.1038/ni0202-121. View

Bailey E, Horne J, Izatt M, Hill L . Concentrations of acetoacetate and 3-hydroxybutyrate in pigeon blood and desert locust haemolymph. Life Sci II. 1971; 10(24):1415-9. DOI: 10.1016/0024-3205(71)90351-1. View

10.

Huang K, Chen W, Zhu F, Li P, Kapahi P, Bai H . RiboTag translatomic profiling of Drosophila oenocytes under aging and induced oxidative stress. BMC Genomics. 2019; 20(1):50. PMC: 6335716. DOI: 10.1186/s12864-018-5404-4. View

11.

Bai H, Kang P, Tatar M . Drosophila insulin-like peptide-6 (dilp6) expression from fat body extends lifespan and represses secretion of Drosophila insulin-like peptide-2 from the brain. Aging Cell. 2012; 11(6):978-85. PMC: 3500397. DOI: 10.1111/acel.12000. View

12.

Bostrom P, Wu J, Jedrychowski M, Korde A, Ye L, Lo J . A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012; 481(7382):463-8. PMC: 3522098. DOI: 10.1038/nature10777. View

13.

Rinterknecht E . Cuticulogenesis correlated with ultrastructural changes in oenocytes and epidermal cells in the late cockroach embryo. Tissue Cell. 1985; 17(5):723-43. DOI: 10.1016/0040-8166(85)90007-2. View

14.

Brun A, Cuany A, Le Mouel T, Berge J, Amichot M . Inducibility of the Drosophila melanogaster cytochrome P450 gene, CYP6A2, by phenobarbital in insecticide susceptible or resistant strains. Insect Biochem Mol Biol. 1996; 26(7):697-703. DOI: 10.1016/s0965-1748(96)00036-7. View

15.

Matsushita R, Nishimura T . Trehalose metabolism confers developmental robustness and stability in Drosophila by regulating glucose homeostasis. Commun Biol. 2020; 3(1):170. PMC: 7138798. DOI: 10.1038/s42003-020-0889-1. View

16.

Vendelbo M, Clasen B, Treebak J, Moller L, Krusenstjerna-Hafstrom T, Madsen M . Insulin resistance after a 72-h fast is associated with impaired AS160 phosphorylation and accumulation of lipid and glycogen in human skeletal muscle. Am J Physiol Endocrinol Metab. 2011; 302(2):E190-200. PMC: 4971894. DOI: 10.1152/ajpendo.00207.2011. View

17.

Stefana M, Driscoll P, Obata F, Pengelly A, Newell C, MacRae J . Developmental diet regulates Drosophila lifespan via lipid autotoxins. Nat Commun. 2017; 8(1):1384. PMC: 5680271. DOI: 10.1038/s41467-017-01740-9. View

18.

Geminard C, Rulifson E, Leopold P . Remote control of insulin secretion by fat cells in Drosophila. Cell Metab. 2009; 10(3):199-207. DOI: 10.1016/j.cmet.2009.08.002. View

19.

Heier C, Kuhnlein R . Triacylglycerol Metabolism in . Genetics. 2018; 210(4):1163-1184. PMC: 6283168. DOI: 10.1534/genetics.118.301583. View

20.

Weaver L, Drummond-Barbosa D . The nuclear receptor seven up functions in adipocytes and oenocytes to control distinct steps of Drosophila oogenesis. Dev Biol. 2019; 456(2):179-189. PMC: 6884690. DOI: 10.1016/j.ydbio.2019.08.015. View