Juvenile hormone mediates lipid storage in the oocytes of Dipetalogaster maxima

Insect Biochem Mol Biol. 2021 Jun:133:103499. doi: 10.1016/j.ibmb.2020.103499. Epub 2020 Nov 16.

Abstract

Triatomines are vectors of Chagas disease and important model organisms in insect physiology. "Kissing bugs" are obligatory hematophagous insects. A blood meal is required to successfully complete oogenesis, a process primarily controlled by juvenile hormone (JH). We used Dipetalogaster maxima as an experimental model to further understand the roles of JH in the regulation of vitellogenesis and oogenesis. A particular focus was set on the role of JH controlling lipid and protein recruitment by the oocytes. The hemolymph titer of JH III skipped bisepoxide increased after a blood meal. Following a blood meal there were increased levels of mRNAs in the fat body for the yolk protein precursors, vitellogenin (Vg) and lipophorin (Lp), as well as of their protein products in the hemolymph; mRNAs of the Vg and Lp receptors (VgR and LpR) were concomitantly up-regulated in the ovaries. Topical administration of JH induced the expression of Lp/LpR and Vg/VgR genes, and prompted the uptake of Lp and Vg in pre-vitellogenic females. Knockdown of the expression of LpR by RNA interference in fed females did not impair the Lp-mediated lipid transfer to oocytes, suggesting that the bulk of lipid acquisition by oocytes occurred by other pathways rather than by the endocytic Lp/LpR pathway. In conclusion, our results strongly suggest that JH signaling is critical for lipid storage in oocytes, by regulating Vg and Lp gene expression in the fat body as well as by modulating the expression of LpR and VgR genes in ovaries.

Keywords: Endocytic receptors; Juvenile hormone; Lipid metabolism; Lipophorin; Oogenesis; Triatomine.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Insect Proteins / metabolism
  • Insecta / metabolism
  • Insecta / physiology
  • Juvenile Hormones / metabolism*
  • Lipid Metabolism*
  • Lipoproteins / metabolism
  • Oocytes / metabolism
  • Oogenesis / physiology*
  • Ovary / metabolism
  • RNA Interference
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Signal Transduction
  • Triatominae* / metabolism
  • Triatominae* / physiology
  • Vitellogenesis / physiology*
  • Vitellogenins / metabolism

Substances

  • Insect Proteins
  • Juvenile Hormones
  • Lipoproteins
  • Receptors, Cytoplasmic and Nuclear
  • Vitellogenins
  • lipophorin
  • lipophorin receptor