E93 confers steroid hormone responsiveness of digestive enzymes to promote blood meal digestion in the midgut of the mosquito Aedes aegypti

Insect Biochem Mol Biol. 2021 Jul:134:103580. doi: 10.1016/j.ibmb.2021.103580. Epub 2021 Apr 24.

Abstract

Anautogenous female mosquitoes obtain the nutrients needed for egg development from vertebrate blood, and consequently they transmit numerous pathogens of devastating human diseases. Digestion of blood proteins into amino acids that are used for energy production, egg maturation and replenishment of maternal reserves is an essential part of the female mosquito reproductive cycle. However, the regulatory mechanisms underlying this process remain largely unknown. Here, we report that the transcription factor E93 is a critical factor promoting blood meal digestion in adult females of the major arboviral vector Aedes aegypti in response to the steroid hormone 20-hydroxyecdysone (20E). E93 was upregulated in the female mosquito midgut after a blood meal, and RNA interference (RNAi)-mediated knockdown of E93 inhibited midgut blood digestion. E93 RNAi depletion repressed late trypsin (LT), serine protease I (SPI), SPVI and SPVII, and activated early trypsin (ET) expression in the female mosquito midgut after a blood meal. Injection of 20E activated E93, LT, SPI, SPVI and SPVII, and repressed ET expression, whereas RNAi knockdown of the ecdysone receptor (EcR) repressed E93, LT, SPI, SPVI and SPVII, and activated ET expression in the midgut. Furthermore, E93 depletion resulted in a complete loss of 20E responsiveness of LT, SPVI and SPVII. Our findings reveal important mechanisms regulating blood meal digestion in disease-transmitting mosquitoes.

Keywords: 20-Hydroxyecdysone; Blood meal digestion; E93; Mosquito; Serine protease; Steroid hormone.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aedes* / genetics
  • Aedes* / metabolism
  • Aedes* / physiology
  • Animal Feed
  • Animals
  • Blood / metabolism*
  • Blood Proteins / metabolism
  • Digestion
  • Digestive System / metabolism*
  • Drosophila Proteins / genetics
  • Ecdysterone / metabolism
  • Gene Knockdown Techniques
  • Insect Proteins / metabolism
  • Mosquito Vectors / genetics
  • Mosquito Vectors / metabolism
  • Mosquito Vectors / physiology
  • RNA Interference
  • Serine Proteases / metabolism
  • Transcription Factors / genetics*

Substances

  • Blood Proteins
  • Drosophila Proteins
  • Eip93F protein, Drosophila
  • Insect Proteins
  • Transcription Factors
  • Ecdysterone
  • Serine Proteases