The extraembryonic serosa is a frontier epithelium providing the insect egg with a full-range innate immune response

Elife. 2014 Dec 9:3:e04111. doi: 10.7554/eLife.04111.

Abstract

Drosophila larvae and adults possess a potent innate immune response, but the response of Drosophila eggs is poor. In contrast to Drosophila, eggs of the beetle Tribolium are protected by a serosa, an extraembryonic epithelium that is present in all insects except higher flies. In this study, we test a possible immune function of this frontier epithelium using Tc-zen1 RNAi-mediated deletion. First, we show that bacteria propagate twice as fast in serosa-less eggs. Then, we compare the complete transcriptomes of wild-type, control RNAi, and Tc-zen1 RNAi eggs before and after sterile or septic injury. Infection induces genes involved in Toll and IMD-signaling, melanisation, production of reactive oxygen species and antimicrobial peptides in wild-type eggs but not in serosa-less eggs. Finally, we demonstrate constitutive and induced immune gene expression in the serosal epithelium using in situ hybridization. We conclude that the serosa provides insect eggs with a full-range innate immune response.

Keywords: NF-kappaB; RNA sequencing; Toll; Tribolium castaneum; developmental biology; immunology; innate immunity; serosa; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antimicrobial Cationic Peptides / pharmacology
  • Colony Count, Microbial
  • Epithelium / drug effects
  • Epithelium / embryology*
  • Epithelium / immunology
  • Extraembryonic Membranes / drug effects
  • Extraembryonic Membranes / immunology*
  • Extraembryonic Membranes / microbiology
  • Gene Expression Regulation, Developmental / drug effects
  • Genes, Insect
  • Immunity, Innate* / drug effects
  • Immunity, Innate* / genetics
  • In Situ Hybridization
  • Ovum / drug effects
  • Ovum / immunology*
  • Ovum / microbiology
  • RNA Interference
  • Reproducibility of Results
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sepsis / immunology
  • Sepsis / microbiology
  • Sepsis / pathology
  • Sequence Analysis, RNA
  • Serous Membrane / drug effects
  • Serous Membrane / embryology
  • Serous Membrane / immunology*
  • Serous Membrane / microbiology
  • Tribolium / drug effects
  • Tribolium / embryology*
  • Tribolium / genetics
  • Tribolium / immunology*

Substances

  • Antimicrobial Cationic Peptides

Associated data

  • GEO/GSE54018

Grants and funding

The funder had no role in study design, data collection and interpretation, or the decision to submit the work for publication.