Genome-wide regulation of innate immunity by juvenile hormone and 20-hydroxyecdysone in the Bombyx fat body

Ling Tian,Qin Peng,Yupu Diao,Yang Cao,Shun Zhou,Erjun Ling,Sheng Li,Enen Guo

doi:10.1186/1471-2164-11-549

Abstract

BackgroundInsect innate immunity can be affected by juvenile hormone (JH) and 20-hydroxyecdysone (20E), but how innate immunity is developmentally regulated by these two hormones in insects has not yet been elucidated. In the silkworm, Bombyx mori, JH and 20E levels are high during the final larval molt (4 M) but absent during the feeding stage of 5th instar (5 F), while JH level is low and 20E level is high during the prepupal stage (PP). Fat body produces humoral response molecules and hence is considered as the major organ involved in innate immunity.ResultsA genome-wide microarray analysis of Bombyx fat body isolated from 4 M, 5 F and PP uncovered a large number of differentially-expressed genes. Most notably, 6 antimicrobial peptide (AMP) genes were up-regulated at 4 M versus PP suggesting that Bombyx innate immunity is developmentally regulated by the two hormones. First, JH treatment dramatically increased AMP mRNA levels and activities. Furthermore, 20E treatment exhibited inhibitory effects on AMP mRNA levels and activities, and RNA interference of the 20E receptor EcR-USP had the opposite effects to 20E treatment.ConclusionTaken together, we demonstrate that JH acts as an immune-activator while 20E inhibits innate immunity in the fat body during Bombyx postembryonic development.

Highlights

Insect innate immunity can be affected by juvenile hormone (JH) and 20-hydroxyecdysone (20E), but how innate immunity is developmentally regulated by these two hormones in insects has not yet been elucidated
Insect fat body is the major organ involved in innate immunity, producing antimicrobial peptides (AMP) and other humoral response molecules [5]
AMP plays a central role in fighting against invading pathogens, which in turn up-regulate AMP gene expression via two distinct signaling pathways: the Toll pathway that is largely activated by fungi and Gram-positive bacteria and the Imd pathway that is mainly activated by Gramnegative bacteria [6]

Summary

Introduction

Insect innate immunity can be affected by juvenile hormone (JH) and 20-hydroxyecdysone (20E), but how innate immunity is developmentally regulated by these two hormones in insects has not yet been elucidated. Insect fat body is the major organ involved in innate immunity, producing antimicrobial peptides (AMP) and other humoral response molecules [5]. It was shown that RNA interference (RNAi) of genes encoding the 20E receptor complex EcR-USP in Drosophila S2 cells prevented 20E-induced immune competence. The genome-wide microarray study by Beckstead et al (2005) revealed that several AMP genes, including cecropin C, attacin A, drosocin, drosomycin, and defensin, were down-regulated by 20E in EcRdependent manners. These authors assumed that 20E blocked innate immunity at the onset of metamorphosis [13]. The conflicting reports in Drosophila imply that 20E and JH regulate AMP mRNA expression in a complex manner and it is necessary to clarify this conflict in other insect species

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