The hydroxyproline motif of male sex peptide elicits the innate immune response in Drosophila females

Abstract

Seminal fluid elicits a variety of physiological and behavioral changes in insect females. In Drosophila melanogaster females, sex peptide (SP) is the major seminal agent eliciting oviposition and reduction of receptivity. But SP also has many other effects; for example, it stimulates food intake, egg production, ovulation, juvenile hormone production and antimicrobial peptide synthesis. Thus, SP very probably has several receptors. To identify putative targets and signaling cascades, we studied the genome-wide regulation of genes by microarray analysis of RNA isolated from females after mating with wild-type males or males lacking SP, respectively. In addition, we studied the effects of SP on the proteome of females. Sex peptide regulates gene activity differentially in the head and in the abdomen. Genes coding for unspecific antimicrobial peptides are specifically transcribed in the abdomen, e.g. the antimicrobial peptide drosocin in epithelial tissues of the female genital tract (oviduct and calyx). Hence, SP elicits a systemic [Peng J, Zipperlen P & Kubli E (2005) Curr Biol15, 1690-1694] and an epithelial immune response. Ectopic expression of SP in the fat body of transgenic virgin females (with subsequent secretion into the hemolymph) does not elicit drosocin synthesis in the genital tract. Thus, the receptors for the stimulation of the systemic and the epithelial responses by SP are compartmentalized. The hydroxyproline (P*) motif of SP, P*TKFP*IP*SP*NP*, is identified as a novel elicitor of the innate immune response. We suggest that SP acts by chemical mimicry of sugar components of the bacterial cell wall. Thus, SP may induce the immune system via pattern recognition receptors.

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

“…SP leads to rejection of courting males and increases egg production and oviposition [4][5][6][7][8], but also leads to other behavioural and physiological changes. These include an increase in feeding, a change in food choice and sleep, and stimulation of the immune system [9][10][11][12][13]. In addition, SP is required for release of stored sperm and imposes costs of mating [14,15].…”

Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females

“…Particularly well studied are the functions and fitness effects of seminal fluid proteins (Sfps) in males [2,18], which cause a substantial reprogramming of female behaviour and physiology [2]. The genomewide profiles of gene expression changes in response to courtship and mating [12,13,16,17] and to the receipt of Sfps [12,15,19] have been investigated. Here, we aimed to capture an in-depth genomic profile of gene expression changes resulting from the transfer of a single Sfp with striking fitness effects [20 -26], the sex peptide (SP).…”

Molecular and cellular components of the mating machinery in Anopheles gambiae females

“…Across a number of microarray studies, only 1 functional class shows a consistently strong response to mating: immune genes, in particular antimicrobial peptides (AMPs), are highly induced (5)(6)(7)(8)(9)(10). In the only other insect analyzed to date, the honey bee Apis mellifera, mating mainly causes transcriptional changes in genes associated with egg production in the ovaries (11).…”