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The transfer of complex mixtures of signals and nutrients between individuals is a key step in several biologically important events in our lives, such as breastfeeding and sexual intercourse. However, we know relatively little about the ways in which the molecular gifts involved are packaged to ensure their successful delivery to the recipient.

Seminal fluid in the male accessory gland is full of elliptical lipid-containing microcarriersBy studying such events during mating in the fruit fly, researchers at the University of Oxford have identified a new communication mechanism in which nutrients and signals are combined in fatty droplets that stably store their bioactive cargos in males, until they are transferred to females when they dissipate within minutes. These specialised multi-molecular assemblies called microcarriers, are made by the prostate-like accessory gland of the male and contain a central fatty (lipid) core wrapped with multiple proteins, including a molecule called Sex Peptide. When Sex Peptide is released in the mated female, it stimulates her to produce more progeny and reprogrammes her brain so she rejects other male suitors.

The remarkable role of Sex Peptide in mediating this form of sexual conflict has been recognised for several decades. However, it has been unclear how this peptide can remain stable in the secretions of the male accessory gland, then rapidly become biologically active in the female uterus. The contrasting behaviour of microcarriers in the male and female reproductive tracts provides the answer to that question. Even more surprisingly, analysis of males that lack Sex Peptide reveals that this protein provides an essential part of the wrapping that shapes these reproductive gifts. In its absence, the male accessory gland becomes filled with giant lipid droplets that do not dissipate properly when transferred to females, partly explaining the inability of these males to reprogramme female behaviour after mating.

Although Sex Peptide is only produced by a limited group of fruit fly species, lipids and lipid droplets are secreted by many glands, including the human prostate and breast. Preliminary work in flies suggests that one of the genes that is essential for the release of microcarriers from secreting cells also plays a critical role in human glands, including the breast. In fact, this regulatory gene is highly expressed in some breast cancers. This suggests that the mechanisms controlling microcarrier formation may be evolutionarily conserved and that microcarriers may play much broader roles in physiological and pathological cell-cell communication, which have yet to be recognised.

“We are increasingly appreciating that signals between cells can be packaged in complex multi-molecular structures, such as membrane-bounded vesicles, but the identification of a structured lipid droplet as a carrier for such signals was really unexpected”, commented Professor Clive Wilson, who led the research. “And it was even more of a surprise when we realised that a key signal on the surface of these microcarriers is also vital in determining their shape. Our data suggest that this might be a more evolutionarily ancient function for Sex Peptide, raising the possibility that some signals can evolve from molecules that originally had structural functions. Microcarriers are of particular interest, because their properties allow them to store and then rapidly dissipate their cargos, which might be an ideal combination for signals in seminal fluid and breast milk that need to be rapidly dispersed and activated when transferred from one individual to another”

The study was a collaboration between the groups of Professor Clive Wilson and Associate Professor Deborah Goberdhan from the Department of Physiology, Anatomy and Genetics. This work has been supported by funding from the Biotechnology and Biological Sciences Research Council (BBSRC), Cancer Research UK, the Wellcome Trust and the Medical Research Council.

The full paper "Drosophila Sex Peptide Controls the Assembly of Lipid Microcarriers in Seminal Fluid" is available to read on the PNAS journal website.

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