Journal Article

Endocrine remodelling of the adult intestine sustains reproduction in Drosophila

Cognigni, Paola, Reiff, Tobias, Miguel-Aliaga, Irene, Yew, Joanne Y, Antonello, Zeus, Dominguez, Maria, Jacobson, Jake, Tan, Kah Junn, Ballesta, Esther

2015

Overview

The production of offspring is energetically costly and relies on incompletely understood mechanisms that generate a positive energy balance. In mothers of many species, changes in key energy-associated internal organs are common yet poorly characterised functionally and mechanistically. In this study, we show that, in adult Drosophila females, the midgut is dramatically remodelled to enhance reproductive output. In contrast to extant models, organ remodelling does not occur in response to increased nutrient intake and/or offspring demands, but rather precedes them. With spatially and temporally directed manipulations, we identify juvenile hormone (JH) as an anticipatory endocrine signal released after mating. Acting through intestinal bHLH-PAS domain proteins Methoprene-tolerant (Met) and Germ cell-expressed (Gce), JH signals directly to intestinal progenitors to yield a larger organ, and adjusts gene expression and sterol regulatory element-binding protein (SREBP) activity in enterocytes to support increased lipid metabolism. Our findings identify a metabolically significant paradigm of adult somatic organ remodelling linking hormonal signals, epithelial plasticity, and reproductive output. Producing offspring places extra energy demands on individuals. Female animals—which generally invest more time and resources than the males—need to ensure that sufficient nutrients reach their offspring during pregnancy and lactation. The small intestines of many female animals increase in size during this period, but it is not clear to what extent these changes help to maximise reproduction, or how they are regulated. Reiff, Jacobson, Cognigni, Antonello et al. investigated what happens to the middle section of the gut in female fruit flies after mating. A fly's ‘midgut’ performs a similar role to the small intestine in humans and other mammals. The experiments show that mating increases the numbers of cells in the midgut so that it increases in size. These changes are due to a hormone called ‘juvenile hormone’, which is released after the fly mates. In particular cells of the midgut, juvenile hormone also regulates some genes involved in the metabolism of lipids. If the activity of juvenile hormone is blocked in these cells, the female flies produce fewer eggs. These changes in the midgut still happen in mutant flies that cannot produce eggs and don't increase their food intake after they mate. Therefore, the changes appear to prepare flies for the increased nutritional demands rather than being caused by it. Altogether, these findings reveal that changes in the midgut play an important role in the ability of female fruit flies to reproduce. Similar changes to the gut may also increase reproductive success in humans and other mammals. However, if the changes are maintained after reproduction, it is possible that they may contribute to weight gain and an increased risk of cancer in females after pregnancy.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animal reproduction / Animals / Developmental Biology and Stem Cells / Drosophila / Drosophila - physiology / Energy balance / Enterocytes / Fatty acids / Females / Gene expression / Insects / Intestine / Intestines - drug effects / Intestines - growth & development / Juvenile hormones / Juvenile Hormones - metabolism / Lipid metabolism / Mammals / Mating / Methoprene / Midgut / Offspring / organ plasticity / Physiology / Reproduction / stem cell / Stem cells / Sterol regulatory element-binding protein / Sterols