Editors' ChoicePhysiology

An insulin-like message from mother

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Science Signaling  14 Mar 2017:
Vol. 10, Issue 470, eaan1464
DOI: 10.1126/scisignal.aan1464

Nematodes experiencing osmotic stress signal to the germ-line to prepare their offspring.

When organisms experience stressful conditions, it can influence how their offspring will respond to the same stressor, either adaptively or maladaptively. After the nematode Caenorhabditis elegans is exposed to osmotic stress, its offspring can tolerate much greater osmotic stress. Burton et al. examined how this response to environmental conditions is transmitted to offspring. Worms resisted osmotic stress by reversibly arresting their larval development until normal osmotic conditions were restored. Protective developmental arrest required DAF-16, a FOXO transcription factor that is activated in response to reduced insulin-like signaling and induces a similar developmental arrest response to nutrient limitation. Offspring of parents with constitutively reduced insulin-like signaling tolerated high osmotic conditions without arrested development, similarly to offspring of osmotically stressed parents. Tolerance in the offspring of parents with reduced insulin signaling required glycerol-3-phosphate dehydrogenase (GPDH-2), an enzyme that catalyzes the rate-limiting step in glycerol biosynthesis, in the offspring (but not in the parents), suggesting that maternal insulin-like signaling influences glycerol production in embryos. Indeed, worms with mutations that conferred constitutive tolerance of osmotic stress had increased expression of gpdh2 and concentrations of glycerol. Germline-specific expression of genes involved in insulin-like signaling confirmed that the activation of glycerol production in the offspring by either parental osmotic stress or constitutively reduced insulin-like signaling in the parents occurred through inhibition of parental insulin-like signaling in the germ cells. Because insulin signaling is involved in human metabolic diseases, the development of some of which is also influenced by the conditions experienced in previous generations, these results suggest mechanisms through which information about parental environments can influence offspring physiology. Kaneshiro and Strome discuss the connections that can be drawn between basic research on model organisms and biomedical applications.

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