Abstract Gap junctions allow the exchange of small molecules between cells. How this function could be used to promote cell growth has never been explored. During Drosophila ovarian follicle development, germ cells, which are surrounded by epithelial somatic cells, undergo massive growth. We found that this growth depends on gap junctions between these cell populations, with a requirement for Innexin4 and Innexin2, in the germ cells and the somatic cells, respectively. Somatic cells express enzymes and transporters involved in amino acid metabolism that are absent in germ cells. Among them, we identified a proline transporter required for germline growth. Its ectopic expression in the germline can compensate for its absence in somatic cells, confirming the metabolic exchange between these cell types. Moreover, in somatic cells, innexin2 expression and gap junction assembly are regulated by the insulin receptor/PI3K kinase pathway. Altogether these data illustrate how metabolic exchange through gap junctions can promote cell growth and how such mechanism can be integrated into a developmental programme, coupling growth control by extrinsic systemic signals with the intrinsic coordination between cell populations. Summary statement We demonstrate that gap junction-dependent metabolic flow from a cell population to another promotes cell growth and can be regulated to coordinate cell growth.

Gap junction-dependent amino acid transfer promotes germ cell growth