Abstract
Dietary nutrients provide macromolecules necessary for organism growth and development. In response to animal feeding, evolutionarily conserved growth signaling pathways are activated, leading to increased rates of cell proliferation and tissue growth. It remains unclear how different cell types within developing tissues coordinate growth in response to dietary nutrients and whether coordinated growth of different cell types is necessary for proper tissue function. Using the early Drosophila larval brain, we asked whether nutrient-dependent growth of neural stem cells (neuroblasts), glia, and trachea is coordinated and whether coordinated growth among these major brain cell types is required for neural development. It is known that in response to dietary nutrients and PI3-kinase activation, brain and ventral nerve cord neuroblasts reactivate from quiescence and ventral nerve cord glia expand their membranes. Here, we assay growth in a cell-type specific manner at short time intervals in the brain and determine that growth is coordinated among different cell types and that coordinated growth is mediated in part through activation of PI3-kinase signaling. Of the 7 Drosophila insulin-like peptides (Dilps), we find that Dilp-2 is required for PI3-kinase activation and growth coordination between neuroblasts and glia in the brain. Dilp-2 induces brain cortex glia to initiate membrane growth and make first contact with quiescent neuroblasts. Once reactivated, neuroblasts promote cortex glia growth to ultimately form a selective membrane barrier. Our results highlight the importance of bidirectional growth signaling between neural stem cells and surrounding cell types in the brain in response to nutrition and demonstrate how coordinated growth among different cell types drives tissue morphogenesis and function.
Highlights
Organs must be appropriately sized and patterned to function properly and meet physiological needs of adult animals
We find that Drosophila insulin-like peptide 2 (Dilp-2) mediates PI3-kinase activation in neuroblasts and glia and that Dilp-2–mediated PI3-kinase activity is required to coordinate the growth of central brain neuroblasts with the development of their cortex glial niche
Glial growth in the central brain is reduced when PI3-kinase levels are reduced in neuroblasts, a result reported in the ventral nerve cord as well [23]
Summary
Organs must be appropriately sized and patterned to function properly and meet physiological needs of adult animals. To achieve proper organ size and function, a multitude of different cell types are produced over time and in space. It remains unclear how different cell types with different molecular programs integrate their own growth with that of their nearby neighbors, some of which have different developmental origins. This is true for stem cells, many of which reside within specialized microenvironments composed of many different cell types. Dietary nutrients play important roles in growth regulation because they provide the building blocks for biosynthesis of macromolecules (lipids, proteins, and nucleic acids) and serve as cofactors used in metabolic reactions
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