Abstract
SummaryDuring development, multicellular organisms undergo stereotypical patterns of tissue growth in space and time. How developmental growth is orchestrated remains unclear, largely due to the difficulty of observing and quantitating this process in a living organism. Drosophila histoblast nests are small clusters of progenitor epithelial cells that undergo extensive growth to give rise to the adult abdominal epidermis and are amenable to live imaging. Our quantitative analysis of histoblast proliferation and tissue mechanics reveals that tissue growth is driven by cell divisions initiated through basal extracellular matrix degradation by matrix metalloproteases secreted by the neighboring larval epidermal cells. Laser ablations and computational simulations show that tissue mechanical tension does not decrease as the histoblasts fill the abdominal epidermal surface. During tissue growth, the histoblasts display oscillatory cell division rates until growth termination occurs through the rapid emergence of G0/G1 arrested cells, rather than a gradual increase in cell-cycle time as observed in other systems such as the Drosophila wing and mouse postnatal epidermis. Different developing tissues can therefore achieve their final size using distinct growth termination strategies. Thus, adult abdominal epidermal development is characterized by changes in the tissue microenvironment and a rapid exit from the cell cycle.
Highlights
During development, tissue growth must be tightly coordinated in time and space.[1,2,3] due to the difficulty of measuring quantitative growth parameters in living organisms, we lack the ability to analyze factors that dictate developmental growth with the high level of precision achieved in expanding populations of unicellular organisms or animal cells in culture.[4,5] For instance, while much evidence links proliferation rates with cell geometry, mechanical tension, and compression,[3,6] this relationship has not been systematically examined throughout the growth of a model tissue
Our quantitative analysis of histoblast proliferation and tissue mechanics reveals that tissue growth is driven by cell divisions initiated through basal extracellular matrix degradation by matrix metalloproteases secreted by the neighboring larval epidermal cells
Laser ablations and computational simulations show that tissue mechanical tension does not decrease as the histoblasts fill the abdominal epidermal surface
Summary
Tissue growth must be tightly coordinated in time and space.[1,2,3] due to the difficulty of measuring quantitative growth parameters in living organisms, we lack the ability to analyze factors that dictate developmental growth with the high level of precision achieved in expanding populations of unicellular organisms or animal cells in culture.[4,5] For instance, while much evidence links proliferation rates with cell geometry, mechanical tension, and compression,[3,6] this relationship has not been systematically examined throughout the growth of a model tissue. The recent development of analytical tools that capture cell and tissue deformations,[8,9] combined with progress in live imaging in vivo,[10] have transformed our ability to derive quantitative parameters that can be used to understand and model complex developmental processes. Drosophila histoblasts are a population of precursor cells that give rise to the adult abdominal epidermis, and whose growth occur mainly during the pupal stages when the animal is sessile (Figure 1A). Histoblasts are amenable to live imaging during their entire growth period and are an ideal system to exploit tools developed for analyzing tissue deformation.[12,13,14]
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