Abstract
During embryonic development, most organs are in a state of mechanical compression because they grow in a confined and limited amount of space within the embryo’s body; the early gut is an exception because it physiologically herniates out of the coelom. We demonstrate here that physiological hernia is caused by a tensile force transmitted by the vitelline duct on the early gut loop at its attachment point at the umbilicus. We quantify this tensile force and show that applying tension for 48 h induces stress-dependent elongational growth of the embryonic gut in culture, with an average 90% length increase (max: 200%), 65% volume increase (max: 160%), 50% dry mass increase (max: 100%), and 165% cell number increase (max: 300%); this mechanical cue is required for organ growth as guts not subject to tension do not grow. We demonstrate that growth results from increased cell proliferation when tension is applied. These results outline the essential role played by mechanical forces in shaping and driving the proliferation of embryonic organs.
Highlights
We find that the mesentery + omphalomesenteric artery (OMA) absorbs ~25% of the total force transmitted via the vitelline duct; each gut branch is subject to a minimal tension of 3.4–6.6 μN
Our results suggest that in-ovo mechanical tension transmitted by the vitelline duct and omphalomesenteric artery on the embryonic gut plays an important role in shaping this embryonic organ by driving proliferation, elongation and providing free space outside of the embryo body for the organ to grow unimpeded
We found that applying mechanical tension to the embryonic gut in culture is necessary to induce its growth; guts not subject to tension did not grow
Summary
We demonstrate here that physiological hernia is caused by a tensile force transmitted by the vitelline duct on the early gut loop at its attachment point at the umbilicus. We quantify this tensile force and show that applying tension for 48 h induces stressdependent elongational growth of the embryonic gut in culture, with an average 90% length increase (max: 200%), 65% volume increase (max: 160%), 50% dry mass increase (max: 100%), and 165% cell number increase (max: 300%); this mechanical cue is required for organ growth as guts not subject to tension do not grow. We question here the influence of mechanical forces on embryonic gut overall growth and shape
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