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Mechanical Tension Drives Elongational Growth of the Embryonic Gut

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Journal Sci Rep
Specialty Science
Date 2018 Apr 18
PMID 29662083
Citations 3
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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.

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References
1.
Safford S, Freemerman A, Safford K, Bentley R, Skinner M . Longitudinal mechanical tension induces growth in the small bowel of juvenile rats. Gut. 2005; 54(8):1085-90. PMC: 1774906. DOI: 10.1136/gut.2004.061481. View

2.
Chaturvedi L, Gayer C, Marsh H, Basson M . Repetitive deformation activates Src-independent FAK-dependent ERK motogenic signals in human Caco-2 intestinal epithelial cells. Am J Physiol Cell Physiol. 2008; 294(6):C1350-61. PMC: 3971650. DOI: 10.1152/ajpcell.00027.2008. View

3.
Hearn C, Young H, Ciampoli D, Lomax A, Newgreen D . Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev Dyn. 1999; 214(3):239-47. DOI: 10.1002/(SICI)1097-0177(199903)214:3<239::AID-AJA7>3.0.CO;2-O. View

4.
Geske M, Zhang X, Patel K, Ornitz D, Stappenbeck T . Fgf9 signaling regulates small intestinal elongation and mesenchymal development. Development. 2008; 135(17):2959-68. PMC: 2678066. DOI: 10.1242/dev.020453. View

5.
Cheeseman B, Zhang D, Binder B, Newgreen D, Landman K . Cell lineage tracing in the developing enteric nervous system: superstars revealed by experiment and simulation. J R Soc Interface. 2014; 11(93):20130815. PMC: 3928926. DOI: 10.1098/rsif.2013.0815. View