Material properties of the embryonic small intestine during buckling morphogenesis

During embryonic development, tissues undergo dramatic deformations as functional morphologies are stereotypically sculpted from simple rudiments. Formation of healthy, functional organs therefore requires tight control over the material properties of embryonic tissues during development, yet the biological basis of embryonic tissue mechanics is poorly understood. The present study investigates the mechanics of the embryonic small intestine, a tissue that is compactly organized in the body cavity by a mechanical instability during development, wherein differential elongation rates between the intestinal tube and its attached mesentery create compressive forces that buckle the tube into loops. The wavelength and curvature of these loops are tightly conserved for a given species. Focusing on the intestinal tube, we combined micromechanical testing with histologic analyses and enzymatic degradation experiments to conclude that elastic fibers closely associated with intestinal smooth muscle layers are responsible for the bending stiffness of the tube, and for establishing its pronounced mechanical anisotropy. These findings provide insights into the developmental role of elastic fibers in controlling tissue stiffness, and raise new questions on the physiologic function of elastic fibers in the intestine during adulthood.

Statement of Significance

The functional form of adult organs is established during embryogenesis through the action of physical forces on tissues with precise material properties. Despite this, however, biological control of material properties during embryogenesis is poorly understood. Focusing on the small intestine, we identified elastic fibers - rather than oriented smooth muscle - as defining bending stiffness, prescribing the lengthy intestine to be buckled precisely into compact loops for proper placement within the body cavity. We revealed a role for elastin in storing elastic energy during cell contraction, highlighting a potential role for elastin in gut motility through the ability to resist cyclic deformations associated with peristalsis. These results provide insights into intestinal development and adult function, and highlight elastin's diverse roles during organogenesis.