Three-Dimensional Structure of the Rat Intestinal Wall (Mucosa and Submucosa)

Abstract

The three-dimensional organization of the mucosa and submucosa of the rat intestine was analysed by scanning electron microscopy (SEM) aided by microdissection methods. New functional aspects raised by the SEM observations were examined by transmission electron microscopy (TEM). Morphogenesis of the intestinal villi was also illustrated three dimensionally. Removal of the epithelium by osmic acid maceration revealed the presence of many round fenestrations averaging 3 μm in diameter over the villous basal lamina. TEM confirmed that they were not artifacts but represented passages or tracks of cells of the immune system such as lymphocytes, eosinophils and macrophages. Penetration of the epithelial processes into the lamina propria was also observed. Close contacts between these free cells and the epithelial cells suggest an intercellular communication between these different cell types. The basal lamina is thus appears as a structure that allows dynamic interaction between the epithelial layer and the lamina propria, though it is generally regarded as a rigid structure acting as a barrier. Beneath the basal lamina, a cellular reticulum of fibro-blast-like cells overlies the capillary network in the villi. These cells are characterized by bundles of actin filaments and contact with each other by gap junctions. This cellular reticulum probably influences the absorption of nutrients from the villi by its contractile ability in addition to its supportive role. A similar cellular network occurs beneath the epithelium of the intestinal glands. These cells may also mechanically support the glandular organization, maintaining the delicate microvascular bed. The submucosa is considered the skeleton of the intestine. SEM reveals the main framework of the submucosa is as being composed of two sets of collagen fibers running diagonally around the intestinal wall, one set in a clockwise direction, the other, counter-clockwise. These fibers - in different arrays - interweave to form a lattice sheet, which presumably provides the tissue with a high resistance to mechanical forces, particularly in respect to radial forces. The diagonal orientation of the collagen fibers is essential for the flexibility of the submucosa in allowing deformation of the intestinal wall during peristalsis. Despite the nonelastic nature of the collagen fibers, the submucosa can adapt to the various shapes of the intestinal lumen by simply changing the angles formed by these fibers. Structures of the villous microcirculation, the muscularis mucosae and of the submucous plexus are also discussed. © 1990, International Society of Histology and Cytology. All rights reserved.