Dynamics of epithelial cells in the corpus of the mouse stomach. II. Outward migration of pit cells

Abstract

The pit cells (or surface mucous cells) present along pit walls and gastric surface have been investigated by electron microscopy and radioautography after a pulse or continuous infusion of 3 H‐thymidine. For these studies, the pit region has been subdivided into four segments: three of equal length along the pit wall, respectively named low pit, mid pit and high pit, and a last one at the surface named pit top. The pit region includes an average of 37 pit cells, characterized by dense mucous granules accumulated along the apical membrane in an organelle‐free zone referred to as ectoplasm. Continuous 3 H‐thymidine infusion reveals that pit cells come from pre‐pit cells, which are believed to arise in the isthmus region from the undifferentiated granule‐free cells through a pre‐pit cell precursor stage. The pre‐pit cells, characterized by the presence of a few mucous secretory granules scattered in the cytoplasm, migrate outward (i.e., in the direction of the gastric lumen). When the secretory granules line up along the apical membrane in the ectoplasm, the pre‐pit cell becomes pit cell. It is estimated that 87% of pit cells differentiate from pre‐pit cells, while the remaining 13% come from their own mitoses. Observations at successive times after a 3 H‐thymidine pulse demonstrate that pit cells, like pre‐pit cells, migrate toward the gastric surface where they are eventually lost. The continuous 3 H‐thymidine infusion results indicate that this migration takes 3.1 days on the average. Cells spend almost a day in each pit wall segment. In the low pit segment, cells produce more and larger mucous secretory granules than do pre‐pit cells. In the mid and high pit segments, the number and size of the granules generally keeps on increasing, thus indicating that mucous differentiation is progressing. The secretory granules arising in the Golgi apparatus of pit wall cells are mostly spherical; they retain this shape during the few minutes taken to cross the cytoplasm and enter the apical ectoplasm. They spend about an hour in the ectoplasm, where they change to an ovoid shape as they approach the apical membrane to finally release their content by exocytosis. The mucous differentiation along the pit wall is associated with a progressive decline in the organelles: nucleoli and mitochondria decrease in size while the amount of free ribosomes diminishes. When pit cells reach the free surface, they produce fewer, smaller secretory granules and at a lower rate than in mid and high pit. Meanwhile, organelles decline further, while mitochondria tend to swell and disintegrate. Clearcut signs of degeneration appear in some of the cells. These cells find their way into the gastric lumen either by direct extrusion or indirectly after being phagocytosed by a neighbor cell which is itself eventually extruded. Thus a sequence of cells—the pit cell lineage—derived from the stationary undifferentiated granule‐free cells, includes pre‐pit cell precursors, pre‐pit cells, and pit cells, which all migrate in the direction of the gastric lumen, where pit cells are eventually lost. © 1993 Wiley‐Liss, Inc.