Morphological studies on the translocation of tubulovesicular system toward the intracellular canaliculus during stimulation of the gastric parietal cell

Abstract

The gastric parietal has two characteristic membrane systems. One is the intracellular canaliculus, which is specialized networks of enfolded luminal membrane channels lined with numerous microvilli. The other structures common to all parietal cells are the tubulovesicles or the tubulovesicular membranes, a system of tubules and vesicles. The tubulovesicular compartment is drastically depleted during maximal gastric acid secretion and this is coincident with an increase in the canalicular cell surface membrane. A plausible explanation for this redistribution is the fusion and transfer of tubulovesicular membranes to the plasma membrane. However, for many years there was no convincing evidence of connections between these two membrane systems. The mechanism of the transformation of tubulovesicular membrane into the plasma membrane without demonstrable connections has been an enigma to electron microscopists. Using a recently developed fixation technique for parietal cells [Sugai et al. (1995) Acta Anat Nippon 74:S101], we have investigated the organization of the cytoplasmic membrane systems in the rat resting and tetragastrin stimulated stomachs by ultra‐high‐resolution scanning electron microscopy (SEM). Gastric mucosae were microwave‐fixed in a cacodylate buffer, (334 milliosmoles/kgH2O (mOsm)), to which 1.0% glutaraldehyde and 0.5% formaldehyde were added. Specimens examined by TEM of thin sections revealed the cytoplasm packed with tubular membranes similar to images detected by rapid‐freeze/freeze‐substitution fixation. To render the cytoplasmic membranes visible by SEM, fixed mucosae were treated by the aldehyde‐osmium‐DMSO‐osmium maceration procedure. With much of the cell matrix and filaments removed, SEM revealed numerous 30–60‐nm tubules, which formed a meshwork with small cisternae. Vesicles or isolated tubules were not found in adequately macerated parietal cells. The cytoplasmic surface of the intracellular canaliculus was smooth except for round openings representing the bases of macerated microvilli. In favorable sites, connections of the tubular membranes to the canaliculi were clearly visible. Stereo pair views were particularly useful to demonstrate these continuities. Connections between these two membrane compartments suggest the probability of rapid membrane transposition. In this article, the form and distribution of membrane systems of parietal cells in the resting state and after tetragastrin stimulation will be presented and discussed. Special emphasis is made to demonstrate connections between the tubulovesicular system and the intracellular canaliculus. Microsc. Res. Tech. 48:282–292, 2000 © 2000 Wiley‐Liss, Inc.

Effect of Nitric Oxide on Histamine-Induced Cytological Transformations in Parietal Cells in Isolated Human Gastric Glands

“…Studies on rat, rabbit, and human parietal cells have demonstrated that histamine induces (1) redistribution of the proton pump H + /K + -ATPase from cytoplasmic localizations to the canalicular membrane, (2) association of F-actin to the canalicular membrane, (3) stimulation-associated colocalization of ezrin and F-actin, and (4) immense expansion or swelling of the canalicular lumen [6,10,11]. Inhibition of gastric acid secretion is often associated with alterations in one or more of these processes [6].…”

“…Furthermore, the number of tubulovesicles was reduced and an elongation of the microvilli at the surface of the canalicular membrane was observed, which tends to indicate that the surface of the canalicular membrane was increased and that a fusion between tubulovesicles and the apical membrane had occurred [10].…”

“…The observed cytological transformations of human parietal cells after histamine stimulation were in accordance with previous animal studies [10,11,19]. Treatment of the glands with the NO donor SNAP prior to the administration of histamine did not seem to alter the histamine-induced rearrangement of the cytoskeleton or to affect the translocation of the proton pump H + /K + -ATPase.…”

H+/K+ ATPase expression in human parietal cells and gastric acid secretion in elderly individuals

“…The other is the tubulovesicular system composed of tubules and vesicles formed by smooth endoplasmic reticulum and a cystic‐like membrane structure, mostly seen in the resting stage. Ogata and Yamasaki investigated the plasma membrane system of rat parietal cells in the resting stage and that stimulated by tetragastrin under electron microscopy and proved the connection between these two plasma membrane systems. The process of acid secretion was powered by mitochondria.…”

Histological study of the effect of leflunomide on fundic mucosa of Adult male albino rat and the possible alleviating effect of L-arginine

“…Dilatation of intracellular canaliculi of parietal cell might be due to the stimulation of the cell by histamine leading to re-arrangement of cytoskeleton and recruitment of (H + /K + -ATPase) rich tubulo-vesicles to the apical membrane expanding the intracellular canaliculi with loss of luminal microvilli (Ogata & Yamasaki, 2000). This dilatation occurs in the active phase of secretion.…”