Summary
The topographical distribution of cations, anions and polyanions in the guinea-pig stomach has been studied by ultrastructural cytochemical methods. After fixation with the pyroantimonate-osmium tetroxide solution, variable-sized precipitates were localized in the basolateral extracellular space bordering parietal cells or chief cells but not in that bordering mucus-secreting cells. The basal lamina of all gastric cells disclosed a continuous layer of heavy antimonate deposits. Parietal cells disclosed uniformly fine deposits also on the apical plasmalemma both at the main lumen and in the intracellular canaliculi, and revealed, as well, coarse precipitates in the mitochondria. Fixation with a silver acetate-osmium tetroxide solution yielded nitric acid-resistant, silver deposits confined to the luminal surface of the apical plasmalemma in the main lumen and intracellular canaliculi, the lateral intercellular space, the outer surface of the basal plasmalemma and the basal lamina of the parietal cell.
Staining with dialyzed iron demonstrated a glycocalyx rich in acid mucosubstance on the basolateral plasmalemma but not on the apical plasmalemma of parietal cells. In contrast, acid glycoconjugate was visualized on the apical plasmalemma of isthmus cells, mucous neck cells and the transitional cell between isthmus and mucous neck cells but little or no acidic glycoconjugate was demonstrated on the basolateral plasmalemma of these cells. The entire plasmalemma of gastroendocrine cells, unlike other epithelial cells, stained uniformly for acidic glycoconjugate. The dialyzed iron and high iron diamine methods stained the outer compartment of mitochondria in parietal cells intensely and that in other gastric cells lightly. These reagents stained the basal lamina of all gastric cells as did ruthenium red. The several characteristic cytochemical properties of parietal cells presumably relate to the unique secretory activity of these cells and are consistent with the view of the intracellular canaliculi of the parietal cell as the main route for hydrogen and chloride ion secretion.
Similar content being viewed by others
References
Bordi C, Perrelet A (1978) Orthogonal arrays of particles in plasma membranes of the gastric parietal cell. Anat Rec 192:297–304
Chang H, Saccomani G, Rabon E, Schackmann R, Sachs G (1977) Proton transport by gastric membrane vesicles. Biochim Biophys Acta 464:313–327
Cotlove E, Hogben CAM (1956) Spatially oriented heterogeneity of chloride exchange across epithelial cell surfaces of gastric mucosa. Fed Proc 15:41 (abst.)
Cotlove E, Green ND, Hogben CAM (1959) Localization of chloride transport in the gastric mucosa. Fed Proc 18:31 (abst.)
Dermietzel R (1974) Junctions in the central nervous system of cat. III. Gap junctions and membrane-associated orthogonal particle complexes (MOPC) in astrocytic membranes. Cell Tissue Res 149:121–135
Ellisman MH, Rash JE, Staehelin LA, Porter KR (1976) Studies of excitable membranes. II. A comparison of specializations at neuromuscular junctions and nonjunctional sarcolemmas of mammalian fast and slow twitch muscle fibers. J Cell Biol 68:752–774
Firth JA (1980) Recently characterized plasma membrane adenosine triphosphatases. VIth International Histochemistry and Cytochemistry Congress. Brighton, England, Program 119a
Firth JA, Bock R (1976) Distribution and properties of an adenosine triphosphatase in the tanycyte ependyma of the IIIrd ventricle of the rat. Histochem 47:145–157
Forte JG, Lee HC (1977) Gastric adenosine triphosphatases: a review of their possible role in HCl secretion. Gastroenterology 73:921–926
Forte JG, Fiorte GM, Saltman P (1967) K+-stimulated phosphatase of microsomes from gastric mucosa. J Cell Physiol 69:293–304
Forte TM, Machen TE, Forte JG (1977) Ultrastructural changes in oxyntic cells associated with secretory function: a membrane-recycling hypothesis. Gastroenterology 73:941–955
Ganser Al, Forte JG (1973) K+-stimulated ATPase in purified microsomes of bullfrog oxyntic cells. Biochim Biophys Acta 307:169–180
Grand RJ, Spicer SS (1967) Preliminary studies on the electron microscopic localization of sites of sodium transport in the human eccrine sweat gland. Proceedings of the 4th International Conference on Cystic Fibrosis of the Pancreas (Mucoviscidosis), Berneρindelwald 1966, Part I, Mod Probl Pediat. Karger, Basel New York, Vol 10, pp 100–106
Hardin JH, Spicer SS (1971) Ultrastructural localization of dialyzed ironreactive mucosubstance in rabbit heterophils, basophils, and eosinophils. J Cell Biol 48:368–386
Helander HF Hirschowitz BI (1974) Quantitative ultrastructural studies on inhibited and on partly stimulated gastric parietal cells. Gastroenterology 67:447–451
Humbert F, Pricam C, Perrelet A, Orci L (1975) Specific membrane differentiations in the cells of the kidney collecting tubule. J Ultrastruct Res 52:13–20
Ito S, Schofield GC (1974) Studies on the depletion and accumulation of microvilli and changes in the tubulovesicular compartment of mouse parietal cells in relation to gastric acid secretion. J Cell Biol 63:364–382
Katsuyama T, Spicer SS (1977) A cation-retaining layer in the alveolar-capillary membrane. Lab Invest 36:428–435
Katsuyama T, Poon KC, Spicer SS (1977) The ultrastructural histochemistry of the basement membranes of the exocrine pancreas. Anat Rec 188:371–386
Klein RL, Horton CR, Klein ÅT (1970) Studies on nuclear amino acid transport and cation content in embryonic myocardium of the chick. Am J Cardiol 25:300–310
Komnick H (1962) Elektronenmikroskopische Lokalisation von Na+ und Cl- in Zellen und Geweben. Protoplasma 55:414–418
Komnick H, Bierther M (1969) Zur histochemischen Ionenlokalisation mit Hilfe der Elektronenmikroskopie unter besonderer Berücksichtigung der Chloridreaktion. Histochemie 18:337–362
Komnick H, Komnick U (1963) Elektronenmikroskopische Untersuchungen zur funktionellen Morphologie des Ionentransportes in der Salzdrüse von Larus argentatus. V. Teil. Experimenteller Nachweis der Transportwege. Z Zellforsch 60:162–203
Landis DMD, Reese TS (1974) Arrays of particles in freeze-fractured astrocytic membranes. J Cell Biol 60:316–320
Luft JH (1971) Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat Rec 171:347–368
Martin BJ, Philpott CW (1974) The biochemical nature of the cell periphery of the salt gland secretory cells of fresh and salt water adapted mallard ducks. Cell Tissue Res 150:193–211
Michelangeli F (1978) Acid secretion and intracellular pH in isolated oxyntic cells. J Membr Biol 38:31–50
Mizuhira V (1972) Electronmicroscopic histo and cytochemistry. I. Electron microscopic visualization of low molecular weight material, especially electrolytes. In: Electron microscopy; its application to medical biology. Ishiyaku Publication Co., Tokyo, pp 142–145
Mizuhira V, Nakamura H, Yotsumoto H, Namae T (1972) An application of the electron probe x-ray microanalyzer to the biological sections. II. Chloride and some other elemental distribution in the gastric mucosal epithelium. Histochemistry and Cytochemistry, Proceedings of the 4th International Congress of Histochemistry and Cytochemistry. Kyoto, Japan, pp 275–276
Moody FG (1972) Water flow through gastric secretory mucosa. In: Sachs G, Heinz E, Ullrich KJ (eds) Gastric secretion. Academic Press, New York London, pp 432–452
Rinehart JF, Abul-Haj SK (1951) An improved method for histologic demonstration of acid mucopolysaccharides in tissues. AMA Arch Pathol 52:189–194
Sachs G, Shah G, Strych A, Cline G, Hirschowitz BI (1972) Properties of ATPase of gastric mucosa. III. Distribution of HCO 3/-stimulated ATPase in gastric mucosa. Biochim Biophys Acta 266:625–638
Sachs G, Chang H, Rabon E, Shackman R, Sarau HM, Saccomani G (1977) Metabolic and membrane aspects of gastric H+ transport. Gastroenterology 73:931–940
Sato A, Spicer SS (1980) Ultrastructural cytochemistry of complex carbohydrates of gastric epithelium in the guinea pig. Am J Anat 159:307–329
Sato A, Spicer SS (1981) An ultrastructural assessment of mitochondria in the gastric parietal cell with the high iron diamine method. Histochem J, in press
Sato A, Spicer SS, Tashian RE (1981) Ultrastructural localization of carbonic anhydrase in gastric parietal cells with the immunoglobulin-enzyme bridge method. Histochem J, in press
Sedar AW (1965). Fine structure of the stimulated oxyntic cell. Fed Proc 24:1360–1367
Shiina S, Mizuhira V, Amakawa T, Futaesaku Y (1970) An analysis of the histochemical procedure for sodium ion detection. J Histochem Cytochem 18:644–649
Simson JAV, Spicer SS (1975) Selective subcellular localization of cations with variants of the potassium (pyro) antimonate technique. J Histochem Cytochem 23:575–598
Spicer SS, Swanson AA (1972) Elemental analysis of precipitates formed in nuclei by antimonateosmium tetroxide fixation. J Histochem Cytochem 20:518–526
Spicer SS, Hardin JH, Setser ME (1978) Ultrastructural visualization of sulphated complex carbohydrates in blood and epithelial cells with the high iron diamine procedure. Histochem J 10:435–452
Spicer SS, Sannes PL, Katsuyama T (1979) Cytochemical characterization of secretory and cell surface glycoconjugates by light and electron microscopy. J Histochem Cytochem 27:1182–1184
Sugai N, Ito S (1980) Carbonic anhydrase, ultrastructural localization in the mouse gastric mucosa and improvements in the technique. J Histochem Cytochem 28:511–525
Torack RM, LaValle M (1970) The specificity of the pyroantimonate technique to demonstrate sodium. J Histochem Cytochem 18:635–643
Ussing HH, Erlij D, Lassen U (1974) Transport pathways in biological membranes. Ann Rev Physiol 36:17–49
Van Harreveld A, Potter RL (1961) Histochemical differentiation of chloride from other ions precipitated by silver nitrate in freeze-substitution fixation. Stain Technol 36:185–193
Villegas L (1962) Cellular location of the electrical potential difference in frog gastric mucosa. Biochim Biophys Acta 64:359–367
Wolf S (1965) Gastric secretions. In: The stomach. Oxford University Press, New York, pp 53–79
Yarom R, Chandler JA (1974) Electron probe microanalysis of skeletal muscle. J Histochem Cytochem 22:147–154
Yarom R, Meiri U (1973) Pyroantimonate precipitates in frog skeletal muscle: Changes produced by alterations in compositon of bathing fluid. J Histochem Cytochem 21:146–154
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sato, A., Spicer, S.S. Subcellular distribution of ionic components in gastric mucosa of the guinea pig. Cell Tissue Res. 219, 143–158 (1981). https://doi.org/10.1007/BF00210024
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00210024