Summary
Examination of the toad urinary bladder by freeze-fracture electron-microscopy demonstrates structural specialization of the granular cell's luminal membrane compared to its basal membrane. Although both membranes appear to possess about 1,700 intramembranous particles per μm2, those of the luminal membrane tend to be significantly larger in size. In addition, the fracturing properties of the two membranes are markedly different: the majority of particles are found on fracture face B (outer membrane face), in the case of the luminal membrane, and the majority are found on fracture face A (inner membrane face), in the case of the basal membrane. While the two fracture faces of the basal membrane possess a similar distribution of particle sizes, in the case of the luminal membrane the B face was found to possess particles generally larger than those found on the A face. It was established that the probability of luminal membrane particles adhering to face B instead of face A is closely correlated with the size of the particle. The structural specialization of the granular cell's luminal membrane may have an important relationship to the characteristic permeability properties of this membrane and the capacity of this cell type to respond physiologically to the hormone vasopressin.
Similar content being viewed by others
References
Branton, D. 1966. Fracture faces of frozen membranes.Proc. Nat. Acad. Sci. U.S.A. 55:1048
Branton, D. 1967. Fracture faces of frozen myelin.Exp. Cell Res. 45:703
Branton, D. 1969. Membrane structure.Annu. Rev. Pl. Physiol. 20:209
Branton, D., Deamer, D.W. 1972. Membrane structure.Protoplasmatologia II/E/1:1
Carasso, N., Favard, P., Valérien, J. 1962. Variations des ultrastructures dans les cellules épithéliaes de la vessie du crapaud après stimulation par l'harmone neurohypophysaire.J. Microscopie 1:143
Chevalier, J., Bourguet, J., Hugon, J.S. 1974. Membrane associated particles: Distribution in frog urinary bladder epithelium at rest and after oxytocin treatment.Cell Tiss. Res. 152:129
Choi, J.K. 1963. The fine structure of the urinary bladder of the toad,Bufo marinus.J. Cell Biol. 16:53
Civan, M.M., Frazier, H.S. 1968. The site of the stimulatory action of vasopressin on sodium transport in toad bladder.J. Gen. Physiol. 51:589
Danon, D., Strum, J.M., Edelman, I.S. 1974. The membrane surfaces of the toad bladder: Scanning and transmission electron-microscopy.J. Membrane Biol. 16:279
Davis, W.L., Goodman, D.B.P., Martin, J.H., Matthews, J.L., Rasmussen, H. 1974. Vasopressin-induced changes in the toad urinary bladder epithelial surface.J. Cell Biol. 61:544
Dempsey, G.P., Bullivant, S., Watkins, W.B. 1973. Endothelial cell membranes: Polarity of particles as seen by freeze-fracturing.Science 179:190
DiBona, D.R., Civan, M.M., Leaf, A. 1969. The cellular specificity of the effect of vasopressin on toad urinary bladder.J. Membrane Biol. 1:79
Gfeller, E., Walser, M. 1971. Stretch-induced changes in geometry and ultrastructure of transporting surfaces of toad bladder.J. Membrane Biol. 4:16
Glover, A.J., Garvitch, Z.S. 1974. The freezing rate of freeze-etch specimens for electron microscopy.Cryobiology 11:248
Keller, A.R. 1963. A histochemical study of the toad urinary bladder.Anat. Rec. 147:367
Macknight, A.D.C., Leaf, A., Civan, M.M. 1971. Effects of vasopressin on the water and ionic composition of toad bladder epithelial cells.J. Membrane Biol. 6:127
MacLennan, D.H., Seeman, P., Iles, G.H., Yip, C.C. 1971. Membrane formation by the adenosine triphosphatase of sarcoplasmic reticulum.J. Biol. Chem. 246:2702
Masur, S.K., Holtzman, E., Walter, R. 1972. Hormone-stimulated exocytosis in the toad urinary bladder.J. Cell Biol. 52:211
Misra, D.N., Das Gupta, N.N. 1966. Distortion in dimensions produced by shadowing for electron microscopy.J. R. Micr. Soc. 84:373
Ojakian, G.K., Satir, P. 1974. Particle movements in chloroplast membranes: Quantitative measurements of membrane fluidity by the freeze-fracture technique.Proc. Nat. Acad. Sci. U.S.A. 71:2052
Orci, L., Perrelet, A. 1973. Membrane-associated particels: Increase at sites of pinocytosis demonstrated by freeze etching.Science 181:868
Peachey, L.D., Rasmussen, H. 1961. Structure of the toad's urinary bladder as related to its physiology.J. Biophys. Biochem. Cytol. 10:529
Pinto da Silva, P. 1972. Translational mobility of the membrane intercalated particles of human erythrocyte ghosts. pH-dependent, reversible aggregation.J. Cell Biol. 53:777
Pinto da Silva, P. 1973. Membrane intercalated particles in human erythrocyte ghosts: Sites of preferred passage of water molecules at low temperature.Proc. Nat. Acad. Sci. U.S.A. 70:1339
Pinto da Silva, P., Douglas, S.D., Branton, D. 1971. Localization of A antigen sites on human erythrocyte ghosts.Nature 232:194
Porter, K.R., Kenyon, K., Badenhausen, S. 1967. Specializations of the unit membrane.Protoplasma 63:262
Satir, B., Schooley, C., Satir, P. 1973. Membrane fusion in a model system. Mucocyst secretion inTetrahymena.J. Cell Biol. 56:153
Satir, P., Satir, B. 1974. Design and function of site-specific particle arrays in the cell membrane.In: Coldspring Harbor Meeting: Control of Cell Proliferation. p. 233
Staehelin, L.A. 1968. The interpretation of freeze-etched artificial and biological membranes.J. Ultrastruct. Res. 22:326
Staehelin, L.A., Chlapowski, F.J., Bonneville, M.A. 1972. Luminal plasma membrane of the urinary bladder. I. Three-dimensional reconstruction from freeze-etch images.J. Cell Biol. 53:73
Taylor, A., Mamelak, M., Reaven, E., Maffly, R. 1973. Vasopressin: Possible role of microtubules and microfilaments in its action.Science 181:347
Tillack, T.W., Scott, R.E., Marchesi, V.T. 1972. The structure of erythrocyte membranes studied by freeze-etching. II. Localization of receptors for phytohemagglutinin and influenza virus to the intramembranous particles.J. Exp. Med. 135:1209
Tourtellotte, M.E., Zupnik, J.S. 1973. Freeze-fracturedAcholeplasma laidlawii membranes: Nature of particles observed.Science 179:84
Vergara, J., Zambrano, F., Robertson, J.D., Elrod, H. 1974. Isolation and characterization of luminal membranes from urinary bladder.J. Cell Biol. 61:83
Wade, J.B., Revel, J.P., DiScala, V.A. 1973. Effect of osmotic gradients on intercellular junctions of the toad bladder.Amer. J. Physiol. 224:407
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wade, J.B., DiScala, V.A. & Karnovsky, M.J. Membrane structural specialization of the toad urinary bladder revealed by the freeze-fracture technique. J. Membrain Biol. 22, 385–402 (1975). https://doi.org/10.1007/BF01868182
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01868182