Summary
The isolated and perfused cortical collecting tubule of the rabbit was examined by differential interference contrast microscopy in order to characterize the morphologic response of this nephron segment to peritubular hypotonicity. Computer-assisted, morphometric procedures were developed to obtain measurements of cell volume and lateral intercellular space geometry from interference contrast images of perfused nephron segments. Following dilution of the bath from 290 to 190 mOsm in the absence of antidiuretic hormone (T=25°C), the cells swelled rapidly to a new steady-state volume which was maintained for at least 20 to 30 min and which was about 90% of that predicted for ideal osmometric behavior. The increase in cell volume was accomplished entirely by bulging of the cells into the lumen; lateral space width and outside tubule diameter were unaffected by peritubular hypotonicity. In addition, the swelling of the cells was associated with an apparent swelling of intracellular organelles, e.g., nuclei and mitochondria. Our results indicate that cells of the mammalian collecting tubule swell without the capacity for significant volume regulation at 25°C and without the cytoplasmic vacuolation and dilation of the lateral intercellular spaces observed following the onset of antidiuretic hormone-dependent volume reabsorption (E. Ganote, J. Grantham, H. Moses, M. Burg and J. Orloff,J. Cell Biol. 36:355, 1968).
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References
Allen, R.D., David, G.B., Nomarski, G. 1969. The Zeiss-Nomarski differential interference equipment for transmitted light microscopy.Z. Wiss. Mikrosk. 69:193–221
Al-Zahid, G., Schafer, J.A., Troutman, S.L., Andreoli, T.E. 1977. Effect of antidiuretic hormone on water and solute permeation, and the activation energies for these processes, in mammalian cortical collecting tubules: Evidence for parallel ADH-sensitive pathways for water and solute diffusion in luminal plasma membranes.J. Membrane Biol. 31:103–129
Berglindh, T., DiBona, D.R., Ito, S., Sachs, G. 1980. Probes of parietal cell function.Am. J. Physiol. 238:G165-G176
Burg, M., Grantham, J., Abramow, M., Orloff, J. 1966. Preparation and study of fragments of single rabbit nephrons.Am. J. Physiol 210:1293–1298
Dellasega, M., Grantham, J.J. 1973. Regulation of renal tubule cell volume in hypotonic media.Am. J. Physiol. 224:1288–1294
DiBona, D.R. 1981. Vasopressin action on the conformational state of the granular cell in the amphibian urinary bladder.In: Epithelial Ion and Water Transport. A.D.C. MacKnight and J.P. Leader, editors. pp. 241–255. Raven, New York
Ebbesson, S.O.E., Tang, D.B. 1967. A comparison of sampling procedures in a structured cell population.In: Sterology. H. Elias, editor. p. 131. Springer-Verlag, New York
Ege, R. 1927. The dispersed phase of the blood corpuscles.Biochem. J. 21:967–970
Ganote, C.E., Grantham, J.J., Moses, H.L., Burg, M.B., Orloff, J. 1968. Ultrastructural studies of vasopressin effect on isolated perfused renal collecting tubules of the rabbit.J. Cell Biol. 36:355–367
Grantham, J.J., Ganote, C.E., Burg, M.B., Orloff, J. 1969. Paths of transtubular water flow in isolated renal collecting tubules.J. Cell Biol. 41:562–576
Harmanci, M.C., Kachadorian, W.A., Valtin, H., DiScala, V.A. 1978. Antidiuretic hormone-induced intramembranous alterations in mammalian collecting ducts.Am. J. Physiol. 235:F440-F443
Hoffman, E. 1977. Control of cell volume.In: Transport of Ions and Water in Animals. B.L. Gupta, R.B. Moreno, J.L. Aschman and B.J. Wall, editors. pp. 285–332. Academic, London
Horster, M., Gundlach, H. 1979. Application of differential interference contrast with inverted microscopes to thein vitro perfused nephron.J. Microsc. 117:375–379
Kaissling, B., Kriz, W. 1979. Structural analysis of the rabbit kidney.Adv. Anat. Embryol. Cell Biol. 56:1–123
Kirk, K.L., Schafer, J.A., DiBona, D.R. 1983. Microscopic methods for analysis of function in isolated renal tubules.In: Membrane Biophysics. II: Physical Methods in the Study of Epithelia. M.A. Dinno, A.B. Callahan and T.C. Rozzell, editors. pp. 21–36. Alan R. Liss, New York
Kirk, K.L., Schafer, J.A., DiBona, D.R. 1984. Quantitative analysis of the structural events associated with antidiuretic hormone-induced volume reabsorption in the rabbit cortical collecting tubule.J. Membrane Biol. 79:65–74
Law, R.O. 1975. Volume adjustment by renal medullary cells in hypo- and hyper-osmolal solutions containing permeant and impermeant solutes.J. Physiol. (London) 247:55–70
LeFurgey, A., Tisher, C.C. 1979. Morphology of rabbit collecting duct.Am. J. Anat. 155:111–124
Persson, B., Spring, K.R. 1982. Gallbladder epithelial cell hydraulic water permeability and volume regulation.J. Gen. Physiol. 79:481–505
Schafer, J.A., Andreoli, T.E. 1972. Cellular constraints to diffusion. The effect of antidiuretic hormone on water flows in isolated mammalian collecting tubules.J. Clin. Invest. 51:1264–1278
Spring, K.R., Hope, A. 1979. Fluid transport and the dimensions of cells and interspaces of livingNecturus gallbladder.J. Gen. Physiol. 73:287–305
Tisher, C.C., Bulger, R.E., Valtin, H. 1971. Morphology of renal medulla in water diuresis and vasopressin-induced antidiuresis.Am. J. Physiol. 220:87–94
Weibel, E.R., Bolender, R.P. 1973. Stereological techniques for electron microscopic morphometry.In: Principles and Techniques of Electron Microscopy. Vol. 3. M.A. Hayat, editor. pp. 237–296. Van Nostrand Reinhold, New York
Welling, L.W., Evan, A.P., Welling, D.J. 1981. Shape of cells and extracellular channels in rabbit cortical collecting ducts.Kidney Int. 20:211–222
Welling, L.W., Grantham, J.J. 1972. Physical properties of isolated perfused renal tubules and tubular basement membranes.J. Clin. Invest. 51:1063–1075
Woodhall, P.B., Tisher, C.C. 1973. Response of the distal tubule and cortical collecting duct to vasopressin in the rat.J. Clin. Invest. 52:3095–3108
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Kirk, K.L., DiBona, D.R. & Schafer, J.A. Morphologic response of the rabbit cortical collecting tubule to peritubular hypotonicity: Quantitative examination with differential interferene contrast microscopy. J. Membrain Biol. 79, 53–64 (1984). https://doi.org/10.1007/BF01868526
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DOI: https://doi.org/10.1007/BF01868526