Skip to main content
Log in

Structural and enzymatic studies on the plasma membrane domains and sodium pump enzymes of absorptive epithelial cells in the avian lower intestine

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The coprodaeum of the domestic hen maintained on a low-NaCl diet adapts by enhanced sodium transport. This study examines the adaptive response at the single cell and whole organ levels. Surface areas of apical (microvillous) and basolateral plasma membranes of columnar absorptive epithelial cells were estimated by use of ultrastructural stereology. The activities of succinic dehydrogenase (a mitochondrial enzyme) and ouabain-sensitive, potassium-dependent paranitrophenyl phosphatase (a sodium pump enzyme) were determined in tissue homogenates. Sodium, potassium-ATPase (pump enzyme) activity in cell membranes was localized by ultrastructural cytochemistry. Apical and basolateral membranes responded differently. In high-NaCl hens, the membrane signature of the average cell was 32 μm2 (apical), 932 μm2 (lateral) and 17 μm2 (basal). Cells from low-NaCl hens had more apical membrane (49 μm2 per cell) but essentially the same area of basolateral membrane. However, total surfaces per organ were greater for all membranes. Sodium pump enzymes were localized in basolateral membranes. Enzyme activities per unit mitochondrial volume and per unit basolateral membrane surface were higher in low-NaCl birds. These findings are discussed in the context of known mechanisms of transcellular sodium transport via apical ion channels and basolateral pumps.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baddeley AJ, Gundersen HJG, Gruz-Orive LM (1986) Estimation of surface area from vertical sections. J Microsc 142:259–276

    Google Scholar 

  • Bindslev N (1979) Sodium transport in the hen lower intestine. Induction of sodium sites in the brush border by a low sodium diet. J Physiol (Lond) 288:449–466

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Google Scholar 

  • Bulger RE (1965) The shape of rat kidney tubular cells. Am J Anat 116:237–256

    Google Scholar 

  • Buschmann RJ, Manke DJ (1981a) Morphometric analysis of the membranes and organelles of small intestinal enterocytes. I. Fasted hamster. J Ultrastruct Res 76:1–14

    Google Scholar 

  • Buschmann RJ, Manke DJ (1981b) Morphometric analysis of the membranes and organelles of small intestinal enterocytes. II. Lipid-fed hamster. J Ultrastruct Res 76:15–26

    Google Scholar 

  • Cala PM, Cogswell N, Mandell LJ (1978) Binding of [3H]-ouabain to split frog skin. J Gen Physiol 71:347–367

    Google Scholar 

  • Choshniak I, Munck BG, Skadhauge E (1977) Sodium chloride transport across the chicken coprodeum. Basic characteristics and dependence on sodium chloride intake. J Physiol (Lond) 271:489–504

    Google Scholar 

  • Christensen O, Bindslev N (1982) Fluctuation analysis of shortcircuit current in a warm-blooded sodium-retaining epithelium: site current, density, and interaction with triamterene. J Membrane Biol 65:19–30

    Google Scholar 

  • Clauss W, Arnason SS, Munck BG, Skadhauge E (1984) Aldosterone-induced sodium transport in lower intestine. Effects of varying NaCl intake. Pflügers Arch 401:354–360

    Google Scholar 

  • Clauss W, Dürr JE, Guth D, Skadhauge E (1987) Effects of adrenal steroids on Na transport in the lower intestine (coprodeum) of the hen. J Membrane Biol 96:141–152

    Google Scholar 

  • Clauss W, Dantzer V, Skadhauge E (1988) A low-salt diet facilitates Cl secretion in hen lower intestine. J Membrane Biol 102:83–96

    Google Scholar 

  • Cuthbert AW, Edwardson JM, Bindslev N, Skadhauge E (1982) Identification of potential components of the transport mechanism for Na+ in the hen colon and coprodaeum. Pflügers Archiv 392:347–351

    Google Scholar 

  • Dantzer V, Møller O, Skadhauge E (1988) Morphological and enzymic adaptation to aldosterone of the epithelium of the caudal hindgut of the hen. J Physiol (Lond) 396:30P

    Google Scholar 

  • Elbrønd VS, Dantzer V, Mayhew TM, Skadhauge E (1991) Avian lower intestine adapts to dietary salt (NaCl) depletion by increasing transepithelial sodium transport and microvillous membrane surface area. Exper Physiol 76:733–744

    Google Scholar 

  • Eldrup E, Møllgaard K, Bindslev N (1979) Possible sodium channels in the luminal membrane of the hen lower intestine visualized by freeze fracture. In: Bourguet J, Chevalier J, Parisi M, Ripoche P (eds) Hormonal control of epithelial transport. vol 85. INSERM, Paris, pp 253–260

    Google Scholar 

  • Eldrup E, Møllgaard K, Bindslev N (1980) Possible epithelial sodium channels visualized by freeze-fracture. Biochim Biophys Acta 596:152–157

    Google Scholar 

  • Ernst SA (1975) Transport ATPase cytochemistry: ultrastructural localization of potassium-dependent and potassium-independent phosphatase activities in rat kidney cortex. J Cell Biol 66:586–608

    Google Scholar 

  • Ernst SA, Ellis RA (1969) The development of surface specialization in the secretory epithelium of the avian salt gland in response to osmotic stress. J Cell Biol 40:305–321

    Google Scholar 

  • Ernst SA, Mills JW (1977) Basolateral plasma membrane localization of ouabain-sensitive sodium transport sites in the secretory epithelium of the avian salt gland. J Cell Biol 75:74–94

    Google Scholar 

  • Ernst SA, Mills JW (1980) Autoradiographic localization of tritiated ouabain-sensitive sodium pump sites in ion transporting epithelia. J Histochem Cytochem 28:72–77

    Google Scholar 

  • Firth JA (1983) Microscopical analysis of electrolyte secretion. In: Navaratnam V, Harrison RJ (eds) Progress in anatomy, vol 3, Cambridge University Press, Cambridge, pp 33–55

    Google Scholar 

  • Garrahan PJ, Pouchan MI, Rega AF (1969) Potassium activated phosphatase from human red blood cells. J Physiol (Lond) 202:305–327

    Google Scholar 

  • Garty H, Benos DJ (1988) Characteristics and regulatory mechanisms of the amiloride-blockable Na+ channel. Physiol Rev 68:309–373

    Google Scholar 

  • Gundersen HJG, Jensen EB (1985) Stereological estimation of the volume-weighted mean volume of arbitrary particles observed on random sections. J Microsc 138:127–142

    Google Scholar 

  • Jørgensen PL (1986) Structure, function and regulation of Na+, K+-ATPase in the kidney, Kidney Int 29:10–20

    Google Scholar 

  • Landsverk T (1986) Histochemical distribution of potassium-dependent p-nitrophenylphosphatase in the calf intestine. Histochem J 18:519–523

    Google Scholar 

  • Lyngdorf-Henriksen P, Munck BG, Skadhauge E (1978) Sodium chloride transport across the lower intestine of the chicken. Pflügers Arch 378:161–165

    Google Scholar 

  • Mayhew TM (1990) The striated brush border of intestinal absorptive epithelial cells: stereological studies on microvillous morphology in different adaptive states. J Electron Microsc Tech 16:45–55

    Google Scholar 

  • Mayhew TM (1991) The new stereological methods for interpreting functional morphology from slices of cells and organs. Exper Physiol 76:639–665

    Google Scholar 

  • Mayhew TM, Middleton C (1985) Crypts, villi and microvilli in the small intestine of the rat. A stereological study of their variability within and between animals. J Anat 141:1–17

    Google Scholar 

  • Mayhew TM, Dantzer V, Elbrønd VS, Skadhauge E (1990) A sampling scheme intended for tandem measurements of sodium transport and microvillous surface area in the coprodaeal epithelium of hens on high-and low-salt diets. J Anat 173:19–31

    Google Scholar 

  • Porteus JW, Clark B (1965) The isolation and characterization of subcellular components of the epithelial cells of rabbit small intestine. Biochem J 96:159–171

    Google Scholar 

  • Robinson DH, Mills JW (1987) Ouabain binding to tadpole ventral skin. II. Localization of sodium pump sites. Am J Physiol 253:R410-R417

    Google Scholar 

  • Roden M, Turnheim K (1988) Sodium pump quantity and turnover in rabbit descending colon at different rates of sodium absorption. Pflügers Arch 413:181–189

    Google Scholar 

  • Rostgaard J, Møller O (1980) Localization of Na+,K+-ATPase to the inside of the basolateral cell membranes of epithelial cells of proximal and distal tubules in rabbit kidney. Cell Tissue Res 212:17–28

    Google Scholar 

  • Skadhauge E (1980) Intestinal osmoregulation. In: Epple A, Stetson MH (eds) Avian endocrinology. Springer, Berlin Heidelberg, pp 1–203

    Google Scholar 

  • Skadhauge E, Clauss W, Arnason SS, Thomas DH (1985) Mineralocorticoid regulation of lower intestinal ion transport. In: Gilles R, Gilles-Baillien M (eds) Transport processes, iono-and osmoregulation. Springer, Berlin Heidelberg New York, pp 118–133

    Google Scholar 

  • Smith PR, Benos DJ (1991) Epithelial Na+ channels. Annu Rev Physiol 53:509–530

    Google Scholar 

  • Smith PR, Saccomani G, Bradford AL, Dantzer V, Benos DJ, Skadhauge E (1991) Immunochemical identification of amiloride-sensitive sodium channels from an intestinal epithelium. In: Bonvalet JP, Farman N, Lombes M, Rafestin-Oblin ME (eds) Aldosterone-fundamental aspects. (Colloque Inserm vol. 215) John Libbey Eurotext, Paris London, p 319

    Google Scholar 

  • Stirling CE (1972) Radioautographic localization of sodium pump sites in rabbit intestine. J Cell Biol 53:704–714

    Google Scholar 

  • Thomas DH, Skadhauge E (1982) Time course of adaptation to low and high NaCl diets in the domestic fowl. Effects on electrical behaviour of isolated epithelia from the lower intestine. Pflügers Arch 395:165–170

    Google Scholar 

  • Thomas DH, Jallageas M, Munck BG, Skadhauge E (1980) Aldosterone effects on electrolyte transport of the lower intestine (coprodeum and colon) of the fowl (Gallus domesticus) in vitro. Gen Comp Endocrinol 40:44–51

    Google Scholar 

  • Tousson A, Alley CD, Sorscher EJ, Brinkley BR, Benos DJ (1989) Immunochemical localization of amiloride-sensitive sodium channels in sodium-transporting eqithelia. J Cell Sci 93:349–362

    Google Scholar 

  • Turnheim K (1991) Intrinsic regulation of apical sodium entry in epithelia. Physiol Rev 71:429–445

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mayhew, T.M., Elbrønd, V.S., Dantzer, V. et al. Structural and enzymatic studies on the plasma membrane domains and sodium pump enzymes of absorptive epithelial cells in the avian lower intestine. Cell Tissue Res. 270, 577–585 (1992). https://doi.org/10.1007/BF00645061

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00645061

Key words

Navigation