Skip to main content
Log in

Functional heterogeneity of the descending limbs of Henle's loop

II. Interspecies differences among rabbits, rats, and hamsters

  • Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Permeability properties of the descending limbs of Henle's loop were compared among rabbits, hamsters, and rats by measuring transepithelial voltage (Vt) across the isolated renal tubules perfused in vitro. From the deflection of the Vt when the composition of the bathing fluid was varied, the permeabilities of sodium and of potassium relative to chloride (P Na/P Cl andP K/P Cl, respectively) were determined in either the descending limbs of the short-loop nephron (SDL) or the segments of the upper protion of the long-loop nephron (LDLu). In hamsters and rats, the values ofP Na/P Cl of the LDLu (3.98±0.66 and 5.03±0.79) were higher than those of the SDL (0.68±0.03 and 0.61±0.00). In contrast, inrrabbits the value ofP Na/P Cl of the LDLu (0.96±0.05) was only slightly higher than that of the SDLu (0.75±0.03). The similar tendency was also noted in the values ofP K/P Cl. In hamsters and rats, theP K/P Cl ratios were 4.90±0.82 and 6.44±0.90, respectively, in the LDLu and 1.09±0.04 and 1.02±0.0, respectively in the SDL. When a transepithelial osmotic gradient was imposed by adding raffinose to the bath, a lumen-negative streaming voltage of about −8 mV was generated in the hamster and the rat LDLu. Taken together with the findings in the preceding paper, these observations support the view that the descending limbs of rabbits are different from those of hamsters and rats in that internephron heterogeneity is less remarkeble, and that the LDLu of hamsters and rats is highly permeable to sodium and to potassium as well as to water.

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

  1. Bachman S, Kriz W (1982) Histotopography and ultrastructure of the thin limbs of the loop of Henle in the hamster. Cell Tissue Res 225:111–127

    Google Scholar 

  2. Barrett JM, Kriz W, Kaissling B, Rouffignac C de (1978a) The ultrastructure of the nephrons of the desert rodent. (Psammomys obesus) kidney. I. Thin limbs of Henle of short-looped nephrons. Am J Anat 151:487–498

    Google Scholar 

  3. Barrett JM, Kriz W, Kaissling B, Rouffignac C de (1978b) The ultrastructure of the nephrons of the desert rodent (Psammomys obesus) kidney. II. Thin limb of Henle of long-looped nephrons. Am J Anat 151:499–514

    Google Scholar 

  4. Barrett JM, Majack RA (1977) The ultrastructural organization of long and short nephrons in the kidney of the rodentOctodon degus (abstr.). Anat Rec 187:530–531

    Google Scholar 

  5. Barry PH, Diamond JM (1970) Junction potentials, electrode standard potentials, and other problems in interpreting electrical properties of membranes. J Membr Biol 3:93–121

    Google Scholar 

  6. Berry CA, Warnock DG, Rector FC, Jr (1978) Ion selectivity and proximal salt reabsorption. Am J Physiol 235:F234-F245

    Google Scholar 

  7. Burg MB, Grantham J, Abramow M, Orloff J (1966) Preparation and study of fragments of single rabbit nephrons. Am J Physiol 210:1293–1298

    Google Scholar 

  8. Burg MB, Green N (1973) Function of the thick ascending limb of Henle's loop. Am J Physiol 224:659–668

    Google Scholar 

  9. Chevalier J, Bourguet J, Hugon JS (1974) membrane associated particles: distribution in frog urinary bladder epithelium at rest and after oxytocin treatment. Cell Tissue Res 152:129–140

    Google Scholar 

  10. Dietrich HJ, Barrett JM, Kriz W, Bulhoff JP (1975) The ultrastructure of the thin loop limbs in the mouse kidney. Anat Embryol 147:1–18

    Google Scholar 

  11. Gibra IN (1973) Probability and Statistical Inference for Scientists and Engeneers. Prentice-Hall, Englewood Cliffs, New Jersey

    Google Scholar 

  12. Hebert SC, Culpepper RM, Andreoli TE (1981) NaCl transport in mouse medullary thick ascending limbs. II. ADH enhancement of transcellular NaCl contransport: origin of the transepithelial voltage. Am J Physiol 241:F432-F442

    Google Scholar 

  13. Humbert F, Pricam C, Perrelet A, Orci L (1975) Freeze-fracture differences between plasma membranes of descending and ascending branches of the rat Henle's thin loop. Lab Invest 33:407–411

    Google Scholar 

  14. Imai M (1977) Function of the thin ascending limb of Henle of rats and hamsters perfused in vitro. Am J Physiol 232:F201-F209

    Google Scholar 

  15. Imai M, Hayashi M, Araki M (1984) Functional heterogeneity of the descending limbs of Henle's loop. I. Internephron heterogeneity in the hamster kidney. Pflügers Arch 402:385–392

    Google Scholar 

  16. Imai M, Kokko JP (1974) NaCl, urea and water transport in the thin ascending limb of Henle: generation of osmotic gradients by passive diffusion of solutes. J Clin Invest 53:393–402

    Google Scholar 

  17. Imai M, Kusano E (1982) Effects of arginine vasopressin on the thin ascending limb of Henle's loop of hamsters. Am J Physiol 243:F167-F172

    Google Scholar 

  18. Imbert M, Rouffignac C de (1976) Role of sodium and urea in the renal concentrating mechanism. Pflügers Arch 361:107–114

    Google Scholar 

  19. Jamison RL, Buerkert J, Lacy F (1973) A micropuncture study of Henle's thin loop in Brattleboro rats. Am J Physiol 224:180–185

    Google Scholar 

  20. Jamison RL, Roinel N, Rouffignac C de (1979) Urinary concentrating mechanism in the desert rodentPsammomys obesus. Am J Physiol 236:F448-F453

    Google Scholar 

  21. Jamison RL, Work J, Schafer JA (1982) New pathways for potassium transport in the kidney. Am J Physiol 242:F297-F312

    Google Scholar 

  22. Kachadorian WA, Wade JB, DiScala VA (1975) Vasopressin induced structural change in toad bladder luminal membrane. Science 190:67–69

    Google Scholar 

  23. Kaissling B, Kriz W (1979) Structural analysis of rabbit kidney. Adv Anat Embryol Cell Biol 56:1–123

    Google Scholar 

  24. Kawamura S, Imai M, Kokko JP (1975) Characteristics of salt and water transport in superficial and juxtamedullary straight segments of proximal tubules. J Clin Invest 55:1269–1277

    Google Scholar 

  25. Kielland J (1937) Individual activity coefficients of ions in aqueous solutions. J Am Chem Soc 59:1675–1678

    Google Scholar 

  26. Kokko JP (1970) Sodium chloride and water transport in the descending limb of Henle. J Clin Invest 49:1838–1846

    Google Scholar 

  27. Kokko JP (1972) Urea transport in the proximal tubule and the descending limb of Henle. J Clin Invest 51:1999–2008

    Google Scholar 

  28. Kriz W, Kaissling B, Psczolla M (1978) Morphological characterization of the cells in Henle's loop and the distal tubule. In: Vogel HG, Ullrich K (eds) New aspects of renal function. Excepta Medica, Amsterdam/Oxford, pp 67–78

    Google Scholar 

  29. Kriz W, Schiller A, Kaissling B, Taugner R (1980) Comparative and functional aspects of thin loop limb ultrastructure. In: Maunsbach AB, Olsen TS, Christensen EI (eds) Functional ultrastructure of the kidney. Academic Press, London, pp 241–250

    Google Scholar 

  30. Miwa T, Imai M (1984) Flow-dependent water permeability of the rabbit descending limb of Henle's loop. Am J Physiol 245:F743-F754

    Google Scholar 

  31. Morgan T, Berliner RW (1968) Permeability of loop of Henle, vasa recta and collecting duct to water, urea, and sodium. Am J Physiol 215:108–115

    Google Scholar 

  32. Nagle RB, Altschuler EM, Dobyan DC, Dong S, Bulger RE (1981) The ultrastructure of the thin limbs of Henle in kidney of the heteromyid (Perognathus penicillatus). Am J Anat 161:34–47

    Google Scholar 

  33. Pennell JP, Lacy FB, Jamison RL (1975) An in vivo study of the concentrating process in the descending limb of Henle's loop. Kidney Int 5:337–347

    Google Scholar 

  34. Rocha AS, Kokko JP (1973) Sodium chloride and water transport in the medullary thick ascending limb of Henle. J Clin Invest 52:612–624

    Google Scholar 

  35. Rouffignac C de (1972) Physiological role of the loop of Henle in urinary concentration. Kidney Int 2:297–303

    Google Scholar 

  36. Rouffignac C de, Morel F (1969) Micropuncture study on water, electrolyte, and urea movement along the loop of Henle in Psammomys. J Clin Invest 48:474–486

    Google Scholar 

  37. Rouffignac C de, Morel F, Moss N, Roinel N (1973) Micropuncture study of water and electrolyte movements along the loop of Henle in Psammomys with special reference to magnesium, calcium and phosphorus. Pflügers Arch 344:309–326

    Google Scholar 

  38. Salling N, Siggard-Andersen O (1971) Liquid-junction potentials between plasma or erythrolysate and KCl solutions. Scand J Clin Invest 28:33–40

    Google Scholar 

  39. Sasaki S, Imai M (1980) Effects vasopressin on water and NaCl transport across the in vitro perfused medullary thick ascending limb of Henle's loop of mouse, rat and rabbit kidneys. Pflügers Arch 383:215–221

    Google Scholar 

  40. Schiller A, Taugner R, Kriz W (1980) The thin limbs of Henle's loop in the rabbit. Cell Tiss Res 207:249–265

    Google Scholar 

  41. Schwartz MM, Karnovsky MJ, Venkatachalam MA (1979) Regional membrane specialization in the thin limbs of Henle's loops as seen by freeze-fracture electron microscopy. Kidney Int 16:577–589

    Google Scholar 

  42. Schwartz MM, Venkatachalam MA (1974) Structural differences in thin limbs of Henle: Physiological implications. Kidney Int 6:193–208

    Google Scholar 

  43. Tabei K, Imai M (1983) Cation selectivity of the descending limbs of the long-loop nephron (LDLu) of hamsters (Abstract in Japanese). 26th Annual Meeting of Japanese Society of Nephrology, Kyoto, p 493

  44. Warnock DG, Burg MB (1977) Urinary acidification: CO2 transport by the rabbit proximal straight tubule. Am J Physiol 232:F20-F25

    Google Scholar 

  45. Wasserstein AG, Agus ZS (1983) Potassium secretion in the rabbit proximal straight tubules. Am J Physiol 245:F167-F174

    Google Scholar 

  46. Work J, Troutman SL, Schafer JA (1982) Transport of potassium in the rabbit pars recta. Am J Physiol 242:F226-F237

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Imai, M. Functional heterogeneity of the descending limbs of Henle's loop. Pflugers Arch. 402, 393–401 (1984). https://doi.org/10.1007/BF00583940

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00583940

Key words

Navigation