Structure-Function Correlations of Colon and Distal Nephron

  • John P. Hayslett
Part of the Advances in Comparative and Environmental Physiology book series (COMPARATIVE, volume 16)

Abstract

Intestinal epithelia and epithelia lining the nephron have a special attraction for membrane physiologists because of prominent structure-function correlations, unique segmental differentiation, and highly specialized functional differences between individual cell types within segments. This review aims to compare the similarities and differences in structure-function characteristics of epithelia in the colon and collecting duct system in the mammal. Our intent is to provide support for the proposition that the terminal segments of intestine and nephron, involved in the final regulation of electrolyte composition of fecal water and urine, employ anatomical structures and transport mechanisms for the regulation of transepithelial movement of electrolytes that are basically similar. Differences in structure and the incorporation of specialized cells are best explained by the unique roles played by intestine and kidney in the absorbance of nutrients as a source of energy and in overall regulation of water and electrolyte homeostasis, respectively. Details of molecular mechanisms that subserve ion transport will only be listed to the extent that they serve our aim, since they are comprehensively reviewed in other parts of this volume and elsewhere.

Keywords

Adenosine Assimilation Dexamethasone Luminal Convolution 

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References

  1. Ahn J, Chang EB, Field M (1985) Phorbol ester inhibition of Na-K exchange in rabbit proximal colon. Am J Physiol 249: 527–530Google Scholar
  2. Backman KA, Hayslett JP (1982) Role of the medullary collecting duct in potassium conservation. Pflügers Arch Eur J Physiol 396: 297–300CrossRefGoogle Scholar
  3. Bankir L, deRouffignac C (1988) Urinary concentrating ability: insights from comparative anatomy. Am J Physiol 249: 643–666Google Scholar
  4. Basti CP (1987) Regulation of cation transport by low doses of glucocorticoids in in vivo adrenalectomized rat colon. J Clin Invest 80: 348–359CrossRefGoogle Scholar
  5. Bastl CP, Barnett CA, Schmidt TJ, Litwack G (1989a) Glucocorticoid stimulation of sodium absorption in colon epithelium is mediated by corticosteroid IB receptor. J Biol Chem 259: 1186–1195Google Scholar
  6. Basti CP, Schulman G, Cragoe EJ (1989b) Low-dose glucocorticoids stimulate electroneutral NaCl absorption in rat colon. Am J Physiol 257: F1027 - F1038Google Scholar
  7. Beck FX, Dörge A, Rick R, Schramm M, Thurau K (1987) Effect of potassium adaptation in the distribution of potassium, sodium and chloride across the apical membrane of renal tubular cells. Pflügers Arch Eur J Physiol 409: 477–485CrossRefGoogle Scholar
  8. Billich CO, Levitan R (1969) Effects of sodium concentration and osmolarity on water and electrolyte absorption from the intact human colon. J Clin Invest 48: 1336–1347PubMedCentralPubMedCrossRefGoogle Scholar
  9. Binder HJ (1970) A comparison of intestinal and renal transport systems. Am J Clin Nutr 23: 330–335PubMedGoogle Scholar
  10. Binder HJ (1983) Absorption and secretion of water and electrolytes by small and large intestine. In: Sleisenger MH, Fordtran JS (eds) Gastrointestinal disease 3rd edn. Edition Saunders, Philadelphia, pp 133–155Google Scholar
  11. Binder HJ, Rawlins CL (1973) Electrolyte transport across isolated large intestine mucosa. Am J Physiol 225: 1232–1239PubMedGoogle Scholar
  12. Binder HJ, Stange G, Murer H, Stieger B, Jauri J-P (1986) Sodium-proton exchanges in colon brush-border membranes. Am J Physiol 251: G382 - G390PubMedGoogle Scholar
  13. Binder HJ, Foster ES, Budinger ME, Hayslett JP (1987) Mechanism of electroneutral sodium chloride absorption in distal colon of the rat. Gastroenterology 93: 449–455PubMedGoogle Scholar
  14. Borgstrom B, Dahlgvist A, Luordh G, Sjovall J (1957) Studies of intestinal digestion and absorption in the human. J Clin Invest 36: 1521–1536PubMedCentralPubMedCrossRefGoogle Scholar
  15. Boulpaep EL (1976) Electrical phenomena in the nephron. Kidney Int 9: 88–102PubMedCrossRefGoogle Scholar
  16. Brown AL Jr (1962) Microvilli of the human jejunal epithelium cell. J Cell Biol 12: 623–627PubMedCentralPubMedCrossRefGoogle Scholar
  17. Burg MB (1986) Renal handling of sodium, chloride, water, amino acids and glucose. In: Brenner BM, Rector FC (eds) The kidney. Saunders, Philadelphia, pp 145–176Google Scholar
  18. Cartright CA, McRoberts JA, Mandel KG, Dharmsathaphorn K (1985) Synergistic action of cyclic adenosine monophosphate-and calcium-mediated chloride secretion in a colonic epithelial cell line. J Clin Invest 76: 1837–1842CrossRefGoogle Scholar
  19. Charney A, Feldman G (1984) Systemic acid-base disorders and intestinal electrolyte transport. Am J Physiol 247: G1 - G12PubMedGoogle Scholar
  20. Doucet A, Katz AI (1980) Renal potassium adaptation: Na-K-ATPase activity along the nephron after chronic potassium loading. Am J Physiol 238: F380 - F386PubMedGoogle Scholar
  21. Doucet A, Katz AI (1981) Mineralocorticord receptors along the nephron: [3H] aldosterone binding in rabbit tubules. Am J Physiol 241: F605 - F611PubMedGoogle Scholar
  22. Escobar E, Ibarra C, Todesco E, Parise M (1990) Water and ion handling in the rat cecum. Am J Physiol 259: G786 - G791PubMedGoogle Scholar
  23. Field MJ, Stanton BA, Giebisch GH (1984) Differential acute effect of aldosterone, dexamethasone and hyperkalemia on distal tubule potassium secretion in the rat kidney. J Clin Invest 74: 1792–1802PubMedCentralPubMedCrossRefGoogle Scholar
  24. Fine LG, Yanagawa N, Schultze RG, Tuck M, Trizna W (1979) Functional profile of the isolated uremic nephron. J Clin Invest 64: 1033–1042PubMedCentralPubMedCrossRefGoogle Scholar
  25. Fisher KA, Binder HJ, Hayslett JP (1976) Potassium secretion by colonic mucosal cells after potassium adaptation. Am J Physiol 281: 987–994Google Scholar
  26. Foster ES, Zimmerman TW, Hayslett JP, Binder HJ (1983) Corticosteroid alteration of active electrolyte transport in rat distal colon. Am J Physiol 245: G668 - G675PubMedGoogle Scholar
  27. Foster ES, Hayslett JP, Binder HJ (1984) Mechanism of active potassium absorption and secretion in the rat colon. Am J Physiol 246: G611 - G617PubMedGoogle Scholar
  28. Foster ES, Budinger ME, Hayslett JP, Binder HJ (1986a) Ion transport in proximal colon of the rat. J Clin Invest 77: 228–235PubMedCentralPubMedCrossRefGoogle Scholar
  29. Foster ES, Dudeja PK, Brasitus TA (1986b) Na+-H+ exchange in rat colon brush-border membrane vesicles. Am J Physiol 250: G781 - G787PubMedGoogle Scholar
  30. Frizzell RA, Koch MJ, Schultz SG (1976) Ion transport by rabbit colon. I. Active and passive components. J Membr Biol 27: 297–316PubMedCrossRefGoogle Scholar
  31. Giebisch G, Klose RM, Windhager EE (1964) Micropuncture study of hypertonic sodium chloride loading in the rat. Am J Physiol 206: 687–693PubMedGoogle Scholar
  32. Grantham JJ, Burg MB, Orloff J (1970) The nature of transtubular Na and K transport in isolated rabbit collecting tubules. J Clin Invest 49: 1815–1826PubMedCentralPubMedCrossRefGoogle Scholar
  33. Gross JB, Imai M, Kokko J (1975) A functional comparison of the cortical collecting tubule and the distal convoluted tubule. J Clin Invest 55: 1284–1294PubMedCentralPubMedCrossRefGoogle Scholar
  34. Hayes CP Jr, McLeod M, Robinson R (1967) An extrarenal mechanism for the maintenance of potassium balance in severe chronic renal failure. Trans Assoc Am Phys 80: 207–216PubMedGoogle Scholar
  35. Hayslett JP, Backman KA, Schon DA (1980) Electrical properties of the medullary collecting duct in the rat. Am J Physiol 239: F258 - F264PubMedGoogle Scholar
  36. Hayslett JP, Halevy J, Pace PE, Binder HJ (1982) Demonstration of net potassium absorption in mammalian colon. Am J Physiol 242: G209 - G214PubMedGoogle Scholar
  37. Hierholzer K, Wiederholt M, Holzgreve N, Giebisch G, Klose RM, Windhager EE (1965) Micropuncture study of renal transtubular concentration gradients of sodium and potassium in adrenalectomized rats. Pflügers Arch 285: 193–210CrossRefGoogle Scholar
  38. Hirsch D, Kashgarian M, Boulpaep EL, Hayslett JP (1984) Role of aldosterone in the mechanism of potassium adaptation in the initial collecting tubule. Kidney Int Eur J Physiol 26: 798–807CrossRefGoogle Scholar
  39. Jamison RL, Kriz W (1982) Urinary concentrations mechanism: structure and function. Oxford University Press, New YorkGoogle Scholar
  40. Kaissling B, Kriz W (1979) Structural analysis of the rabbit kidney. Adv Anat Embryol Cell Biol 56: 1–123PubMedCrossRefGoogle Scholar
  41. Kashgarian M, Taylor CR, Binder HJ, Hayslett JP (1980) Amplification of cell membrane surfaces in potassium adaptation. Lab Invest 42: 580–581Google Scholar
  42. Kliger AS, Binder HJ, Bastl CP, Hayslett JP (1981) Demonstration of active potassium transport in the mammalian colon. J Clin Invest 67: 1189–1196PubMedCentralPubMedCrossRefGoogle Scholar
  43. Lacy ER (1991) Functional morphology of the large intestine. In: Schultz SG (ed) The gastrointestinal tract, sect 6. Handbook of physiology. American Physiological Society, Bethesda, Maryland, pp 121–194Google Scholar
  44. Lee SMK, Chekal MA, Katz AI (1983) Corticosterone binding along the rat nephron. Am J Physiol 244: F504 - F509PubMedGoogle Scholar
  45. Lombès M, Farman N, Oblin ME, Baulieu EE, Bonvalet JP, Erlanger BF, Gasc JM (1990) Immunohistochemical localization of renal mineralocorticoid receptor by using an anti-idiotypic antibody that is an internal image of aldosterone. Proc Natl Acad Sci USA 87: 1086–1088PubMedCentralPubMedCrossRefGoogle Scholar
  46. Madsen KM, Clapp WL, Verlander JW (1988) Structure and function of the inner medullary collecting duct. Kidney Int 34: 441–454PubMedCrossRefGoogle Scholar
  47. Malnic G, Klose RM, Giebisch G (1964) Micropuncture study of renal potassiun excretion in the rat. Am J Physiol 206: 674–686PubMedGoogle Scholar
  48. Malnic G, Klose RM, Giebisch G (1966) Micropuncture study of distal tubular potassium and sodium transport in rat kidney. Am J Physiol 211: 548–559PubMedGoogle Scholar
  49. O’Neil RG (1990) Aldosterone regulation of sodium and potassium transport in the cortical collecting duct. Semin Nephrol 10: 365–374PubMedGoogle Scholar
  50. Potter EL (1972) Normal and abnormal development of the kidney. Year Book Medical Publ, ChicagoGoogle Scholar
  51. Rajendran VM, Oesterlin N, Binder HJ (1991) PH regulated Cl uptake in apical membrane vesicles ( AMV) of rat distal colon. Gastroenterology 100: A700Google Scholar
  52. Sandle GI, McClone F (1987) Segmental variability of membrane conductances in rat and human colonic epithelia. Pflügers Arch Eur J Physiol 410: 173–180CrossRefGoogle Scholar
  53. Sandle GI, Hayslett JP, Binder HJ (1984) Effect of chronic hyperaldosteronism on the electrophysiology of rat distal colon. Pflügers Arch Eur J Physiol 401: 22–26CrossRefGoogle Scholar
  54. Sandle GI, Foster ES, Lewis SA, Binder HJ, Hayslett JP (1985) The electrical basis for enhanced potassium secretion in rat distal colon during dietary potassium loading. Pflügers Arch Eur J Physiol 403: 433–439CrossRefGoogle Scholar
  55. Sansom SC, O’Neil RG (1985) Mineralocorticoid regulation of apical cell membrane Na+ and K+ transport of the cortical collecting duct. Am J Physiol 248: F858 - F868PubMedGoogle Scholar
  56. Sansom SC, Agulian S, Mirto S, Illig V, Giebisch G (1989) K activity in CCD principal cells from normal and DOCA-treated rabbits. Am J Physiol 256: F136 - F142PubMedGoogle Scholar
  57. Schon DR, Backman KA, Hayslett JP (1981) Role of the medullary collecting duct in potassium excretion in potassium-adapted animal. Kidney Int 20: 655–662PubMedCrossRefGoogle Scholar
  58. Schulman G, Miller-Diener A, Litwack G, Bastl CP (1986) Characterization of the rat colonic aldosterone receptor and its activation process. J Biol Chem 261: 12102–12108PubMedGoogle Scholar
  59. Schultz SG, Curran PF (1968) Intestinal absorption of sodium chloride and water. In: Code CF (ed) Handbook of physiology, sect 6. Alimentary canal. American Physiological Society, Bethesda, MarylandGoogle Scholar
  60. Schwartz GJ, Burg MB (1978) Cation transport by the cortical collecting tubule in vitro. Am J Physiol 253: F576 - F585Google Scholar
  61. Sellin JH, DeSoignie RC (1984) Rabbit proximal colon: a distinct transport epithelium. Am J Physiol 26: G603 - G610Google Scholar
  62. Sellin JH, DeSoignie RC (1987) Ion transport in human colon in vitro. Gastroenterology 93: 441–448PubMedGoogle Scholar
  63. Sellin JH, Oyarzabal H, Cragoe EF (1988) Electrogenic sodium absorption in rabbit cecum in vitro. J Clin Invest 81: 1275–1283PubMedCentralPubMedCrossRefGoogle Scholar
  64. Silva P, Hayslett JP, Epstein FH (1973) The role of Na-K-activated adenosine triphosphate in potassium adaptation. J Clin Invest 52: 2665–2671PubMedCentralPubMedCrossRefGoogle Scholar
  65. Sonnenberg H (1977) Effect of adrenalectomy on medullary collecting-duct function in rats before and during blood volume expansion. Pflügers Arch Eur J Physiol 368: 55–62CrossRefGoogle Scholar
  66. Stanton BA, Biemesderfer D, Wade JB, Giebisch G (1981) Structural and functional study of the rat distal nephron: effects of potassium adaptation and depletion. Kidney Int 19: 36–48PubMedCrossRefGoogle Scholar
  67. Steinmetz PR (1986) Cellular organization of urinary acidification. Am J Physiol 251: F173 - F187PubMedGoogle Scholar
  68. Stevens CE (1977) Comparative physiology of the digestive system. In: Swenson MJ (ed) Duke’s physiology of domestic animals, 9th edn. Cornell University Press, Ithaca, NYGoogle Scholar
  69. Stokes JB (1982) Na and K transport across the cortical and outer medullary collecting tubule of the rabbit: evidence for diffusion across the outer medullary portion. Am J Physiol 242: F514 - F520PubMedGoogle Scholar
  70. Sullivan SK, Field M (1991) Ion transport across mammalian small intestine. In: Schultz SG (ed) The gastrointestinal tract, sect 6. Handbook of physiology. American Physiological Society, Bethesda, Maryland, pp 287–301Google Scholar
  71. Tomito K, Pisano JJ, Burg MB, Knepper MA (1986) Effects of vasopressin and bradykinin on anion transport by the rat cortical collecting duct. J Clin Invest 77: 136–141CrossRefGoogle Scholar
  72. Turnheim K, Hudson RL, Schultz SG (1987) Cell Na+ activities and transcellular Na+ absorption by descending colon from animal and Na+-deprived rabbits. Pflügers Arch Eur J Physiol 410: 279–283CrossRefGoogle Scholar
  73. Ullrich KJ (1976) Renal tubular mechanisms of organic solute transport. Kidney Int 9: 134–148PubMedCrossRefGoogle Scholar
  74. Ullrich KJ, Papavassilisu F (1979) Sodium reabsorption in the papillary collecting duct of rats. Effect of adrenalectomy, low Na+ diet, acetazolamide, HCO3- free solutions and of amiloride. Pflügers Arch Eur J Physiol 379: 49–52CrossRefGoogle Scholar
  75. Welling LE, Welling DJ (1976) Shape of epithelial cells and intercellular channels in the rabbit proximal nephron. Kidney Int 9: 385–394PubMedCrossRefGoogle Scholar
  76. Wiederholt M, Stolte H, Brecht JP, Hierholzer K (1966) Micropuncture research on the effect of aldosterone, cortisone and dexamethasone on renal sodium resorption in adrenalectomized rats. Pflügers Arch Eur J Physiol 292: 316–333CrossRefGoogle Scholar
  77. Wills NK, Biagi B (1982) Active potassium transport by rabbit descending colon epithelium. J Membr Biol 64: 195–203PubMedCrossRefGoogle Scholar
  78. Wills NK, Lewis SA, Eaton DC (1979) Active and passive properties of rabbit discending colon. A microelectrode and nystatin study. J Membr Biol 45: 81–108PubMedCrossRefGoogle Scholar
  79. Wingo CS (1989) Active proton secretions and potassium absorption in the rabbit outer medullary collecting duct. Functional evidence for proton-potassiun-activated adenosine triphosphatase. J Clin Invest 84: 361–365PubMedCentralPubMedCrossRefGoogle Scholar
  80. Wingo CS, Madsen KM, Smolka A, Tisher CC (1990) H-K-ATPase immunoreactivity in cortical and outer medullary collecting duct. Kidney Int 38: 985–990PubMedCrossRefGoogle Scholar
  81. Wright F, Strieder N, Fowler N, Giebisch G (1971) Potassium secretion by distal tubule after potassium adaptation. Am J Physiol 221: 437–448PubMedGoogle Scholar
  82. Wrong OM, Edmonds CJ, Chadwick VS (1981) The large intestine: its role in mammalian nutrition and homeostasis. Wiley, New YorkGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1993

Authors and Affiliations

  • John P. Hayslett
    • 1
  1. 1.Department of Internal Medicine, Section of NephrologyYale University School of MedicineNew HavenUSA

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