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Contribution of solvent drag through intercellular junctions to absorption of nutrients by the small intestine of the rat

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The lumen of the small intestine in anesthetized rats was recirculated with 50 ml perfusion fluid containing normal salts, 25mm glucose and low concentrations of hydrophilic solutes ranging in size from creatinine (mol wt 113) to Inulin (mol wt 5500). Ferrocyanide, a nontoxic, quadrupally charged anion was not absorbed; it could therefore be used as an osmotically active solute with reflection coefficient of 1.0 to adjust rates of fluid absorption,J v , and to measure the coefficient of osmotic flow,L p . The clearances from the perfusion fluid of all other test solutes were approximately proportional toJ v . FromL p and rates of clearances as a function ofJ v and molecular size we estimate (a) the fraction of fluid absorption which passes paracellularly (approx. 50%), (b) coefficients of solvent drag of various solutes within intercellular junctions, (c) the equivalent pore radius of intercellular junctions (50 Å) and their cross sectional area per unit path length (4.3 cm per cm length of intestine). Glucose absorption also varied as a function ofJ v . From this relationship and the clearances of inert markers we calculate the rate of active transport of glucose, the amount of glucose carried paracellularly by solvent drag or back-diffusion at any givenJ v and luminal glucose concentration and the concentration of glucose in the absorbate. The results indicate that solvent drag through paracellular channels is the principal route for intestinal transport of glucose or amino acids at physiological rates of fluid absorption and concentration. In the absence of luminal glucose the rate of fluid absorption and the clearances of all inert hydrophilic solutes were greatly reduced. It is proposed that Na-coupled transport of organic solutes from lumen to intercellular spaces provides the principal osmotic force for fluid absorption and triggers widening of intercellular junctions, thus promoting bulk absorption of nutrients by solvent drag. Further evidence for regulation of channel width is provided in accompanying papers on changes in electrical impedance and ultrastructure of junctions during Na-coupled solute transport.

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References

  1. Adibi, S., Kim, Y.S. 1981. Peptide absorption and hydrolysis.In: Physiology of the Digestive Tract. Johnson, editor. Raven, New York

    Google Scholar 

  2. Atkinson, R.M., Parsons, D.S., Smyth, D.H. 1957. The intestinal absorption of glucose.J. Physiol. (London) 135:581–585

    Google Scholar 

  3. Auchinachie, D.W., Macleod, J.J., Magee, H.E. 1930. Studies on diffusion through surviving isolated intestine.J. Physiol. (London) 69:185–209

    Google Scholar 

  4. Barry, B.A., Matthews, J.M., Smyth, D.H. 1961. Transfer of fluid by different parts of the small intestine of the rat.J. Physiol. (London) 157:279–288

    Google Scholar 

  5. Berliner, R.W., Kennedy, T.J., Hilton, J.G. 1950. Renal clearance of ferrocyanide in the dog.Am. J. Physiol. 160:325–329

    PubMed  Google Scholar 

  6. Bolufer, J.M., Delgado, J., Murillo, F., Murillo, M.L. 1986. Galactose transport across rat small intestine in vivo following distal resections of varying extents.Q. J. Exptl. Physiol. 71:423–431

    Google Scholar 

  7. Borgstrom, B., Dahlquist, A., Lundh, G., Sjovall, J.S. 1957. Studies of intestinal digestion and absorption in the human.J. Clin. Invest. 36:1521–1536

    PubMed  Google Scholar 

  8. Claude, P. 1978. Morphological factors influencing transepithelial permeability: A model for the resistance of the zonula occludens.J. Membrane Biol. 39:219–232

    Google Scholar 

  9. Claude, P., Goodenough, D.A. 1973. Fracture faces of Zonnulae Occludentes from “tight” and “leaky” epithelia.J. Cell Biol. 58:390–400

    PubMed  Google Scholar 

  10. Crane, R.K. 1968. Absorption of sugars.In: APS Handbook of Physiology. Alimentary Canal III, Intestinal Absorption. pp. 1323–1307. C.F. Code, editor. Williams & Wilkins, Washington, D.C.

    Google Scholar 

  11. Crane, R.K. 1979. Intestinal structure and function related to toxicology.Environ. Health Perspect. 33:3–8

    PubMed  Google Scholar 

  12. Crone, C., Christensen, O. 1979. Transcapillary transport of small solutes and water.In: International Review of Physiology, Cardiovascular III. A.C. Guyton and A.B. Young, editors. pp. 149–213. University Park, Baltimore

  13. Cummins, A.J. 1952. Absorption of glucose and methionine from the human intestine: The influence of glucose concentration in the blood and in the intestinal lumen.J. Clin. Invest. 31:928–937

    PubMed  Google Scholar 

  14. Curran, P.F. 1960. Na, Cl and water transport by rat ileum in vitro.J. Gen. Physiol. 43:1137–1148

    PubMed  Google Scholar 

  15. Curran, P.F., Solomon, A.K. 1957. Ion and water fluxes in the ileum of rats.J. Gen. Physiol. 41:143–168

    PubMed  Google Scholar 

  16. Curry, F.E. 1984. Mechanics and thermodynamics of capillary exchange.In: APS Handbook of Physiology: Microcirculation. E.M. Renkin and C.C. Michel, editors. pp. 309–374. Williams & Wilkins, Washington, D.C.

    Google Scholar 

  17. Fisher, R.B. 1955. The absorption of water and of some small molecules from the isolated intestine of the rat.J. Physiol. (London) 130:655–664

    Google Scholar 

  18. Fisher, R.B., Parsons, D.S. 1949. A preparation of surviving rat small intestine for the study of absorption.J. Physiol. (London) 110:36–46

    Google Scholar 

  19. Fisher, R.B., Parsons, D.S. 1953. Glucose movements across the wall of the rat small intestine.J. Physiol. (London) 119:210–223

    Google Scholar 

  20. Fisher, R.B., Parsons, D.S. 1957. Surface area of rat intestinal mucosa.J. Anat. 84:272–282

    Google Scholar 

  21. Fordtran, J.S., Ingelfinger, F.J. 1968. Absorption of water, electrolytes and sugars from the human gut.In: APS Handbook of Physiology. Alimentary Canal III, Intestinal Absorption. C.F. Code, editor. pp. 1457–1490. Williams & Wilkins, Washington, D.C.

    Google Scholar 

  22. Fordtran, J.S., Rector, F.C., Ewton, M.F., Soter, N., Kinney, J. 1965. Permeability characteristics of the human small intestine.J. Clin. Invest. 44:1935–1944

    PubMed  Google Scholar 

  23. Frömter, E., Diamond, J.M. 1972. Route of passive ion permeation in epithelia.Nature New Biol. 235:9–13

    PubMed  Google Scholar 

  24. Fullerton, P.M., Parsons, D.S. 1956. Absorption of sugars and water from rat intestine in vivo.Q. J. Exp. Physiol. 41:387–397

    Google Scholar 

  25. Hakim, A., Lester, R.G., Lifson, N. 1963. Absorption by an in vitro preparation of dog intestinal mucosa.J. Appl. Physiol. 16:409–413

    Google Scholar 

  26. Hemmings, C., Hemmings, W.A., Patey, A.L., Wood, C. 1978. The ingestion of dietary protein as large molecular mass degradation products in adult rats.Proc. R. Soc. London B 198:439–453

    Google Scholar 

  27. Holdsworth, C.D., 1972. Absorption of proteins, aminoacids and peptides.In: Transport Across the Intestine. Glaxco Symposium, pp. 136–153.

  28. Holdsworth, C.D., Dawson, A.M. 1964. The absorption of monosaccharides in man.Clin. Sci. 27:371–379

    PubMed  Google Scholar 

  29. Jacobsen, E.D., Bordy, D.C., Broitman, S.A., Fordtran, S.J. 1963. Validity of PEG in estimating water volume.Gastroenterology 44:761–767

    PubMed  Google Scholar 

  30. Jodal, M., Lundgren, O. 1986. Countercurrent mechanism in the mammalian gastrointestinal tract.Gastroenterology 91:225–241

    PubMed  Google Scholar 

  31. Katchalsky, A., Curran, P.F. 1965. Non-Equilibrium Thermodynamics in Biophysics. Harvard University Press, Cambridge

    Google Scholar 

  32. Kedem, O., Katchalsky, A. 1958. Thermodynamics analysis of the permeability of biological membranes to non-electrolytes.Biochim. Biophys. Acta 27:229–246

    PubMed  Google Scholar 

  33. Krueger, J.M., Pappenheimer, J.R., Karnovsky, M.L. 1982. Sleep-promoting effects of muramyl peptides.Proc. Natl. Acad. Sci. USA 79:6102–6106

    PubMed  Google Scholar 

  34. Lesse, H.J., Mansford, K.R. 1971. The effect of insulin and insulin deficiency on the transport and metabolism of glucose by the small intestine.J. Physiol. (London) 212:819–836

    Google Scholar 

  35. Macleod, J.J.R., Magee, H.E., Purves, C.B. 1930. Selective absorption of carbohydrates.J. Physiol. (London) 70:404–416

    Google Scholar 

  36. Madara, J.L., Pappenheimer, J.R. 1987. The structural basis for physiological regulation of paracellular pathways in intestinal epithelia.J. Membrane Biol. 100:149–164

    Google Scholar 

  37. Magee, H.E., Reid, E. 1931. The absorption of glucose from the alimentary canal.J. Physiol. (London) 73:163–183

    Google Scholar 

  38. Miller, B.F., Winkler, A. 1936. The ferrocyanide clearance in man.J. Clin. Invest. 15:489–492

    Google Scholar 

  39. Munck, B.G., Rasmussen, S.N. 1977. Paracellular permeability of extracellular space markers across rat jejunum in vitro. Indication of a transepithelial fluid circuit.J. Physiol. (London) 271:473–488

    Google Scholar 

  40. Naftalin, R.J., Tripathi, S. 1986. The roles of paracellular and transcellular pathways and submucosal space in isotonic water absorption by the rabbit ileum.J. Physiol. (London) 370:409–432

    Google Scholar 

  41. Olmstead, W.W., Nasset, E.S., Kelley, M.L., Jr. 1966. Amino acids in postprandial gut contents of man.J. Nutrition 90:291–294

    Google Scholar 

  42. Pappenheimer, J.R. 1953. Passage of molecules through capillary walls.Physiol. Rev. 33:387–423

    PubMed  Google Scholar 

  43. Pappenheimer, J.R. 1954. Uber die Permeabilitat der Glomerulumembranes in der Niere.Klin. Wochenschr. 33:362–365

    Google Scholar 

  44. Pappenheimer, J.R. 1987. Physiological regulation of transepithelial impedance in the intestinal mucosa of rats and hamsters.J. Membrane Biol. 100:137–148

    Google Scholar 

  45. Pappenheimer, J.R., Renkin, E.M., Borrero, L.B. 1950. Filtration and molecular diffusion from the capillary circulation in muscle, with deductions concerning the number and dimensions of ultramicroscopic openings in the capillary wall.Proc. Int. Congr. Physiol. 18:384–385

    Google Scholar 

  46. Pappenheimer, J.R., Zich, K.E. 1985. Absorption of hydrophilic solutes from the rat small intestine.J. Physiol. (London) 371:138P

    Google Scholar 

  47. Parsons, D.S., Prichard, J.S. 1966. Properties of some model systems for transcellular active transport.Biochim. Biophys. Acta 126:471

    PubMed  Google Scholar 

  48. Schanker, L.S., Tocco, D.J., Brodie, B.B., Hogben, C.A.M. 1958. Absorption of drugs from the rat small intestine.J. Expt. Pharmacol. Ther. 123:81–88

    Google Scholar 

  49. Schultz, S. 1980. Basic Principles of Membrane Transport. Cambridge University Press, Cambridge

    Google Scholar 

  50. Schultz, S.G. 1972. Electrical potential differences and electromotive forces in epithelial tissues.J. Gen. Physiol. 59:794–798

    PubMed  Google Scholar 

  51. Schultz, S.G. 1977. The role of paracellular pathways in isotonic fluid transport.Yale J. Bio. Med. 50:99–113

    Google Scholar 

  52. Schultz, S.G. 1981. Salt and water absorption by mammalian small intestine.In: Physiology of the Gastrointestinal Tract. pp. 983–989. Raven Press, New York

    Google Scholar 

  53. Smyth, D.H., Taylor, C.B. 1957. Transfer of water and solutes by an in vitro intestinal preparation.J. Physiol. (London) 136:632–648

    Google Scholar 

  54. Smyth, D.H., Wright, E.M. 1966. Streaming potentials in the rat small intestine.J. Physiol. (London) 182:591–602

    Google Scholar 

  55. Thomson, A.B.R. 1986. Resection of rabbit ileum: Effect on jejeunal structure and carrier-mediated and passive uptake.Q. J. Expt. Physiol. 71:29–46

    Google Scholar 

  56. Van Slyke, D.D., Hiller, A., Miller, B.F. 1935. The clearance, extraction and estimated filtration of Na-ferrocyanide in the mammalian kidney. Comparison with inulin, creatinine and urea. Am. J. Physiol.113:611–628

    Google Scholar 

  57. Vinardell, M.P., Bolufer, J. 1983. Paracellular absorption ofd-glucose by rat small intestine in vivo.Rev. Esp. Fisiol. 39:193–196

    PubMed  Google Scholar 

  58. Whittembury, G., deMartinez, C.V., Linares, H., Paz-Aliaga, A. 1980. Solvent drag of large solutes indicates paracellular water flow in leaky epithelia.Proc. R. Soc. London B 211:63–81

    Google Scholar 

  59. Wiseman, G. 1968. Absorption of amino-acids.In: APS Handbook of Physiology. Alimentary Canal III, Intestinal Absorption. C.F. Code, editor. pp. 1277–1307, Williams & Wilkins, Washington, D.C.

    Google Scholar 

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Pappenheimer, J.R., Reiss, K.Z. Contribution of solvent drag through intercellular junctions to absorption of nutrients by the small intestine of the rat. J. Membrain Biol. 100, 123–136 (1987). https://doi.org/10.1007/BF02209145

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