Abstract
Lumen to bath J 12/C 1 and bath to lumen J 21/ C 2 fluxes per unit concentration of 19 probes with diameters (d m) ranging from 3.0–30.0 Å (water, urea, erythritol, mannitol, sucrose, raffinose and 13 dextrans with d m 9.1–30.0 Å) were measured during volume secretion (J v ) in the upper segment of the Malpighian Tubule of Rhodnius by perfusing lumen and bath with 14C or 3H-labeled probes. J net=(J 12/C 1 − J 21/C 2) was studied as a function of J v · J v was varied by using different concentrations of 5-hydroxy tryptamine. J net for 3H-water was not different from J v We found: (i) A strong correlation between J net and J v for 8 probes d m=3.0–11.8 Å (group a probes), indicating that the convective component of J net is more important than its diffusive component and than unstirred layers effects which are negligible. Therefore group a probes are solvent dragged as they cross the epithelium, (ii) There is no correlation between J net and J v for 11 probes with d m=11.8–30 Å (group b). Therefore these probes must cross the epithelium by diffusion and not by solvent drag, (iii) In a plot of J net/J v vs. d m group a probes show a steep linear relation with a slope = −0.111, while for group b probes the slope is −0.002. Thus there is a break between groups a and b in this plot. We tried to fit the data with models for restricted diffusion and convention through cylindrical or parallel slit pathways. We conclude that (i) group a probes are dragged by water through an 11.0 Å-wide slit, (ii) Most of J v must follow an extracellular noncytosolic pathway, (iii) Group b probes must diffuse through a 42 Å-wide slit, (iv) A cylindrical pathway does not fit the data.
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References
Barry, P.H., Diamond, J.M. 1984. Effects of unstirred layers on membrane phenomena. Physiol. Rev. 64:736–872
Bean, C.P. 1972. The physics of porous membranes. In: Membranes, G. Eisenman, editor. Vol. 1, pp. 1–54. Marcel Dekker, New York
Berthelet F., Beaudry-Lonergan, M., Linares, H., Whittembury, G., Bergeron, M. 1987. Polimorphic organization of the endoplasmic reticulum of the Malpighian tubule. Evidence for a transcellular route. La Cellule. 74:281–293
Carpi-Medina, P. Lindemann, B., González, E., Whittembury, G. 1984. The continuous measurement of tubular volume changes in response to step changes in contraluminal osmolality. Pfluegers Arch. 400:343–348
Deetjen, P. 1978. Microperfusion of superficial tubules and peritubular capillaries. In: Andreucci, V.E., ed Manual of Renal Micropuncture. pp. 208–218. Idelson, Naples
Hill, A.E., Shachar-Hill, B. 1993. A mechanism for isotonic fluid flow through the tight junctions of Necturus gallbladder epithelium. J. Membrane Biol. 136:253–262
Kedem, O., Katchalsky, A. 1958. Thermodynamics analysis of the permeability of biological membranes to nonelectrolytes. Biochim. Biophys. Acta. 27:229–246
Kristensen, P., Ussing, H.H. 1992. Epithelial Organization. In: The Kidney, Physiology and Pathophysiology, D.W. Seldin and G. Giebisch, editors, pp. 265–286. Raven Press, New York
Lane, N.J., Skaer, H.leB. 1980. Intercellular junctions in insect tissues. Adv. Insect Physiol. 15:35–213
Maddrell, S.H.P. 1980. Characteristics of Epithelial transport in Malpighian Tubules. Curr. Topics in Membranes & Transport. 14:427–463
Maddrell, S.H.P., Herman, W.S., Farndale, R.W., Riegel, J.A. 1993. Synergism of hormones controlling epithelial fluid transport in an insect. J. Exp. Biol. 174:65–80
Maddrell, S.H.P., Herman, W.S., Mooney, R.L., Overton J.A. 1991. 5-Hydroxytryptamine: a second diuretic hormone in Rhodnius prolixus. J. Exp. Biol. 156:557–566
McElwain, D.L.S. 1984. A theoretical investigation of fluid transport in the Malpighian tubules of an insect, Rhodnius prolixus Stål. Proc. R. Soc. London B. 222:363–372
O'Donnell, M.J., Aldis, S.K., Maddrell, S.H.P. 1982. Measurements of osmotic permeability in the Malpighian tubules of an insect, Rhodnius prolixus Stål. Proc. R. Soc. London B. 216:267–277
O'Donnell, M.J., Maddrell, S.H.P. 1983. Paracellular and transcellular routes for water and solute movements across insect epithelia. J. Exp. Biol. 106:231–253
O'Donnell, M.J., Maddrell, S.H.P., Gardiner, B.O.C. 1984. Passage of solutes through walls of Malpighian tubules of Rhodnius by paracellular and transcellular routes. Am. J. Physiol. 246:R759-R769
Ogston, A.G. 1958. The spaces in a uniform suspension of fibres. Trans. Faraday Soc. 54:1754–1757
Renkin, E.M., Curry, F.E. 1979. Transport of water and solutes across capillary endothelium. In: Membrane Transport in Biology. Vol IV-A. G. Giebisch, D.C. Tosteson and H.H. Ussing, editors, pp. 1–45. Springer Verlag, New York
Shachar-Hill, B., Hill, A.E. 1993. Convective fluid flow through the paracellular system of Necturus gallbladder epithelium as revealed by dextran probes. J. Physiol. 468:463–486
Shipp, J.C. Hanenson, I.B., Windhager, E.E., Schatzmann, H.J., Whittembury, G., Yoshimura, H., Solomon, A.K. 1958. Single proximal tubules of the Necturus Kidney. Methods for micropuncture and microperfusion. Am. J. Physiol. 195:563–569
Skaer H.leB., Harrison, J.B., Lee, W.M. 1979. Topographical variation in the structure of the smooth septate junction. J. Cell Sci. 37:373–389
Steward, M.C. 1982. Paracellular nonelectrolyte permeation during fluid transport across rabbit gallbladder epithelium. J. Physiol. 322:419–439
Ussing, H.H., Eskesen, K. 1989. Mechanism of isotonic water transport in glands. Acta Physiol. Scand. 136:443–454
Wessing, A. 1965. Die Funktion der Malpigischen Gefaesse. In: Funktionelle und Morphologische Organisation der Zelle: Sekretion und Exkretion. K.E. Wohlfarth-Bottermann, editor, pp. 228–268. Springer Verlag, Berlin
Whittembury, G. 1967. Sobre los mecanismos de absorción en el túbulo proximal del riñón. Acta Client. Venezol. 18:(Suppl. 3) 43–56
Whittembury, G., Reuss, L. 1992. Mechanisms of coupling of solute and solvent transport in epithelia. In: The Kidney, Physiology and Pathophysiology, D.W. Seldin and G. Giebisch, editors, pp. 317–360. Raven Press, New York
Whittembury, G., Biondi, A.C., Paz-Aliaga, A., Linares, H., Parthe, V., Linares, N. 1986. Transcellular and paracellular flow of water during secretion in the upper segment of the Malpighian tubule of Rhodnius prolixus: solvent drag of molecules of graded size. J. Exp. Biol. 123:71–92
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E.G. is a Visiting Scientist at IVIC. It is a pleasure to thank Drs. A.E. Hill and Bruria Shachar-Hill for their suggestion of the use of dextrans, their instruction and help with the dextran separation technique, and their extensive discussions. Dr. R. Apitz, Mr H. Rojas and Mrs. Fulvia Bartoli were most helpful with suggestions during the course of the experimental work. Mr. Jose Mora was fundamental help with the equipment. Mrs. Lelis Ochoa and Mr. Luis F. Alvarez helped with some of the drawings. This work was partially supported by CONICIT, Fundación Polar and CDCH of UCV. It is a pleasure to thank Dr. H. Passow and Dr. K.J. Ullrich at the Max Planck Institut für Biophysik (Frankfurt/Main) where this work was initiated.
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Hernández, C.S., González, E. & Whittembury, G. The paracellular channel for water secretion in the upper segment of the Malpighian Tubule of Rhodnius prolixus . J. Membarin Biol. 148, 233–242 (1995). https://doi.org/10.1007/BF00235041
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DOI: https://doi.org/10.1007/BF00235041