Passage of ions and dextran molecules across the rete mirabile of the eel. The effects of charge.

Abstract

SUMMARY. The countercurrent-perfused rete mirabile of the eel is a preparation in which capillary permeability values can be determined accurately in broadscale fashion. To provide insight into charge effects on transendothelial passage, the permeability values of small inorganic cations (labeled sodium and rubidium, and stable potassium) and anions (labeled chloride, iodide, sulfate, and ferrocyanide) were compared to those expected for neutral solutes with approximately matched diffusion coefficients, and that of a neutral dextran fraction was compared to that of a negatively charged dextran sulfate with a similar diffusion coefficient. In the small ion experiments, the labeled iodide values were unexpectedly high, apparently due to the contamination of the labeled iodide solution with IJ~. The permeabilities of the rest of the ions clustered at a level about 0.5 of the values which would have been expected for neutral solutes with similar diffusion coefficients. The decrement was interpreted to reflect the presence, of both positive and negative charges along the transendothelial pathway, which effectively decrease the dimensions of the limiting part of the pathway for the charged microions relative to that accessible to comparable nonelectrolytes. The larger negatively charged dextran sulfate was also reduced in its passage, in comparison with its matching neutral dextran; this was taken to indicate the presence of a larger1 scale average net negative charge along its pathway. The data indicate the presence of a staggering of positive and negative charges along the transendothelial pathway accessible to the microions, and a net negative charge in the more restricted part of the pathway available to the dextrans. (CircRes 56: 74-83, 1985) BLOOD capillary permeability to small ions has long been known to be a minute fraction of that for water, irrespective of the methods used and tissues investigated. The data have been interpreted as indicating the presence of differing paths for the passage of ions and water across the endothelial wall, the mechanism for the transfer of each usually being thought to be passive [except in certain special areas, such as the tight capillaries of the central nervous system and the eye, where evidence for some active transport of sodium and potassium ions has been presented (Bradbury and Stulcova, 1970;Eisenberg and Suddith, 1979;Betz and Goldstein, 1980)]. It has been expected that appropriately designed studies with ions and charged molecules would provide information concerning the effects of local fixed charges, if these are present in the regions where inorganic ions and other charged materials traverse the capillary wall.Few capillary beds have been thoroughly examined from this point of view. The glomerular apparatus of the kidney constitutes the one exception. Studies of glomerular filtration of moderately large molecules with different charges and comparable molecular size have provided evidence for a charge effect in this structure. These studies indicate that, altho...

True

“…The charge-dependence in vascular permeability in tumours is consistent with observations in normal tissues (Jain, 1997;Curry et al, 1987;Turner et al, 1983;Vehaskari et al, 1984;Deen et al, 1980;Baldwin et al, 1991;Dermietzel et al, 1983;Adamson et al, 1988;Barrowcliffe et al, 1990;Gandhi and Bell, 1992;Gilchrist and Parker, 1985;Haraldsson et al, 1983;Khaw et al, 1991;Leypoldt and Henderson, 1993;Michel and Phillips, 1985;Öjteg et al, 1987;Parker et al, 1985;Rasio and Goresky, 1985;Triguero et al, 1989), suggesting the luminal surface of tumour vascular endothelium is negatively charged as well.…”

“…Thus, it restricts the extravasation of anionic macromolecules, as has been demonstrated in cultured endothelial cell monolayer (Sahagun et al, 1990) and various normal tissues (Jain, 1997;Curry et al, 1987;Turner et al, 1983;Vehaskari et al, 1984;Deen et al, 1980;Baldwin et al, 1991;Dermietzel et al, 1983;Adamson et al, 1988;Barrowcliffe et al, 1990;Gandhi and Bell, 1992;Gilchrist and Parker, 1985;Haraldsson et al, 1983;Khaw et al, 1991;Leypoldt and Henderson, 1993;Michel and Phillips, 1985;Öjteg et al, 1987;Parker et al, 1985;Rasio and Goresky, 1985;Triguero et al, 1989). Adamson et al (1988) have demonstrated that the microvascular permeability to α-lactalbumin (M r = 14 176, net charge -10) is approximately 50% of that to ribonuclease (M r = 13 683, net charge +4), suggesting that the microvascular permeability to the positively charged molecules is higher than the permeability to the negative ones.…”

The Uptake of Ions and Neutral Solutes by the Artery and by Artery Wall Preparations

“…No data have been reported on measurement of the iodide space, although our values are rather higher than the chloride spaces reported by Villamil et a f and Headings eta1.2' This is consistent with the results of our direct comparison of Iand C1uptake in different tissue preparations and may in part be due to the formation of the highly lipid-soluble 13ion. 28 The effects of cyanide poisoning on monovalent anion distribution' are qualitatively similar to those we found after freezing and thawing. We are not aware of any previous work on the effect of changing ionic strength on ionic uptake, other than the work of Hudgins on Ca++, which shows a large increase at low ionic strengths very similar in magnitude to that which we observed.…”

Effect of reduced energy metabolism and reperfusion on the permeability and morphology of the capillaries of an isolated rete mirabile.

“…This space is likely to be filled by a matrix of fibrous molecules, with associated charge effects. 35 Our observation that ionic transport is reduced in the rete capillaries by comparison with neutral solutes with similar diffusion coefficients 36 is consonant with this idea. Alterations of the matrix density or charge during hypoxia could potentially account for changes in small solute permeability without visible widening of interendothelial junctions.…”