Laboratory Investigation

Kidney International (1980) 17, 732–748; doi:10.1038/ki.1980.86

Hydrostatic pressure changes related to paracellular shunt ultrastructure in proximal tubule

Arvid B Maunsbach and Emile L Boulpaep

Department of Cell Biology, Institute of Anatomy, University of Aarhus, Aarhus, Denmark, and Department of Physiology, School of Medicine Yale University, New Haven, Connecticut

Correspondence: Dr A B Maunsbach, Department of Cell Biology, Institute of Anatomy, University of Aarhus, DK-8000 Aarhus C, Denmark

Received 5 June 1979; Revised 1 November 1979.

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Abstract

Hydrostatic pressure changes related to paracellular shunt ultrastructure in proximal tubule. We examined the effects of changes in hydrostatic pressures on the ultrastructural geometry of the lateral intercellular space and tight junctions in proximal tubules of control (C) and volume-expanded (VE) Necturus kidney. The following groups of tubules were studied: (1) C, free-flow pressure, (2) C, stopped-flow, high-luminal pressure, (3) C, stopped-flow, low-luminal pressure, (4) VE, free-flow pressure, and (5) VE, stopped-flow, high-luminal pressure. Intratubular and peritubular capillary pressures were monitored before and during standardized perfusion-fixation for electron microscopy, and complete cross-sections of all sampled tubules were subjected to morphometric analysis. Average lateral intercellular space widths decreased significantly in C and VE stopped-flow tubules with high-luminal pressures but widened greatly in C stopped-flow tubules with low-luminal pressures. The length or width of the tight junctions did not change between the five experimental conditions. The ultrastructural changes correlate with the applied transepithelial pressure gradients rather than with transepithelial volume fluxes. The narrowing of lateral intercellular spaces in high pressure tubules correlate with the previously described increase in electrical resistance expressed per unit length tubule indicating that in these conditions part of the paracellular resistance is located in the free interspaces. The geometry of the lateral intercellular space in the proximal tubule of Necturus favors models of near-isotonic transport that do not depend on long and narrow interspaces.

Modifications de la pression hydrostatique liées à l'ultrastructure du shunt paracellulaire dans le tube proximal. Ce travail étudie les effets de modifications des pressions hydrostatiques dans la géométrie ultrastructurale de l'espace intercellulaire latéral et des jonctions serrées des tubes proximaux de reins de Necturus contrôles (C) ou ayant subi une expansion du volume extracellulaire (VE). Les groupes de tubules suivants ont été étudiés: (1) C, pression en flux libre, (2) C, débit interrompu, pression luminale élevée, (3) C, débit interrompu, pression luminale faible, (4) VE, pression en flux libre, et (5) VE, débit interrompu, pression luminale élevée. Les pressions intratubulaire et capillaire péritubulaire ont été contrôlées avant et pendant la perfusion-fixation pour la microscopie électronique. Tous les tubules ont été soumis à une analyse morphométrique. La largeur moyenne de l'espace intercellulaire latéral a diminué significativement dans les tubules C et VE en débit interrompu avec une pression intraluminale élevée, mais a augmenté considérablement dans les tubules C en débit interrompu avec une pression intraluminale faible. La longueur, ni la largeur des jonctions serrées n'ont été affectées par les cinq conditions expérimentales. Les modifications ultrastructurales sont mieux corrélées avec le gradient transepithelial de pression qu'avec les débits transépithéliaux. La diminution de l'espace intercellulaire latéral dans les tubules à pression élevée est en accord avec l'augmentation, rapportée antérieurement, de la résistance électrique exprimée par unité de longueur du tubule, ce qui indique que dans ces conditions une partie de la résistance paracellulaire est localisée dans les espaces libres. La géométrie de l'espace intercellulaire latéral dans le tube proximal de Necturus est en faveur de modèles de transport proche de l'isotonicité, qui ne dépend pas de la présence d'espaces longs et étroits.

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