Osmotic gradient dependence of osmotic water permeability in rabbit proximal convoluted tubule

Berry, Christine; Verkman, A. S.

doi:10.1007/bf01871104

Cited by 43 publications

(21 citation statements)

References 47 publications

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“…The results also indicate that Ͻ 20% of osmotically driven transepithelial water transport in proximal tubule is paracellular. This conclusion is in agreement with previous measurements showing strong inhibition of proximal tubule water permeability by mercurials (26) and with a theoretical analysis based on the apparent size of paracellular pores (23). Our conclusion does not agree with data suggesting similar transcellular and paracellular water permeabilities based on fast video measurements of apical and basolateral membrane P f in perfused proximal tubules (4).…”

Section: Discussionsupporting

confidence: 93%

Defective proximal tubular fluid reabsorption in transgenic aquaporin-1 null mice

Schnermann

Chou

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

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To investigate the role of aquaporin-1 (AQP1) water channels in proximal tubule function, in vitro proximal tubule microperfusion and in vivo micropuncture measurements were done on AQP1 knockout mice. The knockout mice were generated by targeted gene disruption and found previously to be unable to concentrate their urine in response to water deprivation. Unanesthetized knockout mice consumed 2.8-fold more f luid than wild-type mice and had lower urine osmolality (505 ؎ 40 vs. 1081 ؎ 68 milliosmolar). An important function of the kidney proximal tubule is the near-isosmolar reabsorption of a significant fraction of fluid that is filtered by the glomerulus. The proximal tubule also reabsorbs nearly all of the filtered glucose, amino acids, and bicarbonate. The apical and basolateral plasma membranes of proximal tubule cells contain water channel protein aquaporin-1 (AQP1), which is thought to provide an important water-selective pathway for transcellular fluid transport (1-3). However, there is conflicting evidence that significant paracellular water transport occurs (4), and it has been suggested that other water channels (AQP7, ref. 5) and transporters (glucose transporter GLUT1, refs. 6, 7; sodium-glucose cotransporter SGLT1, ref. 8) might contribute to transcellular water movement. It is generally believed, but without direct evidence, that high proximal tubule water permeability is important to permit the efficient coupling of solute and water transport to accomplish near-isosmolar fluid absorption.The AQP1 water channel is a water-selective transporter (9, 10) that is found in membranes as tetramers (11) in which each functionally independent monomer (12) contains six transmembrane, tilted helical domains surrounding a putative aqueous pore (13-15). In kidney, AQP1 is strongly expressed in apical and basolateral plasma membranes of epithelial cells in proximal tubule and thin descending limb of Henle and in endothelial cells of descending vasa recta (1-3, 16, 17). Recently, a transgenic AQP1 knockout mouse was generated by targeted gene disruption and shown to manifest a severe defect in urinary concentrating ability (18). When given access to water, the mice appeared grossly normal except for mild growth retardation compared with wild-type mice. When deprived of water, the mice were unable to concentrate their urine and conserve fluid, resulting in marked dehydration and serum hyperosmolality in 1-2 days.The purpose of this study was to define the role of AQP1 in proximal tubule water transport and fluid reabsorption. Isolated tubule microperfusion was used to measure transepithelial osmotic water permeability and fluid absorption under defined in vitro conditions. Free-flow micropuncture was used to determine the in vivo consequences of decreased proximal tubule water permeability. A remarkable decrease in proximal tubule water permeability and fluid reabsorption was found in the AQP1 knockout mice. The results have important implications regarding the mechanisms of proximal tubule fluid reabsorpt...

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Section: Discussionsupporting

confidence: 93%

Defective proximal tubular fluid reabsorption in transgenic aquaporin-1 null mice

Schnermann

Chou

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

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400

299

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“…The cytoplasmic compartment is a complex unstirred layer (5) and may account for Ͼ50% of the transcellular resistance to water movement (4). Thus small changes in the cellular compartment may significantly affect transepithelial water permeability.…”

Section: Discussionmentioning

confidence: 99%

Water transport in neonatal and adult rabbit proximal tubules

Quigley¹,

Baum

2002

American Journal of Physiology-Renal Physiology

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Quigley, Raymond, and Michel Baum. Water transport in neonatal and adult rabbit proximal tubules. Am J Physiol Renal Physiol 283: F280-F285, 2002; 10.1152/ajprenal.00341.2001.-We have recently demonstrated that although the osmotic water permeability (P f) of neonatal proximal tubules is higher than that of adult tubules, the P f of brush-border and basolateral membrane vesicles from neonatal rabbits is lower than that of adults. The present study examined developmental changes in the water transport characteristics of proximal convoluted tubules (PCTs) in neonatal (9-16 days old) and adult rabbits to determine whether the intracellular compartment or paracellular pathway is responsible for the maturational difference in transepithelial water transport. The permeability of n-butanol was higher in the neonatal PCT than the adult PCT at all temperatures examined, whereas the diffusional water permeability was identical. Increasing the osmotic gradient increased volume absorption in both the neonatal and the adult PCT to the same degree. The P f was not different between the neonatal and the adult PCT at any osmotic gradient studied. To assess solvent drag as a measure of the paracellular transport of water, the effect of the osmotic gradient on mannitol and chloride transport were measured. There was no change in chloride or mannitol transport with the increased osmotic gradient in either group, indicating that there was no detectable paracellular water movement. In addition, the mannitol permeability of the neonatal PCT was found to be lower than that of the adult PCT with the isotonic bath (8.97 Ϯ 4.01 vs. 40.49 Ϯ 13.89 m/s, P Ͻ 0.05). Thus the intracellular compartment of the neonatal PCT has a lower resistance for water transport than the adult PCT and is responsible for the higher than expected P f in the neonatal PCT.proximal convoluted tubules; development; butanol permeability; diffusional water permeability; in vitro microperfusion WATER TRANSPORT ACROSS CELLULAR membranes is a fundamental biological process that occurs either by diffusion through the lipid bilayer or by movement through specific water channels (aquaporins) (3,11,28). There is also evidence that water can traverse across other membrane transport proteins (12). Transport of water through the lipid bilayer is characterized by a high activation energy (Ͼ9 kcal ⅐ mol Ϫ1 ⅐ degree Ϫ1 ) and resistance to inhibition by mercury, whereas water movement through aquaporins is characterized by a low activation energy (ϳ4-5 kcal ⅐ mol Ϫ1 ⅐ degree Ϫ1) and is inhibited by mercury for most aquaporin isoforms (28).The proximal tubule of the mammalian kidney is responsible for reabsorbing the bulk of the glomerular ultrafiltrate (24). This process is nearly isosmotic because the proximal tubule has a very high water permeability, which is thought to be due to the constitutive presence of the water channel aquaporin-1 (AQP1). The importance of AQP1 to water transport by this nephron segment is evidenced by the fact that mice lacking AQP1 have a much lower r...

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“…The cytoplasmic compartment is a complex unstirred layer (Berry & Verkman, 1988) and may account for over 50% of the transcellular resistance to water movement (Berry, 1985). Thus, small changes in the cellular compartment may significantly affect transepithelial water permeability.…”

Section: Discussionmentioning

confidence: 99%

Maturational Changes in Rabbit Renal Basolateral Membrane Vesicle Osmotic Water Permeability

Quigley

Gupta

Lisec

et al. 2000

Journal of Membrane Biology

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We have recently demonstrated that while the osmotic water permeability (P f ) of neonatal proximal tubules is higher than that of adult tubules, the P f of brush-border membrane vesicles from neonatal rabbits is lower than that of adults. The present study examined developmental changes in the water transport characteristics of proximal tubule basolateral membranes by determining aquaporin 1 (AQP1) protein abundance and the P f in neonatal (10-14 days old) and adult rabbit renal basolateral membrane vesicles (BLMV). At 25°C the P f of neonatal BLMV was significantly lower than the adult BLMV at osmotic gradients ranging from 40 to 160 mOsm/kg water. The activation energies for osmotic water movement were identical in the neonatal and adult BLMV (8.65 ± 0.47 vs. 8.86 ± 1.35 kcal · deg −1 · mol −1 ). Reflection coefficients for sodium chloride and sodium bicarbonate were identical in both the neonatal and adult BLMV and were not different from one. Mercury chloride (0.5 mM) reduced osmotic water movement by 31.3 ± 5.5% in the adult BLMV, but by only 4.0 ± 4.0% in neonatal vesicles (P < 0.01). Adult BLMV AQP1 abundance was higher than that in the neonate. These data demonstrate that neonatal BLMV have a lower P f and AQP1 protein abundance than adults and that a significantly greater fraction of water traverses the basolateral membrane lipid bilayer and not water channels in neonates compared to adults. The lower P f of the neonatal BLMV indicates that the basolateral membrane is not responsible for the higher transepithelial P f in the neonatal proximal tubule.

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Osmotic gradient dependence of osmotic water permeability in rabbit proximal convoluted tubule

Cited by 43 publications

References 47 publications

Defective proximal tubular fluid reabsorption in transgenic aquaporin-1 null mice

Defective proximal tubular fluid reabsorption in transgenic aquaporin-1 null mice

Water transport in neonatal and adult rabbit proximal tubules

Maturational Changes in Rabbit Renal Basolateral Membrane Vesicle Osmotic Water Permeability

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