Water transport in neonatal and adult rabbit proximal tubules

Abstract

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...

Glucocorticoids increase osmotic water permeability (Pf) of neonatal rabbit renal brush border membrane vesicles

“…The neonatal brush border membrane also had a higher activation energy (E a ) for water permeability and a lower sensitivity to mercury inhibition (24). We have also demonstrated that the intracellular compartment of the tubule cells plays a role in the developmental changes in the water permeability that likely explained the discrepancy (22). Thus the maturational changes in water transport in the proximal tubule involve several factors.…”

“…This occurs in a nearly isoosmotic manner due to the high water permeability of this nephron segment provided by the abundance of aquaporin-1 (AQP1), the water channel in the kidney proximal tubule (1,18,26). The functional aspects of water transport in the proximal tubule during development have recently been studied and reviewed (21)(22)(23)(24)(25). In vitro microperfusion revealed that the osmotic water permeability coefficient (P f ) of the proximal tubule is higher in the neonatal rabbit than that in the adult (21).…”

Claudin-2, a component of the tight junction, forms a paracellular water channel

“…Since the discovery of aquaporin (AQP) water channels in both epithelial cell membranes, the molecular basis of a transcellular pathway has been evident . By contrast, the contribution of the paracellular pathway through the tight junctions (TJ) was estimated to be between 0 and 100%, depending on the method used for analysis (Kovbasnjuk et al, 1998;Quigley and Baum, 2002;Shachar-Hill and Hill, 2002;Spring, 1998;Zeuthen, 1995). Although TJs are often named aqueous pores, there is, as yet, no direct experimental evidence of paracellular water flux.…”

Renal Tubular Development

“…For this to occur, the proximal tubule must be very permeable to water. Water movement is predominantly through the cell and not across the paracellular pathway [213,214]. The constitutively water-permeable proximal tubule and thin descending limb have water channels on the apical and basolateral membranes [1].…”

“…The apparent paradox between the higher water permeability in the neonatal proximal tubule and the lower water permeability of the apical and basolateral membranes was resolved with measurements of the contribution of the intracellular compartment to water movement in the neonatal and adult proximal tubule. The intracellular compartment was found to cause a large resistance to water flow, and neonatal proximal tubule intracellular compartment was less of a constraint to transcellular water movement than that of the adult [214]. Blunted synthesis in the medullary and cortical collecting tubule [352] The postnatal increase in glucocorticoids is a likely factor in mediating the above noted maturational changes in water permeability and aquaporin 1 expression.…”