Abstract
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 fluid than wild-type mice and had lower urine osmolality (505 +/- 40 vs. 1081 +/- 68 milliosmolar). Transepithelial osmotic water permeability (Pf) in isolated microperfused S2 segments of proximal tubule from AQP1 knockout [-/-] mice was 0.033 +/- 0.005 cm/s (SE, n = 6 mice, 37 degreesC), much lower than that of 0.15 +/- 0.03 cm/s (n = 8) in tubules from wild-type [+/+] mice (P < 0.01). In the presence of isosmolar luminal perfusate and bath solutions, spontaneous fluid absorption rates (nl/min/mm tubule length) were 0.31 +/- 0.12 (-/-, n = 5) and 0.64 +/- 0.15 (+/+, n = 8). As determined by free-flow micropuncture, the ratios of tubular fluid-to-plasma concentrations of an impermeant marker TF/P in end proximal tubule fluid were 1.36 +/- 0. 05 (-/-, n = 8 mice [53 tubules]) and 1.95 +/- 0.09 (+/+, n = 7 mice [40 tubules]) (P < 0.001), corresponding to 26 +/- 3% [-/-] and 48 +/- 2% [+/+] absorption of the filtered fluid load. In collections of distal tubule fluid, TF/P were 2.8 +/- 0.3 [-/-] and 4.4 +/- 0.5 [+/+], corresponding to 62 +/- 4% [-/-] and 76 +/- 3% [+/+] absorption (P < 0.02). These data indicate that AQP1 deletion in mice results in decreased transepithelial proximal tubule water permeability and defective fluid absorption. Thus, the high water permeability in proximal tubule of wild-type mice is primarily transcellular, mediated by AQP1 water channels, and required for efficient near-isosmolar fluid absorption.
MeSH Terms
Animals
Aquaporin 1
Aquaporins
Female
Ion Channels/genetics,physiology
Kidney Tubules, Proximal/physiopathology
Male
Mice
Mice, Knockout
Mice, Transgenic
Osmosis
Chemicals
Aqp1 protein, mouse
Aquaporins
Ion Channels
Aquaporin 1
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Schnermann J
Department of Physiology, University of Michigan Medical School, Ann Arbor, MI 48109-0622, USA.
Chou C L
Ma T
Traynor T
Knepper M A
Verkman A S
References (27)
27 references, click to expand
-
Osmotic gradient dependence of osmotic water permeability in rabbit proximal convoluted tubule.
J Membr Biol. 1988 Oct;105(1):33-43
PMID: 2852255
-
Comparison of transcellular and transepithelial water osmotic permeabilities (Pos) in the isolated proximal straight tubule (PST) of the rabbit kidney.
Pflugers Arch. 1988 Jul;412(1-2):66-74
PMID: 2845357
-
Glucose transporters serve as water channels.
Proc Natl Acad Sci U S A. 1990 Apr;87(8):3244-7
PMID: 2326282
-
Evidence from oocyte expression that the erythrocyte water channel is distinct from band 3 and the glucose transporter.
J Clin Invest. 1991 Nov;88(5):1553-8
PMID: 1939644
-
Kinetics of urea and water permeability activation by vasopressin in rat terminal IMCD.
Am J Physiol. 1992 Jun;262(6 Pt 2):F989-98
PMID: 1320335
-
Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein.
Biochemistry. 1992 Aug 25;31(33):7436-40
PMID: 1510932
-
Functional reconstitution of the isolated erythrocyte water channel CHIP28.
J Biol Chem. 1992 Sep 15;267(26):18267-9
PMID: 1526967
-
Localization of the CHIP28 water channel in rat kidney.
Am J Physiol. 1992 Dec;263(6 Pt 1):C1225-33
PMID: 1282299
-
Cloning, functional analysis and cell localization of a kidney proximal tubule water transporter homologous to CHIP28.
J Cell Biol. 1993 Jan;120(2):359-69
PMID: 8421053
-
CHIP28 water channels are localized in constitutively water-permeable segments of the nephron.
J Cell Biol. 1993 Jan;120(2):371-83
PMID: 7678419
-
Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: a freeze-fracture study.
J Cell Biol. 1993 Nov;123(3):605-18
PMID: 7693713
-
Functional independence of monomeric CHIP28 water channels revealed by expression of wild-type mutant heterodimers.
J Biol Chem. 1994 Apr 8;269(14):10417-22
PMID: 7511600
-
Mutations in aquaporin-1 in phenotypically normal humans without functional CHIP water channels.
Science. 1994 Sep 9;265(5178):1585-7
PMID: 7521540
-
Quantification of Aquaporin-CHIP water channel protein in microdissected renal tubules by fluorescence-based ELISA.
J Clin Invest. 1995 Jan;95(1):422-8
PMID: 7529263
-
Cotransport of water by the Na+/glucose cotransporter.
Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13367-70
PMID: 8917597
-
Molecular design of aquaporin-1 water channel as revealed by electron crystallography.
Nat Struct Biol. 1997 Apr;4(4):263-5
PMID: 9095192
-
Evidence that aquaporin-1 mediates NaCl-induced water flux across descending vasa recta.
Am J Physiol. 1997 May;272(5 Pt 2):F587-96
PMID: 9176368
-
The three-dimensional structure of aquaporin-1.
Nature. 1997 Jun 5;387(6633):624-7
PMID: 9177353
-
Three-dimensional organization of a human water channel.
Nature. 1997 Jun 5;387(6633):627-30
PMID: 9177354
-
Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea.
J Biol Chem. 1997 Aug 15;272(33):20782-6
PMID: 9252401
-
Absence of tubuloglomerular feedback responses in AT1A receptor-deficient mice.
Am J Physiol. 1997 Aug;273(2 Pt 2):F315-20
PMID: 9277593
-
Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels.
J Biol Chem. 1998 Feb 20;273(8):4296-9
PMID: 9468475
-
Perfusion of isolated renal tubules.
Yale J Biol Med. 1972 Jun-Aug;45(3-4):321-6
PMID: 4629410
-
Surface areas of brush border and lateral cell walls in the rabbit proximal nephron.
Kidney Int. 1975 Dec;8(6):343-8
PMID: 1206850
-
Quantitative characterization of the tubuloglomerular feedback response: effect of growth.
Am J Physiol. 1984 Nov;247(5 Pt 2):F808-15
PMID: 6496746
-
Evidence for transcellular osmotic water flow in rat proximal tubules.
Am J Physiol. 1985 Jul;249(1 Pt 2):F124-31
PMID: 4014469
-
Reflection coefficients and water permeability in rat proximal tubule.
Am J Physiol. 1989 Oct;257(4 Pt 2):F658-68
PMID: 2801963