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PMID: 7517548 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells.

Ishibashi K, Sasaki S, Fushimi K, Uchida S, Kuwahara M, Saito H, Furukawa T, Nakajima K, Yamaguchi Y, Gojobori T

Abstract

Water transport in highly water-permeable membranes is conducted by water-selective pores--namely, water channels. The recent cloning of water channels revealed the water-selective characteristics of these proteins when expressed in Xenopus oocytes or reconstituted in liposomes. Currently, it is assumed that the function of water channels is to transport only water. We now report the cloning of a member of the water channel that also transports nonionic small molecules such as urea and glycerol. We named this channel aquaporin 3 (AQP3) for its predominant water permeability. AQP3 has amino acid sequence identity with major intrinsic protein (MIP) family proteins including AQP-channel-forming integral membrane protein, AQP-collecting duct, MIP, AQP-gamma tonoplast intrinsic protein, nodulin 26, and glycerol facilitator (33-42%). Thus, AQP3 is an additional member of the MIP family. Osmotic water permeability of Xenopus oocytes measured by videomicroscopy was 10-fold higher in oocytes injected with AQP3 transcript than with water-injected oocytes. The increase in osmotic water permeability was inhibited by HgCl2, and this effect was reversed by a reducing agent, 2-mercaptoethanol. Although to a smaller degree, AQP3 also facilitated the transport of nonionic small solutes such as urea and glycerol, while the previously cloned water channels are permeable only to water when expressed in Xenopus oocytes. AQP3 mRNA was expressed abundantly in kidney medulla and colon. In kidney, it was exclusively immunolocalized at the basolateral membrane of collecting duct cells. AQP3 may function as a water and urea exit mechanism in antidiuresis in collecting duct cells.

MeSH Terms
Amino Acid Sequence Animals Aquaporin 3 Aquaporins Base Sequence Cell Membrane/metabolism Female Gene Library Glycerol/metabolism Ion Channels/metabolism Kidney Cortex/metabolism Kidney Medulla/metabolism Kidney Tubules, Collecting/metabolism Kinetics Membrane Proteins/biosynthesis,genetics,metabolism Molecular Sequence Data Oocytes/physiology Phylogeny Polymerase Chain Reaction Rats Recombinant Proteins/biosynthesis,metabolism Urea/metabolism Water/metabolism Xenopus laevis
Chemicals
Aqp3 protein, rat Aquaporins Ion Channels Membrane Proteins Recombinant Proteins Water Aquaporin 3 Urea Glycerol
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Ishibashi K
School of Medicine, Tokyo Medical and Dental University, Japan.
Sasaki S
Fushimi K
Uchida S
Kuwahara M
Saito H
Furukawa T
Nakajima K
Yamaguchi Y
Gojobori T
References (32)
32 references, click to expand
  1. Cloning and characterization of the vasopressin-regulated urea transporter.
    Nature. 1993 Oct 28;365(6449):844-7 PMID: 8413669
  2. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  3. Tissue-specific expression of mRNA encoding rat kidney water channel CHIP28k by in situ hybridization.
    Am J Physiol. 1993 Jan;264(1 Pt 1):C237-45 PMID: 7679251
  4. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein.
    Science. 1992 Apr 17;256(5055):385-7 PMID: 1373524
  5. A common ancestor for bovine lens fiber major intrinsic protein, soybean nodulin-26 protein, and E. coli glycerol facilitator.
    Cell. 1990 Jan 26;60(2):185-6 PMID: 2404610
  6. Osmotically induced volume and turbidity changes of Escherichia coli due to salts, sucrose and glycerol, with particular reference to the rapid permeation of glycerol into the cell.
    J Gen Microbiol. 1974 May;82(1):125-42 PMID: 4604867
  7. Transport of water and urea in red blood cells.
    Am J Physiol. 1984 Mar;246(3 Pt 1):C195-203 PMID: 6199982
  8. Aquaporins: a family of water channel proteins.
    Am J Physiol. 1993 Sep;265(3 Pt 2):F461 PMID: 7692747
  9. The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning.
    Cell. 1984 Nov;39(1):49-59 PMID: 6207938
  10. Structure and regulation of the glpFK operon encoding glycerol diffusion facilitator and glycerol kinase of Escherichia coli K-12.
    J Biol Chem. 1992 Mar 25;267(9):6122-31 PMID: 1372899
  11. Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli.
    J Bacteriol. 1980 Oct;144(1):274-8 PMID: 6998951
  12. Nucleotide sequence of the region encompassing the glpKF operon and its upstream region containing a bent DNA sequence of Escherichia coli.
    Nucleic Acids Res. 1989 Jun 12;17(11):4378 PMID: 2544860
  13. Water channels in cell membranes.
    Annu Rev Physiol. 1992;54:97-108 PMID: 1373280
  14. 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
  15. Cell membrane water permeability of rabbit cortical collecting duct.
    J Membr Biol. 1987;96(1):27-43 PMID: 3585984
  16. Root-specific genes from tobacco and Arabidopsis homologous to an evolutionarily conserved gene family of membrane channel proteins.
    Nucleic Acids Res. 1990 Dec 25;18(24):7449 PMID: 2129561
  17. Glucose transporters serve as water channels.
    Proc Natl Acad Sci U S A. 1990 Apr;87(8):3244-7 PMID: 2326282
  18. Cloning and expression of apical membrane water channel of rat kidney collecting tubule.
    Nature. 1993 Feb 11;361(6412):549-52 PMID: 8429910
  19. Developmental gene expression and tissue distribution of the CHIP28 water-channel protein.
    Proc Natl Acad Sci U S A. 1993 May 15;90(10):4500-4 PMID: 8506291
  20. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11110-4 PMID: 1722319
  21. Similarity of the product of the Drosophila neurogenic gene big brain to transmembrane channel proteins.
    Nature. 1990 May 10;345(6271):163-7 PMID: 1692392
  22. Expression of mRNA coding for kidney and red cell water channels in Xenopus oocytes.
    J Biol Chem. 1990 Sep 15;265(26):15375-8 PMID: 2394728
  23. Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7275-9 PMID: 8346245
  24. Inhibition of urea transport in inner medullary collecting duct by phloretin and urea analogues.
    Am J Physiol. 1989 Sep;257(3 Pt 2):F359-65 PMID: 2506765
  25. Soybean nodulin 26 is homologous to the major intrinsic protein of the bovine lens fiber membrane.
    Nucleic Acids Res. 1988 Oct 11;16(19):9347 PMID: 3174457
  26. Vegetative and Seed-Specific Forms of Tonoplast Intrinsic Protein in the Vacuolar Membrane of Arabidopsis thaliana.
    Plant Physiol. 1992 Jun;99(2):561-70 PMID: 16668923
  27. The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes.
    EMBO J. 1993 Jun;12(6):2241-7 PMID: 8508761
  28. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs.
    Nucleic Acids Res. 1987 Oct 26;15(20):8125-48 PMID: 3313277
  29. Tandem sequence repeats in transmembrane channel proteins.
    Trends Biochem Sci. 1991 May;16(5):170-1 PMID: 1715617
  30. A multifunctional aqueous channel formed by CFTR.
    Science. 1992 Nov 27;258(5087):1477-9 PMID: 1279809
  31. Growth factor-induced delayed early response genes.
    Mol Cell Biol. 1992 Sep;12(9):3919-29 PMID: 1508193
  32. Evolution of the MIP family of integral membrane transport proteins.
    Mol Microbiol. 1991 Jan;5(1):33-7 PMID: 2014003
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1994-07-05
Pages
6269-73
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC44182
Subset
IM
Databases
GENBANK
D17695
Corrections
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