Home LiteratureArticle Details
PMID: 11375422 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability.

The Journal of clinical investigation ·Vol. 107 ·No. 10 ·2001-05-00 ·Pages 1319-27

Van Itallie C, Rahner C, Anderson JM

Abstract

Tight junctions regulate paracellular conductance and ionic selectivity. These properties vary among epithelia but the molecular basis of this variation remains unknown. To test whether members of the claudin family of tight junction proteins influence paracellular ionic selectivity, we expressed human claudin-4 in cultured MDCK cells using an inducible promoter. Overexpression increased the complexity of tight junction strands visible by freeze-fracture microscopy without affecting the levels of claudin-1, -2, or -3, occludin, or ZO-1. A decrease in conductance correlated directly with the kinetics of claudin-4 induction. Dilution potentials revealed that the decrease in paracellular conductance resulted from a selective decrease in Na(+) permeability without a significant effect on Cl(-) permeability. Flux for an uncharged solute, mannitol, and the rank order of permeabilities for the alkali metal cations were unchanged. A paracellular site for these effects was supported by the lack of apical/basal directionality of the dilution potentials, the linearity of current-voltage relationships, and the lack of influence of inhibitors of major transcellular transporters. These results provide, to our knowledge, the first direct demonstration of the ability of a claudin to influence paracellular ion selectivity and support a role for the claudins in creating selective channels through the tight-junction barrier.

MeSH Terms
Animals Biological Transport Claudin-4 Dogs Electric Conductivity Electric Impedance Gene Expression Regulation Humans Membrane Proteins/biosynthesis,genetics Permeability Phosphoproteins Recombinant Proteins/biosynthesis Sodium/metabolism Tight Junctions/physiology,ultrastructure Zonula Occludens-1 Protein
Chemicals
CLDN4 protein, human Claudin-4 Membrane Proteins Phosphoproteins Recombinant Proteins TJP1 protein, human Zonula Occludens-1 Protein Sodium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Van Itallie C
Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 06520-8019, USA. [email protected]
Rahner C
Anderson J M
References (36)
36 references, click to expand
  1. Manner of interaction of heterogeneous claudin species within and between tight junction strands.
    J Cell Biol. 1999 Nov 15;147(4):891-903 PMID: 10562289
  2. Ca(2+)-independent cell-adhesion activity of claudins, a family of integral membrane proteins localized at tight junctions.
    Curr Biol. 1999 Sep 23;9(18):1035-8 PMID: 10508613
  3. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins.
    J Cell Biol. 1999 Dec 13;147(6):1351-63 PMID: 10601346
  4. CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice.
    Cell. 1999 Dec 10;99(6):649-59 PMID: 10612400
  5. Claudin-1 contributes to the epithelial barrier function in MDCK cells.
    Eur J Cell Biol. 1999 Dec;78(12):849-55 PMID: 10669103
  6. Molecular physiology and pathophysiology of tight junctions I. Tight junction structure and function: lessons from mutant animals and proteins.
    Am J Physiol Gastrointest Liver Physiol. 2000 Aug;279(2):G250-4 PMID: 10915631
  7. Inducible expression of claudin-1-myc but not occludin-VSV-G results in aberrant tight junction strand formation in MDCK cells.
    J Cell Sci. 2000 Oct;113 Pt 19:3387-98 PMID: 10984430
  8. Occludin localization at the tight junction requires the second extracellular loop.
    J Membr Biol. 2000 Dec 1;178(3):235-47 PMID: 11140279
  9. Mutations in the gene encoding tight junction claudin-14 cause autosomal recessive deafness DFNB29.
    Cell. 2001 Jan 12;104(1):165-72 PMID: 11163249
  10. Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas, and gut.
    Gastroenterology. 2001 Feb;120(2):411-22 PMID: 11159882
  11. Transepithelial transport in cell culture.
    Proc Natl Acad Sci U S A. 1976 Apr;73(4):1212-6 PMID: 1063404
  12. Twenty-first Bowditch lecture. The epithelial junction: bridge, gate, and fence.
    Physiologist. 1977 Feb;20(1):10-8 PMID: 16304
  13. A comparison of ion concentrations, potentials and conductances of amphibian, bovine and cephalopod lenses.
    J Physiol. 1977 Oct;272(1):167-86 PMID: 304100
  14. Polarized monolayers formed by epithelial cells on a permeable and translucent support.
    J Cell Biol. 1978 Jun;77(3):853-80 PMID: 567227
  15. Distribution and characteristics of the occluding junctions in a monolayer of a cell line (MDCK) derived from canine kidney.
    J Membr Biol. 1978 Nov 8;43(4):351-65 PMID: 731681
  16. Barrier function of epithelia.
    Am J Physiol. 1981 Oct;241(4):G275-88 PMID: 7032321
  17. Tight junction structure and ZO-1 content are identical in two strains of Madin-Darby canine kidney cells which differ in transepithelial resistance.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2401-8 PMID: 3058723
  18. Clostridium perfringens enterotoxin acts by producing small molecule permeability alterations in plasma membranes.
    Toxicology. 1994 Feb 28;87(1-3):43-67 PMID: 8160188
  19. Cell division does not increase transepithelial permeability of LLC-PK1 cell sheets.
    Exp Cell Res. 1995 Oct;220(2):446-55 PMID: 7556454
  20. Nucleotide receptor-mediated decrease of tight-junctional permeability in cultured human cervical epithelium.
    Am J Physiol. 1996 Jun;270(6 Pt 1):C1715-25 PMID: 8764155
  21. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein.
    J Cell Biol. 1996 Aug;134(4):1031-49 PMID: 8769425
  22. Occludin is a functional component of the tight junction.
    J Cell Sci. 1996 Sep;109 ( Pt 9):2287-98 PMID: 8886979
  23. Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments.
    J Cell Biol. 1997 Jul 14;138(1):181-92 PMID: 9214391
  24. Tumor necrosis factor-alpha increases sodium and chloride conductance across the tight junction of CACO-2 BBE, a human intestinal epithelial cell line.
    J Membr Biol. 1998 Feb 1;161(3):263-74 PMID: 9493132
  25. Regulation of the movement of solutes across tight junctions.
    Annu Rev Physiol. 1998;60:143-59 PMID: 9558458
  26. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin.
    J Cell Biol. 1998 Jun 29;141(7):1539-50 PMID: 9647647
  27. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts.
    J Cell Biol. 1998 Oct 19;143(2):391-401 PMID: 9786950
  28. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton.
    J Biol Chem. 1998 Nov 6;273(45):29745-53 PMID: 9792688
  29. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands.
    Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):511-6 PMID: 9892664
  30. Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis.
    J Cell Biol. 1999 May 3;145(3):579-88 PMID: 10225958
  31. Paracellin-1, a renal tight junction protein required for paracellular Mg2+ resorption.
    Science. 1999 Jul 2;285(5424):103-6 PMID: 10390358
  32. Opposite regulation of transepithelial electrical resistance and paracellular permeability by Rho in Madin-Darby canine kidney cells.
    J Biol Chem. 1999 Jul 23;274(30):20982-8 PMID: 10409646
  33. Paracellular channels!
    Science. 1999 Jul 2;285(5424):62 PMID: 10428705
  34. Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells.
    J Cell Biol. 1999 Oct 4;147(1):185-94 PMID: 10508865
  35. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: Evidence for direct involvement of claudins in tight junction barrier.
    J Cell Biol. 1999 Oct 4;147(1):195-204 PMID: 10508866
  36. Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3.
    J Biol Chem. 1999 Dec 3;274(49):35179-85 PMID: 10575001
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2001-05-00
Pages
1319-27
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC209303
Subset
IM
Grants
NIDDK NIH HHS · R01 DK045134 · United States
NIDDK NIH HHS · DK-45134 · United States
NIDDK NIH HHS · DK-34989 · United States
NIDDK NIH HHS · DK-38979 · United States
NIDDK NIH HHS · P30 DK034989 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]