Journal of Cell Science, Vol 109, Issue 9 2287-2298, Copyright © 1996 by Company of Biologists

JOURNAL ARTICLES

Occludin is a functional component of the tight junction

KM McCarthy, IB Skare, MC Stankewich, M Furuse, S Tsukita, RA Rogers, RD Lynch and EE Schneeberger
Department of Pathology, Massachusetts General Hospital, Boston 02114, USA.

Occludin's role in mammalian tight junction activity was examined by 'labeling' the occludin pool with immunologically detectable chick occludin. This was accomplished by first transfecting MDCK cell with the Lac repressor gene. HygR clones were then transfected with chick occludin cDNA inserted into a Lac operator construct. The resulting HygR/NeoR clones were plated on porous inserts and allowed to form tight junctions. Once steady state transepithelial electrical resistance was achieved, isopropyl- beta-D-thiogalactoside was added to induce chick occludin expression. Confocal laser scanning microscopy of monolayers immunolabeled with Oc-2 monoclonal antibody revealed that chick occludin localized precisely to the preformed tight junctions. When sparse cultures were maintained in low Ca2+ medium, chick occludin and canine ZO-1 co-localized to punctate sites in the cytoplasm suggesting their association within the same vesicular structures. In low calcium medium both proteins also co-localized to contact sites between occasional cell pairs, where a prominent bar was formed at the plasma membrane. Chick occludin was detectable by western blot within two hours of adding isopropyl- beta-D-thiogalactoside to monolayers that had previously achieved steady state transepithelial electrical resistance; this coincided with focal immunofluorescence staining for chick occludin at the cell membrane of some cells. A gradual rise in transepithelial electrical resistance, above control steady state values, began five hours after addition of the inducing agent reaching new steady state values, which were 30-40% above baseline, 31 hours later. Upon removal of isopropyl- beta-D-thiogalactoside chick occludin expression declined slowly until it was no longer detected in western blots 72 hours later; transepithelial electrical resistance also returned to baseline values during this time. While densitometric analysis of western blots indicated that the presence of chick occludin had no detectable effect on E-cadherin or ZO-1 expression, the possibility cannot be excluded that ZO-1 might be a limiting factor in the expression of chick occludin at the cell surface. To test whether expression of chick occludin affected the process of tight junction assembly, monolayers in low Ca2+ medium were treated with isopropyl- beta-D-thiogalactoside for 24 or 48 hours, before Ca2+ was added to stimulate tight junction assembly. Chick occludin did not alter the rate at which transepithelial electrical resistance developed, however, steady state values were 30-40% above control monolayers not supplemented with the inducing agent. By freeze fracture analysis, the number of parallel tight junction strands shifted from a mode of three in controls to four strands in cells expressing chick occludin and the mean width of the tight junction network increased from 175 +/- 11 nm to 248 +/- 16 nm. Two days after plating confluent monolayers that were induced to express chick occludin, mannitol flux was reduced to a variable degree relative to control monolayers. With continued incubation with the inducing agent, mannitol flux increased on day 11 to 50%, and TER rose to 45% above controls. Both of these changes were reversible upon removal of isopropyl- beta-D-thiogalactoside. These data are consistent with the notion that occludin contributes to the electrical barrier function of the tight junction and possibly to the formation of aqueous pores within tight junction strands.
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				K. Morita, H. Sasaki, M. Furuse, and S. Tsukita Endothelial Claudin: Claudin-5/Tmvcf Constitutes Tight Junction Strands in Endothelial Cells J. Cell Biol., October 4, 1999; 147(1): 185 - 194. [Abstract] [Full Text] [PDF]

				N. Sonoda, M. Furuse, H. Sasaki, S. Yonemura, J. Katahira, Y. Horiguchi, and S. Tsukita Clostridium perfringens Enterotoxin Fragment Removes Specific Claudins from Tight Junction Strands: Evidence for Direct Involvement of Claudins in Tight Junction Barrier J. Cell Biol., October 4, 1999; 147(1): 195 - 204. [Abstract] [Full Text] [PDF]

				J. Ye, T. Tsukamoto, A. Sun, and S. K. Nigam A role for intracellular calcium in tight junction reassembly after ATP depletion-repletion Am J Physiol Renal Physiol, October 1, 1999; 277(4): F524 - F532. [Abstract] [Full Text] [PDF]

				D. A. Antonetti, A. J. Barber, L. A. Hollinger, E. B. Wolpert, and T. W. Gardner Vascular Endothelial Growth Factor Induces Rapid Phosphorylation of Tight Junction Proteins Occludin and Zonula Occluden 1. A POTENTIAL MECHANISM FOR VASCULAR PERMEABILITY IN DIABETIC RETINOPATHY AND TUMORS J. Biol. Chem., August 13, 1999; 274(33): 23463 - 23467. [Abstract] [Full Text] [PDF]

				L. L. Mitic, E. E. Schneeberger, A. S. Fanning, and J. M. Anderson Connexin-Occludin Chimeras Containing the Zo-Binding Domain of Occludin Localize at Mdck Tight Junctions and Nrk Cell Contacts J. Cell Biol., August 9, 1999; 146(3): 683 - 693. [Abstract] [Full Text] [PDF]

				J. L. Underwood, C. G. Murphy, J. Chen, L. Franse-Carman, I. Wood, D. L. Epstein, and J. A. Alvarado Glucocorticoids regulate transendothelial fluid flow resistance and formation of intercellular junctions Am J Physiol Cell Physiol, August 1, 1999; 277(2): C330 - C342. [Abstract] [Full Text] [PDF]

				H. Hasegawa, H. Fujita, H. Katoh, J. Aoki, K. Nakamura, A. Ichikawa, and M. Negishi Opposite Regulation of Transepithelial Electrical Resistance and Paracellular Permeability by Rho in Madin-Darby Canine Kidney Cells J. Biol. Chem., July 23, 1999; 274(30): 20982 - 20988. [Abstract] [Full Text] [PDF]

				A. S. FANNING, L. L. MITIC, and J. M. ANDERSON Transmembrane Proteins in the Tight Junction Barrier J. Am. Soc. Nephrol., June 1, 1999; 10(6): 1337 - 1345. [Abstract] [Full Text]

				K. H. Cheong, D. Zacchetti, E. E. Schneeberger, and K. Simons VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells PNAS, May 25, 1999; 96(11): 6241 - 6248. [Abstract] [Full Text] [PDF]

				K. Morita, H. Sasaki, K. Fujimoto, M. Furuse, and S. Tsukita Claudin-11/OSP-based Tight Junctions of Myelin Sheaths in Brain and Sertoli Cells in Testis J. Cell Biol., May 3, 1999; 145(3): 579 - 588. [Abstract] [Full Text] [PDF]

				V. Wong, D. Ching, P. D. McCrea, and G. L. Firestone Glucocorticoid Down-regulation of Fascin Protein Expression Is Required for the Steroid-induced Formation of Tight Junctions and Cell-Cell Interactions in Rat Mammary Epithelial Tumor Cells J. Biol. Chem., February 26, 1999; 274(9): 5443 - 5453. [Abstract] [Full Text] [PDF]

				D. A. Goodenough Plugging the leaks PNAS, January 19, 1999; 96(2): 319 - 321. [Full Text] [PDF]

				K. Morita, M. Furuse, K. Fujimoto, and S. Tsukita Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands PNAS, January 19, 1999; 96(2): 511 - 516. [Abstract] [Full Text] [PDF]

				M Wachtel, K Frei, E Ehler, A Fontana, K Winterhalter, and S. Gloor Occludin proteolysis and increased permeability in endothelial cells through tyrosine phosphatase inhibition J. Cell Sci., January 12, 1999; 112(23): 4347 - 4356. [Abstract] [PDF]

				L. Lapierre, P. Tuma, J Navarre, J. Goldenring, and J. Anderson VAP-33 localizes to both an intracellular vesicle population and with occludin at the tight junction J. Cell Sci., January 11, 1999; 112(21): 3723 - 3732. [Abstract] [PDF]

				S. Bamforth, U Kniesel, H Wolburg, B Engelhardt, and W Risau A dominant mutant of occludin disrupts tight junction structure and function J. Cell Sci., January 6, 1999; 112(12): 1879 - 1888. [Abstract] [PDF]

				C. YEAMAN, K. K. GRINDSTAFF, and W. J. NELSON New Perspectives on Mechanisms Involved in Generating Epithelial Cell Polarity Physiol Rev, January 1, 1999; 79(1): 73 - 98. [Abstract] [Full Text] [PDF]

				A. S. Fanning, B. J. Jameson, L. A. Jesaitis, and J. M. Anderson The Tight Junction Protein ZO-1 Establishes a Link between the Transmembrane Protein Occludin and the Actin Cytoskeleton J. Biol. Chem., November 6, 1998; 273(45): 29745 - 29753. [Abstract] [Full Text] [PDF]

				M. Furuse, H. Sasaki, K. Fujimoto, and S. Tsukita A Single Gene Product, Claudin-1 or -2, Reconstitutes Tight Junction Strands and Recruits Occludin in Fibroblasts J. Cell Biol., October 19, 1998; 143(2): 391 - 401. [Abstract] [Full Text] [PDF]