Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: Evidence for direct involvement of claudins in tight junction barrier

Journal of Cell Biology

Volumn 147, Issue 1, 1999, Pages 195-204

  Sonoda, Noriyuki ^a   Furuse, Mikio ^a   Sasaki, Hiroyuki ^c,d   Yonemura, Shigenobu ^a   Katahira, Jun ^b   Horiguchi, Yasuhiko ^b   Tsukita, Shoichiro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c 600 8815   (Japan)

^d JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Claudin; Clostridium perfringens enterotoxin; Epithelial barrier; Freezefracture; Tight junction

Indexed keywords

CLAUDIN; ENTEROTOXIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; FREEZE FRACTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TIGHT JUNCTION;

ANIMALS; CELL DEATH; CELL LINE; CELL MEMBRANE; CELL SIZE; CYTOPLASM; DOGS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ELECTRIC IMPEDANCE; ENTEROTOXINS; FLUORESCENT ANTIBODY TECHNIQUE; L CELLS (CELL LINE); MEMBRANE PROTEINS; MICE; PEPTIDE FRAGMENTS; PROTEIN BINDING; TIGHT JUNCTIONS; TIME FACTORS; TRANSFECTION;

ANIMALIA; CLOSTRIDIUM PERFRINGENS; POSIBACTERIA;

EID: 0033523773     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.1.195     Document Type: Article

References (42)

1. Anderson, J.M., and C.M. Van Itallie. 1995. Tight junctions and the molecular basis for regulation of paracellular permeability. Am. J. Physiol. 269:G467-G475.
2. Ando-Akatsuka, Y., M. Saitou, T. Hirase, M. Kishi, A. Sakakibara, M. Itoh, S. Yonemura, M. Furuse, and Sh. Tsukita. 1996. Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. J. Cell Biol. 133:43-47.
3. Balda, M.S., J.A. Whitney, C. Flores, S. Gonzalez, M. Cereijido, and K. Matter. 1996. 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. 134:1031-1049.
4. Bricht, M.M., and R.L. Miesfeld. 1991. Isolation and characterization of transcripts induced by androgen withdrawal and apoptotic cell death in the rat ventral prostate. Mol. Endocrinol. 5:1381-1388.
5. Chen, Y.-H., C. Merzdorf, D.L. Paul, and D.A. Goodenough. 1997. COOH terminus of occludin is required for tight junction barrier function in early Xenopus embryos. J. Cell Biol. 138:891-899.
6. Farquhar, M.G., and G.E. Palade. 1963. Junctional complexes in various epithelia. J. Cell Biol. 17:375-412.
7. Fujimoto, K. 1995. Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J. Cell Sci. 108:3443-3449.
8. Furuse, M., K. Fujimoto, N. Sato, T. Hirase, Sa. Tsukita, and Sh. Tsukita. 1996. Overexpression of occludin, a tight junction-associated integral membrane protein, induces the formation of intracellular multilamellar bodies bearing tight junction-like structures. J. Cell Sci. 109:429-435.
9. Furuse, M., K. Fujita, T. Hiiragi, K. Fujimoto, and Sh. Tsukita. 1998a. Claudin-1 and -2: Novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141:1539-1550.
10. Furuse, M., T. Hirase, M. Itoh, A. Nagafuchi, S. Yonemura, Sa. Tsukita, and Sh. Tsukita. 1993. Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 123:1777-1788.
11. Furuse, M., H. Sasaki, K. Fujimoto, and Sh. Tsukita. 1998b. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J. Cell Biol. 143:391-401.
12. Furuse, M., H. Sasaki, and Sh. Tsukita. 1999. Manner of interaction of heterogeneous claudin species within and between tight junction strands. J. Cell Biol. 20:429-435.
13. Goodenough, D.A. 1999. Plugging the leaks. Proc. Natl. Acad. Sci. USA. 96: 319-321.
14. Gumbiner, B. 1987. Structure, biochemistry, and assembly of epithelial tight junctions. Am. J. Physiol. 253:C749-C758.
15. Gumbiner, B. 1993. Breaking through the tight junction barrier. J. Cell Biol. 123:1631-1633.
16. Hanna, P.C., T.A. Mietzner, G.K. Schoolnik, and B.A. McClane. 1991. Localization of the receptor-binding region of Clostridium perfringens enterotoxin utilizing cloned toxin fragments and synthetic peptides. J. Biol. Chem. 17: 11037-11043.
17. Hanna, P.C., E.H. Wieckowski, T.A. Mietzner, and B.A. McClane. 1992. Mapping of functional regions of Clostridium perfringens type A enterotoxin. Infect. Immun. 60:2110-2114.
18. Hayashi, K., S. Yonemura, T. Matsui, Sa, Tsukita, and Sh. Tsukita. 1999. Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxyl-terminal threonine phosphorylated in cultured cells and tissues: Application of a novel fixation protocol using trichloroacetic acids (TCA) as a fixative. J. Cell Sci. 112:1149-1158.
19. Horiguchi, Y., T. Akai, and G. Sakaguchi. 1987. Isolation and function of a Clostridium perfringens enterotoxin fragment. Infect. Immun. 55:2912-2915.
20. Horiguchi, Y., T. Uemura, Y. Kamata, S. Kozaki, and G. Sakaguchi. 1986. Production and characterization of monoclonal antibodies to Clostridium perfringens enterotoxin. Infect. Immun. 52:31-35.
21. Katahira, J., N. Inoue, Y. Horiguchi, M. Matsuda, and N. Sugimoto. 1997a. Molecular cloning and functional characterization of the receptor for Clostridium perfringens enterotoxin. J. Cell Biol. 136:1239-1247.
22. Katahira, J., H. Sugiyama, N. Inoue, Y. Horiguchi, M. Matsuda, and N. Sugimoto. 1997b. Clostridium perfringens enterotoxin utilizes two structurally related membrane proteins as functional receptors in vivo. J. Biol. Chem. 272: 26652-26658.
23. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
24. Martin-Padura, I., S. Lostaglio, M. Schneemann, L. Williams, M. Romano, P. Fruscella, C. Panzeri, A. Stoppacciaro, L. Ruco, A. Villa, et al. 1998. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell Biol. 142:117-127.
25. Matsuda, M., and N. Sugimoto. 1979. Calcium-independent and dependent steps in action of Clostridium perfringens enterotoxin on hela and vero cells. Biochem. Biophys. Res. Commun. 91:629-636.
26. Matter, K., and M.S. Balda. 1998. Biogenesis of tight junctions: the C-terminal domain of occludin mediates basolateral targeting. J. Cell Sci. 111:511-519.
27. McCarthy, K.M., I.B. Skare, M.C. Stankewich, M. Furuse, Sh. Tsukita, R.A. Rogers, R.D. Lynch, and E.E. Schneeberger. 1996. Occludin is a functional component of the tight junction. J. Cell Sci. 109:2287-2298.
28. McClane, B.A., and J.L. McDonel. 1981. Protective effects of osmotic stabilizers on morphological and permeability alterations induced in Vero cells by Clostridium perfringens enterotoxin. Biochim. Biophys. Acta. 641:401-409.
29. McClane, B.A., A.P. Wnek, K.I. Hulkower, and P.C. Hanna. 1988. Divalent cation involvement in the action of Clostridium perfringens type A enterotoxin. J. Biol. Chem. 263:2423-2435.
30. Morita, K., M. Furuse, K. Fujimoto, and Sh. Tsukita. 1999a. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc. Natl. Acad. Sci. USA. 96:511-516.
31. Morita, K., H. Sasaki, K. Fujimoto, M. Furuse, and Sh. Tsukita. 1999b. Claudin-11/OSP-based tight junctions in myelinated sheaths of oligodendrocytes and Sertoli cells in testis. J. Cell Biol. 145:579-588.
32. Moroi, S., M. Saitou, K. Fujimoto, A. Sakakibara, M. Furuse, O. Yoshida, and Sh. Tsukita. 1998. Occludin is concentrated at tight junctions of mouse/rat but not human/guinea pig Sertoli cells in testes. Am. J. Physiol. 274:C1708-C1717.
33. Saitou, M., K. Fujimoto, Y. Doi, M. Itoh, T. Fujimoto, M. Furuse, H. Takano, T. Noda, and Sh. Tsukita. 1998. Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J. Cell Biol. 141:397-408.
34. Sakaguchi, G., T. Uemura, and H. Riemann. 1973. Simplified method for purification of Clostridium perfringens type A enterotoxin. Appl. Microbiol. 27: 762-767.
35. Sakakibara, A., M. Furuse, M. Saitou, Y. Ando-Akatsuka, and Sh. Tsukita. 1997. Possible involvement of phosphorylation of occludin in tight junction formation. J. Cell Biol. 137:1393-1401.
36. Schneeberger, E.E., and R.D. Lynch. 1992. Structure, function, and regulation of cellular tight junctions. Am. J. Physiol. 262:L647-L661.
37. Staehelin, L.A. 1973. Further observations on the fine structure of freeze-cleaved tight junctions. J. Cell Sci. 13:763-786.
38. Staehelin, L.A. 1974. Structure and function of intercellular junctions. Int. Rev. Cytol. 39:191-283.
39. Stevenson, B.R., J.M. Anderson, D.A. Goodenough, and M.S. Mooseker. 1988. Tight junction structure and ZO-1 constant are identical in two strains of Madin-Darby Canine Kidney cells which differ in transepithelial resistance. J. Cell Biol. 107:2401-2408.
40. Tsukita, Sh., and M. Furuse. 1999. Occludin and claudins in tight junction strands: leading or supporting players? Trend. Cell Biol. 9:268-273.
41. Wolburg, H., J. Neuhaus, U. Kniesel, B. Krauss, E.-M. Schmid, M. Öcalan, C. Farrell, and W. Risau. 1994. Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes. J. Cell Sci. 107:1347-1357.
42. Wong, V., and B.M. Gumbiner. 1997. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J. Cell Biol. 136:399-409.