Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions

Journal of Cell Biology

Volumn 141, Issue 2, 1998, Pages 397-408

  Saitou, Mitinori ^a   Fujimoto, Kazushi ^a   Doi, Yoshinori ^a,b   Itoh, Masahiko ^a   Fujimoto, Toyoshi ^c   Furuse, Mikio ^a   Takano, Hiroshi ^d,e   Noda, Tetsuo ^d,e   Tsukita, Shoichiro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^c GUNMA UNIVERSITY   (Japan)

^d CANCER INSTITUTE   (Japan)

^e TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; OCCLUDIN; RNA DIRECTED DNA POLYMERASE; UNCLASSIFIED DRUG; ZONULA OCCLUDENS 1;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; ELECTRON MICROSCOPY; EPITHELIUM CELL; GENE TARGETING; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL; TIGHT JUNCTION;

ANIMALS; BIOTIN; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CELL POLARITY; CELLS, CULTURED; EPITHELIAL CELLS; FREEZE FRACTURING; GENE TARGETING; MEMBRANE PROTEINS; MICE; PHOSPHOPROTEINS; STEM CELLS; SUCCINIMIDES; TIGHT JUNCTIONS;

ANIMALIA;

EID: 0032550221     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.2.397     Document Type: Article

References (65)

1. Anderson, J.M., A.S. Fanning, L. Lapierre, and C.M. Van Itallie. 1995. Zonula occludens (ZO)-1 and ZO-2: membrane-associated guanylate kinase homologues (MAGuKs) of the tight junction. Biochem. Soc. Trans. 23:470-475.
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. Anzini, P., D.H.-H. Neuberg, M. Schachner, E. Nelles, K. Willecke, J. Zielasek, K. V. Toyka, U. Suter, and R. Martini. 1997. Structural abnormalities and deficient maintenance of peripheral nerve myelin in mice lacking the gap junction protein connexin 32. J. Neurosci. 17:4545-4551.
4. 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.
5. Baribault, H., and R.G. Oshima. 1991. Polarized and functional epithelia can form after the targeted inactivation of both mouse keratin 8 alleles. J. Cell Biol 115:1675-1684.
6. Brink, P.R., K. Cronin, K. Banach, E. Peterson, E.M. Westphale, K.H. Seul, S.V. Ramanan, and E.C. Beyer. 1997. Evidence for heteromeric gap junction channels formed from rat connexin43 and human connexin37. Am. J. Physiol. 273:1386-1396.
7. 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.
8. Chomczymski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
9. Citi, S., H. Sabanay, R. Jakes, B. Geiger, and J. Kendrick-Jones. 1988. Cingulin, a new peripheral component of tight junctions. Nature. 333:272-276.
10. Doetschman, T.C., H. Eistetter, M. Katz, W. Schmidt, and R. Kemler. 1985. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morph. 87:27-45.
11. Farquhar, M.G., and G.E. Palade. 1963. Junctional complexes in various epithelia. J. Cell Biol. 17:375-412.
12. Friedrich, G., and P, Soriano. 1991. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5:1513-1523.
13. 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.
14. Fujimoto, T., S. Nakade, A. Miyawaki, K. Mikoshiba, and K. Ogawa. 1992. Localization of inositol 1,4,5-trisphosphate receptor-like protein in plasmalemmal caveolae. J. Cell Biol. 119:1507-1513.
15. 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.
16. Furuse, M., M. Itoh, T. Hirase, A. Nagafuchi, S. Yonemura, Sa. Tsukita, and Sh. Tsukita. 1994. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J. Cell Biol. 127: 1617-1626.
17. 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.
18. Gumbiner, B. 1987. Structure, biochemistry, and assembly of epithelial tight junctions. Am. J. Physiol. 253:C749-C758.
19. Gumbiner, B.M. 1993. Breaking through the tight junction barrier. J. Cell Biol. 123:1631-1633.
20. Gumbiner, B., T. Lowenkopf, and D. Apatira. 1991. Identification of a 160kDa polypeptide that binds to the tight junction protein ZO-1. Proc. Natl. Acad. Sci. USA. 88:3460-3464.
21. Heuser, J.E., T.S. Reese, M.J. Dennis, Y. Jan, L. Van, and L. Evans. 1979. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol. 81:275-300.
22. Hirase, T., J.M. Staddon, M. Saitou, Y. Ando-Akatsuka, M. Itoh, M. Furuse, K. Fujimoto, Sh. Tsukita, and L.L. Rubin. 1997. Occludin as a possible determinant of tight junction permeability in endothelial cells. J. Cell Sci. 110:1603-1613.
23. Irie, M., Y. Hata, M. Takeuchi, K. Ichtchenko, A. Toyoda, K. Hirao, Y. Takai, T.W. Rosahl, and T.C. Südhof. 1997. Binding of Neuroligins to PSD-95. Science. 277:1511-1515.
24. Itoh, M., A. Nagafuchi, S. Yonemura, T. Kitani-Yasuda, Sa. Tsukita, and Sh. Tsukita. 1993. The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J. Cell Biol. 121:491-502.
25. Itoh, M., A. Nagafuchi, S. Moroi, and Sh. Tsukita. 1997. Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to α catenin and actin filaments. J. Cell Biol. 138:181-192.
26. Jiang, J.X., and D.A. Goodenough. 1996. Heteromeric connexons in lens gap junction channels. Proc. Natl. Acad. Sci. USA. 93:1287-1291.
27. Kachar, B., and T.S. Reese. 1982. Evidence for the lipidic nature of tight junction strands. Nature. 296:464-466.
28. Kalderon, D., B.L. Roberts, W.D. Richardson, and A.E. Smith. 1984. A short amino acid sequence able to specify nuclear location. Cell. 39:499-509.
29. Keller, G., M. Kennedy, T. Papayannopoulou, and M.V. Wiles. 1993. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell. Biol. 13:473-486.
30. Keon, B.H., S. Schäfer, C. Kuhn, C. Grund, and W.W. Franke. 1996. Symplekin, a novel type of tight junction plaque protein. J. Cell Biol. 134:1003-1018.
31. Kim, S.K. 1995. Tight junctions, membrane-associated guanylate kinases and cell signaling. Curr. Opin. Cell Biol. 7:641-649.
32. + channels by interaction with a family of membraneassociated guanylate kinases. Nature. 378:85-88.
33. Kornau, H.-C., L.T. Schenker, M.B. Kennedy, and P.H. Seeburg. 1995. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science. 269:1737-1740.
34. Kumar, N.M., and N.B. Gilula. 1996. The gap junction communication channel. Cell. 84:381-388.
35. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
36. Laird, P.W., A. Zijderveld, K. Linders, M.A. Rudnicki, R. Jaenisch, and A. Berns. 1991. Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19:4293.
37. Li, E., T.H. Bestor, and R. Jaenisch. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell. 69:915-926.
38. 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.
39. Mortensen, R.M., D.A. Conner, S. Chao, A.A.T. Geisterfer-Lowrance, and J.G. Seidman. 1992. Production of homozygous mutant ES cells with a single targeting construct. Mol. Cell. Biol. 12:2391-2395.
40. Nelles, E., C. Butzler, D. Jung, A. Temme, H.D. Gabriel, U. Dahl, O. Traub, F. Stumpel, K. Jungermann, J. Zielasek, K.V. Toyka, R. Dermietzel, and K. Willecke. 1996. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. USA. 93:9565-9570.
41. Niethammer, M., E. Kim, and M. Sheng. 1996. Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J. Neurosci. 16:2157-2163.
42. Pinto da Silva, P., and B. Kachar. 1982. On tight-junction structure. Cell. 28: 441-450.
43. Reaume, A.C., P.A. de Sousa, S. Kulkarni, B.L. Langille, D. Zhu, T.C. Davies, S.C. Juneja, G.M. Kidder, and J. Rossant. 1995. Cardiac malformation in neonatal mice lacking connexin 43. Science. 267:1831-1834.
44. Rodriguez-Boulan. E., and W.J. Nelson. 1989. Morphogenesis of the polarized epithelial cell phenotype. Science. 245:718-725.
45. Rudnicki, M.A., T. Braun, S. Hinuma, and R. Jaenisch. 1992. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene myf-5 and results in apparently normal muscle development. Cell. 71:383-390.
46. Saitou. M., Y. Ando-Akatsuka, M. Itoh, M. Furuse, J. Inazawa, K. Fujimoto, and Sh. Tsukita. 1997. Mammalian occludin in epithelial cells: its expression and subcellular distribution. Eur. J. Cell Biol. 73:222-231.
47. 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.
48. Sauer, B., and N. Henderson. 1988. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc. Natl. Acad. Sci. USA. 85:5166-5170.
49. Schneeberger, E.E., and R.D. Lynch. 1992. Structure, function, and regulation of cellular tight junctions. Am. J. Physiol. 262:L647-L661.
50. Simon, A.M., D.A. Goodenough, E. Li, and D.L. Paul. 1997. Female infertility in mice lacking connexin 37. Nature. 385:525-529.
51. Staehelin, L.A. 1973. Further observations on the fine structure of freezecleaved tight junctions. J. Cell Sci. 13:763-786.
52. Staehelin, L. A. 1974. Structure and function of intercellular junctions. Int. Rev. Cytol. 39:191-283.
53. Sternberg. N., and D. Hamilton. 1981. Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites. J. Mol. Biol 150:467-486.
54. Stevenson, B.R., and D.A. Goodenough. 1984. Zonulae occludentes in junctional complex-enriched fractions from mouse liver: Preliminary morphological and biochemical characterization. J. Cell Biol. 98:1209-1221.
55. Stevenson, B.R., J.D. Siliciano, M.S. Mooseker, and D.A. Goodenough. 1986. Identification of ZO-1: A high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol. 103:755-766.
56. Stevenson, B.R., J.M. Anderson, and S. Bullivant. 1988. The epithelial tight junction: structure, function and preliminary biochemical characterization. Mol. Cell. Biochem. 83:129-145.
57. Thomas, K.R., and M.R. Capecchi. 1987. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell. 51:503-512.
58. Tokuyasu, K.T. 1980. Immunochemistry on ultrathin frozen sections. Histochem. J. 12:381-403.
59. Tsukiyama-Kohara, K., N. Iizuka, M. Kohara, and A. Nomoto. 1992. Internal ribosome entry site within hepatitis C virus RNA. J. Virol. 66:1476-1483.
60. Verkleiji, A.J. 1984. Lipidic intramembranous particles. Biochem. Biophys. Acta A. 779:43-63.
61. Watakabe, A., K. Tanaka, and Y. Shimura. 1993. The role of exon sequences in splice site section. Genes Dev. 7:407-418.
62. 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.
63. Woods, D.A., and P.J. Bryant. 1993. ZO-1, DlgA and PSD95/SAP90: homologous proteins in tight, septate and synaptic cell junctions. Mech. Dev. 44:85-89
64. Yagi, T., Y. Ikawa, K. Yoshida, Y. Shigetani, N. Takeda, I. Mabuchi, T. Yamamoto, and S. Aizawa. 1990. Homologous recombination at c-fyn locus of mouse embryonic stem cells with use of diphtheria toxin A-fragment gene in negative selection. Proc. Natl. Acad. Sci. USA. 87:9918-9922.
65. Zhong, Y., T. Saitoh, T. Minase, N. Sawada, K. Enomoto, and M. Mori. 1993 Monoclonal antibody 7H6 reacts with a novel tight junction-associated protein distinct from ZO-1, cingulin, and ZO-2. J. Cell Biol. 120:477-483.