Post-translational control of occludin membrane assembly in mouse trophectoderm: A mechanism to regulate timing of tight junction biogenesis and blastocyst formation

Development

Volumn 127, Issue 4, 2000, Pages 831-840

  Sheth, Bhavwanti ^a   Moran, Breda ^a   Anderson, James M ^b   Fleming, Tom P ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Blastocyst; Epithelial differentiation; Mouse embryo; Occludin; Tight junction; Trophectoderm

Indexed keywords

BREFELDIN A; MEMBRANE PROTEIN; MESSENGER RNA; OCCLUDIN; TRITON X 100; UVOMORULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL ADHESION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; FEMALE; IMMUNOBLOTTING; MEMBRANE FORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIGHT JUNCTION;

ANIMALS; BASE SEQUENCE; BLASTOCYST; DNA PRIMERS; ECTODERM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMBRANE PROTEINS; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; TIGHT JUNCTIONS; TROPHOBLASTS;

ANIMALIA; MAMMALIA;

EID: 0034012846     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Anderson, J. M. (1996). Cell signalling: MAGUK magic. Current Biol. 6, 382-384.
2. Ando-Akatsuka, Y., Saitou, M., Hirase, T. Kishi, M., Sakakibara, A., Itoh, H., Yonemura, S., Furuse, M. and Tsukita, S. (1996). Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. J. Cell Biol. 133, 43-47.
3. Bachvarova, R., Cohen, E. M., De Leon, V., Tokunaga, K., Sakiyama, S. and Paynton, B. V. (1989). Amounts and modulation of actin mRNAs in mouse oocytes and embryos. Development 106, 561-565.
4. Balda, M. S. and Anderson, J. M. (1993). Two classes of tight junctions are revealed by ZO-1 isoforms. Am. J. Physiol. 264, C918-C924.
5. Balda, M. S., Whitney, J. A., Flores, C., Gonzalez, M., Cerejido, M. and Matter, K. (1996). Functional dissociation of paracellular permeability and TER and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant junction membrane protein. J. Cell Biol. 134, 1031-1049.
6. Beatch, M., Jesaitis, L. A., Gallin, W. J., Goodenough, D. A. and Stevenson, B. R. (1996). The tight junction protein ZO-2 contains three PDZ (PSD-95/Discs-Large/ZO-1) domains and an alternatively spliced region. J. Biol. Chem. 271, 25723-25726.
7. Chisolm, J. C., Johnson, M. H., Warren, P. D., Fleming, T. P. and Pickering, S. J. (1985). Developmental variability within and between mouse expanding blastocysts and their ICMs. J. Embryol. Exp. Morph. 86, 311-336
8. Citi, S., Sabanay, H., Jakes, R., Geiger, B. and Kendrick-Jones, J. (1988). Cingulin, a new peripheral componenet of tight junctions. Nature 333, 272-276.
9. Citi, S., Sabanay, H., Kendrick-Jones, J. and Geiger, B. (1989). Cingulin: characterisation and localisation. J. Cell Sci. 93, 107-122.
10. Citi, S. and Cordenonsi, M. (1998). Tight junction proteins. Biochim. Biophys. Acta 1448, 1-11.
11. Collins, J. K. and Fleming, T. P. (1995). Specific mRNA detection in single lineage-marked blastomeres from preimplantation embryos. Trends in Genet. 11, 5-7.
12. Collins, J. E., Lorimer, J. E., Garrod, D. R., Pidsley, S. C., Buxton, R. S. and Fleming, T. P. (1995). Regulation of desmocollin transcription in mouse preimplantation embryos. Development 121, 743-752.
13. Cordenonsi, M., Mazzon, E., de Rigo, L., Baraldo, S., Meggio, F. and Citi, S. (1997). Occludin dephosphorylation in early development of Xenopus laevis. J. Cell Sci. 110, 3131-3139.
14. Ducibella, T and Anderson, E. (1975). Cell shape and membrane changes in the eight-cell mouse embryo: prerquisites for morphogenesis of the blastocyst. Dev. Biol. 47, 45-58
15. Fanning, A. S., Jameson, B. J., Jesaitis, L. A. and Anderson, J. M. (1998). The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 273, 29745-29753.
16. Fallon, M. B., Brecher, A. R., Balda, M. S., Matter, K. and Anderson, J. M. (1995). Altered hepatic localisation and expression of occludin after common bile duct ligation. Am. J. Physiol. 269, C1057-C1062.
17. Fleming, T. P. and Hay, M. J. (1991). Tissue specific control of expression of the tight junction polypeptide ZO-1 in the mouse early embryo. Development 113, 295-304.
18. Fleming, T. P. and Pickering, S. J. (1985). Maturation and polarisation of the endocytotic system in outside blastomeres during mouse preimplantation development. J. Embryol. Exp Morph. 89, 175-208.
19. Fleming, T. P., McConnell J., Johnson, M. H. and Stevenson, B. R. (1989). Development of tight junctions de novo in the mouse early embryo: control of assembly of the tight junction-specific protein, ZO-1. J. Cell Biol. 108, 1407-1418.
20. Fleming, T. P., Garrod, D. R. and Elsmore, A. J. (1991). Desmosome biogenesis in the mouse preimplantation embryo. Development 112, 527-539.
21. Fleming, T. P., Hay, M., Javed, Q. and Citi, S. (1993). Localisation of tight junction protein cingulin is temporally and spatially regulated during early mouse development. Development 117, 1135-1144.
22. Fleming, T. P., Butler, E., Collins, J., Sheth, B. and Wild, A. E. (1998). Cell polarity and mouse early development. Adv. Molec. Cell Biol. 26, 67-94.
23. Furuse, M., Hirase, T., Itoh, M., Nagafuchi, A., Yonemura, S., Tsukita, S. and Tsukita, S. (1993) Occludin: A novel integral membrane protein localising at tight junctions. J. Cell Biol. 123, 1777-1788.
24. Furuse, M., Itoh, M., Hirase, T., Nagafuchi, A., Yonemura, S., Tsukita, S. and Tsukita, S. (1994). Direct association of occludin with ZO-1 and its possible involvement in the localisation of occludin at tight junctions. J. Cell Biol. 127, 1617-1626.
25. Furuse, M., Fujimoto, K., Sato, N., Hirase, T. and Tsukita, S. (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.
26. Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K. and Tsukita, S. (1998). Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141, 1539-1550.
27. Gumbiner, B., Lowekopf, T. and Apatira, D. (1991). Identification of a 160KDa polypeptide that binds to the tight junction protein ZO-1. Proc. Natl. Acad. Sci. USA 88, 3460-3464.
28. Haskins, J., Gu, L., Wittchen, E. S., Hibbard, J. and Stevenson, B. R. (1998). ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J. Cell Biol. 141, 199-208.
29. Hirase, T., Staddon, J. M., Saitou, M., Ando-Akatsuka, Y., Itoh, M., Furuse, M., Fujimoto, K., Tsukita, S. and Rubin, L. L. (1997). Occludin as a possible determinant of tight junction permeability in endothelial cells. J. Cell. Sci. 110, 1603-1613.
30. Houghton, F. D., Sheth, B., Moran, B., Leese, H. J. and Fleming, T. P. (1996). Expression and activity of hexokinase in the early mouse embryo. Molec. Hum. Reprod. 2, 793-798.
31. Hyafil, F., Morello, D., Babinet, C. and Jacob, F. (1980) A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos. Cell 21, 927-934.
32. Itoh, M., Nagafuchi, A., Yonemura, S., Kitani-Yasuda, T., Tsukita, S. and Tsukita, S. (1993). The 220-kD protein colocalising wilh 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.
33. Itoh, M., Morita, K. and Tsukita, S. (1999). Characterization of ZO-2 as a MAGuK family member associated with light as well as adherens junctions with a binding affinity to occludin and α-catenin. J. Biol. Chem. 274, 5981-5986.
34. Javed, Q., Fleming, T. P., Hay, M. and Citi, S. (1993). Tight junction protein cingulin is expressed by maternal and embryonic genomes during early mouse development. Development 117, 1145-1151.
35. Jesaitis, L. A. and Goodenough, D. A. (1994). Molecular characterisation and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the drosophila discs-large tumour suppressor protein. J. Cell Biol. 124, 949-961.
36. Johnson, M. H. and Ziomek, C. A. (1983). Cell interactions influence the fate of mouse blastomeres undergoing the transition from the 16-to the 32-cell stage. Dev. Biol. 95, 211-218.
37. Johnson, M. H., Maro, B. and Takeichi, M. (1986) The role of cell adhesion in the synchronisation and orientation of polarization in 8-cell mouse blastomeres. J. Embryol. Exp. Morph. 93, 239-255.
38. Keon, B. H., Schafer, S., Kuhn, C., Grund, C. and Franke, W. W. (1996). Symplekin, a novel type of tight junction plaque protein. J. Cell Biol. 134, 1003-1018.
39. Klausner, R. D., Donaldson, J. G. and Lippincott-Schwartz, J. (1992). Brefeldin A: Insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116, 1071-1080.
40. Larue, L., Ohsugi, M., Hirchenhain, J. and Kemler, R. (1994). E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc. Natl. Acad. Sci. USA 91, 8263-8267.
41. Matter, K. and Balda, M. S. (1999). Occludin and the functions of tight junction. Int. Rev. Cytol. 186, 117-146.
42. McCarthy, K. M., Skare, I. B., Stankewich, M. C., Furuse, M., Tsukita, S., Rogers, R. A., Lynch, R. D. and Schneeberger, E. E. (1996). Occludin is a functional component of the tight junction. J. Cell Sci. 109, 2287-2298.
43. Mitic, L. L. and Anderson, J. M. (1998). Molecular architechture of tight junctions. Ann. Rev. Physiol. 60, 121-142.
44. Morita, K., Furuse, M., Fujimoto, K. and Tsukita, S. (1999). Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc. Natl. Acad. Sci. USA 96, 511-516.
45. Muresan, Z., Paul, D. L. and Goodenough, D. A. (1998). Occludin-2, an isoform of the tight junction protein occludin. Mol. Biol. Cell. S9, 83a.
46. Ohsugi, M., Hwang, S., Butz, S., Knowles, B. B., Solter, D. and Kemler, R. (1996). Expression and cell membrane localisation of catenins during mouse preimplantation development. Devl. Dynamics 206, 391-402.
47. Paynton, B. V., Rempel, R. and Bachvarova, R. (1988). Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and embryonic development in the mouse. Dev. Biol. 129, 304-314.
48. Pratt, H. P. M. (1985). Membrane organization in the preimplantation embryo. J. Embryol. Exp. Morph. 90, 101-121.
49. Riethmacher, D., Brinkmann, V. and Birchmeier, C. (1995). A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc. Natl. Acad Sci. USA 92, 855-859.
50. Saitou, M., Ando-Akatsuka, Y., Itoh, M., Furuse, M., Inazawa, J., Figimoto, K. and Tsukita, S. (1997). Mammalian occludin in epithelial cells: its expression and subcellular distribution. Eur. J. Cell Biol. 73, 222-231.
51. Saitou, M., Fujimoto, K., Doi, Y., Itoh, M., Fijimoto, T., Furuse, M., Takano, H., Noda, T. and Tsukita, S. (1998) Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J. Cell Biol. 141, 397-408.
52. Sakakibara, A., Furuse, M., Saitou, M., Ando-Akatsuka, Y. and Tsukita, S. (1997). Possible involvement of phosphorylation of occludin in tight junction formation. J. Cell Biol 137, 1393-1401.
53. Sheth, B., Fesenko, I., Collins, J. E., Moran, B., Wild, A. E., Anderson, J. M. and Fleming, T. P. (1997). Tight junction assembly during mouse blastocyst formation is regulated by late expression of ZO-1α+ isoform. Development 124, 2027-2037.
54. Shirayoshi, Y., Okada, T. S. and Takeichi, M. (1983). The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. Cell 35, 631-638.
55. Stevenson, B. R., Siliciano, J. D., Mooseker, M. S. and Goodenough, D. A. (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. Van Itallie, C. M. and Anderson, J. M. (1997). Occludin confers adhesiveness when expressed in fibroblasts. J. Cell Sci. 110, 1113-1121.
57. Vestweber, D., Gossler, A., Boller, K. and Kemler, R. (1987). Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev. Biol. 124, 451-456.
58. Weber, E., Berta, G., Tousson, A., St. John, P., Gree, M. W., Gopalokrishnam, U., Jilling, E. J., Sorscher, T. S., Abrahamson, D. R. and Kirk, K. L. (1994). Expression and polarisation of a Rab3 isoform in epithelial cells. J. Cell Biol. 125, 583-594.
59. Willott, E., Balda, M. S., Fanning, A. S., Jameson, B., Van Itallie, C. and Anderson, J. M. (1993) The tight junction protein ZO-1 is homologous to the Drosophila discs-large tumour suppressor protein of septate junctions. Proc. Natl. Acad. Sci. USA 90, 7834-7838.
60. Wittchen, E. S. and Stevenson, B. R. (1998) Novel binding interactions among tight junction-associated proteins. Mol. Biol. Cell. 9 SS 475.
61. Wong, V. (1997). Phosphorylation of occludin correlates with occludin localization and function at the tight junction. Am. J. Physiol. 42, C1859-C1867.
62. Wong, V. and Gumbiner, B. M. (1997). A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J. Cell Biol. 136, 399-409.
63. Yamamoto, T., Harada, N., Kano, K., Taya, S., Canaani, E., Matsuura, Y., Mizoguchi, A., Ide, C. and Kaibuchi, K. (1997). The Ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells. J. Cell Biol. 139, 785-795.
64. Zahraoui, A., Joberty, G., Arpin, M., Fontaine, J. J., Hellio, R., Tavitian, A. and Louvard, D. (1994). A small rab GTPase is distributed in cytoplasmic vesicles in non-polarised cells but colocalised with the tight junction marker ZO-1 in polarised epithelial cells. J. Cell Biol. 124, 101-115.
65. Zhong, Y., Saitoh, T., Minase, T., Sawada, N., Emomoto, K. and Mori, M. (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.