Tight junction assembly during mouse blastocyst formation is regulated by late expression of ZO-1 α+ isoform

Development

Volumn 124, Issue 10, 1997, Pages 2027-2037

  Sheth, Bhavwanti ^a   Fesenko, Ira ^a,c   Collin, Jane E ^a,d   Moran, Breda ^a   Wild, Arthur E ^a   Anderson, James M ^b   Fleming, Tom P ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Blastocyst; Epithelial differentiation; Mouse embryo; Occludin; Tight junction; Trophectoderm; ZO 1

Indexed keywords

BREFELDIN A; CYTOPLASM PROTEIN; ISOPROTEIN; MESSENGER RNA; SULFUR 35;

ALPHA CHAIN; ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL CONTACT; DEVELOPMENTAL GENETICS; ECTODERM; EMBRYO; GOLGI COMPLEX; IMMUNOHISTOCHEMISTRY; INTRACELLULAR TRANSPORT; MORULA; MOUSE; NONHUMAN; OOCYTE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; TIGHT JUNCTION;

ALTERNATIVE SPLICING; ANIMALS; ANTIBODY SPECIFICITY; BLASTOCYST; BREFELDIN A; CELL COMMUNICATION; CELL MEMBRANE; CYCLOPENTANES; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMBRANE PROTEINS; MICE; MORULA; OOCYTES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITORS; RNA, MESSENGER; TIGHT JUNCTIONS;

EID: 0030962073     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Anderson, E. and Albertini, D. F. (1976). Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J. Cell Biol. 71, 680-686.
2. Anderson, J.M. (1996). Cell signalling: MAGUK magic. Current Biol. 6, 382-384.
3. Anderson, J. M. and Van Itallie, C. M. (1995). Tight junctions and the molecular basis for regulation of paracellular permeability. Am. J. Physiol. 269, G467-G475.
4. Anderson, J. M., Fanning, A. S., Lapierre, L. and Van Itallie, C. M. (1995). Zonula occludens (ZO)-1 and ZO-2: membrane-associated guanylate kinase homologues (MAGuKs) of the tight junction. Biochem. Soc. Trans. 23, 470-475.
5. 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.
6. Balda, M. S., and Anderson, J. M. (1993). Two classes of tight junctions are revealed by ZO-1 isoforms. Am. J. Phvsiol. 264, C918-C924.
7. Balda, M. S., Gonzales-Mariscal, L., Matter, K., Contreras, R. G., Cerejido, M. and Anderson, J. M. (1993). Assembly of the tight junctions: the role of diacylglycerol. J. Cell Biol. 123, 293-302.
8. 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.
9. 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
10. Cho, K. O., Hunt, C. and Kennedy, M. (1992). The rat brain post-synaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929-942.
11. Citi, S. (1993). The molecular organisation of tight junctions. J. Cell Biol. 121, 485-489.
12. 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.
13. Citi, S., Sabanay, H., Kendrick-Jones, J. and Geiger, B. (1989). Cingulin: characterisation and localisation. J. Cell Sci. 93, 107-122.
14. Claude, P. (1978). Morphological factors influencing transepithelial permeability: a model for the resistance of the zonula occludentes. J. Membrane Biol. 39, 219-232.
15. Collins, J. E. and Fleming, T. P. (1995a). Epithelial differentiation in the mouse preimplantation embryo: making adhesive cell contacts for the first time. TIBS 20, 307-312.
16. Collins, J. E. and Fleming, T. P. (1995b). Specific mRNA detection in single lineage-marked blastomeres from preimplantation embryos. TIG 11, 5-7.
17. 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.
18. Eppig, J. J. (1991). Intercommunication between mammalian oocytes and companion somatic cells. BioEssays 13, 569-574.
19. 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.
20. Flach, G., Johnson, M. H., Braude, P. R., Taylor, R. and Bolton, V. N. (1982). The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J. 1, 681-686.
21. Fleming, T. P. (1987). A quantitative analysis of cell allocation to trophectoderm and inner cell mass in the mouse blastocyst. Dev. Biol. 119, 520-531.
22. Fleming, T. P. (1992). Trophectoderm biogenesis in the preimplantation mouse embryo. In Epithelial Organisation and Development (ed. T. P. Fleming), pp111-136, London: Chapman and Hall.
23. Fleming, T. P. and Goodall, H. (1986). Endocytic traffic in trophectoderm and polarised blastomeres of the mouse preimplantation embryo. The Anatomical Record 216, 490-503.
24. 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.
25. Fleming, T. P. and Johnson, M. H. (1988). From egg to epithelium. Ann. Rev. Cell Biol. 4, 459-485.
26. 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.
27. 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.
28. Fleming, T. P., Garrod, D.R. and Elsmore, A. J. (1991). Desmosome biogenesis in the mouse preimplantation embryo. Development 112, 527-539.
29. Fleming, T. P., Hay, M., Javed, Q. and Citi, S. (1993a). Localisation of tight junction protein cingulin is temporally and spatially regulated during early mouse development. Development 117, 1135-1144.
30. Fleming, T. P., Javed, Q., Collins. J. E. and Hay, M. (1993b). Biogenesis of structural intercellular junctions during cleavage in the mouse embryo. J. Cell Sci. Suppl. 17, 119-125.
31. 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.
32. Furuse, Itoh, M., 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.
33. Giebelhaus, D. H., Heikkila, J. J. and Schultz, G. A. (1983). Changes in the quantity of histone and actin mRNA during the development of preimplantation embryos. Dev. Biol. 98, 148-154.
34. Gumbiner, B. (1987). Structure, biochemistry and assembly of epithelial tight junctions. Am. J. Physiol. 253, C749-C758.
35. Gumbiner, B., Lowekopf, T. and Apatira, D. (1991). Identification of a 160KDa polypeptidethat binds to the tight junction protein ZO-1. Proc. Natl. Acad. Sci. USA 88, 3460-3464.
36. Hoskins, R., Hajnal, A. F., Harp, S. A. and Kim, S. (1996). The C. elegans vulval induction gene lin-2 encodes a member of the MAGUK family of cell junction proteins. Development 122, 97-111.
37. 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.
38. Itoh, M., Nagafuchi, A., Yonemura, S., Kitani-Yasuda, T., Tsukita, S. and Tsukita, S. (1993). The 220-kD protein colocalising 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.
39. 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.
40. Jesaitis, L. A. and Goodenough, D. A. (1994). Molecular characterisation and tissue distribution of ZO-1, a tight junction protein homologous to ZO-1 and the drosophila discs-large tumour suppressor protein. J. Cell Biol. 124, 949-961.
41. Johnson, M. H. and Ziomek, C. A. (1981). The foundation of two distinct cell lineages within the mouse morula. Cell 24, 71-80.
42. Kidder, G. M. and McLachlin, J. R. (1985). Timing of transcription and protein synthesis underlying morphogenesis in preimplantation mouse embryos. Dev. Biol. 112, 265-275.
43. 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.
44. Kurihara, H., Anderson, J. M. and Farquhar, M. G. (1995). Increased Tyr phosphorylation of ZO-1 during modification of tight junctions between glomerular toot processes. Am. J. Physiol. 268, F514-524.
45. 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.
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. Dev. 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. Rajasekaran, A. K., Hojo, M., Huima, T. and Rodriguez-Boulan, E. (1996). Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J. Cell Biol. 132, 451-463.
49. Rappolee, D. A., Brenner, C. A., Schultz, R., Mark, D. and Werb, Z. (1988). Developmental expression of PDGF. TGF-α and TGF-β genes in preimplantation mouse embryos. Science 241, 1823-1825.
50. Ruff, P., Speicher, D. W. and Husain-Chishti, A. (1991). A molecular identification of a major palmotylated erythrocyte membrane protein containing the src homology 3 motif. Proc. Natl. Acad. Sci. USA 88, 6595-6599.
51. Sellens, M. H., Stein, S. and Sherman, M. I. (1981). Protein and free amino acid content in preimplantation mouse embryos and in blastocysts under various culture conditions. J. Reprod. Fert. 61, 307-315.
52. Staddon, J. M., Herrenknecht, K., Smales, C. and Rubin, L. L. (1995) Evidence that tyrosine phosphorylation may increase tight junction permeability. J. Cell Sci. 108, 609-619.
53. 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.
54. Takeda, H., Nagafuchi, A., Yonemura, S., Tsukita, S., Behrens, J., Birchmeier, W. and Tsukita, S. (1995). V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and β-catenin is not required for the shift. J. Cell Biol. 131, 1839-1847.
55. Telford, N. A., Watson, A. J. and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev. 26, 90-100.
56. Van Itallie, C. M., Balda, M. S. and Anderson, J. M. (1995). Epidermal growth factor induces tyrosine phosphorylation and reorganisation of the tight junction protein ZO-1 in A431 cells. J. Cell Sci. 108, 1735-1742.
57. Watson, A. J., Pape, C., Emanuel, J. R., Levenson, R. and Kidder, G. M. (1990). Expression of Na,K-ATPase α- and β-subunit genes during preimplantation development of the mouse. Devl. Gen. 11, 41-48.
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., Heintzelman, M., Jameson, B., and Anderson, J. M. (1992) Localisation and differential expression of two isoforms of the tight junction protein ZO-1. Am. J. Physiol. 262, C1119-C1124.
60. 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 septata junctions. Proc. Natl. Acad. Sci. USA 90, 7834-7838.
61. Woods, D. and Bryant, P. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localised at septate junctions. Cell 66, 451-464
62. 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.
63. 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.
64. Ziomek, C. A. and Johnson, M. H. (1980). Cell surface interactions induce polarisation of mouse 8-cell blastomeres at compaction. Cell 21, 935-942.