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Tight junction biogenesis in the early Xenopus embryo

Tight junction biogenesis in the early Xenopus embryo
Tight junction biogenesis in the early Xenopus embryo
Tight junctions (TJs) perform a critical role in the transport functions and morphogenetic activity of the primary epithelium formed during Xenopus cleavage. Biogenesis of these junctions was studied by immunolocalization of TJ-associated proteins (cingulin, ZO-1 and occludin) and by an in vivo biotin diffusion assay. Using fertilized eggs synchronized during the first division cycle, we found that membrane assembly of the TJ initiated at the animal pole towards the end of zygote cytokinesis and involved sequential incorporation of components in the order cingulin, ZO-1 and occludin. The three constituents appeared to be recruited from maternal stores and were targeted to the nascent TJ site by different pathways. TJ protein assembly was focused precisely to the border between the oolemma-derived apical membrane and newly-inserted basolateral membrane generated during cytokinesis and culminated in the formation of functional TJs in the two-cell embryo, which maintained a diffusion barrier. New membrane formation and the generation of cell surface polarity therefore precede initiation of TJ formation. Moreover, assembly of TJ marker protein precisely at the apical-basolateral membrane boundary was preserved in the complete absence of intercellular contacts and adhesion. Thus, the mechanism of TJ biogenesis in the Xenopus early embryo relies on intrinsic cues of a cell autonomous mechanism. These data reveal a distinction between Xenopus and mammalian early embryos in the origin and mechanisms of epithelial cell polarization and TJ formation during cleavage of the egg.
tight junctions, xenopus, cleavage, occludin, ZO-1, cingulin, epithelial cell polarity, cell–cell adhesion
0925-4773
51-65
Fesenko, I.
faa964d0-ed40-47c9-bc9c-930b8010aab7
Kurth, T.
2c0f008d-e38a-44bc-9351-aed3fe2a36d5
Sheth, B.
2ca6ed58-a992-47b7-b3a5-3c5df82aada7
Fleming, T.P.
2abf761a-e5a1-4fa7-a2c8-12e32d5d4c03
Citi, S.
680742ee-4d59-4f77-90e9-2e47439c11f4
Hausen, P.
5b29b870-342c-4467-ae39-b1f9d28596a9
Fesenko, I.
faa964d0-ed40-47c9-bc9c-930b8010aab7
Kurth, T.
2c0f008d-e38a-44bc-9351-aed3fe2a36d5
Sheth, B.
2ca6ed58-a992-47b7-b3a5-3c5df82aada7
Fleming, T.P.
2abf761a-e5a1-4fa7-a2c8-12e32d5d4c03
Citi, S.
680742ee-4d59-4f77-90e9-2e47439c11f4
Hausen, P.
5b29b870-342c-4467-ae39-b1f9d28596a9

Fesenko, I., Kurth, T., Sheth, B., Fleming, T.P., Citi, S. and Hausen, P. (2000) Tight junction biogenesis in the early Xenopus embryo. Mechanisms of Development, 96 (1), 51-65. (doi:10.1016/S0925-4773(00)00368-3).

Record type: Article

Abstract

Tight junctions (TJs) perform a critical role in the transport functions and morphogenetic activity of the primary epithelium formed during Xenopus cleavage. Biogenesis of these junctions was studied by immunolocalization of TJ-associated proteins (cingulin, ZO-1 and occludin) and by an in vivo biotin diffusion assay. Using fertilized eggs synchronized during the first division cycle, we found that membrane assembly of the TJ initiated at the animal pole towards the end of zygote cytokinesis and involved sequential incorporation of components in the order cingulin, ZO-1 and occludin. The three constituents appeared to be recruited from maternal stores and were targeted to the nascent TJ site by different pathways. TJ protein assembly was focused precisely to the border between the oolemma-derived apical membrane and newly-inserted basolateral membrane generated during cytokinesis and culminated in the formation of functional TJs in the two-cell embryo, which maintained a diffusion barrier. New membrane formation and the generation of cell surface polarity therefore precede initiation of TJ formation. Moreover, assembly of TJ marker protein precisely at the apical-basolateral membrane boundary was preserved in the complete absence of intercellular contacts and adhesion. Thus, the mechanism of TJ biogenesis in the Xenopus early embryo relies on intrinsic cues of a cell autonomous mechanism. These data reveal a distinction between Xenopus and mammalian early embryos in the origin and mechanisms of epithelial cell polarization and TJ formation during cleavage of the egg.

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More information

Published date: August 2000
Keywords: tight junctions, xenopus, cleavage, occludin, ZO-1, cingulin, epithelial cell polarity, cell–cell adhesion

Identifiers

Local EPrints ID: 56649
URI: https://eprints.soton.ac.uk/id/eprint/56649
ISSN: 0925-4773
PURE UUID: 66280e37-5a8f-4fc0-96bf-9084837d2325

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Date deposited: 21 Aug 2008
Last modified: 13 Mar 2019 20:34

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Contributors

Author: I. Fesenko
Author: T. Kurth
Author: B. Sheth
Author: T.P. Fleming
Author: S. Citi
Author: P. Hausen

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