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The ups and downs of life in an epithelium.

Krämer H - J. Cell Biol. (2000)

View Article: PubMed Central - PubMed

Affiliation: Center for Basic Neuroscience and Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9111, USA. kramer@utsw.swmed.edu

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This “outside” is faced by an epithelial cell's apical domain, which contains a set of membrane proteins and cytoskeletal elements that is distinct from the proteins found on the cell's basolateral domain (Yeaman et al. 1999)... In vertebrates, tight junctions located just apical to the adherens junctions seal the epithelium against diffusion between the cells (“gate function”) and also provide a barrier for lipids and proteins within the membrane (“fence function”) (Yeaman et al. 1999)... The structure of tight junctions is not well understood, though several constituents are known (Furuse et al. 1998; Izumi et al. 1998; Tsukita and Furuse 1999; Yeaman et al. 1999)... Unlike apically located tight junctions, insect septate junctions are found just basal to the adherens junction... Furthermore, the LET-413 gene encodes a LAP protein that is required for situating adherens junctions and apical markers in C. elegans (Legouis et al. 2000), which is in striking similarity to the scribble phenotype in Drosophila (Bilder and Perrimon 2000)... Therefore, LAP proteins provide an example of a familiar theme found in many specialized membrane domains, including epithelial junctions, synapses, and Drosophila rhabdomeres... The functional assembly of each of these membrane domains depends on PDZ domain–containing proteins clustering distinct transmembrane and cytoskeletal proteins and excluding others (for reviews see Fanning and Anderson 1999; Garner et al. 2000)... Both were especially enriched in the lateral domains just apical to the adherens junctions, a site which corresponds to that of tight junctions in vertebrates (Tanentzapf et al. 2000)... Although no morphological specialization in this region is distinguishable, it will be interesting to see whether some of the cell signaling, “gate” or “fence,” functions associated with vertebrate tight junctions (Yeaman et al. 1999) are also found in this domain of invertebrate epithelia... The bazooka gene was implicated in establishing cell polarity by its mutant phenotype and its similarity to the Par-3 gene, which is necessary for orienting mitotic spindles in early cell divisions of C. elegans embryos (Etemad-Moghadam et al. 1995; Kuchinke et al. 1998)... Because in C. elegans and vertebrates aPKCs bind to Bazooka homologs (Izumi et al. 1998; Tabuse et al. 1998), Knust and co-workers explored the role of the single DaPKC gene found in the Drosophila genome... These initial junctions contain the junctional proteins ARM, Cadherin, and Disc-lost (Bhat et al. 1999; Hunter and Wieschaus 2000; Lecuit and Wieschaus 2000), a composition very similar to the second junctional complex formed later during cellularization in a more conventional position, separating the apical and lateral membrane domains... To form the unusual set of basal junctions, cells require the Nullo protein; in its absence elements of basal junctions are scattered along the lateral domains (Hunter and Wieschaus 2000)... Whereas homologs of other junctional-complex components are found in C. elegans and vertebrates, Nullo is a novel protein, consistent with its role in a process unique to Drosophila... In this model the Sec6/8 multiprotein complex acts to restrict delivery of secretory vesicles to the basolateral membrane (Grindstaff et al. 1998; Yeaman et al. 1999).

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Establishment of polarity is tightly coupled to cellularization in Drosophila embryos. The temporal order of membrane insertion is translated into spatial differences by the isolation of different membrane domains from the main site of insertion (Hunter and Wieschaus 2000; Lecuit and Wieschaus 2000). (A) Shortly after the initial stage of cellularization, (B) a first set of junctional complexes, marked by ARM, is formed just below the embryonic cell surface. These complexes seal off the most basal membrane domain that forms the furrow canals. (C) As cellularization proceeds, the initial set (red) of junctions move basally together with the furrow canals. A second set of junctions (blue) is formed just below the cell surface and separates the apical and lateral domains. Membrane insertion basal to these junctions continues to extend the lateral domain. (D) The furrow canals will form the basal membrane domains and shortly thereafter, as the embryo initiates gastrulation, the unusual basal junctions disappear.
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Figure 2: Establishment of polarity is tightly coupled to cellularization in Drosophila embryos. The temporal order of membrane insertion is translated into spatial differences by the isolation of different membrane domains from the main site of insertion (Hunter and Wieschaus 2000; Lecuit and Wieschaus 2000). (A) Shortly after the initial stage of cellularization, (B) a first set of junctional complexes, marked by ARM, is formed just below the embryonic cell surface. These complexes seal off the most basal membrane domain that forms the furrow canals. (C) As cellularization proceeds, the initial set (red) of junctions move basally together with the furrow canals. A second set of junctions (blue) is formed just below the cell surface and separates the apical and lateral domains. Membrane insertion basal to these junctions continues to extend the lateral domain. (D) The furrow canals will form the basal membrane domains and shortly thereafter, as the embryo initiates gastrulation, the unusual basal junctions disappear.

Mentions: The extent to which the determinants of apical–basal polarity and the components of epithelial junctions are conserved suggests that the basic mechanism by which apical–basal polarity is established is also universal. It is therefore intriguing to study cellularization, the one hour during Drosophila embryogenesis in which 6,000 polarized cells are formed. Two recent papers from the Wieschaus laboratory closely examine this time window (Hunter and Wieschaus 2000; Lecuit and Wieschaus 2000) and present two striking findings. First, the emergence of polarity in the epithelium is tightly integrated with the process of cellularization. Second, the Drosophila embryo not only establishes cellular junctions in a synchronized manner, it actually does so twice in each cell (Fig. 2).


The ups and downs of life in an epithelium.

Krämer H - J. Cell Biol. (2000)

Establishment of polarity is tightly coupled to cellularization in Drosophila embryos. The temporal order of membrane insertion is translated into spatial differences by the isolation of different membrane domains from the main site of insertion (Hunter and Wieschaus 2000; Lecuit and Wieschaus 2000). (A) Shortly after the initial stage of cellularization, (B) a first set of junctional complexes, marked by ARM, is formed just below the embryonic cell surface. These complexes seal off the most basal membrane domain that forms the furrow canals. (C) As cellularization proceeds, the initial set (red) of junctions move basally together with the furrow canals. A second set of junctions (blue) is formed just below the cell surface and separates the apical and lateral domains. Membrane insertion basal to these junctions continues to extend the lateral domain. (D) The furrow canals will form the basal membrane domains and shortly thereafter, as the embryo initiates gastrulation, the unusual basal junctions disappear.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2169448&req=5

Figure 2: Establishment of polarity is tightly coupled to cellularization in Drosophila embryos. The temporal order of membrane insertion is translated into spatial differences by the isolation of different membrane domains from the main site of insertion (Hunter and Wieschaus 2000; Lecuit and Wieschaus 2000). (A) Shortly after the initial stage of cellularization, (B) a first set of junctional complexes, marked by ARM, is formed just below the embryonic cell surface. These complexes seal off the most basal membrane domain that forms the furrow canals. (C) As cellularization proceeds, the initial set (red) of junctions move basally together with the furrow canals. A second set of junctions (blue) is formed just below the cell surface and separates the apical and lateral domains. Membrane insertion basal to these junctions continues to extend the lateral domain. (D) The furrow canals will form the basal membrane domains and shortly thereafter, as the embryo initiates gastrulation, the unusual basal junctions disappear.
Mentions: The extent to which the determinants of apical–basal polarity and the components of epithelial junctions are conserved suggests that the basic mechanism by which apical–basal polarity is established is also universal. It is therefore intriguing to study cellularization, the one hour during Drosophila embryogenesis in which 6,000 polarized cells are formed. Two recent papers from the Wieschaus laboratory closely examine this time window (Hunter and Wieschaus 2000; Lecuit and Wieschaus 2000) and present two striking findings. First, the emergence of polarity in the epithelium is tightly integrated with the process of cellularization. Second, the Drosophila embryo not only establishes cellular junctions in a synchronized manner, it actually does so twice in each cell (Fig. 2).

View Article: PubMed Central - PubMed

Affiliation: Center for Basic Neuroscience and Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9111, USA. kramer@utsw.swmed.edu

AUTOMATICALLY GENERATED EXCERPT
Please rate it.

This “outside” is faced by an epithelial cell's apical domain, which contains a set of membrane proteins and cytoskeletal elements that is distinct from the proteins found on the cell's basolateral domain (Yeaman et al. 1999)... In vertebrates, tight junctions located just apical to the adherens junctions seal the epithelium against diffusion between the cells (“gate function”) and also provide a barrier for lipids and proteins within the membrane (“fence function”) (Yeaman et al. 1999)... The structure of tight junctions is not well understood, though several constituents are known (Furuse et al. 1998; Izumi et al. 1998; Tsukita and Furuse 1999; Yeaman et al. 1999)... Unlike apically located tight junctions, insect septate junctions are found just basal to the adherens junction... Furthermore, the LET-413 gene encodes a LAP protein that is required for situating adherens junctions and apical markers in C. elegans (Legouis et al. 2000), which is in striking similarity to the scribble phenotype in Drosophila (Bilder and Perrimon 2000)... Therefore, LAP proteins provide an example of a familiar theme found in many specialized membrane domains, including epithelial junctions, synapses, and Drosophila rhabdomeres... The functional assembly of each of these membrane domains depends on PDZ domain–containing proteins clustering distinct transmembrane and cytoskeletal proteins and excluding others (for reviews see Fanning and Anderson 1999; Garner et al. 2000)... Both were especially enriched in the lateral domains just apical to the adherens junctions, a site which corresponds to that of tight junctions in vertebrates (Tanentzapf et al. 2000)... Although no morphological specialization in this region is distinguishable, it will be interesting to see whether some of the cell signaling, “gate” or “fence,” functions associated with vertebrate tight junctions (Yeaman et al. 1999) are also found in this domain of invertebrate epithelia... The bazooka gene was implicated in establishing cell polarity by its mutant phenotype and its similarity to the Par-3 gene, which is necessary for orienting mitotic spindles in early cell divisions of C. elegans embryos (Etemad-Moghadam et al. 1995; Kuchinke et al. 1998)... Because in C. elegans and vertebrates aPKCs bind to Bazooka homologs (Izumi et al. 1998; Tabuse et al. 1998), Knust and co-workers explored the role of the single DaPKC gene found in the Drosophila genome... These initial junctions contain the junctional proteins ARM, Cadherin, and Disc-lost (Bhat et al. 1999; Hunter and Wieschaus 2000; Lecuit and Wieschaus 2000), a composition very similar to the second junctional complex formed later during cellularization in a more conventional position, separating the apical and lateral membrane domains... To form the unusual set of basal junctions, cells require the Nullo protein; in its absence elements of basal junctions are scattered along the lateral domains (Hunter and Wieschaus 2000)... Whereas homologs of other junctional-complex components are found in C. elegans and vertebrates, Nullo is a novel protein, consistent with its role in a process unique to Drosophila... In this model the Sec6/8 multiprotein complex acts to restrict delivery of secretory vesicles to the basolateral membrane (Grindstaff et al. 1998; Yeaman et al. 1999).

Show MeSH