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The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis.

Pettitt J, Cox EA, Broadbent ID, Flett A, Hardin J - J. Cell Biol. (2003)

Bottom Line: We have examined the role of the single Caenorhabditis elegans p120ctn homologue JAC-1 (juxtamembrane domain [JMD]-associated catenin) during epidermal morphogenesis.Surprisingly, depleting JAC-1 expression using RNA interference (RNAi) does not result in any obvious defects in embryonic or postembryonic development.However, jac-1(RNAi) does increase the severity and penetrance of morphogenetic defects caused by a hypomorphic mutation in the hmp-1/alpha-catenin gene.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cell Biology, University of Aberdeen Institute of Medical Sciences, Aberdeen AB25 2ZD, Scotland, UK. j.pettitt@abdn.ac.uk

ABSTRACT
The cadherin-catenin complex is essential for tissue morphogenesis during animal development. In cultured mammalian cells, p120 catenin (p120ctn) is an important regulator of cadherin-catenin complex function. However, information on the role of p120ctn family members in cadherin-dependent events in vivo is limited. We have examined the role of the single Caenorhabditis elegans p120ctn homologue JAC-1 (juxtamembrane domain [JMD]-associated catenin) during epidermal morphogenesis. Similar to other p120ctn family members, JAC-1 binds the JMD of the classical cadherin HMR-1, and GFP-tagged JAC-1 localizes to adherens junctions in an HMR-1-dependent manner. Surprisingly, depleting JAC-1 expression using RNA interference (RNAi) does not result in any obvious defects in embryonic or postembryonic development. However, jac-1(RNAi) does increase the severity and penetrance of morphogenetic defects caused by a hypomorphic mutation in the hmp-1/alpha-catenin gene. In these hmp-1 mutants, jac-1 depletion causes failure of the embryo to elongate into a worm-like shape, a process that involves contraction of the epidermis. Associated with failed elongation is the detachment of actin bundles from epidermal adherens junctions and failure to maintain cadherin in adherens junctions. These results suggest that JAC-1 acts as a positive modulator of cadherin function in C. elegans.

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jac-1 is expressed in the early epidermis and JAC-1–GFP localizes to epidermal cell borders during morphogenesis. (A) Representative images from in situ hybridization with a control jac-1 sense probe (left) and jac-1 antisense probe (right). (B) Confocal images of JAC-1–GFP expression. (a) Dorsal view showing JAC-1–GFP localization during dorsal intercalation (two interdigitating cells are marked with asterisks). (b and c) Lateral views showing JAC-1–GFP localization during elongation. (d–f) Time course of an embryo undergoing ventral enclosure. Bar, 10 μm.
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fig2: jac-1 is expressed in the early epidermis and JAC-1–GFP localizes to epidermal cell borders during morphogenesis. (A) Representative images from in situ hybridization with a control jac-1 sense probe (left) and jac-1 antisense probe (right). (B) Confocal images of JAC-1–GFP expression. (a) Dorsal view showing JAC-1–GFP localization during dorsal intercalation (two interdigitating cells are marked with asterisks). (b and c) Lateral views showing JAC-1–GFP localization during elongation. (d–f) Time course of an embryo undergoing ventral enclosure. Bar, 10 μm.

Mentions: To gain insight into the physiological function of JAC-1, its expression and subcellular localization were examined. In situ hybridization demonstrates that jac-1 mRNA is expressed in the early epidermis that lies on the dorsal posterior side of the embryo (Fig. 2Figure 2.


The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis.

Pettitt J, Cox EA, Broadbent ID, Flett A, Hardin J - J. Cell Biol. (2003)

jac-1 is expressed in the early epidermis and JAC-1–GFP localizes to epidermal cell borders during morphogenesis. (A) Representative images from in situ hybridization with a control jac-1 sense probe (left) and jac-1 antisense probe (right). (B) Confocal images of JAC-1–GFP expression. (a) Dorsal view showing JAC-1–GFP localization during dorsal intercalation (two interdigitating cells are marked with asterisks). (b and c) Lateral views showing JAC-1–GFP localization during elongation. (d–f) Time course of an embryo undergoing ventral enclosure. Bar, 10 μm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2172718&req=5

fig2: jac-1 is expressed in the early epidermis and JAC-1–GFP localizes to epidermal cell borders during morphogenesis. (A) Representative images from in situ hybridization with a control jac-1 sense probe (left) and jac-1 antisense probe (right). (B) Confocal images of JAC-1–GFP expression. (a) Dorsal view showing JAC-1–GFP localization during dorsal intercalation (two interdigitating cells are marked with asterisks). (b and c) Lateral views showing JAC-1–GFP localization during elongation. (d–f) Time course of an embryo undergoing ventral enclosure. Bar, 10 μm.
Mentions: To gain insight into the physiological function of JAC-1, its expression and subcellular localization were examined. In situ hybridization demonstrates that jac-1 mRNA is expressed in the early epidermis that lies on the dorsal posterior side of the embryo (Fig. 2Figure 2.

Bottom Line: We have examined the role of the single Caenorhabditis elegans p120ctn homologue JAC-1 (juxtamembrane domain [JMD]-associated catenin) during epidermal morphogenesis.Surprisingly, depleting JAC-1 expression using RNA interference (RNAi) does not result in any obvious defects in embryonic or postembryonic development.However, jac-1(RNAi) does increase the severity and penetrance of morphogenetic defects caused by a hypomorphic mutation in the hmp-1/alpha-catenin gene.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cell Biology, University of Aberdeen Institute of Medical Sciences, Aberdeen AB25 2ZD, Scotland, UK. j.pettitt@abdn.ac.uk

ABSTRACT
The cadherin-catenin complex is essential for tissue morphogenesis during animal development. In cultured mammalian cells, p120 catenin (p120ctn) is an important regulator of cadherin-catenin complex function. However, information on the role of p120ctn family members in cadherin-dependent events in vivo is limited. We have examined the role of the single Caenorhabditis elegans p120ctn homologue JAC-1 (juxtamembrane domain [JMD]-associated catenin) during epidermal morphogenesis. Similar to other p120ctn family members, JAC-1 binds the JMD of the classical cadherin HMR-1, and GFP-tagged JAC-1 localizes to adherens junctions in an HMR-1-dependent manner. Surprisingly, depleting JAC-1 expression using RNA interference (RNAi) does not result in any obvious defects in embryonic or postembryonic development. However, jac-1(RNAi) does increase the severity and penetrance of morphogenetic defects caused by a hypomorphic mutation in the hmp-1/alpha-catenin gene. In these hmp-1 mutants, jac-1 depletion causes failure of the embryo to elongate into a worm-like shape, a process that involves contraction of the epidermis. Associated with failed elongation is the detachment of actin bundles from epidermal adherens junctions and failure to maintain cadherin in adherens junctions. These results suggest that JAC-1 acts as a positive modulator of cadherin function in C. elegans.

Show MeSH
Related in: MedlinePlus