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The Caenorhabditis elegans vab-10 spectraplakin isoforms protect the epidermis against internal and external forces.

Bosher JM, Hahn BS, Legouis R, Sookhareea S, Weimer RM, Gansmuller A, Chisholm AD, Rose AM, Bessereau JL, Labouesse M - J. Cell Biol. (2003)

Bottom Line: We suggest that this isoform protects against forces external to the epidermis.In contrast, lack of VAB-10B leads to increased epidermal thickness during embryonic morphogenesis when epidermal cells change shape.We suggest that this isoform protects cells against tension that builds up within the epidermis.

View Article: PubMed Central - PubMed

Affiliation: Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP, BP10142, CU de Strasbourg, Illkirch Cedex F-67404, France.

ABSTRACT
Morphogenesis of the Caenorhabditis elegans embryo is driven by actin microfilaments in the epidermis and by sarcomeres in body wall muscles. Both tissues are mechanically coupled, most likely through specialized attachment structures called fibrous organelles (FOs) that connect muscles to the cuticle across the epidermis. Here, we report the identification of new mutations in a gene known as vab-10, which lead to severe morphogenesis defects, and show that vab-10 corresponds to the C. elegans spectraplakin locus. Our analysis of vab-10 reveals novel insights into the role of this plakin subfamily. vab-10 generates isoforms related either to plectin (termed VAB-10A) or to microtubule actin cross-linking factor plakins (termed VAB-10B). Using specific antibodies and mutations, we show that VAB-10A and VAB-10B have distinct distributions and functions in the epidermis. Loss of VAB-10A impairs the integrity of FOs, leading to epidermal detachment from the cuticle and muscles, hence demonstrating that FOs are functionally and molecularly related to hemidesmosomes. We suggest that this isoform protects against forces external to the epidermis. In contrast, lack of VAB-10B leads to increased epidermal thickness during embryonic morphogenesis when epidermal cells change shape. We suggest that this isoform protects cells against tension that builds up within the epidermis.

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Model for the distributions and roles of VAB-10 isoforms in the epidermis. Enlarged view of a muscle–epidermis–cuticle contact area in elongating wild-type (left), vab-10A (middle), and vab-10B (right) embryos. FOs correspond to the structure formed by electron-dense plaques found at the apical and basal epidermal plasma membranes (black bars) and the interconnecting IFs. Myotactin, MUP-4, and MUA-3 connect FOs to the cuticle (Cut) or the ECM separating the epidermis (Epid) from muscles (Mus). VAB-10A (pink) is an FO component (green), and VAB-10B is interspersed between FOs (pink) and coincides with the furrows separating annuli where actin MFs have also been observed (Costa et al., 1997). Myotactin bands do not fully coincide with VAB-10A bands in young larvae, but do so at later stages. VAB-10B is clearly apical and basal in young embryos, but we do not know if this is also the case later. VAB-10A absence affects FO assembly, causing the epidermis to detach from the ECM and the cuticle. VAB-10B absence causes the epidermal thickness to increase. The molecules that help maintain the distance between apical and basal plasma membranes together with VAB-10B are further discussed in the text. The respective thickness of each layer is not drawn to scale.
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fig9: Model for the distributions and roles of VAB-10 isoforms in the epidermis. Enlarged view of a muscle–epidermis–cuticle contact area in elongating wild-type (left), vab-10A (middle), and vab-10B (right) embryos. FOs correspond to the structure formed by electron-dense plaques found at the apical and basal epidermal plasma membranes (black bars) and the interconnecting IFs. Myotactin, MUP-4, and MUA-3 connect FOs to the cuticle (Cut) or the ECM separating the epidermis (Epid) from muscles (Mus). VAB-10A (pink) is an FO component (green), and VAB-10B is interspersed between FOs (pink) and coincides with the furrows separating annuli where actin MFs have also been observed (Costa et al., 1997). Myotactin bands do not fully coincide with VAB-10A bands in young larvae, but do so at later stages. VAB-10B is clearly apical and basal in young embryos, but we do not know if this is also the case later. VAB-10A absence affects FO assembly, causing the epidermis to detach from the ECM and the cuticle. VAB-10B absence causes the epidermal thickness to increase. The molecules that help maintain the distance between apical and basal plasma membranes together with VAB-10B are further discussed in the text. The respective thickness of each layer is not drawn to scale.

Mentions: Our data demonstrate that vab-10 corresponds to the C. elegans spectraplakin locus, a plakin subfamily defined by Drosophila shot and vertebrate BPAG1 and MACF1 loci (Roper et al., 2002). By alternative splicing of a common 5′ region to different sets of 3′ exons, vab-10 generates two distinct classes of isoforms with essentially nonoverlapping subcellular distributions and different functions in the epidermis. Isoforms related to plectin and BPAG1-e (termed VAB-10A) are essential to maintain the epidermis–ECM attachment. Isoforms related to MACF and BPAG1-a (termed VAB-10B) maintain a connection between the apical and basal epidermal plasma membranes during morphogenesis. A model for VAB-10 distribution and function is presented in Fig. 9 and discussed further in the next paragraph.


The Caenorhabditis elegans vab-10 spectraplakin isoforms protect the epidermis against internal and external forces.

Bosher JM, Hahn BS, Legouis R, Sookhareea S, Weimer RM, Gansmuller A, Chisholm AD, Rose AM, Bessereau JL, Labouesse M - J. Cell Biol. (2003)

Model for the distributions and roles of VAB-10 isoforms in the epidermis. Enlarged view of a muscle–epidermis–cuticle contact area in elongating wild-type (left), vab-10A (middle), and vab-10B (right) embryos. FOs correspond to the structure formed by electron-dense plaques found at the apical and basal epidermal plasma membranes (black bars) and the interconnecting IFs. Myotactin, MUP-4, and MUA-3 connect FOs to the cuticle (Cut) or the ECM separating the epidermis (Epid) from muscles (Mus). VAB-10A (pink) is an FO component (green), and VAB-10B is interspersed between FOs (pink) and coincides with the furrows separating annuli where actin MFs have also been observed (Costa et al., 1997). Myotactin bands do not fully coincide with VAB-10A bands in young larvae, but do so at later stages. VAB-10B is clearly apical and basal in young embryos, but we do not know if this is also the case later. VAB-10A absence affects FO assembly, causing the epidermis to detach from the ECM and the cuticle. VAB-10B absence causes the epidermal thickness to increase. The molecules that help maintain the distance between apical and basal plasma membranes together with VAB-10B are further discussed in the text. The respective thickness of each layer is not drawn to scale.
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Related In: Results  -  Collection

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fig9: Model for the distributions and roles of VAB-10 isoforms in the epidermis. Enlarged view of a muscle–epidermis–cuticle contact area in elongating wild-type (left), vab-10A (middle), and vab-10B (right) embryos. FOs correspond to the structure formed by electron-dense plaques found at the apical and basal epidermal plasma membranes (black bars) and the interconnecting IFs. Myotactin, MUP-4, and MUA-3 connect FOs to the cuticle (Cut) or the ECM separating the epidermis (Epid) from muscles (Mus). VAB-10A (pink) is an FO component (green), and VAB-10B is interspersed between FOs (pink) and coincides with the furrows separating annuli where actin MFs have also been observed (Costa et al., 1997). Myotactin bands do not fully coincide with VAB-10A bands in young larvae, but do so at later stages. VAB-10B is clearly apical and basal in young embryos, but we do not know if this is also the case later. VAB-10A absence affects FO assembly, causing the epidermis to detach from the ECM and the cuticle. VAB-10B absence causes the epidermal thickness to increase. The molecules that help maintain the distance between apical and basal plasma membranes together with VAB-10B are further discussed in the text. The respective thickness of each layer is not drawn to scale.
Mentions: Our data demonstrate that vab-10 corresponds to the C. elegans spectraplakin locus, a plakin subfamily defined by Drosophila shot and vertebrate BPAG1 and MACF1 loci (Roper et al., 2002). By alternative splicing of a common 5′ region to different sets of 3′ exons, vab-10 generates two distinct classes of isoforms with essentially nonoverlapping subcellular distributions and different functions in the epidermis. Isoforms related to plectin and BPAG1-e (termed VAB-10A) are essential to maintain the epidermis–ECM attachment. Isoforms related to MACF and BPAG1-a (termed VAB-10B) maintain a connection between the apical and basal epidermal plasma membranes during morphogenesis. A model for VAB-10 distribution and function is presented in Fig. 9 and discussed further in the next paragraph.

Bottom Line: We suggest that this isoform protects against forces external to the epidermis.In contrast, lack of VAB-10B leads to increased epidermal thickness during embryonic morphogenesis when epidermal cells change shape.We suggest that this isoform protects cells against tension that builds up within the epidermis.

View Article: PubMed Central - PubMed

Affiliation: Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP, BP10142, CU de Strasbourg, Illkirch Cedex F-67404, France.

ABSTRACT
Morphogenesis of the Caenorhabditis elegans embryo is driven by actin microfilaments in the epidermis and by sarcomeres in body wall muscles. Both tissues are mechanically coupled, most likely through specialized attachment structures called fibrous organelles (FOs) that connect muscles to the cuticle across the epidermis. Here, we report the identification of new mutations in a gene known as vab-10, which lead to severe morphogenesis defects, and show that vab-10 corresponds to the C. elegans spectraplakin locus. Our analysis of vab-10 reveals novel insights into the role of this plakin subfamily. vab-10 generates isoforms related either to plectin (termed VAB-10A) or to microtubule actin cross-linking factor plakins (termed VAB-10B). Using specific antibodies and mutations, we show that VAB-10A and VAB-10B have distinct distributions and functions in the epidermis. Loss of VAB-10A impairs the integrity of FOs, leading to epidermal detachment from the cuticle and muscles, hence demonstrating that FOs are functionally and molecularly related to hemidesmosomes. We suggest that this isoform protects against forces external to the epidermis. In contrast, lack of VAB-10B leads to increased epidermal thickness during embryonic morphogenesis when epidermal cells change shape. We suggest that this isoform protects cells against tension that builds up within the epidermis.

Show MeSH
Related in: MedlinePlus