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LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling.

Chen L, Ong B, Bennett V - J. Cell Biol. (2001)

Bottom Line: In addition, the ubiquitously expressed LAD-1, which binds to ankyrin-G, colocalizes with the C. elegans ankyrin, UNC-44, in multiple tissues at sites of cell-cell contact.These findings suggest a novel ankyrin-independent role for LAD-1 related to FGFR signaling.Taken together, these results indicate that L1CAMs constitute a family of ubiquitous adhesion molecules, which participate in tissue morphogenesis and maintaining tissue integrity in metazoans.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Department of Cell Biology, and Department of Biochemistry, Duke University Medical Center, Durham, NC 27710, USA. l.chen@cellbio.duke.edu

ABSTRACT
This study shows that L1-like adhesion (LAD-1), the sole Caenorhabditis elegans homologue of the L1 family of neuronal adhesion molecules, is required for proper development of the germline and the early embryo and embryonic and gonadal morphogenesis. In addition, the ubiquitously expressed LAD-1, which binds to ankyrin-G, colocalizes with the C. elegans ankyrin, UNC-44, in multiple tissues at sites of cell-cell contact. Finally, we show that LAD-1 is phosphorylated in a fibroblast growth factor receptor (FGFR) pathway-dependent manner on a tyrosine residue in the highly conserved ankyrin-binding motif, FIGQY, which was shown previously to abolish the L1 family of cell adhesion molecule (L1CAM) binding to ankyrin in cultured cells. Immunofluorescence studies revealed that FIGQY-tyrosine-phosphorylated LAD-1 does not colocalize with nonphosphorylated LAD-1 or UNC-44 ankyrin but instead is localized to sites that undergo mechanical stress in polarized epithelia and axon-body wall muscle junctions. These findings suggest a novel ankyrin-independent role for LAD-1 related to FGFR signaling. Taken together, these results indicate that L1CAMs constitute a family of ubiquitous adhesion molecules, which participate in tissue morphogenesis and maintaining tissue integrity in metazoans.

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LAD-1 is required for the gonad morphogenesis. (A) A cartoon (not to scale) of a wild-type U-shaped gonad in C. elegans. Below each panel (A–F) is a schematic of an animal opened dorsally and spread out, displaying the migration path of the DTCs as seen in the corresponding DIC micrograph. In wild-type animals (A and B), the gonad arms, led by a DTC on each arm, grow in opposite directions along the ventral length of the body. Each DTC makes the appropriate turns to meet the other at the middle of the body. DL, dorsal left; VL, ventral left; VR, ventral right; DR, dorsal right; red bar, vulva. In C, one DTC migrated a little too far to meet the other DTC that did not migrate far enough. D–F show various gonadal morphogenesis defects due to abnormal cell adhesion and/or DTC migration. The green arrows in B–F indicate the DTC, the numbered arrowheads indicate the progression of the DTC migration, and the red arrowhead points to the vulva. Bar, 50 μm.
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fig10: LAD-1 is required for the gonad morphogenesis. (A) A cartoon (not to scale) of a wild-type U-shaped gonad in C. elegans. Below each panel (A–F) is a schematic of an animal opened dorsally and spread out, displaying the migration path of the DTCs as seen in the corresponding DIC micrograph. In wild-type animals (A and B), the gonad arms, led by a DTC on each arm, grow in opposite directions along the ventral length of the body. Each DTC makes the appropriate turns to meet the other at the middle of the body. DL, dorsal left; VL, ventral left; VR, ventral right; DR, dorsal right; red bar, vulva. In C, one DTC migrated a little too far to meet the other DTC that did not migrate far enough. D–F show various gonadal morphogenesis defects due to abnormal cell adhesion and/or DTC migration. The green arrows in B–F indicate the DTC, the numbered arrowheads indicate the progression of the DTC migration, and the red arrowhead points to the vulva. Bar, 50 μm.

Mentions: The transgenic animals also displayed abnormal gonad morphology. The wild-type hermaphrodite gonad consists of two U-shaped tubular arms that are formed by distal tip cells (DTCs) located at the tip of each arm, which migrate during larval development along a characteristic path that originates at the ventral midbody (Fig. 10 A, schematic) (Kimble and Ward, 1988). Fig. 10 C shows a mild defect where the DTCs are positioned slightly posterior of the midbody, marked by the vulva (arrows indicate the ends of the gonad arms). More severe defects are shown in Fig. 10, D–F, where extra DTC turns were observed.


LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling.

Chen L, Ong B, Bennett V - J. Cell Biol. (2001)

LAD-1 is required for the gonad morphogenesis. (A) A cartoon (not to scale) of a wild-type U-shaped gonad in C. elegans. Below each panel (A–F) is a schematic of an animal opened dorsally and spread out, displaying the migration path of the DTCs as seen in the corresponding DIC micrograph. In wild-type animals (A and B), the gonad arms, led by a DTC on each arm, grow in opposite directions along the ventral length of the body. Each DTC makes the appropriate turns to meet the other at the middle of the body. DL, dorsal left; VL, ventral left; VR, ventral right; DR, dorsal right; red bar, vulva. In C, one DTC migrated a little too far to meet the other DTC that did not migrate far enough. D–F show various gonadal morphogenesis defects due to abnormal cell adhesion and/or DTC migration. The green arrows in B–F indicate the DTC, the numbered arrowheads indicate the progression of the DTC migration, and the red arrowhead points to the vulva. Bar, 50 μm.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2196473&req=5

fig10: LAD-1 is required for the gonad morphogenesis. (A) A cartoon (not to scale) of a wild-type U-shaped gonad in C. elegans. Below each panel (A–F) is a schematic of an animal opened dorsally and spread out, displaying the migration path of the DTCs as seen in the corresponding DIC micrograph. In wild-type animals (A and B), the gonad arms, led by a DTC on each arm, grow in opposite directions along the ventral length of the body. Each DTC makes the appropriate turns to meet the other at the middle of the body. DL, dorsal left; VL, ventral left; VR, ventral right; DR, dorsal right; red bar, vulva. In C, one DTC migrated a little too far to meet the other DTC that did not migrate far enough. D–F show various gonadal morphogenesis defects due to abnormal cell adhesion and/or DTC migration. The green arrows in B–F indicate the DTC, the numbered arrowheads indicate the progression of the DTC migration, and the red arrowhead points to the vulva. Bar, 50 μm.
Mentions: The transgenic animals also displayed abnormal gonad morphology. The wild-type hermaphrodite gonad consists of two U-shaped tubular arms that are formed by distal tip cells (DTCs) located at the tip of each arm, which migrate during larval development along a characteristic path that originates at the ventral midbody (Fig. 10 A, schematic) (Kimble and Ward, 1988). Fig. 10 C shows a mild defect where the DTCs are positioned slightly posterior of the midbody, marked by the vulva (arrows indicate the ends of the gonad arms). More severe defects are shown in Fig. 10, D–F, where extra DTC turns were observed.

Bottom Line: In addition, the ubiquitously expressed LAD-1, which binds to ankyrin-G, colocalizes with the C. elegans ankyrin, UNC-44, in multiple tissues at sites of cell-cell contact.These findings suggest a novel ankyrin-independent role for LAD-1 related to FGFR signaling.Taken together, these results indicate that L1CAMs constitute a family of ubiquitous adhesion molecules, which participate in tissue morphogenesis and maintaining tissue integrity in metazoans.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Department of Cell Biology, and Department of Biochemistry, Duke University Medical Center, Durham, NC 27710, USA. l.chen@cellbio.duke.edu

ABSTRACT
This study shows that L1-like adhesion (LAD-1), the sole Caenorhabditis elegans homologue of the L1 family of neuronal adhesion molecules, is required for proper development of the germline and the early embryo and embryonic and gonadal morphogenesis. In addition, the ubiquitously expressed LAD-1, which binds to ankyrin-G, colocalizes with the C. elegans ankyrin, UNC-44, in multiple tissues at sites of cell-cell contact. Finally, we show that LAD-1 is phosphorylated in a fibroblast growth factor receptor (FGFR) pathway-dependent manner on a tyrosine residue in the highly conserved ankyrin-binding motif, FIGQY, which was shown previously to abolish the L1 family of cell adhesion molecule (L1CAM) binding to ankyrin in cultured cells. Immunofluorescence studies revealed that FIGQY-tyrosine-phosphorylated LAD-1 does not colocalize with nonphosphorylated LAD-1 or UNC-44 ankyrin but instead is localized to sites that undergo mechanical stress in polarized epithelia and axon-body wall muscle junctions. These findings suggest a novel ankyrin-independent role for LAD-1 related to FGFR signaling. Taken together, these results indicate that L1CAMs constitute a family of ubiquitous adhesion molecules, which participate in tissue morphogenesis and maintaining tissue integrity in metazoans.

Show MeSH
Related in: MedlinePlus