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Filamin is required for ring canal assembly and actin organization during Drosophila oogenesis.

Li MG, Serr M, Edwards K, Ludmann S, Yamamoto D, Tilney LG, Field CM, Hays TS - J. Cell Biol. (1999)

Bottom Line: In consequence, actin-binding proteins are increasingly a focus of investigations into effectors of cell signaling and the coordination of cellular behaviors within developmental processes.Mutations in Drosophila filamin disrupt actin filament organization and compromise membrane integrity during oocyte development, resulting in female sterility.The genetic and molecular characterization of Drosophila filamin provides the first genetic model system for the analysis of filamin function and regulation during development.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, Cell and Developmental Biology, University of Minnesota, St. Paul, Minnesota 55108, USA.

ABSTRACT
The remodeling of the actin cytoskeleton is essential for cell migration, cell division, and cell morphogenesis. Actin-binding proteins play a pivotal role in reorganizing the actin cytoskeleton in response to signals exchanged between cells. In consequence, actin-binding proteins are increasingly a focus of investigations into effectors of cell signaling and the coordination of cellular behaviors within developmental processes. One of the first actin-binding proteins identified was filamin, or actin-binding protein 280 (ABP280). Filamin is required for cell migration (Cunningham et al. 1992), and mutations in human alpha-filamin (FLN1; Fox et al. 1998) are responsible for impaired migration of cerebral neurons and give rise to periventricular heterotopia, a disorder that leads to epilepsy and vascular disorders, as well as embryonic lethality. We report the identification and characterization of a mutation in Drosophila filamin, the homologue of human alpha-filamin. During oogenesis, filamin is concentrated in the ring canal structures that fortify arrested cleavage furrows and establish cytoplasmic bridges between cells of the germline. The major structural features common to other filamins are conserved in Drosophila filamin. Mutations in Drosophila filamin disrupt actin filament organization and compromise membrane integrity during oocyte development, resulting in female sterility. The genetic and molecular characterization of Drosophila filamin provides the first genetic model system for the analysis of filamin function and regulation during development.

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Panels a through d show thin sections through ring canals between nurse cells of stage 4 egg chambers. (a and b) Wild-type: Attached to the cytoplasmic side of the plasma membrane limiting the ring canal is some electron dense material (arrow). Inside this is a fuzzy layer of filamentous material that is composed of a bundle of circumferentially arranged actin filaments, A. See Tilney et al., 1996 for details. (b) Higher magnification of a portion of a. (c and d) sko/sko mutant. The plasma membrane of the ring canal is coated on its cytoplasmic surface with the same dense material (arrow) seen in wild-type, but no actin filaments are attached to it. (e and f) Thin sections through nurse cells of sko/sko mutant stage 5 egg chambers. (e) By this stage the ring canals are beginning to break down. Although the dense material remains attached to the plasma membrane, the shape of the canal margin has collapsed. Note, the other half of this ring canal was not located in the section and was presumably disrupted. (f) A thin section through the cytoplasm of two nurse cells (N) where the plasma membrane limiting the interface between the cells has vesiculated and is breaking down (arrows).
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Figure 3: Panels a through d show thin sections through ring canals between nurse cells of stage 4 egg chambers. (a and b) Wild-type: Attached to the cytoplasmic side of the plasma membrane limiting the ring canal is some electron dense material (arrow). Inside this is a fuzzy layer of filamentous material that is composed of a bundle of circumferentially arranged actin filaments, A. See Tilney et al., 1996 for details. (b) Higher magnification of a portion of a. (c and d) sko/sko mutant. The plasma membrane of the ring canal is coated on its cytoplasmic surface with the same dense material (arrow) seen in wild-type, but no actin filaments are attached to it. (e and f) Thin sections through nurse cells of sko/sko mutant stage 5 egg chambers. (e) By this stage the ring canals are beginning to break down. Although the dense material remains attached to the plasma membrane, the shape of the canal margin has collapsed. Note, the other half of this ring canal was not located in the section and was presumably disrupted. (f) A thin section through the cytoplasm of two nurse cells (N) where the plasma membrane limiting the interface between the cells has vesiculated and is breaking down (arrows).

Mentions: Thin sections through wild-type and sko ring canals at stage 3 and 4 (Fig. 3, a–d) are consistent with what we have described by light microscopy and expand our resolution of the ring canal structures. As noted in Tilney et al. 1996, in vertical section the plasma membrane lining the inner margin of each side of the ring canal appears as a T-shaped junction limiting adjacent nurse cells (Fig. 3, a and b). Attached to these T-shaped extensions of plasma membrane in both wild-type and sko ring canals is a layer of dense material. Inside this material in the wild-type ring canal is a thick layer of actin filaments that is organized circumferentially as a purse string (Fig. 3, a and b; Tilney et al. 1996). This layer of filaments is missing altogether (Fig. 3c and Fig. d) in the sko mutants or is reduced to a tiny fraction of the number of filaments seen at this same stage in wild-type. Note that in the sko mutants, the T-shaped extensions are formed with their associated dense material, even though actin filaments are sparse or missing altogether. Since anillin is present through stage 6 in sko mutants, it seems reasonable that anillin may be one (possibly major) component of this dense material lining the cytoplasmic surface of the canal.


Filamin is required for ring canal assembly and actin organization during Drosophila oogenesis.

Li MG, Serr M, Edwards K, Ludmann S, Yamamoto D, Tilney LG, Field CM, Hays TS - J. Cell Biol. (1999)

Panels a through d show thin sections through ring canals between nurse cells of stage 4 egg chambers. (a and b) Wild-type: Attached to the cytoplasmic side of the plasma membrane limiting the ring canal is some electron dense material (arrow). Inside this is a fuzzy layer of filamentous material that is composed of a bundle of circumferentially arranged actin filaments, A. See Tilney et al., 1996 for details. (b) Higher magnification of a portion of a. (c and d) sko/sko mutant. The plasma membrane of the ring canal is coated on its cytoplasmic surface with the same dense material (arrow) seen in wild-type, but no actin filaments are attached to it. (e and f) Thin sections through nurse cells of sko/sko mutant stage 5 egg chambers. (e) By this stage the ring canals are beginning to break down. Although the dense material remains attached to the plasma membrane, the shape of the canal margin has collapsed. Note, the other half of this ring canal was not located in the section and was presumably disrupted. (f) A thin section through the cytoplasm of two nurse cells (N) where the plasma membrane limiting the interface between the cells has vesiculated and is breaking down (arrows).
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Figure 3: Panels a through d show thin sections through ring canals between nurse cells of stage 4 egg chambers. (a and b) Wild-type: Attached to the cytoplasmic side of the plasma membrane limiting the ring canal is some electron dense material (arrow). Inside this is a fuzzy layer of filamentous material that is composed of a bundle of circumferentially arranged actin filaments, A. See Tilney et al., 1996 for details. (b) Higher magnification of a portion of a. (c and d) sko/sko mutant. The plasma membrane of the ring canal is coated on its cytoplasmic surface with the same dense material (arrow) seen in wild-type, but no actin filaments are attached to it. (e and f) Thin sections through nurse cells of sko/sko mutant stage 5 egg chambers. (e) By this stage the ring canals are beginning to break down. Although the dense material remains attached to the plasma membrane, the shape of the canal margin has collapsed. Note, the other half of this ring canal was not located in the section and was presumably disrupted. (f) A thin section through the cytoplasm of two nurse cells (N) where the plasma membrane limiting the interface between the cells has vesiculated and is breaking down (arrows).
Mentions: Thin sections through wild-type and sko ring canals at stage 3 and 4 (Fig. 3, a–d) are consistent with what we have described by light microscopy and expand our resolution of the ring canal structures. As noted in Tilney et al. 1996, in vertical section the plasma membrane lining the inner margin of each side of the ring canal appears as a T-shaped junction limiting adjacent nurse cells (Fig. 3, a and b). Attached to these T-shaped extensions of plasma membrane in both wild-type and sko ring canals is a layer of dense material. Inside this material in the wild-type ring canal is a thick layer of actin filaments that is organized circumferentially as a purse string (Fig. 3, a and b; Tilney et al. 1996). This layer of filaments is missing altogether (Fig. 3c and Fig. d) in the sko mutants or is reduced to a tiny fraction of the number of filaments seen at this same stage in wild-type. Note that in the sko mutants, the T-shaped extensions are formed with their associated dense material, even though actin filaments are sparse or missing altogether. Since anillin is present through stage 6 in sko mutants, it seems reasonable that anillin may be one (possibly major) component of this dense material lining the cytoplasmic surface of the canal.

Bottom Line: In consequence, actin-binding proteins are increasingly a focus of investigations into effectors of cell signaling and the coordination of cellular behaviors within developmental processes.Mutations in Drosophila filamin disrupt actin filament organization and compromise membrane integrity during oocyte development, resulting in female sterility.The genetic and molecular characterization of Drosophila filamin provides the first genetic model system for the analysis of filamin function and regulation during development.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, Cell and Developmental Biology, University of Minnesota, St. Paul, Minnesota 55108, USA.

ABSTRACT
The remodeling of the actin cytoskeleton is essential for cell migration, cell division, and cell morphogenesis. Actin-binding proteins play a pivotal role in reorganizing the actin cytoskeleton in response to signals exchanged between cells. In consequence, actin-binding proteins are increasingly a focus of investigations into effectors of cell signaling and the coordination of cellular behaviors within developmental processes. One of the first actin-binding proteins identified was filamin, or actin-binding protein 280 (ABP280). Filamin is required for cell migration (Cunningham et al. 1992), and mutations in human alpha-filamin (FLN1; Fox et al. 1998) are responsible for impaired migration of cerebral neurons and give rise to periventricular heterotopia, a disorder that leads to epilepsy and vascular disorders, as well as embryonic lethality. We report the identification and characterization of a mutation in Drosophila filamin, the homologue of human alpha-filamin. During oogenesis, filamin is concentrated in the ring canal structures that fortify arrested cleavage furrows and establish cytoplasmic bridges between cells of the germline. The major structural features common to other filamins are conserved in Drosophila filamin. Mutations in Drosophila filamin disrupt actin filament organization and compromise membrane integrity during oocyte development, resulting in female sterility. The genetic and molecular characterization of Drosophila filamin provides the first genetic model system for the analysis of filamin function and regulation during development.

Show MeSH
Related in: MedlinePlus