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Long continuous actin bundles in Drosophila bristles are constructed by overlapping short filaments.

Guild GM, Connelly PS, Ruggiero L, Vranich KA, Tilney LG - J. Cell Biol. (2003)

Bottom Line: These long bundles are built from much shorter modules that graft together.Thus, bundle morphogenesis has several components: module formation, elongation, grafting, and bundle smoothing.These actin bundles are much like a rope or cable, made by overlapping elements that run a small fraction of the overall length, and stiffened by cross-linking.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018, USA. gguild@sas.upenn.edu

ABSTRACT
The actin bundles essential for Drosophila bristle elongation are hundreds of microns long and composed of cross-linked unipolar filaments. These long bundles are built from much shorter modules that graft together. Using both confocal and electron microscopy, we demonstrate that newly synthesized modules are short (1-2 microm in length); modules elongate to approximately 3 microm by growing over the surface of longitudinally adjacent modules to form a graft; the grafted regions are initially secured by the forked protein cross-bridge and later by the fascin cross-bridge; actin bundles are smoothed by filament addition and appear continuous and without swellings; and in the absence of grafting, dramatic alterations in cell shape occur that substitutes cell width expansion for elongation. Thus, bundle morphogenesis has several components: module formation, elongation, grafting, and bundle smoothing. These actin bundles are much like a rope or cable, made by overlapping elements that run a small fraction of the overall length, and stiffened by cross-linking.

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Actin bundles are made smooth by the addition of actin filaments to grafting modules. Three serial longitudinal sections through a bristle from a 35-h pupa. At this age, the bristles are very short so stages in grafting of modules should be present. In these sections, a graft can be seen and the overlap visualized (arrows). We believe that cross-linking of the filaments in the grafted region is beginning. Bar, 0.1 μm.
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fig5: Actin bundles are made smooth by the addition of actin filaments to grafting modules. Three serial longitudinal sections through a bristle from a 35-h pupa. At this age, the bristles are very short so stages in grafting of modules should be present. In these sections, a graft can be seen and the overlap visualized (arrows). We believe that cross-linking of the filaments in the grafted region is beginning. Bar, 0.1 μm.

Mentions: We also examined longitudinal sections through bundles that had just completed the first few modules (Fig. 5). We believe these three serial sections illustrate a graft in which the ends of the modules are being “glued” or cross-linked together. This can be appreciated by noting that the space between bundles (Fig. 5 a, arrow) in one section is filled in the other sections (Fig. 5, b and c). The grafted region also exhibits a 12-nm striping typical of the transverse period across a bundle in longitudinal section due to fascin cross-bridging (Tilney et al., 1995) indicating that the fascin cross-bridge is ultimately present in the graft.


Long continuous actin bundles in Drosophila bristles are constructed by overlapping short filaments.

Guild GM, Connelly PS, Ruggiero L, Vranich KA, Tilney LG - J. Cell Biol. (2003)

Actin bundles are made smooth by the addition of actin filaments to grafting modules. Three serial longitudinal sections through a bristle from a 35-h pupa. At this age, the bristles are very short so stages in grafting of modules should be present. In these sections, a graft can be seen and the overlap visualized (arrows). We believe that cross-linking of the filaments in the grafted region is beginning. Bar, 0.1 μm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2172841&req=5

fig5: Actin bundles are made smooth by the addition of actin filaments to grafting modules. Three serial longitudinal sections through a bristle from a 35-h pupa. At this age, the bristles are very short so stages in grafting of modules should be present. In these sections, a graft can be seen and the overlap visualized (arrows). We believe that cross-linking of the filaments in the grafted region is beginning. Bar, 0.1 μm.
Mentions: We also examined longitudinal sections through bundles that had just completed the first few modules (Fig. 5). We believe these three serial sections illustrate a graft in which the ends of the modules are being “glued” or cross-linked together. This can be appreciated by noting that the space between bundles (Fig. 5 a, arrow) in one section is filled in the other sections (Fig. 5, b and c). The grafted region also exhibits a 12-nm striping typical of the transverse period across a bundle in longitudinal section due to fascin cross-bridging (Tilney et al., 1995) indicating that the fascin cross-bridge is ultimately present in the graft.

Bottom Line: These long bundles are built from much shorter modules that graft together.Thus, bundle morphogenesis has several components: module formation, elongation, grafting, and bundle smoothing.These actin bundles are much like a rope or cable, made by overlapping elements that run a small fraction of the overall length, and stiffened by cross-linking.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018, USA. gguild@sas.upenn.edu

ABSTRACT
The actin bundles essential for Drosophila bristle elongation are hundreds of microns long and composed of cross-linked unipolar filaments. These long bundles are built from much shorter modules that graft together. Using both confocal and electron microscopy, we demonstrate that newly synthesized modules are short (1-2 microm in length); modules elongate to approximately 3 microm by growing over the surface of longitudinally adjacent modules to form a graft; the grafted regions are initially secured by the forked protein cross-bridge and later by the fascin cross-bridge; actin bundles are smoothed by filament addition and appear continuous and without swellings; and in the absence of grafting, dramatic alterations in cell shape occur that substitutes cell width expansion for elongation. Thus, bundle morphogenesis has several components: module formation, elongation, grafting, and bundle smoothing. These actin bundles are much like a rope or cable, made by overlapping elements that run a small fraction of the overall length, and stiffened by cross-linking.

Show MeSH
Related in: MedlinePlus