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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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Smooth actin bundles are built from modules grafted together. Confocal image through a portion of an unfixed 46-h pupal bristle in which the bundles have been labeled with GFP actin. The bristle was bent during preparation and the actin bundles fractured (arrowheads). Of interest here is that individual bundle fracture points occur at the same place along the bristle longitudinal axis and that module overlap is disrupted at the breaks. The tip (upward arrowhead) indicates the orientation of the Drosophila bristle. Bar, 5 μm.
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fig2: Smooth actin bundles are built from modules grafted together. Confocal image through a portion of an unfixed 46-h pupal bristle in which the bundles have been labeled with GFP actin. The bristle was bent during preparation and the actin bundles fractured (arrowheads). Of interest here is that individual bundle fracture points occur at the same place along the bristle longitudinal axis and that module overlap is disrupted at the breaks. The tip (upward arrowhead) indicates the orientation of the Drosophila bristle. Bar, 5 μm.

Mentions: To examine bristles prepared with a minimum of manipulation, we labeled the bundles with GFP actin and examined live pupae after careful removal from the pupal case. Nevertheless, we occasionally bend a bristle. Close examination of these bends (Fig. 2) showed that the actin bundles were fractured revealing two tapered ends that before breaking had overlapped, much like horticulture grafts in which a branch of one twig overlaps another at the graft site. We presume that such a graft is the result of the joining of adjacent modules, a conclusion that is consistent with the observation that during bundle breakdown the gaps between the modules are also frequently in transverse register (Tilney et al., 1996).


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)

Smooth actin bundles are built from modules grafted together. Confocal image through a portion of an unfixed 46-h pupal bristle in which the bundles have been labeled with GFP actin. The bristle was bent during preparation and the actin bundles fractured (arrowheads). Of interest here is that individual bundle fracture points occur at the same place along the bristle longitudinal axis and that module overlap is disrupted at the breaks. The tip (upward arrowhead) indicates the orientation of the Drosophila bristle. Bar, 5 μm.
© Copyright Policy
Related In: Results  -  Collection

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

fig2: Smooth actin bundles are built from modules grafted together. Confocal image through a portion of an unfixed 46-h pupal bristle in which the bundles have been labeled with GFP actin. The bristle was bent during preparation and the actin bundles fractured (arrowheads). Of interest here is that individual bundle fracture points occur at the same place along the bristle longitudinal axis and that module overlap is disrupted at the breaks. The tip (upward arrowhead) indicates the orientation of the Drosophila bristle. Bar, 5 μm.
Mentions: To examine bristles prepared with a minimum of manipulation, we labeled the bundles with GFP actin and examined live pupae after careful removal from the pupal case. Nevertheless, we occasionally bend a bristle. Close examination of these bends (Fig. 2) showed that the actin bundles were fractured revealing two tapered ends that before breaking had overlapped, much like horticulture grafts in which a branch of one twig overlaps another at the graft site. We presume that such a graft is the result of the joining of adjacent modules, a conclusion that is consistent with the observation that during bundle breakdown the gaps between the modules are also frequently in transverse register (Tilney et al., 1996).

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