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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 bundle morphogenesis during bristle development illustrated by confocal images of phalloidin-stained actin bundles. A portion of a bristle is shown in each panel. Bristle tips are up. (a) Microchaete from of a 44-h pupa showing that the bundles are continuous with no gaps. (b) Macrochaete from a 48-h pupa bristle during an early stage in bundle disassembly. Note the gaps between modules in the bundles. (c) Macrochaete tip from a 33-h pupa showing very small modules that eventually morph into smooth bundles (bottom). Bars, 5 μm.
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fig1: Actin bundle morphogenesis during bristle development illustrated by confocal images of phalloidin-stained actin bundles. A portion of a bristle is shown in each panel. Bristle tips are up. (a) Microchaete from of a 44-h pupa showing that the bundles are continuous with no gaps. (b) Macrochaete from a 48-h pupa bristle during an early stage in bundle disassembly. Note the gaps between modules in the bundles. (c) Macrochaete tip from a 33-h pupa showing very small modules that eventually morph into smooth bundles (bottom). Bars, 5 μm.

Mentions: If the actin bundles in bristle cells are examined after staining with fluorescently labeled phalloidin (Appel et al., 1993; Petersen et al., 1994; Tilney et al., 1996; Wulfkuhle et al., 1998) or if they are examined in living cells using GFP decoration (Guild et al., 2002), we see bundles that extend from the socket region at the base of the bristle shaft to the tip of the bristle. At higher magnification, these bundles are continuous (Fig. 1 a). However, once the bristles have fully elongated and a chitinous exoskeleton is laid down (Tilney et al., 1996), the actin bundles breakdown. During this breakdown, the bundles appear to have been “sawed” into shorter segments (Fig. 1 b). Further disassembly of the bundles occurs by the removal of subunits from the apical end of each module so that module length becomes shorter and shorter (Guild et al., 2002).


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 bundle morphogenesis during bristle development illustrated by confocal images of phalloidin-stained actin bundles. A portion of a bristle is shown in each panel. Bristle tips are up. (a) Microchaete from of a 44-h pupa showing that the bundles are continuous with no gaps. (b) Macrochaete from a 48-h pupa bristle during an early stage in bundle disassembly. Note the gaps between modules in the bundles. (c) Macrochaete tip from a 33-h pupa showing very small modules that eventually morph into smooth bundles (bottom). Bars, 5 μm.
© Copyright Policy
Related In: Results  -  Collection

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

fig1: Actin bundle morphogenesis during bristle development illustrated by confocal images of phalloidin-stained actin bundles. A portion of a bristle is shown in each panel. Bristle tips are up. (a) Microchaete from of a 44-h pupa showing that the bundles are continuous with no gaps. (b) Macrochaete from a 48-h pupa bristle during an early stage in bundle disassembly. Note the gaps between modules in the bundles. (c) Macrochaete tip from a 33-h pupa showing very small modules that eventually morph into smooth bundles (bottom). Bars, 5 μm.
Mentions: If the actin bundles in bristle cells are examined after staining with fluorescently labeled phalloidin (Appel et al., 1993; Petersen et al., 1994; Tilney et al., 1996; Wulfkuhle et al., 1998) or if they are examined in living cells using GFP decoration (Guild et al., 2002), we see bundles that extend from the socket region at the base of the bristle shaft to the tip of the bristle. At higher magnification, these bundles are continuous (Fig. 1 a). However, once the bristles have fully elongated and a chitinous exoskeleton is laid down (Tilney et al., 1996), the actin bundles breakdown. During this breakdown, the bundles appear to have been “sawed” into shorter segments (Fig. 1 b). Further disassembly of the bundles occurs by the removal of subunits from the apical end of each module so that module length becomes shorter and shorter (Guild et al., 2002).

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