Limits...
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.

Show MeSH

Related in: MedlinePlus

Model for stages in bundle morphogenesis. Three views of a developing bundle. The side view (left) and top view (center) represent a time-lapse view of a forming bundle. A schematic representation of actin filaments (right) shows a possible mechanism by which actin filaments accomplish bundle morphogenesis. For simplicity, consider a tandem array of three modules arranged head to tail. The filament polarity in all modules is identical with the barbed ends (+) oriented toward the bristle tip. Short modules are assembled as linear arrays (a) at the tip of a growing bristle and lengthen toward their neighbors by barbed end elongation (b). This elongation results in module overlap and subsequent cross-bridge–mediated grafting giving rise to periodic actin knuckles along the bundle (c). The modules in c–e are staggered to show this process more clearly. The regions of module overlap are extended by filament addition and elongation (d) to fill the gaps between grafts and to smooth the actin filament density along the length of the bundle (e). These events take place during a ∼30-min time window.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2172841&req=5

fig10: Model for stages in bundle morphogenesis. Three views of a developing bundle. The side view (left) and top view (center) represent a time-lapse view of a forming bundle. A schematic representation of actin filaments (right) shows a possible mechanism by which actin filaments accomplish bundle morphogenesis. For simplicity, consider a tandem array of three modules arranged head to tail. The filament polarity in all modules is identical with the barbed ends (+) oriented toward the bristle tip. Short modules are assembled as linear arrays (a) at the tip of a growing bristle and lengthen toward their neighbors by barbed end elongation (b). This elongation results in module overlap and subsequent cross-bridge–mediated grafting giving rise to periodic actin knuckles along the bundle (c). The modules in c–e are staggered to show this process more clearly. The regions of module overlap are extended by filament addition and elongation (d) to fill the gaps between grafts and to smooth the actin filament density along the length of the bundle (e). These events take place during a ∼30-min time window.

Mentions: First, modules form in head to tail linear arrays at the growing tip of the bristle (Fig. 10 a). These modules are short but not fixed in length. Second, modules elongate to fill in the gaps between them (Fig. 10 b). Third, modules overlap by one extending over another (Fig. 10 c). This can be seen as a local increase in actin staining intensity (a knuckle) along a bundle from a top-down perspective or as overlapping modules seen in profile. Fourth, module overlaps seem to elongate (Fig. 10 d) resulting in a thickening of the bundle and filling in between the overlaps. Finally, bundle diameter increases with the subsequent loss of module–module distinctions (Fig. 10 e). This maturation process results in a smooth bundle with no detectable discontinuities. However, the modular components of mature bundles are still detectable in these bundles.


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)

Model for stages in bundle morphogenesis. Three views of a developing bundle. The side view (left) and top view (center) represent a time-lapse view of a forming bundle. A schematic representation of actin filaments (right) shows a possible mechanism by which actin filaments accomplish bundle morphogenesis. For simplicity, consider a tandem array of three modules arranged head to tail. The filament polarity in all modules is identical with the barbed ends (+) oriented toward the bristle tip. Short modules are assembled as linear arrays (a) at the tip of a growing bristle and lengthen toward their neighbors by barbed end elongation (b). This elongation results in module overlap and subsequent cross-bridge–mediated grafting giving rise to periodic actin knuckles along the bundle (c). The modules in c–e are staggered to show this process more clearly. The regions of module overlap are extended by filament addition and elongation (d) to fill the gaps between grafts and to smooth the actin filament density along the length of the bundle (e). These events take place during a ∼30-min time window.
© Copyright Policy
Related In: Results  -  Collection

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

fig10: Model for stages in bundle morphogenesis. Three views of a developing bundle. The side view (left) and top view (center) represent a time-lapse view of a forming bundle. A schematic representation of actin filaments (right) shows a possible mechanism by which actin filaments accomplish bundle morphogenesis. For simplicity, consider a tandem array of three modules arranged head to tail. The filament polarity in all modules is identical with the barbed ends (+) oriented toward the bristle tip. Short modules are assembled as linear arrays (a) at the tip of a growing bristle and lengthen toward their neighbors by barbed end elongation (b). This elongation results in module overlap and subsequent cross-bridge–mediated grafting giving rise to periodic actin knuckles along the bundle (c). The modules in c–e are staggered to show this process more clearly. The regions of module overlap are extended by filament addition and elongation (d) to fill the gaps between grafts and to smooth the actin filament density along the length of the bundle (e). These events take place during a ∼30-min time window.
Mentions: First, modules form in head to tail linear arrays at the growing tip of the bristle (Fig. 10 a). These modules are short but not fixed in length. Second, modules elongate to fill in the gaps between them (Fig. 10 b). Third, modules overlap by one extending over another (Fig. 10 c). This can be seen as a local increase in actin staining intensity (a knuckle) along a bundle from a top-down perspective or as overlapping modules seen in profile. Fourth, module overlaps seem to elongate (Fig. 10 d) resulting in a thickening of the bundle and filling in between the overlaps. Finally, bundle diameter increases with the subsequent loss of module–module distinctions (Fig. 10 e). This maturation process results in a smooth bundle with no detectable discontinuities. However, the modular components of mature bundles are still detectable in these bundles.

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