Blown fuse regulates stretching and outgrowth but not myoblast fusion of the circular visceral muscles in Drosophila

Differentiation. 2006 Dec;74(9-10):608-21. doi: 10.1111/j.1432-0436.2006.00080.x.

Abstract

Circular visceral muscles of Drosophila are binuclear syncytia arising from fusion of two different kinds of myoblasts: a circular visceral founder cell and one visceral fusion-competent myoblast. In contrast to fusion leading to the somatic body-wall musculature, myoblast fusion for the circular visceral muscles does not result in massive syncytia but instead in syncytia interconnected with multiple cytoplasmic bridges, which differentiate into large web-shaped muscles. Here, we show that these syncytial circular visceral muscles build a gut-enclosing network with the interwoven longitudinal visceral muscles. At the ultrastructural level, during circular visceral myoblast fusion and the first step of somatic myoblast fusion prefusion complexes and electron-dense plaques were not detectable which was surprising as these structures are characteristic for the second step of somatic myoblast fusion. Moreover, we demonstrate that Blown fuse (Blow), a cytoplasmic protein essential for the second step of somatic myoblast fusion, plays a different role in circular visceral myogenesis. Blow is known to be essential for progression beyond the prefusion complex in the somatic mesoderm; however, analysis of blow mutants established that it has a restricted role in stretching and outgrowth of the syncytia in the circular visceral muscles. Furthermore, we also found that in the visceral mesoderm, Blow is expressed in both the fusion-competent myoblasts and circular visceral founders, while expression in the somatic mesoderm is initially restricted to fusion-competent myoblasts. We also demonstrate that different enhancer elements in the first intron of blow are responsible for this distinct expression pattern. Thus, we propose a model for Blow in which this protein is involved in at least two clearly differing processes during Drosophila muscle formation, namely somatic myoblast fusion on the one hand and stretching and outgrowth of circular visceral muscles on the other.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila / embryology
  • Drosophila / growth & development*
  • Drosophila / physiology
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila Proteins / physiology*
  • Giant Cells / cytology
  • Giant Cells / physiology
  • Giant Cells / ultrastructure
  • In Situ Hybridization
  • Introns
  • Microfilament Proteins / genetics
  • Microfilament Proteins / physiology
  • Microscopy, Electron, Scanning
  • Models, Biological
  • Morphogenesis
  • Muscle Development*
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism
  • Muscle Proteins / physiology*
  • Muscle, Skeletal / cytology*
  • Muscle, Skeletal / physiology
  • Myoblasts / physiology
  • Myoblasts / ultrastructure*

Substances

  • Drosophila Proteins
  • Microfilament Proteins
  • Muscle Proteins
  • blow protein, Drosophila
  • hem protein, Drosophila