Function and dynamics of slam in furrow formation in early Drosophila embryo

Dev Biol. 2014 Feb 15;386(2):371-84. doi: 10.1016/j.ydbio.2013.12.022. Epub 2013 Dec 22.

Abstract

The Drosophila embryo undergoes a developmental transition in the blastoderm stage switching from syncytial to cellular development. The cleavage furrow, which encloses nuclei into cells, is a prominent morphological feature of this transition. It is not clear how the pattern of the furrow array is defined and how zygotic genes trigger the formation and invagination of interphase furrows. A key to these questions is provided by the gene slam, which has been previously implicated in controlling furrow invagination. Here we investigate the null phenotype of slam, the dynamics of Slam protein, and its control by the recycling endosome. We find that slam is essential for furrow invagination during cellularisation and together with nullo, for specification of the furrow. During cellularisation, Slam marks first the furrow, which is derived from the metaphase furrow of the previous mitosis. Slightly later, Slam accumulates at new furrows between daughter cells early in interphase. Slam is stably associated with the furrow canal except for the onset of cellularisation as revealed by FRAP experiments. Restriction of Slam to the furrow canal and Slam mobility during cellularisation is controlled by the recycling endosome and centrosomes. We propose a three step model. The retracting metaphase furrow leaves an initial mark. This mark and the border between corresponding daughter nuclei are refined by vesicular transport away from pericentrosomal recycling endosome towards the margins of the somatic buds. Following the onset of zygotic gene expression, Slam and Nullo together stabilise this mark and Slam triggers invagination of the cleavage furrow.

Keywords: Blastoderm; Cellularization; Centrosome; Cleavage furrow; Drosophila; Endosome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Centrosome / metabolism
  • Cleavage Stage, Ovum / physiology*
  • Cloning, Molecular
  • Cytoskeletal Proteins / metabolism*
  • Drosophila / embryology*
  • Drosophila / metabolism
  • Drosophila Proteins / metabolism*
  • Embryo, Nonmammalian / metabolism
  • Embryo, Nonmammalian / physiology
  • Fluorescence Recovery After Photobleaching
  • Gene Expression Regulation, Developmental / genetics
  • Gene Expression Regulation, Developmental / physiology*
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Membrane Proteins
  • Microinjections
  • Models, Biological
  • Time-Lapse Imaging

Substances

  • Adaptor Proteins, Signal Transducing
  • Cytoskeletal Proteins
  • Drosophila Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Rip11 protein, Drosophila
  • Slam protein, Drosophila
  • nullo protein, Drosophila