Integrin-dependent apposition of Drosophila extraembryonic membranes promotes morphogenesis and prevents anoikis

Curr Biol. 2004 Mar 9;14(5):372-80. doi: 10.1016/j.cub.2004.02.029.

Abstract

Background: Two extraembryonic tissues form early in Drosophila development. One, the amnioserosa, has been implicated in the morphogenetic processes of germ band retraction and dorsal closure. The developmental role of the other, the yolk sac, is obscure.

Results: By using live-imaging techniques, we report intimate interactions between the amnioserosa and the yolk sac during germ band retraction and dorsal closure. These tissue interactions fail in a subset of myospheroid (mys: betaPS integrin) mutant embryos, leading to failure of germ band retraction and dorsal closure. The Drosophila homolog of mammalian basigin (EMMPRIN, CD147)-an integrin-associated transmembrane glycoprotein-is highly enriched in the extraembryonic tissues. Strong dominant genetic interactions between basigin and mys mutations cause severe defects in dorsal closure, consistent with basigin functioning together with betaPS integrin in extraembryonic membrane apposition. During normal development, JNK signaling is upregulated in the amnioserosa, as midgut closure disrupts contact with the yolk sac. Subsequently, the amnioserosal epithelium degenerates in a process that is independent of the reaper, hid, and grim cell death genes. In mys mutants that fail to establish contact between the extraembryonic membranes, the amnioserosa undergoes premature disintegration and death.

Conclusions: Intimate apposition of the amnioserosa and yolk sac prevents anoikis of the amnioserosa. Survival of the amnioserosa is essential for germ band retraction and dorsal closure. We hypothesize that during normal development, loss of integrin-dependent contact between the extraembryonic tissues results in JNK-dependent amnioserosal disintegration and death, thus representing an example of developmentally programmed anoikis.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Anoikis / physiology*
  • Antigens, CD*
  • Antigens, Neoplasm*
  • Basigin
  • Conserved Sequence
  • Drosophila / embryology*
  • Drosophila / genetics
  • Drosophila / metabolism
  • Embryo, Nonmammalian / metabolism
  • Embryo, Nonmammalian / ultrastructure
  • Immunohistochemistry
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Membranes / embryology
  • Membranes / metabolism
  • Microscopy, Electron
  • Molecular Sequence Data
  • Morphogenesis / physiology
  • Mutation / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Alignment
  • Yolk Sac / metabolism*

Substances

  • Antigens, CD
  • Antigens, Neoplasm
  • Membrane Glycoproteins
  • Basigin