A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis

J Cell Biol. 1997 Nov 3;139(3):817-29. doi: 10.1083/jcb.139.3.817.

Abstract

Localization of maternally provided RNAs during oogenesis is required for formation of the antero-posterior axis of the Drosophila embryo. Here we describe a subcellular structure in nurse cells and oocytes which may function as an intracellular compartment for assembly and transport of maternal products involved in RNA localization. This structure, which we have termed "sponge body," consists of ER-like cisternae, embedded in an amorphous electron-dense mass. It lacks a surrounding membrane and is frequently associated with mitochondria. The sponge bodies are not identical to the Golgi complexes. We suggest that the sponge bodies are homologous to the mitochondrial cloud in Xenopus oocytes, a granulo-fibrillar structure that contains RNAs involved in patterning of the embryo. Exuperantia protein, the earliest factor known to be required for the localization of bicoid mRNA to the anterior pole of the Drosophila oocyte, is highly enriched in the sponge bodies but not an essential structural component of these. RNA staining indicates that sponge bodies contain RNA. However, neither the intensity of this staining nor the accumulation of Exuperantia in the sponge bodies is dependent on the amount of bicoid mRNA present in the ovaries. Sponge bodies surround nuage, a possible polar granule precursor. Microtubules and microfilaments are not present in sponge bodies, although transport of the sponge bodies through the cells is implied by their presence in cytoplasmic bridges. We propose that the sponge bodies are structures that, by assembly and transport of included molecules or associated structures, are involved in localization of mRNAs in Drosophila oocytes.

MeSH terms

  • Animals
  • Biological Transport / genetics
  • Body Patterning / genetics
  • Body Patterning / physiology*
  • Drosophila Proteins*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / physiology*
  • Drosophila melanogaster / ultrastructure
  • Egg Proteins / chemistry
  • Egg Proteins / genetics
  • Egg Proteins / metabolism
  • Female
  • Gene Dosage
  • Golgi Apparatus / physiology
  • Intracellular Fluid / chemistry
  • Intracellular Fluid / metabolism
  • Intracellular Fluid / physiology
  • Microtubules / physiology
  • Oogenesis / genetics
  • Oogenesis / physiology*
  • Organelles / genetics
  • Organelles / physiology*
  • Organelles / ultrastructure
  • Ovary / physiology
  • RNA / analysis
  • RNA-Binding Proteins / chemistry
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism

Substances

  • Drosophila Proteins
  • Egg Proteins
  • RNA-Binding Proteins
  • exu protein, Drosophila
  • RNA