Drosophila Doublefault protein coordinates multiple events during male meiosis by controlling mRNA translation

Development. 2019 Nov 18;146(22):dev183053. doi: 10.1242/dev.183053.

Abstract

During the extended prophase of Drosophila gametogenesis, spermatocytes undergo robust gene transcription and store many transcripts in the cytoplasm in a repressed state, until translational activation of select mRNAs in later steps of spermatogenesis. Here, we characterize the Drosophila Doublefault (Dbf) protein as a C2H2 zinc-finger protein, primarily expressed in testes, that is required for normal meiotic division and spermiogenesis. Loss of Dbf causes premature centriole disengagement and affects spindle structure, chromosome segregation and cytokinesis. We show that Dbf interacts with the RNA-binding protein Syncrip/hnRNPQ, a key regulator of localized translation in Drosophila We propose that the pleiotropic effects of dbf loss-of-function mutants are associated with the requirement of dbf function for translation of specific transcripts in spermatocytes. In agreement with this hypothesis, Dbf protein binds cyclin B mRNA and is essential for translation of cyclin B in mature spermatocytes.

Keywords: Centrosome; Cytokinesis; Drosophila; Male meiosis; Spermatogenesis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axoneme / metabolism
  • Cell Nucleus / metabolism
  • Centrosome / metabolism
  • Chromosome Segregation
  • Cloning, Molecular
  • Crosses, Genetic
  • Cyclin B
  • Cytokinesis
  • Drosophila Proteins / genetics
  • Drosophila Proteins / physiology*
  • Drosophila melanogaster / embryology*
  • Gene Expression Regulation, Developmental*
  • In Situ Hybridization, Fluorescence
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Male
  • Meiosis*
  • Microtubules / metabolism
  • Mutation
  • RNA, Messenger / genetics*
  • RNA-Binding Proteins
  • Spermatocytes / metabolism
  • Spermatogenesis*
  • Spindle Apparatus / metabolism
  • Transgenes
  • Zinc Fingers

Substances

  • Cyclin B
  • Drosophila Proteins
  • Intracellular Signaling Peptides and Proteins
  • RNA, Messenger
  • RNA-Binding Proteins
  • Syp protein, Drosophila
  • dbf protein, Drosophila