Maternal Nanos inhibits Importin-α2/Pendulin-dependent nuclear import to prevent somatic gene expression in the Drosophila germline

PLoS Genet. 2019 May 15;15(5):e1008090. doi: 10.1371/journal.pgen.1008090. eCollection 2019 May.

Abstract

Repression of somatic gene expression in germline progenitors is one of the critical mechanisms involved in establishing the germ/soma dichotomy. In Drosophila, the maternal Nanos (Nos) and Polar granule component (Pgc) proteins are required for repression of somatic gene expression in the primordial germ cells, or pole cells. Pgc suppresses RNA polymerase II-dependent global transcription in pole cells, but it remains unclear how Nos represses somatic gene expression. Here, we show that Nos represses somatic gene expression by inhibiting translation of maternal importin-α2 (impα2) mRNA. Mis-expression of Impα2 caused aberrant nuclear import of a transcriptional activator, Ftz-F1, which in turn activated a somatic gene, fushi tarazu (ftz), in pole cells when Pgc-dependent transcriptional repression was impaired. Because ftz expression was not fully activated in pole cells in the absence of either Nos or Pgc, we propose that Nos-dependent repression of nuclear import of transcriptional activator(s) and Pgc-dependent suppression of global transcription act as a 'double-lock' mechanism to inhibit somatic gene expression in germline progenitors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Female
  • Fushi Tarazu Transcription Factors / genetics
  • Fushi Tarazu Transcription Factors / metabolism
  • Gene Expression Regulation, Developmental
  • Male
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Ovary / cytology
  • Ovary / growth & development
  • Ovary / metabolism
  • Ovum / cytology
  • Ovum / metabolism*
  • Positive Transcriptional Elongation Factor B / genetics
  • Positive Transcriptional Elongation Factor B / metabolism
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism
  • Spermatozoa / cytology
  • Spermatozoa / metabolism*
  • Testis / cytology
  • Testis / growth & development
  • Testis / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription, Genetic
  • alpha Karyopherins / genetics*
  • alpha Karyopherins / metabolism

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • Fushi Tarazu Transcription Factors
  • Nuclear Proteins
  • RNA-Binding Proteins
  • Transcription Factors
  • alpha Karyopherins
  • ftz protein, Drosophila
  • karyopherin alpha 2
  • nuclear hormone receptor FTZ-F1, Drosophila
  • pendulin
  • pgc protein, Drosophila
  • nos protein, Drosophila
  • Positive Transcriptional Elongation Factor B
  • RNA Polymerase II

Grant support

This work was supported in part by Grants-in-Aid for Scientific Research on Innovative Areas (grant#25114002 and 18H05552) to SK from Japan Society for the promotion of Science (JSPS) (http://www.jsps.go.jp/english/egrants/ index.html), Grants-in-Aid for Scientific Research (grant#26114508 and 17H03686) to AN from JSPS, research grants from the NOVARTIS Foundation (Japan) for the Promotion of Science, the Takeda Science Foundation and the Mitsubishi Foundation to A.N. K.H.-N. was a JSPS Research Fellow. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.