zif-1 translational repression defines a second, mutually exclusive OMA function in germline transcriptional repression

Tugba Guven-Ozkan, Scott M. Robertson, Yuichi Nishi, Rueyling Lin

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

Specification of primordial germ cells requires global repression of transcription. In C. elegans, primordial germ cells are generated through four rounds of asymmetric divisions, starting from the zygote P0, each producing a transcriptionally repressed germline blastomere (P1-P4). Repression in P2-P4 requires PIE-1, which is provided maternally in oocytes and segregated to all germline blastomeres. We have shown previously that OMA-1 and OMA-2 repress global transcription in P0 and P1 by sequestering TAF-4, an essential component of TFIID. Soon after the first mitotic cycle, OMA proteins undergo developmentally regulated degradation. Here, we show that OMA proteins also repress transcription in P2-P4 indirectly, through a completely different mechanism that operates in oocytes. OMA proteins bind to both the 3′ UTR of the zif-1 transcript and the eIF4E-binding protein, SPN-2, repressing translation of zif-1 mRNA in oocytes. zif-1 encodes the substrate-binding subunit of the E3 ligase for PIE-1 degradation. Inhibition of zif-1 translation in oocytes ensures high PIE-1 levels in oocytes and germline blastomeres. The two OMA protein functions are strictly regulated in both space and time by MBK-2, a kinase activated following fertilization. Phosphorylation by MBK-2 facilitates the binding of OMA proteins to TAF-4 and simultaneously inactivates their function in repressing zif-1 translation. Phosphorylation of OMA proteins displaces SPN-2 from the zif-1 3′ UTR, releasing translational repression. We propose that MBK-2 phosphorylation serves as a developmental switch, converting OMA proteins from specific translational repressors in oocytes to global transcriptional repressors in embryos, together effectively repressing transcription in all germline blastomeres.

Original languageEnglish (US)
Pages (from-to)3373-3382
Number of pages10
JournalDevelopment
Volume137
Issue number20
DOIs
StatePublished - Oct 15 2010

Fingerprint

Oocytes
Blastomeres
Proteins
Phosphorylation
3' Untranslated Regions
Germ Cells
Carrier Proteins
Transcription Factor TFIID
Ubiquitin-Protein Ligases
Zygote
Fertilization
Phosphotransferases
Embryonic Structures
Messenger RNA

Keywords

  • C. Elegans
  • Germline
  • MBK-2
  • Oma proteins
  • Oocyte-to-embryo transition
  • Translational repression
  • Zif-1

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology
  • Medicine(all)

Cite this

zif-1 translational repression defines a second, mutually exclusive OMA function in germline transcriptional repression. / Guven-Ozkan, Tugba; Robertson, Scott M.; Nishi, Yuichi; Lin, Rueyling.

In: Development, Vol. 137, No. 20, 15.10.2010, p. 3373-3382.

Research output: Contribution to journalArticle

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