Phosphorylation of the SQ H2A.X motif is required for proper meiosis and mitosis in Tetrahymena thermophila

Xiaoyuan Song, Elizabeta Gjoneska, Qinghu Ren, Sean Dixon Taverna, C. David Allis, Martin A. Gorovsky

Research output: Contribution to journalArticle

Abstract

Phosphorylation of the C terminus SQ motif that defines H2A.X variants is required for efficient DNA double-strand break (DSB) repair in diverse organisms but has not been studied in ciliated protozoa. Tetrahymena H2A.X is one of two similarly expressed major H2As, thereby differing both from mammals, where H2A.X is a quantitatively minor component, and from Saccharomyces cerevisiae where it is the only type of major H2A. Tetrahymena H2A.X is phosphorylated in the SQ motif in both the mitotic micronucleus and the amitotic macronucleus in response to DSBs induced by chemical agents and in the micronucleus during prophase of meiosis, which occurs in the absence of a synaptonemal complex. H2A.X is phosphorylated when programmed DNA rearrangements occur in developing macronuclei, as for immunoglobulin gene rearrangements in mammals, but not during the DNA fragmentation that accompanies breakdown of the parental macronucleus during conjugation, correcting the previous interpretation that this process is apoptosis-like. Using strains containing a mutated (S134A) SQ motif, we demonstrate that phosphorylation of this motif is important for Tetrahymena cells to recover from exogenous DNA damage and is required for normal micronuclear meiosis and mitosis and, to a lesser extent, for normal amitotic macronuclear division; its absence, while not lethal, leads to the accumulation of DSBs in both micro- and macronuclei. These results demonstrate multiple roles of H2A.X phosphorylation in maintaining genomic integrity in different phases of the Tetrahymena life cycle.

Original languageEnglish (US)
Pages (from-to)2648-2660
Number of pages13
JournalMolecular and Cellular Biology
Volume27
Issue number7
DOIs
StatePublished - Apr 2007
Externally publishedYes

Fingerprint

Macronucleus
Tetrahymena thermophila
Tetrahymena
Meiosis
Mitosis
Phosphorylation
Gene Rearrangement
Mammals
Synaptonemal Complex
Prophase
Immunoglobulin Genes
Double-Stranded DNA Breaks
DNA Fragmentation
Life Cycle Stages
DNA Damage
Saccharomyces cerevisiae
Apoptosis

ASJC Scopus subject areas

  • Molecular Biology
  • Genetics
  • Cell Biology

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Phosphorylation of the SQ H2A.X motif is required for proper meiosis and mitosis in Tetrahymena thermophila. / Song, Xiaoyuan; Gjoneska, Elizabeta; Ren, Qinghu; Taverna, Sean Dixon; Allis, C. David; Gorovsky, Martin A.

In: Molecular and Cellular Biology, Vol. 27, No. 7, 04.2007, p. 2648-2660.

Research output: Contribution to journalArticle

Song, Xiaoyuan ; Gjoneska, Elizabeta ; Ren, Qinghu ; Taverna, Sean Dixon ; Allis, C. David ; Gorovsky, Martin A. / Phosphorylation of the SQ H2A.X motif is required for proper meiosis and mitosis in Tetrahymena thermophila. In: Molecular and Cellular Biology. 2007 ; Vol. 27, No. 7. pp. 2648-2660.
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