Meiosis-Specific Noncoding RNA Mediates Robust Pairing of Homologous Chromosomes in Meiosis

Ding, Da‐Qiao; Okamasa, Kasumi; Yamane, Miho; Tsutsumi, Chihiro; Haraguchi, Tokuko; Yamamoto, Masayuki; Hiraoka, Yasushi

doi:10.1126/science.1219518

Cited by 124 publications

(164 citation statements)

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“…A recent study in mice reported that a DSB-independent mechanism promotes homolog pairing during premeiotic S phase prior to DSB formation (Boateng et al 2013). The molecular mechanism of DSB-independent homolog recognition remains a mystery, although the aggregation of heterochromatin, noncoding RNA, the SPO11 protein, or sequence-specific DNA-binding proteins such as transcription factors are suggested to contribute to this process (Page and Hawley 2004;Barzel and Kupiec 2008;Dombecki et al 2011;Ding et al 2012;Boateng et al 2013).…”

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confidence: 99%

Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes

Ishiguro¹,

et al. 2014

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During meiosis, homologous chromosome (homolog) pairing is promoted by several layers of regulation that include dynamic chromosome movement and meiotic recombination. However, the way in which homologs recognize each other remains a fundamental issue in chromosome biology. Here, we show that homolog recognition or association initiates upon entry into meiotic prophase before axis assembly and double-strand break (DSB) formation. This homolog association develops into tight pairing only during or after axis formation. Intriguingly, the ability to recognize homologs is retained in Sun1 knockout spermatocytes, in which telomere-directed chromosome movement is abolished, and this is the case even in Spo11 knockout spermatocytes, in which DSB-dependent DNA homology search is absent. Disruption of meiosis-specific cohesin RAD21L precludes the initial association of homologs as well as the subsequent pairing in spermatocytes. These findings suggest the intriguing possibility that homolog recognition is achieved primarily by searching for homology in the chromosome architecture as defined by meiosis-specific cohesin rather than in the DNA sequence itself.

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confidence: 99%

Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes

Ishiguro¹,

et al. 2014

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“…This process relies on the coordinated action of the long noncoding RNA meiRNA and the protein Mei2 (Watanabe and Yamamoto 1994;Yamamoto 2010). During meiosis, Mei2 is phosphorylated and binds to meiRNA, forming a complex that can efficiently sequester Mmi1 from binding to DSR-containing transcripts, thereby inactivating MTREC-mediated degradation (Watanabe and Yamamoto 1994;Harigaya et al 2006;Ding et al 2012). During vegetative growth, Mmi1 colocalizes with Red1, a core subunit of MTREC.…”

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confidence: 99%

The fission yeast MTREC and EJC orthologs ensure the maturation of meiotic transcripts during meiosis

Marayati

Hoskins

Boger

et al. 2016

RNA

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Meiosis is a highly regulated process by which genetic information is transmitted through sexual reproduction. It encompasses unique mechanisms that do not occur in vegetative cells, producing a distinct, well-regulated meiotic transcriptome. During vegetative growth, many meiotic genes are constitutively transcribed, but most of the resulting mRNAs are rapidly eliminated by the Mmi1-MTREC (Mtl1-Red1 core) complex. While Mmi1-MTREC targets premature meiotic RNAs for degradation by the nuclear 3 ′ -5 ′ exoribonuclease exosome during mitotic growth, its role in meiotic gene expression during meiosis is not known. Here, we report that Red5, an essential MTREC component, interacts with pFal1, an ortholog of eukaryotic translation initiation factor eIF4aIII in the fission yeast Schizosaccharomyces pombe. In mammals, together with MAGO (Mnh1), Rnps1, and Y14, elF4AIII (pFal1) forms the core of the exon junction complex (EJC), which is essential for transcriptional surveillance and localization of mature mRNAs. In fission yeast, two EJC orthologs, pFal1 and Mnh1, are functionally connected with MTREC, specifically in the process of meiotic gene expression during meiosis. Although pFal1 interacts with Mnh1, Y14, and Rnps1, its association with Mnh1 is not disrupted upon loss of Y14 or Rnps1. Mutations of Red1, Red5, pFal1, or Mnh1 produce severe meiotic defects; the abundance of meiotic transcripts during meiosis decreases; and mRNA maturation processes such as splicing are impaired. Since studying meiosis in mammalian germline cells is difficult, our findings in fission yeast may help to define the general mechanisms involved in accurate meiotic gene expression in higher eukaryotes.

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“…This 'horse-tail' nuclear movement is essential for promoting homologue pairing [5]. In their live-cell observations of Mei2-GFP, Ding and co-workers noticed that Mei2 dots located at the homologous sme2 loci pair robustly in the early stages of the horse-tail movement, before most other chromo somal loci are paired [1]. When the sme2 locus translocates to another chromosomal site, the robust pairing mechanism also transfers to this new site.…”

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confidence: 99%

“…When the sme2 locus translocates to another chromosomal site, the robust pairing mechanism also transfers to this new site. Inactivation of the promoter in only one sme2 locus of a pair of homologues impairs the robust pairing, suggesting that the transcribed meiRNAs must be tethered to homologous loci for pairing [1].…”

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confidence: 99%

“…Whilst RNA-RNA or RNA-DNA interactions might be involved in the pairing process, there is no evidence to support this, as the RNA interference machinery is dispensable [1]. Chromosome pairing, mediated by non-coding RNA, is reminiscent of the mammalian X chromosome inactivation process, in which the inactive centre of an X chromosome transiently pairs, possibly through a de novo assembled RNA-protein complex [6].…”

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confidence: 99%

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