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The 3′ Pol II pausing at replication-dependent histone genes is regulated by Mediator through Cajal bodies’ association with histone locus bodies

Author

Listed:
  • Hidefumi Suzuki

    (Yokohama City University Graduate School of Medical Science)

  • Ryota Abe

    (Yokohama City University Graduate School of Medical Science)

  • Miho Shimada

    (Yokohama City University Graduate School of Medical Science)

  • Tomonori Hirose

    (Yokohama City University Graduate School of Medical Science)

  • Hiroko Hirose

    (Yokohama City University Graduate School of Medical Science)

  • Keisuke Noguchi

    (Yokohama City University Graduate School of Medical Science)

  • Yoko Ike

    (Yokohama City University Graduate School of Medical Science)

  • Nanami Yasui

    (Yokohama City University Graduate School of Medical Science)

  • Kazuki Furugori

    (Yokohama City University Graduate School of Medical Science)

  • Yuki Yamaguchi

    (Tokyo Institute of Technology)

  • Atsushi Toyoda

    (National Institute of Genetics)

  • Yutaka Suzuki

    (The University of Tokyo)

  • Tatsuro Yamamoto

    (The Cancer Institute of JFCR)

  • Noriko Saitoh

    (The Cancer Institute of JFCR)

  • Shigeo Sato

    (Stowers Institute for Medical Research)

  • Chieri Tomomori-Sato

    (Stowers Institute for Medical Research)

  • Ronald C. Conaway

    (Stowers Institute for Medical Research
    University of Kansas Medical Center)

  • Joan W. Conaway

    (Stowers Institute for Medical Research
    University of Kansas Medical Center)

  • Hidehisa Takahashi

    (Yokohama City University Graduate School of Medical Science)

Abstract

Non-polyadenylated mRNAs of replication-dependent histones (RDHs) are synthesized by RNA polymerase II (Pol II) at histone locus bodies (HLBs). HLBs frequently associate with Cajal bodies (CBs), in which 3′-end processing factors for RDH genes are enriched; however, this association’s role in transcription termination of RDH genes remains unclear. Here, we show that Pol II pauses immediately upstream of transcript end sites of RDH genes and Mediator plays a role in this Pol II pausing through CBs’ association with HLBs. Disruption of the Mediator docking site for Little elongation complex (LEC)–Cap binding complex (CBC)–Negative elongation factor (NELF), components of CBs, interferes with CBs’ association with HLBs and 3′ Pol II pausing, resulting in increased aberrant unprocessed RDH gene transcripts. Our findings suggest Mediator’s involvement in CBs’ association with HLBs to facilitate 3′ Pol II pausing and subsequent 3′-end processing of RDH genes by supplying 3′-end processing factors.

Suggested Citation

  • Hidefumi Suzuki & Ryota Abe & Miho Shimada & Tomonori Hirose & Hiroko Hirose & Keisuke Noguchi & Yoko Ike & Nanami Yasui & Kazuki Furugori & Yuki Yamaguchi & Atsushi Toyoda & Yutaka Suzuki & Tatsuro Y, 2022. "The 3′ Pol II pausing at replication-dependent histone genes is regulated by Mediator through Cajal bodies’ association with histone locus bodies," Nature Communications, Nature, vol. 13(1), pages 1-24, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30632-w
    DOI: 10.1038/s41467-022-30632-w
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    References listed on IDEAS

    as
    1. Junichi Yamamoto & Yuri Hagiwara & Kunitoshi Chiba & Tomoyasu Isobe & Takashi Narita & Hiroshi Handa & Yuki Yamaguchi, 2014. "DSIF and NELF interact with Integrator to specify the correct post-transcriptional fate of snRNA genes," Nature Communications, Nature, vol. 5(1), pages 1-10, September.
    2. Qiuyan Wang & Iain A. Sawyer & Myong-Hee Sung & David Sturgill & Sergey P. Shevtsov & Gianluca Pegoraro & Ofir Hakim & Songjoon Baek & Gordon L. Hager & Miroslav Dundr, 2016. "Cajal bodies are linked to genome conformation," Nature Communications, Nature, vol. 7(1), pages 1-17, April.
    3. Hidehisa Takahashi & Amol Ranjan & Shiyuan Chen & Hidefumi Suzuki & Mio Shibata & Tomonori Hirose & Hiroko Hirose & Kazunori Sasaki & Ryota Abe & Kai Chen & Yanfeng He & Ying Zhang & Ichigaku Takigawa, 2020. "The role of Mediator and Little Elongation Complex in transcription termination," Nature Communications, Nature, vol. 11(1), pages 1-20, December.
    4. Hidehisa Takahashi & Ichigaku Takigawa & Masashi Watanabe & Delnur Anwar & Mio Shibata & Chieri Tomomori-Sato & Shigeo Sato & Amol Ranjan & Chris W. Seidel & Tadasuke Tsukiyama & Wataru Mizushima & Ma, 2015. "MED26 regulates the transcription of snRNA genes through the recruitment of little elongation complex," Nature Communications, Nature, vol. 6(1), pages 1-15, May.
    5. Krishanpal Anamika & Àkos Gyenis & Laetitia Poidevin & Olivier Poch & Làszlò Tora, 2012. "RNA Polymerase II Pausing Downstream of Core Histone Genes Is Different from Genes Producing Polyadenylated Transcripts," PLOS ONE, Public Library of Science, vol. 7(6), pages 1-14, June.
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