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Article

  • The EMBO Journal (2006) 25, 3832 - 3842
  • doi:10.1038/sj.emboj.7601262

Published online: 3 August 2006

TOR regulates late steps of ribosome maturation in the nucleoplasm via Nog1 in response to nutrients

Yoshimi Honma1,a, Aiko Kitamura1,a, Ryo Shioda1,b, Hironori Maruyama1, Kanako Ozaki1, Yoko Oda1, Thierry Mini2, Paul Jenö2, Yasushi Maki3, Kazuyoshi Yonezawa4, Ed Hurt5, Masaru Ueno1,c, Masahiro Uritani1, Michael N Hall2 and Takashi Ushimaru1,2

  1. Faculty of Science, Shizuoka University, Shizuoka, Japan
  2. Department of Biochemistry, Biozentrum, University of Basel, Basel, Switzerland
  3. Department of Biology, Faculty of Science, Niigata University, Niigata, Japan
  4. Biosignal Research Center, Kobe University, Kobe, Japan
  5. Biochemie-Zentrum Heidelberg (BZH), Heidelberg, Germany

Correspondence to:

Takashi Ushimaru, Department of Biology and Geoscience, Faculty of Science, Shizuoka University, Ohya 836, Shizuoka 422-8529, Japan. Tel.: +81 54 238 4772; Fax: +81 54 238 0986; E-mail: sbtushi@ipc.shizuoka.ac.jp

aThese authors contributed equally to this work

bPresent address: Department of Biochemistry, Biozentrum, University of Basel, Klingelbergstrasse 70, 4056 Basel, Switzerland

cPresent address: Department of Molecular Biotechnology, Graduate School of Advanced Sciences of Matter, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima 739-8530, Japan

Received 23 August 2005; Accepted 6 May 2006

The protein kinase TOR (target of rapamycin) controls several steps of ribosome biogenesis, including gene expression of rRNA and ribosomal proteins, and processing of the 35S rRNA precursor, in the budding yeast Saccharomyces cerevisiae. Here we show that TOR also regulates late stages of ribosome maturation in the nucleoplasm via the nuclear GTP-binding protein Nog1. Nog1 formed a complex that included 60S ribosomal proteins and pre-ribosomal proteins Nop7 and Rlp24. The Nog1 complex shuttled between the nucleolus and the nucleoplasm for ribosome biogenesis, but it was tethered to the nucleolus by both nutrient depletion and TOR inactivation, causing cessation of the late stages of ribosome biogenesis. Furthermore, after this, Nog1 and Nop7 proteins were lost, leading to complete cessation of ribosome maturation. Thus, the Nog1 complex is a critical regulator of ribosome biogenesis mediated by TOR. This is the first description of a physiological regulation of nucleolus-to-nucleoplasm translocation of pre-ribosome complexes.

  • Keywords:

    • Nog1,
    • nucleolus,
    • rapamycin,
    • ribosome maturation,
    • TOR