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J. Biol. Chem., Vol. 278, Issue 36, 34309-34319, September 5, 2003

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Proteomic Analysis of Human Nop56p-associated Pre-ribosomal Ribonucleoprotein Complexes

POSSIBLE LINK BETWEEN Nop56p AND THE NUCLEOLAR PROTEIN TREACLE RESPONSIBLE FOR TREACHER COLLINS SYNDROME^*,

Toshiya Hayano  , Mitsuaki Yanagida  , Yoshio Yamauchi  ¶, Takashi Shinkawa ¶, Toshiaki Isobe  ¶ and Nobuhiro Takahashi   ||

From the Department of Applied Biological Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Integrated Proteomics System Project, Pioneer Research on Genome the Frontier, Ministry of Education, Culture, Sports, Science & Technology of Japan, and the ^¶Department of Chemistry, Graduate School of Science, Tokyo Metropolitan University, 1-1 Minami-ohsawa, Hachioji, Tokyo 192-0397, Japan

Nop56p is a component of the box C/D small nucleolar ribonucleoprotein complexes that direct 2'-O-methylation of pre-rRNA during its maturation. Genetic analyses in yeast have shown that Nop56p plays important roles in the early steps of pre-rRNA processing. However, its precise function remains elusive, especially in higher eukaryotes. Here we describe the proteomic characterization of human Nop56p (hNop56p)-associated pre-ribosomal ribonucleoprotein complexes. Mass spectrometric analysis of purified pre-ribosomal ribonucleoprotein complexes identified 61 ribosomal proteins, 16 trans-acting factors probably involved in ribosome biogenesis, and 29 proteins whose function in ribosome biogenesis is unknown. Identification of pre-rRNA species within hNop56p-associated pre-ribosomal ribonucleoprotein complexes, coupled with the known functions of yeast orthologs of the probable trans-acting factors identified in human, demonstrated that hNop56p functions in the early to middle stages of 60 S subunit synthesis in human cells. Interestingly, the nucleolar phosphoprotein treacle, which is responsible for the craniofacial disorder associated with Treacher Collins syndrome, was found to be a constituent of hNop56p-associated pre-rRNP complexes. The association of hNop56p and treacle within the complexes was independent of rRNA integrity, indicating a direct interaction. In addition, the protein compositions of the treacle-associated and hNop56p-associated pre-ribosomal ribonucleoprotein complexes were very similar, suggesting functional similarities between these two complexes with respect to ribosome biogenesis in human cells.

Received for publication, April 24, 2003 , and in revised form, May 27, 2003.

^* This work was supported by a Pioneer Research on Genome the Frontier, Ministry of Education, Culture, Sports, Science & Technology of Japan. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains Tables I, II, III and Fig. 1.

^|| To whom correspondence should be addressed: Dept. of Applied Biological Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Japan. Tel./Fax: 81-042-367-5709; E-mail: ntakahas{at}cc.tuat.ac.jp.

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