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Originally published In Press as doi:10.1074/jbc.M413209200 on December 6, 2004

J. Biol. Chem., Vol. 280, Issue 6, 4102-4110, February 11, 2005
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Defining the SUMO-modified Proteome by Multiple Approaches in Saccharomyces cerevisiae*{boxs}

J. Thomas Hannich{ddagger}§, Alaron Lewis{ddagger}||, Mary B. Kroetz{ddagger}**, Shyr-Jiann Li{ddagger}{ddagger}{ddagger}, Heinrich Heide§§, Andrew Emili§§, and Mark Hochstrasser{ddagger}¶¶

From the {ddagger}Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520-8114 and the §§Banting & Best Department of Medical Research, University of Toronto, Toronto, Ontario M5G 1L6, Canada

SUMO, or Smt3 in Saccharomyces cerevisiae, is a ubiquitin-like protein that is post-translationally attached to multiple proteins in vivo. Many of these substrate modifications are cell cycle-regulated, and SUMO conjugation is essential for viability in most eukaryotes. However, only a limited number of SUMO-modified proteins have been definitively identified to date, and this has hampered study of the mechanisms by which SUMO ligation regulates specific cellular pathways. Here we use a combination of yeast two-hybrid screening, a high copy suppressor selection with a SUMO isopeptidase mutant, and tandem mass spectrometry to define a large set of proteins (>150) that can be modified by SUMO in budding yeast. These three approaches yielded overlapping sets of proteins with the most extensive set by far being those identified by mass spectrometry. The two-hybrid data also yielded a potential SUMO-binding motif. Functional categories of SUMO-modified proteins include SUMO conjugation system enzymes, chromatin- and gene silencing-related factors, DNA repair and genome stability proteins, stress-related proteins, transcription factors, proteins involved in translation and RNA metabolism, and a variety of metabolic enzymes. The results point to a surprisingly broad array of cellular processes regulated by SUMO conjugation and provide a starting point for detailed studies of how SUMO ligation contributes to these different regulatory mechanisms.

Received for publication, November 23, 2004

* This work was supported in part by National Institutes of Health Grant GM53756 (to M. H.) and grants from the Protein Engineering Network Centre of Excellence of Canada and the National Science and Engineering Research Council of Canada (to A. E.). 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.

{boxs} The on-line version of this article (available at http://www.jbc.org) contains an additional table.

§ Supported in part by a Studienstiftung des Deutschen Volkes Fellowship.

Present address: JTH, MPI-CBG, Dresden 01307, Germany.

|| Supported in part by National Institutes of Health Grant GM007223.

** Supported in part by a National Science Foundation predoctoral fellowship.

{ddagger}{ddagger} Present address: Celera, S. San Francisco, CA 94080.

¶¶ To whom correspondence should be addressed: Dept. of Molecular Biophysics and Biochemistry, Yale University, 266 Whitney Ave., New Haven, CT 06520-8114. Tel.: 203-432-5101; Fax: 203-432-5175; E-mail: mark.hochstrasser{at}yale.edu.




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