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Originally published In Press as doi:10.1074/jbc.M207442200 on September 26, 2002

J. Biol. Chem., Vol. 277, Issue 49, 47938-47945, December 6, 2002
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Identification of a Multifunctional Binding Site on Ubc9p Required for Smt3p Conjugation*

Kalman P. BencsathDagger , Michael S. PodgorskiDagger , Vishwajeeth R. Pagala§, Clive A. Slaughter§, and Brenda A. SchulmanDagger ||

From the Dagger  Department of Structural Biology, § Hartwell Center for Bioinformatics and Biotechnology, and  Department of Genetics/Tumor Cell Biology, St. Jude Children's Research Hospital, Memphis, Tennessee 38105

Ubiquitin-like proteins (ub-lps) are conjugated by a conserved enzymatic pathway, involving ATP-dependent activation at the C terminus by an activating enzyme (E1) and formation of a thiolester intermediate with a conjugating enzyme (E2) prior to ligation to the target. Ubc9, the E2 for SUMO, synthesizes polymeric chains in the presence of its E1 and MgATP. To better understand conjugation of ub-lps, we have performed mutational analysis of Saccharomyces cerevisiae Ubc9p, which conjugates the SUMO family member Smt3p. We have identified Ubc9p surfaces involved in thiolester bond and Smt3p-Smt3p chain formation. The residues involved in thiolester bond formation map to a surface we show is the E1 binding site, and E2s for other ub-lps are likely to bind to their E1s at a homologous site. We also find that this same surface binds Smt3p. A mutation that impairs binding to E1 but not Smt3p impairs thiolester bond formation, suggesting that it is the E1 interaction at this site that is crucial. Interestingly, other E2s and their relatives also use this same surface for binding to ubiquitin, E3s, and other proteins, revealing this to be a multipurpose binding site and suggesting that the entire E1-E2-E3 pathway has coevolved for a given ub-lp.

* This work was supported in part by American Lebanese Syrian Associated Charities, Developmental Funds from St. Jude Cancer Center Core Grant NCI 2 P30 CA 21765-24-25, a Special Fellowship from the Leukemia and Lymphoma Society, and the Pew Scholars Program in Biomedical Sciences.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

|| To whom correspondence should be addressed: Dept. of Structural Biology, MS #311, St. Jude Children's Research Hospital, 332 N. Lauderdale, Memphis, TN 38105. Tel.: 901-495-5147; Fax: 901-495-5060; E-mail: Brenda.schulman@stjude.org.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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