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J. Biol. Chem., Vol. 280, Issue 6, 4289-4298, February 11, 2005

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Specificity Changes in the Evolution of Type II Restriction Endonucleases

A BIOCHEMICAL AND BIOINFORMATIC ANALYSIS OF RESTRICTION ENZYMES THAT RECOGNIZE UNRELATED SEQUENCES^*

Vera Pingoud, Anna Sudina¶, Hildegard Geyer||, Janusz M. Bujnicki**, Rudi Lurz, Gerhild Lüder, Richard Morgan¶¶, Elena Kubareva¶, and Alfred Pingoud

From the Institut für Biochemie, Justus-Liebig-Universität, Heinrich-Buff-Ring 58, D-35392 Giessen, Germany, the ^¶A. N. Belozersky Institute of Physico-chemical Biology and Chemistry Department, Moscow State University, Moscow 119899, Russia, the ^||Biochemisches Institut, Justus-Liebig-Universität, Friedrichstrasse 24, D-35392 Giessen, Germany, the ^**Bioinformatics Laboratory, International Institute of Molecular and Cell Biology, Trojdena 4, 02-108 Warsaw, Poland, the Max-Planck-Institut für Molekulare Genetik, Ihnestrasse 63-73, D-14195 Berlin, Germany, and ^¶¶New England Biolabs, Beverly, Massachusetts 01915

How restriction enzymes with their different specificities and mode of cleavage evolved has been a long standing question in evolutionary biology. We have recently shown that several Type II restriction endonucleases, namely SsoII (CCNGG), PspGI (CCWGG), Eco-RII (CCWGG), NgoMIV (GCCGGC), and Cfr10I (RCCGGY), which recognize similar DNA sequences (as indicated, where the downward arrows denote cleavage position), share limited sequence similarity over an interrupted stretch of 70 amino acid residues with MboI, a Type II restriction endonuclease from Moraxella bovis (Pingoud, V., Conzelmann, C., Kinzebach, S., Sudina, A., Metelev, V., Kubareva, E., Bujnicki, J. M., Lurz, R., Luder, G., Xu, S. Y., and Pingoud, A. (2003) J. Mol. Biol. 329, 913–929). Nevertheless, MboI has a dissimilar DNA specificity (GATC) compared with these enzymes. In this study, we characterize MboI in detail to determine whether it utilizes a mechanism of DNA recognition similar to SsoII, PspGI, EcoRII, NgoMIV, and Cfr10I. Mutational analyses and photocross-linking experiments demonstrate that MboI exploits the stretch of 70 amino acids for DNA recognition and cleavage. It is therefore likely that MboI shares a common evolutionary origin with SsoII, PspGI, EcoRII, NgoMIV, and Cfr10I. This is the first example of a relatively close evolutionary link between Type II restriction enzymes of widely different specificities.

Received for publication, August 6, 2004 , and in revised form, November 22, 2004.

^* This work was supported by the Deutsche Forschungsgemeinschaft (Grants Pi 122/13-4 and SFB535,Z1), the Fonds der Chemischen Industrie, the Deutscher Akademischer Austauschdienst (International Quality Network Biochemistry of Nucleic Acids), Grant 07.03.066 from the State Program Universities of Russia, and Grant 3P04A001124 from the State Committee for Scientific Research in Poland. 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.

This report is dedicated to Prof. Dr. G. Maass on the occasion of his 70th birthday.

An EMBO/Howard Hughes Medical Institute Young Investigator and a Recipient of the fellowship for young scientists from the Foundation for Polish Science.

To whom correspondence should be addressed: Tel.: 49-641-99-35402; Fax.: 49-641-99-35409; E-mail: vera.pingoud{at}chemie.bio.uni-giessen.de.

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