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Originally published In Press as doi:10.1074/jbc.M105481200 on June 19, 2001

J. Biol. Chem., Vol. 276, Issue 33, 31053-31058, August 17, 2001
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Redundant Exonuclease Involvement in Escherichia coli Methyl-directed Mismatch Repair*

Mohan ViswanathanDagger §, Vickers Burdett||, Celia Baitinger||, Paul Modrich||**, and Susan T. LovettDagger Dagger Dagger

From the Dagger  Department of Biology and Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, Massachusetts 02254-9110 and the  Department of Biochemistry and || Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina 27710

Previous biochemical analysis of Escherichia coli methyl-directed mismatch repair implicates three redundant single-strand DNA-specific exonucleases (RecJ, ExoI, and ExoVII) and at least one additional unknown exonuclease in the excision reaction (Cooper, D. L., Lahue, R. S., and Modrich, P. (1993) J. Biol. Chem. 268, 11823-11829). We show here that ExoX also participates in methyl-directed mismatch repair. Analysis of the reaction with crude extracts and purified components demonstrated that ExoX can mediate repair directed from a strand signal 3' of a mismatch. Whereas extracts of all possible single, double, and triple exonuclease mutants displayed significant residual mismatch repair, extracts deficient in RecJ, ExoI, ExoVII, and ExoX exonucleases were devoid of normal repair activity. The RecJ- ExoVII- ExoI- ExoX- strain displayed a 7-fold increase in mutation rate, a significant increase, but less than that observed for other blocks of the mismatch repair pathway. This elevation is epistatic to deficiency for MutS, suggesting an effect via the mismatch repair pathway. Our other work (Burdett, V., Baitinger, C., Viswanathan, M., Lovett, S. T., and Modrich, P. (2001) Proc. Natl. Acad. Sci. U. S. A. 98, 6765-6770) suggests that mutants are under-recovered in the exonuclease-deficient strain due to loss of viability that is triggered by mismatched base pairs in this genetic background. The availability of any one exonuclease is enough to support full mismatch correction, as evident from the normal mutation rates of all triple mutants. Because three of these exonucleases possess a strict polarity of digestion, this suggests that mismatch repair can occur exclusively from a 3' or a 5' direction to the mismatch, if necessary.

* This work was supported by Grants GM43889 (to S. T. L.), GM07122 (to M. V.), and GM23719 (to P. M.) from the General Medical Institute of the National Institutes of Health.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.

§ Present address: Massachusetts Institute of Technology, 68-288D, 77 Massachusetts Ave., Cambridge, MA 02139.

** An Investigator of the Howard Hughes Medical Institute.

Dagger Dagger To whom correspondence should be addressed: Rosenstiel Basic Medical Sciences Research Center, MS029, Waltham, MA 02454-9110. Tel.: 781-736-2497; Fax: 781-736-2405; E-mail lovett@brandeis.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.


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