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Originally published In Press as doi:10.1074/jbc.M204826200 on July 3, 2002

J. Biol. Chem., Vol. 277, Issue 37, 34198-34207, September 13, 2002
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Fidelity of Escherichia coli DNA Polymerase IV
PREFERENTIAL GENERATION OF SMALL DELETION MUTATIONS BY dNTP-STABILIZED MISALIGNMENT*

Sawami KobayashiDagger , Michael R. ValentineDagger , Phuong PhamDagger , Mike O'Donnell§, and Myron F. GoodmanDagger

From the Dagger  Department of Biological Sciences and Chemistry, Hedco Molecular Biology Laboratories, University of Southern California, University Park, Los Angeles, California 90089-1340 and the § Rockefeller University and Howard Hughes Medical Institute, New York, New York 10021

Escherichia coli DNA polymerase IV (pol IV), a member of the error-prone Y family, predominantly generates -1 frameshifts when copying DNA in vitro. T right-arrow G transversions and T right-arrow C transitions are the most frequent base substitutions observed. The in vitro data agree with mutational spectra obtained when pol IV is overexpressed in vivo. Single base deletion and base substitution rates measured in the lacZalpha gene in vitro are, on average, 2 × 10-4 and 5 × 10-5, respectively. The range of misincorporation and mismatch extension efficiencies determined kinetically are 10-3 to 10-5. The presence of beta  sliding clamp and gamma -complex clamp loading proteins strongly enhance pol IV processivity but have no discernible influence on fidelity. By analyzing changes in fluorescence of a 2-aminopurine template base undergoing replication in real time, we show that a "dNTP-stabilized" misalignment mechanism is responsible for making -1 frameshift mutations on undamaged DNA. In this mechanism, a dNTP substrate is paired "correctly" opposite a downstream template base, on a "looped out" template strand instead of mispairing opposite a next available template base. By using the same mechanism, pol IV "skips" past an abasic template lesion to generate a -1 frameshift. A crystal structure depicting dNTP-stabilized misalignment was reported recently for Sulfolubus solfataricus Dpo4, a Y family homolog of Escherichia coli pol IV.

* This work was supported by National Institutes of Health Grants GM42554 and GM21422.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 Biological Sciences, University of Southern California, SHS Rm. 172, University Park, Los Angeles, CA 90089-1340. Tel.: 213-740-5190; Fax: 213-740-8631; E-mail: mgoodman@mizar.usc.edu.

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


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