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Molecular and Cellular Biology, July 2004, p. 5687-5693, Vol. 24, No. 13
0270-7306/04/$08.00+0     DOI: 10.1128/MCB.24.13.5687-5693.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Efficient and Error-Free Replication Past a Minor-Groove DNA Adduct by the Sequential Action of Human DNA Polymerases {iota} and {kappa}

M. Todd Washington,1,{dagger} Irina G. Minko,2 Robert E. Johnson,1 William T. Wolfle,1 Thomas M. Harris,3 R. Stephen Lloyd,2 Satya Prakash,1 and Louise Prakash1*

Sealy Center for Molecular Science, University of Texas Medical Branch at Galveston, Galveston, Texas 77555-1061,1 Center for Research in Occupational and Environmental Toxicology, Oregon Health and Science University, Portland, Oregon 97239,2 Department of Chemistry, Center in Molecular Toxicology, Vanderbilt University, Nashville, Tennessee 372353

Received 1 March 2004/ Returned for modification 25 March 2004/ Accepted 1 April 2004

DNA polymerase {iota} (Pol{iota}) is a member of the Y family of DNA polymerases, which promote replication through DNA lesions. The role of Pol{iota} in lesion bypass, however, has remained unclear. Pol{iota} is highly unusual in that it incorporates nucleotides opposite different template bases with very different efficiencies and fidelities. Since interactions of DNA polymerases with the DNA minor groove provide for the nearly equivalent efficiencies and fidelities of nucleotide incorporation opposite each of the four template bases, we considered the possibility that Pol{iota} differs from other DNA polymerases in not being as sensitive to distortions of the minor groove at the site of the incipient base pair and that this enables it to incorporate nucleotides opposite highly distorting minor-groove DNA adducts. To check the validity of this idea, we examined whether Pol{iota} could incorporate nucleotides opposite the {gamma}-HOPdG adduct, which is formed from an initial reaction of acrolein with the N2 of guanine. We show here that Pol{iota} incorporates a C opposite this adduct with nearly the same efficiency as it does opposite a nonadducted template G residue. The subsequent extension step, however, is performed by Pol{kappa}, which efficiently extends from the C incorporated opposite the adduct. Based upon these observations, we suggest that an important biological role of Pol{iota} and Pol{kappa} is to act sequentially to carry out the efficient and accurate bypass of highly distorting minor-groove DNA adducts of the purine bases.

* Corresponding author. Mailing address: University of Texas Medical Branch, Sealy Center for Molecular Science, 6.104 Blocker Medical Research Building, 11th and Mechanic St., Galveston, TX 77555-1061. Phone: (409) 747-8601. Fax: (409) 747-8608. E-mail: l.prakash{at}utmb.edu.

{dagger} Present address: Department of Biochemistry, University of Iowa, Iowa City, IA 52242-1109.

Molecular and Cellular Biology, July 2004, p. 5687-5693, Vol. 24, No. 13
0022-538X/04/$08.00+0     DOI: 10.1128/MCB.24.13.5687-5693.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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