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Molecular and Cellular Biology, December 2006, p. 9555-9563, Vol. 26, No. 24
0270-7306/06/$08.00+0     doi:10.1128/MCB.01671-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Complex Formation with Rev1 Enhances the Proficiency of Saccharomyces cerevisiae DNA Polymerase {zeta} for Mismatch Extension and for Extension Opposite from DNA Lesions{triangledown}

Narottam Acharya, Robert E. Johnson, Satya Prakash, and Louise Prakash*

Sealy Center for Molecular Science, University of Texas Medical Branch, Galveston, Texas 77555-1061

Received 6 September 2006/ Returned for modification 24 September 2006/ Accepted 27 September 2006

Rev1, a Y family DNA polymerase (Pol) functions together with Pol{zeta}, a B family Pol comprised of the Rev3 catalytic subunit and Rev7 accessory subunit, in promoting translesion DNA synthesis (TLS). Extensive genetic studies with Saccharomyces cerevisiae have indicated a requirement of both Pol{zeta} and Rev1 for damage-induced mutagenesis, implicating their involvement in mutagenic TLS. Pol{zeta} is specifically adapted to promote the extension step of lesion bypass, as it proficiently extends primer termini opposite DNA lesions, and it is also a proficient extender of mismatched primer termini on undamaged DNAs. Since TLS through UV-induced lesions and various other DNA lesions does not depend upon the DNA-synthetic activity of Rev1, Rev1 must contribute to Pol{zeta}-dependent TLS in a nonenzymatic way. Here, we provide evidence for the physical association of Rev1 with Pol{zeta} and show that this binding is mediated through the C terminus of Rev1 and the polymerase domain of Rev3. Importantly, a rev1 mutant that lacks the C-terminal 72 residues which inactivate interaction with Rev3 exhibits the same high degree of UV sensitivity and defectiveness in UV-induced mutagenesis as that conferred by the rev1{Delta} mutation. We propose that Rev1 binding to Pol{zeta} is indispensable for the targeting of Pol{zeta} to the replication fork stalled at a DNA lesion. In addition to this structural role, Rev1 binding enhances the proficiency of Pol{zeta} for the extension of mismatched primer termini on undamaged DNAs and for the extension of primer termini opposite DNA lesions.

* Corresponding author. Mailing address: Sealy Center for Molecular Science, University of Texas Medical Branch at Galveston, 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.

{triangledown} Published ahead of print on 9 October 2006.

Molecular and Cellular Biology, December 2006, p. 9555-9563, Vol. 26, No. 24
0270-7306/06/$08.00+0     doi:10.1128/MCB.01671-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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