Complex Formation of Yeast Rev1 and Rev7 Proteins: a Novel Role for the Polymerase-associated Domain

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2005 Oct 18

PMID 16227619

Citations 49

Authors

Narottam Acharya

Lajos Haracska

Robert E Johnson

Ildiko Unk

Satya Prakash

Louise Prakash

Affiliations

Soon will be listed here.

Abstract

The Rev1 protein of Saccharomyces cerevisiae functions in translesion synthesis (TLS) together with DNA polymerase (Pol) zeta, which is comprised of the Rev3 catalytic and the Rev7 accessory subunits. Rev1, a member of the Y family of Pols, differs from other members in its high degree of specificity for incorporating a C opposite template G as well as opposite an abasic site. Although Rev1 is indispensable for Polzeta-dependent TLS, its DNA synthetic activity is not required for many of the Polzeta-dependent lesion bypass events. This observation has suggested a structural role for Rev1 in this process. Here we show that in yeast, Rev1 forms a stable complex with Rev7, and the two proteins copurify. Importantly, the polymerase-associated domain (PAD) of Rev1 mediates its binding to Rev7. These observations reveal a novel role for the PAD region of Rev1 in protein-protein interactions, and they raise the possibility of a similar involvement of the PAD of other Y family Pols in protein-protein interactions. We discuss the possible roles of Rev1 versus the Rev1-Rev7 complex in TLS.

Citing Articles

REV7: a small but mighty regulator of genome maintenance and cancer development.

Maggs L, McVey M Front Oncol. 2025; 14:1516165.

PMID: 39839778 PMC: 11747621. DOI: 10.3389/fonc.2024.1516165.

REV1 coordinates a multi-faceted tolerance response to DNA alkylation damage and prevents chromosome shattering in Drosophila melanogaster.

Khodaverdian V, Sano T, Maggs L, Tomarchio G, Dias A, Tran M PLoS Genet. 2024; 20(7):e1011181.

PMID: 39074150 PMC: 11309488. DOI: 10.1371/journal.pgen.1011181.

REV7 in Cancer Biology and Management.

Murakumo Y, Sakurai Y, Kato T, Hashimoto H, Ichinoe M Cancers (Basel). 2023; 15(6).

PMID: 36980607 PMC: 10046837. DOI: 10.3390/cancers15061721.

Pol32, an accessory subunit of DNA polymerase delta, plays an essential role in genome stability and pathogenesis of .

Patel S, Sahu S, Utkalaja B, Bose S, Acharya N Gut Microbes. 2023; 15(1):2163840.

PMID: 36601868 PMC: 9828637. DOI: 10.1080/19490976.2022.2163840.

Interdomain connecting loop and J loop structures determine cross-species compatibility of PCNA.

Kumari P, Sundaram R, Manohar K, Vasudevan D, Acharya N J Biol Chem. 2021; 297(1):100911.

PMID: 34175309 PMC: 8319368. DOI: 10.1016/j.jbc.2021.100911.

References

Johnson R, Washington M, Prakash S, Prakash L . Fidelity of human DNA polymerase eta. J Biol Chem. 2000; 275(11):7447-50. DOI: 10.1074/jbc.275.11.7447. View

Uljon S, Johnson R, Edwards T, Prakash S, Prakash L, Aggarwal A . Crystal structure of the catalytic core of human DNA polymerase kappa. Structure. 2004; 12(8):1395-404. DOI: 10.1016/j.str.2004.05.011. View

Johnson R, Torres-Ramos C, Izumi T, Mitra S, Prakash S, Prakash L . Identification of APN2, the Saccharomyces cerevisiae homolog of the major human AP endonuclease HAP1, and its role in the repair of abasic sites. Genes Dev. 1998; 12(19):3137-43. PMC: 317187. DOI: 10.1101/gad.12.19.3137. View

Bailly V, Lauder S, Prakash S, Prakash L . Yeast DNA repair proteins Rad6 and Rad18 form a heterodimer that has ubiquitin conjugating, DNA binding, and ATP hydrolytic activities. J Biol Chem. 1997; 272(37):23360-5. DOI: 10.1074/jbc.272.37.23360. View

Lawrence C, CHRISTENSEN R . Ultraviolet-induced reversion of cyc1 alleles in radiation-sensitive strains of yeast. III. rev3 mutant strains. Genetics. 1979; 92(2):397-408. PMC: 1213966. DOI: 10.1093/genetics/92.2.397. View

Mcdonald J, Levine A, Woodgate R . The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics. 1997; 147(4):1557-68. PMC: 1208331. DOI: 10.1093/genetics/147.4.1557. View

Zhou B, Pata J, Steitz T . Crystal structure of a DinB lesion bypass DNA polymerase catalytic fragment reveals a classic polymerase catalytic domain. Mol Cell. 2001; 8(2):427-37. DOI: 10.1016/s1097-2765(01)00310-0. View

Haracska L, Unk I, Johnson R, Johansson E, Burgers P, Prakash S . Roles of yeast DNA polymerases delta and zeta and of Rev1 in the bypass of abasic sites. Genes Dev. 2001; 15(8):945-54. PMC: 312678. DOI: 10.1101/gad.882301. View

Guo C, Fischhaber P, Luk-Paszyc M, Masuda Y, Zhou J, Kamiya K . Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 2003; 22(24):6621-30. PMC: 291821. DOI: 10.1093/emboj/cdg626. View

10.

Lawrence C . Cellular functions of DNA polymerase zeta and Rev1 protein. Adv Protein Chem. 2004; 69:167-203. DOI: 10.1016/S0065-3233(04)69006-1. View

11.

Waters H, Seetharam S, Seidman M, Kraemer K . Ultraviolet hypermutability of a shuttle vector propagated in xeroderma pigmentosum variant cells. J Invest Dermatol. 1993; 101(5):744-8. DOI: 10.1111/1523-1747.ep12371686. View

12.

Lawrence C, Das G, CHRISTENSEN R . REV7, a new gene concerned with UV mutagenesis in yeast. Mol Gen Genet. 1985; 200(1):80-5. DOI: 10.1007/BF00383316. View

13.

Masuda Y, Takahashi M, Tsunekuni N, Minami T, Sumii M, Miyagawa K . Deoxycytidyl transferase activity of the human REV1 protein is closely associated with the conserved polymerase domain. J Biol Chem. 2001; 276(18):15051-8. DOI: 10.1074/jbc.M008082200. View

14.

Masuda Y, Takahashi M, Fukuda S, Sumii M, Kamiya K . Mechanisms of dCMP transferase reactions catalyzed by mouse Rev1 protein. J Biol Chem. 2001; 277(4):3040-6. DOI: 10.1074/jbc.M110149200. View

15.

Haracska L, Prakash S, Prakash L . Yeast Rev1 protein is a G template-specific DNA polymerase. J Biol Chem. 2002; 277(18):15546-51. DOI: 10.1074/jbc.M112146200. View

16.

Murakumo Y, Ogura Y, Ishii H, Numata S, Ichihara M, Croce C . Interactions in the error-prone postreplication repair proteins hREV1, hREV3, and hREV7. J Biol Chem. 2001; 276(38):35644-51. DOI: 10.1074/jbc.M102051200. View

17.

Baynton K, Fuchs R . Distinct roles for Rev1p and Rev7p during translesion synthesis in Saccharomyces cerevisiae. Mol Microbiol. 1999; 34(1):124-33. DOI: 10.1046/j.1365-2958.1999.01583.x. View

18.

Ohashi E, Murakumo Y, Kanjo N, Akagi J, Masutani C, Hanaoka F . Interaction of hREV1 with three human Y-family DNA polymerases. Genes Cells. 2004; 9(6):523-31. DOI: 10.1111/j.1356-9597.2004.00747.x. View

19.

Gibbs P, Borden A, Lawrence C . The T-T pyrimidine (6-4) pyrimidinone UV photoproduct is much less mutagenic in yeast than in Escherichia coli. Nucleic Acids Res. 1995; 23(11):1919-22. PMC: 306963. DOI: 10.1093/nar/23.11.1919. View

20.

Lawrence C, OBrien T, Bond J . UV-induced reversion of his4 frameshift mutations in rad6, rev1, and rev3 mutants of yeast. Mol Gen Genet. 1984; 195(3):487-90. DOI: 10.1007/BF00341451. View