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NMR structure and dynamics of the C-terminal domain from human Rev1 and its complex with Rev1 interacting region of DNA polymerase η.

Pozhidaeva A, Pustovalova Y, D'Souza S, Bezsonova I, Walker GC, Korzhnev DM
Biochemistry 51 5506-20 (2012)
Cited: 57 times
EuropePMC logo PMID: 22691049

Abstract

Rev1 is a translesion synthesis (TLS) DNA polymerase essential for DNA damage tolerance in eukaryotes. In the process of TLS stalled high-fidelity replicative DNA polymerases are temporarily replaced by specialized TLS enzymes that can bypass sites of DNA damage (lesions), thus allowing replication to continue or postreplicational gaps to be filled. Despite its limited catalytic activity, human Rev1 plays a key role in TLS by serving as a scaffold that provides an access of Y-family TLS polymerases polη, ι, and κ to their cognate DNA lesions and facilitates their subsequent exchange to polζ that extends the distorted DNA primer-template. Rev1 interaction with the other major human TLS polymerases, polη, ι, κ, and the regulatory subunit Rev7 of polζ, is mediated by Rev1 C-terminal domain (Rev1-CT). We used NMR spectroscopy to determine the spatial structure of the Rev1-CT domain (residues 1157-1251) and its complex with Rev1 interacting region (RIR) from polη (residues 524-539). The domain forms a four-helix bundle with a well-structured N-terminal β-hairpin docking against helices 1 and 2, creating a binding pocket for the two conserved Phe residues of the RIR motif that upon binding folds into an α-helix. NMR spin-relaxation and NMR relaxation dispersion measurements suggest that free Rev1-CT and Rev1-CT/polη-RIR complex exhibit μs-ms conformational dynamics encompassing the RIR binding site, which might facilitate selection of the molecular configuration optimal for binding. These results offer new insights into the control of TLS in human cells by providing a structural basis for understanding the recognition of the Rev1-CT by Y-family DNA polymerases.

Reviews - 2lsk mentioned but not cited (8)

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  2. R.I.P. to the PIP: PCNA-binding motif no longer considered specific: PIP motifs and other related sequences are not distinct entities and can bind multiple proteins involved in genome maintenance. Boehm EM, Washington MT. Bioessays 38 1117-1122 (2016)
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Articles - 2lsk mentioned but not cited (8)

  1. Structural basis of recruitment of DNA polymerase ζ by interaction between REV1 and REV7 proteins. Kikuchi S, Hara K, Shimizu T, Sato M, Hashimoto H. J Biol Chem 287 33847-33852 (2012)
  2. NMR structure and dynamics of the C-terminal domain from human Rev1 and its complex with Rev1 interacting region of DNA polymerase η. Pozhidaeva A, Pustovalova Y, D'Souza S, Bezsonova I, Walker GC, Korzhnev DM. Biochemistry 51 5506-5520 (2012)
  3. Interaction between the Rev1 C-Terminal Domain and the PolD3 Subunit of Polζ Suggests a Mechanism of Polymerase Exchange upon Rev1/Polζ-Dependent Translesion Synthesis. Pustovalova Y, Magalhães MT, D'Souza S, Rizzo AA, Korza G, Walker GC, Korzhnev DM. Biochemistry 55 2043-2053 (2016)
  4. Involvement of budding yeast Rad5 in translesion DNA synthesis through physical interaction with Rev1. Xu X, Lin A, Zhou C, Blackwell SR, Zhang Y, Wang Z, Feng Q, Guan R, Hanna MD, Chen Z, Xiao W. Nucleic Acids Res 44 5231-5245 (2016)
  5. Identification of Small Molecule Translesion Synthesis Inhibitors That Target the Rev1-CT/RIR Protein-Protein Interaction. Sail V, Rizzo AA, Chatterjee N, Dash RC, Ozen Z, Walker GC, Korzhnev DM, Hadden MK. ACS Chem Biol 12 1903-1912 (2017)
  6. The C-terminal domain of human Rev1 contains independent binding sites for DNA polymerase η and Rev7 subunit of polymerase ζ. Pustovalova Y, Bezsonova I, Korzhnev DM. FEBS Lett 586 3051-3056 (2012)
  7. XRCC1 interaction with the REV1 C-terminal domain suggests a role in post replication repair. Gabel SA, DeRose EF, London RE. DNA Repair (Amst) 12 1105-1113 (2013)
  8. First report and genetic characterization of bovine torovirus in diarrhoeic calves in China. Shi Z, Wang W, Chen C, Zhang X, Wang J, Xu Z, Lan Y. BMC Vet Res 16 272 (2020)


Reviews citing this publication (13)

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  2. Translesion DNA polymerases in eukaryotes: what makes them tick? Vaisman A, Woodgate R. Crit Rev Biochem Mol Biol 52 274-303 (2017)
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  6. The roles of DNA polymerase ζ and the Y family DNA polymerases in promoting or preventing genome instability. Sharma S, Helchowski CM, Canman CE. Mutat Res 743-744 97-110 (2013)
  7. REV1 and DNA polymerase zeta in DNA interstrand crosslink repair. Sharma S, Canman CE. Environ Mol Mutagen 53 725-740 (2012)
  8. Regulation of translesion DNA synthesis: Posttranslational modification of lysine residues in key proteins. McIntyre J, Woodgate R. DNA Repair (Amst) 29 166-179 (2015)
  9. Translesion DNA Synthesis in Cancer: Molecular Mechanisms and Therapeutic Opportunities. Zafar MK, Eoff RL. Chem Res Toxicol 30 1942-1955 (2017)
  10. DNA Damage Tolerance Pathways in Human Cells: A Potential Therapeutic Target. Ler AAL, Carty MP. Front Oncol 11 822500 (2021)
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Articles citing this publication (28)

  1. Structural basis of Rev1-mediated assembly of a quaternary vertebrate translesion polymerase complex consisting of Rev1, heterodimeric polymerase (Pol) ζ, and Pol κ. Wojtaszek J, Lee CJ, D'Souza S, Minesinger B, Kim H, D'Andrea AD, Walker GC, Zhou P. J Biol Chem 287 33836-33846 (2012)
  2. Rev7 dimerization is important for assembly and function of the Rev1/Polζ translesion synthesis complex. Rizzo AA, Vassel FM, Chatterjee N, D'Souza S, Li Y, Hao B, Hemann MT, Walker GC, Korzhnev DM. Proc Natl Acad Sci U S A 115 E8191-E8200 (2018)
  3. PCNA tool belts and polymerase bridges form during translesion synthesis. Boehm EM, Spies M, Washington MT. Nucleic Acids Res 44 8250-8260 (2016)
  4. REV1-Polζ maintains the viability of homologous recombination-deficient cancer cells through mutagenic repair of PRIMPOL-dependent ssDNA gaps. Taglialatela A, Leuzzi G, Sannino V, Cuella-Martin R, Huang JW, Wu-Baer F, Baer R, Costanzo V, Ciccia A. Mol Cell 81 4008-4025.e7 (2021)
  5. NMR mapping of PCNA interaction with translesion synthesis DNA polymerase Rev1 mediated by Rev1-BRCT domain. Pustovalova Y, Maciejewski MW, Korzhnev DM. J Mol Biol 425 3091-3105 (2013)
  6. The Proliferating Cell Nuclear Antigen (PCNA)-interacting Protein (PIP) Motif of DNA Polymerase η Mediates Its Interaction with the C-terminal Domain of Rev1. Boehm EM, Powers KT, Kondratick CM, Spies M, Houtman JC, Washington MT. J Biol Chem 291 8735-8744 (2016)
  7. Rev1 promotes replication through UV lesions in conjunction with DNA polymerases η, ι, and κ but not DNA polymerase ζ. Yoon JH, Park J, Conde J, Wakamiya M, Prakash L, Prakash S. Genes Dev 29 2588-2602 (2015)
  8. Structural insights into the assembly of human translesion polymerase complexes. Xie W, Yang X, Xu M, Jiang T. Protein Cell 3 864-874 (2012)
  9. Structure and mechanism of B-family DNA polymerase ζ specialized for translesion DNA synthesis. Malik R, Kopylov M, Gomez-Llorente Y, Jain R, Johnson RE, Prakash L, Prakash S, Ubarretxena-Belandia I, Aggarwal AK. Nat Struct Mol Biol 27 913-924 (2020)
  10. The Polymerase Activity of Mammalian DNA Pol ζ Is Specifically Required for Cell and Embryonic Viability. Lange SS, Tomida J, Boulware KS, Bhetawal S, Wood RD. PLoS Genet 12 e1005759 (2016)
  11. FF483-484 motif of human Polη mediates its interaction with the POLD2 subunit of Polδ and contributes to DNA damage tolerance. Baldeck N, Janel-Bintz R, Wagner J, Tissier A, Fuchs RP, Burkovics P, Haracska L, Despras E, Bichara M, Chatton B, Cordonnier AM. Nucleic Acids Res 43 2116-2125 (2015)
  12. Ubiquitin mediates the physical and functional interaction between human DNA polymerases η and ι. McIntyre J, Vidal AE, McLenigan MP, Bomar MG, Curti E, McDonald JP, Plosky BS, Ohashi E, Woodgate R. Nucleic Acids Res 41 1649-1660 (2013)
  13. Structure and functional analysis of the BRCT domain of translesion synthesis DNA polymerase Rev1. Pryor JM, Gakhar L, Washington MT. Biochemistry 52 254-263 (2013)
  14. The Protein Level of Rev1, a TLS Polymerase in Fission Yeast, Is Strictly Regulated during the Cell Cycle and after DNA Damage. Uchiyama M, Terunuma J, Hanaoka F. PLoS One 10 e0130000 (2015)
  15. Assembly of a G-Quadruplex Repair Complex by the FANCJ DNA Helicase and the REV1 Polymerase. Lowran K, Campbell L, Popp P, Wu CG. Genes (Basel) 11 E5 (2019)
  16. Non-bulky Lesions in Human DNA: the Ways of Formation, Repair, and Replication. Ignatov AV, Bondarenko KA, Makarova AV. Acta Naturae 9 12-26 (2017)
  17. Rev1 plays central roles in mammalian DNA-damage tolerance in response to UV irradiation. Niu X, Chen W, Bi T, Lu M, Qin Z, Xiao W. FEBS J 286 2711-2725 (2019)
  18. A hand-off of DNA between archaeal polymerases allows high-fidelity replication to resume at a discrete intermediate three bases past 8-oxoguanine. Cranford MT, Kaszubowski JD, Trakselis MA. Nucleic Acids Res 48 10986-10997 (2020)
  19. Phosphorylation Alters the Properties of Pol η: Implications for Translesion Synthesis. Peddu C, Zhang S, Zhao H, Wong A, Lee EYC, Lee MYWT, Zhang Z. iScience 6 52-67 (2018)
  20. Structural Basis for the Interaction of Mutasome Assembly Factor REV1 with Ubiquitin. Cui G, Botuyan MV, Mer G. J Mol Biol 430 2042-2050 (2018)
  21. Virtual Pharmacophore Screening Identifies Small-Molecule Inhibitors of the Rev1-CT/RIR Protein-Protein Interaction. Dash RC, Ozen Z, McCarthy KR, Chatterjee N, Harris CA, Rizzo AA, Walker GC, Korzhnev DM, Hadden MK. ChemMedChem 14 1610-1617 (2019)
  22. REV1 Inhibition Enhances Radioresistance and Autophagy. Ikeh KE, Lamkin EN, Crompton A, Deutsch J, Fisher KJ, Gray M, Argyle DJ, Lim WY, Korzhnev DM, Hadden MK, Hong J, Zhou P, Chatterjee N. Cancers (Basel) 13 5290 (2021)
  23. Structure-Based Drug Design of Phenazopyridine Derivatives as Inhibitors of Rev1 Interactions in Translesion Synthesis. McPherson KS, Zaino AM, Dash RC, Rizzo AA, Li Y, Hao B, Bezsonova I, Hadden MK, Korzhnev DM. ChemMedChem 16 1126-1132 (2021)
  24. Yeast DNA polymerase η possesses two PIP-like motifs that bind PCNA and Rad6-Rad18 with different specificities. Ripley BM, Reusch DT, Washington MT. DNA Repair (Amst) 95 102968 (2020)
  25. Evaluation and modulation of DNA lesion bypass in an SV40 large T antigen-based in vitro replication system. Szeltner Z, Póti Á, Harami GM, Kovács M, Szüts D. FEBS Open Bio 11 1054-1075 (2021)
  26. Determination of DNA lesion bypass using a ChIP-based assay. Wu D, Banerjee A, Cai S, Li N, Han C, Bai X, Zhang J, Wang QE. DNA Repair (Amst) 108 103230 (2021)
  27. Genetic and physical interactions between Polη and Rev1 in response to UV-induced DNA damage in mammalian cells. Bi T, Niu X, Qin C, Xiao W. Sci Rep 11 21364 (2021)
  28. REV1: A novel biomarker and potential therapeutic target for various cancers. Zhu N, Zhao Y, Mi M, Lu Y, Tan Y, Fang X, Weng S, Yuan Y. Front Genet 13 997970 (2022)


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