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Structure-function analysis of ribonucleotide bypass by B family DNA replicases.

Clausen AR, Murray MS, Passer AR, Pedersen LC, Kunkel TA
Proc Natl Acad Sci U S A 110 16802-7 (2013)
Related entries: 4khq, 4khs, 4khu, 4khw, 4khy, 4ki6

Cited: 36 times
EuropePMC logo PMID: 24082122

Abstract

Ribonucleotides are frequently incorporated into DNA during replication, they are normally removed, and failure to remove them results in replication stress. This stress correlates with DNA polymerase (Pol) stalling during bypass of ribonucleotides in DNA templates. Here we demonstrate that stalling by yeast replicative Pols δ and ε increases as the number of consecutive template ribonucleotides increases from one to four. The homologous bacteriophage RB69 Pol also stalls during ribonucleotide bypass, with a pattern most similar to that of Pol ε. Crystal structures of an exonuclease-deficient variant of RB69 Pol corresponding to multiple steps in single ribonucleotide bypass reveal that increased stalling is associated with displacement of Tyr391 and an unpreferred C2'-endo conformation for the ribose. Even less efficient bypass of two consecutive ribonucleotides in DNA correlates with similar movements of Tyr391 and displacement of one of the ribonucleotides along with the primer-strand DNA backbone. These structure-function studies have implications for cellular signaling by ribonucleotides, and they may be relevant to replication stress in cells defective in ribonucleotide excision repair, including humans suffering from autoimmune disease associated with RNase H2 defects.

Articles - 4ki4 mentioned but not cited (1)

  1. Structure-function analysis of ribonucleotide bypass by B family DNA replicases. Clausen AR, Murray MS, Passer AR, Pedersen LC, Kunkel TA. Proc Natl Acad Sci U S A 110 16802-16807 (2013)


Reviews citing this publication (11)

  1. Ribonucleotides in DNA: origins, repair and consequences. Williams JS, Kunkel TA. DNA Repair (Amst) 19 27-37 (2014)
  2. Processing ribonucleotides incorporated during eukaryotic DNA replication. Williams JS, Lujan SA, Kunkel TA. Nat Rev Mol Cell Biol 17 350-363 (2016)
  3. DNA Replication-A Matter of Fidelity. Ganai RA, Johansson E. Mol Cell 62 745-755 (2016)
  4. How the misincorporation of ribonucleotides into genomic DNA can be both harmful and helpful to cells. Potenski CJ, Klein HL. Nucleic Acids Res 42 10226-10234 (2014)
  5. The Balancing Act of Ribonucleotides in DNA. Cerritelli SM, Crouch RJ. Trends Biochem Sci 41 434-445 (2016)
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  8. Distribution and effects of amino acid changes in drug-resistant α and β herpesviruses DNA polymerase. Topalis D, Gillemot S, Snoeck R, Andrei G. Nucleic Acids Res 44 9530-9554 (2016)
  9. Mechanisms of damage tolerance and repair during DNA replication. Ashour ME, Mosammaparast N. Nucleic Acids Res 49 3033-3047 (2021)
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  11. One, No One, and One Hundred Thousand: The Many Forms of Ribonucleotides in DNA. Nava GM, Grasso L, Sertic S, Pellicioli A, Muzi Falconi M, Lazzaro F. Int J Mol Sci 21 E1706 (2020)

Articles citing this publication (24)

  1. Tracking replication enzymology in vivo by genome-wide mapping of ribonucleotide incorporation. Clausen AR, Lujan SA, Burkholder AB, Orebaugh CD, Williams JS, Clausen MF, Malc EP, Mieczkowski PA, Fargo DC, Smith DJ, Kunkel TA. Nat Struct Mol Biol 22 185-191 (2015)
  2. Mechanism of Ribonucleotide Incorporation by Human DNA Polymerase η. Su Y, Egli M, Guengerich FP. J Biol Chem 291 3747-3756 (2016)
  3. Altered spatio-temporal dynamics of RNase H2 complex assembly at replication and repair sites in Aicardi-Goutières syndrome. Kind B, Muster B, Staroske W, Herce HD, Sachse R, Rapp A, Schmidt F, Koss S, Cardoso MC, Lee-Kirsch MA. Hum Mol Genet 23 5950-5960 (2014)
  4. Impact of ribonucleotide incorporation by DNA polymerases β and λ on oxidative base excision repair. Crespan E, Furrer A, Rösinger M, Bertoletti F, Mentegari E, Chiapparini G, Imhof R, Ziegler N, Sturla SJ, Hübscher U, van Loon B, Maga G. Nat Commun 7 10805 (2016)
  5. Human DNA polymerase η accommodates RNA for strand extension. Su Y, Egli M, Guengerich FP. J Biol Chem 292 18044-18051 (2017)
  6. Human DNA polymerase η has reverse transcriptase activity in cellular environments. Su Y, Ghodke PP, Egli M, Li L, Wang Y, Guengerich FP. J Biol Chem 294 6073-6081 (2019)
  7. RNase HII Saves rnhA Mutant Escherichia coli from R-Loop-Associated Chromosomal Fragmentation. Kouzminova EA, Kadyrov FF, Kuzminov A. J Mol Biol 429 2873-2894 (2017)
  8. Ribonucleotide incorporation by human DNA polymerase η impacts translesion synthesis and RNase H2 activity. Mentegari E, Crespan E, Bavagnoli L, Kissova M, Bertoletti F, Sabbioneda S, Imhof R, Sturla SJ, Nilforoushan A, Hübscher U, van Loon B, Maga G. Nucleic Acids Res 45 2600-2614 (2017)
  9. Structural and Kinetic Studies of the Effect of Guanine N7 Alkylation and Metal Cofactors on DNA Replication. Kou Y, Koag MC, Lee S. Biochemistry 57 5105-5116 (2018)
  10. A cancer-associated point mutation disables the steric gate of human PrimPol. Díaz-Talavera A, Calvo PA, González-Acosta D, Díaz M, Sastre-Moreno G, Blanco-Franco L, Guerra S, Martínez-Jiménez MI, Méndez J, Blanco L. Sci Rep 9 1121 (2019)
  11. Impact of Ribonucleotide Backbone on Translesion Synthesis and Repair of 7,8-Dihydro-8-oxoguanine. Sassa A, Çağlayan M, Rodriguez Y, Beard WA, Wilson SH, Nohmi T, Honma M, Yasui M. J Biol Chem 291 24314-24323 (2016)
  12. RNase H activities counteract a toxic effect of Polymerase η in cells replicating with depleted dNTP pools. Meroni A, Nava GM, Bianco E, Grasso L, Galati E, Bosio MC, Delmastro D, Muzi-Falconi M, Lazzaro F. Nucleic Acids Res 47 4612-4623 (2019)
  13. The role of RNase H2 in processing ribonucleotides incorporated during DNA replication. Williams JS, Gehle DB, Kunkel TA. DNA Repair (Amst) 53 52-58 (2017)
  14. Structural Impact of Single Ribonucleotide Residues in DNA. Evich M, Spring-Connell AM, Storici F, Germann MW. Chembiochem 17 1968-1977 (2016)
  15. The Incorporation of Ribonucleotides Induces Structural and Conformational Changes in DNA. Meroni A, Mentegari E, Crespan E, Muzi-Falconi M, Lazzaro F, Podestà A. Biophys J 113 1373-1382 (2017)
  16. Structural basis for the inefficient nucleotide incorporation opposite cisplatin-DNA lesion by human DNA polymerase β. Koag MC, Lai L, Lee S. J Biol Chem 289 31341-31348 (2014)
  17. Atomic resolution structure of a chimeric DNA-RNA Z-type duplex in complex with Ba(2+) ions: a case of complicated multi-domain twinning. Gilski M, Drozdzal P, Kierzek R, Jaskolski M. Acta Crystallogr D Struct Biol 72 211-223 (2016)
  18. Bypass of the Major Alkylative DNA Lesion by Human DNA Polymerase η. Koag MC, Jung H, Kou Y, Lee S. Molecules 24 E3928 (2019)
  19. Pre-steady state kinetic analysis of HIV-1 reverse transcriptase for non-canonical ribonucleoside triphosphate incorporation and DNA synthesis from ribonucleoside-containing DNA template. Nguyen LA, Domaoal RA, Kennedy EM, Kim DH, Schinazi RF, Kim B. Antiviral Res 115 75-82 (2015)
  20. Evaluation of repair activity by quantification of ribonucleotides in the genome. Iida T, Iida N, Sese J, Kobayashi T. Genes Cells 26 555-569 (2021)
  21. Structural basis for promutagenicity of 8-halogenated guanine. Koag MC, Min K, Lee S. J Biol Chem 289 6289-6298 (2014)
  22. High Flexibility of RNaseH2 Catalytic Activity with Respect to Non-Canonical DNA Structures. Dede M, Napolitano S, Melati A, Pirota V, Maga G, Crespan E. Int J Mol Sci 22 5201 (2021)
  23. Primer terminal ribonucleotide alters the active site dynamics of DNA polymerase η and reduces DNA synthesis fidelity. Chang C, Lee Luo C, Eleraky S, Lin A, Zhou G, Gao Y. J Biol Chem 299 102938 (2023)
  24. DNA polymerase ε harmonizes topological states and R-loops formation to maintain genome integrity in Arabidopsis. Li Q, Zhou J, Li S, Zhang W, Du Y, Li K, Wang Y, Sun Q. Nat Commun 14 7763 (2023)


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