Repriming of DNA synthesis at stalled replication forks by human PrimPol

Nature Structural and Molecular Biology

Volumn 20, Issue 12, 2013, Pages 1383-1389

  Mourón, Silvana ^a   Rodriguez Acebes, Sara ^a   Martínez Jiménez, María I ^b   García Gómez, Sara ^b   Chocrón, Sandra ^b   Blanco, Luis ^b   Méndez, Juan ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DNA PRIMASE; PRIMPOL ENZYME; UNCLASSIFIED DRUG;

ARTICLE; CANCER THERAPY; CELL CYCLE S PHASE; CHROMATIN; CHROMOSOME BREAKAGE; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA MODIFICATION; DNA REPLICATION; DNA STRUCTURE; DNA SYNTHESIS; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; GENE DUPLICATION; GENE EXPRESSION; GENE LOSS; GENETIC RISK; GENOMIC INSTABILITY; HUMAN; PRIORITY JOURNAL; TRANSLESION SYNTHESIS; ULTRAVIOLET IRRADIATION;

EID: 84890105942     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2719     Document Type: Article

References (41)

1. Kelly, T.J. & Stillman, B. in DNA Replication and Human Disease (ed. DePamphilis, M.L.) 1-29 (Cold Spring Harbor Laboratory Press, 2006).
2. Lopez-Contreras, A.J. et al. A proteomic characterization of factors enriched at nascent DNA molecules. Cell Rep. 3, 1105-1116 (2013).
3. Sirbu, B.M. et al. Identification of proteins at active, stalled, and collapsed replication forks using Isolation of proteins on nascent DNA (iPOND) coupled with mass spectrometry. J. Biol. Chem. doi:10.1074/jbc.M113.511337 (18 September 2013).
4. Yao, N.Y. & O'Donnell, M. SnapShot: The replisome. Cell 141, 1088 (2010).
5. Conti, C. et al. Replication fork velocities at adjacent replication origins are coordinately modified during DNA replication in human cells. Mol. Biol. Cell 18, 3059-3067 (2007).
6. Branzei, D. & Foiani, M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11, 208-219 (2010).
7. Petermann, E. & Helleday, T. Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol. 11, 683-687 (2010).
8. Tourriere, H. & Pasero, P. Maintenance of fork integrity at damaged DNA and natural pause sites. DNA Repair (Amst.) 6, 900-913 (2007).
9. Sale, J.E., Lehmann, A.R. & Woodgate, R. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat. Rev. Mol. Cell Biol. 13, 141-152 (2012).
10. Zahn, K.E., Wallace, S.S. & Doublie, S. DNA polymerases provide a canon of strategies for translesion synthesis past oxidatively generated lesions. Curr. Opin. Struct. Biol. 21, 358-369 (2011).
11. Lopes, M., Foiani, M. & Sogo, J.M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21, 15-27 (2006).
12. Callegari, A.J. & Kelly, T.J. UV irradiation induces a postreplication DNA damage checkpoint. Proc. Natl. Acad. Sci. USA 103, 15877-15882 (2006).
13. Callegari, A.J., Clark, E., Pneuman, A. & Kelly, T.J. Postreplication gaps at UV lesions are signals for checkpoint activation. Proc. Natl. Acad. Sci. USA 107, 8219-8224 (2010).
14. Elvers, I., Johansson, F., Groth, P., Erixon, K. & Helleday, T. UV stalled replication forks restart by re-priming in human fibroblasts. Nucleic Acids Res. 39, 7049-7057 (2011).
15. Heller, R.C. & Marians, K.J. Replication fork reactivation downstream of a blocked nascent leading strand. Nature 439, 557-562 (2006).
16. Heller, R.C. & Marians, K.J. Replisome assembly and the direct restart of stalled replication forks. Nat. Rev. Mol. Cell Biol. 7, 932-943 (2006).
17. Langston, L.D. & O'Donnell, M. DNA replication: Keep moving and don't mind the gap. Mol. Cell 23, 155-160 (2006).
18. Iyer, L.M., Koonin, E.V., Leipe, D.D. & Aravind, L. Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: Structural insights and new members. Nucleic Acids Res. 33, 3875-3896 (2005).
19. Garcia-Gomez, S. et al. PrimPol, an archaic primase/polymerase operating in human cells. Mol. Cell doi:10.1016/j.molcel.2013.09.025 (24 October 2013).
20. Jackson, D.A. & Pombo, A. Replicon clusters are stable units of chromosome structure: Evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 140, 1285-1295 (1998).
21. Ge, X.Q., Jackson, D.A. & Blow, J.J. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 21, 3331-3341 (2007).
22. Ibarra, A., Schwob, E. & Mendez, J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl. Acad. Sci. USA 105, 8956-8961 (2008).
23. Woodward, A.M. et al. Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell Biol. 173, 673-683 (2006).
24. Biertumpfel, C. et al. Structure and mechanism of human DNA polymerase eta. Nature 465, 1044-1048 (2010).
25. Johnson, R.E., Prakash, S. & Prakash, L. Efficient bypass of a thymine-Thymine dimer by yeast DNA polymerase, Poleta. Science 283, 1001-1004 (1999).
26. Temviriyanukul, P. et al. Temporally distinct translesion synthesis pathways for ultraviolet light-induced photoproducts in the mammalian genome. DNA Repair (Amst.) 11, 550-558 (2012).
27. Daigaku, Y., Davies, A.A. & Ulrich, H.D. Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature 465, 951-955 (2010).
28. Karras, G.I. & Jentsch, S. The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell 141, 255-267 (2010).
29. Edmunds, C.E., Simpson, L.J. & Sale, J.E. PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol. Cell 30, 519-529 (2008).
30. Lipps, G., Weinzierl, A.O., von Scheven, G., Buchen, C. & Cramer, P. Structure of a bifunctional DNA primase-polymerase. Nat. Struct. Mol. Biol. 11, 157-162 (2004).
31. De Silva, F.S., Lewis, W., Berglund, P., Koonin, E.V. & Moss, B. Poxvirus DNA primase. Proc. Natl. Acad. Sci. USA 104, 18724-18729 (2007).
32. McGeoch, A.T. & Bell, S.D. Eukaryotic/archaeal primase and MCM proteins encoded in a bacteriophage genome. Cell 120, 167-168 (2005).
33. Sanchez-Berrondo, J. et al. Molecular architecture of a multifunctional MCM complex. Nucleic Acids Res. 40, 1366-1380 (2012).
34. Kilkenny, M.L., Longo, M.A., Perera, R.L. & Pellegrini, L. Structures of human primase reveal design of nucleotide elongation site and mode of Pol alpha tethering. Proc. Natl. Acad. Sci. USA 110, 15961-15966 (2013).
35. Zhao, F. et al. Exome sequencing reveals CCDC111 mutation associated with high myopia. Hum. Genet. 132, 913-921 (2013).
36. Ekholm-Reed, S. et al. Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J. Cell Biol. 165, 789-800 (2004).
37. Mendez, J. & Stillman, B. Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: Assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20, 8602-8612 (2000).
38. Harlow, E. & Lane, D. in Using Antibodies: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 1998).
39. Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
40. Terret, M.E., Sherwood, R., Rahman, S., Qin, J. & Jallepalli, P.V. Cohesin acetylation speeds the replication fork. Nature 462, 231-234 (2009).
41. Bianco, J.N. et al. Analysis of DNA replication profiles in budding yeast and mammalian cells using DNA combing. Methods 57, 149-157 (2012).