Publications

Primary papers

(* joint first authors; † communicating author)

Lerner, L.K.*, Holzer, S.* Kilkenny, M.L., Murat, P., Šviković1, S., Schiavone, D., Bittleston, A. Maman, J.D., Branzei, D., Stott, K., Pellegrini, L. † and Sale, J.E. † (2020) Timeless couples G quadruplex detection with processing by DDX11 during DNA replication. Bioarxiv doi: https://doi.org/10.1101/826578


Quinet, A., Tirman, S., Jackson, J., Šviković, S., Lemaçon, D., Carvajal-Maldonado, D., Gonzalez, D., Vessoni, A.T., Tavis, S., Batista, L.F.Z., Mendez, J., Sale J.E. and Vindigni, A. (2020) PrimPol-mediated adaptive response suppresses replication fork reversal in BRCA-deficient tumours. Molecular Cell advanced online PMID 31676232


Lerner, L.K. & Sale, J.E. † (2019) Replication of G quadruplex DNA. Genes (Basel) 10(2). pii: E95. PMID 30700033


Mohiuddin, M., Rahman, M.M., Sale, J.E. & Pearson, C.E. (2019) CtIP-BRCA1 complex and MRE11 maintain replication forks in the presence of chain terminating nucleoside analogs. Nucleic Acids Research 47, 2966-2980 PMID 30657944


Šviković S., Crisp, A., Tan-Wong, S.M., Guilliam, T.A., Doherty, A.J., Proudfoot, .J., Guilbaud, G. and Sale J.E. † (2019) R-loop formation during S phase is restricted by PrimPol-mediated repriming. EMBO Journal 38(3). pii: e99793 304781925


Christov, C.P., Dingwell, K.S., Skehel, M., Wilkes, H.S., Sale, J.E., Smith, J.C. and Krude, T. (2018) A NuRD complex from Xenopus laevis eggs is essential for DNA replication. Cell Reports 22, 2265-2278 29490265


Guilbaud, G.*, Murat, P.*, Recolin, B., Campbell, B.C., Maiter, A., Sale, J.E. † and Balasubramanian, S. † (2017) Local epigenetic reprogramming induced by G quadruplex ligands Nature Chemistry 9, 1110-1117. 29064488


Tsuda, M., Terada, K., Ooka, M., Kobayashi, K., Sasanuma, H., Fujisawa, R., Tsurimoto, T., Yamamoto, J., Iwai, S., Kadoda, K., Akagawa, R., Huang, S.N., Pommier, Y., Sale, J.E., Takeda, S. and Hirota, K. (2017). The Dominant Role of the Proofreading Exonuclease Activity of Replicative Polymerase ε Contributes to Cellular Tolerance of Cytarabine (Ara-C). Oncotarget 8, 133457-33474. PMID:28380422


Tian, X., Patel, K., Ridpath, J.R., Chen, Y., Zhou, Y.-H., Neo, D., Clement, J., Takata, M., Takeda, S., Sale, J.E., Wright, F., Swenberg, J. and Nakamura, J. (2016). Time- and Dose-Dependent Genotoxicity of Trace Levels of Hexavalent Chromium. PLoS One 11, e0167503. PMID:27907204


Romanello, M.*, Schiavone, D.*, Frey, A. and Sale J.E.† (2016). H3.3 promotes AID-mediated immunoglobulin V gene diversification. EMBO Journal 35, 1452 - 1464 PMID:27220848


Hirota, K., Tsuda, M., Mohiudin, Tsurimoto, T., Livneh, Z., Kobayashi, K., Narita, T., Nishihara, K., Murai, J., Iwai, S., Guilbaud, G., Sale, J.E.† and Takeda, S.† (2016). Evidence for translesion synthesis by DNA polymerase δ in vivo. Nucleic Acids Research 44, 7242-50 PMID:27185888


Ho, T.L.F., Guilbaud, G., Blow, J.J., Sale, J.E. and Watson, C.J. (2016). The KRAB zinc finger protein Roma / Zfp157 is a critical regulator of cell cycle progression and genomic stability in concert with Gata3. Cell Reports 15, 724 - 734 PMID:27149840


Morganella, S., Alexandrov, L.B., Glodzik, D., Zou, X., Davies, H., Staaf, J., Sieuwerts, A.M., Brinkman, A.B., Martin, S., Ramakrishna, M., Butler, A., Kim, Hyung.-Y, Borg, Å., Sotiriou, C., Futreal, P.A., Campbell, P.J., Span, P.N., Van Laere, S., Lakhani, S.R., Eyfjord, J.E., Thompson, A.M., Stunnenberg, H.G., van de Vijver, M.J., Martens, J.W.M., Børresen-Dale, A.-L., Richardson, A.L., Kong, G., Thomas, G., Sale, J.E., Rada, C., Stratton, M.R., Birney, E. and Nik-Zainal, S. (2016). The topography of mutational processes in breast cancer genomes. Nature Communications 7, 11383 PMID:27136393


Mohiuddin, Kobayashi, S., Keka, I.S., Guilbaud, G., Sale, J.E., Abdel-Aziza, H.I., Wang, X., Ogawaa, S., Sasanuma, H., Chiu, R., Oestergaard, V.H., Lisby, M. and Takeda, S. (2016). The role of HERC2 and RNF8 ubiquitin E3 ligases in the promotion of translesion synthesis in the chicken DT40 cell line. DNA Repair 40, 67-76. PMID:26994443


Lim, A.W.Y., Williams, G.T., Rada, C and Sale, J.E.† (2016). Directed evolution of human scFvs in DT40 cells. Protein Engineering, Design and Selection 29, 39-48. PMID:26519451


Zimmer, J., Tacconi, E.M.C., Badie, S., Klare, K., Halder, S., Markkanen, E., Teulade-Fichou, M.-P., Kuznetsov, S., Ryan, A., Jackson, S.P., Ramadan, K., Sale, J.E. and Tarsounas, M. (2016). Targeting BRCA2 deficiency with G-quadruplex interacting drugs. Molecular Cell 61, 449-60. PMID:26748828


Schiavone, D.*, Jozwiakowski, S.K.*, Romanello, M., Guilbaud, G., Bailey, L.J., Sale, J.E.† & Doherty, A.J.† (2016). PrimPol is required for replicative tolerance of G quadruplexes in vertebrate cells. Molecular Cell 61, 161-169. PMID:26626482


Papadopoulou, C., Guilbaud, G., Schiavone, D. and Sale J.E.† (2015). G quadruplexes potentiate replication stress-induced epigenetic instability. Cell Reports 13, 2491-503. PMID:26686635


Alexandrov, L.B., Jones, P.H., Wedge, D.C., Sale, J.E., Campbell, P.J., Nik-Zainal, S. and Stratton, M.R. (2015). Clock-like mutational processes in human somatic cells. Nature Genetics 47, 1402-7. PMID:26551669


Hirota, K., Yoshikiyo, K., Guilbaud, G., Murai, J., Tsuda, M., Phillips, L.G., Narita, T., Nishihara, K., Kobayashi,K., Yamada, K., Nakamura, J., Tsurimoto, T., Pommier, Y., Lehmann, A., Sale, J.E.† and Takeda, S.† (2015). The POLD3 subunit of DNA polymerase δ promotes translesion synthesis independently of DNA polymerase ζ Nucleic Acids Research, 43, 1671-83. PMID:25628356


Frey, A., Listovsky, T., Guilbaud, G., Sarkies, P. and Sale, J.E.† (2014). Histone H3.3 is required to maintain replication fork progression after UV damage Current Biology 24, 2195-201. PMID:25201682


Schiavone, D.*, Guilbaud, G.*, Murat, P., Papadopoulou, C., Sarkies, P., Prioleau, M.-N., Balasubramanian, S. and Sale, J.E.† (2014). Determinants of G quadruplex-mediated epigenetic instability in REV1-deficient cells EMBO Journal 33, 2507-20. PMID:25190518


Brindle N.P.J., Sale, J.E., Arakawa, H., Buerstedde, J.-M., Teonchit, N., Sharma, S. and Steele, K.H. (2013). Directed evolution of an Angiopoietin-2 ligand trap by somatic hypermutation and cell surface display Journal of Biological Chemistry 288, 33205-12. PMID:24106271


Listovsky T and Sale J.E.† (2013). Sequestration of CDH1 by MAD2L2 prevents premature APC/C activation prior to anaphase onset. Journal of Cell Biology 203, 87-100. PMID:24100295


Sarkies, P., Murat, P., Phillips, L.G., Patel, K.J., Balasubramanian S. and Sale, J.E.† (2012). FANCJ coordinates two pathways that maintain epigenetic stability at G-quadruplex DNA.Nucleic Acids Research 40, 1485-98. PMID:22021381


Sarkies, P., Reams, C., Simpson, L.J. and Sale, J.E. (2010). Epigenetic instability due to defective replication of structured DNA. Molecular Cell 40, 703-713. PMID:21145480


Hirota, K., Sonoda, E., Kawamoto, T., Motegi. A., Masutani, C., Hanaoka, F., Szüts, D., Iwai, S., Sale, J.E., Lehmann, A. and Takeda, S. (2010). Restoration of effective translesion synthesis by disruption of both Polη and Polζ supports two-step lesion bypass of diverse DNA damage in vivo. PLoS Genetics 6(10): e1001151. PMID:20949111


Phillips, L.G. and Sale, J.E. (2010). WRN and REV1 collaborate at the fork to promote replication through damaged DNA. DNA Repair 9, 1064-1072. PMID:20691646


Batters, C., Zhu, H. and Sale, J.E.† (2010). Visualisation of PCNA monoubiquitination in vivo by single pass spectral imaging FRET microscopy. PLoS One 5(2): e9008. PMID:20126408


Nakahara, M., Sonoda, E., Nojima, K., Sale, J.E., Takenaka, K., Kikuchi, K., Taniguchi, Y., Nakamura, K., Sumimoto, K., Bree, R.T., Lowndes, N.F. and Takeda, S.(2009) Genetic evidence for single-strand lesions initiating Nbs1-dependent homologous recombination in diversification of IgV in chicken B lymphocytes. PLoS Genetics 5(1): e1000356. PMID:19180185


Szüts, D., Marcus, A.P., Himoto, M., Iwai, S. and Sale J.E.† (2008). REV1 restrains DNA polymerase ζ to ensure frame fidelity during bypass of a UV photoproduct in vivo. Nucleic Acids Research 36, 6767-80. PMID:18953031


Saberi, A., Nakahara, M., Sale, J.E., Kikuchi, K., Arakawa, H. Buerstedde, J-M., Takeda, S. and Sonoda, E. (2008). The 9-1-1 DNA clamp is required for immunoglobulin gene conversion. Molecular and Cellular Biology 28, 6113-6122. PMID:18662998


Edmunds, C.E., Simpson, L.J. and Sale, J.E.† (2008). PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Molecular Cell 30, 519-529. PMID:18498753


Oestergaard, V.H., Langevin, F., Kuiken, H.J., Niedzwiedz, W., Simpson, L.J., Ohzeki, M., Takata, M., Sale, J.E. and Patel K.J. (2007). Deubiquitination of FANCD2 is required for DNA crosslink repair. Molecular Cell 28, 798-809. PMID:18082605


Kohzaki, M., Hatanaka, A., Sonoda, E., Yamazoe, M., Kikuchi, K, Trung, N.V., Szüts, D., Sale, J.E., Shinagawa, H., Watanabe, M., and Takeda, S. (2007). Cooperative roles of vertebrate Fbh1 and Blm in avoidance of crossovers during recombination initiated by replication fork collapse. Molecular and Cellular Biology 27, 2812-2820. PMID:17283053


Saberi, A., Hochegger, H., Szüts, D., Lan, L., Yasui, A., Sale J.E., Taniguchi, Y., Murakawa, Y., Hua, W., Yokomori, K., Helleday, T., Teraoka, H., Arakawa, H., Buerstedde, J.M. and Takeda, S. (2007). RAD18 and poly[ADP ribose]polymerase independently suppress the access of nonhomologous end joining to double strand breaks and facilitate homologous recombination mediated repair. Molecular and Cellular Biology 27, 2562-2571. PMID:17242200


Ridpath, J.R., Nakamura, A., Tano, K., Luke, A.M., Sonoda, E., Arakawa, H., Buerstedde, J.-M., Gillespie, D.A.F., Sale, J.E., Yamazoe, M., Bishop, D.K., Takata, M., Takeda, S., Watanabe, M., Swenberg, J.A., Nakamura, J. (2007). Cells deficient in the FANC/BRCA pathway are hypersensitive to plasma levels of formaldehyde. Cancer Research 67, 11117-22. PMID:18056434


Szüts, D., Simpson L.J., Kabani, S., Yamazoe, M. and Sale J.E.† (2006). Role for RAD18 in homologous recombination in DT40. Molecular and Cellular Biology 26, 8032-8041. PMID:16923963


Simpson L.J., Ross, A.-L., Szüts, D., Alviani, C.A., Oestergaard, V.H., Patel, K.J. and Sale J.E.† (2006). RAD18-independent ubiquitination of PCNA in the avian cell line DT40. EMBO Reports 7, 927-32. PMID:16888649


Shen X., Jun S, O'Neal L.E., Sonoda E., Bemark M., Sale J.E. and Li L. (2006). REV3 and REV1 play major roles in recombination-independent repair of DNA interstrand cross-links mediated by monoubiquitinated proliferating cell nuclear antigen (PCNA). Journal of Biological Chemistry 281, 13869-72. PMID:16571727


Ross, A.-L. and Sale J.E.† (2006). The catalytic activity of REV1 is employed during immunoglobulin gene diversification in DT40. Molecular Immunology 43, 1587-94.PMID:16263170


Ross, A.-L., Simpson, L.J. and Sale J.E.† (2005). Vertebrate DNA damage tolerance requires the C terminus but not BRCT or transferase domains of REV1. Nucleic Acids Research 33, 1280-1289. PMID:15741181


Simpson, L.J. and Sale J.E.† (2005). UBE2V2 (MMS2) is not required for effective immunoglobulin gene conversion or DNA damage tolerance in DT40. DNA Repair 4, 503-510. PMID:15725630


Hatanaka, A., Yamazoe, M., Sale, J.E., Takata, M., Yamamoto, K., Kitao, H., Sonoda, E., Kikuchi, K., Yonetani, Y. and Takeda, S. (2005). Similar effects of Brca2 truncation and Rad51 paralog deficiency on immunoglobulin V gene diversification in DT40 cells support an early role for Rad51 paralogs in homologous recombination. Molecular and Cellular Biology 25, 1124-1134. PMID:15657438


Simpson, L.J. and Sale, J.E.† (2003). Rev1 is essential for DNA damage tolerance and non-templated immunoglobulin gene mutation in a vertebrate cell line. EMBO Journal. 22, 1654-1664. PMID:12660171


Cumbers S.J, Williams G.T., Davies, S.L., Grenfell R.L., Takeda S., Batista, F.D., Sale, J.E. and Neuberger M.S. (2002). Generation and iterative affinity maturation of antibodies in vitro using hypermutating B-cell lines. Nature Biotechnology 20, 1129-1134. PMID:12379869


Harris, R.S., Sale, J.E., Petersen-Mahrt, S.K. and Neuberger, M.S. (2002). AID is essential for immunoglobulin V gene conversion in a cultured B cell line Current Biology 12, 435-438. PMID:11882297


Sale, J.E.†, Calandrini, D.M., Takata, M., Takeda. S. and Neuberger, M.S.† (2001). Ablation of XRCC2/3 transforms immunoglobulin V gene conversion into somatic hypermutation. Nature 412, 921-926. PMID:11528482


Bemark, M.*, Sale, J.E.*, Kim, H-J., Berek, C., Cosgrove, R.A. and Neuberger, M.S. (2000). Somatic hypermutation in the absence of DNA-PKcs or RAG1 activity. Journal of Experimental Medicine 192, 1509-1514. PMID:11085752


Sale, J.E. and Neuberger, M.S. (1998). TdT accessible breaks are scattered over the V domain in a constitutively hypermutating cell line. Immunity 9, 859-869. PMID:9881976


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Reviews

Lerner, L.K. and Sale J.E.† (2019). Replication of G quadruplex DNA. Genes(Basel) 10(2). pii E95. PMID:30700033


Šviković S. and Sale J.E.† (2017). The effects of replication stress on S phase histone management and epigenetic memory. J. Mol. Biol. 429, 2011-2029. PMID:27876548


Wickramasinghe, C.M., Arzouk, H., Frey, A., Maiter, A. & Sale, J.E.† (2015). Contributions of the specialised DNA polymerases to replication of structured DNA. DNA Repair, 29, 83-90. PMID:25704659


Sale J.E.† (2013). Translesion synthesis and mutagenesis in eukaryotes Cold Spring Harbor Perspectives in Biology 5(3):a012708. PMID:23457261


Sale J.E.† (2012). Competition, collaboration and coordination - determining how cells bypass DNA damage. Journal of Cell Science 125, 1633-1643. PMID:22499669


Sale J.E.†, Lehmann A.R.†, Woodgate R.† (2012). Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nature Reviews Molecular & Cellular Biology 13, 141-52. PMID:22358330


Sarkies, P. and Sale, J.E.† (2012). Cellular epigenetic memory and cancer. Trends in Genetics 28, 118-127. PMID:22226176


Sarkies, P. and Sale, J.E.† (2012). Propagation of histone marks and epigenetic memory during normal and interrupted DNA replication. Cell and Molecular Life Sciences 69, 697-716. PMID:21964926


Phillips, L.G. and Sale, J.E.† (2010). Be prepared: DNA polymerase η gets ready for action - in G1. Cell Cycle 8, 3258-3259.PMID:20691646


Sale, J.E.†, Batters, C., Edmunds, C.E., Phillips, L.G. Simpson, L.J. and Szüts, D. (2009). Timing matters: lesion bypass in immunoglobulin gene hypermutation. Phil. Trans. R. Soc. Lond. B 364,595-603. PMID:19008194


Simpson L.J. and Sale J.E. (2006)†. Analysis of replicative DNA damage bypass and its role in immunoglobulin repertoire development. Subcellular Biochemistry 40, 271-94. PMID:17623911


Sale, J.E.†, Bemark, M., Williams, G.T., Jolly, C.J., Ehrenstein, M.R., Rada, C.A, Milstein, C. and Neuberger, M.S. (2001). In vivo and in vitro studies of immunoglobulin gene somatic hypermutation. Phil. Trans. R. Soc. Lond. B 356, 21-18. PMID:11205326


Neuberger, M.S., Sale J.E., Cumbers, S.J., Jolly, C.J., Bemark, M., Ehrenstein, M.R., Lanoue, A., Brüggeman, M., Batista, F.D., Davies, S.L. and Williams, G.T. (2000). Diversification and selection mechanisms for the production of protein repertoires – lessons from the immune system. Applied Biochem. Biotechnol. 83, 56-62. PMID:10826948


Sale, J.E.† (2004). Immunoglobulin gene diversification in DT40: a model for vertebrate DNA damage tolerance. DNA Repair 3, 693-702. PMID:15177178


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Commentaries

Sale J.E.† (2016). Starting over: PrimPol reprimes after chain termination. Cell Cycle 15, 2099 - 2100. PMID:27384604


Sale, J.E.† (2015). REV7/MAD2L2: the multitasking maestro emerges as a barrier to recombination. EMBO J. 34, 1609-11. PMID:25896508


Sale, J.E.†, Patel K.J.† and Batista, F.D.† (2013). Retrospective. Michael Neuberger (1953-2013) Science 342, 1335. PMID:24337288


Guilbaud, G. and Sale, J.E.† (2012). Unwinding to recombine Molecular Cell 47, 493-4. PMID:22920289


Phillips, L.G. and Sale, J.E.† (2010). Be prepared: DNA polymerase η gets ready for action - in G1. Cell Cycle 8, 3258-3259.PMID:20691646


Sale, J.E.† (2007). Radiation Resistance: Resurrection by Recombination. Current Biology 17, R12-R14. PMID:17208168


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Methods

Sale, J.E.† (2012). Measurement of diversification in the immunoglobulin light chain gene of DT40 cells. Meth Mol Biol 920, 417-432. PMID:25896508


Du Plessis, D. and Sale, J.E.† (2012). Monitoring I-SceI induced double strand break repair in DT40 Cells. Meth Mol Biol 920, 371-377. PMID:25896508


Franklin, R. and Sale, J.E.† (2006). 2D cell cycle analysis. Subcell. Biochem. 40, 405-8. PMID:17623930


Simpson, L.J. and Sale, J.E.† (2006). Sister chromatid exchange assay. Subcell. Biochem. 40, 399-403. PMID:17623929


Szüts, D. and Sale, J.E.† (2006). Subnuclear immunofluorescence. Subcell. Biochem. 40, 395-8. PMID:17623928


Simpson, L.J. and Sale, J.E.† (2006). Colony survival assay Subcell. Biochem. 40, 387-91. PMID:17623926


Randow, F. and Sale, J.E.† (2006). Retroviral transduction of DT40. Subcell. Biochem. 40, 383-6. PMID:17623925


Franklin, R. and Sale, J.E.† (2006). Stable non-targeted transfection of DT40. Subcell. Biochem. 40, 379-82. PMID:17623924


Sale, J.E.† (2006). Stable non-targeted transfection of DT40. Subcell. Biochem. 40, 341-344. PMID:17623915


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