SLFN11 Blocks Stressed Replication Forks Independently of ATR

Molecular Cell

Volumn 69, Issue 3, 2018, Pages 371-384.e6

  Murai, Junko ^a   Tang, Sai Wen ^a,c   Leo, Elisabetta ^a,d   Baechler, Simone A ^a   Redon, Christophe E ^a   Zhang, Hongliang ^a   Al Abo, Muthana ^a   Rajapakse, Vinodh N ^a   Nakamura, Eijiro ^b   Jenkins, Lisa M Miller ^a   Aladjem, Mirit I ^a   Pommier, Yves ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Oncology Innovative Medicines and Early Clinical Development   (United Kingdom)

Author keywords

ATAC seq; ATR; camptothecin; cell cycle checkpoints; CHK1; hydroxyurea; PARP inhibitors; prexasertib (LY2606368); replication origin; SLFN11

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ATR PROTEIN; CAMPTOTHECIN; PREXASERTIB; SLFN11 PROTEIN; TUMOR PROTEIN; UNCLASSIFIED DRUG; ATM PROTEIN; ATR PROTEIN, HUMAN; CDC45 PROTEIN, HUMAN; CELL CYCLE PROTEIN; DNA HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN; NUCLEAR PROTEIN; PYRAZINE DERIVATIVE; PYRAZOLE DERIVATIVE; REPLICATION FACTOR A; RPA1 PROTEIN, HUMAN; SINGLE STRANDED DNA; SLFN11 PROTEIN, HUMAN;

ARTICLE; CELL DEATH; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA REPLICATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PROTEIN BINDING; S PHASE CELL CYCLE CHECKPOINT; STRESS; CHROMATIN; DNA DAMAGE; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CAMPTOTHECIN; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHROMATIN; DNA DAMAGE; DNA HELICASES; DNA REPLICATION; DNA, SINGLE-STRANDED; HUMANS; MINICHROMOSOME MAINTENANCE PROTEINS; NUCLEAR PROTEINS; PYRAZINES; PYRAZOLES; REPLICATION PROTEIN A;

EID: 85041685396     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2018.01.012     Document Type: Article

References (33)

1. Aladjem, M.I., Redon, C.E., Order from clutter: selective interactions at mammalian replication origins. Nat. Rev. Genet. 18 (2016), 101–116.
2. Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A.A., Kim, S., Wilson, C.J., Lehár, J., Kryukov, G.V., Sonkin, D., et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483 (2012), 603–607.
3. Branzei, D., Foiani, M., Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 9 (2008), 297–308.
4. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., Greenleaf, W.J., Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10 (2013), 1213–1218.
5. Feijoo, C., Hall-Jackson, C., Wu, R., Jenkins, D., Leitch, J., Gilbert, D.M., Smythe, C., Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J. Cell Biol. 154 (2001), 913–923.
6. Fragkos, M., Ganier, O., Coulombe, P., Méchali, M., DNA replication origin activation in space and time. Nat. Rev. Mol. Cell Biol. 16 (2015), 360–374.
7. Fu, H., Besnard, E., Desprat, R., Ryan, M., Kahli, M., Lemaitre, J.M., Aladjem, M.I., Mapping replication origin sequences in eukaryotic chromosomes. Curr. Protoc. Cell Biol. 65 (2014), 1–17 17.
8. Gardner, E.E., Lok, B.H., Schneeberger, V.E., Desmeules, P., Miles, L.A., Arnold, P.K., Ni, A., Khodos, I., de Stanchina, E., Nguyen, T., et al. Chemosensitive relapse in small cell lung cancer proceeds through an EZH2-SLFN11 axis. Cancer Cell 31 (2017), 286–299.
9. Jossé, R., Martin, S.E., Guha, R., Ormanoglu, P., Pfister, T.D., Reaper, P.M., Barnes, C.S., Jones, J., Charlton, P., Pollard, J.R., et al. ATR inhibitors VE-821 and VX-970 sensitize cancer cells to topoisomerase i inhibitors by disabling DNA replication initiation and fork elongation responses. Cancer Res. 74 (2014), 6968–6979.
10. King, C., Diaz, H.B., McNeely, S., Barnard, D., Dempsey, J., Blosser, W., Beckmann, R., Barda, D., Marshall, M.S., LY2606368 causes replication catastrophe and antitumor effects through CHK1-dependent mechanisms. Mol. Cancer Ther. 14 (2015), 2004–2013.
11. Liaw, H., Lee, D., Myung, K., DNA-PK-dependent RPA2 hyperphosphorylation facilitates DNA repair and suppresses sister chromatid exchange. PLoS ONE, 6, 2011, e21424.
12. Lok, B.H., Gardner, E.E., Schneeberger, V.E., Ni, A., Desmeules, P., Rekhtman, N., de Stanchina, E., Teicher, B.A., Riaz, N., Powell, S.N., et al. PARP inhibitor activity correlates with SLFN11 expression and demonstrates synergy with temozolomide in small cell lung cancer. Clin. Cancer Res. 23 (2017), 523–535.
13. Maréchal, A., Li, J.M., Ji, X.Y., Wu, C.S., Yazinski, S.A., Nguyen, H.D., Liu, S., Jiménez, A.E., Jin, J., Zou, L., PRP19 transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin-mediated circuitry. Mol. Cell 53 (2014), 235–246.
14. Martin, M.M., Ryan, M., Kim, R., Zakas, A.L., Fu, H., Lin, C.M., Reinhold, W.C., Davis, S.R., Bilke, S., Liu, H., et al. Genome-wide depletion of replication initiation events in highly transcribed regions. Genome Res. 21 (2011), 1822–1832.
15. Mavrommatis, E., Fish, E.N., Platanias, L.C., The schlafen family of proteins and their regulation by interferons. J. Interferon Cytokine Res. 33 (2013), 206–210.
16. Mu, Y., Lou, J., Srivastava, M., Zhao, B., Feng, X.H., Liu, T., Chen, J., Huang, J., SLFN11 inhibits checkpoint maintenance and homologous recombination repair. EMBO Rep. 17 (2016), 94–109.
17. Murai, J., Huang, S.Y., Das, B.B., Renaud, A., Zhang, Y., Doroshow, J.H., Ji, J., Takeda, S., Pommier, Y., Trapping of PARP1 and PARP2 by clinical PARP inhibitors. Cancer Res. 72 (2012), 5588–5599.
18. Murai, J., Feng, Y., Yu, G.K., Ru, Y., Tang, S.W., Shen, Y., Pommier, Y., Resistance to PARP inhibitors by SLFN11 inactivation can be overcome by ATR inhibition. Oncotarget 7 (2016), 76534–76550.
19. Nogales, V., Reinhold, W.C., Varma, S., Martinez-Cardus, A., Moutinho, C., Moran, S., Heyn, H., Sebio, A., Barnadas, A., Pommier, Y., Esteller, M., Epigenetic inactivation of the putative DNA/RNA helicase SLFN11 in human cancer confers resistance to platinum drugs. Oncotarget 7 (2016), 3084–3097.
20. Petermann, E., Woodcock, M., Helleday, T., Chk1 promotes replication fork progression by controlling replication initiation. Proc. Natl. Acad. Sci. USA 107 (2010), 16090–16095.
21. Pommier, Y., Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6 (2006), 789–802.
22. Ray Chaudhuri, A., Hashimoto, Y., Herrador, R., Neelsen, K.J., Fachinetti, D., Bermejo, R., Cocito, A., Costanzo, V., Lopes, M., Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nat. Struct. Mol. Biol. 19 (2012), 417–423.
23. Ribeyre, C., Zellweger, R., Chauvin, M., Bec, N., Larroque, C., Lopes, M., Constantinou, A., Nascent DNA proteomics reveals a chromatin remodeler required for topoisomerase I loading at replication forks. Cell Rep. 15 (2016), 300–309.
24. Seiler, J.A., Conti, C., Syed, A., Aladjem, M.I., Pommier, Y., The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Mol. Cell. Biol. 27 (2007), 5806–5818.
25. Sirbu, B.M., Couch, F.B., Cortez, D., Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat. Protoc. 7 (2012), 594–605.
26. Stewart, C.A., Tong, P., Cardnell, R.J., Sen, T., Li, L., Gay, C.M., Masrorpour, F., Fan, Y., Bara, R.O., Feng, Y., et al. Dynamic variations in epithelial-to-mesenchymal transition (EMT), ATM, and SLFN11 govern response to PARP inhibitors and cisplatin in small cell lung cancer. Oncotarget 8 (2017), 28575–28587.
27. Syljuåsen, R.G., Sørensen, C.S., Hansen, L.T., Fugger, K., Lundin, C., Johansson, F., Helleday, T., Sehested, M., Lukas, J., Bartek, J., Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol. Cell. Biol. 25 (2005), 3553–3562.
28. Toledo, L.I., Altmeyer, M., Rask, M.B., Lukas, C., Larsen, D.H., Povlsen, L.K., Bekker-Jensen, S., Mailand, N., Bartek, J., Lukas, J., ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell 155 (2013), 1088–1103.
29. Weibezahn, J., Schlieker, C., Bukau, B., Mogk, A., Characterization of a trap mutant of the AAA+ chaperone ClpB. J. Biol. Chem. 278 (2003), 32608–32617.
30. Yang, W., Soares, J., Greninger, P., Edelman, E.J., Lightfoot, H., Forbes, S., Bindal, N., Beare, D., Smith, J.A., Thompson, I.R., et al. Genomics of Drug Sensitivity in Cancer (GDSC): a resource for therapeutic biomarker discovery in cancer cells. Nucleic Acids Res. 41 (2013), D955–D961.
31. Zeman, M.K., Cimprich, K.A., Causes and consequences of replication stress. Nat. Cell Biol. 16 (2014), 2–9.
32. Zhang, Y.W., Brognard, J., Coughlin, C., You, Z., Dolled-Filhart, M., Aslanian, A., Manning, G., Abraham, R.T., Hunter, T., The F box protein Fbx6 regulates Chk1 stability and cellular sensitivity to replication stress. Mol. Cell 35 (2009), 442–453.
33. Zoppoli, G., Regairaz, M., Leo, E., Reinhold, W.C., Varma, S., Ballestrero, A., Doroshow, J.H., Pommier, Y., Putative DNA/RNA helicase Schlafen-11 (SLFN11) sensitizes cancer cells to DNA-damaging agents. Proc. Natl. Acad. Sci. USA 109 (2012), 15030–15035.