Super-resolution visualization of distinct stalled and broken replication fork structures
Autoři:
Donna R. Whelan aff001; Wei Ting C. Lee aff002; Frances Marks aff002; Yu Tina Kong aff002; Yandong Yin aff002; Eli Rothenberg aff002
Působiště autorů:
Department of Pharmacy and Biomedical Sciences, La Trobe Institute for Molecular Science, La Trobe University, Bendigo, Victoria, Australia
aff001; Department of Biochemistry and Molecular Pharmacology, Perlmutter Cancer Center, New York University School of Medicine, New York, New York, United States of America
aff002
Vyšlo v časopise:
Super-resolution visualization of distinct stalled and broken replication fork structures. PLoS Genet 16(12): e1009256. doi:10.1371/journal.pgen.1009256
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009256
Souhrn
Endogenous genotoxic stress occurs in healthy cells due to competition between DNA replication machinery, and transcription and topographic relaxation processes. This causes replication fork stalling and regression, which can further collapse to form single-ended double strand breaks (seDSBs). Super-resolution microscopy has made it possible to directly observe replication stress and DNA damage inside cells, however new approaches to sample preparation and analysis are required. Here we develop and apply multicolor single molecule microscopy to visualize individual replication forks under mild stress from the trapping of Topoisomerase I cleavage complexes, a damage induction which closely mimics endogenous replicative stress. We observe RAD51 and RAD52, alongside RECQ1, as the first responder proteins to stalled but unbroken forks, whereas Ku and MRE11 are initially recruited to seDSBs. By implementing novel super-resolution imaging assays, we are thus able to discern closely related replication fork stress motifs and their repair pathways.
Klíčová slova:
DNA damage – DNA repair – DNA replication – Fluorescence imaging – In vivo imaging – Monte Carlo method – Non-homologous end joining – Recombinase polymerase amplification
Zdroje
1. Mehta A, Haber JE. Sources of DNA Double-Strand Breaks and Models of Recombinational DNA Repair. Cold Spring Harbor Perspectives in Biology. 2014;6(9). doi: 10.1101/cshperspect.a016428 WOS:000341576800008. 25104768
2. Ceccaldi R, Rondinelli B, D'Andrea AD. Repair Pathway Choices and Consequences at the Double-Strand Break. Trends in Cell Biology. 2016;26(1):52–64. doi: 10.1016/j.tcb.2015.07.009 WOS:000368206000007. 26437586
3. Neelsen KJ, Chaudhuri AR, Follonier C, Herrador R, Lopes M. Visualization and Interpretation of Eukaryotic DNA Replication Intermediates In Vivo by Electron Microscopy. Functional Analysis of DNA and Chromatin. 2014;1094:177–208. doi: 10.1007/978-1-62703-706-8_15 WOS:000332345200016. 24162989
4. Neelsen KJ, Lopes M. Replication fork reversal in eukaryotes: from dead end to dynamic response. Nature Reviews Molecular Cell Biology. 2015;16(4):207–20. doi: 10.1038/nrm3935 WOS:000351630500006. 25714681
5. Saleh-Gohari N, Bryant HE, Schultz N, Parker KA, Cassel TN, Helleday T. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Molecular and Cellular Biology. 2005;25(16):7158–69. doi: 10.1128/MCB.25.16.7158-7169.2005 WOS:000231000800026. 16055725
6. Chaudhuri AR, Hashimoto Y, Herrador R, Neelsen KJ, Fachinetti D, Bermejo R, et al. Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nature Structural & Molecular Biology. 2012;19(4):417–23. doi: 10.1038/nsmb.2258 WOS:000302514400009. 22388737
7. Yeeles JTP, Poli J, Marians KJ, Pasero P. Rescuing stalled or damaged replication forks. Cold Spring Harbor perspectives in biology. 5(5):a012815–a. doi: 10.1101/cshperspect.a012815 23637285.
8. Kolinjivadi AM, Sannino V, De Antoni A, Zadorozhny K, Kilkenny M, Techer H, et al. Smarcal1-Mediated Fork Reversal Triggers Mre11-Dependent Degradation of Nascent DNA in the Absence of Brca2 and Stable Rad51 Nucleofilaments. Molecular Cell. 2017;67(5):867–+. doi: 10.1016/j.molcel.2017.07.001 WOS:000411128900014. 28757209
9. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. Hydroxyurea-Stalled Replication Forks Become Progressively Inactivated and Require Two Different RAD51-Mediated Pathways for Restart and Repair. Molecular Cell. 2010;37(4):492–502. doi: 10.1016/j.molcel.2010.01.021 PMC2958316. 20188668
10. Mazouzi A, Velimezi G, Loizou JI. DNA replication stress: Causes, resolution and disease. Exp Cell Res. 2014;329(1):85–93. doi: 10.1016/j.yexcr.2014.09.030 WOS:000345489700012. 25281304
11. Krejci L, Altmannova V, Spirek M, Zhao XL. Homologous recombination and its regulation. Nucleic Acids Res. 2012;40(13):5795–818. doi: 10.1093/nar/gks270 WOS:000306970700009. 22467216
12. Vilenchik MM, Knudson AG. Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci U S A. 2003;100(22):12871–6. doi: 10.1073/pnas.2135498100 WOS:000186301100066. 14566050
13. Heyer W-D, Ehmsen KT, Liu J. Regulation of Homologous Recombination in Eukaryotes. Annual Review of Genetics, Vol 44. 2010;44:113–39. doi: 10.1146/annurev-genet-051710-150955 WOS:000286042600006. 20690856
14. Willis NA, Chandramouly G, Huang B, Kwok A, Follonier C, Deng CX, et al. BRCA1 controls homologous recombination at Tus/Ter-stalled mammalian replication forks. Nature. 2014;510(7506):556–+. doi: 10.1038/nature13295 WOS:000337806300051. 24776801
15. Prakash R, Zhang Y, Feng WR, Jasin M. Homologous Recombination and Human Health: The Roles of BRCA1, BRCA2, and Associated Proteins. Cold Spring Harbor Perspectives in Biology. 2015;7(4). doi: 10.1101/cshperspect.a016600 WOS:000355194500006. 25833843
16. Liu T, Huang J. DNA End Resection: Facts and Mechanisms. Genomics Proteomics & Bioinformatics. 2016;14(3):126–30. doi: 10.1016/j.gpb.2016.05.002 WOS:000379516500003. 27240470
17. Daddacha W, Koyen AE, Bastien AJ, Head PE, Dhere VR, Nabeta GN, et al. SAMHD1 Promotes DNA End Resection to Facilitate DNA Repair by Homologous Recombination. Cell Reports. 2017;20(8):1921–35. doi: 10.1016/j.celrep.2017.08.008 28834754
18. Chapman JR, Taylor MRG, Boulton SJ. Playing the End Game: DNA Double-Strand Break Repair Pathway Choice. Molecular Cell. 2012;47(4):497–510. doi: 10.1016/j.molcel.2012.07.029 WOS:000308061100003. 22920291
19. Brandsma I, Gent DC. Pathway choice in DNA double strand break repair: observations of a balancing act. Genome Integrity. 2012;3:9–. doi: 10.1186/2041-9414-3-9 PMC3557175. 23181949
20. Arnoult N, Correia A, Ma J, Merlo A, Garcia-Gomez S, Maric M, et al. Regulation of DNA repair pathway choice in S and G2 phases by the NHEJ inhibitor CYREN. Nature. 2017;549(7673):548–+. doi: 10.1038/nature24023 WOS:000411930000056. 28959974
21. Hartlerode AJ, Morgan MJ, Wu Y, Buis J, Ferguson DO. Recruitment and activation of the ATM kinase in the absence of DNA-damage sensors. Nature Structural & Molecular Biology. 2015;22(9):736–U124. doi: 10.1038/nsmb.3072 WOS:000360933200017. 26280532
22. Lamarche BJ, Orazio NI, Weitzman MD. The MRN complex in Double-Strand Break Repair and Telomere Maintenance. FEBS letters. 2010;584(17):3682–95. doi: 10.1016/j.febslet.2010.07.029 PMC2946096. 20655309
23. Filippo JS, Sung P, Klein H. Mechanism of eukaryotic homologous recombination. Annual Review of Biochemistry. 2008;77:229–57. doi: 10.1146/annurev.biochem.77.061306.125255 WOS:000257596800011. 18275380
24. Sun J, Lee KJ, Davis AJ, Chen DJ. Human Ku70/80 Protein Blocks Exonuclease 1-mediated DNA Resection in the Presence of Human Mre11 or Mre11/Rad50 Protein Complex. J Biol Chem. 2012;287(7):4936–45. doi: 10.1074/jbc.M111.306167 WOS:000300608500054. 22179609
25. Lemacon D, Jackson J, Quinet A, Brickner JR, Li S, Yazinski S, et al. MRE11 and EXO1 nucleases degrade reversed forks and elicit MUS81-dependent fork rescue in BRCA2-deficient cells. Nature Communications. 2017;8. doi: 10.1038/s41467-017-01180-5 WOS:000412998100002. 29038425
26. Ying S, Hamdy FC, Helleday T. Mre11-Dependent Degradation of Stalled DNA Replication Forks Is Prevented by BRCA2 and PARP1. Cancer Res. 2012;72(11):2814–21. doi: 10.1158/0008-5472.CAN-11-3417 WOS:000307348000014. 22447567
27. Bryant HE, Petermann E, Schultz N, Jemth AS, Loseva O, Issaeva N, et al. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. Embo Journal. 2009;28(17):2601–15. doi: 10.1038/emboj.2009.206 WOS:000269494200010. 19629035
28. Whelan DR, Bell TDM. Super-Resolution Single-Molecule Localization Microscopy: Tricks of the Trade. Journal of Physical Chemistry Letters. 2015;6(3):374–82. doi: 10.1021/jz5019702 WOS:000349137400012. 26261950
29. Raderschall E, Golub EI, Haaf T. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc Natl Acad Sci U S A. 1999;96(5):1921–6. doi: 10.1073/pnas.96.5.1921 WOS:000078956600023. 10051570
30. Klein T, Proppert S, Sauer M. Eight years of single-molecule localization microscopy. Histochemistry and Cell Biology. 2014;141(6):561–75. doi: 10.1007/s00418-014-1184-3 WOS:000336388300002. 24496595
31. Whelan DR, Lee WTC, Yin Y, Ofri DM, Bermudez-Hernandez K, Keegan S, et al. Spatiotemporal dynamics of homologous recombination repair at single collapsed replication forks. Nature Communications. 2018;9(1):3882. doi: 10.1038/s41467-018-06435-3 30250272
32. Schlacher K, Christ N, Siaud N, Egashira A, Wu H, Jasin M. Double-Strand Break Repair-Independent Role for BRCA2 in Blocking Stalled Replication Fork Degradation by MRE11. Cell. 2011;145(4):529–42. doi: 10.1016/j.cell.2011.03.041 WOS:000290560800007. 21565612
33. Chaudhuri AR, Callen E, Ding X, Gogola E, Duarte AA, Lee JE, et al. Replication fork stability confers chemoresistance in BRCA-deficient cells. Nature. 2016;535(7612):382–+. doi: 10.1038/nature18325 WOS:000380344200032. 27443740
34. Kolinjivadi AM, Sannino V, de Antoni A, Techer H, Baldi G, Costanzo V. Moonlighting at replication forks—a new life for homologous recombination proteins BRCA1, BRCA2 and RAD51. Febs Letters. 2017;591(8):1083–100. doi: 10.1002/1873-3468.12556 WOS:000400968800002. 28079255
35. Heilemann M, van de Linde S, Schuttpelz M, Kasper R, Seefeldt B, Mukherjee A, et al. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angewandte Chemie-International Edition. 2008;47(33):6172–6. doi: 10.1002/anie.200802376 WOS:000258355200005. 18646237
36. Reid DA, Keegan S, Leo-Macias A, Watanabe G, Strande NT, Chang HH, et al. Organization and dynamics of the nonhomologous end-joining machinery during DNA double-strand break repair. Proc Natl Acad Sci U S A. 2015;112(20):E2575–E84. doi: 10.1073/pnas.1420115112 WOS:000354729500007. 25941401
37. Zessin PJM, Finan K, Heilemann M. Super-resolution fluorescence imaging of chromosomal DNA. Journal of Structural Biology. 2012;177(2):344–8. doi: 10.1016/j.jsb.2011.12.015 WOS:000300755400019. 22226957
38. Raulf A, Spahn CK, Zessin PJM, Finan K, Bernhardt S, Heckel A, et al. Click chemistry facilitates direct labelling and super-resolution imaging of nucleic acids and proteins. Rsc Advances. 2014;4(57):30462–6. doi: 10.1039/c4ra01027b WOS:000340497600069. 25580242
39. Chagin VO, Casas-Delucchi CS, Reinhart M, Schermelleh L, Markaki Y, Maiser A, et al. 4D Visualization of replication foci in mammalian cells corresponding to individual replicons. Nature Communications. 2016;7. doi: 10.1038/ncomms11231 WOS:000373827000001. 27052570
40. Triemer T, Messikommer A, Glasauer SMK, Alzeer J, Paulisch MH, Luedtke NW. Superresolution imaging of individual replication forks reveals unexpected prodrug resistance mechanism. Proceedings of the National Academy of Sciences. 2018;115(7):E1366. doi: 10.1073/pnas.1714790115 29378947
41. Gorczyca W, Gong JP, Darzynkiewicz Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 1993;53(8):1945–51. WOS:A1993KY09600040. 8467513
42. Mijic S, Zellweger R, Chappidi N, Berti M, Jacobs K, Mutreja K, et al. Replication fork reversal triggers fork degradation in BRCA2-defective cells. Nature Communications. 2017;8(1):859. doi: 10.1038/s41467-017-01164-5 29038466
43. Zellweger R, Dalcher D, Mutreja K, Berti M, Schmid JA, Herrador R, et al. Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells. Journal of Cell Biology. 2015;208(5):563–79. doi: 10.1083/jcb.201406099 WOS:000350530600009. 25733714
44. Berti M, Ray Chaudhuri A, Thangavel S, Gomathinayagam S, Kenig S, Vujanovic M, et al. Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nature Structural &Amp; Molecular Biology. 2013;20:347. doi: 10.1038/nsmb.2501 https://www.nature.com/articles/nsmb.2501#supplementary-information. 23396353
45. Chanut P, Britton S, Coates J, Jackson SP, Calsou P. Coordinated nuclease activities counteract Ku at single-ended DNA double-strand breaks. Nature Communications. 2016;7:12889. doi: 10.1038/ncomms12889 https://www.nature.com/articles/ncomms12889#supplementary-information. 27641979
46. Britton S, Coates J, Jackson SP. A new method for high-resolution imaging of Ku foci to decipher mechanisms of DNA double-strand break repair. Journal of Cell Biology. 2013;202(3):579–95. doi: 10.1083/jcb.201303073 WOS:000322769400016. 23897892
47. Garcia V, Phelps SEL, Gray S, Neale MJ. Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature. 2011;479(7372):241–U123. doi: 10.1038/nature10515 WOS:000298030800045. 22002605
48. Bermudez-Hernandez K, Keegan S, Whelan DR, Reid DA, Zagelbaum J, Yin Y, et al. A Method for Quantifying Molecular Interactions Using Stochastic Modelling and Super-Resolution Microscopy. Scientific Reports. 2017;7(1):14882. doi: 10.1038/s41598-017-14922-8 29093506
49. MacPhail SH, Banath JP, Yu Y, Chu E, Olive PL. Cell cycle-dependent expression of phosphorylated histone H2AX: Reduced expression in unirradiated but not X-irradiated G(1)-phase cells. Radiat Res. 2003;159(6):759–67. doi: 10.1667/rr3003 WOS:000183291800008. 12751958
50. Bianchi A, de Lange T. Ku binds telomeric DNA in vitro. J Biol Chem. 1999;274(30):21223–7. doi: 10.1074/jbc.274.30.21223 WOS:000081613100069. 10409678
51. de Jager M, Dronkert MLG, Modesti M, Beerens C, Kanaar R, van Gent DC. DNA-binding and strand-annealing activities of human Mre11: implications for its roles in DNA double-strand break repair pathways. Nucleic Acids Res. 2001;29(6):1317–25. doi: 10.1093/nar/29.6.1317 WOS:000167529200008. 11238998
52. Davis AJ, Chen DJ. DNA double strand break repair via non-homologous end-joining. Translational cancer research. 2013;2(3):130–43. doi: 10.3978/j.issn.2218-676X.2013.04.02 PMC3758668. 24000320
53. Daley JM, Sung P. 53BP1, BRCA1, and the Choice between Recombination and End Joining at DNA Double-Strand Breaks. Molecular and Cellular Biology. 2014;34(8):1380–8. doi: 10.1128/MCB.01639-13 PMC3993578. 24469398
54. Shiloh Y, Schans GPVD, Lohman PHML, Becker Y. Induction and repair of DNA damage in normal and ataxiatelangiectasia skin fibroblasts treated with neocarzinostatin. Carcinogenesis. 1983;4(7):917–21. doi: 10.1093/carcin/4.7.917 6223717
55. Lee C-S, Lee K, Legube G, Haber JE. Dynamics of yeast histone H2A and H2B phosphorylation in response to a double-strand break. Nature Structural &Amp; Molecular Biology. 2013;21:103. doi: 10.1038/nsmb.2737 https://www.nature.com/articles/nsmb.2737#supplementary-information. 24336221
56. Mah L-J, El-Osta A, Karagiannis TC. γH2AX as a molecular marker of aging and disease. Epigenetics. 2010;5(2):129–36. doi: 10.4161/epi.5.2.11080 20150765
57. Shao Z, Davis AJ, Fattah KR, So S, Sun J, Lee K-J, et al. Persistently bound Ku at DNA ends attenuates DNA end resection and homologous recombination. DNA Repair. 2012;11(3):310–6. doi: 10.1016/j.dnarep.2011.12.007 PMC3297478. 22265216
58. Lee K-J, Saha J, Sun J, Fattah KR, Wang S-C, Jakob B, et al. Phosphorylation of Ku dictates DNA double-strand break (DSB) repair pathway choice in S phase. Nucleic Acids Res. 2016;44(4):1732–45. doi: 10.1093/nar/gkv1499 26712563
59. Andrews BJ, Lehman JA, Turchi JJ. Kinetic analysis of the Ku-DNA binding activity reveals a redox-dependent alteration in protein structure that stimulates dissociation of the Ku-DNA complex. J Biol Chem. 2006;281(19):13596–603. doi: 10.1074/jbc.M512787200 WOS:000237336600069. 16537541
60. Postow L, Ghenoiu C, Woo EM, Krutchinsky AN, Chait BT, Funabiki H. Ku80 removal from DNA through double strand break-induced ubiquitylation. Journal of Cell Biology. 2008;182(3):467–79. doi: 10.1083/jcb.200802146 WOS:000258529100008. 18678709
61. Krasner DS, Daley JM, Sung P, Niu HY. Interplay between Ku and Replication Protein A in the Restriction of Exo1-mediated DNA Break End Resection. J Biol Chem. 2015;290(30):18806–16. doi: 10.1074/jbc.M115.660191 WOS:000358512100047. 26067273
62. Bakr A, Oing C, Kocher S, Borgmann K, Dornreiter I, Petersen C, et al. Involvement of ATM in homologous recombination after end resection and RAD51 nucleofilament formation. Nucleic Acids Res. 2015;43(6):3154–66. doi: 10.1093/nar/gkv160 WOS:000354719300022. 25753674
63. Godthelp BC, Artwert F, Joenje H, Zdzienicka MZ. Impaired DNA damage-induced nuclear Rad51 foci formation uniquely characterizes Fanconi anemia group D1. Oncogene. 2002;21(32):5002–5. doi: 10.1038/sj.onc.1205656 WOS:000176874800016. 12118380
64. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Current Biology. 2000;10(15):886–95. doi: 10.1016/s0960-9822(00)00610-2 WOS:000088979300016. 10959836
65. Wray J, Liu JM, Nickoloff JA, Shen ZY. Distinct RAD51 associations with RAD52 and BCCIP in response to DNA damage and replication stress. Cancer Res. 2008;68(8):2699–707. doi: 10.1158/0008-5472.CAN-07-6505 WOS:000255100500020. 18413737
66. Liu YL, Maizels N. Coordinated response of mammalian Rad51 and Rad52 to DNA damage. Embo Reports. 2000;1(1):85–90. doi: 10.1093/embo-reports/kvd002 WOS:000165765800020. 11256631
67. Li L. BRCA1 Forks Over New Roles in DNA-Damage Response–Before and Beyond the Breaks. Molecular Cell. 2011;44(2):174–6. doi: 10.1016/j.molcel.2011.10.003 22017867
68. Gonzalez-Prieto R, Munoz-Cabello AM, Cabello-Lobato MJ, Prado F. Rad51 replication fork recruitment is required for DNA damage tolerance. Embo Journal. 2013;32(9):1307–21. doi: 10.1038/emboj.2013.73 WOS:000319122600011. 23563117
69. Irmisch A, Ampatzidou E, Mizuno K, O'Connell MJ, Murray JM. Smc5/6 maintains stalled replication forks in a recombination-competent conformation. Embo Journal. 2009;28(2):144–55. doi: 10.1038/emboj.2008.273 WOS:000262580800009. 19158664
70. Hanamshet K, Mazina OM, Mazin AV. Reappearance from Obscurity: Mammalian Rad52 in Homologous Recombination. Genes. 2016;7(9). doi: 10.3390/genes7090063 WOS:000385535300009. 27649245
71. Lok BH, Carley AC, Tchang B, Powell SN. RAD52 inactivation is synthetically lethal with deficiencies in BRCA1 and PALB2 in addition to BRCA2 through RAD51-mediated homologous recombination. Oncogene. 2013;32(30):3552–8. doi: 10.1038/onc.2012.391 WOS:000322220800008. 22964643
72. Maya-Mendoza A, Moudry P, Merchut-Maya JM, Lee M, Strauss R, Bartek J. High speed of fork progression induces DNA replication stress and genomic instability. Nature. 2018;559(7713):279–84. doi: 10.1038/s41586-018-0261-5 29950726
73. Karanam K, Kafri R, Loewer A, Lahav G. Quantitative Live Cell Imaging Reveals a Gradual Shift between DNA Repair Mechanisms and a Maximal Use of HR in Mid S Phase. Molecular Cell. 2012;47(2):320–9. doi: 10.1016/j.molcel.2012.05.052 WOS:000307084000017. 22841003
74. Myler LR, Gallardo IF, Soniat MM, Deshpande RA, Gonzalez XB, Kim Y, et al. Single-Molecule Imaging Reveals How Mre11-Rad50-Nbs1 Initiates DNA Break Repair. Molecular Cell. 2017;67(5):891–8.e4. doi: 10.1016/j.molcel.2017.08.002 28867292
75. Chen Y-H, Jones MJK, Yin Y, Crist SB, Colnaghi L, Sims RJ III, et al. ATR-Mediated Phosphorylation of FANCI Regulates Dormant Origin Firing in Response to Replication Stress. Molecular Cell. 2015;58(2):323–38. doi: 10.1016/j.molcel.2015.02.031 WOS:000353222900013. 25843623
76. Yin YD, Rothenberg E. Probing the Spatial Organization of Molecular Complexes Using Triple-Pair-Correlation. Scientific Reports. 2016;6. doi: 10.1038/srep30819 WOS:000381698000001. 27545293
77. Teixeira-Silva A, Ait Saada A, Hardy J, Iraqui I, Nocente MC, Fréon K, et al. The end-joining factor Ku acts in the end-resection of double strand break-free arrested replication forks. Nature communications. 2017;8(1):1982–. doi: 10.1038/s41467-017-02144-5 29215009.
78. Cooper S. Reappraisal of serum starvation, the restriction point, G0, and G1 phase arrest points. Faseb Journal. 2003;17(3):333–40. doi: 10.1096/fj.02-0352rev WOS:000181892600032. 12631573
79. Wagner LM. Profile of veliparib and its potential in the treatment of solid tumors. Oncotargets and Therapy. 2015;8:1931–9. doi: 10.2147/OTT.S69935 WOS:000358650600001. 26251615
80. Whelan DR, Bell TDM. Image artifacts in Single Molecule Localization Microscopy: why optimization of sample preparation protocols matters. Scientific Reports. 2015;5. doi: 10.1038/srep07924 WOS:000348104600002. 25603780
81. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Methods. 2012;9(7):671–5. doi: 10.1038/nmeth.2089 WOS:000305942200020. 22930834
82. Henriques R, Lelek M, Fornasiero EF, Valtorta F, Zimmer C, Mhlanga MM. QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ. Nature Methods. 2010;7(5):339–40. doi: 10.1038/nmeth0510-339 WOS:000277175100006. 20431545
83. Gyori BM, Venkatachalam G, Thiagarajan PS, Hsu D, Clement MV. Open Comet: An automated tool for comet assay image analysis. Redox Biology. 2014nn2:457–65. doi: 10.1016/j.redox.2013.12.020 WOS:000350769600055. 24624335
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 12
- Antibiotika na nachlazení nezabírají! Jak můžeme zpomalit šíření rezistence?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- Ibuprofen jako alternativa antibiotik při léčbě infekcí močových cest
- Jak a kdy u celiakie začíná reakce na lepek? Možnou odpověď poodkryla čerstvá kanadská studie
Nejčtenější v tomto čísle
- Exploiting codon usage identifies intensity-specific modifiers of Ras/MAPK signaling in vivo
- Common maternal and fetal genetic variants show expected polygenic effects on risk of small- or large-for-gestational-age (SGA or LGA), except in the smallest 3% of babies
- PEA15 loss of function and defective cerebral development in the domestic cat
- Precision medicine in cats—The right biomedical model may not be the mouse!