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Research Paper

Measuring cell cycle-dependent DNA damage responses and p53 regulation on a cell-by-cell basis from image analysis

ORCID Icon & ORCID Icon
Pages 1358-1371 | Received 11 Jan 2018, Accepted 11 May 2018, Published online: 25 Jul 2018

References

  • Marnett LJ. Oxyradicals and DNA damage. Carcinogenesis. 2000;21(3):361–370.
  • Friedberg EC, Walker GC, Siede W, et al. DNA repair and mutagenesis. ASM Press; 2006. DOI:10.1097/01.shk.0000232588.61871.ff
  • Branzei D, Foiani M. Regulation of DNA Repair Throughout the Cell Cycle. Nat Rev Mol Cell Biol. 2008;9(4):297–308.
  • Schroering AG, Edelbrock MA, Richards TJ, et al. The cell cycle and DNA mismatch repair. Exp Cell Res. 2007;313(2):292–304.
  • Chaudhry MA. Base excision repair of ionizing radiation-induced DNA damage in G1 and G2 cell cycle phases. Cancer Cell Int. 2007;7:15.
  • Malkin D, Li FP, Strong LC, et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science (New York, N.Y.). 1990;250(4985):1233–1238.
  • Classon M, Harlow E. The retinoblastoma tumour suppressor in development and cancer. Nat Rev Cancer. 2002;2(12):910–917.
  • Bartek J, Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell. 2003;3(5):421–429.
  • Jazayeri A, Falck J, Lukas C, et al. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol. 2006;8(1):37–45.
  • Escribano-Díaz C, Orthwein A, Fradet-Turcotte A, et al. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol Cell. 2013;49(5):872–883.
  • Chen F, Nastasi A, Shen Z, et al. Cell cycle-dependent protein expression of mammalian homologs of yeast DNA double-strand break repair genes Rad51 and Rad52. DNA Repair. 1997;384(3):205–211.
  • Halicka HD, Huang X, Traganos F, et al. Histone H2AX phosphorylation after cell irradiation with UV-B: relationship to cell cycle phase and induction of apoptosis. Cell Cycle. 2005;4(2):339–345.
  • Chen L, Nievera CJ, Lee AY-L, et al. Cell Cycle-dependent complex formation of BRCA•CtIP•MRN is important for DNA double-strand break repair. J Biol Chem. 2008;283(12):7713–7720.
  • Kaneko YS, Watanabe N, Morisaki H, et al. Cell-cycle-dependent and ATM-independent expression of human Chk1 kinase. Oncogene. 1999;18(25):3673–3681.
  • Karanam K, Kafri R, Loewer A, et al. Quantitative live cell imaging reveals a gradual shift between DNA repair mechanisms and a maximal use of HR in Mid S phase. Mol Cell. 2012;47(2):320–329.
  • Ichijima Y, Sakasai R, Okita N, et al. Phosphorylation of histone H2AX at M phase in human cells without DNA damage response. Biochem Biophys Res Commun. 2005;336(3):807–812.
  • Reisman D, Takahashi P, Polson A, et al. Transcriptional regulation of the p53 tumor suppressor gene in S-phase of the cell-cycle and the cellular response to DNA damage. Biochem Res Int. 2012;2012. DOI:10.1155/2012/808934
  • Katsumoto T, Higaki K, Ohno K, et al. Cell-cycle dependent biosynthesis and localization of p53 protein in untransformed human cells. Biol Cell. 1995;84(3):167–173.
  • Guo Z, Kumagai A, Wang SX, et al. Requirement for Atr in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev. 2000;14(21):2745–2756.
  • Shi Y, Felley-Bosco E, Marti TM, et al. Starvation-induced activation of ATM/Chk2/p53 signaling sensitizes cancer cells to cisplatin. BMC Cancer. 2012;12:571.
  • Lu C, Shi Y, Wang Z, et al. Serum starvation induces H2AX phosphorylation to regulate apoptosis via p38 MAPK pathway. FEBS Lett. 2008;582(18):2703–2708.
  • Hasan NM, Adams GE, Joiner MC. Effect of serum starvation on expression and phosphorylation of PKC-alpha and p53 in V79 cells: implications for cell death. Int J Cancer. 1999;80(3):400–405.
  • Pelkmans L. Cell Biology. Using cell-to-cell variability–a new era in molecular biology. Science (New York, N.Y.). 2012;336(6080):425–426.
  • Altschuler SJ, Wu LF. Cellular heterogeneity: do differences make a difference? Cell. 2010;141(4):559–563.
  • Huang X, Halicka HD, Traganos F, et al. Cytometric assessment of DNA damage in relation to cell cycle phase and apoptosis. Cell Prolif. 2005;38(4):223–243.
  • Mazumder A, Tummler K, Bathe M, et al. Single-cell analysis of ribonucleotide reductase transcriptional and translational response to DNA damage. Mol Cell Biol. 2013;33(3):635–642.
  • Raj A, Van Den Bogaard P, Rifkin SA, et al. Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods. 2008;5(10):877–879.
  • Zenklusen D, Larson DR, Singer RH. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat Struct Mol Biol. 2008;15(12):1263–1271.
  • Bocker W, Gatenberg H-W, Muller WU, et al. Automated cell cycle analysis with fluorescence microscopy and image analysis. Phys Med Biol. 1996;41:523–537.
  • Roukos V, Pegoraro G, Voss TC, et al. Cell cycle staging of individual cells by fluorescence microscopy. Nat Protoc. 2015;10(2):334–348.
  • Mazumder A, Pesudo LQ, McRee S, et al. Genome-wide single-cell-level screen for protein abundance and localization changes in response to DNA damage in S. cerevisiae. Nucleic Acids Res. 2013;41(20):9310–9324.
  • Sengupta S, Harris CC. p53: traffic cop at the crossroads of DNA repair and recombination. Nat Rev Mol Biol. 2005;6(1):44–55.
  • Dulić V, Lees E, Reed SI. Association of human cyclin E with a periodic G1-S phase protein kinase. Science. 1992;257(5078):1958–1961.
  • Pagano M, Pepperkok R, Verde F, et al. Cyclin A is required at two points in the human cell cycle. EMBO J. 1992;11(3):961–971.
  • Henglein B, Chenivesse X, Wang J, et al. Structure and cell cycle-regulated transcription of the human cyclin A gene. Proc Natl Acad Sci U S A. 1994;91(12):5490–5494.
  • Geng Y, Eaton EN, Picón M, et al. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene. 1996;12(6):1173–1180. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8649818
  • Padovan-Merhar O, Nair GP, Biaesch AG, et al. Single mammalian cells compensate for differences in cellular volume and DNA copy number through independent global transcriptional mechanisms. Mol Cell. 2015;58(2):339–352.
  • Sakaue-Sawano A, Kurokawa H, Morimura T, et al. Visualizing Spatiotemporal Dynamics of Multicellular Cell-Cycle Progression. Cell. 2008;132(3):487–498.
  • Rickles R, Marashi F, Sierra F, et al. Analysis of histone gene expression during the cell cycle in HeLa cells by using cloned human histone genes. Proc Natl Acad Sci U S A. 1982;79(3):749–753.
  • Osley MA. The regulation of histone synthesis in the cell cycle. Annu Rev Biochem. 1991;60(1):827–861.
  • Lemaître C, Grabarz A, Tsouroula K. Nuclear position dictates DNA repair pathway choice Nuclear position dictates DNA repair pathway choice. Genes Dev. 2014;0–14. DOI:10.1101/gad.248369.114
  • Soutoglou E, Misteli T. Activation of the cellular DNA damage response in the absence of DNA lesions. Science (New York, N.Y.). 2008;320(5882):1507–1510.
  • Fragkos M, Jurvansuu J, Beard P. H2AX is required for cell cycle arrest via the p53/p21 pathway. Mol Cell Biol. 2009;29(10):2828–2840.
  • Efeyan A, Serrano M. p53: guardian of the genome and policeman of the oncogenes. Cell Cycle. 2007;6(9):1006–1010.
  • Smith ML, Seo YR. p53 regulation of DNA excision repair pathways. Mutagenesis. 2002;17(2):149–156.
  • Mesaeli N, Phillipson C. Impaired p53 expression, function, and nuclear localization in calreticulin-deficient cells. Mol Biol Cell. 2004;15(4):1862–1870.
  • Ofir-Rosenfeld Y, Boggs K, Michael D, et al. Mdm2 regulates p53 mRNA Translation through inhibitory interactions with ribosomal protein L26. Mol Cell. 2008;32(2):180–189.
  • Yajima H, Lee K-J, Zhang S, et al. DNA double-strand break formation upon UV-induced replication stress activates ATM and DNA-PKcs kinases. J Mol Biol. 2009;385(3):800–810.
  • Miao Z-H, Rao VA, Agama K, et al. 4-nitroquinoline-1-oxide induces the formation of cellular topoisomerase I-DNA cleavage complexes. Cancer Res. 2006;66(13):6540–6545.
  • Banáth JP, Olive PL. Expression of phosphorylated histone H2AX as a surrogate of cell killing by drugs that create DNA double-strand breaks. Cancer Res. 2003;63(15):4347–4350. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12907603
  • Ashcroft M, Kubbutat MH, Vousden KH. Regulation of p53 function and stability by phosphorylation. Mol Cell Biol. 1999;19(3):1751–1758.
  • Kurihara A, Nagoshi H, Yabuki M, et al. Ser 46 phosphorylation of p53 is not always sufficient to induce apoptosis: multiple mechanisms of regulation of p53-dependent apoptosis. Genes to Cells. 2007;12(7):853–861.
  • Smeenk L, Van Heeringen SJ, Koeppel M, et al. Role of p53 serine 46 in p53 target gene regulation. Plos One. 2011;6(3):e17574.
  • Fu L, Minden MD, Benchimol S. Translational regulation of human p53 gene expression. EMBO J. 1996;15(16):4392–4401.
  • Lakin ND, Jackson SP. Regulation of p53 in response to DNA damage. Oncogene. 1999;18(53):7644–7655.
  • Kastan MB, Onyekwere O, Sidransky D, et al. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 1991;51(23 Pt 1):6304–6311. Available from: http://www.ncbi.nlm.nih.gov/pubmed/1933891
  • Marine J-C. P53 stabilization: the importance of nuclear import. Cell Death Differ. 2010;17(2):191–192.
  • Shirangi TR, Zaika A, Moll UM. Nuclear degradation of p53 occurs during down-regulation of the p53 response after DNA damage. FASEB J. 2002;16(3):420–422.
  • Giunta S, Belotserkovskaya R, Jackson SP. DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol. 2010;190(2):197–207.
  • Arrigucci R, Bushkin Y, Radford F, et al. FISH-Flow, a protocol for the concurrent detection of mRNA and protein in single cells using fluorescence in situ hybridization and flow cytometry. Nat Protoc. 2017;12(6):1245–1260.
  • Baerlocher GM, Vulto I, De Jong G, et al. Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat Protoc. 2006;1(5):2365–2376.
  • Skinner SO, Xu H, Nagarkar-Jaiswal S, et al. Single-cell analysis of transcription kinetics across the cell cycle. eLife. 2016;5:e12175.
  • Brooks CL, Gu W. p53 ubiquitination: mdm2 and beyond. Mol Cell. 2006;21(3):307–315.
  • Trotta E, Paci M. Solution structure of DAPI selectively bound in the minor groove of DNA T·T mismatch-containing site: NMR and molecular dynamics studies. Nucleic Acids Res. 1998;26(20):4706–4713.
  • Dean PN, Jett JH. Mathematical analysis of DNA distributions derived from flow microfluorometry. J Cell Biol. 1974;60(2):523–527. Available from: http://www.ncbi.nlm.nih.gov/pubmed/4855906

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