A computational platform for robotized fluorescence microscopy (II): DNA damage, replication, checkpoint activation, and cell cycle progression by high-content high-resolution multiparameter image-cytometry

Cytometry Part A

Volumn 83 A, Issue 4, 2013, Pages 344-355

  Furia, Laura ^a   Pelicci, Pier Giuseppe ^a   Faretta, Mario ^a  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

Cell cycle; DNA damage response; Image cytometry

Indexed keywords

DNA; H2AFX PROTEIN, HUMAN; HISTONE; KI 67 ANTIGEN; P21 ACTIVATED KINASE; PROTEIN P53; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN;

ARTICLE; CELL CYCLE CHECKPOINT; CELL LINE; COMPUTER PROGRAM; CONFOCAL MICROSCOPY; CYTOLOGY; DNA DAMAGE; DNA REPLICATION; EPITHELIUM CELL; EQUIPMENT; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETICS; HUMAN; IMAGE CYTOMETRY; IMAGE PROCESSING; MAMMARY GLAND; METABOLISM; ROBOTICS; STANDARD; STATISTICS;

CELL CYCLE CHECKPOINTS; CELL LINE; DNA; DNA DAMAGE; DNA REPLICATION; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; HISTONES; HUMANS; IMAGE CYTOMETRY; IMAGE PROCESSING, COMPUTER-ASSISTED; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KI-67 ANTIGEN; MAMMARY GLANDS, HUMAN; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; P21-ACTIVATED KINASES; ROBOTICS; SOFTWARE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84875519987     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.22265     Document Type: Article

References (52)

1. Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008; 319: 1352-1355.
2. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009; 461: 1071-1078.
3. Lamarche BJ, Orazio NI, Weitzman MD. The MRN complex in double-strand break repair and telomere maintenance. FEBS Lett 2010; 584: 3682-3695.
4. Kim JE, Minter-Dykhouse K, Chen J. Signaling networks controlled by the MRN complex and MDC1 during early DNA damage responses. Mol Carcinog 2006; 45: 403-408.
5. Lisby M, Rothstein R. Choreography of recombination proteins during the DNA damage response. DNA Repair (Amst) 2009; 8: 1068-1076.
6. Rupnik A, Lowndes NF, Grenon M. MRN and the race to the break. Chromosoma 2010; 119: 115-35.
7. Darzynkiewicz Z, Traganos F, Zhao H, Halicka HD, Skommer J, Wlodkowic D. Analysis of individual molecular events of DNA damage response by flow- and image-assisted cytometry. Methods Cell Biol 2011; 103: 115-147.
8. Tanaka T, Halicka D, Traganos F, Darzynkiewicz Z. Cytometric analysis of DNA damage: Phosphorylation of histone H2AX as a marker of DNA double-strand breaks (DSBs). Methods Mol Biol 2009; 523: 161-168.
9. Beck H, Menzel T, Syljuasen RG, Sorensen CS. High-throughput siRNA screens using gammaH2AX as marker uncover key regulators of genome integrity in mammalian cells. Cell Cycle 2010; 9: 2257-2258.
10. Lowndes NF, Toh GW. DNA repair: The importance of phosphorylating histone H2AX. Curr Biol 2005; 15: R99-R102.
11. Mah LJ, El-Osta A, Karagiannis TC. gammaH2AX: A sensitive molecular marker of DNA damage and repair. Leukemia 2010; 24: 679-686.
12. Srivastava N, Gochhait S, de Boer P, Bamezai RN. Role of H2AX in DNA damage response and human cancers. Mutat Res 2009; 681: 180-188.
13. Cleaver JE. gammaH2Ax: Biomarker of damage or functional participant in DNA repair "all that glitters is not gold!". Photochem Photobiol 2011; 87: 1230-1239.
14. Cleaver JE, Feeney L, Revet I. Phosphorylated H2Ax is not an unambiguous marker for DNA double-strand breaks. Cell Cycle 2011; 10: 3223-3224.
15. de Feraudy S, Revet I, Bezrookove V, Feeney L, Cleaver JE. A minority of foci or pan-nuclear apoptotic staining of gammaH2AX in the S phase after UV damage contain DNA double-strand breaks. Proc Natl Acad Sci USA 2010; 107: 6870-6875.
16. Revet I, Feeney L, Bruguera S, Wilson W, Dong TK, Oh DH, Dankort D, Cleaver JE. Functional relevance of the histone gammaH2Ax in the response to DNA damaging agents. Proc Natl Acad Sci USA 2011; 108: 8663-8667.
17. Takahashi A, Ohnishi T. Does gammaH2AX foci formation depend on the presence of DNA double strand breaks?. Cancer Lett 2005; 229: 171-179.
18. Goodarzi AA, Jeggo P, Lobrich M. The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair (Amst) 2010; 9: 1273-1282.
19. Goodarzi AA, Noon AT, Jeggo PA. The impact of heterochromatin on DSB repair. Biochem Soc Trans 2009; 37: 569-576.
20. Langerak P, Russell P. Regulatory networks integrating cell cycle control with DNA damage checkpoints and double-strand break repair. Philos Trans R Soc Lond B Biol Sci 2011; 366: 3562-3571.
21. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, Hiddingh S, Thanasoula M, Kulkarni A, Yang Q, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 2010; 17: 688-695.
22. Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010; 141: 243-254.
23. Harrigan JA, Belotserkovskaya R, Coates J, Dimitrova DS, Polo SE, Bradshaw CR, Fraser P, Jackson SP. Replication stress induces 53BP1-containing OPT domains in G1 cells. J Cell Biol 2011; 193: 97-108.
24. Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, Pedersen RS, Grofte M, Chan KL, Hickson ID, Bartek J, et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 2011; 13: 243-253.
25. Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, Morales JC, Naka K, Xia Z, Camerini-Otero RD, Motoyama N, et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 2002; 4: 993-997.
26. Yu T, MacPhail SH, Banath JP, Klokov D, Olive PL. Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability. DNA Repair (Amst) 2006; 5: 935-946.
27. Gerashchenko BI, Dynlacht JR. A tool for enhancement and scoring of DNA repair foci. Cytometry Part A 2009; 75A: 245-252.
28. Darzynkiewicz Z, Halicka DH, Tanaka T. Cytometric assessment of DNA damage induced by DNA topoisomerase inhibitors. Methods Mol Biol 2009; 582: 145-153.
29. Darzynkiewicz Z, Halicka HD, Zhao H, Podhorecka M. Cell synchronization by inhibitors of DNA replication induces replication stress and DNA damage response: Analysis by flow cytometry. Methods Mol Biol 2011; 761: 85-96.
30. Huang X, Halicka HD, Traganos F, Tanaka T, Kurose A, Darzynkiewicz Z. Cytometric assessment of DNA damage in relation to cell cycle phase and apoptosis. Cell Prolif 2005; 38: 223-243.
31. Tanaka T, Huang X, Halicka HD, Zhao H, Traganos F, Albino AP, Dai W, Darzynkiewicz Z. Cytometry of ATM activation and histone H2AX phosphorylation to estimate extent of DNA damage induced by exogenous agents. Cytometry Part A 2007; 71A: 648-661.
32. Zhao H, Dobrucki J, Rybak P, Traganos F, Dorota Halicka H, Darzynkiewicz Z. Induction of DNA damage signaling by oxidative stress in relation to DNA replication as detected using "click chemistry". Cytometry Part A 2011; 79A: 897-902.
33. Zhao H, Traganos F, Darzynkiewicz Z. Kinetics of the UV-induced DNA damage response in relation to cell cycle phase. Correlation with DNA replication. Cytometry Part A 2010; 77A: 285-293.
34. 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 G1-phase cells. Radiat Res 2003; 159: 759-767.
35. Cai Z, Vallis KA, Reilly RM. Computational analysis of the number, area and density of gamma-H2AX foci in breast cancer cells exposed to (111)In-DTPA-hEGF or gamma-rays using Image-J software. Int J Radiat Biol 2009; 85: 262-271.
36. Gonzalez JE, Lee M, Barquinero JF, Valente M, Roch-Lefevre S, Garcia O. Quantitative image analysis of gamma-H2AX foci induced by ionizing radiation applying open source programs. Anal Quant Cytol Histol 2012; 34: 66-71.
37. Ishikawa A, Yamauchi M, Suzuki K, Yamashita S. Image-based quantitative determination of DNA damage signal reveals a threshold for G2 checkpoint activation in response to ionizing radiation. Genome Integr 2010; 1: 10.
38. Jucha A, Wegierek-Ciuk A, Koza Z, Lisowska H, Wojcik A, Wojewodzka M, Lankoff A. FociCounter: A freely available PC programme for quantitative and qualitative analysis of gamma-H2AX foci. Mutat Res 2010; 696: 16-20.
39. Mistrik M, Oplustilova L, Lukas J, Bartek J. Low-dose DNA damage and replication stress responses quantified by optimized automated single-cell image analysis. Cell Cycle 2009; 8: 2592-2599.
40. Hou YN, Lavaf A, Huang D, Peters S, Huq R, Friedrich V, Rosenstein BS, Kao J. Development of an automated gamma-H2AX immunocytochemistry assay. Radiat Res 2009; 171: 360-367.
41. Salic A, Mitchison TJ. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci USA 2008; 105: 2415-2420.
42. Chagin VO, Stear JH, Cardoso MC. Organization of DNA replication. Cold Spring Harb Perspect Biol 2010; 2: a000737.
43. Shibata A, Barton O, Noon AT, Dahm K, Deckbar D, Goodarzi AA, Lobrich M, Jeggo PA. Role of ATM and the damage response mediator proteins 53BP1 and MDC1 in the maintenance of G(2)/M checkpoint arrest. Mol Cell Biol 2010; 30: 3371-3383.
44. Stiff T, Cerosaletti K, Concannon P, O'Driscoll M, Jeggo PA. Replication independent ATR signalling leads to G2/M arrest requiring Nbs1, 53BP1 and MDC1. Hum Mol Genet 2008; 17: 3247-3253.
45. Leuchowius KJ, Weibrecht I, Soderberg O. In situ proximity ligation assay for microscopy and flow cytometry. Curr Protoc Cytom 2011;Chapter 9:Unit 9 36.
46. Mallette FA, Ferbeyre G. The DNA damage signaling pathway connects oncogenic stress to cellular senescence. Cell Cycle 2007; 6: 1831-1836.
47. Mallette FA, Gaumont-Leclerc MF, Ferbeyre G. The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev 2007; 21: 43-48.
48. Vilenchik MM, Knudson AG. Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci USA 2003; 100: 12871-12876.
49. Zhao H, Tanaka T, Halicka HD, Traganos F, Zarebski M, Dobrucki J, Darzynkiewicz Z. Cytometric assessment of DNA damage by exogenous and endogenous oxidants reports aging-related processes. Cytometry Part A 2007; 71A: 905-914.
50. Giunta S, Belotserkovskaya R, Jackson SP. DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol 2010; 190: 197-207.
51. Lowndes NF. The interplay between BRCA1 and 53BP1 influences death, aging, senescence and cancer. DNA Repair (Amst); 9: 1112-1116.
52. Sengupta S, Linke SP, Pedeux R, Yang Q, Farnsworth J, Garfield SH, Valerie K, Shay JW, Ellis NA, Wasylyk B, et al. BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J 2003; 22: 1210-1222.