ATM acts downstream of ATR in the DNA damage response signaling of bystander cells

Cancer Research

Volumn 68, Issue 17, 2008, Pages 7059-7065

  Burdak Rothkamm, Susanne ^a   Rothkamm, Kai ^b,c   Prise, Kevin M ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; BRCA1 PROTEIN; DNA DEPENDENT PROTEIN KINASE; PROTEIN 53BP1; PROTEIN P21; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; ATR PROTEIN, HUMAN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; PROTEIN SERINE THREONINE KINASE; TP53BP1 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; BYSTANDER EFFECT; CELL SURVIVAL; CLONOGENESIS; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RADIATION; SIGNAL TRANSDUCTION; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

BYSTANDER EFFECT; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA DAMAGE; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 52049090123     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-0545     Document Type: Article

References (47)

1. Shao C, Stewart V, Folkard M, Michael BD, Prise KM. Nitric oxide-mediated signaling in the bystander response of individually targeted glioma cells. Cancer Res 2003;63:8437-42.
2. Shao C, Folkard M, Michael BD, Prise KM. Targeted cytoplasmic irradiation induces bystander responses. Proc Natl Acad Sci U S A 2004;101:13495-500.
3. Mothersill C, Seymour CB. Radiation-induced bystander effects-implications for cancer. Nat Rev Cancer 2004;4:158-64.
4. Belyakov OV, Mitchell SA, Parikh D, et al. Biological effects in unirradiated human tissue induced by radiation damage up to 1 mm away. Proc Natl Acad Sci U S A 2005;102:14203-8.
5. Huang L, Kim PM, Nickoloff JA, Morgan WF. Targeted and nontargeted effects of low-dose ionizing radiation on delayed genomic instability in human cells. Cancer Res 2007;67:1099-104.
6. Morgan WF, Sowa MB. Effects of ionizing radiation in nonirradiated cells. Proc Natl Acad Sci U S A 2005;102:14127-8.
7. Sokolov MV, Smilenov LB, Hall EJ, et al. Ionizing radiation induces DNA double-strand breaks in bystander primary human fibroblasts. Oncogene 2005;24:7257-65.
8. Burdak-Rothkamm S, Short SC, Folkard M, Rothkamm K, Prise KM. ATR-dependent radiation-induced γH2AX foci in bystander primary human astrocytes and glioma cells. Oncogene 2007;26:993-1002.
9. Han W, Wu L, Chen S, et al. Constitutive nitric oxide acting as a possible intercellular signaling molecule in the initiation of radiation-induced DNA double strand breaks in non-irradiated bystander cells. Oncogene 2007;26:2330-9.
10. Yang H, Asaad N, Held KD. Medium-mediated intercellular communication is involved in bystander responses of X-ray-irradiated normal human fibroblasts. Oncogene 2005;24:2096-103.
11. Hu B, Wu L, Han W, et al. The time and spatial effects of bystander response in mammalian cells induced by low dose radiation. Carcinogenesis 2006;27:245-51.
12. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998;273:5858-68.
13. Prise KM, Folkard M, Kuosaite V, et al. What role for DNA damage and repair in the bystander response? Mutat Res 2006;597:1-4.
14. Ewald B, Sampath D, Plunkett W. H2AX phosphorylation marks gemcitabine-induced stalled replication forks and their collapse upon S-phase checkpoint abrogation. Mol Cancer Ther 2007;6:1239-48.
15. Andreassen PR, Ho GP, D'Andrea AD. DNA damage responses and their many interactions with the replication fork. Carcinogenesis 2006;27:883-92.
16. Rouse J, Jackson SP. Interfaces between the detection, signaling, and repair of DNA damage. Science 2002;297:547-51.
17. Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003;300:1542-8.
18. Adams KE, Medhurst AL, Dart DA, Lakin ND. Recruitment of ATR to sites of ionising radiation-induced DNA damage requires ATM and components of the MRN protein complex. Oncogene 2006;25:3894-904.
19. Stiff T, Walker SA, Cerosaletti K, et al. ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J 2006;25:5775-82.
20. Matsuoka S, Ballif BA, Smogorzewska A, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007;316:1160-6.
21. Lees-Miller SP, Godbout R, Chan DW, et al. Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science 1995;267:1183-5.
22. Reitsema T, Klokov D, Banath JP, Olive PL. DNA-PK is responsible for enhanced phosphorylation of histone H2AX under hypertonic conditions. DNA Repair (Amst) 2005;4:1172-81.
23. Karimi-Busheri F, Rasouli-Nia A, Allalunis-Turner J, Weinfeld M. Human polynucleotide kinase participates in repair of DNA double-strand breaks by nonhomologous end joining but not homologous recombination. Cancer Res 2007;67:6619-25.
24. Povirk LF, Zhou RZ, Ramsden DA, Lees-Miller SP, Valerie K. Phosphorylation in the serine/threonine 2609-2647 cluster promotes but is not essential for DNA-dependent protein kinase-mediated nonhomologous end joining in human whole-cell extracts. Nucleic Acids Res 2007;35:3869-78.
25. Daido S, Yamamoto A, Fujiwara K, et al. Inhibition of the DNA-dependent protein kinase catalytic subunit radiosensitizes malignant glioma cells by inducing autophagy. Cancer Res 2005;65:4368-75.
26. O'Driscoll M, Ruiz-Perez VL, Woods CG, Jeggo PA, Goodship JA. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat Genet 2003;33:497-501.
27. Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 1992;103:857-62.
28. Costes SV, Daelemans D, Cho EH, et al. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 2004;86:3993-4003.
29. Shao C, Folkard M, Michael BD, Prise KM. Bystander signaling between glioma cells and fibroblasts targeted with counted particles. Int J Cancer 2005;116:45-51.
30. Sarkaria JN, Busby EC, Tibbetts RS, et al. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 1999;59:4375-82.
31. Cortez D. Caffeine inhibits checkpoint responses without inhibiting the ataxia-telangiectasia-mutated (ATM) and ATM- and Rad3-related (ATR) protein kinases. J Biol Chem 2003;278:37139-45.
32. Adams MM, Carpenter PB. Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Div 2006;1:19.
33. Anderson L, Henderson C, Adachi Y. Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol Cell Biol 2001;21:1719-29.
34. Bekker-Jensen S, Lukas C, Melander F, Bartek J, Lukas J. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J Cell Biol 2005;170:201-11.
35. Mochan TA, Venere M, DiTullio RA, Jr., Halazonetis TD. 53BP1, an activator of ATM in response to DNA damage. DNA Repair (Amst) 2004;3:945-52.
36. Ward IM, Minn K, Jorda KG, Chen J. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J Biol Chem 2003;278:19579-82.
37. Tartier L, Gilchrist S, Burdak-Rothkamm S, Folkard M, Prise KM. Cytoplasmic irradiation induces mitochondrial-dependent 53BP1 protein relocalization in irradiated and bystander cells. Cancer Res 2007;67:5872-9.
38. Hickson I, Zhao Y, Richardson CJ, et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 2004;64:9152-9.
39. Veuger SJ, Curtin NJ, Richardson CJ, Smith GC, Durkacz BW. Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1. Cancer Res 2003;63:6008-15.
40. Belyakov OV, Folkard M, Mothersill C, Prise KM, Michael BD. Bystander-induced apoptosis and premature differentiation in primary urothelial explants after charged particle microbeam irradiation. Radiat Prot Dosimetry 2002;99:249-51.
41. Lyng FM, Maguire P, Kilmurray N, et al. Apoptosis is initiated in human keratinocytes exposed to signalling factors from microbeam irradiated cells. Int J Radiat Biol 2006;82:393-9.
42. Enns L, Bogen KT, Wizniak J, Murtha AD, Weinfeld M. Low-dose radiation hypersensitivity is associated with p53-dependent apoptosis. Mol Cancer Res 2004;2:557-66.
43. Nagasawa H, Little JB. Unexpected sensitivity to the induction of mutations by very low doses of α-particle radiation: evidence for a bystander effect. Radiat Res 1999;152:552-7.
44. Hu T, Miller CM, Ridder GM, Aardema MJ. Characterization of p53 in Chinese hamster cell lines CHO-K1, CHO-WBL, and CHL: implications for genotoxicity testing. Mutat Res 1999;426:51-62.
45. Zhang Y, Zhou J, Held KD, et al. Deficiencies of double-strand break repair factors and effects on mutagenesis in directly γ-irradiated and medium-mediated bystander human lymphoblastoid cells. Radiat Res 2008;169:197-206.
46. Bowler DA, Moore SR, Macdonald DA, et al. Bystander-mediated genomic instability after high LET radiation in murine primary haemopoietic stem cells. Mutat Res 2006;597:50-61.
47. Lorimore SA, Coates PJ, Wright EG. Radiation-induced genomic instability and bystander effects: inter-related nontargeted effects of exposure to ionizing radiation. Oncogene 2003;22:7058-69.