DNA damage response induced by tobacco smoke in normal human bronchial epithelial and A549 pulmonary adenocarcinoma cells assessed by laser scanning cytometry

Cytometry Part A

Volumn 75, Issue 10, 2009, Pages 840-847

  Zhao, Hong ^a   Albino, Anthony P ^a,b   Jorgensen, Ellen ^a,b   Traganos, Frank ^a   Darzynkiewicz, Zbigniew ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b Vector Research Ltd   (United States)

Author keywords

ATM activation; Cell cycle; Checkpoint; Chk2 activation; gammaH2AX; Histone H2AX phosphorylation; Laser scanning cytometry; Ser15 p53 phosphorylation

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 2; HISTONE H2AX; PROTEIN P53; SERINE; THREONINE;

ARTICLE; BRONCHUS; CANCER CELL; CELL CYCLE PHASE; CELL TYPE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; EPITHELIUM CELL; GENOTOXICITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; KINETICS; LASER SCANNING CYTOMETRY; LUNG ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SMOKING;

BRONCHI; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA DAMAGE; DNA-BINDING PROTEINS; EPITHELIAL CELLS; HISTONES; HUMANS; LASER SCANNING CYTOMETRY; PHOSPHOSERINE; PROTEIN-SERINE-THREONINE KINASES; SMOKING; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 70349495882     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.20778     Document Type: Article

References (72)

1. Hecht SS. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat Rev Cancer 2003;3:733-744. (Pubitemid 37328812)
2. Vineis P, Alavanja M, Buffler P, Fontham E, Franceschi S, Gao YT, Gupta PC, Hackshaw A, Matos E, Samet J, Sitas F, Smith J, Stayner L, Straif K, Thun MJ, Wichmann HE, Wu AH, Zaridze D, Peto R, Doll, R. Tobacco and cancer: Recent epidemiological evidence. J Natl Cancer Inst 2004;96:99-106.
3. Rubin H. Synergistic mechanisms in carcinogenesis by polycyclic aromatic hydrocarbons and by tobacco smoke: A bio-historical perspective with updates. Carcinogenesis 2001;22:1903-1930. (Pubitemid 34065385)
4. DeMarini DM. Genotoxicity of tobacco smoke and tobacco smoke condensate: A review. Mutat Res 2004;567:447-474.
5. Fowles J, Dybing E. Application of toxicological risk assessment principles to the chemical constituents of cigarette smoke. Tob Control 2003;2:424-430. (Pubitemid 39452045)
6. Hoffman D, Hecht SS. Advances in tobacco carcinogenesis. In: Cooper CS, Grover PL, editors. Handbook of Experimental Pharmacology. Heidelberg: Springer-Verlag; 1990. pp 63-102.
7. International Agency for Research on Cancer. Tobacco smoke and involuntary smoking. In: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol.83. Lyon, France: IARC; 2004. pp 1012-1065.
8. Hecht SS. Progress and challenges in selected areas of tobacco carcinogenesis. Chem Res Toxicol 2008;21:160-171.
9. Hatsukami DK, Benowitz NL, Rennard SI, Oncken C, Hecht SS. Biomarkers to assess the utility of potential reduced exposure tobacco products. Nicotine Tob Res 2006;8:600-622. (Pubitemid 43675073)
10. Kim TM, Yim SH, Lee JS, Kwon MS, Ryu JW, Kang HM, Fiegler H, Carter NP, Chung YJ. Genome-wide screening of genomic alterations and their clinico-pathologic implications in non-small cell lung cancers. Clin Cancer Res 2005;11:8235-8242. (Pubitemid 41746932)
11. Laugesen M, Fowles J. Scope for regulation of cigarette smoke toxicity according to brand differences in toxicant emissions. N Z Med J 2005;118:U1401. (Pubitemid 41519570)
12. Pankow JF. A consideration of the role of gas/particle partitioning in the deposition of nicotine and other tobacco smoke compounds in the respiratory tract. Chem Res Toxicol 2001;4:1465-1481.
13. Franklin WA, Gazdar AF, Haney J, Wistuba II, La Rosa FG, Kennedy T, Ritchey DM, Miller YE. Widely dispersed p53 mutation in respiratory epithelium. A novel mechanism for field carcinogenesis. J Clin Invest 1997;100:2133-2137. (Pubitemid 27459370)
14. Fujii T, Dracheva T, Player A, Chacko S, Clifford R, Strausberg RL, Buetow K, Azumi N, Travis WD, Jen J. A preliminary transcriptome map of non-small cell lung cancer. Cancer Res 2002;62:3340-3346. (Pubitemid 34651374)
15. Guo M, House MG, Hooker C, Han Y, Heath E, Gabrielson E, Yang SC, Baylin SB, Herman JG, Brock MV. Promoter hypermethylation of resected bronchial margins: A field defect of changes? Clin Cancer Res 2004;10:5131-5136.
16. Minna JD, Fong K, Zochbauer-Muller S, Gazdar AF. Molecular pathogenesis of lung cancer and potential translational applications. Cancer J 2002;8 (Suppl 1):S41-S46.
17. Sikkink SK, Liloglou T, Maloney P, Gosney JR, Field JK. In-depth analysis of molecular alterations within normal and tumour tissue from an entire bronchial tree. Int J Oncol 2003;22:589-595.
18. Godtfredsen NS, Prescott E, Osler M. Effect of smoking reduction on lung cancer risk. JAMA 2005;294:1505-1510. (Pubitemid 41362687)
19. Kiyohara C, Takayama K, Nakanishi Y. Association of genetic polymorphisms in the base excision repair pathway with lung cancer risk: A meta-analysis. Lung Cancer 2006;54267-54283 (Pubitemid 44634141)
20. Wu X, Gu J, Spitz MR. Mutagen sensitivity: A genetic predisposition factor for cancer. Cancer Res 2007;67:3493-3495. (Pubitemid 46762125)
21. Elliott B, Jasin M. Double-strand breaks and translocations in cancer. Cell Mol Life Sci 2002;59:373-385.
22. Masuda A, Takahashi T. Chromosome instability in human lung cancers: Possible underlying mechanisms and potential consequences in the pathogenesis. Oncogene 2002;21:6884-6897. (Pubitemid 35221935)
23. Mills KD, Ferguson DO, Alt FW. The role of DNA breaks in genomic instability and tumorigenesis. Immunol Rev 2003;194:77-95. (Pubitemid 36886430)
24. Sekido Y, Fong KM, Minna JD. Molecular genetics of lung cancer. Annu Rev Med 2003;54:73-87.
25. Albino AP, Huang X, Yang J, Gietl D, Jorgensen E, Traganos F, Darzynkiewicz Z. Induction of histone H2AX phosphorylation in A549 human pulmonary epithelial cells by tobacco smoke and in human bronchial epithelial cells by smoke condensate: A new assay to detect the presence of potential carcinogens in tobacco. Cell Cycle 2004;3:1062-1068.
26. Albino AP, Huang X, Jorgensen E, Gietl D, Traganos F, Darzynkiewicz Z. Induction of DNA double-strand breaks in A549 and normal human pulmonary epithelial cells by cigarette smoke is mediated by free radicals. Int J Oncol 2006;28:1491-1505.
27. Tanaka T, Huang X, Jorgensen E, Gietl E, Traganos F, Darzynkiewicz Z, Albino AP. ATM activation accompanies histone H2AX phosphorylation in A549 cells upon exposure to tobacco smoke. BMC Cell Biol 2007;8:26. (Pubitemid 47086723)
28. Kastan MB, Lim DS. The many substrates and functions of ATM. Nat Rev Mol Cell Biol 2000;1:179-186.
29. Helt CE, Cliby WA, Keng PC, Bambara RA, O'Reilly MA. Ataxia telangiectasia mutated (ATM) and ATM and Rad3-related protein exhibit selective target specificities in response to different forms of DNA damage. J Biol Chem 2005;280:1186-1192.
30. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003;421:499-506.
31. Bakkenist CJ, Kastan MB. Initiating cellular stress responses. Cell 2004;118:9-17.
32. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001;276:42462-42467. (Pubitemid 37371158)
33. Lee J-H, Paull TT. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 2005;308:551-554. (Pubitemid 40570585)
34. Paull TT, Lee JH. The Mre11/Rad50/Nbs1 complex and its role as a DNA-double strand break sensor for ATM. Cell Cycle 2005;4:737-740.
35. Zhao H, Traganos F, Darzynkiewicz Z. Phosphorylation of p53 on Ser15 during cell cycle caused by Topo I and Topo II inhibitors in relation to ATM and Chk2 activation. Cell Cycle 2008;7:3048-3055.
36. Zhao H, Traganos F, Albino AP, Darzynkiewicz Z. Oxidative stress induces cell cycledependent Mre11 recruitment. ATM and Chk2 activation and histone H2AX phosphorylation. Cell Cycle 2008;7:1490-1495.
37. Zhao H, Traganos F, Darzynkiewicz Z. Kinetics of histone H2AX phosphorylation and Chk2 activation in A549 cells treated with topotecan and mitoxantrone in relation to the cell cycle phase. Cytometry Part A 2008;73A:480-489. (Pubitemid 351812843)
38. 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 the aging-related processes. Cytometry Part A 2007;71A:905-914. (Pubitemid 350076854)
39. Pozarowski P, Holden E, Darzynkiewicz Z. Laser scanning cytometry: Principles and applications. Methods Mol Biol 2005;319:165-192.
40. Darzynkiewicz Z, Bedner E, Gorczyca W, Melamed MR. Laser scanning cytometry. A new instrumentation with many applications. Exp Cell Res 1999;249:1-12.
41. Tanaka T, Halicka HD, Huang X, Traganos F, Darzynkiewicz Z. Constitutive histone H2AX phosphorylation and ATM activation, the reporters of DNA damage by endogenous oxidants. Cell Cycle 2006;5:1940-1945. (Pubitemid 44435299)
42. Murga M, Jaco I, Soria R, Martinez-Pastor B, Cuadrado M, Yang S-M, Blasco MA, Skoultchi AI, Fernandez-Capetillo O. Global chromatin compaction limits the strength of the DNA damage response. J Cell Biol 2007;178:1101-1108. (Pubitemid 47480219)
43. Gerlitz G, Hock R, Ueda T, Bustin M. The dynamics of HMG protein-chromatin interactions in living cells. Biochem Cell Biol 2009;87:127-137.
44. Halicka HD, Zhao H, Podhorecka M, Traganos F, Darzynkiewicz Z. Cytometric detection of chromatin relaxation, an early reporter of DNA damage response. Cell Cycle 2009; 8:2233-2237.
45. Abraham RT, Tibbetts RS. Guiding ATM to broken DNA. Science 2005;308:510-511.
46. Downs JA, Cote J. Dynamics of chromatin during the repair of DNA double-strand breaks. Cell Cycle 2005;4:1373-1376. (Pubitemid 41437125)
47. Kitagawa R, Kastan MB. The ATM-dependent DNA damage signaling pathway. Cold Spring Harb Symp Quant Biol 2005;70:99-109. (Pubitemid 44124861)
48. Sun Y, Jiang X, Chen S, Fernandes N, Price BD. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc Natl Acad Sci USA 2005;102:13182-13187. (Pubitemid 41324998)
49. Ismail IH, Nystrom S, Nygren J., Hammersten O. Activation of ataxia telangiectasia mutated by DNA strand break-inducing agents correlates closely with the number of DNA double strand breaks. J Biol Chem 2005;280:4649-4655 (Pubitemid 40288634)
50. Ahn J, Urist M, Prives C. The Chk2 protein kinase. DNA Repair (Amst) 2004;3:1039-1047.
51. Matsuoka S, Rotman G, Ogawa A, Shiloh K, Tamai SJ, Elledge SJ. Ataxia telangiectasia- mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci USA 2000;97:10289-10394. (Pubitemid 30707276)
52. Stevens C, Smith L, La Thangue NB. Chk2 activates E2F-1 in response to DNA damage. Nat Cell Biol 2003;5:4465-4479. (Pubitemid 36592262)
53. Lin J, Reichner C, Wu X, Levine AJ. Analysis of wild-type and mutant p21WAF-1 gene activities. Mol Cell Biol 1996;16:86-1793. (Pubitemid 26095651)
54. Tan Y, Raychaudhuri P, Costa RH. Chk2 mediates stabilization of the FoxM1 transcription factor to stimulate expression of DNA repair genes. Mol Cell Biol 2007;27:1007-1016. (Pubitemid 46174563)
55. Rudolph J. Cdc25 phosphatases: Structure, specificity and mechanism. Biochemistry 2007;46:3595-3604. (Pubitemid 46493460)
56. Sedelnikova OA, Rogakou EP, Panuytin IG, Bonner W. Quantitative detection of (125)IdU-induced DNA double-strand breaks with γ-H2AX antibody. Radiat Res 2002;158:486-492.
57. Stiff TO, Driscoll M, Rief N, Iwabuchi K, Lobrich M, Jeggo PA. ATM and DNA-PK function redundantly to phosphorylated H2AX after exposure to ionizing radiation. Cancer Res 2004;64:2390-2396. (Pubitemid 38523891)
58. Wang H, Wang M, Wang H, Bocker W, Illiakis G. Complex H2AX phosphorylation patterns by multiple kinases including ATM and DNA-PK in human cells exposed to ionizing radiation and treated with kinase inhibitors. J Cell Phys 2005;202:492-502. (Pubitemid 40041320)
59. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, Pommier Y. cH2AX and cancer. Nat Rev Cancer 2008;8:957-967.
60. Bartkova J, Bakkenist CJ, Rajpert-De Meyts E, Skakkebaek NE, Sehested M, Lukas J, Kastan MB, Bartek J. ATM activation in normal human tissues and testicular cancer. Cell Cycle 2005;4:838-845. (Pubitemid 41353838)
61. Chowdhury D, Keogh MC, Ishii H, Peterson CL, Buratowski S, Lieberman J. Gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol Cell 2005;20:801-809. (Pubitemid 41740701)
62. Heideker J, Lis ET, Romesberg FE. Phosphatases, DNA damage checkpoints and checkpoint deactivation. Cell Cycle 2007;6:3058-3064.
63. Nakada S, Chen GI, Gingras AC, Darocher D. PP4 is a gamma H2AX phosphatase required for recovery from DNA damage checkpoint. EMBO Rep 2008; 9:1019-1026.
64. Juan G, Li X, Darzynkiewicz Z. Correlation between DNA replication and expression of cyclins A and B1 in individual MOLT-4 cells. Cancer Res 1997;57:803-807. (Pubitemid 27097997)
65. Huang X, Tanaka T, Kurose A, Traganos F, Darzynkiewicz Z. Constitutive histone H2AX phosphorylation on Ser-139 in cells untreated by genotoxic agents is cell-cycle phase specific and attenuated by scavenging reactive oxygen species. Int J Oncol 2006;29:495-501.
66. Toyooka T, Ibuki Y. Cigarette sidestream smoke induces phosphorylated histone H2AX. Mutat Res 2009;676:34-40.
67. Valavanidis A, Vlachogianni T, Fiotakis K. Tobacco smoke: Involvement of reactive oxygen species and stable free radicals in mechanisms of oxidative damage, carcinogenesis and synergistic effects with other respirable particles. Int J Environ Res Public Health 2009;6:445-462.
68. Asami S, Manabe H, Miyake J, Tsurudone Y, Hirano T. Cigarette smoking induces an increase in oxidative DNA damage, 8-hydroxydeoxyguanosine, in a central site of human lung. Carcinogenesis 1997;18:1763-1766. (Pubitemid 28134683)
69. Robles AI, Linke SP, Harris CC. The p53 network in lung carcinogenesis. Oncogene 2002;21:6898-6907.
70. Pfeifer GP, Hainaut P. On the origin of G→T transversions in lung cancer. Mutat Res 2003;526:39-43.
71. Zhang P, Wang J, Gao, Yuan BZ, Rogers J, Reed E. CHK2 kinase expression is down-regulated due to promoter methylation in non-small lung cancer. Mol Cancer 2004;3:14. (Pubitemid 38751499)
72. Leng S, Stidley CA, Willink R, Bernauer A, Do K, Picchi MA, Sheng X, Frasco MA, Van Den Berg D, Gilliland FD, Zima C, Crowell RE, Belinsky SA. Double-strand break damage and associated DNA repair genes predispose smokers to gene methylation. Cancer Res 2008;68:3049-3056. (Pubitemid 351556307)