Use of the γ-H2AX assay to monitor DNA damage and repair in translational cancer research

Cancer Letters

Volumn 327, Issue 1-2, 2012, Pages 123-133

  Ivashkevich, Alesia ^a   Redon, Christophe E ^b   Nakamura, Asako J ^c   Martin, Roger F ^a   Martin, Olga A ^a  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b NATIONAL CANCER INSTITUTE   (United States)

^c OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

Biodosimetry; Chemotherapy; Double strand breaks (DSBs); Imaging; Radiation therapy; Radiosensitivity; Translational research; H2AX

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; GAMMA HISTONE H2AX; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; SJG 136; TOPOTECAN; UNCLASSIFIED DRUG; VELIPARIB;

ADVANCED CANCER; APOPTOSIS; BIODOSIMETRY; CANCER COMBINATION CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER RESEARCH; DIAGNOSTIC IMAGING; DNA DAMAGE; DNA DETERMINATION; DNA REPAIR; DOSIMETRY; DOUBLE STRANDED DNA BREAK; DRUG DNA BINDING; DRUG DNA INTERACTION; DRUG MONITORING; EXTERNAL BEAM RADIOTHERAPY; HUMAN; INFORMATION PROCESSING; LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN PHOSPHORYLATION; RADIATION MONITORING; RADIOISOTOPE THERAPY; RADIOSENSITIVITY; SHORT SURVEY; SINGLE STRANDED DNA BREAK; SOLID TUMOR; TRANSLATIONAL RESEARCH;

EID: 84861893199     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.12.025     Document Type: Review

References (141)

1. MacManus M.P., Hicks R.J. Where do we draw the line? Contouring tumors on positron emission tomography/computed tomography. International Journal of Radiation Oncology, Biology, Physics 2008, 71:2-4.
2. Croswell J.M., Kramer B.S., Crawford E.D. Screening for prostate cancer with PSA testing: current status and future directions. Oncology (Williston Park) 2011, 25:452-460. 463.
3. Sikaroodi M., Galachiantz Y., Baranova A. Tumor markers: the potential of "omics" approach. Current Molecular Medicine 2010, 10:249-257.
4. Bonner W.M., Redon C.E., Dickey J.S., Nakamura A.J., Sedelnikova O.A., Solier S., Pommier Y. gammaH2AX and cancer. Nature Reviews Cancer 2008, 8:957-967.
5. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. The Journal of Biological Chemistry 1998, 273:5858-5868.
6. Kinner A., Wu W., Staudt C., Iliakis G. {gamma}-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Research 2008.
7. Rogakou E.P., Boon C., Redon C., Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. The Journal of Cell Biology 1999, 146:905-916.
8. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Current Biology 2000, 10:886-895.
9. Celeste A., Fernandez-Capetillo O., Kruhlak M.J., Pilch D.R., Staudt D.W., Lee A., Bonner R.F., Bonner W.M., Nussenzweig A. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nature Cell Biology 2003, 5:675-679.
10. Redon C., Pilch D., Rogakou E., Sedelnikova O., Newrock K., Bonner W. Histone H2A variants H2AX and H2AZ. Current Opinion in Genetics and Development 2002, 12:162-169.
11. Sedelnikova O.A., Pilch D.R., Redon C., Bonner W.M. Histone H2AX in DNA damage and repair. Cancer Biology and Therapy 2003, 2:233-235.
12. Pilch D.R., Sedelnikova O.A., Redon C., Celeste A., Nussenzweig A., Bonner W.M. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochemistry and Cell Biology 2003, 81:123-129.
13. Fernandez-Capetillo O., Celeste A., Nussenzweig A. Focusing on foci: H2AX and the recruitment of DNA-damage response factors. Cell Cycle 2003, 2:426-427.
14. Stucki M., Clapperton J.A., Mohammad D., Yaffe M.B., Smerdon S.J., Jackson S.P. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 2005, 123:1213-1226.
15. Celeste A., Petersen S., Romanienko P.J., Fernandez-Capetillo O., Chen H.T., Sedelnikova O.A., Reina-San-Martin B., Coppola V., Meffre E., Difilippantonio M.J., Redon C., Pilch D.R., Olaru A., Eckhaus M., Camerini-Otero R.D., Tessarollo L., Livak F., Manova K., Bonner W.M., Nussenzweig M.C., Nussenzweig A. Genomic instability in mice lacking histone H2AX. Science 2002, 296:922-927.
16. Redon C.E., Nakamura A.J., Zhang Y.W., Ji J.J., Bonner W.M., Kinders R.J., Parchment R.E., Doroshow J.H., Pommier Y. Histone gammaH2AX and poly(ADP-ribose) as clinical pharmacodynamic biomarkers. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2010, 16:4532-4542.
17. Takagi K., Dexheimer T.S., Redon C., Sordet O., Agama K., Lavielle G., Pierre A., Bates S.E., Pommier Y. Novel E-ring camptothecin keto analogues (S38809 and S39625) are stable, potent, and selective topoisomerase I inhibitors without being substrates of drug efflux transporters. Molecular Cancer Therapeutics 2007, 6:3229-3238.
18. Bridges K.A., Hirai H., Buser C.A., Brooks C.S., Liu H., Buchholz T.A., Molkentine J.M., Mason K.A., Meyn R.E. MK-1775, a novel wee1 kinase inhibitor, radiosensitizes p53-defective human tumor cells. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2011.
19. Ziech D., Franco R., Pappa A., Panayiotidis M.I. Reactive oxygen species (ROS) - induced genetic and epigenetic alterations in human carcinogenesis. Mutation Research 2011, 711:167-173.
20. Nowsheen S., Wukovich R.L., Aziz K., Kalogerinis P.T., Richardson C.C., Panayiotidis M.I., Bonner W.M., Sedelnikova O.A., Georgakilas A.G. Accumulation of oxidatively induced clustered DNA lesions in human tumor tissues. Mutation Research 2009, 674:131-136.
21. Georgakilas A.G. Processing of DNA damage clusters in human cells: current status of knowledge. Molecular Biosystems 2008, 4:30-35.
22. Georgakilas A. Detection of clustered DNA lesions: biological and clinical applications. World Journal of Biological Chemistry 2011, 2:173-176.
23. Giunta S., Belotserkovskaya R., Jackson S.P. DNA damage signaling in response to double-strand breaks during mitosis. The Journal of Cell Biology 2010, 190:197-207.
24. Nakamura A.J., Rao V.A., Pommier Y., Bonner W.M. The complexity of phosphorylated H2AX foci formation and DNA repair assembly at DNA double-strand breaks. Cell Cycle 2010, 9:389-397.
25. Nelson G., Buhmann M., von Zglinicki T. DNA damage foci in mitosis are devoid of 53BP1. Cell Cycle 2009, 8:3379-3383.
26. Dickey J.S., Redon C.E., Nakamura A.J., Baird B.J., Sedelnikova O.A., Bonner W.M. H2AX: functional roles and potential applications. Chromosoma 2009, 118:683-692.
27. Wang L.H., Pfister T.D., Parchment R.E., Kummar S., Rubinstein L., Evrard Y.A., Gutierrez M.E., Murgo A.J., Tomaszewski J.E., Doroshow J.H., Kinders R.J. Monitoring drug-induced gammaH2AX as a pharmacodynamic biomarker in individual circulating tumor cells. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2010, 16:1073-1084.
28. Matsuzaki K., Harada A., Takeiri A., Tanaka K., Mishima M. Whole cell-ELISA to measure the gammaH2AX response of six aneugens and eight DNA-damaging chemicals. Mutation Research 2010, 700:71-79.
29. Dellas K., Bache M., Pigorsch S.U., Taubert H., Kappler M., Holzapfel D., Zorn E., Holzhausen H.J., Haensgen G. Prognostic impact of HIF-1alpha expression in patients with definitive radiotherapy for cervical cancer. Strahlentherapie und Onkologie: Organ der Deutschen Rontgengesellschaft .. [et al] 2008, 184:169-174.
30. Lianidou E.S., Markou A. Circulating tumor cells in breast cancer: detection systems, molecular characterization, and future challenges. Clinical Chemistry 2011.
31. Papini S., Cecchetti D., Campani D., Fitzgerald W., Grivel J.C., Chen S., Margolis L., Revoltella R.P. Isolation and clonal analysis of human epidermal keratinocyte stem cells in long-term culture. Stem Cells 2003, 21:481-494.
32. Qvarnstrom O.F., Simonsson M., Johansson K.A., Nyman J., Turesson I. DNA double strand break quantification in skin biopsies. Radiotherapy and Oncology: Journal of the European Society for Therapeutic Radiology and Oncology 2004, 72:311-317.
33. Geisel D., Heverhagen J.T., Kalinowski M., Wagner H.J. DNA double-strand breaks after percutaneous transluminal angioplasty. Radiology 2008, 248:852-859.
34. Rothkamm K., Lobrich M. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low X-ray doses. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:5057-5062.
35. Yoon A.J., Shen J., Wu H.C., Angelopoulos C., Singer S.R., Chen R., Santella R.M. Expression of activated checkpoint kinase 2 and histone 2AX in exfoliative oral cells after exposure to ionizing radiation. Radiation Research 2009, 171:771-775.
36. Cabral L.A., Lima C.F., Coutinho de Oliveira M.L., Brandao A.A., Almeida J.D. Oral exfoliative cytology for the diagnosis of paracoccidoidomycosis in a patient with human immunodeficiency virus: a case report. Acta Cytologica 2010, 54:1127-1129.
37. Perez-Sayansm M., Somoza-Martin J.M., Barros-Angueira F., Reboiras-Lopez M.D., Gandara-Vila P., Gandara Rey J.M., Garcia-Garcia A. Exfoliative cytology for diagnosing oral cancer. Biotechnic and Histochemistry: Official Publication of the Biological Stain Commission 2010, 85:177-187.
38. Gonzalez J.E., Roch-Lefevre S.H., Mandina T., Garcia O., Roy L. Induction of gamma-H2AX foci in human exfoliated buccal cells after in vitro exposure to ionising radiation. International Journal of Radiation Biology 2010, 86:752-759.
39. Fong P.C., Boss D.S., Yap T.A., Tutt A., Wu P., Mergui-Roelvink M., Mortimer P., Swaisland H., Lau A., O'Connor M.J., Ashworth A., Carmichael J., Kaye S.B., Schellens J.H., de Bono J.S. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. The New England Journal of Medicine 2009, 361:123-134.
40. Redon C.E., Nakamura A.J., Gouliaeva K., Rahman A., Blakely W.F., Bonner W.M. The use of gamma-H2AX as a biodosimeter for total-body radiation exposure in non-human primates. PloS One 2010, 5:e15544.
41. Gho C.G., Braun J.E., Tilli C.M., Neumann H.A., Ramaekers F.C. Human follicular stem cells: their presence in plucked hair and follicular cell culture. The British Journal of Dermatology 2004, 150:860-868.
42. Ismail I.H., Wadhra T.I., Hammarsten O. An optimized method for detecting gamma-H2AX in blood cells reveals a significant interindividual variation in the gamma-H2AX response among humans. Nucleic Acids Research 2007, 35:e36.
43. Gavrilov B., Vezhenkova I., Firsanov D., Solovjeva L., Svetlova M., Mikhailov V., Tomilin N. Slow elimination of phosphorylated histone gamma-H2AX from DNA of terminally differentiated mouse heart cells in situ. Biochemical and Biophysical Research Communications 2006, 347:1048-1052.
44. Bhogal N., Jalali F., Bristow R.G. Microscopic imaging of DNA repair foci in irradiated normal tissues. International Journal of Radiation Biology 2009, 85:732-746.
45. Rube C.E., Grudzenski S., Kuhne M., Dong X., Rief N., Lobrich M., Rube C. DNA double-strand break repair of blood lymphocytes and normal tissues analysed in a preclinical mouse model: implications for radiosensitivity testing. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2008, 14:6546-6555.
46. Huang X., Darzynkiewicz Z. Cytometric assessment of histone H2AX phosphorylation: a reporter of DNA damage. Methods in Molecular Biology 2006, 314:73-80.
47. Hou Y.N., Lavaf A., Huang D., Peters S., Huq R., Friedrich V., Rosenstein B.S., Kao J. Development of an automated gamma-H2AX immunocytochemistry assay. Radiation Research 2009, 171:360-367.
48. Ivashkevich A.N., Martin O.A., Smith A.J., Redon C.E., Bonner W.M., Martin R.F., Lobachevsky P.N. gammaH2AX foci as a measure of DNA damage: a computational approach to automatic analysis. Mutation Research 2011, 711:49-60.
49. Bailey K.E., Costantini D.L., Cai Z., Scollard D.A., Chen Z., Reilly R.M., Vallis K.A. Epidermal growth factor receptor inhibition modulates the nuclear localization and cytotoxicity of the Auger electron emitting radiopharmaceutical 111In-DTPA human epidermal growth factor. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine 2007, 48:1562-1570.
50. Costantini D.L., Chan C., Cai Z., Vallis K.A., Reilly R.M. (111)In-labeled trastuzumab (Herceptin) modified with nuclear localization sequences (NLS): an Auger electron-emitting radiotherapeutic agent for HER2/neu-amplified breast cancer. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine 2007, 48:1357-1368.
51. Cai Z., Vallis K.A., Reilly R.M. 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. International Journal of Radiation Biology 2009, 85:262-271.
52. Bocker W., Iliakis G. Computational methods for analysis of foci: validation for radiation-induced gamma-H2AX foci in human cells. Radiation Research 2006, 165:113-124.
53. MacPhail S.H., Banath J.P., Yu T.Y., Chu E.H., Lambur H., Olive P.L. Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. International Journal of Radiation Biology 2003, 79:351-358.
54. Leatherbarrow E.L., Harper J.V., Cucinotta F.A., O'Neill P. Induction and quantification of gamma-H2AX foci following low and high LET-irradiation. International Journal of Radiation Biology 2006, 82:111-118.
55. Mahrhofer H., Burger S., Oppitz U., Flentje M., Djuzenova C.S. Radiation induced DNA damage and damage repair in human tumor and fibroblast cell lines assessed by histone H2AX phosphorylation. International Journal of Radiation Oncology, Biology, Physics 2006, 64:573-580.
56. Markova E., Schultz N., Belyaev I.Y. Kinetics and dose-response of residual 53BP1/gamma-H2AX foci: co-localization, relationship with DSB repair and clonogenic survival. International Journal of Radiation Biology 2007, 83:319-329.
57. Roch-Lefevre S., Mandina T., Voisin P., Gaetan G., Mesa J.E., Valente M., Bonnesoeur P., Garcia O., Roy L. Quantification of gamma-H2AX foci in human lymphocytes: a method for biological dosimetry after ionizing radiation exposure. Radiation Research 2010, 174:185-194.
58. 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. Mutation Research 2009.
59. Garty G., Chen Y., Salerno A., Turner H., Zhang J., Lyulko O., Bertucci A., Xu Y., Wang H., Simaan N., Randers-Pehrson G., Yao Y.L., Amundson S.A., Brenner D.J. The RABIT: a rapid automated biodosimetry tool for radiological triage. Health Physics 2010, 98:209-217.
60. Garty G., Chen Y., Turner H.C., Zhang J., Lyulko O.V., Bertucci A., Xu Y., Wang H., Simaan N., Randers-Pehrson G., Lawrence Yao Y., Brenner D.J. The RABiT: a rapid automated biodosimetry tool for radiological triage. II. Technological developments. International Journal of Radiation Biology 2011, 87:776-790.
61. Turner H.C., Brenner D.J., Chen Y., Bertucci A., Zhang J., Wang H., Lyulko O.V., Xu Y., Shuryak I., Schaefer J., Simaan N., Randers-Pehrson G., Yao Y.L., Amundson S.A., Garty G. Adapting the gamma-H2AX assay for automated processing in human lymphocytes. 1. Technological aspects. Radiation Research 2010.
62. Turner H.C., Brenner D.J., Chen Y., Bertucci A., Zhang J., Wang H., Lyulko O.V., Xu Y., Shuryak I., Schaefer J., Simaan N., Randers-Pehrson G., Yao Y.L., Amundson S.A., Garty G. Adapting the gamma-H2AX assay for automated processing in human lymphocytes. 1. Technological aspects. Radiation Research 2011, 175:282-290.
63. Guzi T.J., Paruch K., Dwyer M.P., Labroli M., Shanahan F., Davis N., Taricani L., Wiswell D., Seghezzi W., Penaflor E., Bhagwat B., Wang W., Gu D., Hsieh Y., Lee S., Liu M., Parry D. Targeting the replication checkpoint using SCH 900776, a potent and functionally selective CHK1 inhibitor identified via high content screening. Molecular Cancer Therapeutics 2011, 10:591-602.
64. Karp J.E., Ricklis R.M., Balakrishnan K., Briel J., Greer J., Gore S.D., Smith B.D., McDevitt M.A., Carraway H., Levis M.J., Gandhi V. A phase 1 clinical-laboratory study of clofarabine followed by cyclophosphamide for adults with refractory acute leukemias. Blood 2007, 110:1762-1769.
65. Hochhauser D., Meyer T., Spanswick V.J., Wu J., Clingen P.H., Loadman P., Cobb M., Gumbrell L., Begent R.H., Hartley J.A., Jodrell D. Phase I study of sequence-selective minor groove DNA binding agent SJG-136 in patients with advanced solid tumors. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2009, 15:2140-2147.
66. Kyle S., Thomas H.D., Mitchell J., Curtin N.J. Exploiting the Achilles heel of cancer: the therapeutic potential of poly(ADP-ribose) polymerase inhibitors in BRCA2-defective cancer. The British Journal of Radiology 2008, 81(1):S6-11.
67. Kummar S., Chen A., Ji J., Zhang Y., Reid J.M., Ames M., Jia L., Weil M., Speranza G., Murgo A.J., Kinders R., Wang L., Parchment R.E., Carter J., Stotler H., Rubinstein L., Hollingshead M., Melillo G., Pommier Y., Bonner W., Tomaszewski J.E., Doroshow J.H. Phase I study of PARP inhibitor ABT-888 in combination with topotecan in adults with refractory solid tumors and lymphomas. Cancer Research 2011, 71:5626-5634.
68. Fandy T.E. Development of DNA methyltransferase inhibitors for the treatment of neoplastic diseases. Current Medicinal Chemistry 2009, 16:2075-2085.
69. Leonard A., Rueff J., Gerber G.B., Leonard E.D. Usefulness and limits of biological dosimetry based on cytogenetic methods. Radiation Protection Dosimetry 2005, 115:448-454.
70. Kleinerman R.A., Romanyukha A.A., Schauer D.A., Tucker J.D. Retrospective assessment of radiation exposure using biological dosimetry: chromosome painting, electron paramagnetic resonance and the glycophorin a mutation assay. Radiation Research 2006, 166:287-302.
71. Pinto M.M., Santos N.F., Amaral A. Current status of biodosimetry based on standard cytogenetic methods. Radiation and Environmental Biophysics 2010, 49:567-581.
72. Sak A., Grehl S., Erichsen P., Engelhard M., Grannass A., Levegrun S., Pottgen C., Groneberg M., Stuschke M. gamma-H2AX foci formation in peripheral blood lymphocytes of tumor patients after local radiotherapy to different sites of the body: dependence on the dose-distribution, irradiated site and time from start of treatment. International Journal of Radiation Biology 2007, 83:639-652.
73. Redon C.E., Nakamura A.J., Gouliaeva K., Rahman A., Blakely W.F., Bonner W.M. Qgamma-H2AX, an analysis method for partial-body radiation exposure using gamma-H2AX in non-human primate lymphocytes. Radiation Measurements 2011, 146:877-881.
74. Ohnishi T., Takahashi A., Nagamatsu A., Omori K., Suzuki H., Shimazu T., Ishioka N. Detection of space radiation-induced double strand breaks as a track in cell nucleus. Biochemical and Biophysical Research Communications 2009, 390:485-488.
75. Zhou H., Rodriguez M., van den Haak F., Nelson G., Jogani R., Xu J., Zhu X., Xian Y., Tran P.T., Felsher D.W., Keall P.J., Graves E.E. Development of a micro-computed tomography-based image-guided conformal radiotherapy system for small animals. International Journal of Radiation Oncology, Biology, Physics 2010, 78:297-305.
76. Redon C.E., Dickey J.S., Bonner W.M., Sedelnikova O.A. gamma-H2AX as a biomarker of DNA damage induced by ionizing radiation in human peripheral blood lymphocytes and artificial skin. Advances in Space Research 2009, 43:1171-1178.
77. Andrievski A., Wilkins R.C. The response of gamma-H2AX in human lymphocytes and lymphocytes subsets measured in whole blood cultures. International Journal of Radiation Biology 2009, 85:369-376.
78. Rothkamm K., Horn S. gamma-H2AX as protein biomarker for radiation exposure. Annali dell'Istituto superiore di sanita 2009, 45:265-271.
79. Ford E.C., Achanta P., Purger D., Armour M., Reyes J., Fong J., Kleinberg L., Redmond K., Wong J., Jang M.H., Jun H., Song H.J., Quinones-Hinojosa A. Localized CT-guided irradiation inhibits neurogenesis in specific regions of the adult mouse brain. Radiation Research 2011, 175:774-783.
80. Lobrich M., Rief N., Kuhne M., Heckmann M., Fleckenstein J., Rube C., Uder M. In vivo formation and repair of DNA double-strand breaks after computed tomography examinations. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:8984-8989.
81. Rothkamm K., Balroop S., Shekhdar J., Fernie P., Goh V. Leukocyte DNA damage after multi-detector row CT: a quantitative biomarker of low-level radiation exposure. Radiology 2007, 242:244-251.
82. Kuefner M.A., Grudzenski S., Schwab S.A., Wiederseiner M., Heckmann M., Bautz W., Lobrich M., Uder M. DNA double-strand breaks and their repair in blood lymphocytes of patients undergoing angiographic procedures. Investigative Radiology 2009, 44:440-446.
83. Kuefner M.A., Grudzenski S., Hamann J., Achenbach S., Lell M., Anders K., Schwab S.A., Haberle L., Lobrich M., Uder M. Effect of CT scan protocols on x-ray-induced DNA double-strand breaks in blood lymphocytes of patients undergoing coronary CT angiography. European Radiology 2010, 20:2917-2924.
84. Kuefner M.A., Hinkmann F.M., Alibek S., Azoulay S., Anders K., Kalender W.A., Achenbach S., Grudzenski S., Lobrich M., Uder M. Reduction of X-ray induced DNA double-strand breaks in blood lymphocytes during coronary CT angiography using high-pitch spiral data acquisition with prospective ECG-triggering. Investigative Radiology 2010, 45:182-187.
85. Zwicker F., Swartman B., Sterzing F., Major G., Weber K.J., Huber P.E., Thieke C., Debus J., Herfarth K. Biological in-vivo measurement of dose distribution in patients' lymphocytes by gamma-H2AX immunofluorescence staining: 3D conformal- vs. step-and-shoot IMRT of the prostate gland. Radiation Oncology 2011, 6:62.
86. Martin R.F., Haseltine W.A. Range of radiochemical damage to DNA with decay of iodine-125. Science 1981, 213:896-898.
87. Sedelnikova O.A., Rogakou E.P., Panyutin I.G., Bonner W.M. Quantitative detection of (125)IdU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiation Research 2002, 158:486-492.
88. Martin R.F. Induction of double-stranded breaks in DNA by binding with an 125i-labelled acridine. International Journal of Radiation Biology and Related Studies in Physics, Chemistry, and Medicine 1977, 32:491-497.
89. Kassis A.I., Fayad F., Kinsey B.M., Sastry K.S., Adelstein S.J. Radiotoxicity of an 125I-labeled DNA intercalator in mammalian cells. Radiation Research 1989, 118:283-294.
90. Martin R.F., Holmes N. Use of an 125I-labelled DNA ligand to probe DNA structure. Nature 1983, 302:452-454.
91. Adelstein S.J., Kassis A.I. Strand breaks in plasmid DNA following positional changes of Auger-electron-emitting radionuclides. Acta Oncologica 1996, 35:797-801.
92. Panyutin I.G., Neumann R.D. The potential for gene-targeted radiation therapy of cancers. Trends in Biotechnology 2005, 23:492-496.
93. Sedelnikova O.A., Panyutin I.V., Neumann R.D., Bonner W.M., Panyutin I.G. Assessment of DNA damage produced by 125I-triplex-forming oligonucleotides in cells. International Journal of Radiation Biology 2004, 80:927-931.
94. Panyutin I.V., Sedelnikova O.A., Bonner W.M., Panyutin I.G., Neumann R.D. DNA damage produced by 125I-triplex-forming oligonucleotides as a measure of their successful delivery into cell nuclei. Annals of the New York Academy of Sciences 2005, 1058:140-150.
95. Kelly M.P., Lee F.T., Tahtis K., Smyth F.E., Brechbiel M.W., Scott A.M. Radioimmunotherapy with alpha-particle emitting 213Bi-C-functionalized trans-cyclohexyl-diethylenetriaminepentaacetic acid-humanized 3S193 is enhanced by combination with paclitaxel chemotherapy. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2007, 13:5604s-5612s.
96. Lassmann M., Hanscheid H., Gassen D., Biko J., Meineke V., Reiners C., Scherthan H. In vivo formation of gamma-H2AX and 53BP1 DNA repair foci in blood cells after radioiodine therapy of differentiated thyroid cancer. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine 2010, 51:1318-1325.
97. Tucker S.L., Geara F.B., Peters L.J., Brock W.A. How much could the radiotherapy dose be altered for individual patients based on a predictive assay of normal-tissue radiosensitivity?. Radiotherapy and Oncology: Journal of the European Society for Therapeutic Radiology and Oncology 1996, 38:103-113.
98. Sprung C.N., Chao M., Leong T., McKay M.J. Chromosomal radiosensitivity in two cell lineages derived from clinically radiosensitive cancer patients. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2005, 11:6352-6358.
99. Leong T., Borg M., McKay M. Clinical and cellular radiosensitivity in inherited human syndromes. Clinical Oncology (Royal College of Radiologist) 2004, 16:206-209.
100. Turesson I., Nyman J., Holmberg E., Oden A. Prognostic factors for acute and late skin reactions in radiotherapy patients. International Journal of Radiation Oncology, Biology, Physics 1996, 36:1065-1075.
101. Bourguignon M.H., Gisone P.A., Perez M.R., Michelin S., Dubner D., Giorgio M.D., Carosella E.D. Genetic and epigenetic features in radiation sensitivity. Part II: implications for clinical practice and radiation protection. European Journal of Nuclear Medicine and Molecular Imaging 2005, 32:351-368.
102. Bourguignon M.H., Gisone P.A., Perez M.R., Michelin S., Dubner D., Giorgio M.D., Carosella E.D. Genetic and epigenetic features in radiation sensitivity Part I: cell signalling in radiation response. European Journal of Nuclear Medicine and Molecular Imaging 2005, 32:229-246.
103. Chistiakov D.A., Potapov V.A., Khodirev D.C., Shamkhalova M.S., Shestakova M.V., Nosikov V.V. Genetic variations in the pancreatic ATP-sensitive potassium channel, beta-cell dysfunction, and susceptibility to type 2 diabetes. Acta Diabetologica 2009, 46:43-49.
104. Pollard J.M., Gatti R.A. Clinical radiation sensitivity with DNA repair disorders: an overview. International Journal of Radiation Oncology, Biology, Physics 2009, 74:1323-1331.
105. Wood R.D., Mitchell M., Sgouros J., Lindahl T. Human DNA repair genes. Science 2001, 291:1284-1289.
106. Wood R.D., Mitchell M., Lindahl T. Human DNA repair genes, 2005. Mutation Research 2005, 577:275-283.
107. Twardella D., Chang-Claude J. Studies on radiosensitivity from an epidemiological point of view - overview of methods and results. Radiotherapy and Oncology: Journal of the European Society for Therapeutic Radiology and Oncology 2002, 62:249-260.
108. Huber R., Braselmann H., Geinitz H., Jaehnert I., Baumgartner A., Thamm R., Figel M., Molls M., Zitzelsberger H. Chromosomal radiosensitivity and acute radiation side effects after radiotherapy in tumour patients - a follow-up study. Radiation Oncology 2011, 6:32.
109. Geara F.B., Peters L.J., Ang K.K., Wike J.L., Sivon S.S., Guttenberger R., Callender D.L., Malaise E.P., Brock W.A. Intrinsic radiosensitivity of normal human fibroblasts and lymphocytes after high- and low-dose-rate irradiation. Cancer Research 1992, 52:6348-6352.
110. Burnet N.G., Nyman J., Turesson I., Wurm R., Yarnold J.R., Peacock J.H. Prediction of normal-tissue tolerance to radiotherapy from in-vitro cellular radiation sensitivity. Lancet 1992, 339:1570-1571.
111. Baeyens A., Thierens H., Vandenbulcke K., De Ridder L., Vral A. The use of EBV-transformed cell lines of breast cancer patients to measure chromosomal radiosensitivity. Mutagenesis 2004, 19:285-290.
112. Baeyens A., Vandenbulcke K., Philippe J., Thierens H., De Ridder L., Vral A. The use of IL-2 cultures to measure chromosomal radiosensitivity in breast cancer patients. Mutagenesis 2004, 19:493-498.
113. Geara F.B., Peters L.J., Ang K.K., Wike J.L., Brock W.A. Radiosensitivity measurement of keratinocytes and fibroblasts from radiotherapy patients. International Journal of Radiation Oncology, Biology, Physics 1992, 24:287-293.
114. Vasireddy R.S., Sprung C.N., Cempaka N.L., Chao M., McKay M.J. H2AX phosphorylation screen of cells from radiosensitive cancer patients reveals a novel DNA double-strand break repair cellular phenotype. British Journal of Cancer 2010, 102:1511-1518.
115. Golfier S., Jost G., Pietsch H., Lengsfeld P., Eckardt-Schupp F., Schmid E., Voth M. Dicentric chromosomes and gamma-H2AX foci formation in lymphocytes of human blood samples exposed to a CT scanner: a direct comparison of dose response relationships. Radiation Protection Dosimetry 2009, 134:55-61.
116. Menegakis A., Yaromina A., Eicheler W., Dorfler A., Beuthien-Baumann B., Thames H.D., Baumann M., Krause M. Prediction of clonogenic cell survival curves based on the number of residual DNA double strand breaks measured by gammaH2AX staining. International Journal of Radiation Biology 2009, 85:1032-1041.
117. Rube C.E., Fricke A., Schneider R., Simon K., Kuhne M., Fleckenstein J., Graber S., Graf N., Rube C. DNA repair alterations in children with pediatric malignancies: novel opportunities to identify patients at risk for high-grade toxicities. International Journal of Radiation Oncology, Biology, Physics 2010, 78:359-369.
118. Goodarzi A.A., Jeggo P.A. Irradiation induced foci (IRIF) as a biomarker for radiosensitivity. Mutation Research 2011.
119. Porcedda P., Turinetto V., Lantelme E., Fontanella E., Chrzanowska K., Ragona R., De Marchi M., Delia D., Giachino C. Impaired elimination of DNA double-strand break-containing lymphocytes in ataxia telangiectasia and Nijmegen breakage syndrome. DNA Repair 2006, 5:904-913.
120. Abbaszadeh F., Clingen P.H., Arlett C.F., Plowman P.N., Bourton E.C., Themis M., Makarov E.M., Newbold R.F., Green M.H., Parris C.N. A novel splice variant of the DNA-PKcs gene is associated with clinical and cellular radiosensitivity in a patient with xeroderma pigmentosum. Journal of Medical Genetics 2010, 47:176-181.
121. Leskovac A., Vujic D., Guc-Scekic M., Petrovic S., Joksic I., Slijepcevic P., Joksic G. Fanconi anemia is characterized by delayed repair kinetics of DNA double-strand breaks. The Tohoku Journal of Experimental Medicine 2010, 221:69-76.
122. Kato T.A., Wilson P.F., Nagasawa H., Fitzek M.M., Weil M.M., Little J.B., Bedford J.S. A defect in DNA double strand break processing in cells from unaffected parents of retinoblastoma patients and other apparently normal humans. DNA Repair 2007, 6:818-829.
123. Bourton E.C., Plowman P.N., Smith D., Arlett C.F., Parris C.N. Prolonged expression of the gamma-H2AX DNA repair biomarker correlates with excess acute and chronic toxicity from radiotherapy treatment. International Journal of Cancer. Journal International du Cancer 2011.
124. Kato T.A., Wilson P.F., Nagasaw H., Peng Y., Weil M.M., Little J.B., Bedford J.S. Variations in radiosensitivity among individuals: a potential impact on risk assessment?. Health Physics 2009, 97:470-480.
125. Werbrouck J., De Ruyck K., Beels L., Vral A., Van Eijkeren M., De Neve W., Thierens H. Prediction of late normal tissue complications in RT treated gynaecological cancer patients: potential of the gamma-H2AX foci assay and association with chromosomal radiosensitivity. Oncology Reports 2010, 23:571-578.
126. Werbrouck J., Duprez F., De Neve W., Thierens H. Lack of a correlation between gammaH2AX foci kinetics in lymphocytes and the severity of acute normal tissue reactions during IMRT treatment for head and neck cancer. International Journal of Radiation Biology 2011, 87:46-56.
127. Fleckenstein J., Kuhne M., Seegmuller K., Derschang S., Melchior P., Graber S., Fricke A., Rube C.E., Rube C. The impact of individual in vivo repair of DNA double-strand breaks on oral mucositis in adjuvant radiotherapy of head-and-neck cancer. International Journal of Radiation Oncology, Biology, Physics 2010.
128. Lobrich M., Shibata A., Beucher A., Fisher A., Ensminger M., Goodarzi A.A., Barton O., Jeggo P.A. gammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle 2010, 9:662-669.
129. Bentzen S.M. Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nature Reviews Cancer 2006, 6:702-713.
130. Sokolov M.V., Dickey J.S., Bonner W.M., Sedelnikova O.A. gamma-H2AX in bystander cells: not just a radiation-triggered event, a cellular response to stress mediated by intercellular communication. Cell Cycle 2007, 6:2210-2212.
131. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., Orntoft T., Lukas J., Bartek J. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864-870.
132. Prise K.M., Folkard M., Kuosaite V., Tartier L., Zyuzikov N., Shao C. What role for DNA damage and repair in the bystander response?. Mutation Research 2006, 597:1-4.
133. Sedelnikova O.A., Bonner W.M. GammaH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle 2006, 5:2909-2913.
134. Redon C.E., Dickey J.S., Nakamura A.J., Kareva I.G., Naf D., Nowsheen S., Kryston T.B., Bonner W.M., Georgakilas A.G., Sedelnikova O.A. Tumors induce complex DNA damage in distant proliferative tissues in vivo. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:17992-17997.
135. Belhocine T.Z., Blankenberg F.G. The imaging of apoptosis with the radiolabelled annexin A5: a new tool in translational research. Current Clinical Pharmacology 2006, 1:129-137.
136. Blankenberg F.G., Vanderheyden J.L., Strauss H.W., Tait J.F. Radiolabeling of HYNIC-annexin V with technetium-99m for in vivo imaging of apoptosis. Nature Protocols 2006, 1:108-110.
137. Tait J.F., Smith C., Levashova Z., Patel B., Blankenberg F.G., Vanderheyden J.L. Improved detection of cell death in vivo with annexin V radiolabeled by site-specific methods. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine 2006, 47:1546-1553.
138. Edgington L.E., Berger A.B., Blum G., Albrow V.E., Paulick M.G., Lineberry N., Bogyo M. Noninvasive optical imaging of apoptosis by caspase-targeted activity-based probes. Nature Medicine 2009, 15:967-973.
139. Aloya R., Shirvan A., Grimberg H., Reshef A., Levin G., Kidron D., Cohen A., Ziv I. Molecular imaging of cell death in vivo by a novel small molecule probe. Apoptosis: An International Journal on Programmed Cell Death 2006, 11:2089-2101.
140. Cornelissen B., Kersemans V., Darbar S., Thompson J., Shah K., Sleeth K., Hill M.A., Vallis K.A. Imaging DNA damage in vivo using {gamma}H2AX-targeted immunoconjugates. Cancer Research 2011, 71:4539-4549.
141. Li W., Li F., Huang Q., Shen J., Wolf F., He Y., Liu X., Hu Y.A., Bedford J.S., Li C.Y. Quantitative, noninvasive imaging of radiation-induced DNA double-strand breaks in vivo. Cancer Research 2011, 71:4130-4137.