764
Views
33
CrossRef citations to date
0
Altmetric
Review Article

Gamma histone 2AX (γ-H2AX)as a predictive tool in radiation oncology

&
Pages 167-180 | Received 03 Jan 2014, Accepted 21 Feb 2014, Published online: 10 Mar 2014

References

  • Asakawa H, Koizumi H, Koike A, et al. (2010). Prediction of breast cancer sensitivity to neo adjuvant chemotherapy based on status of DNA damage repair proteins. Breast Cancer Res 12:R17
  • Avondoglio D, Scott T, Kil WJ, et al. (2009). High throughput evaluation of γ-H2AX. Radiat Oncol 24:4–31
  • Bakkenist CJ, Kastan MB. (2003). DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499–506
  • Balcer-Kubiczek EK, Attarpour M, Edelman MJ. (2007). The synergistic effect of dimethylamino benzoylphenylurea (NSC #639829) and X-irradiation on human lung carcinoma cell lines. Cancer Chemother Pharmacol 59:781–7
  • Bannik K, Rössler U, Faus-Kessler T, et al. (2013). Are mouse lens epithelial cells more sensitive to γ-irradiation than lymphocytes? Radiat Environ Biophys 52:279–8
  • Bañuelos CA, Banáth JP, Kim JY, et al. (2009). γH2AX expression in tumors exposed to cisplatin and fractionated irradiation. Clin Cancer Res 15:3344–53
  • Baschnagel A, Russo A, Burgan WE, et al. (2009). Vorinostat enhances the radiosensitivity of a breast cancer brain metastatic cell line grown in vitro and as intracranial xenografts. Mol Cancer Ther 28:1589–95
  • Baumgart T, Klautke G, Kriesen S, et al. (2012). Radiosensitizing effect of epothilone B on human epithelial cancer cells. Strahlenther Onkologie 188:177–84
  • Beucher A, Deckbar D, Schumann E, et al. (2011). Elevated RT-induced γH2AX foci in G2 phase heterozygous BRCA2 fibroblasts. Radiother Oncol 101:46–50
  • Blattmann C, Oertel S, Thiemann M, et al. (2012). Suberoylanilide hydroxamic acid affects γH2AX expression in osteosarcoma, atypical teratoid rhabdoid tumor and normal tissue cell lines after irradiation. Strahlenther Onkologie 188:168–76
  • Bonner WM, Redon CE, Dickey JS, et al. (2008). γH2AX and cancer. Nat Rev Cancer 8:957–67
  • Bouquet F, Muller C, Salles B. (2006). The loss of γH2AX signal is a marker of DNA double strand breaks repair only at low levels of DNA damage. Cell Cycle 5:1116–22
  • Bouquet F, Pal A, Pilones KA, Demaria S, et al. (2011). TGFβ1 inhibition increases the radiosensitivity of breast cancer cells in vitro and promotes tumor control by radiation in vivo. Clin Cancer Res 17:6754–65
  • Bourton EC, Plowman PN, Smith D, et al. (2011). Prolonged expression of the g-H2AX DNA repair biomarker correlates with excess acute and chronic toxicity from radiotherapy treatment. Int J Cancer 129:2928–34
  • Brzozowska K, Pinkawa M, Eble MJ, et al. (2012). In vivo versus in vitro individual radiosensitivity analysed in healthy donors and in prostate cancer patients with and without severe side effects after radiotherapy. Int J Radiation Biol 88:405–13
  • Buchanan IM, Scott T, Tandle AT, et al. (2011). Radiosensitization of glioma cells by modulation of Met signalling with the hepatocyte growth factor neutralizing antibody, AMG102. J Cell Mol Med 15:1999–2006
  • Camphausen K, Brady KJ, Burgan WE, et al. (2004). Flavopiridol enhances human tumor cell radiosensitivity and prolongs expression of γH2AX foci. Mol Cancer Ther 3:409–16
  • Catts VS, Catts SV, Jablensky A, et al. (2011). Evidence of aberrant DNA damage response signalling but normal rates of DNA repair in dividing lymphoblasts from patients with schizophrenia. World J Biol Psychiatry 2:114–25
  • Celeste A, Petersen S, Romanienko PJ, et al. (2002). Genomic instability in mice lacking histone H2AX. Science 296:922–7
  • Cha H, Lowe JM, Li H, et al. (2010). Wip1 directly dephosphorylates γ-H2AX and attenuates the DNA damage response. Cancer Res 70:4112–22
  • Chan N, Bristow RG. (2010). “Contextual” synthetic lethality and/or loss of heterozygoty: tumor hypoxia and modification of DNA repair. Clin Cancer Res 16:4553–60
  • Chen HH, Jia RF, Yu L, et al. (2008). Bystander effects induced by continuous low-dose-rate 125I seeds potentiate the killing action of irradiation on human lung cancer cells in vitro. Int J Radiat Oncol 72:1560–6
  • Choi EJ, Ryu YK, Kim SY, et al. (2010). Targeting epidermal growth factor receptor-associated signaling pathways in non-small cell lung cancer cells: implication in radiation response. Mol Cancer Res 8:1027–36
  • Choi EK, Terai K, Ji IM, et al. (2007). Upregulation of NAD(P)H:quinone oxidoreductase by radiation potentiates the effect of bioreductive beta-lapachone on cancer cells. Neoplasia 9:634–42
  • Choudhuri R, Degraff W, Gamson J, et al. (2011). Guggulsterone-mediated enhancement of radiosensitivity in human tumor cell lines. Front Oncol 21:1–19
  • Chua ML, Somaiah N, A'Hern R, et al. (2011). Residual DNA and chromosomal damage in ex vivo irradiated blood lymphocytes correlated with late normal tissue response to breast radiotherapy. Radiother Oncol 99:362–6
  • Chuykin IA, Lianguzova MS, Pospelova TV, et al. (2008). Activation of DNA damage response signaling in mouse embryonic stem cells. Cell Cycle 7:2922–8
  • Colin C, Devic C, Noël A, et al. (2011). DNA double-strand breaks induced by mammographic screening procedures in human mammary epithelial cells. Int J Radiat Biol 87:1103–12
  • Cortez D, Guntuku S, Qin J, et al. (2001). ATR and ATRIP: Partners in checkpoint signaling. Science 294:1713–16
  • Cowell IG, Durkacz BW, Tilby MJ. (2005). Sensitization of breast carcinoma cells to ionizing radiation by small molecule inhibitors of DNA-dependent protein kinase and ataxia telangiectsia mutated. Biochem Pharmacol 71:13–20
  • Dai Y, DeSano JT, Meng Y, et al. (2009). Celastrol potentiates radiotherapy by impairment of DNA damage processing in human prostate cancer. Int J Radiat Oncol 74:1217–25
  • Dang L, Lisowska H, Manesh SS, et al. (2012). Radioprotective effect of hypothermia on cells - a multiparametric approach to delineate the mechanisms. Int J Radiat Biol 88:507–14
  • Depuydt J, Baert A, Vandersickel V, et al. (2013). Relative biological effectiveness of mammography X-rays at the level of DNA and chromosomes in lymphocytes. Int J Radiat Biol 89:532–8
  • Dieriks B, De Vos W, Baatout S, et al. (2011). Repeated exposure of human fibroblasts to ionizing radiation reveals an adaptive response that is not mediated by interleukin-6 or TGF-β. Mutation Res 715:19–24
  • Dittmann KH, Mayer C, Ohneseit PA, et al. (2008). Celecoxib induced tumor cell radiosensitization by inhibiting radiation induced nuclear EGFR transport and DNA-repair: a COX-2 independent mechanism. Int J Radiat Oncol Biol Phys 70:203–12
  • Dote H, Cerna D, Burgan WE, et al. (2005). Enhancement of in vitro and in vivo tumor cell radiosensitivity by the DNA methylation inhibitor zebularine. Clin Cancer Res 11:4571–9
  • Endt H, Sprung CN, Keller U, et al. (2011). Detailed analysis of DNA repair and senescence marker kinetics over the life span of a human fibroblast cell line. J Gerontology A Biol Sci Med Sci 66:367–75
  • Fauquette W, Amourette C, Dehouck MP, et al. (2012). Radiation-induced blood-brain barrier damages: an in vitro study. Brain Res 1433:114–26
  • Fernandez-Capetillo O, Lee M. (2004). H2AX: the histone guardian of the genome. DNA Repair 3:959–67
  • Fernando R, Eleuteri B, Abdelhady S, et al. (2011). Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells. Proc Natl Acad Sci USA 108: 5837–42
  • Firsanov D, Vasilishina A, Kropotov A, et al. (2012). Dynamics of γH2AX formation and elimination in mammalian cells after X-irradiation. Biochimie 94: 2416–22
  • Fleckenstein J, Kühne M, Seegmüller K, et al. (2011). The impact of individual in vivo repair of DNA double-strand breaks on oral mucositis in adjuvant radiotherapy of head-and-neck cancer. Int J Radiat Oncol 81:1465–72
  • Fokas E, Yoshimura M, Prevo R, et al. (2012). NVP-BEZ235 and NVP-BGT226, dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitors, enhance tumor and endothelial cell radiosensitivity. Radiat Oncol 27:7–48
  • Fuhrman CB, Kilgore J, La Coursiere YD, et al. (2008). Radiosensitization of cervical cancer cells via double-strand DNA break repair inhibition. Gynecol Oncol 110:93–8
  • Gho CG, Braun JE, Tilli CM, et al. (2004). Human follicular stem cells: their presence in plucked hair and follicular cell culture. Br J Dermatol 150:860–8
  • Goutham HV, Mumbrekar KD, Vadhiraja BM, et al. (2012). DNA double-strand break analysis by γ-H2AX foci: a useful method for determining the over reactors to radiation-induced acute reactions among head-and-neck cancer patients. Int J Radiat Oncol 84:607–12
  • Guo Q, Guo P, Mao Q, et al. (2013). ID1 affects the efficacy of radiotherapy in glioblastoma through inhibition of DNA repair pathways. Medical Oncol 30:325–32
  • Higgins GS, Prevo R, Lee YF, et al. (2010). A small interfering RNA screen of genes involved in DNA repair identifies tumor-specific radiosensitization by POLQ knockdown. Cancer Res 70:2984–93
  • Huerta S, Gao X, Livingston EH, et al. (2010). In vitro and in vivo radiosensitization of colorectal cancer HT-29 cells by the smac mimetic JP-1201. Surgery 148:346–53
  • Jäämaa S, Af Hällström TM, Sankila A, et al. (2010). DNA damage recognition via activated ATM and p53 pathway in nonproliferating human prostate tissue. Cancer Res 70:8630–41
  • Jamal M, Rath BH, Williams ES, et al. (2011). Microenvironmental regulation of glioblastoma radioresponse. Clin Cancer Res 17:6049–59
  • Jazayeri A, Balestrini A, Garner E, et al. (2008). Mre11-Rad50-Nbs1-dependent processing of DNA breaks generates oligonucleotides that stimulate ATM activity. EMBO J 27:1953–62
  • Kasten-Pisula U, Windhorst S, Dahm-Daphi J, et al. (2007). Radiosensitization of tumour cell lines by the polyphenol Gossypol results from depressed double-strand break repair and not from enhanced apoptosis. Radiother Oncol 83:296–303
  • Kataoka Y, Bindokas VP, Duggan RC, et al. (2006). Flow cytometric analysis of phosphorylated histone H2AX following exposure to ionizing radiation in human microvascular endothelial cells. J Radiat Res 47:245–57
  • Kendziorra E, Ahlborn K, Spitzner M, et al. (2011). Silencing of the Wnt transcription factor TCF4 sensitizes colorectal cancer cells to (chemo-) radiotherapy. Carcinogenesis 32:1824–31
  • Kim HJ, Kim JH, Chie EK, et al. (2012). DNMT (DNA methyltransferase) inhibitors radiosensitize human cancer cells by suppressing DNA repair activity. Radiat Oncol 20:7–39
  • Kiviharju-af Hällström TM, Jäämaa S, Mönkkönen M, et al. (2007). Human prostate epithelium lacks Wee1A-mediated DNA damage-induced checkpoint enforcement. Proc Natl Acad Sci USA 104:7211–16
  • Klokov D, MacPhail SM, Banáth JP, et al. (2006). Phosphorylated histone H2AX in relation to cell survival in tumor cells and xenografts exposed to single and fractionated doses of X-rays. Radiother Oncol 80:223–9
  • Koch U, Höhne K, von Neubeck C, et al. (2013). Residual γH2AX foci predict local tumour control after radiotherapy. Radiother Oncol 108:434–9
  • Koike M, Sugasawa J, Yasuda M, et al. (2008). Tissue-specific DNA-PK-dependent H2AX phosphorylation and γH2AX elimination after X-irradiation in vivo. Biochem Biophys Res Commun 376:52–5
  • Koike M, Yutoku Y, Koike A. (2013). The defect of Ku70 affects sensitivity to X-ray and radiation-induced caspase-dependent apoptosis in lung cells. J Vet Med Sci 75:415–20
  • Konsoula Z, Cao H, Velena A, Jung M. (2011). Adamantanyl-histone deacetylase inhibitor H6CAHA exhibits favorable pharmacokinetics and augments prostate cancer radiation sensitivity. Int J Radiat Oncol Biol Phys 79:1541–8
  • Kummar S, Kinders R, Gutierrez ME, et al. (2009). Phase 0 clinical trial of the poly (ADP-ribose) polymerase inhibitor ABT-888 in patients with advanced malignancies. J Clinical Oncol 27:2705–11
  • Lei J, Zhou C, Hu H, et al. (2012). Mangiferin aglycone attenuates radiation-induced damage on human intestinal epithelial cells. J Cellular Biochem 113:2633–42
  • Lett JT. (1992). Damage to cellular DNA from particulate radiation, the efficacy of its processing and the radiosensitivity of mammalian cells. Emphasis on DNA double strand breaks and chromatin breaks. Radiat Environ Biophysics 31:257–77
  • Li P, Du CR, X WC, et al. (2013). Correlation of dynamic changes in γ-H2AX expression in peripheral blood lymphocytes from head and neck cancer patients with radiation-induced oral mucositis. Radiat Oncol 8:155–62
  • Lisby M, Mortensen UH, Rothstein R. (2003). Colocalization of multiple DNA double-strand breaks at a single Rad52 repair center. Nature Cell Biol 5:572–7
  • Liu ZG, Liu L, Xu LH, et al. (2012). Bmi-1 induces radioresistance in MCF-7 mammary carcinoma cells. Oncol Rep 27:1116–22
  • Lobachevsky PN, Vasireddy RS, Broadhurst S, et al. (2011). Protection by methylproamine of irradiated human keratinocytes correlates with reduction of DNA damage. Int J Radiat Biol 87:274–83
  • Lobrich M, Shibata A, Beucher A, et al. (2010). γH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle 9:662–9
  • Lowndes NF, Toh GW. (2005). DNA repair: The importance of phosphorylating histone H2AX. Curr Biol 15:99–102
  • Maheswaran S, Haber DA. (2010). Circulating tumor cells: a window into cancer biology and metastasis. Curr Opin Genet Dev 20:96–9
  • Manke IA, Lowery DM, Nguyen A, et al. (2003). BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302:636–9
  • Mannironi C, Bonner WM, Hatch CL. (1989). H2AX histone isoprotein with a conserved C-terminal sequence is encoded by a novel mRNA with both DNA replication type and poly A 3 processing signals. Nucleic Acids Res 17:9113–26
  • Martin LM, Marples B, Davies AM, et al. (2013). DNA mismatch repair protein MSH2 dictates cellular survival in response to low dose radiation in endometrial carcinoma cells. Cancer Lett 335:19–25
  • Maurya DK, Devasagayam TP. (2013). Ferulic acid inhibits gamma radiation-induced DNA strand breaks and enhances the survival of mice. Cancer Biother Radiopharm 28:51–7
  • Menegakis A, Eicheler W, Yaromina A, et al. (2011). Residual DNA double strand breaks in perfused but not in unperfused areas determine different radiosensitivity of tumours. Radiother Oncol 100:137–44
  • Miura K, Sakata K, Someya M, et al. (2012). The combination of olaparib and camptothecin for effective radiosensitization. Radiat Oncol 23:7–62
  • Moiseenko V, Banáth JP, Duzenli C, et al. (2008). Effect of prolonging radiation delivery time on retention of γH2AX. Radiat Oncol 27:3–18
  • Nishimaki N, Tsukimoto M, Kitami A, et al. (2012). Autocrine regulation of γ-irradiation-induced DNA damage response via extracellular nucleotides-mediated activation of P2Y6 and P2Y12 receptors. DNA Repair (Amst) 11:657–65
  • Oka K, Tanaka T, Enoki T, et al. (2010). DNA damage signaling is activated during cancer progression in human colorectal carcinoma. Cancer Biol Ther 9:246–52
  • Olive PL, Banáth JP, Keyes M. (2008). Residual γH2AX after irradiation of human lymphocytes and monocytes in vitro and its relation to late effects after prostate brachytherapy. Radiother Oncol 86:336–46
  • Olive PL, Banuelos CA, Durand RE, et al. (2010). Endogenous and radiation-induced expression of γH2AX in biopsies from patients treated for carcinoma of the uterine cervix. Radiother Oncol 94:82–9
  • Palayoor ST, Mitchell JB, Cerna D, et al. (2008). Inducible factor-1alpha, enhances radiosensitivity of prostate carcinoma cells. Int J Cancer 123:2430–7
  • Paques F, Haber E. (1999). Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol 63:349–404
  • Pathe C, Eble K, Schmitz-Beuting D, et al. (2011). The presence of iodinated contrast agents amplifies DNA radiation damage in computed tomography. Contrast Media Mol Imaging 6:507–13
  • Peterson C, Côté J. (2004). Cellular machineries for chromosomal DNA repair. Genes Dev 18:602–16
  • Porcedda P, Turinetto V, Brusco A, et al. (2008). A rapid flow cytometry test based on histone H2AX phosphorylation for the sensitive and specific diagnosis of ataxia telangiectasia. Cytometry A 6:508–16
  • Porcedda P, Turinetto V, Lantelme E, et al. (2006). Impaired elimination of DNA double-strand break-containing lymphocytes in ataxia telangiectasia and Nijmegen breakage syndrome. DNA Repair 8: 904–13
  • Potiron VA, Abderrahmani R, Giang E, et al. (2013). Radiosensitization of prostate cancer cells by the dual PI3K/mTOR inhibitor BEZ235 under normoxic and hypoxic conditions. Radiother Oncol 106:138–46
  • Prevo R, Fokas E, Reaper PM, et al. (2012). The novel ATR inhibitor VE-821 increases sensitivity of pancreatic cancer cells to radiation and chemotherapy. Cancer Biol Ther 13:1072–81
  • Redon C, Pilch D, Rogakou E, et al. (2002). Histone H2A variants H2AX and H2AZ. Curr Opin Genetics Dev 12:162–9
  • Redon C, Pilch DR, Rogakou EP, et al. (2003). Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint blind DNA damage. EMBO Rep 4:678–84
  • Rieckmann T, Tribius S, Grob TJ, et al. (2013). HNSCC cell lines positive for HPV and p16 possess higher cellular radiosensitivity due to an impaired DSB repair capacity. Radiother Oncol 107:242–6
  • Rogakou EP, Boon C, Redon C, et al. (1999). Megabase chromatin domains involved in DNA double strand breaks in vivo. J Cell Biol 146:905–16
  • Rogakou EP, Pilch DR, Orr AH, et al. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858–68
  • Rübe CE, Fricke A, Schneider R. (2010b). DNA repair alterations in children with pediatric malignancies: novel opportunities to identify patients at risk for high-grade toxicities. Int J Radiat Oncol 7:359–69
  • Rübe CE, Dong X, Kühne M, et al. (2008). DNA double-strand break rejoining in complex normal tissues. Int J Radiat Oncol 72:1180–7
  • Rübe CE, Fricke A, Wendorf J, et al. (2010a). Accumulation of DNA double-strand breaks in normal tissues after fractionated irradiation. Int J Radiat Oncol 76:1206–13
  • Russo AL, Kwon HC, Burgan WE, et al. (2009). In vitro and in vivo radiosensitization of glioblastoma cells by the poly (ADP-ribose) polymerase inhibitor E7016. Clin Cancer Res 15:607–12
  • Sarcar B, Kahali S, Prabhu AH, et al. (2011). Targeting radiation-induced G(2) checkpoint activation with the Wee-1 inhibitor MK-1775 in glioblastoma cell lines. Mol Cancer Ther 10:2405–14
  • Shelton JW, Waxweiler TV, Landry J, et al. (2013). In vitro and in vivo enhancement of chemo radiation using the oral PARP inhibitor ABT-888 in colorectal cancer cells. Int J Radiat Oncol 86:469–76
  • Shoji M, Ninomiya I, Makino I, et al. (2012). Valproic acid, a histone deacetylase inhibitor, enhances radiosensitivity in esophageal squamous cell carcinoma. Int J Oncol 40:2140–6
  • Sorokina S, Markova E, Gursky J, et al. (2013). Relative biological efficiency of protons at low and therapeutic doses in induction of 53BP1/γH2AX foci in lymphocytes from umbilical cord blood. Int J Radiat Biol 89:716–23
  • Sprung CN, Vasireddy RS, Karagiannis TC, et al. (2010). Methylproamine protects against ionizing radiation by preventing DNA double-strand breaks. Mutat Res 692:49–52
  • Stingl L, Stühmer T, Chatterjee M, et al. (2010). Novel HSP90 inhibitors, NVP-AUY922 and NVP-BEP800, radiosensitise tumour cells through cell-cycle impairment, increased DNA damage and repair protraction. Br J Cancer 102:1578–91
  • Szeto YT, Benzie IF, Collins AR, et al. (2005). A buccal cell model comet assay: development and evaluation for human biomonitoring and nutritional studies. Mutat Res 578:371–81
  • Tanaka T, Huang X, D. Halicka H, et al. (2007). Cytometry of ATM activation and histone H2AX phosphorylation to estimate extent of DNA damage induced by exogenous agents. Cytometry A 71:648–61
  • Tandle AT, Kramp T, Kil WJ, et al. (2013). Inhibition of polo-like kinase 1 in glioblastoma multiforme induces mitotic catastrophe and enhances radiosensitisation. Eur J Cancer 49:3020–8
  • Tian M, Feng Y, Min J, et al. (2011). DNA damage response in resting and proliferating peripheral blood lymphocytes treated by camptothecin or X-ray. J Huazhong Univ Sci Technol Med Sci 31:147–53
  • Tsai YC, Yeh CH, Tzen KY, et al. (2013). Targeting epidermal growth factor receptor/human epidermal growth factor receptor 2 signalling pathway by a dual receptor tyrosine kinase inhibitor afatinib for radiosensitisation in murine bladder carcinoma. Eur J Cancer 49:1458–66
  • Turesson I, Nyman J, Qvarnström F, et al. (2010). A low-dose hypersensitive keratinocyte loss in response to fractionated radiotherapy is associated with growth arrest and apoptosis. Radiother Oncol 94:90–101
  • Turney BW, Kerr M, Chitnis MM, et al. (2012). Depletion of the type 1 IGF receptor delays repair of radiation-induced DNA double strand breaks. Radiother Oncol 103:402–9
  • Uziel T, Lerenthal Y, Moyal L, et al. (2003). Requirement of the MRN complex for ATM activation by DNA damage. EMBO J 22:5612–2
  • Valdiglesias V, Giunta S, Fenech M, et al. (2013). γH2AX as a marker of DNA double strand breaks and genomic instability in 4 human population studies. Mutat Res 753:24–40
  • Vandersickel V, Depuydt J, Van Bockstaele B, et al. (2010). Early increase of radiation-induced γH2AX foci in a human Ku70/80 knockdown cell line characterized by an enhanced radiosensitivity. J Radiat Res 51:633–41
  • Vasilyev SA, Kubes M, Markova E, et al. (2013). DNA damage response in CD133 + stem/progenitor cells from umbilical cord blood: low level of endogenous foci and high recruitment of 53BP1. Int J Radiat Biol 89:301–9
  • Vasireddy RS, Sprung CN, Cempaka NL, et al. (2010). H2AX phosphorylation screen of cells from radiosensitive cancer patients reveals a novel DNA double-strand break repair cellular phenotype. Br J Cancer 102:1511–18
  • Wang C, Nakamura S, Oshima M, et al. (2013). Compromised hematopoiesis and increased DNA damage following non-lethal ionizing radiation of a human hematopoietic system reconstituted in immunodeficient mice. Int J Radiat Biol 89:132–7
  • Wang L, Raju U, Milas L, et al. (2011). Huachansu, containing cardiac glycosides, enhances radiosensitivity of human lung cancer cells. Anticancer Res 31:2141–8
  • Warters RL, Adamson PJ, Pond CD, et al. (2005). Melanoma cells express elevated levels of phosphorylated histone H2AX foci. J Invest Dermatol 124:807–17
  • Werbrouck J, Duprez F, De Neve W, et al. (2011). Lack of a correlation between γ-H2AX foci kinetics in lymphocytes and the severity of acute normal tissue reactions during IMRT treatment for head and neck cancer. Int J Radiat Biol 87:46–56
  • Williams RS, Moncalian G, Williams JS, et al. (2008). Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 135:97–109
  • Xiao W, Graham PH, Power CA, et al. (2012). CD44 is a biomarker associated with human prostate cancer radiation sensitivity. Clin Exp Metastasis 29:1–9
  • Yang C, Wang Y, Zhang GF, et al. (2013). Inhibiting UHRF1 expression enhances radiosensitivity in human esophageal squamous cell carcinoma. Mol Biol Reports 40:5225–35
  • Yoon AJ, Shen J, Wu HC. (2009). Expression of activated checkpoint kinase 2 and histone 2AX in exfoliative oral cells after exposure to ionizing radiation. Radiat Res 171:771–5

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.