Extreme variation in apoptosis capacity amongst lymphoid cells of Nijmegen breakage syndrome patients

Allday, 1995, Epstein-Barr virus efficiently immortalizes human B cells without neutralizing the function of p53, EMBO J., 14, 1382, 10.1002/j.1460-2075.1995.tb07124.x Antoccia, 1999, Impaired p53-mediated DNA damage response, cell-cycle disturbance and chromosome aberrations in Nijmegen breakage syndrome lymphoblastoid cell lines, Int. J. Radiat. Biol., 75, 583, 10.1080/095530099140221 Barber, 2000, Detection of individual differences in radiation-induced apoptosis of peripheral blood lymphocytes in normal individuals, ataxia telangiectasia homozygotes and heterozygotes, and breast cancer patients after radiotherapy, Radiat. Res., 153, 570, 10.1667/0033-7587(2000)153[0570:DOIDIR]2.0.CO;2 Bebb, 2001, Radiation induced apoptosis in ataxia telangiectasia homozygote, heterozygote and normal cells, Mutat. Res., 476, 13, 10.1016/S0027-5107(00)00168-8 Brink, 1998, Low p53 and high bcl-2 expression in Reed–Sternberg cells predicts poor clinical outcome for Hodgkin's disease: involvement of apoptosis resistance?, Mod. Pathol., 11, 376 Chrzanowska, 1995, Eleven Polish patients with microcephaly, immunodeficiency, and chromosomal instability: the Nijmegen breakage syndrome, Am. J. Med. Genet., 57, 462, 10.1002/ajmg.1320570321 Clodi, 2000, Cell-surface exposure of phosphatidylserine correlates with the stage of fludarabine-induced apoptosis in chronic lymphocytic leukemia and expression of apoptosis-regulating genes, Cytometry, 40, 19, 10.1002/(SICI)1097-0320(20000501)40:1<19::AID-CYTO3>3.0.CO;2-3 Crompton, 2001, Sources of variation in patient response to radiation treatment, Int. J. Radiat. Oncol. Biol. Phys., 49, 547, 10.1016/S0360-3016(00)01477-2 Demuth, 2004, An inducible null mutant murine model of Nijmegen breakage syndrome proves the essential function of NBS1 in chromosomal stability and cell viability, Hum. Mol. Genet., 13, 2385, 10.1093/hmg/ddh278 Duchaud, 1996, Deregulated apoptosis in ataxia telangiectasia: association with clinical stigmata and radiosensitivity, Cancer Res., 56, 1400 Fernet, 2003, Variation in radiation-induced apoptosis in ataxia telangiectasia lymphoblastoid cell lines, Int. J. Radiat. Biol., 79, 193, 10.1080/0955300031000085731 Friesen, 1996, Involvement of the CD95 (APO-1/FAS) receptor/ligand system in drug-induced apoptosis in leukemia cells, Nat. Med., 2, 574, 10.1038/nm0596-574 Hainaut, 1995, The tumor suppressor protein p53: a receptor to genotoxic stress that controls cell growth and survival, Curr. Opin. Oncol., 7, 76, 10.1097/00001622-199507010-00012 Hamilton, 1995, Bleomycin induces apoptosis in human alveolar macrophages, Am. J. Physiol., 269, L318 Hermine, 1996, Prognostic significance of bcl-2 protein expression in aggressive non-Hodgkin's lymphoma. Groupe d’Etude des Lymphomes de l’Adulte (GELA), Blood, 87, 265, 10.1182/blood.V87.1.265.265 Humar, 1997, Elevated frequency of p53-independent apoptosis after irradiation increases levels of DNA breaks in ataxia telangiectasia lymphoblasts, Int. J. Radiat. Biol., 72, 257, 10.1080/095530097143257 Jongmans, 1998, The p53-mediated DNA damage response to ionizing radiation in fibroblasts from ataxia-without-telangiectasia patients, Int. J. Radiat. Biol., 74, 287, 10.1080/095530098141438 Kinzler, 1997, Cancer-susceptibility genes. Gatekeepers and caretakers, Nature, 386, 761, 10.1038/386761a0 Koopman, 1994, Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis, Blood, 84, 1415, 10.1182/blood.V84.5.1415.bloodjournal8451415 Kramer, 1998, Clinical relevance of BCL2, BCL6, and MYC rearrangements in diffuse large B-cell lymphoma, Blood, 92, 3152, 10.1182/blood.V92.9.3152 Kruger, 2007, Cancer incidence in Nijmegen breakage syndrome is modulated by the amount of a variant NBS protein, Carcinogenesis, 28, 107, 10.1093/carcin/bgl126 Lee, 2004, Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex, Science, 304, 93, 10.1126/science.1091496 Liao, 1999, Ataxia telangiectasia-mutated gene product inhibits DNA damage-induced apoptosis via ceramide synthase, J. Biol. Chem., 274, 17908, 10.1074/jbc.274.25.17908 Lim, 2000, ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway, Nature, 404, 613, 10.1038/35007091 Los, 1997, Cross-resistance of CD95- and drug-induced apoptosis as a consequence of deficient activation of caspases (ICE/Ced-3 proteases), Blood, 90, 3118, 10.1182/blood.V90.8.3118 Maser, 2001, An alternative mode of translation permits production of a variant NBS1 protein from the common Nijmegen breakage syndrome allele, Nat. Genet., 27, 417, 10.1038/86920 Matsuura, 1998, Radiation induction of p53 in cells from Nijmegen breakage syndrome is defective but not similar to ataxia-telangiectasia, Biochem. Biophys. Res. Commun., 242, 602, 10.1006/bbrc.1997.7924 Meijer, 1999, Epstein-Barr virus-transformed lymphoblastoid cell lines of ataxia telangiectasia patients are defective in X-ray-induced apoptosis, Int. J. Radiat. Biol., 75, 709, 10.1080/095530099140041 Muris, 2005, Immunohistochemical profiling of caspase signaling pathways predicts clinical response to chemotherapy in primary nodal diffuse large B-cell lymphomas, Blood, 105, 2916, 10.1182/blood-2004-07-2716 Neitzel, 1986, A routine method for the establishment of permanent growing lymphoblastoid cell lines, Hum. Genet., 73, 320, 10.1007/BF00279094 Nicoletti, 1991, A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry, J. Immunol. Methods, 139, 271, 10.1016/0022-1759(91)90198-O Portis, 2003, Epstein-Barr Virus (EBV) LMP2A induces alterations in gene transcription similar to those observed in Reed–Sternberg cells of Hodgkin lymphoma, Blood, 102, 4166, 10.1182/blood-2003-04-1018 Powers, 2004, E2F1 uses the ATM signaling pathway to induce p53 and Chk2 phosphorylation and apoptosis, Mol. Cancer Res., 2, 203, 10.1158/1541-7786.203.2.4 Rogoff, 2004, Apoptosis associated with deregulated E2F activity is dependent on E2F1 and Atm/Nbs1/Chk2, Mol. Cell. Biol., 24, 2968, 10.1128/MCB.24.7.2968-2977.2004 Seemanova, 1985, Familial microcephaly with normal intelligence, immunodeficiency, and risk for lymphoreticular malignancies: a new autosomal recessive disorder, Am. J. Med. Genet., 20, 639, 10.1002/ajmg.1320200410 Shi, 2001, High levels of delayed radiation-induced apoptosis observed in lymphoblastoid cell lines from ataxia-telangiectasia patients, Int. J. Radiat. Oncol. Biol. Phys., 49, 555, 10.1016/S0360-3016(00)01478-4 Shigeta, 1999, Defective control of apoptosis and mitotic spindle checkpoint in heterozygous carriers of ATM mutations, Cancer Res., 59, 2602 Shiloh, 1997, Ataxia-telangiectasia and the Nijmegen breakage syndrome: related disorders but genes apart, Annu. Rev. Genet., 31, 635, 10.1146/annurev.genet.31.1.635 Siwicki, 2003, Telomere maintenance and cell cycle regulation in spontaneously immortalized T-cell lines from Nijmegen breakage syndrome patients, Exp. Cell Res., 287, 178, 10.1016/S0014-4827(03)00140-X Span, 2002, The dynamic process of apoptosis analyzed by flow cytometry using annexin-V/propidium iodide and a modified in situ end labeling technique, Cytometry, 47, 24, 10.1002/cyto.10028 Stracker, 2007, The carboxy terminus of NBS1 is required for induction of apoptosis by the MRE11 complex, Nature, 447, 218, 10.1038/nature05740 Takagi, 1998, Defective control of apoptosis, radiosensitivity, and spindle checkpoint in ataxia telangiectasia, Cancer Res., 58, 4923 ten Berge, 2002, Expression levels of apoptosis-related proteins predict clinical outcome in anaplastic large cell lymphoma, Blood, 99, 4540, 10.1182/blood.V99.12.4540 2000, Nijmegen breakage syndrome, Arch. Dis. Child., 82, 400, 10.1136/adc.82.5.400 Varon, 1998, Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome, Cell, 93, 467, 10.1016/S0092-8674(00)81174-5 Vernole, 1998, Induction of apoptosis by bleomycin in resting and cycling human lymphocytes, Mutagenesis, 1, 209, 10.1093/mutage/13.3.209 Vit, 2000, ATM protein is required for radiation-induced apoptosis and acts before mitochondrial collapse, Int. J. Radiat. Biol., 76, 841, 10.1080/09553000050029002 Weemaes, 1981, A new chromosomal instability disorder: the Nijmegen breakage syndrome, Acta Paediatr. Scand., 70, 557, 10.1111/j.1651-2227.1981.tb05740.x Weemaes, 1994, Nijmegen breakage syndrome: a progress report, Int. J. Radiat. Biol., 66, S185, 10.1080/09553009414552021 Wesselborg, 1999, Anticancer drugs induce caspase-8/FLICE activation and apoptosis in the absence of CD95 receptor/ligand interaction, Blood, 93, 3053, 10.1182/blood.V93.9.3053 Yamazaki, 1998, Characterization of cell cycle checkpoint responses after ionizing radiation in Nijmegen breakage syndrome cells, Cancer Res., 58, 2316 Zhang, 2001, Ionizing radiation-induced apoptosis in ataxia-telangiectasia fibroblasts. Roles of caspase-9 and cellular inhibitor of apoptosis protein-1, J. Biol. Chem., 276, 28842, 10.1074/jbc.M010525200