Somatic inactivation of ATM in hematopoietic cells predisposes mice to cyclin D3 dependent T cell acute lymphoblastic leukemia

References

• Paganin M, Ferrando A. Molecular pathogenesis and targeted therapies for NOTCH1-induced T-cell acute lymphoblastic leukemia. Blood Rev 2011; 25:83-90; PMID:20965628; http://dx.doi.org/10.1016/j.blre.2010.09.004
   PubMed Web of Science ®Google Scholar
• Pui CH, Robison LL, Look AT. Acute lympho-blastic leukaemia. Lancet 2008; 371:1030-43; PMID:18358930; http://dx.doi.org/10.1016/S0140-6736(08)60457-2
   PubMed Web of Science ®Google Scholar
• Aifantis I, Raetz E, Buonamici S. Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat Rev Immunol 2008; 8:380-90; PMID:18421304; http://dx.doi.org/10.1038/nri2304
   PubMed Web of Science ®Google Scholar
• Grabher C, von Boehmer H, Look AT. Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat Rev Cancer 2006; 6:347-59; PMID:16612405; http://dx.doi.org/10.1038/nrc1880
   PubMed Web of Science ®Google Scholar
• Ko RH, Ji L, Barnette P, Bostrom B, Hutchinson R, Raetz E, Seibel NL, Twist CJ, Eckroth E, Sposto R, et al. Outcome of patients treated for relapsed or refractory acute lymphoblastic leukemia: a Therapeutic Advances in Childhood Leukemia Consortium study. J Clin Oncol 2010; 28:648-54; PMID:19841326; http://dx.doi.org/10.1200/JCO.2009.22.2950
   PubMed Web of Science ®Google Scholar
• Maloney KW, Giller R, Hunger SP. Recent advances in the understanding and treatment of pediatric leukemias. Adv Pediatr 2012; 59:329-58; PMID:22789585; http://dx.doi.org/10.1016/j.yapd.2012.04.010
   PubMedGoogle Scholar
• Smith MA, Seibel NL, Altekruse SF, Ries LA, Melbert DL, O’Leary M, Smith FO, Reaman GH. Outcomes for children and adolescents with cancer: challenges for the twenty-first century. J Clin Oncol 2010; 28:2625-34; PMID:20404250; http://dx.doi.org/10.1200/JCO.2009.27.0421
   PubMed Web of Science ®Google Scholar
• Oeffinger KC, Mertens AC, Sklar CA, Kawashima T, Hudson MM, Meadows AT, Friedman DL, Marina N, Hobbie W, Kadan-Lottick NS, et al. Chronic health conditions in adult survivors of childhood cancer. N Engl J Med 2006; 355:1572-82; PMID:17035650; http://dx.doi.org/10.1056/NEJMsa060185
   PubMed Web of Science ®Google Scholar
• Brady BL, Steinel NC, Bassing CH. Antigen receptor allelic exclusion: an update and reappraisal. J Immunol 2010; 185:3801-8; http://dx.doi.org/10.4049/jimmunol.1001158
   PubMed Web of Science ®Google Scholar
• Bhandoola A, von Boehmer H, Petrie HT, Zuniga-Pflucker JC. Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from. Immunity 2007; 26:678-89; PMID:17582341; http://dx.doi.org/10.1016/j.immuni.2007.05.009
   PubMed Web of Science ®Google Scholar
• Sicinska E, Aifantis I, Le Cam L, Swat W, Borowski C, Yu Q, Ferrando AA, Levin SD, Geng Y, von Boehmer H, et al. Requirement for cyclin D3 in lymphocyte development and T cell leukemias. Cancer Cell 2003; 4:451-61; PMID:14706337; http://dx.doi.org/10.1016/S1535-6108(03)00301-5
   PubMed Web of Science ®Google Scholar
• Bassing CH, Alt FW. The cellular response to general and programmed DNA double strand breaks. DNA Repair 2004; 3:781-96; PMID:15279764; http://dx.doi.org/10.1016/j.dnarep.2004.06.001
   PubMed Web of Science ®Google Scholar
• Shiloh Y, Ziv Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat Rev Mol Cell Biol 2013; 14:197-210; http://dx.doi.org/10.1038/nrm3546
   Web of Science ®Google Scholar
• Morgan SE, Kastan MB. p53 and ATM: cell cycle, cell death, and cancer. Adv Cancer Res 1997; 71:1-25; PMID:9111862; http://dx.doi.org/10.1016/S0065-230X(08)60095-0
   PubMed Web of Science ®Google Scholar
• Franco S, Gostissa M, Zha S, Lombard DB, Murphy MM, Zarrin AA, Yan C, Tepsuporn S, Morales JC, Adams MM, et al. H2AX Prevents DNA Breaks from Progressing to Chromosome Breaks and Translocations. Mol Cell 2006; 21:201-14; PMID:16427010; http://dx.doi.org/10.1016/j.molcel.2006.01.005
   PubMed Web of Science ®Google Scholar
• Yin B, Savic V, Juntilla MM, Bredemeyer AL, Yang-Iott KS, Helmink BA, Koretzky GA, Sleckman BP, Bassing CH. Histone H2AX stabilizes broken DNA strands to suppress chromosome breaks and translocations during V(D)J recombination. J Exp Med 2009; 206:2625-39; PMID:19887394; http://dx.doi.org/10.1084/jem.20091320
   PubMed Web of Science ®Google Scholar
• Ramiro AR, Jankovic M, Callen E, Difilippantonio S, Chen HT, McBride KM, Eisenreich TR, Chen J, Dickins RA, Lowe SW, et al. Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 2006; 440:105-9; PMID:16400328; http://dx.doi.org/10.1038/nature04495
   PubMed Web of Science ®Google Scholar
• Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou F, Campos-Torres J, Leder P. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc Natl Acad Sci U S A 1996; 93:13084-9; PMID:8917548; http://dx.doi.org/10.1073/pnas.93.23.13084
   PubMed Web of Science ®Google Scholar
• Barlow C, Brown KD, Deng CX, Tagle DA, Wynshaw-Boris A. Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nature genetics 1997; 17:453-6; PMID:9398849; http://dx.doi.org/10.1038/ng1297-453
   PubMed Web of Science ®Google Scholar
• Borghesani PR, Alt FW, Bottaro A, Davidson L, Aksoy S, Rathbun GA, Roberts TM, Swat W, Segal RA, Gu Y. Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc Natl Acad Sci U S A 2000; 97:3336-41; PMID:10716718; http://dx.doi.org/10.1073/pnas.97.7.3336
   PubMed Web of Science ®Google Scholar
• Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 1996; 10:2411-22; PMID:8843194; http://dx.doi.org/10.1101/gad.10.19.2411
   PubMed Web of Science ®Google Scholar
• Taylor AM, Metcalfe JA, Thick J, Mak YF. Leukemia and lymphoma in ataxia telangiectasia. Blood 1996; 87:423-38; PMID:8555463
   PubMed Web of Science ®Google Scholar
• Bredemeyer AL, Sharma GG, Huang CY, Helmink BA, Walker LM, Khor KC, Nuskey B, Sullivan KE, Pandita TK, Bassing CH, et al. ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature 2006; 442:466-70; PMID:16799570; http://dx.doi.org/10.1038/nature04866
   PubMed Web of Science ®Google Scholar
• Petiniot LK, Weaver Z, Barlow C, Shen R, Eckhaus M, Steinberg SM, Ried T, Wynshaw-Boris A, Hodes RJ. Recombinase-activating gene (RAG) 2-mediated V(D)J recombination is not essential for tumorigenesis in Atm-deficient mice. Proc Natl Acad Sci U S A 2000; 97:6664-9; PMID:10841564; http://dx.doi.org/10.1073/pnas.97.12.6664
   PubMed Web of Science ®Google Scholar
• Petiniot LK, Weaver Z, Vacchio M, Shen R, Wangsa D, Barlow C, Eckhaus M, Steinberg SM, Wynshaw-Boris A, Ried T, et al. RAG-mediated V(D)J recombination is not essential for tumorigenesis in Atm-deficient mice. Mol Cell Biol 2002; 22:3174-7; PMID:11940674; http://dx.doi.org/10.1128/MCB.22.9.3174-3177.2002
   PubMed Web of Science ®Google Scholar
• Liyanage M, Weaver Z, Barlow C, Coleman A, Pankratz DG, Anderson S, Wynshaw-Boris A, Ried T. Abnormal rearrangement within the alpha/delta T-cell receptor locus in lymphomas from Atm-deficient mice. Blood 2000; 96:1940-6; PMID:10961898
   PubMed Web of Science ®Google Scholar
• Meier M, den Boer ML, Hall AG, Irving JA, Passier M, Minto L, van Wering ER, Janka-Schaub GE, Pieters R. Relation between genetic variants of the ataxia telangiectasia-mutated (ATM) gene, drug resistance, clinical outcome and predisposition to childhood T-lineage acute lymphoblastic leukaemia. Leukemia 2005; 19:1887-95; http://dx.doi.org/10.1038/sj.leu.2403943
   PubMed Web of Science ®Google Scholar
• Ferrando AA, Neuberg DS, Staunton J, Loh ML, Huard C, Raimondi SC, Behm FG, Pui CH, Downing JR, Gilliland DG, et al. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 2002; 1:75-87; PMID:12086890; http://dx.doi.org/10.1016/S1535-6108(02)00018-1
   PubMed Web of Science ®Google Scholar
• Gumy Pause F, Wacker P, Maillet P, Betts D, Sappino AP. ATM gene alterations in childhood acute lymphoblastic leukemias. Human Mutation 2003; 21:554; http://dx.doi.org/10.1002/humu.9140
   Web of Science ®Google Scholar
• Gumy-Pause F, Wacker P, Maillet P, Betts DR, Sappino AP. ATM variants and predisposition to childhood T-lineage acute lymphoblastic leukaemia. Leukemia 2006; 20:526-7; author reply 7; PMID:16408093; http://dx.doi.org/10.1038/sj.leu.2404091
   PubMed Web of Science ®Google Scholar
• Zha S, Sekiguchi J, Brush JW, Bassing CH, Alt FW. Complementary functions of ATM and H2AX in development and suppression of genomic instability. Proc Natl Acad Sci U S A 2008; 105:9302-6; PMID:18599436; http://dx.doi.org/10.1073/pnas.0803520105
   PubMed Web of Science ®Google Scholar
• Yin B, Yang-Iott KS, Chao LH, Bassing CH. Cellular context-dependent effects of H2ax and p53 deletion on the development of thymic lymphoma. Blood 2011; 117:175-85; PMID:20947684; http://dx.doi.org/10.1182/blood-2010-03-273045
   PubMed Web of Science ®Google Scholar
• DeMicco A, Yang-Iott K, Bassing CH. Somatic inactivation of Tp53 in hematopoietic stem cells or thymocytes predisposes mice to thymic lymphomas with clonal translocations. Cell Cycle 2013; 12:3307-16; PMID:24036547; http://dx.doi.org/10.4161/cc.26299
   PubMed Web of Science ®Google Scholar
• Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, Venere M, Ditullio RA Jr, Kastrinakis NG, Levy B, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434:907-13; PMID:15829965; http://dx.doi.org/10.1038/nature03485
   PubMed Web of Science ®Google Scholar
• Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, Guldberg P, Sehested M, Nesland JM, Lukas C, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434:864-70; PMID:15829956; http://dx.doi.org/10.1038/nature03482
   PubMed Web of Science ®Google Scholar
• Georgiades P, Ogilvy S, Duval H, Licence DR, Charnock-Jones DS, Smith SK, Print CG. VavCre transgenic mice: a tool for mutagenesis in hematopoietic and endothelial lineages. Genesis 2002; 34:251-6; PMID:12434335; http://dx.doi.org/10.1002/gene.10161
   PubMed Web of Science ®Google Scholar
• Stadtfeld M, Graf T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development 2005; 132:203-13; PMID:15576407; http://dx.doi.org/10.1242/dev.01558
   PubMed Web of Science ®Google Scholar
• Ogilvy S, Metcalf D, Gibson L, Bath ML, Harris AW, Adams JM. Promoter elements of vav drive transgene expression in vivo throughout the hematopoietic compartment. Blood 1999; 94:1855-63; PMID:10477714
   PubMed Web of Science ®Google Scholar
• Yin B, Lee BS, Yang-Iott KS, Sleckman BP, Bassing CH. Redundant and nonredundant functions of ATM and H2AX in alphabeta T-lineage lymphocytes. J Immunol 2012; 189:1372-9; http://dx.doi.org/10.4049/jimmunol.1200829
   PubMed Web of Science ®Google Scholar
• Zha S, Bassing CH, Sanda T, Brush JW, Patel H, Goff PH, Gatti R, Look AT, Alt FW. ATM-deficient thymic lymphoma is associated with aberrant TCRd rearrangement and gene amplification. J Exp Med 2010; 207:1369-80; In Press; PMID:20566716
   PubMed Web of Science ®Google Scholar
• Brady BL, Oropallo MA, Yang-Iott KS, Serwold T, Hochedlinger K, Jaenisch R, Weissman IL, Bassing CH. Position-dependent silencing of germline Vss segments on TCRss alleles containing preassembled VssDJssCss1 genes. J Immunol 2010; 185:3564-73; http://dx.doi.org/10.4049/jimmunol.0903098
   PubMed Web of Science ®Google Scholar
• Callen E, Bunting S, Huang CY, Difilippantonio MJ, Wong N, Khor B, Mahowald G, Kruhlak MJ, Ried T, Sleckman BP, et al. Chimeric IgH-TCRalpha/delta translocations in T lymphocytes mediated by RAG. Cell Cycle 2009; 8:2408-12; PMID:19556863; http://dx.doi.org/10.4161/cc.8.15.9085
   PubMed Web of Science ®Google Scholar
• Isoda T, Takagi M, Piao J, Nakagama S, Sato M, Masuda K, Ikawa T, Azuma M, Morio T, Kawamoto H, et al. Process for immune defect and chromosomal translocation during early thymocyte development lacking ATM. Blood 2012; 120:789-99; PMID:22709691; http://dx.doi.org/10.1182/blood-2012-02-413195
   PubMed Web of Science ®Google Scholar
• Liyanage M, Coleman A, du Manoir S, Veldman T, McCormack S, Dickson RB, Barlow C, Wynshaw-Boris A, Janz S, Wienberg J, et al. Multicolour spectral karyotyping of mouse chromosomes. Nat Genet 1996; 14:312-5; PMID:8896561; http://dx.doi.org/10.1038/ng1196-312
   PubMed Web of Science ®Google Scholar
• Krangel MS, Carabana J, Abbarategui I, Schlimgen R, Hawwari A. Enforcing order within a complex locus: current perspectives on the control of V(D)J recombination at the murine T-cell receptor alpha/delta locus. Immunol Rev 2004; 200:224-32; PMID:15242408; http://dx.doi.org/10.1111/j.0105-2896.2004.00155.x
   PubMed Web of Science ®Google Scholar
• Sleckman BP, Bardon CG, Ferrini R, Davidson L, Alt FW. Function of the TCR alpha enhancer in alphabeta and gammadelta T cells. Immunity 1997; 7:505-15; PMID:9354471; http://dx.doi.org/10.1016/S1074-7613(00)80372-6
   PubMed Web of Science ®Google Scholar
• Huang CY, Sharma GG, Walker LM, Bassing CH, Pandita TK, Sleckman BP. Defects in coding joint formation in vivo in developing ATM-deficient B and T lymphocytes. J Exp Med 2007; 204:1371-81; PMID:17502661; http://dx.doi.org/10.1084/jem.20061460
   PubMed Web of Science ®Google Scholar
• Matei IR, Gladdy RA, Nutter LM, Canty A, Guidos CJ, Danska JS. ATM deficiency disrupts Tcra locus integrity and the maturation of CD4+CD8+ thymocytes. Blood 2007; 109:1887-96; PMID:17077325; http://dx.doi.org/10.1182/blood-2006-05-020917
   PubMed Web of Science ®Google Scholar
• Bassing CH, Ranganath S, Murphy M, Savic V, Gleason M, Alt FW. Aberrant V(D)J recombination is not required for rapid development of H2ax/p53-deficient thymic lymphomas with clonal translocations. Blood 2008; 111:2163-9; PMID:17855626; http://dx.doi.org/10.1182/blood-2007-08-104760
   PubMed Web of Science ®Google Scholar
• Venkatachalam S, Shi YP, Jones SN, Vogel H, Bradley A, Pinkel D, Donehower LA. Retention of wild-type p53 in tumors from p53 heterozygous mice: reduction of p53 dosage can promote cancer formation. EMBO J 1998; 17:4657-67; PMID:9707425; http://dx.doi.org/10.1093/emboj/17.16.4657
   PubMed Web of Science ®Google Scholar
• Ide F, Kitada M, Sakashita H, Kusama K, Tanaka K, Ishikawa T. p53 haploinsufficiency profoundly accelerates the onset of tongue tumors in mice lacking the xeroderma pigmentosum group A gene. Am J Pathol 2003; 163:1729-33; PMID:14578172; http://dx.doi.org/10.1016/S0002-9440(10)63531-6
   PubMed Web of Science ®Google Scholar
• Choi YJ, Anders L. Signaling through cyclin D-dependent kinases. Oncogene 2014; 33:1890-903; PMID:23644662; http://dx.doi.org/10.1038/onc.2013.137
   PubMed Web of Science ®Google Scholar
• Choi YJ, Li X, Hydbring P, Sanda T, Stefano J, Christie AL, Signoretti S, Look AT, Kung AL, von Boehmer H, et al. The requirement for cyclin D function in tumor maintenance. Cancer Cell 2012; 22:438-51; PMID:23079655; http://dx.doi.org/10.1016/j.ccr.2012.09.015
   PubMed Web of Science ®Google Scholar
• Sawai CM, Freund J, Oh P, Ndiaye-Lobry D, Bretz JC, Strikoudis A, Genesca L, Trimarchi T, Kelliher MA, Clark M, et al. Therapeutic targeting of the cyclin D3:CDK4/6 complex in T cell leukemia. Cancer Cell 2012; 22:452-65; PMID:23079656; http://dx.doi.org/10.1016/j.ccr.2012.09.016
   PubMed Web of Science ®Google Scholar
• Jonkers J, Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 2001; 29:418-25; PMID:11694875; http://dx.doi.org/10.1038/ng747
   PubMed Web of Science ®Google Scholar