Nucks1 synergizes with Trp53 to promote radiation lymphomagenesis in mice

Yue, Yangbo; Leung, Stanley G.; Liu, Yueyong; Huang, Yurong; Grundt, Kirsten; Østvold, Anne-Carine; Jen, Kuang-Yu; Schild, David; Mao, Jian-Hua; Wiese, Claudia

doi:10.18632/oncotarget.11297

Nucks1 synergizes with Trp53 to promote radiation lymphomagenesis in mice

Journal Article · Tue Aug 16 00:00:00 EDT 2016 · Oncotarget

DOI:https://doi.org/10.18632/oncotarget.11297· OSTI ID:1378756

Yue, Yangbo ^[1]; Leung, Stanley G. ^[1]; Liu, Yueyong ^[1]; Huang, Yurong ^[1]; Grundt, Kirsten ^[2]; Østvold, Anne-Carine ^[2]; Jen, Kuang-Yu ^[3]; Schild, David ^[1]; Mao, Jian-Hua ^[1]; Wiese, Claudia ^[4]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Department of Organismal Systems and Bioresilience, Biological Systems and Engineering Division
Univ. of Oslo (Norway). Department of Molecular Medicine, Institute of Basic Medical Science
Univ. of California, Davis, CA (United States). Department of Pathology and Laboratory Medicine
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Department of Organismal Systems and Bioresilience, Biological Systems and Engineering Division; Colorado State Univ., Fort Collins, CO (United States). Department of Environmental and Radiological Health Sciences

NUCKS1 is a 27 kD vertebrate-specific protein, with a role in the DNA damage response. Here, we show that after 4 Gy total-body X-irradiation, Trp53+/- Nucks1+/- mice more rapidly developed tumors, particularly thymic lymphoma (TL), than Trp53+/- mice. TLs in both cohorts showed loss of heterozygosity (LOH) of the Trp53+ allele in essentially all cases. In contrast, LOH of the Nucks1+ allele was rare. Nucks1 expression correlated well with Nucks1 gene dosage in normal thymi, but was increased in the majority of TLs from Trp53+/- Nucks1+/- mice, suggesting that elevated Nucks1 message may be associated with progression towards malignancy in vivo. Trp53+/- Nucks1+/- mice frequently succumbed to CD4- CD8- TLs harboring translocations involving Igh but not Tcra/d, indicating TLs in Trp53+/- Nucks1+/- mice mostly originated prior to the double positive stage and at earlier lineage than TLs in Trp53+/- mice. Monoclonal rearrangements at Tcrb were more prevalent in TLs from Trp53+/- Nucks1+/- mice, as was infiltration of primary TL cells to distant organs (liver, kidney and spleen). We propose that, in the context of Trp53 deficiency, wild type levels of Nucks1 are required to suppress radiation-induced TL, likely through the role of the NUCKS1 protein in the DNA damage response.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1378756

Journal Information:: Oncotarget, Journal Name: Oncotarget Journal Issue: 38 Vol. 7; ISSN 1949-2553

Publisher:: Impact JournalsCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

Identification of NUCKS1 as a colorectal cancer prognostic marker through integrated expression and copy number analysis Kikuchi, Akifumi; Ishikawa, Toshiaki; Mogushi, Kaoru International Journal of Cancer, Vol. 132, Issue 10 https://doi.org/10.1002/ijc.27911	journal	November 2012
Using mouse models to investigate the biological and physiological consequences of defects in the Fanconi anaemia/breast cancer DNA repair signalling pathway Tischkowitz, Marc; Winqvist, Robert The Journal of Pathology, Vol. 224, Issue 3 https://doi.org/10.1002/path.2903	journal	May 2011
Constitutive and dynamic phosphorylation and acetylation sites on NUCKS, a hypermodified nuclear protein, studied by quantitative proteomics Wiśniewski, Jacek R.; Zougman, Alexandre; Krüger, Sonja Proteins: Structure, Function, and Bioinformatics, Vol. 73, Issue 3 https://doi.org/10.1002/prot.22104	journal	May 2008
Quality control of homologous recombination Liu, Ting; Huang, Jun Cellular and Molecular Life Sciences, Vol. 71, Issue 19 https://doi.org/10.1007/s00018-014-1649-5	journal	May 2014
The role of p53 in tumour suppression: lessons from mouse models Attardi, L. D.; Jacks, T. Cellular and Molecular Life Sciences CMLS, Vol. 55, Issue 1 https://doi.org/10.1007/s000180050269	journal	January 1999
Basics of PD-1 in self-tolerance, infection, and cancer immunity Chikuma, Shunsuke International Journal of Clinical Oncology, Vol. 21, Issue 3 https://doi.org/10.1007/s10147-016-0958-0	journal	February 2016
Identification and characterization of two putative nuclear localization signals (NLS) in the DNA-binding protein NUCKS Grundt, Kirsten; Haga, Ingvild V.; Huitfeldt, Henrik S. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1773, Issue 9 https://doi.org/10.1016/j.bbamcr.2007.05.013	journal	September 2007
Characterisation of the NUCKS gene on human chromosome 1q32.1 and the presence of a homologous gene in different species Grundt, Kirsten; Haga, Ingvild Vågslid; Aleporou-Marinou, Vasiliki Biochemical and Biophysical Research Communications, Vol. 323, Issue 3 https://doi.org/10.1016/j.bbrc.2004.08.153	journal	October 2004
NUCKS Is a Positive Transcriptional Regulator of Insulin Signaling Qiu, Beiying; Shi, Xiaohe; Wong, Ee Tsin Cell Reports, Vol. 7, Issue 6 https://doi.org/10.1016/j.celrep.2014.05.030	journal	June 2014
Ataxia–telangiectasia, an evolving phenotype Chun, Helen H.; Gatti, Richard A. DNA Repair, Vol. 3, Issue 8-9 https://doi.org/10.1016/j.dnarep.2004.04.010	journal	August 2004
Notch in T-ALL: new players in a complex disease Koch, Ute; Radtke, Freddy Trends in Immunology, Vol. 32, Issue 9 https://doi.org/10.1016/j.it.2011.06.005	journal	September 2011
Proteomic Investigations Reveal a Role for RNA Processing Factor THRAP3 in the DNA Damage Response Beli, Petra; Lukashchuk, Natalia; Wagner, Sebastian A. Molecular Cell, Vol. 46, Issue 2 https://doi.org/10.1016/j.molcel.2012.01.026	journal	April 2012
Complicated biallelic inactivation of Pten in radiation-induced mouse thymic lymphomas Yamaguchi, Yu; Takabatake, Takashi; Kakinuma, Shizuko Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 686, Issue 1-2 https://doi.org/10.1016/j.mrfmmm.2009.12.011	journal	April 2010
Chromosomal changes in high- and low-invasive mouse lung adenocarcinoma cell strains derived from early passage mouse lung adenocarcinoma cell strains Sargent, Linda M.; Ensell, Mang X.; Ostvold, Anne-Carine Toxicology and Applied Pharmacology, Vol. 233, Issue 1 https://doi.org/10.1016/j.taap.2008.01.031	journal	November 2008
Genome maintenance mechanisms for preventing cancer Hoeijmakers, Jan H. J. Nature, Vol. 411, Issue 6835 https://doi.org/10.1038/35077232	journal	May 2001
DNA double-strand breaks: signaling, repair and the cancer connection Khanna, Kum Kum; Jackson, Stephen P. Nature Genetics, Vol. 27, Issue 3 https://doi.org/10.1038/85798	journal	March 2001
Altered expression of miR-24, miR-126 and miR-365 does not affect viability of childhood TCF3-rearranged leukemia cells Akbari Moqadam, F.; Boer, J. M.; Lange-Turenhout, E. A. M. Leukemia, Vol. 28, Issue 5 https://doi.org/10.1038/leu.2013.308	journal	October 2013
Fbxw7/Cdc4 is a p53-dependent, haploinsufficient tumour suppressor gene Mao, Jian-Hua; Perez-losada, Jesus; Wu, Di Nature, Vol. 432, Issue 7018 https://doi.org/10.1038/nature03155	journal	December 2004
A sequence-based variation map of 8.27 million SNPs in inbred mouse strains Frazer, Kelly A.; Eskin, Eleazar; Kang, Hyun Min Nature, Vol. 448, Issue 7157 https://doi.org/10.1038/nature06067	journal	July 2007
The RAG2 C terminus suppresses genomic instability and lymphomagenesis Deriano, Ludovic; Chaumeil, Julie; Coussens, Marc Nature, Vol. 471, Issue 7336 https://doi.org/10.1038/nature09755	journal	March 2011
p53-deficient mice are extremely susceptible to radiation-induced tumorigenesis Kemp, Christopher J.; Wheldon, Tom; Balmain, Allan Nature Genetics, Vol. 8, Issue 1 https://doi.org/10.1038/ng0994-66	journal	September 1994
Regulation of Tcrb recombination ordering by c-Fos-dependent RAG deposition Wang, Xiaoming; Xiao, Gang; Zhang, Yafeng Nature Immunology, Vol. 9, Issue 7 https://doi.org/10.1038/ni.1614	journal	May 2008
Atm heterozygosity does not increase tumor susceptibility to ionizing radiation alone or in a p53 heterozygous background Mao, J. H.; Wu, D.; DelRosario, R. Oncogene, Vol. 27, Issue 51 https://doi.org/10.1038/onc.2008.280	journal	August 2008
DNA damage-induced cell cycle checkpoints and DNA strand break repair in development and tumorigenesis Dasika, Gopal K.; Lin, Suh-Chin J.; Zhao, Song Oncogene, Vol. 18, Issue 55 https://doi.org/10.1038/sj.onc.1203283	journal	December 1999
Genetic interactions between Pten and p53 in radiation-induced lymphoma development Mao, Jian-Hua; Wu, Di; Perez-Losada, Jesus Oncogene, Vol. 22, Issue 52 https://doi.org/10.1038/sj.onc.1207083	journal	November 2003
Hypothalamic NUCKS regulates peripheral glucose homoeostasis Qiu, Beiying; Shi, Xiaohe; Zhou, Qiling Biochemical Journal, Vol. 469, Issue 3 https://doi.org/10.1042/bj20150450	journal	July 2015
Site-specific Phosphorylation Dynamics of the Nuclear Proteome during the DNA Damage Response Bennetzen, Martin V.; Larsen, Dorthe Helena; Bunkenborg, Jakob Molecular & Cellular Proteomics, Vol. 9, Issue 6 https://doi.org/10.1074/mcp.m900616-mcp200	journal	June 2010
p53 and its mutants in tumor cell migration and invasion Muller, Patricia A. J.; Vousden, Karen H.; Norman, Jim C. The Journal of Cell Biology, Vol. 192, Issue 2 https://doi.org/10.1083/jcb.201009059	journal	January 2011
Radiation-induced deletions in the 5' end region of Notch1 lead to the formation of truncated proteins and are involved in the development of mouse thymic lymphomas Tsuji, H.; Ishii-Ohba, H.; Ukai, H. Carcinogenesis, Vol. 24, Issue 7 https://doi.org/10.1093/carcin/bgg071	journal	May 2003
A hypomorphic Artemis human disease allele causes aberrant chromosomal rearrangements and tumorigenesis Jacobs, Cheryl; Huang, Ying; Masud, Tehmina Human Molecular Genetics, Vol. 20, Issue 4 https://doi.org/10.1093/hmg/ddq524	journal	December 2010
NUCKS1 is a novel RAD51AP1 paralog important for homologous recombination and genome stability Parplys, Ann C.; Zhao, Weixing; Sharma, Neelam Nucleic Acids Research https://doi.org/10.1093/nar/gkv859	journal	August 2015
Snaps and mends: DNA breaks and chromosomal translocations Javadekar, Saniya M.; Raghavan, Sathees C. FEBS Journal, Vol. 282, Issue 14 https://doi.org/10.1111/febs.13311	journal	May 2015
An Oncogene-Induced DNA Damage Model for Cancer Development Halazonetis, T. D.; Gorgoulis, V. G.; Bartek, J. Science, Vol. 319, Issue 5868 https://doi.org/10.1126/science.1140735	journal	March 2008
ATM-Dependent and -Independent Dynamics of the Nuclear Phosphoproteome After DNA Damage Bensimon, A.; Schmidt, A.; Ziv, Y. Science Signaling, Vol. 3, Issue 151 https://doi.org/10.1126/scisignal.2001034	journal	December 2010
The Mechanism of Double-Strand DNA Break Repair by the Nonhomologous DNA End-Joining Pathway Lieber, Michael R. Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev.biochem.052308.093131	journal	June 2010
Involvement of Illegitimate V(D)J Recombination or Microhomology-Mediated Nonhomologous End-Joining in the Formation of Intragenic Deletions of theNotch1Gene in Mouse Thymic Lymphomas Tsuji, Hideo; Ishii-Ohba, Hiroko; Katsube, Takanori Cancer Research, Vol. 64, Issue 24 https://doi.org/10.1158/0008-5472.can-03-1163	journal	December 2004
Extensive Chromosomal Instability in Rad51d -Deficient Mouse Cells Smiraldo, Phillip G.; Gruver, Aaron M.; Osborn, Joshua C. Cancer Research, Vol. 65, Issue 6 https://doi.org/10.1158/0008-5472.can-04-2079	journal	March 2005
Loss of Rad51c Leads to Embryonic Lethality and Modulation of Trp53-Dependent Tumorigenesis in Mice Kuznetsov, Sergey G.; Haines, Diana C.; Martin, Betty K. Cancer Research, Vol. 69, Issue 3 https://doi.org/10.1158/0008-5472.can-08-3057	journal	January 2009
Array-based comparative genomic hybridization and copy number variation in cancer research Cho, E. K.; Tchinda, J.; Freeman, J. L. Cytogenetic and Genome Research, Vol. 115, Issue 3-4 https://doi.org/10.1159/000095923	journal	January 2006
Sequential mutations in Notch1, Fbxw7, and Tp53 in radiation-induced mouse thymic lymphomas Jen, Kuang-Yu; Song, Ihn Young; Banta, Karl Luke Blood, Vol. 119, Issue 3 https://doi.org/10.1182/blood-2011-01-327619	journal	January 2012
NUCKS overexpression in breast cancer Drosos, Yiannis; Kouloukoussa, Mirsini; Østvold, Anne Cancer Cell International, Vol. 9, Issue 1 https://doi.org/10.1186/1475-2867-9-19	journal	January 2009
High resolution genomic analysis of sporadic breast cancer using array-based comparative genomic hybridization Naylor, Tara L.; Greshock, Joel; Wang, Yan Breast Cancer Research, Vol. 7, Issue 6 https://doi.org/10.1186/bcr1356	journal	November 2005
Radiation-Associated Loss of Heterozygosity at theZnfn1a1(Ikaros) Locus on Chromosome 11 in Murine Thymic Lymphomas Shimada, Yoshiya; Nishimura, Mayumi; Kakinuma, Shizuko Radiation Research, Vol. 154, Issue 3 https://doi.org/10.1667/0033-7587(2000)154[0293:raloha]2.0.co;2	journal	September 2000
Comparison of Properties of Spontaneous and Radiation-Induced Mouse Thymic Lymphomas: Role of Trp53 and Radiation Kubota, Tomoyuki; Yoshikai, Yoshihiro; Tamura, Yasushi Radiation Research, Vol. 163, Issue 2 https://doi.org/10.1667/rr3303	journal	February 2005
Immunohistochemical study of nuclear ubiquitous casein and cyclin-dependent kinase substrate 1 in invasive breast carcinoma of no special type Symonowicz, Krzysztof; DuŚ-Szachniewicz, Kamila; WoŹNiak, Marta Experimental and Therapeutic Medicine, Vol. 8, Issue 4 https://doi.org/10.3892/etm.2014.1847	journal	July 2014
Effect of NUCKS-1 Overexpression on Cytokine Profiling in Obese Women with Breast Cancer Soliman, Nema Ali; Zineldeen, Doaa Hussein; El-Khadrawy, Osama Helmy Asian Pacific Journal of Cancer Prevention, Vol. 15, Issue 2 https://doi.org/10.7314/apjcp.2014.15.2.837	journal	January 2014
Brca2-Null Embryonic Survival is Prolonged on the BALB/c Genetic Background Bennett, L. Michelle; McAllister, Kimberly A.; Blackshear, Pamela E. Molecular Carcinogenesis, Vol. 28, Issue 3 https://doi.org/10.1002/1098-2744(200007)28:3<174::AID-MC6>3.0.CO;2-C	journal	January 2000
Loss of p53 partially rescues embryonic development of Palb2 knockout mice but does not foster haploinsufficiency of Palb2 in tumour suppression Bouwman, Peter; Drost, Rinske; Klijn, Christiaan The Journal of Pathology, Vol. 224, Issue 1 https://doi.org/10.1002/path.2861	journal	March 2011
Combined evaluation of the expression of NUCKS and Ki-67 proteins as independent prognostic factors for patients with gastric adenocarcinoma Yang, Ming; Wang, Xiaoxia; Zhao, Qi Tumor Biology, Vol. 35, Issue 8 https://doi.org/10.1007/s13277-014-1880-6	journal	May 2014
NUCKS1 overexpression is a novel biomarker for recurrence-free survival in cervical squamous cell carcinoma Gu, Lina; Xia, Bairong; Zhong, Lili Tumor Biology, Vol. 35, Issue 8 https://doi.org/10.1007/s13277-014-2035-5	journal	May 2014
A putative DNA-binding domain in the NUCKS protein Grundt, Kirsten; Skjeldal, Lars; Anthonsen, Henrik W. Archives of Biochemistry and Biophysics, Vol. 407, Issue 2 https://doi.org/10.1016/S0003-9861(02)00513-1	journal	November 2002
Histone H2AX Bassing, Craig H.; Suh, Heikyung; Ferguson, David O. Cell, Vol. 114, Issue 3 https://doi.org/10.1016/S0092-8674(03)00566-X	journal	August 2003
Quantitative Proteomic Atlas of Ubiquitination and Acetylation in the DNA Damage Response Elia, Andrew E. H.; Boardman, Alexander P.; Wang, David C. Molecular Cell, Vol. 59, Issue 5 https://doi.org/10.1016/j.molcel.2015.05.006	journal	September 2015
DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis Bartkova, Jirina; Hořejší, Zuzana; Koed, Karen Nature, Vol. 434, Issue 7035 https://doi.org/10.1038/nature03482	journal	April 2005
Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions Gorgoulis, Vassilis G.; Vassiliou, Leandros-Vassilios F.; Karakaidos, Panagiotis Nature, Vol. 434, Issue 7035 https://doi.org/10.1038/nature03485	journal	April 2005
Deletion of Irf5 protects hematopoietic stem cells from DNA damage-induced apoptosis and suppresses γ-irradiation-induced thymic lymphomagenesis Bi, X.; Feng, D.; Korczeniewska, J. Oncogene, Vol. 33, Issue 25 https://doi.org/10.1038/onc.2013.295	journal	August 2013
KIF14 is a candidate oncogene in the 1q minimal region of genomic gain in multiple cancers Corson, Timothy W.; Huang, Annie; Tsao, Ming-Sound Oncogene, Vol. 24, Issue 30 https://doi.org/10.1038/sj.onc.1208641	journal	May 2005
Hypothalamic NUCKS regulates peripheral glucose homoeostasis Qiu, Beiying; Shi, Xiaohe; Zhou, Qiling Biochemical Journal, Vol. 469, Issue 3 https://doi.org/10.1042/BJ20150450	journal	July 2015
Site-specific Phosphorylation Dynamics of the Nuclear Proteome during the DNA Damage Response Bennetzen, Martin V.; Larsen, Dorthe Helena; Bunkenborg, Jakob Molecular & Cellular Proteomics, Vol. 9, Issue 6 https://doi.org/10.1074/mcp.M900616-MCP200	journal	June 2010
ATM-deficient thymic lymphoma is associated with aberrant tcrd rearrangement and gene amplification Zha, Shan; Bassing, Craig H.; Sanda, Takaomi Journal of Experimental Medicine, Vol. 207, Issue 7 https://doi.org/10.1084/jem.20100285	journal	June 2010
Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Ludwig, T.; Chapman, D. L.; Papaioannou, V. E. Genes & Development, Vol. 11, Issue 10 https://doi.org/10.1101/gad.11.10.1226	journal	May 1997
Programmed DNA breaks in lymphoid cells: repair mechanisms and consequences in human disease Prochazkova, Jana; Loizou, Joanna I. Immunology, Vol. 147, Issue 1 https://doi.org/10.1111/imm.12547	journal	November 2015
ATM and ATR Substrate Analysis Reveals Extensive Protein Networks Responsive to DNA Damage Matsuoka, S.; Ballif, B. A.; Smogorzewska, A. Science, Vol. 316, Issue 5828 https://doi.org/10.1126/science.1140321	journal	May 2007
Involvement of Illegitimate V(D)J Recombination or Microhomology-Mediated Nonhomologous End-Joining in the Formation of Intragenic Deletions of theNotch1Gene in Mouse Thymic Lymphomas Tsuji, Hideo; Ishii-Ohba, Hiroko; Katsube, Takanori Cancer Research, Vol. 64, Issue 24 https://doi.org/10.1158/0008-5472.CAN-03-1163	journal	December 2004
Extensive Chromosomal Instability in Rad51d -Deficient Mouse Cells Smiraldo, Phillip G.; Gruver, Aaron M.; Osborn, Joshua C. Cancer Research, Vol. 65, Issue 6 https://doi.org/10.1158/0008-5472.CAN-04-2079	journal	March 2005
Loss of Rad51c Leads to Embryonic Lethality and Modulation of Trp53-Dependent Tumorigenesis in Mice Kuznetsov, Sergey G.; Haines, Diana C.; Martin, Betty K. Cancer Research, Vol. 69, Issue 3 https://doi.org/10.1158/0008-5472.CAN-08-3057	journal	January 2009
Radiation-Associated Loss of Heterozygosity at theZnfn1a1(Ikaros) Locus on Chromosome 11 in Murine Thymic Lymphomas Shimada, Yoshiya; Nishimura, Mayumi; Kakinuma, Shizuko Radiation Research, Vol. 154, Issue 3 https://doi.org/10.1667/0033-7587(2000)154[0293:RALOHA]2.0.CO;2	journal	September 2000
Comparison of Properties of Spontaneous and Radiation-Induced Mouse Thymic Lymphomas: Role of Trp53 and Radiation Kubota, Tomoyuki; Yoshikai, Yoshihiro; Tamura, Yasushi Radiation Research, Vol. 163, Issue 2 https://doi.org/10.1667/RR3303	journal	February 2005
Expression profiles of adult T-cell leukemia–lymphoma and associations with clinical responses to zidovudine and interferon α Alizadeh, Ash A.; Bohen, Sean P.; Lossos, Chen Leukemia & Lymphoma, Vol. 51, Issue 7 https://doi.org/10.3109/10428191003728628	journal	April 2010
Somatic inactivation of Tp53 in hematopoietic stem cells or thymocytes predisposes mice to thymic lymphomas with clonal translocations DeMicco, Amy; Yang-Iott, Katherine; Bassing, Craig H. Cell Cycle, Vol. 12, Issue 20 https://doi.org/10.4161/cc.26299	journal	October 2013
Effect of NUCKS-1 Overexpression on Cytokine Profiling in Obese Women with Breast Cancer Soliman, Nema Ali; Zineldeen, Doaa Hussein; El-Khadrawy, Osama Helmy Asian Pacific Journal of Cancer Prevention, Vol. 15, Issue 2 https://doi.org/10.7314/APJCP.2014.15.2.837	journal	January 2014

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
NUCKS1
V(D)J recombination
double-strand break repair
ionizing radiation
thymic lymphoma

Nucks1 synergizes with Trp53 to promote radiation lymphomagenesis in mice

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