Involvement of V (D) J recombinase in the generation of intragenic deletions in the Rit1/Bcl11b tumor suppressor gene in γ-ray-induced thymic lymphomas and in normal thymus of the mouse

Carcinogenesis

Volumn 25, Issue 6, 2004, Pages 1069-1075

  Sakata, Jun ^a,b   Inoue, Jun ^a   Ohi, Hiroyuki ^a   Kosugi Okano, Hitomi ^a   Mishima, Yukio ^a   Hatakeyama, Katsuyoshi ^a   Niwa, Ohtsura ^c   Kominami, Ryo ^a  

^a NIIGATA UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEOTIDE; PROTEIN BCL 11B; RAG1 PROTEIN; RAG2 PROTEIN; RECOMBINASE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; PRIMER DNA; RAS PROTEIN; RIT1 PROTEIN, MOUSE;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CHROMOSOME 12; CHROMOSOME BREAKAGE; CONTROLLED STUDY; ENZYME ACTIVITY; GAMMA RADIATION; GENE DELETION; GENE SEQUENCE; GENETIC RECOMBINATION; HOMOZYGOSITY; INTRON; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEFICIENCY; THYMOCYTE; THYMUS; THYMUS LYMPHOMA; ANIMAL; ENZYMOLOGY; FEMALE; GENETICS; LYMPHOMA; MALE; METABOLISM; NUCLEOTIDE SEQUENCE; RADIATION INJURY; THYMOMA;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; FEMALE; GAMMA RAYS; GENE DELETION; LYMPHOMA; MALE; MICE; NEOPLASMS, RADIATION-INDUCED; RAS PROTEINS; THYMUS GLAND; THYMUS NEOPLASMS; VDJ RECOMBINASES;

EID: 3042736733     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/bgh094     Document Type: Article

References (41)

1. Little,J.B. (2000) Radiation carcinogenesis. Carcinogenesis, 21, 397-404.
2. Goodhead,D.T., Thacker,J. and Cox,R. (1993) Weiss lecture. Effects of radiations of different quantities on cells: molecular mechanisms of damage and repair. Int. J. Radiat. Biol., 63, 543-556.
3. Ferguson,D.O., Sekiguchi,J.M., Chang,S., Frank,K.M., Gao,Y., DePinho,R.A. and Alt,F.W. (2000) The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc. Natl Acad. Sci. USA, 97, 6630-6633.
4. Richardson,C. and Jasin,M. (2000) Frequent chromosomal translocations induced by DNA double-strand breaks. Nature, 405, 697-700.
5. Davis,M.M. and Bjorkman,P.J. (1988) T-cell antigen receptor genes and T-cell recognition. Nature, 334, 395-402.
6. Bassing,C.H., Swat,W. and Alt,F.W. (2002) The mechanism and regulation of chromosomal V(D)J recombination. Cell, 109, 45-55.
7. Roth,D.B. (2003) Restraining the V(D)J recombinase. Nature Rev. Immunol., 3, 656-666.
8. Hiom,K., Melek,M. and Gellert,M. (1998) DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell, 94, 463-470.
9. Aplan,P.D., Lombardi,D.P., Ginsberg,A.M., Cossman,J., Bertness,V.L. and Kirsch,I.R. (1990) Disruption of the human SCL locus by "illegitimate" V-(D)-J recombinase activity. Science, 250, 1426-1429.
10. Brown,L., Cheng,J.T., Chen,Q., Siciliano,M.J., Crist,W., Buchanan,G. and Baer,R. (1990) Site-specific recombination of the tal-1 gene is a common occurrence in human T cell leukemia. EMBO J., 10, 3343-3351.
11. Fuscoe,J.C., Zimmerman,L.J., Lippert,M.J., Nicklas,J.A., O'Neill,J.P. and Albertini,R.J. (1991) V(D)J recombinase-like activity mediates hprt gene deletion in human fetal T-lymphocytes. Cancer Res., 51, 6001-6005.
12. Aster,J.C., Kobayashi,Y., Shiota,M., Mori,S. and Sklar,J. (1992) Detection of the t(14;18) at similar frequencies in hyperplastic lymphoid tissues from American and Japanese patients. Am. J. Pathol., 141, 291-299.
13. Liu,Y., Hernandez,A.M., Shibata,D. and Cortopassi,G.A. (1994) BCL2 translocation frequency rises with age in humans. Proc. Natl Acad. Sci. USA, 91, 8910-8914.
14. INK4a/CDKN2 by illegitimate V(D)J recombinase activity in T-cell acute lymphoblastic leukemias. Blood, 90, 3720-3726.
15. Kirsch,I.R. and Lista,F. (1997) Lymphocyte-specific genomic instability and risk of lymphoid malignancy. Semin. Immunol., 9, 207-215.
16. Matsumoto,Y., Kosugi,S., Shinbo,T. et al. (1998) Allelic loss analysis of gamma-ray-induced mouse thymic lymphomas: two candidate tumor suppressor gene loci on chromosomes 12 and 16. Oncogene, 16, 2747-2754.
17. Shinbo,T., Matsuki,A., Matsumoto,Y., Kosugi,S., Takahashi,Y., Niwa,O. and Kominami,R. (1999) Allelic loss mapping and physical delineation of a region harboring a putative thymic lymphoma suppressor gene on chromosome 12. Oncogene, 18, 4131-4136.
18. Wakabayashi,Y., Inoue,J., Takahashi,Y., Matsuki,A., Kosugi-Okano,H., Shinbo,T., Mishima,Y., Niwa,O. and Kominami,R. (2003) Homozygous deletions and point mutations of the Rit1/Bcl11b gene in γ-ray induced mouse thymic lymphomas. Bioehem. Biophys. Res. Commun., 301, 598-603.
19. Wakabayashi,Y., Watanabe,H., Inoue,J. et al. (2003) Bcl11b is required for differentiation and survival of αβ T lymphocytes. Nature Immunol., 4, 533-539.
20. 6-methylguanine, in transcribed genes prevents mutation of H-ras in rat mammary tumorigenesis induced by ethynitrosourea in place of methylnitrosourea. Proc. Natl Acad. Sci. USA, 95, 1635-1640.
21. Sato,H., Tamura,Y., Ochiai,Y., Kodama,Y., Hatakeyama,K., Niwa,O. and Kominami,R. (2003) The D4Mit12 locus on mouse chromosome 4 provides susceptibility to both γ-ray induced and N-methyl-N-nitrosourea-induced thymic lymphomas. Cancer Sci., 94, 668-671.
22. Gilfillan,S., Dierich,A., Lemeur,M. Benoist,C. and Mathis,D. (1993) Mice lacking TdT: mature animals with an immature lymphocyte repertoire. Science, 261, 1175-1178.
23. Komori,T., Okada,A., Stewart,V. and Alt,F.W. (1993) Lack of N regions in antigen receptor variable region genes of TdT-deficient lymphocytes. Science, 261, 1171-1175.
24. Ramsden,D.A., McBlane,J.F., van Gent,D.C. and Gellert,M. (1996) Distinct DNA sequence and structure requirements for the two steps of V(D)J recombination signal cleavage. EMBO J., 15, 3197-3206.
25. Lewis,S.M., Agard,E., Suh,S. and Czyzyk,L. (1997) Cryptic signals and the fidelity of V(D)J joining. Mol. Cell. Biol., 17, 3125-3136.
26. Nacht,M. and Jacks,T. (1998) VDJ recombination is not required for the development of lymphoma in p53-deficient mice. Cell Growth Differ., 9, 131-138.
27. Liao,M.J., Zhang,X.X., Hill,R., Gao,J., Qumsiyeh,M.B., Nichols,W. and Dyke,T.V. (1998) No requirement for V(D)J recombination in p53-deficient thymic lymphoma. Mol. Cell. Biol., 18, 3495-3501.
28. Plass,C. (2002) Cancer epigenomics. Hum. Mol. Genet., 11, 2479-2488.
29. Muto,M., Kubo,E. and Sado,T. (1987) Development of prelymphoma cells committed to thymic lymphomas during radiation-induced thymic lymphomagenesis in B10 mice. Cancer Res., 47, 3469-3472.
30. Muto,M., Kubo,E., Kamisaku,H. and Sado,T. (1990) Phenotypic characterization of thymic prelymphoma cells of B10 mice treated with split-dose irradiation. J. Immunol., 144, 849-853.
31. Lista,F., Bertness,V., Guidos,C.J., Danska,J.S. and Kirsch,I.R. (1997) The absolute number of trans-rearrangements between the TCRG and TCRB loci is predictive of lymphoma risk: a severe combined immune deficiency (SCID) murine model. Cancer Res., 57, 4408-4413.
32. Williams,C.J., Grandal,I., Vesprini,D.J., Wojtyra,U., Danska,J.S. and Guidos,C.J. (2001) Irradiation promotes V(D)J joining and RAG-dependent neoplastic transformation in SCID T-cell precursors. Mol. Cell. Biol., 21, 400-413.
33. Kaplan,H.S., Carnes,W.H., Brown,M.B. and Hiesch,B.B. (1956) Indirect induction of lymphomas in irradiated mice. I. Tumor incidence and morphlogy in mice bearing nonirradiated thymic grafts. Cancer Res., 16, 422-425.
34. Kaplan,H.S. and Brown,M.B. (1952) A quantitative dose response study of lymphoid-tumor development in irradiated C57 black mice. J. Natl Cancer Inst., 13, 185-208.
35. Ludwig,F.C., Elashoff,R.M. and Wellington,J.S. (1968) Murine radiation leukemia and the preleukemic state. Lab. Invest., 19, 240-251.
36. Humblet,C., Defresne,M.P., Greimers,R., Rongy,A.M. and Boniver,J. (1989) Further studies on the mechanism of radiation induced thymic lymphoma prevention by bone marrow transplantation in C57BL mice. Leukemia, 3, 813-818.
37. Potworowski,E.F., Gagnon,F., Beauchemin,C. and St Pierre,Y. (1996) Dendritic cells prevent radiation-induced thymic lymphoma. Leukemia, 10, 1639-1647.
38. Sado,T., Kamisaku,H. and Kubo,E. (1991) Bone marrow-thymus interactions during thymic lymphomagenesis induced by fractionated radiation exposure in B10 mice: analysis using bone marrow transplantation between Thy 1 congenic mice. J. Radiat. Res., 32 (suppl. 2), 168-180.
39. Kamisaku,H., Aizawa,S., Tanaka,K., Watanabe,K. and Sado,T. (2000) Different cellular basis for the resistance of C3H and STS strain mice to the development of thymic lymphomas following fractionated whole-body irradiation: analysis using radiation bone marrow chimeras. Int. J. Radiat. Biol., 76, 1105-1111.
40. Kamisaku,H., Aizawa,S., Kitagawa,M., Ikarashi,Y. and Sado,T. (1997) Limiting dilution analysis of T-cell progenitors in the bone marrow of thymic lymphoma-susceptible B10 and -resistant C3H mice after fractionated whole-body X-irradiation. Int. J. Radiat. Biol., 72, 191-199.
41. Barcellos-Hoff,M.H. and Brooks,A.L. (2001) Extracellular signaling through the microenvironment: a hypothesis relating carcinogenesis, bystander effects and genomic instability. Radiat. Res., 156, 618-627.