The Bloom's syndrome helicase is critical for development and function of the αβ T-cell lineage

Molecular and Cellular Biology

Volumn 27, Issue 5, 2007, Pages 1947-1959

  Babbe, Holger ^a   Chester, Nicholas ^a   Leder, Philip ^a   Reizis, Boris ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; PROTEIN P53; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ANIMAL TISSUE; ARTICLE; BLM GENE; BLOOM SYNDROME; CANCER SUSCEPTIBILITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL SURVIVAL; CHROMOSOME DAMAGE; CONTROLLED STUDY; GENE; GENOMIC INSTABILITY; HOMEOSTASIS; IMMUNE DEFICIENCY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE;

ADENOSINE TRIPHOSPHATASES; ALLELES; ANIMALS; CELL LINEAGE; CELLS, CULTURED; CHROMOSOME ABERRATIONS; DNA HELICASES; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTES; THYMUS GLAND;

EID: 33847236576     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01402-06     Document Type: Article

References (54)

1. Bachrati, C. Z., and I. D. Hickson. 2003. RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem. J. 374:577-606.
2. Bogue, M. A., C. Zhu, E. Aguilar-Cordova, L. A. Donehower, and D. B. Roth. 1996. p53 is required for both radiation-induced differentiation and rescue of V(D)J rearrangement in seid mouse thymocytes. Genes Dev. 10:553-565.
3. Chester, N., H. Babbe, J. Pinkas, C. Manning, and P. Leder. 2006. Mutation of the murine Bloom's syndrome gene produces global genome destabilization. Mol. Cell. Biol. 26:6713-6726.
4. Chester, N., F. Kuo, C. Kozak, C. D. O'Hara, and P. Leder. 1998. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev. 12:3382-3393.
5. de Alboran, I. M., R. C. O'Hagan, F. Gartner, B. Malynn, L. Davidson, R. Rickert, K. Rajewsky, R. A. DePinho, and F. W. Alt. 2001. Analysis of C-MYC function in normal cells via conditional gene-targeted mutation. Immunity 14:45-55.
6. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery, Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221.
7. Ellis, N. A., J. Groden, T. Z. Ye, J. Straughen, D. J. Lennon, S. Ciocci, M. Proytcheva, and J. German. 1995. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83:655-666.
8. Elson, A., Y. Wang, C. J. Daugherty, C. C. Morton, F. Zhou, J. Campos-Torres, and P. Leder. 1996. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 93:13084-13089.
9. Fehling, H. J., A. Krotkova, C. Saint-Ruf, and H. von Boehmer. 1995. Crucial role of the pre-T-cell receptor alpha gene in development of alpha beta but not gamma delta T cells. Nature 375:795-798.
10. Gartner, F., F. W. Alt, R. Monroe, M. Chu, B. P. Sleckman, L. Davidson, and W. Swat. 1999. Immature thymocytes employ distinct signaling pathways for allelic exclusion versus differentiation and expansion. Immunity 10:537-546.
11. Gaymes, T. J., P. S. North, N. Brady, I. D. Hickson, G. J. Mufti, and F. V. Rassool. 2002. Increased error-prone nonhomologous DNA end-joining-a proposed mechanism of chromosomal instability in Bloom's syndrome. Oncogene 21:2525-2533.
12. Gennery, A. R., A. J. Cant, and P. A. Jeggo. 2000. Immunodeficiency associated with DNA repair defects. Clin. Exp. Immunol. 121:1-7.
13. Germain, R. N. 2002. T-cell development and the CD4-CD8 lineage decision. Nat. Rev. Immunol. 2:309-322.
14. German, J. 1993. Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine (Baltimore) 72:393-406.
15. German, J. 1995. Bloom's syndrome. Dermatol. Clin. 13:7-18.
16. Goldrath, A. W. 2002. Maintaining the status quo: T-cell homeostasis. Microbes Infect. 4:539-545.
17. Gounari, F., I. Aifantis, C. Martin, H. J. Fehling, S. Hoeflinger, P. Leder, H. von Boehmer, and B. Reizis. 2002. Tracing lymphopoiesis with the aid of a pTalpha-controlled reporter gene. Nat. Immunol. 3:489-496.
18. Reference deleted.
19. Guidos, C. J., C. J. Williams, I. Grandal, G. Knowles, M. T. Huang, and J. S. Danska. 1996. V(D)J recombination activates a p53-dependent DNA damage checkpoint in seid lymphocyte precursors. Genes Dev. 10:2038-2054.
20. Haks, M. C., P. Krimpenfort, J. Borst, and A. M. Kruisbeek. 1998. The CD3gamma chain is essential for development of both the TCRalphabeta and TCRgammadelta lineages. EMBO J. 17:1871-1882.
21. Hand, R., and J. German. 1975. A retarded rate of DNA chain growth in Bloom's syndrome. Proc. Natl. Acad. Sci. USA 72:758-762.
22. Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169-178.
23. Hoffman, E. S., L. Passoni, T. Crompton, T. M. Leu, D. G. Schatz, A. Koff, M. J. Owen, and A. C. Hayday. 1996. Productive T-cell receptor beta-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10:948-962.
24. Hsieh, C. L., C. F. Arlett, and M. R. Lieber. 1993. V(D)J recombination in ataxia telangiectasia, Bloom's syndrome, and a DNA ligase I-associated immunodeficiency disorder. J. Biol. Chem. 268:20105-20109.
25. Hu, P., S. F. Beresten, A. J. van Brabant, T. Z. Ye, P. P. Pandolfi, F. B. Johnson, L. Guarente, and N. A. Ellis. 2001. Evidence for BLM and topoisomerase IIIalpha interaction in genomic stability. Hum. Mol. Genet. 10:1287-1298.
26. Hutteroth, T. H., S. D. Litwin, and J. German. 1975. Abnormal immune responses of Bloom's syndrome lymphocytes in vitro. J. Clin. Investig. 56:1-7.
27. Jiang, D., M. J. Lenardo, and J. C. Zuniga-Pflucker. 1996. p53 prevents maturation to the CD4+CD8+ stage of thymocyte differentiation in the absence of T cell receptor rearrangement. J. Exp. Med. 183:1923-1928.
28. Kaye, J., M. L. Hsu, M. E. Sauron, S. C. Jameson, N. R. Gascoigne, and S. M. Hedrick. 1989. Selective development of CD4+ T cells in transgenic mice expressing a class II MHC-restricted antigen receptor. Nature 341:746-749.
29. Lee, P. P., D. R. Fitzpatrick, C. Beard, H. K. Jessup, S. Lehar, K. W. Makar, M. Perez-Melgosa, M. T. Sweetser, M. S. Schlissel, S. Nguyen, S. R. Cherry, J. H. Tsai, S. M. Tucker, W. M. Weaver, A. Kelso, R. Jaenisch, and C. B. Wilson. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15:763-774.
30. Luo, G., I. M. Santoro, L. D. McDaniel, I. Nishijima, M. Mills, H. Youssoufian, H. Vogel, R. A. Schultz, and A. Bradley. 2000. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet. 26:424-429.
31. Mak, T. W., A. Hakem, J. P. McPherson, A. Shehabeldin, E. Zablocki, E. Migon, G. S. Duncan, D. Bouchard, A. Wakeham, A. Cheung, J. Karaskova, I. Sarosi, J. Squire, J. Marth, and R. Hakem. 2000. Brca1 required for T cell lineage development but not TCR loci rearrangement. Nat. Immunol. 1:77-82.
32. Maraskovsky, E., L. A. O'Reilly, M. Teepe, L. M. Corcoran, J. J. Peschon, and A. Strasser. 1997. Bcl-2 can rescue T lymphocyte development in interleukin-7 receptor-deficient mice but not in mutant rag-1-/- mice. Cell 89:1011-1019.
33. Marsden, V. S., and A. Strasser. 2003. Control of apoptosis in the immune system: Bcl-2, BH3-only proteins and more. Annu. Rev. Immunol. 21:71-105.
34. McDaniel, L. D., N. Chester, M. Watson, A. D. Borowsky, P. Leder, and R. A. Schultz. 2003. Chromosome instability and tumor predisposition inversely correlate with BLM protein levels. DNA Repair (Amsterdam) 2:1387-1404.
35. Mombaerts, P., A. R. Clarke, M. A. Rudnicki, J. Iacomini, S. Itohara, J. J. Lafaille, L. Wang, Y. Ichikawa, R. Jaenisch, M. L. Hooper, et al. 1992. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature 360:225-231.
36. Reference deleted.
37. Myung, K., A. Datta, C. Chen, and R. D. Kolodner. 2001. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet. 27:113-116.
38. Nacht, M., A. Strasser, Y. R. Chan, A. W. Harris, M. Schlissel, R. T. Bronson, and T. Jacks. 1996. Mutations in the p53 and SCID genes cooperate in tumorigenesis. Genes Dev. 10:2055-2066.
39. Newton, K., C. Kurts, A. W. Harris, and A. Strasser. 2001. Effects of a dominant interfering mutant of FADD on signal transduction in activated T cells. Curr. Biol. 11:273-276.
40. Penit, C., B. Lucas, and F. Vasseur. 1995. Cell expansion and growth arrest phases during the transition from precursor (CD4-8-) to immature (CD4+8+) thymocytes in normal and genetically modified mice. J. Immunol. 154:5103-5113.
41. Petrini, J. H., J. W. Donovan, C. Dimare, and D. T. Weaver. 1994. Normal V(D)J coding junction formation in DNA ligase I deficiency syndromes. J. Immunol. 152:176-183.
42. Reizis, B., and P. Leder. 2001. The upstream enhancer is necessary and sufficient for the expression of the pre-T cell receptor alpha gene in immature T lymphocytes. J. Exp. Med. 194:979-990.
43. Saint-Ruf, C., K. Ungewiss, M. Groettrup, L. Bruno, H. J. Fehling, and H. von Boehmer. 1994. Analysis and expression of a cloned pre-T cell receptor gene. Science 266:1208-1212.
44. Sentman, C. L., J. R. Shutter, D. Hockenbery, O. Kanagawa, and S. J. Korsmeyer. 1991. bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 67:879-888.
45. Shinkai, Y., G. Rathbun, K. P. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A. M. Stall, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:855-867.
46. Taghon, T., M. A. Yui, R. Pant, R. A. Diamond, and E. V. Rothenberg. 2006. Developmental and molecular characterization of emerging beta- and gammadelta-selected pre-T cells in the adult mouse thymus. Immunity 24:53-64.
47. Taniguchi, N., M. Mukai, T. Nagaoki, T. Miyawaki, N. Moriya, H. Takahashi, and N. Kondo. 1982. Impaired B-cell differentiation and T-cell regulatory function in four patients with Bloom's syndrome. Clin. Immunol. Immunopathol. 22:247-258.
48. Turley, H., L. Wu, M. Canamero, K. C. Gatter, and I. D. Hickson. 2001. The distribution and expression of the Bloom's syndrome gene product in normal and neoplastic human cells. Br. J. Cancer 85:261-265.
49. van Gent, D. C., J. H. Hoeijmakers, and R. Kanaar. 2001. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2:196-206.
50. Van Kerckhove, C. W., J. L. Ceuppens, M. Vanderschueren-Lodeweyckx, E. Eggermont, S. Vertessen, and E. A. Stevens. 1988. Bloom's syndrome. Clinical features and immunologic abnormalities of four patients. Am. J. Dis. Child. 142:1089-1093.
51. von Boehmer, H., and H. J. Fehling. 1997. Structure and function of the pre-T cell receptor. Annu. Rev. Immunol. 15:433-452.
52. Wang, X. W., A. Tseng, N. A. Ellis, E. A. Spillare, S. P. Linke, A. I. Robles, H. Seker, Q. Yang, P. Hu, S. Beresten, N. A. Bemmels, S. Garfield, and C. C. Harris. 2001. Functional interaction of p53 and BLM DNA helicase in apoptosis. J. Biol. Chem. 276:32948-32955.
53. Wang, Y., D. Cortez, P. Yazdi, N. Neff, S. J. Elledge, and J. Qin. 2000. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14:927-939.
54. Wolfer, A., A. Wilson, M. Nemir, H. R. MacDonald, and F. Radtke. 2002. Inactivation of notch1 impairs VDJbeta rearrangement and allows pre-TCR-independent survival of early alpha beta lineage thymocytes. Immunity 16:869-879.