Growth retardation and leaky SCID phenotype of Ku70-deficient mice

Immunity

Volumn 7, Issue 5, 1997, Pages 653-665

  Gu, Yansong ^a   Seidl, Katherine J ^a   Rathbun, Gary A ^a   Zhu, Chengming ^b   Manis, John P ^a   Van Der Stoep, Nienke ^a   Davidson, Laurie ^a   Cheng, Hwei Ling ^a   Sekiguchi, JoAnn M ^a   Frank, Karen ^a   Stanhope Baker, Patricia ^c   Schlissel, Mark S ^c   Roth, David B ^b   Alt, Frederick W ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; DNA BINDING PROTEIN; DOUBLE STRANDED DNA; PROTEIN KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL CYCLE; COMBINED IMMUNODEFICIENCY; CONTROLLED STUDY; DNA STRAND BREAKAGE; GENE MUTATION; GENE REARRANGEMENT; GROWTH RETARDATION; IMMUNOGLOBULIN VARIABLE REGION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; T LYMPHOCYTE;

EID: 0031433517     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80386-6     Document Type: Article

References (73)

1. Agrawal, A., and Schatz, D.G. (1997). RAG1 and RAG2 form a stable postcleavage synaptic complex with DNA-containing signal ends in V(D)J recombination. Cell 89, 43-53.
2. Blackwell, T.K., Malynn, B.A., Pollock, R.R., Ferrier, P., Covey, L.R., Fulop, G.M., Phillips, R.A., Yancopoulos, G.D., and Alt, F.W. (1989). Isolation of scid pre-B cells that rearrange kappa light chain genes: formation of normal signal and abnormal coding joins. EMBO J. 8, 735-742.
3. Blunt, T., Finnie, N.J., Taccioli, G.E., Smith, G.C.M., Demengeot, J., Gottlieb, T.M., Mizuta, R., Varghese, A.J., Alt, F.W., Jeggo, P.A., et al. (1995). Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80, 813-823.
4. Blunt, T., Gell, D., Fox, M., Taccioli, G.E., Lehmann, A.R., Jackson, S.P., and Jeggo, P.A. (1996). Identification of a nonsense mutation in the carboxyl-terminal region of DNA-dependent protein kinase catalytic subunit in the scid mouse. Proc. Natl. Acad. Sci. USA 93, 10285-10290.
5. Bogue, M.A., Wang, C., Zhu, C., and Roth, D.B. (1997). V(D)J recombination in Ku86-deficient mice: distinct effects on coding, signal, and hybrid joint formation. Immunity 7, 37-47.
6. Bosma, G.C., Custer, R.P., and Bosma, M.J. (1983). A severe combined immunodeficiency mutation in the mouse. Nature 301, 527-530.
7. Boubnov, N.V., Hall, K.T., Will, Z., Lee, S.E., He, D.M., Benjamin, D.M., Pilaski, C.R., Band, H., Reeves, W., Hendrickson, E.A., and Weaver, D.T. (1995). Complementation of the ionizing radiation sensitivity, DNA end binding, and V(D)J recombination defects of double-strand break repair mutants by the p86 Ku antigen. Proc. Natl. Acad. Sci. USA 92, 890-894.
8. Boulton, S.J, and Jackson, S.P. (1996a). Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res. 24, 4639-4648.
9. Boulton, S.J., and Jackson, S.P. (1996b). Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J. 15, 5093-5103.
10. +) lymphocytes in Scid mice. J. Immunol. 143, 1087-1093.
11. Chang, Y., Bosma, G.C., and Bosma, M.J. (1995). Development of B cells in scid mice with immunoglobulin transgenes: implications for the control of V(D)J recombination. Immunity 2, 607-616.
12. Chen, J., and Alt, F.W. (1994). RAG-2-deficient blastocyst complementation. In Transgenesis and Targeted Mutagenesis in Immunology, H. Bluethmann, and P.S. Ohashi, eds. (San Diego, California: Academic Press), pp. 35-49.
13. Critchlow, S.E., Bowater, R.P., and Jackson, S.P. (1997). Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Curr. Biol. 7, 588-598.
14. Custer, R.P., Bosma, G.C., and Bosma, M.J. (1985). Severe combined immunodeficiency (SCID) in the mouse: pathology, reconstitution, neoplasms. Am. J. Pathol. 120, 464-477.
15. Danska, J.S., Holland, D.P., Mariathasan, S., Williams, K.M., and Guidos, C.J. (1996). Biochemical and genetic defects in the DNA-dependent protein kinase in murine scid lymphocytes. Mol. Cell Biol. 16, 5507-5517.
16. Difilippantonio, M.J., McMahan, C.J., Eastman, Q.M., Spanopoulou, E., and Schatz, D.G. (1996). RAG1 mediates signal sequence recognition and recruitment of RAG2 in V(D)J recombination. Cell 87, 253-262.
17. Errami, A., Smider, V., Rathmell, W.K., He, D.M., Hendrickson, E.A., Zdzienicka, M.Z., and Chu, G. (1996). Ku86 defines the genetic defect and restores X-ray resistance and V(D)J recombination to complementation groups hamster cell mutants. Mol. Cell Biol. 16, 1519-1526.
18. Ferrier, P., Covey, L.R., Li, S.C., Suh, H., Malynn, B.A., Blackwell, T.K., Morrow, M.A., and Alt, F.W. (1990). Normal recombination substrate VH to DJH rearrangements in pre-B cell lines from scid mice. J. Exp. Med. 171, 1909-1918.
19. Getts, R.C., and Stamato, T.D. (1994). Absence of a Ku-like DNA end binding activity in the xrs double-strand DNA repair-deficient mutant. J. Biol. Chem. 269, 15981-15984.
20. 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.
21. Gottlieb, T.M., and Jackson, S.P. (1993). The DNA-dependent protein kinase: requirements for DNA ens and association with Ku antigen. Cell 72, 131-142.
22. Grawunder, U., Wilm, M., Wu, X., Kulesza, P., Wilson, T.E., Mann, M., and Lieber, M.R. (1997). Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature 388, 492-495.
23. Gu, Y., Jin, S., Gao, Y., Weaver, D.T., and Alt, F.W. (1997). Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination. Proc. Natl. Acad. Sci. USA 94, 8076-8081.
24. Han, J.O., Steen, S.B., and Roth, D.B. (1997). Ku86 is not required for protection of signal ends or for formation of nonstandard V(D)J recombination products. Mol. Cell Biol. 17, 2226-2234.
25. Hendrickson, E.A., Schlissel, M.S., and Weaver, D.T. (1990). Wild-type V(D)J recombination in scid pre-B cells. Mol. Cell Biol. 10, 5397-5407.
26. Hesse, J.E., Lieber, M.R., Gellert, M., and Mizuuchi, K. (1987). Extra-chromosomal DNA substrates in pre-B cells undergo inversion or deletion at immunoglobulin V-(D)-J joining signals. Cell 49, 775-783.
27. Hiom, K., and Gellert, M. (1997). A stable RAG1-RAG2-DNA complex that is active in V(D)J cleavage. Cell 88, 65-72.
28. Hogan, B., Beddington, R., Costantini, F., and Lacy, E. (1994). Manipulating the Mouse Embryo: A Laboratory Manual, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
29. Jeggo, P.A., Taccioli, G.E., and Jackson, S.P. (1995). Menage a trois: double strand break repair, V(D)J recombination and DNA-PK. Bioessays 17, 949-957.
30. Jin, S., Inoue, S., and Weaver, D.T. (1997). Functions of the DNA dependent protein kinase: checkpoint controls and cancer. Cancer Surveys (Imperial Cancer Research Fund) 29, 221-261.
31. Kharbanda, S., Pandey, P., Jin, S., Inoue, S., Bharti, A., Yuan, Z.M., Weichselbaum, R., Weaver, D., and Kufe, D. (1997). Functional interaction between DNA-PK and c-Abl in response to DNA damage. Nature 386, 732-735.
32. Kirchgessner, C.U., Patil, C.K., Evans, J.W., Cuomo, C.A., Fried, L.M., Carter, T., Oettinger, M.A., and Brown, J.M. (1995). DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 267, 1178-1183.
33. 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.
34. Lee, S.E., Mitchell, R.A., Cheng, A., and Hendrickson, E.A. (1997). Evidence for DNA-PK-dependent and -independent DNA double-strand break repair pathways in mammalian cells as a function of the cell cycle. Mol. Cell Biol. 17, 1425-1433.
35. Lees-Miller, S.P., Godbout, R., Chan, D.W., Weinfeld, M., Day, R.S. III, Barron, G.M., and Allalunis-Turner, J. (1995). Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science 267, 1183-1185.
36. Li, Z., Otevrel, T., Gao, Y., Cheng, H-L., Seed, B., Stamato, T., Taccioli, G.E., and Alt, F.W. (1995). The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination. Cell 83, 1079-1089.
37. Lieber, M.R., Hesse, J.E., Lewis, S., Bosma, G.C., Rosenberg, N., Mizuuchi, K., Bosma, M.J., and Gellert, M. (1988). The defect in murine severe combined immune deficiency: joining of signal sequences but not coding segments in V(D)J recombination. Cell 55, 7-16.
38. Livak, F., and Schatz, D.G. (1996). T-cell receptor alpha locus V(D)J recombination by-products are abundant in thymocytes and mature T cells. Mol. Cell Biol. 16, 609-618.
39. Malynn, B.A., Blackwell, T.K., Fulop, G.M., Rathbun, G.A., Furley, A.J., Ferrier, P., Heinke, L.B., Phillips, R.A., Yancopoulos, G.D., and Alt, F.W. (1988). The scid defect affects the final step of the immunoglobulin VDJ recombinase mechanism. Cell 54, 453-460.
40. McBlane, J.F., van Gent, D.C., Ramsden, D.A., Romeo, C., Cuomo, C.A., Gellert, M., and Oettinger, M.A. (1995). Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell 83, 387-395.
41. Milne, G.T., Jin, S., Shannon, K.B., and Weaver, D.T. (1996). Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 4189-4198.
42. Mizuta, R., Taccioli, G.E., and Alt, F.W. (1996).The V(D)J recombination defect in the xrs-6 cell line results from a point mutation in the Ku80 gene. Int. Immunol. 8, 1467-1471.
43. Nussenzweig, A., Chen, C., da Costa Soares, V., Sanchez, M., Sokol, K., Nussenzweig, M.C., and Li, G.C. (1996). Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382, 551-555.
44. Oettinger, M.A., Schatz, D.G., Gorka, C., and Baltimore, D. (1990). RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 24, 1517-1522.
45. Ouyang, H., Nussenzweig, A., Kurimasa, A., Soares, V.C., Li, X., Cordon-Cardo, C., Li, W., Cheong, N., Nussenzweig, M., Iliakis, G., et al. (1997). Ku70 is required for DNA repair but not for T cell antigen receptor gene recombination in vivo. J. Exp. Med. 186, 921-929.
46. Pergola, F., Zdzienicka, M.Z., and Lieber, M.R. (1993). V(D)J recombination in mammalian cell mutants defective in DNA double-strand break repair. Mol. Cell. Biol. 13, 3464-3471.
47. Rathmell, W.K., and Chu, G. (1994). A DNA end-binding factor involved in double-strand break repair and V(D)J recombination. Mol. Cell. Biol. 14, 4741-4748.
48. Rathmell, W.K., Kaufmann, W.K., Hurt, J.C., Byrd, L.L., and Chu, G. (1997). DNA-dependent protein kinase is not required for accumulation of p53 or cell cycle arrest after DNA damage. Cancer Res. 57, 68-74.
49. Roth, D.B., and Wilson, J.H. (1986). Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction. Mol. Cell Biol. 6, 4295-4304.
50. Roth, D.B., Zhu, C., and Gellert, M. (1993). Characterization of broken DNA moleculesassociated with V(D)J recombination. Proc. Natl. Acad. Sci. USA 90, 10788-10792.
51. Ruley, H.E., and Fried, M. (1983). Clustered illegitimate recombination events in mammalian cells involving very short sequence homologies. Nature 304, 181-184.
52. Satoh, M., Wang, J., and Reeves, W.H. (1995). Role of free p70 (Ku) subunit in posttranslational stabilization of newly synthesized p80 during DNA-dependent protein kinase assembly. Eur. J. Cell Biol. 66, 127-135.
53. Schatz, D.G., Oettinger, M.A., and Baltimore, D. (1989). The V(D)J recombination activating gene, RAG-1. Cell 59, 1035-1048.
54. Schlissel, M.S., Constantinescu, A., Morrow, T., Baxter, M., and Peng, A. (1993). Double-strand signal sequence breaks in V(D)J recombination are blunt, 5′-phosphorylated, RAG-dependent, and cell cycle regulated. Genes Dev. 7, 2520-2532.
55. Seidl, K.J., MacKenzie, J.D., Wang, D., Kantor, A.B., Kabat, E.A., Herzenberg, L.A., and Herzenberg, L.A. (1997). Frequent occurrence of identical heavy and light chain Ig rearrangements. Int. Immunol. 9, 689-702.
56. Siede, W., Friedl, A.A., Dianova, I., Eckardt-Schupp, F., and Friedberg, E.C. (1996). The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics 14, 91-102.
57. Singleton, B.K., Priestley, A., Steingrimsdottir, H., Gell, D., Blunt, T., Jackson, S.P., Lehmann, A.R., and Jeggo, P.A. (1997). Molecular and biochemical characterization of xrs mutants defective in Ku80. Mol. Cell Biol. 17, 1264-1273.
58. Sipley, J.D., Menninger, J.C., Hartley, K.O., Ward, D.C., Jackson, S.P., and Anderson, C.W. (1995). Gene for the catalytic subunit of the human DNA-activated protein kinase maps to the site of the XRCC7 gene on chromosome 8. Proc. Natl. Acad. Sci. USA 92, 7515-7519.
59. Smider, V., Rathmell, W.K., Lieber, M.R., and Chu, G. (1994). Restoration of X-ray resistance and V(D)J recombination in mutant cells by Ku cDNA. Science 266, 288-291.
60. Smith, J.R., and Pereira-Smith, O.M. (1996). Replicative senescence: implications for in vivo aging and tumor suppression. Science 273, 63-67.
61. Sonoda, E., Pewzner-Jung, Y., Schwers, S., Taki, S., Jung, S., Eilat, D., and Rajewsky, K. (1997). B cell development under the condition of allelic inclusion. Immunity 6, 225-233.
62. Taccioli, G.E., Rathbun, G., Oltz, E., Stamato, T., Jeggo, P.A., and Alt, F.W. (1993). Impairment of V(D)J recombination in double-strand break repair mutants. Science 260, 207-210.
63. Taccioli, G.E., Cheng, H-L., Varghese, A.J., Whitmore, G., and Alt, F.W. (1994a). A DNA repair defect in Chinese hamster overy cells affects V(D)J recombination similar to the murine scid mutation. J. Biol. Chem. 269, 1-4.
64. Taccioli, G.E., Gottlieb, T.M., Blunt, T., Priestley, A., Demengeot, J., Mizuta, R., Lehmann, A.R., Alt, F.W., Jackson, S.P., and Jeggo, P.A. (1994b). Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265, 1442-1445.
65. Teo, S.-H., and Jackson, S.P. (1997). Identification of Saccharomyces cerevisiae DNA ligase IV: involvement in DNA double-strand break repair. EMBO J. 16, 4788-4795.
66. Tonegawa, S. (1983). Somatic generation of antibody diversity. Nature 302, 575-581.
67. van Gent, D.C., McBlane, J.F., Ramsden, D.A., Sadofsky, M.J., Hesse, J.E., and Gellert, M. (1995). Initiation of V(D)J recombination in a cell fee system. Cell 81, 925-934.
68. Wiler, R., Leber, R., Moore, B.B., VanDyk, L.F., Perryman, L.E., and Meek, K. (1995). Equine severe combined immunodeficiency: a defect in V(D)J recombination and DNA-dependent protein kinase activity. Proc. Natl. Acad. Sci. USA 92, 11485-11489.
69. Willerford, D.M., Swat, W., and Alt, F.W (1996). Developmental regulation of V(D)J recombination and lymphocyte differentiation. Curr. Opin. Genet. Dev. 6, 603-609.
70. Wilson, T.E., Grawunder, U., and Lieber, M.R. (1997). Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 388, 495-498.
71. Young, F., Ardman, B., Shinkai, Y., Lansford, R., Blackwell, T.K., Mendelsohn, M., Rolink, A., Melchers, F., and Alt, F.W. (1994). Influence of immunoglobulin heavy- and light-chain expression on B-cell differentiation. Genes Dev. 8, 1043-1057.
72. Zhu, C., and Roth, D.B. (1995). Characterization of coding ends in thymocytes of scid mice: implications for the mechanism of V(D)J recombination. Immunity 2, 101-112.
73. Zhu, C., Bogue, M.A., Lim, D-S., Hasty, P., and Roth, D.B. (1996). Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 86, 379-389.