Essential and perilous: V(D)J recombination and DNA damage checkpoints in lymphocyte precursors

Seminars in Immunology

Volumn 9, Issue 3, 1997, Pages 199-206

  Danska, Jayne S ^a   Guidos, Cynthia J ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Ataxia telangiectasia; DNA damage checkpoint; DNA dependent protein kinase; V(D)J recombination

Indexed keywords

APOPTOSIS; ARTICLE; ATAXIA TELANGIECTASIA; CELL CYCLE; DNA DAMAGE; DNA REPAIR; EUKARYOTIC CELL; IMMUNOGLOBULIN VARIABLE REGION; PROLYMPHOCYTE; SACCHAROMYCES CEREVISIAE;

EID: 0031170827     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1006/smim.1997.0072     Document Type: Article

References (81)

1. 1. Lewis SM (1994) The mechanism of V(D)J joining: lessons from molecular, immunological, and comparative analyses. Adv Immunol 56:27-150
2. 2. Robey E, Fowlkes BJ (1994) Selective events in T cell development. Annu Rev Immunol 12:675-705
3. 3. Rajewsky K (1996) Clonal selection and learning in the antibody system. Nature 381:751-758
4. 4. Hartwell L (1992) Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 71:543-546
5. 5. Paulovitch AG, Toczyski DP, Hartwell LH (1997) When checkpoints fail. Cell 88:315-321
6. 6. Rabbitts TH (1994) Chromosomal translocations in human cancer. Nature 372:143-149
7. 7. Elledge SJ (1996) Cell cycle checkpoints: Preventing an identity crisis. Science 274:1664-1672
8. 8. Levine AJ (1997) p53, the cellular gatekeeper for growth and division. Cell 88:323-332
9. 9. Ko LJ, Prives C (1996) p53: puzzle and paradigm. Genes Dev 10:1054-1072
10. 10. Harvey M, Vogel H, Morris D, Bradley A, Bernstein A, Donehower LA (1995) A mutant p53 transgene accelerates tumour development in heterozygous but not nullizygous p53-deficient mice. Nature Genet 9:305-311
11. 11. Jacks T, Remington L, Williams BO, Schmidt EM, Halachmi S, Bronson RT, Weinberg RA (1994) Tumor spectrum analysis in p53-mutant mice. Curr Biol 4:1-7
12. 12. Zakian VA (1995) ATM-related genes: What do they tell us about the functions of the human gene? Cell 82:685-687
13. 13. Keith CT, Schreiber SL (1995) PIK-related kinases: DNA repair, recombination, and cell cycle checkpoints. Science 270:50-51
14. 14. Jeggo PA, Taccioloi GE, Jackson SP (1995) Menage a trois: double strand break repair, V(D)J recombination and DNA-PK BioEssays 17:949-957
15. 15. Lees-Miller SP (1996) The DNA-dependent protein kinase, DNA-PK 10 years and no end in sight. Biochem Cell Biol 74:503-512
16. 16. Keegan KS, Holtzman DA, Plug AW, Christenson ER, Brainerd EE, Flaggs G, Bentley NJ, Taylor EM, Meyn MS, Moss SB, Catt AM, Ashley T, Hoekstra MF (1996) The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev 10:2423-2437
17. 17. Cantley LC, Auger KR, Carpenter C, Duckworth B, Graziani A, Kapeller R, Soltoff S (1991) Oncogenes and signal transduction. Cell 64:281-302
18. 18. Hunter T (1997) Oncoprotein networks. Cell 88:333-346
19. 19. Chan DW, Lees-Miller SP (1996) The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. J Biol Chem 271:8936-8941
20. 20. Casciola-Rosen L, Nicholson DW, Chong T, Rowan KR, Thornberry NA, Miller DK, Rosen A (1996) Apopain/ CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death. J Exp Med 183:1957-1964
21. 21. Han Z, Malik N, Carter T, Reeves WH, Wyche JH, Hendrickson EA (1996) DNA-dependent protein kinase is a target for a CPP32-like apoptotic protease. J Biol Chem 271:25035-25040
22. 22. Song Q, Lees-Miller S, Kumar S, Zhang N, Chan DW, Smith GCM, Jackson SP, Alnemri ES, Litwack G, Lavin MF (1996) DNA-dependent protein kinase catalytic subunit: A target for an ICE-like protease in apoptosis. EMBO J 15:3238-3246
23. 23. Hartley KO, Gell D, Smith GCM, Zhang H, Divecha N, Connelly MA, Admon A, Lees-Miller SP, Anderson CW, Jackson SP (1995) DNA-dependent protein kinase catalytic subunit: A relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82:849-856
24. 24. Bosma GC, Custer RP, Bosma MJ (1983) A severe combined immunodeficiency mutation in the mouse. Nature 301:527-530
25. 25. Fulop GM, Phillips RA (1990) The scid mutation in mice causes a general defect in DNA repair. Nature 347:479482
26. 26. Biedermann KA, Sun J, Giaccia AJ, Tosto LM, Brown JM (1991) Scid mutation in mice confers hypersensitivity to ionizing radiation and a deficiency in DNA double-strand break repair. Proc Natl Acad Sci USA 88:1394-1397
27. 27. Hendrickson EA, Qin X-Q, Bump EA, Schatz DG, Oettinger M, Weaver DT (1991) A link between double-strand break-related repair and V(D)J recombination: The scid mutation proc Natl Acad Sci USA 88:40614065
28. 28. Chang C, Biedermann KA, Mezzina M, Brown JM (1993) Characterization of the DNA double strand break repair defect in scid mice. Cancer Res 53:1244-1248
29. 29. Roth DB, Menetski JP, Nakajima P, Bosma M, Gellert M (1992) V(D)J recombination: Broken DNA molecules with covalently sealed (hairpin) coding ends in scid mouse thymocytes. Cell 70:983-991
30. 30. Roth DB, Nakajima PB, Menetski J, Bosma M, Gellert M (1992) V(D)J recombination in mouse thymocytes: double-strand breaks near T cell receptor δ rearrangement signals. Cell 69:41-53
31. 31. Zhu C, Roth DB (1995) Characterization of coding ends in thymocytes of scid mice: Implications for the mechanism of V(D)J recombination. Immunity 2:101-112
32. 32. Kirchgessner CU, Patil CK, Evans JW, Cuomo CA, Fried LM, Carter T, Oettinger MA, Brown JM (1995) DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 267:1178-1182
33. 33. Peterson SR, Kurimasa A, Oshimura M, Dynan WS, Bradbury EM, Chen DJ (1995) Loss of catalytic subunit of the DNA-dependent protein kinase in DNA double-strand break repair mutant mammalian cells. Proc Natl Acad Sci USA 92:3171-3174
34. 34. Blunt T, Finnie NJ, Taccioli GE, Smith GCM, Demengeot J, Gottlieb TM, Mizuta R, Varghese AJ, Alt FW, Jeggo PA, Jackson SP (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
35. 35. Boubnov NV, Weaver DT (1995) scid cells are deficient in Ku and replication protein A phosphorylation by the DNA-dependent protein kinase. Mol Cell Biol 15:5700-5706
36. 36. Pennycook JL, Chang Y, Celler J, Phillips RA, Wu GE (1993) High frequency of normal DJH joints in B cell progenitors in severe combined immune deficiency mice. J Exp Med 178:1007-1016
37. 37. Bosma MJ, Carroll AM (1991) The SCID mouse mutant: Definition, characterization, and potential uses. Annu Rev Immunol 9:323-350
38. 38. Danska JS, Holland DP, Mariathasan S, Williams KW, Guidos CJ (1996) Biochemical and genetic defects in the DNA-dependent protein kinase in murine scid lymphocytes. Mol Cell Biol 16:5507-5517
39. 39. Blunt T, Gell D, Fox M, Taccioli GE, Lehman AR, Jackson SP, Jeggo PA (1996) Identification of a nonsense mutation in the carboxy-terminal region of the DNA-dependent protein kinase catalytic subunit in the scid mouse. Proc Natl Acad Sci USA 93:10285-10290
40. 40. Hunter T (1995) When is a lipid kinase not a lipid kinase? When it is a protein kinase. Cell 83:1-4
41. 41. Lewis SM (1994) P-nucleotide insertions and the resolution of hairpin DNA structures in mammalian cells. Proc Natl Acad Sci USA 91:1332-1336
42. 42. Ramsden DA, Gellert M (1995) Formation and resolution of double-strand break intermediates in V(D)J rearrangement. Genes Dev 9:2409-2420
43. 43. Livak F, Schatz DG (1996) T cell receptor α locus V(D)J recombination by-products are abundant in thymocytes and mature T cells. Mol Cell Biol 16:609-618
44. 44. Nussenzweig A, Chen C, Costa Soares V, Sanchez M, Sokol K, Nussenzweig MC, Li GC (1996) Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382:551-555
45. 45. Zhu C, Bogue MA, Lim D, Hasty P, Roth DB (1996) Ku86-deficient mice exhibit severe combined immune deficiency and defective processing of V(D)J recombination intermediates. Cell 86:379-389
46. 46. Shakibai N, Kumar V, Eisenberg S (1997) The Ku-like protein from Saccharomyces cerevisiae is required in vitro for the assembly of a stable multiprotein complex at a eukaryotic origin of replication. Proc Natl Acad Sci (USA)
47. 47. Milne GT, Jin S, Shannon KB, Weaver DT (1996) Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol Cell Biol 16:41894198
48. 48. Siede W, Friedl AA, Dianova I, Eckarddt-Schupp F, Friedberg EC (1996) The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics 142:91-102
49. 49. Boulton SJ, Jackson SP (1996) Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand repair and serves as a barrier to error-prone DNA repair pathways. EMBO J 15:5093-5103
50. 50. Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y, Vanagaite L, Tagle DA, Smith S, Uziel T, Stez S, Ashkenazi M, Peckaer I, Frydman M, Harnik R, Patanjali SR, Simmons A, Clines GA, Sartiel A, Gatti RA, Chessa L, Sanal O, Lavin MF, Jaspers NG, Taylor MR, Arlett CF, Miki T, Weissman SM, Lovett M, Collins FS, Shiloh Y (1995) A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268:1749-1753
51. 51. Savitsky K, Sfez S, Tagle DA, Ziv Y, Sartiel A, Collins FS, Shiloh Y, Rotman G (1995) The complete sequence of the coding region of the ATM gene reveals similarity to cell cycle regulators in different species. Hum Molec Genet 4:2025-2032
52. 52. Xu Y, Baltimore D (1996) Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev 10:2401-2410
53. 53. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D (1996) Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects and thymic lymphoma. Genes Dev 10:2411-2422
54. 54. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, Shiloh Y, Crawley JN, Ried T, Tagle D, Wynshaw-Boris A (1996) ATM-deficient mice: a paradigm of Ataxia Telangiectasia. Cell 86:159-171
55. 55. Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou E, Campos-Torres J, Leder P (1996) Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc Natl Acad Sci USA 93:13084-13089
56. 56. Kastan MB, Zhan Q, El-Deiry W, Carrier F, Jacks T, Walsh W, Plunkett B, Vogelstein B, Fornace JA (1992) A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cells 71:587-597
57. 57. Meyn MS (1995) Ataxia-telangiectasia and cellular responses to DNA damage. Cancer Res 55:5991-6001
58. 58. Jorgenson TJ, Shiloh Y (1996) The ATM gene and the radiobiology of ataxia-telangiectasia. Int J Radiat Biol 69:527-537
59. 59. Brown KD, Ziv Y, Sadanandan SN, Chessa L, Collins FS, Shiloh Y, Tagle DA (1997) The ataxia-telangiectasia gene product, a constitutively expressed nuclear protein that is not up-regulated following genome damage. Proc Natl Acad Sci USA 94:1840-1845
60. 60. Donehower L, Harvey M, Slagle B, McArthur M, Montgomery Jr C, Butel J, Bradley A (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221
61. 61. Porter SE, Greenwell PW, Ritchie KB, Petes TD (1996) The DNA-binding protein Hdf1p (a putative Ku homologue) is required for maintaining normal telomere length in Saccharomyces cerevisiae. Nucleic Acids Res 24:582-585
62. 62. Greenwell PW, Kronmal SL, Porter SE, Gassenhuber J, Obermaier B, Petes TD (1995) TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell 82:823-829
63. 63. Morrow DM, Tagle DA, Shiloh Y, Collins FS, Mieter P (1995) TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell 82:831
64. 64. Telatar M, Wang Z, Udar N, Liang T, Bernatowska-Matuszkiewicz E, Lavin M, Shiloh Y, Concannon P, Good RA, Gatti RA (1996) Ataxia-telangiectasia: mutations in ATM cDNA detected by protein-truncation screening. Am J Hum Genet 59:40-44
65. 65. McConville CM, Stankovic T, Byrd PJ, McGuire GM, Yao QY, Lennox GG, Taylor AMR (1996) Mutations associated with variant phenotypes in ataxia-telangiectasia. Am J Hum Genet 59:320-330
66. 66. Gilad S, Khosravi R, Shkedy D, Uziel T, Ziv Y, Savitsky K, Rotman G, Smith S, Chessa L, Jorgensen TJ, Harnik R, Frydman M, Sanal O, Portnoi S, Goldwicz Z, Jaspers NGJ, Gatti RA, Lenoir G, Lavin MF, Tatsumi K, Wegner RD, Shiloh Y, Bar-Shira A (1996) Predominance of null mutations in ataxia-telangiectasia. Hum Mol Genet 5:433439
67. 67. Lakin ND, Weber P, Stankovic T, Rottinghaus ST, Taylor AMR, Jackson SP (1996) Analysis of the ATM protein in wild-type and ataxia teelangiectasia cells. Oncogene 13:2707-2716
68. 68. Desiderio S, Lin WC, Li Z (1996) The cell cycle and V(D)J recombination. Curr Top Micro Immunol 217:45-59
69. 69. Zhong L, Dordai DI, Lee J, Desiderio S (1996) A conserved degradation signal regulates RAG-2 accumulation during cell division and links V(D)J recombination to the cell cycle. Immunity 5:575-589
70. 70. Schlissel M, Constantinescu A, Morrow T, Baxter M, 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
71. 71. Penit C, Lucas B, Vasseur F (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
72. 72. Hoffman ES, Passoni L, Crompton T, Leu TM, Schatz DG, Koff A, Owen MJ, Hayday AC (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
73. 73. Giaccia A, Weinstein R, Hu J, Stamato TD (1985) Cell cycle-dependent repair of double-strand DNA breaks in a gamma-ray-sensitive Chinese hamster cell. Som Cell Mol Genet 11:485491
74. 74. Li Z, Otevrel T, Gao Y, Cheng HL, Seed B, Stamato TD, Taccioli GE, Alt FW (1995) The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination. Cell 83:1079-1089
75. 75. Huang L-C, Clarkin KC, Wahl GM (1996) Sensitivity and selectivity of the DNA damage sensor responsible for activating p53-dependent G1 arrest. Proc Natl Acad Sci USA 93:48274832
76. 76. Lee SE, Mitchell RA, Cheng A, Hendrickson EA (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
77. 77. Nelson WG, Kastan MB (1994) DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol Cell Biol 14:1815-1823
78. 78. Guidos CJ, Williams C, Grandal I, Knowles G, Huang MT, Danska JS (1996) V(D)J recombination activates a p53-dependent DNA damage checkpoint in scid lymphocyte precursors. Genes Dev 10:2038-2054
79. 79. Nacht M, Strasser A, Chan YR, Harris AW, Schlissel M, Bronson RT, Jacks T (1996) Mutations in the p53 and SCID genes cooperate in tumorigenesis. Genes Dev 10:2055-2066
80. 80. Fried LM, Koumenis C, Peterson SR, Green SL, van Zijl P, Allalunis-Turner J, Chen DJ, Fishel R, Giacca AJ, Brown JM, Kirchgessner CU (1996) The DNA damage response in DNA-dependent protein kinase-deficient SCID mouse cells: Replication protein A hyperphosphorylation and p53 induction. Proc Natl Acad Sci (USA) 93:13825-13830
81. 81. Huang LC, Clarkin KC, Wahl GM (1996) p53-dependent cell cycle arrests are preserved in DNA-activated protein kinase-deficient mouse fibroblasts. Cancer Res 56:2940-2944