DNA-PK phosphorylates histone H2AX during apoptotic DNA fragmentation in mammalian cells

DNA Repair

Volumn 5, Issue 5, 2006, Pages 575-590

  Mukherjee, Bipasha ^a   Kessinger, Chase ^a   Kobayashi, Junya ^b   Chen, Benjamin P C ^a   Chen, David J ^a   Chatterjee, Aloke ^c   Burma, Sandeep ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Apoptosis; ATM; DNA fragmentation; DNA PK; H2AX; Phosphorylation; Staurosporine

Indexed keywords

ATM PROTEIN; DNA DEPENDENT PROTEIN KINASE; DNA FRAGMENT; HISTONE H2AX; SERINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; CELL CULTURE; CELL NUCLEUS; CHO CELL; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INACTIVATION; GENETIC LINKAGE; HUMAN; HUMAN CELL; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

ANIMALS; APOPTOSIS; CELL CYCLE PROTEINS; CELL LINE; CHO CELLS; CRICETINAE; DNA FRAGMENTATION; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HISTONES; HUMANS; MICE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; STAUROSPORINE; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA; CRICETULUS GRISEUS; MAMMALIA; MURINAE;

EID: 33646090171     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.01.011     Document Type: Article

References (75)

1. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
2. Strasser A., O'Connor L., and Dixit V.M. Apoptosis signaling. Annu. Rev. Biochem. 69 (2000) 217-245
3. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
4. Jaattela M. Multiple cell death pathways as regulators of tumour initiation and progression. Oncogene 23 (2004) 2746-2756
5. Martin S.J. Destabilizing influences in apoptosis: sowing the seeds of IAP destruction. Cell 109 (2002) 793-796
6. Ashkenazi A., and Dixit V.M. Death receptors: signaling and modulation. Science 281 (1998) 1305-1308
7. Green D.R., and Reed J.C. Mitochondria and apoptosis. Science 281 (1998) 1309-1312
8. Johnstone R.W., Ruefli A.A., and Lowe S.W. Apoptosis: a link between cancer genetics and chemotherapy. Cell 108 (2002) 153-164
9. Shao R.G., Shimizu T., and Pommier Y. 7-Hydroxystaurosporine (UCN-01) induces apoptosis in human colon carcinoma and leukemia cells independently of p53. Exp. Cell. Res. 234 (1997) 388-397
10. Bertrand R., Solary E., O'Connor P., Kohn K.W., and Pommier Y. Induction of a common pathway of apoptosis by staurosporine. Exp. Cell. Res. 211 (1994) 314-321
11. Senderowicz A.M. Novel small molecule cyclin-dependent kinases modulators in human clinical trials. Cancer Biol. Ther. 2 (2003) S84-S95
12. Nagata S. DNA degradation in development and programmed cell death. Annu. Rev. Immunol. 23 (2005) 853-875
13. Samejima K., and Earnshaw W.C. Trashing the genome: the role of nucleases during apoptosis. Nat. Rev. Mol. Cell. Biol. 6 (2005) 677-688
14. Widlak P., and Garrard W.T. Discovery, regulation, and action of the major apoptotic nucleases DFF40/CAD and endonuclease G. J. Cell. Biochem. 94 (2005) 1078-1087
15. Liu X., Li P., Widlak P., Zou H., Luo X., Garrard W.T., and Wang X. The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 8461-8466
16. Napirei M., Karsunky H., Zevnik B., Stephan H., Mannherz H.G., and Moroy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 25 (2000) 177-181
17. Maekawa Y., and Yasutomo K. Defective clearance of nucleosomes and systemic lupus erythematosus. Trends Immunol. 22 (2001) 662-663
18. Yasutomo K., Horiuchi T., Kagami S., Tsukamoto H., Hashimura C., Urushihara M., and Kuroda Y. Mutation of DNASE1 in people with systemic lupus erythematosus. Nat. Genet. 28 (2001) 313-314
19. Zhang J., and Xu M. Apoptotic DNA fragmentation and tissue homeostasis. Trends Cell. Biol. 12 (2002) 84-89
20. Burma S., and Chen D.J. Role of DNA-PK in the cellular response to DNA double-strand breaks. DNA Repair (Amst.) 3 (2004) 909-918
21. Smith G.C., and Jackson S.P. The DNA-dependent protein kinase. Genes Dev. 13 (1999) 916-934
22. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3 (2003) 155-168
23. Chen B.P., Chan D.W., Kobayashi J., Burma S., Asaithamby A., Morotomi-Yano K., Botvinick E., Qin J., and Chen D.J. Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to double-strand breaks. J. Biol. Chem. 280 (2005) 14709-14715
24. Chan D.W., Chen B.P., Prithivirajsingh S., Kurimasa A., Story M.D., Qin J., and Chen D.J. Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev. 16 (2002) 2333-2338
25. Wang S., Guo M., Ouyang H., Li X., Cordon-Cardo C., Kurimasa A., Chen D.J., Fuks Z., Ling C.C., and Li G.C. The catalytic subunit of DNA-dependent protein kinase selectively regulates p53-dependent apoptosis but not cell-cycle arrest. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 1584-1588
26. Woo R.A., Jack M.T., Xu Y., Burma S., Chen D.J., and Lee P.W. DNA damage-induced apoptosis requires the DNA-dependent protein kinase, and is mediated by the latent population of p53. Embo J. 21 (2002) 3000-3008
27. Espejel S., Franco S., Sgura A., Gae D., Bailey S.M., Taccioli G.E., and Blasco M.A. Functional interaction between DNA-PKcs and telomerase in telomere length maintenance. Embo J. 21 (2002) 6275-6287
28. Espejel S., Franco S., Rodriguez-Perales S., Bouffler S.D., Cigudosa J.C., and Blasco M.A. Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. Embo J. 21 (2002) 2207-2219
29. Han Z., Malik N., Carter T., Reeves W.H., Wyche J.H., and Hendrickson E.A. DNA-dependent protein kinase is a target for a CPP32-like apoptotic protease. J. Biol. Chem. 271 (1996) 25035-25040
30. Song Q., Lees-Miller S.P., Kumar S., Zhang Z., Chan D.W., Smith G.C., Jackson S.P., Alnemri E.S., Litwack G., Khanna K.K., and Lavin M.F. DNA-dependent protein kinase catalytic subunit: a target for an ICE-like protease in apoptosis. Embo J. 15 (1996) 3238-3246
31. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 (1997) 251-260
32. Gillespie D.A., and Vousden K.H. The secret life of histones. Cell 114 (2003) 655-656
33. Yan N., and Shi Y. Histone H1.2 as a trigger for apoptosis. Nat. Struct. Biol. 10 (2003) 983-985
34. Konishi A., Shimizu S., Hirota J., Takao T., Fan Y., Matsuoka Y., Zhang L., Yoneda Y., Fujii Y., Skoultchi A.I., and Tsujimoto Y. Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 114 (2003) 673-688
35. Cheung W.L., Ajiro K., Samejima K., Kloc M., Cheung P., Mizzen C.A., Beeser A., Etkin L.D., Chernoff J., Earnshaw W.C., and Allis C.D. Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113 (2003) 507-517
36. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273 (1998) 5858-5868
37. Fernandez-Capetillo O., Lee A., Nussenzweig M., and Nussenzweig A. H2AX: the histone guardian of the genome. DNA Repair (Amst.) 3 (2004) 959-967
38. Redon C., Pilch D., Rogakou E., Sedelnikova O., Newrock K., and Bonner W. Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12 (2002) 162-169
39. Thiriet C., and Hayes J.J. Chromatin in need of a fix: phosphorylation of H2AX connects chromatin to DNA repair. Mol. Cell 18 (2005) 617-622
40. Downs J.A., Allard S., Jobin-Robitaille O., Javaheri A., Auger A., Bouchard N., Kron S.J., Jackson S.P., and Cote J. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16 (2004) 979-990
41. Burma S., Chen B.P., Murphy M., Kurimasa A., and Chen D.J. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276 (2001) 42462-42467
42. Wang J., Pluth J.M., Cooper P.K., Cowan M.J., Chen D.J., and Yannone S.M. Artemis deficiency confers a DNA double-strand break repair defect and Artemis phosphorylation status is altered by DNA damage and cell cycle progression. DNA Repair (Amst.) 4 (2005) 556-570
43. Ward I.M., and Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276 (2001) 47759-47762
44. Stiff T., O'Driscoll M., Rief N., Iwabuchi K., Lobrich M., and Jeggo P.A. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64 (2004) 2390-2396
45. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., and Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10 (2000) 886-895
46. Rogakou E.P., Nieves-Neira W., Boon C., Pommier Y., and Bonner W.M. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J. Biol. Chem. 275 (2000) 9390-9395
47. Peterson S.R., Kurimasa A., Oshimura M., Dynan W.S., Bradbury E.M., and Chen D.J. Loss of the catalytic subunit of the DNA-dependent protein kinase in DNA double-strand-break-repair mutant mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 3171-3174
48. Kurimasa A., Kumano S., Boubnov N.V., Story M.D., Tung C.S., Peterson S.R., and Chen D.J. Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Mol. Cell. Biol. 19 (1999) 3877-3884
49. Ding L.H., Shingyoji M., Chen F., Hwang J.J., Burma S., Lee C., Cheng J.F., and Chen D.J. Gene expression profiles of normal human fibroblasts after exposure to ionizing radiation: a comparative study of low and high doses. Radiat. Res. 164 (2005) 17-26
50. Kraakman-van der Zwet M., Overkamp W.J., Jaspers N.G., Natarajan A.T., Lohman P.H., and Zdzienicka M.Z. Complementation of chromosomal aberrations in AT/NBS hybrids: inadequacy of RDS as an endpoint in complementation studies with immortal NBS cells. Mutat. Res. 485 (2001) 177-185
51. Allalunis-Turner M.J., Zia P.K., Barron G.M., Mirzayans R., and Day R.S. 3rd Radiation-induced DNA damage and repair in cells of a radiosensitive human malignant glioma cell line. Radiat. Res. 144 (1995) 288-293
52. Veuger S.J., Curtin N.J., Richardson C.J., Smith G.C., and Durkacz B.W. Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1. Cancer Res. 63 (2003) 6008-6015
53. Sarkaria J.N., Busby E.C., Tibbetts R.S., Roos P., Taya Y., Karnitz L.M., and Abraham R.T. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59 (1999) 4375-4382
54. Gavrieli Y., Sherman Y., and Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell. Biol. 119 (1992) 493-501
55. Koopman G., Reutelingsperger C.P., Kuijten G.A., Keehnen R.M., Pals S.T., and van Oers M.H. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84 (1994) 1415-1420
56. Crouch S.P., Kozlowski R., Slater K.J., and Fletcher J. The use of ATP bioluminescence as a measure of cell proliferation and cytotoxicity. J. Immunol. Methods 160 (1993) 81-88
57. Burma S., Kurimasa A., Xie G., Taya Y., Araki R., Abe M., Crissman H.A., Ouyang H., Li G.C., and Chen D.J. DNA-dependent protein kinase-independent activation of p53 in response to DNA damage. J. Biol. Chem. 274 (1999) 17139-17143
58. Hollick J.J., Golding B.T., Hardcastle I.R., Martin N., Richardson C., Rigoreau L.J., Smith G.C., and Griffin R.J. 2,6-Disubstituted pyran-4-one and thiopyran-4-one inhibitors of DNA-Dependent protein kinase (DNA-PK). Bioorg. Med. Chem. Lett. 13 (2003) 3083-3086
59. Banin S., Moyal L., Shieh S., Taya Y., Anderson C.W., Chessa L., Smorodinsky N.I., Prives C., Reiss Y., Shiloh Y., and Ziv Y. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281 (1998) 1674-1677
60. Canman C.E., Lim D.S., Cimprich K.A., Taya Y., Tamai K., Sakaguchi K., Appella E., Kastan M.B., and Siliciano J.D. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281 (1998) 1677-1679
61. Tibbetts R.S., Brumbaugh K.M., Williams J.M., Sarkaria J.N., Cliby W.A., Shieh S.Y., Taya Y., Prives C., and Abraham R.T. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13 (1999) 152-157
62. Douglas P., Sapkota G.P., Morrice N., Yu Y., Goodarzi A.A., Merkle D., Meek K., Alessi D.R., and Lees-Miller S.P. Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem. J. 368 (2002) 243-251
63. Ding Q., Reddy Y.V., Wang W., Woods T., Douglas P., Ramsden D.A., Lees-Miller S.P., and Meek K. Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol. Cell. Biol. 23 (2003) 5836-5848
64. Soubeyrand S., Pope L., Pakuts B., and Hache R.J. Threonines 2638/2647 in DNA-PK are essential for cellular resistance to ionizing radiation. Cancer Res. 63 (2003) 1198-1201
65. Smith G.C., d'Adda di Fagagna F., Lakin N.D., and Jackson S.P. Cleavage and inactivation of ATM during apoptosis. Mol. Cell. Biol. 19 (1999) 6076-6084
66. Bakkenist C.J., and Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 (2003) 499-506
67. Paull T.T., and Lee J.H. The Mre11/Rad50/Nbs1 complex and its role as a DNA double-strand break sensor for ATM. Cell Cycle 4 (2005) 737-740
68. Lee J.H., and Paull T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308 (2005) 551-554
69. Bakkenist C.J., and Kastan M.B. Initiating cellular stress responses. Cell 118 (2004) 9-17
70. Jacobson M.D., Burne J.F., and Raff M.C. Programmed cell death and Bcl-2 protection in the absence of a nucleus. Embo J. 13 (1994) 1899-1910
71. Andreau K., Castedo M., Perfettini J.L., Roumier T., Pichart E., Souquere S., Vivet S., Larochette N., and Kroemer G. Preapoptotic chromatin condensation upstream of the mitochondrial checkpoint. J. Biol. Chem. 279 (2004) 55937-55945
72. Vaughan A.T., Betti C.J., and Villalobos M.J. Surviving apoptosis. Apoptosis 7 (2002) 173-177
73. Betti C.J., Villalobos M.J., Diaz M.O., and Vaughan A.T. Apoptotic triggers initiate translocations within the MLL gene involving the nonhomologous end joining repair system. Cancer Res. 61 (2001) 4550-4555
74. Betti C.J., Villalobos M.J., Diaz M.O., and Vaughan A.T. Apoptotic stimuli initiate MLL-AF9 translocations that are transcribed in cells capable of division. Cancer Res. 63 (2003) 1377-1381
75. Roulston D., Espinosa III R., Nucifora G., Larson R.A., Le Beau M.M., and Rowley J.D. CBFA2(AML1) translocations with novel partner chromosomes in myeloid leukemias: association with prior therapy. Blood 92 (1998) 2879-2885