Autophosphorylation-dependent remodeling of the DNA-dependent protein kinase catalytic subunit regulates ligation of DNA ends

Nucleic Acids Research

Volumn 32, Issue 14, 2004, Pages 4351-4357

  Block, Wesley D ^a,b   Yu, Yaping ^a   Merkle, Dennis ^b   Gifford, Jessica L ^b   Ding, Qi ^c   Meek, Katheryn ^c   Lees Miller, Susan P ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; DNA DEPENDENT PROTEIN KINASE; DOUBLE STRANDED DNA; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN SUBUNIT; SERINE; THREONINE; DNA; DNA BINDING PROTEIN; PROTEIN SERINE THREONINE KINASE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA PROTEIN COMPLEX; DNA PURIFICATION; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME DEGRADATION; GENE CLUSTER; GENE EXPRESSION; GENE MUTATION; GENETIC REGULATION; HUMAN; HUMAN CELL; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; WILD TYPE; ANIMAL; CATALYSIS; CELL LINE; DNA DAMAGE; GENETICS; HAMSTER; METABOLISM; MUTATION; PHOSPHORYLATION;

MAMMALIA;

ANIMALS; CATALYSIS; CELL LINE; CRICETINAE; DNA; DNA DAMAGE; DNA LIGASES; DNA REPAIR; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; MUTATION; PHOSPHORYLATION; PROTEIN SUBUNITS; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING;

EID: 4043073590     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh761     Document Type: Article

References (39)

1. West,S.C. (2003) Molecular views of recombination proteins and their control. Nature Rev. Mol. Cell Biol., 4, 435-445.
2. Lees-Miller,S.P. and Meek,K. (2003) Repair of DNA double strand breaks by non-homologous end joining. Biochimie, 85, 1161-1173.
3. Valerie,K. and Povirk,L.F. (2003) Regulation and mechanisms of mammalian double-strand break repair. Oncogene, 22, 5792-5812.
4. Lieber,M.R., Ma,Y., Pannicke,U. and Schwarz,K. (2003) Mechanism and regulation of human non-homologous DNA end-joining. Nature Rev. Mol. Cell Biol., 4, 712-720.
5. O'Neill,T., Dwyer,A.J., Ziv,Y., Chan,D.W., Lees-Miller,S.P., Abraham,R.H., Lai,J.H., Hill,D., Shiloh,Y., Cantley,L.C. and Rathbun,G.A. (2000) Utilization of oriented peptide libraries to identify substrate motifs selected by ATM. J. Biol. Chem., 275, 22719-22727.
6. Lees-Miller,S.P., Sakaguchi,K., Ullrich,S.J., Appella,E. and Anderson,C.W. (1992) Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol., 12, 5041-5049.
7. Ma,Y., Pannicke,U., Schwarz,K. and Lieber,M.R. (2002) Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell, 108, 781-794.
8. Chappell,C., Hanakahi,L.A., Karimi-Busheri,F., Weinfeld,M. and West,S.C. (2002) Involvement of human polynucleotide kinase in double-strand break repair by non-homologous endjoining. EMBO J., 21, 2827-2832.
9. Li,B. and Comai,L. (2002) Displacement of DNA-PKcs from DNA ends by the Werner syndrome protein. Nucleic Acids Res., 30, 3653-3661.
10. Yannone,S.M., Roy,S., Chan,D.W., Murphy,M.B., Huang,S., Campisi,J. and Chen,D.J. (2001) Werner syndrome protein is regulated and phosphorylated by DNA-dependent protein kinase. J. Biol. Chem., 276, 38242-38248.
11. Mahajan,K.N., Nick McElhinny,S.A., Mitchell,B.S. and Ramsden,D.A. (2002) Association of DNA polymerase mu (pol mu) with Ku and ligase IV: role for pol mu in end-joining double-strand break repair. Mol. Cell. Biol., 22, 5194-5202.
12. Lee,J.W., Blanco,L., Zhou,T., Garcia-Diaz,M., Bebenek,K., Kunkel,T.A., Wang,Z. and Povirk,L.F. (2004) Implication of DNA polymerase lambda in alignment-based gap filling for nonhomologous DNA end joining in human nuclear extracts. J. Biol. Chem., 279, 805-811.
13. Kurimana,A., Kumano,S., Boubnov,N.V., Story,M.D., Tung,C.S., Peterson,S.R. and Chen,D.J. (1999) Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Mol. Cell. Biol., 19, 3877-3884.
14. Kienker,L.J., Shin,E.K. and Meek,K. (2000) Both V(D)J recombination and radioresistance require DNA-PK kinase activity, though minimal levels suffice for V(D)J recombination. Nucleic Acids Res., 28, 2752-2761.
15. Chernikova,S.B., Wells,R.L. and Elkind,M.M. (1999) Wortmannin sensitizes mammalian cells to radiation by inhibiting the DNA-dependent protein kinase-mediated rejoining of double-strand breaks. Radiat. Res., 151, 159-166.
16. Okayasu,R., Suetomi,K. and Ullrich,R.L. (1998) Wortmannin inhibits repair of DNA double-strand breaks in irradiated normal human cells. Radiat. Res., 149, 440-445.
17. Rosenzweig,K.E., Youmell,M.B., Palayoor,S.T. and Price,B.D. (1997) Radiosensitization of human tumor cells by the phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 correlates with inhibition of DNA-dependent protein kinase and prolonged G2-M delay. Clin. Cancer Res., 3, 1149-1156.
18. Sarkaria,J.N., Tibbetts,R.S., Busby,E.C., Kennedy,A.P., Hill,D.E. and Abraham,R.T. (1998) Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res., 58, 4375-4382.
19. Izzard,R.A,, Jackson,S.P. and Smith,G.C. (1999) Competitive and noncompetitive inhibition of the DNA-dependent protein kinase. Cancer Res., 59, 2581-2586.
20. Wang,H., Zeng,Z.C., Bui,T.A., DiBiase,S.J., Qin,W., Xia,F., Powell,S.N. and Iliakis,G. (2001) Nonhomologous end-joining of ionizing radiation-induced DNA double-stranded breaks in human tumor cells deficient in BRCA1 or BRCA2. Cancer Res., 61, 270-277.
21. Okayasu,R., Takakura,K., Poole,S. and Bedford,J.S. (2003) Radiosensitization of normal human cells by LY294002: cell killing and the rejoining of DNA and interphase chromosome breaks. J. Radiat. Res. (Tokyo), 44, 329-333.
22. Baumann,P. and West,S.C. (1998) DNA end-joining catalyzed by human cell-free extracts. Proc. Natl Acad. Sci. USA, 95, 14066-14070.
23. Lees-Miller,S.P., Chen,Y.R. and Anderson,C.W. (1990) Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol. Cell. Biol., 10, 6472-6481.
24. Chan,D.W. and Lees-Miller,S.P. (1996) The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. J. Biol. Chem., 271, 8936-8941.
25. Merkle,D., Douglas,P., Moorhead,G.B., Leonenko,Z., Yu,Y., Cramb,D., Bazett-Jones,D.P. and Lees-Miller,S.P. (2002) The DNA-dependent protein kinase interacts with DNA to form a protein-DNA complex that is disrupted by phosphorylation. Biochemistry, 41, 12706-12714.
26. Yoo,S. and Dynan,W.S. (1999) Geometry of a complex formed by double strand break repair proteins at a single DNA end: recruitment of DNA-PKcs induces inward translocation of Ku protein. Nucleic Acids Res., 27, 4679-4686.
27. Cary,R.B., Peterson,S.R., Wang,J., Bear,D.G., Bradbury,E.M. and Chen,D.J. (1997) DNA looping by Ku and the DNA-dependent protein kinase. Proc. Natl Acad. Sci. USA, 94, 4267-4272.
28. Weterings,E., Verkaik,N.S., Bruggenwirth,H.T., Hoeijmakers,J.H. and van Gent,D.C. (2003) The role of DNA dependent protein kinase in synapsis of DNA ends. Nucleic Acids Res., 31, 7238-7246.
29. Allen,C., Halbrook,J. and Nickoloff,J.A. (2003) Interactive competition between homologous recombination and non-homologous end joining. Mol. Cancer Res., 1, 913-920.
30. Ding,Q., Reddy,Y.V., Wang,W., Woods,T., Douglas,P., Ramsden,D.A., Lees-Miller,S.P. and Meek,K. (2003) 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, 5836-5848.
31. Douglas,P., Sapkota,G.P., Morrice,N., Yu,Y., Goodarzi,A.A., Merkle,D., Meek,K., Alessi,D.R. and Lees-Miller,S.P. (2002) Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem J., 368, 243-251.
32. Chan,D.W., Chen,B.P., Prithivirajsingh,S., Kurimasa,A., Story,M.D., Qin,J. and Chen,D.J. (2002) Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev., 16, 2333-2338.
33. Soubeyrand,S., Pope,L., Pakuts,B. and Hache,R.J. (2003) Threonines 2638/2647 in DNA-PK are essential for cellular resistance to ionizing radiation. Cancer Res., 63, 1198-1201.
34. Block,W.D., Merkle,D., Meek,K. and Lees-Miller,S.P. (2004) Selective inhibition of the DNA-dependent protein kinase (DNA-PK) by the radiosensitizing agent caffeine. Nucleic Acids Res., 32, 1967-1972.
35. Goodarzi,A.A. and Lees-Miller,S.P. (2004) Biochemical characterization of the ataxia-telangiectasia mutated (ATM) protein from human cells. DNA Repair (Amst.), 3, 753-767.
36. Chan,D.W., Mody,C.H., Ting,N.S. and Lees-Miller,S.P. (1996) Purification and characterization of the double-stranded DNA-activated protein kinase, DNA-PK, from human placenta. Biochem. Cell Biol., 74, 67-73.
37. Reddy,Y.V, Ding,Q., Lees-Miller,S.P., Meek,K. and Ramsden,D.A. (2004) Nonhomologous end-joining requires that the DNA-PK complex undergo an autophosphorylation-dependent rearrangement at DNA ends. J. Biol. Chem., Jul 15, epub ahead of print.
38. Wechsler,T., Chen,B.P., Harper,R., Morotomi-Yano,K., Huang,B.C., Meek,K., Cleaver,J.E., Chen,D.J. and Wabl,M. (2004) DNA-PKcs function regulated specifically by protein phosphatase 5. Proc. Natl Acad. Sci. USA, 101, 1247-1252.
39. Douglas,P., Moorhead,G.B., Ye,R. and Lees-Miller,S.P. (2001) Protein phosphatases regulate DNA-dependent protein kinase activity. J. Biol. Chem., 276, 18992-18998.