Terminal DNA structure and ATP influence binding parameters of the DNA-dependent protein kinase at an early step prior to DNA synapsis

Nucleic Acids Research

Volumn 34, Issue 4, 2006, Pages 1112-1120

  Jovanovic, Marko ^a   Dynan, William S ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA BASE; DNA DEPENDENT PROTEIN KINASE; DNA FRAGMENT; KU ANTIGEN; RNA POLYMERASE; ADENYLYLIMIDODIPHOSPHATE; CELL NUCLEUS ANTIGEN; DNA; DNA BINDING PROTEIN;

ALLOSTERISM; ARTICLE; AUTOPHOSPHORYLATION; BASE MISPAIRING; CHROMOSOME PAIRING; COMPLEX FORMATION; CONTROLLED STUDY; DNA CROSS LINKING; DNA DENATURATION; DNA STRUCTURE; HUMAN; HUMAN CELL; MOLECULAR MODEL; MOLECULAR STABILITY; NUCLEIC ACID IMMOBILIZATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; REGULATORY MECHANISM; TEMPERATURE DEPENDENCE; CHEMISTRY; HELA CELL; METABOLISM; PHOSPHORYLATION; PROTEIN BINDING; SURFACE PLASMON RESONANCE;

MAMMALIA;

ADENOSINE TRIPHOSPHATE; ADENYLYL IMIDODIPHOSPHATE; ALLOSTERIC REGULATION; ANTIGENS, NUCLEAR; CHROMOSOME PAIRING; DNA; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; PHOSPHORYLATION; PROTEIN BINDING; SURFACE PLASMON RESONANCE;

EID: 33644871780     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkj504     Document Type: Article

References (54)

1. Ward,J.F. (1998) Nature of lesions formed by ionizing radiation. In Nickoloff,J.A. and Hoekstra,M.F. (eds), DNA Damage and Repair, Vol. II, pp. 65-84.
2. Roth,D.B., Menetski,J.P., Nakajima,P.B., Bosma,M.J. and Gellert,M. (1992) V(D)J recombination: Broken DNA molecules with covalently sealed (hairpin) coding ends in scid mouse thymocytes. Cell, 70, 983-991.
3. Sadofsky,M.J. (2001) The RAG proteins in V(D)J recombination: More than just a nuclease. Nucleic Acids Res., 29, 1399-1409.
4. Jin,S., Inoue,S. and Weaver,D.T. (1998) Differential etoposide sensitivity of cells deficient in the Ku and DNA-PKcs components of the DNA-dependent protein kinase. Carcinogenesis, 965-971.
5. Pawelczak,K.S., Andrews,B.J. and Turchi,J.J. (2005) Differential activation of DNA-PK based on DNA strand orientation and sequence bias. Nucleic Acids Res., 33, 152-161.
6. Meek,K., Gupta,S., Ramsden,D.A. and Lees-Miller,S.P. (2004) The DNA-dependent protein kinase: The director at the end. Immunol. Rev., 200, 132-141.
7. Collis,S.J., DeWeese,T.L., Jeggo,P.A. and Parker,A.R. (2005) The life and death of DNA-PK. Oncogene, 24, 949-961.
8. Burma,S. and Chen,D.J. (2004) Role of DNA-PK in the cellular response to DNA double-strand breaks. DNA Repair (Amst.), 3, 909-918.
9. Weterings,E. and van Gent,D.C. (2004) The mechanism of non-homologous end joining: A synopsis of synapsis. DNA Repair (Amst.), 3, 1425-1435.
10. 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.
11. Cui,X., Yu,Y., Gupta,S., Cho,Y.M., Lees-Miller,S.P. and Meek,K. (2005) Autophosphorylation of DNA-dependent protein kinase regulates DNA end processing and may also alter double-strand break repair pathway choice. Mol. Cell. Biol., 25, 10842-10852.
12. Convery,E., Shin,E.K., Ding,Q., Wang,W., Douglas,P., Davis,L.S., Nickoloff,J.A., Lees-Miller,S.P. and Meek,K. (2005) Inhibition of homologous recombination by variants of the catalytic subunit of the DNA-dependent protein kinase (DNA-PKcs). Proc. Natl Acad. Sci. USA, 102, 1345-1350.
13. Calsou,P., Delteil,C., Frit,P., Drouet,J. and Salles,B. (2003) Coordinated assembly of Ku and p460 subunits of the DNA-dependent protein kinase on DNA ends is necessary for XRCC4-ligase IV recruitment. J. Mol. Biol., 326, 93-103.
14. Hsu,H.L., Yannone,S.M. and Chen,D.J. (2002) Defining interactions between DNA-PK and ligase IV/XRCC4. DNA Repair (Amst.), 1, 225-235.
15. Leber,R., Wise,T.W., Mizuta,R. and Meek,K. (1998) The XRCC4 gene product is a target for and interacts with the DNA-dependent protein kinase. J. Biol. Chem., 273, 1794-1801.
16. Ma,Y., Pannicke,U., Lu,H., Niewolik,D., Schwarz,K. and Lieber,M.R. (2005) The DNA-dependent protein kinase catalytic subunit phosphorylation sites in human Artemis. J. Biol. Chem., 280, 33839-33846.
17. 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.
18. Peterson,S.R., Dvir,A., Anderson,C.W. and Dynan,W.S. (1992) DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats. Genes Dev., 6, 426-438.
19. Gottlieb,T.M. and Jackson,S.P. (1993) The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell, 72, 131-142.
20. 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.
21. Llorca,O. and Pearl,L.H. (2004) Electron microscopy studies on DNA recognition by DNA-PK. Micron, 35, 625-633.
22. Rivera-Calzada,A., Maman,J.P., Spagnolo,L., Pearl,L.H. and Llorca,O. (2005) Three-dimensional structure and regulation of the DNA-dependent protein kinase catalytic subunit (DNA-PKcs). Structure, 13, 243-255.
23. Kurimasa,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.
24. 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.
25. 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.
26. Ding,Q., Reddy,Y.T.R., 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., 268, 5836-5848.
27. Block,W.D., Yu,Y., Merkle,D., Gifford,J.L., Ding,Q., Meek,K. and Lees-Miller,S.P. (2004) Autophosphorylation-dependent remodeling of the DNA-dependent protein kinase catalytic subunit regulates ligation of DNA ends. Nucleic Acids Res., 32, 4351-4357.
28. 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., 279, 39408-39413.
29. Wang,Y.G., Nnakwe,C., Lane,W.S., Modesti,M. and Frank,K.M. (2004) Phosphorylation and regulation of DNA ligase IV stability by DNA-dependent protein kinase. J. Biol. Chem., 279, 37282-37290.
30. Modesti,M., Hesse,J.E. and Gellert,M. (1999) DNA binding of Xrcc4 protein is associated with V (D)J recombination but not with stimulation of DNA ligase IV activity. EMBO J., 18, 2008-2018.
31. Lee,K.J., Jovanovic,M., Udayakumar,D., Bladen,C.L. and Dynan,W.S. (2004) Identification of DNA-PKcs phosphorylation sites in XRCC4 and effects of mutations at these sites on DNA end joining in a cell-free system. DNA Repair (Amst.), 3, 267-276.
32. Smider,V., Rathmell,W.K., Brown,G., Lewis,S. and Chu,G. (1998) Failure of hairpin-ended and nicked DNA to activate DNA-dependent protein kinase: Implications for V(D)J recombination. Mol. Cell. Biol., 6853-6858.
33. Hammarsten,O., DeFazio,L.G. and Chu,G. (2000) Activation of DNA-dependent protein kinase by single-stranded DNA ends. J. Biol. Chem., 275, 1541-1550.
34. Soubeyrand,S., Torrance,H., Griffin,W., Gong,W., Schild-Poulter,C. and Hache,R.J. (2001) Activation and autoregulation of DNA-PKcs from structured single-stranded DNA and coding end hairpins. Proc. Natl Acad. Sci. USA, 98, 9605-9610.
35. West,R.B., Yaneva,M. and Lieber,M.R. (1998) Productive and nonproductive complexes of Ku and DNA-dependent protein kinase at DNA temini. Mol. Cell. Biol., 18, 5908-5920.
36. Mangel,W.F. and Chamberlin,M.J. (1974) Studies of ribonucleic acid chain initiation by Escherichia coli ribonucleic acid polymerase bound to T7 deoxyribonucleic acid. 3. The effect of temperature on ribonucleic acid chain initiation and on the conformation of binary complexes. J. Biol. Chem., 249, 3007-3013.
37. Dvir,A., Stein,L.Y., Calore,B.L. and Dynan,W.S. (1993) Purification and characterization of a template-associated protein kinase that phosphorylates RNA polymerase II. J. Biol. Chem., 268, 10440-10447.
38. Ono,M., Tucker,P.W. and Capra,J.D. (1994) Production and characterization of recombinant human Ku antigen. Nucleic Acids Res., 22, 3918-3924.
39. Yoo,S., Kimzey,A. and Dynan,W.S. (1999) Photocross-linking of an oriented DNA repair complex. Ku bound at a single DNA end. J. Biol. Chem., 274, 20034-20039.
40. Stenberg,E., Persson,B., Roos,H. and Urbaniczky,C. (1991) Quantitative determination of surface concentration of protein with surface plasmon resonance by using radiolabeled proteins. Colloid Interface Sci., 143, 513-526.
41. Martensson,S. and Hammarsten,O. (2002) DNA-dependent protein kinase catalytic subunit - structural requirements for kinase activation by DNA ends. J. Biol. Chem., 277, 3020-3029.
42. Zhang,W.W. and Yaneva,M. (1992) On the mechanisms of Ku protein binding to DNA. Biochem. Biophys. Res. Commun., 186, 574-579.
43. Mimori,T. and Hardin,J.A. (1986) Mechanism of interaction between Ku protein and DNA. J. Biol. Chem., 261, 10375-10379.
44. Hammarsten,O. and Chu,G. (1998) DNA-dependent protein kinase: DNA binding and activation in the absence of Ku. Proc. Natl Acad. Sci. USA, 95, 525-530.
45. 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.
46. Jafri,F., Hardin,J.A. and Dynan,W.S. (2001) A method to detect particle-specific antibodies against Ku and the DNA-dependent protein kinase catalytic subunit in autoimmune sera. J. Immunol. Methods, 251, 53-61.
47. DeFazio,L.G., Stansel,R., Griffith,J.D. and Chu,G. (2002) Synapsis of DNA ends by DNA-dependent protein kinase. 21, 3192-3200.
48. Mekler,V., Kortkhonjia,E., Mukhopadhyay,J., Knight,J., Revyakin,A., Kapanidis,A.N., Niu,W., Ebright,Y.W., Levy,R. and Ebright,R.H. (2002) Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex. Cell, 108, 599-614.
49. Budman,J. and Chu,G. (2005) Processing of DNA for nonhomologous end-joining by cell-free extract. EMBO J., 24, 849-860.
50. Ma,Y., Lu,H., Tippin,B., Goodman,M.F., Shimazaki,N., Koiwai,O., Hsieh,C.L., Schwarz,K. and Lieber,M.R. (2004) A biochemically defined system for mammalian nonhomologous DNA end joining. Mol. Cell, 16, 701-713.
51. Woo,R.A., McLure,K.G., Lees-Miller,S.P., Rancourt,D.E. and Lee,P.W. (1998) DNA-dependent protein kinase acts upstream of p53 in response to DNA damage. Nature, 394, 700-704.
52. 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. (2000) The catalytic subunit of DNA-dependent protein kinase selectively regulates p53-dependent apoptosis but not cell-cycle arrest. Proc. Natl Acad. Sci. USA, 97, 1584-1588.
53. Aylon,Y. and Kupiec,M. (2004) New insights into the mechanism of homologous recombination in yeast. Mutat. Res., 566, 231-248.
54. Lee,J.H. and Paull,T.T. (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science, 308, 551-554.