DNA repair in the context of chromatin: New molecular insights by the nanoscale detection of DNA repair complexes using transmission electron microscopy

DNA Repair

Volumn 10, Issue 4, 2011, Pages 427-437

  Rübe, Claudia E ^a   Lorat, Yvonne ^a   Schuler, Nadine ^a   Schanz, Stefanie ^a   Wennemuth, Gunther ^a   Rübe, Christian ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

H2AX; 53BP1; DNA double strand break repair; Ku70 Ku80 heterodimer; MDC1; Non homologous end joining; Transmission electron microscopy

Indexed keywords

CELL PROTEIN; GAMMA HISTONE H2AX; HISTONE; HISTONE H2AX; PROTEIN 53BP1; PROTEIN MDC1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CHROMATIN STRUCTURE; DNA DAMAGE; DNA PACKAGING; DNA REPAIR; EUCHROMATIN; HETEROCHROMATIN; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CELL NUCLEUS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; KINETICS; METAL NANOPARTICLES; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; NUCLEAR PROTEINS; WHOLE-BODY IRRADIATION;

EID: 79952705536     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2011.01.012     Document Type: Article

References (41)

1. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
2. Schneider R., Grosschedl R. Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev. 2007, 21:3027-3043.
3. Misteli T, Soutoglou E. The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat. Rev. Mol. Cell. Biol. 2009, 10:243-254.
4. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
5. Fernandez-Capetillo O., Nussenzweig A. ATM breaks into heterochromatin. Mol. Cell 2008, 31:303-304.
6. Goodarzi A.A., Noon A.T., Deckbar D., Ziv Y., Shiloh Y., Lobrich M., Jeggo P.A. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 2008, 31:167-177.
7. Goodarzi A.A., Noon A.T., Jeggo P.A. The impact of heterochromatin on DSB repair. Biochem. Soc. Trans. 2009, 37:569-576.
8. Murga M., Jaco I., Fan Y., Soria R., Martinez-Pastor B., Cuadrado M., Yang S.M., Blasco M.A., Skoultchi A.I., Fernandez-Capetillo O. Global chromatin compaction limits the strength of the DNA damage response. J. Cell. Biol. 2007, 178:1101-1108.
9. Noon A.T., Shibata A., Rief N., Lobrich M., Stewart G.S., Jeggo P.A., Goodarzi A.A. 53BP1-dependent robust localized KAP-1 phosphorylation is essential for heterochromatic DNA double-strand break repair. Nat. Cell. Biol. 2010, 12:177-184.
10. Mahaney B.L., Meek K., Lees-Miller S.P. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem. J. 2009, 417:639-650.
11. W.Y. Mansour, T. Rhein and J. Dahm-Daphi, The alternative end-joining pathway for repair of DNA double-strand breaks requires PARP1 but is not dependent upon microhomologies, Nucleic Acids Res. ([published online ahead of print May 18, 2010]).
12. Walker J.R., Corpina R.A., Goldberg J. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 2001, 412:607-614.
13. Schulte-Uentrop L., El-Awady R.A., Schliecker L., Willers H., Dahm-Daphi J. Distinct roles of XRCC4 and Ku80 in non-homologous end-joining of endonuclease- and ionizing radiation-induced DNA double-strand breaks. Nucleic Acids Res. 2008, 36:2561-2569.
14. Cary R.B., Peterson S.R., Wang J., Bear D.G., Bradbury E.M., Chen D.J. DNA looping by Ku and the DNA-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:4267-4272.
15. van Attikum H., Gasser S.M. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 2009, 19:207-217.
16. Zhu Q., Wani A.A. Histone modifications: crucial elements for damage response and chromatin restoration. J. Cell Physiol. 2010, 223:283-288.
17. Kinner A., Wu W., Staudt C., Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 2008, 36:5678-5694.
18. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273:5858-5868.
19. Nakamura A.J., Rao V.A., Pommier Y., Bonner W.M. The complexity of phosphorylated H2AX foci formation and DNA repair assembly at DNA double-strand breaks. Cell Cycle 2010, 9:389-397.
20. Jakob B., Splinter J., Taucher-Scholz G. Positional stability of damaged chromatin domains along radiation tracks in mammalian cells. Radiat. Res. 2009, 171:405-418.
21. Stewart G.S., Wang B., Bignell C.R., Taylor A.M., Elledge S.J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 2003, 421:961-966.
22. Eliezer Y., Argaman L., Rhie A., Doherty A.J., Goldberg M. The direct interaction between 53BP1 and MDC1 is required for the recruitment of 53BP1 to sites of damage. J. Biol. Chem. 2009, 284:426-435.
23. Stenerlow B., Hoglund E. Rejoining of double-stranded DNA-fragments studied in different size-intervals. Int. J. Radiat. Biol. 2002, 78:1-7.
24. Prise K.M., Ahnstrom G., Belli M., Carlsson J., Frankenberg D., Kiefer J., Lobrich M., Michael B.D., Nygren J., Simone G., Stenerlow B. A review of dsb induction data for varying quality radiations. Int. J. Radiat. Biol. 1998, 74:173-184.
25. Lobrich M., Shibata A., Beucher A., Fisher A., Ensminger M., Goodarzi A.A., Barton O., Jeggo P.A. gammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle 2010, 9:662-669.
26. Rube C.E, Dong X., Kuhne M., Fricke A., Kaestner L., Lipp P., Rube C. DNA double-strand break rejoining in complex normal tissues. Int. J. Radiat. Oncol. Biol. Phys. 2008, 72:1180-1187.
27. Rube C.E., Fricke A., Wendorf J., Stutzel A., Kuhne M., Ong M.F., Lipp P., Rube C. Accumulation of DNA double-strand breaks in normal tissues after fractionated irradiation. Int. J. Radiat. Oncol. Biol. Phys. 2010, 76:1206-1213.
28. Rube C.E., Grudzenski S., Kuhne M., Dong X., Rief N., Lobrich M., Rube C. DNA double-strand break repair of blood lymphocytes and normal tissues analysed in a preclinical mouse model: implications for radiosensitivity testing. Clin. Cancer Res. 2008, 14:6546-6555.
29. Bhogal N., Jalali F., Bristow R.G. Microscopic imaging of DNA repair foci in irradiated normal tissues. Int. J. Radiat. Biol. 2009, 85:732-746.
30. Morrison A.J., Shen X. DNA repair in the context of chromatin. Cell Cycle 2005, 4:568-571.
31. Downs J.A., Nussenzweig M.C., Nussenzweig A. Chromatin dynamics and the preservation of genetic information. Nature 2007, 447:951-958.
32. Fernandez-Capetillo O., Murga M. Why cells respond differently to DNA damage: a chromatin perspective. Cell Cycle 2008, 7:980-983.
33. Rothkamm K., Lobrich M. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low X-ray doses. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5057-5062.
34. Costes S.V., Chiolo I., Pluth J.M., Barcellos-Hoff M.H., Jakob B. Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutat. Res. 2010, 704:78-87.
35. Iliakis G., Wang H., Perrault A.R., Boecker W., Rosidi B., Windhofer F., Wu W., Guan J., Terzoudi G., Pantelias G. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet. Genome Res. 2004, 104:14-20.
36. Aten J.A., Stap J., Krawczyk P.M., van Oven C.H., Hoebe R.A., Essers J., Kanaar R. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 2004, 303:92-95.
37. Jakob B., Splinter J., Durante M., Taucher-Scholz G. Live cell microscopy analysis of radiation-induced DNA double-strand break motion. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3172-3177.
38. Kruhlak M.J., Celeste A., Dellaire G., Fernandez-Capetillo O., Muller W.G., McNally J.G., Bazett-Jones D.P., Nussenzweig A. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 2006, 172:823-834.
39. Misteli T. Beyond the sequence: cellular organization of genome function. Cell 2007, 128:787-800.
40. Maison C., Almouzni G. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell. Biol. 2004, 5:296-304.
41. Dinant C., Luijsterburg M.S. The emerging role of HP1 in the DNA damage response. Mol. Cell. Biol. 2009, 29:6335-6340.