Heterochromatin protein 1 is recruited to various types of DNA damage

Journal of Cell Biology

Volumn 185, Issue 4, 2009, Pages 577-586

  Luijsterburg, Martijn S ^a,g   Dinant, Christoffel ^c,d,h   Lans, Hannes ^d   Stap, Jan ^b   Wiernasz, Elzbieta ^a,e   Lagerwerf, Saskia ^f   Warmerdam, Daniël O ^d   Lindh, Michael ^g   Brink, Maartje C ^a   Dobrucki, Jurek W ^e   Aten, Jacob A ^b   Fousteri, Maria I ^f   Jansen, Gert ^d   Dantuma, Nico P ^g   Vermeulen, Wim ^d   Mullenders, Leon H F ^f   Houtsmuller, Adriaan B ^c   Verschure, Pernette J ^a   Van Driel, Roel ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

^d ERASMUS MEDICAL CENTER   (Netherlands)

^e JAGIELLONIAN UNIVERSITY   (Poland)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^g KAROLINSKA INSTITUTE   (Sweden)

^h DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DNA; ENHANCED GREEN FLUORESCENT PROTEIN; HETEROCHROMATIN PROTEIN 1; HISTONE H2AX;

ALPHA RADIATION; ARTICLE; CAENORHABDITIS ELEGANS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; EXCISION REPAIR; HETEROCHROMATIN; HUMAN; HUMAN CELL; IONIZING RADIATION; LASER; NEMATODE; PRIORITY JOURNAL; ULTRAVIOLET IRRADIATION; X RAY;

ANIMALS; CAENORHABDITIS ELEGANS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; HISTONES; MUTATION; PROTEIN ISOFORMS; RADIATION, IONIZING; ULTRAVIOLET RAYS;

CAENORHABDITIS ELEGANS; NEMATODA;

EID: 66149094160     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200810035     Document Type: Article

References (50)

1. Agarwal, B.K., and J.H. Sparrow. 1981. Line intensities in the soft x-ray region. J. Phys. F Met. Phys. 11:1303-1309.
2. Aten, J.A., J. Stap, P.M. Krawczyk, C.H. van Oven, R.A. Hoebe, J. Essers, and R. Kanaar. 2004. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science. 303:92-95. (Pubitemid 38055778)
3. Aucott, R., J. Bullwinkel, Y. Yu, W. Shi, M. Billur, J.P. Brown, U. Menzel, D. Kioussis, G. Wang, I. Reisert, et al. 2008. HP1-β is required for development of the cerebral neocortex and neuromuscular junctions. J. Cell Biol. 183:597-606.
4. Ayoub, N., A.D. Jeyasekharan, J.A. Bernal, and A.R. Venkitaraman. 2008. HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature. 453:682-686.
5. Bartek, J., and J. Lukas. 2007. DNA damage checkpoints: from initiation to recovery or adaptation. Curr. Opin. Cell Biol. 19:238-245. (Pubitemid 46386406)
6. Bergink, S., F.A. Salomons, D. Hoogstraten, T.A. Groothuis, H. de Waard, J. Wu, L. Yuan, E. Citterio, A.B. Houtsmuller, J. Neefjes, et al. 2006. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 20:1343-1352. (Pubitemid 43727594)
7. Cheutin, T., A.J. McNairn, T. Jenuwein, D.M. Gilbert, P.B. Singh, and T. Misteli. 2003. Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science. 299:721-725. (Pubitemid 36159490)
8. Coustham, V., C. Bedet, K. Monier, S. Schott, M. Karali, and F. Palladino. 2006. The C. elegans HP1 homologue HPL-2 and the LIN-13 zinc finger protein form a complex implicated in vulval development. Dev. Biol. 297:308-322. (Pubitemid 44353464)
9. Dialynas, G.K., S. Terjung, J.P. Brown, R.L. Aucott, B. Baron-Luhr, P.B. Singh, and S.D. Georgatos. 2007. Plasticity of HP1 proteins in mammalian cells. J. Cell Sci. 120:3415-3424. (Pubitemid 350028349)
10. Dinant, C., M. de Jager, J. Essers, W.A. van Cappellen, R. Kanaar, A.B. Houtsmuller, and W. Vermeulen. 2007. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J. Cell Sci. 120:2731-2740. (Pubitemid 47323879)
11. Eskeland, R., A. Eberharter, and A. Imhof. 2007. HP1 binding to chromatin methylated at H3K9 is enhanced by auxiliary factors. Mol. Cell. Biol. 27:453-465. (Pubitemid 46080116)
12. Filesi, I., A. Cardinale, S. van der Sar, I.G. Cowell, P.B. Singh, and S. Biocca. 2002. Loss of heterochromatin protein 1 (HP1) chromodomain function in mammalian cells by intracellular antibodies causes cell death. J. Cell Sci. 115:1803-1813. (Pubitemid 34567242)
13. Fousteri, M., W. Vermeulen, A.A. van Zeeland, and L.H. Mullenders. 2006. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell. 23:471-482. (Pubitemid 44226450)
14. Fuks, F., P.J. Hurd, R. Deplus, and T. Kouzarides. 2003. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res. 31:2305-2312. (Pubitemid 37442098)
15. Goodarzi, A.A., A.T. Noon, D. Deckbar, Y. Ziv, Y. Shiloh, M. Lobrich, and P.A. Jeggo. 2008. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell. 31:167-177.
16. Hoeijmakers, J.H. 2001. Genome maintenance mechanisms for preventing cancer. Nature. 411:366-374. (Pubitemid 32467046)
17. Hoogstraten, D., A.L. Nigg, H. Heath, L.H. Mullenders, R. van Driel, J.H. Hoeijmakers, W. Vermeulen, and A.B. Houtsmuller. 2002. Rapid switching of TFIIH between RNA polymerase I and II transcription and DNA repair in vivo. Mol. Cell. 10:1163-1174. (Pubitemid 35453833)
18. Houtsmuller, A.B., S. Rademakers, A.L. Nigg, D. Hoogstraten, J.H. Hoeijmakers, and W. Vermeulen. 1999. Action of DNA repair endonuclease ERCC1/XPF in living cells. Science. 284:958-961. (Pubitemid 29288433)
19. Jacobs, S.A., and S. Khorasanizadeh. 2002. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science. 295:2080-2083. (Pubitemid 34229471)
20. Kruhlak, M.J., A. Celeste, G. Dellaire, O. Fernandez-Capetillo, W.G. Muller, J.G. McNally, D.P. Bazett-Jones, and A. Nussenzweig. 2006. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172:823-834.
21. Luijsterburg, M.S., J. Goedhart, J. Moser, H. Kool, B. Geverts, A.B. Houtsmuller, L.H. Mullenders, W. Vermeulen, and R. van Driel. 2007. Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC. J. Cell Sci. 120:2706-2716. (Pubitemid 47323877)
22. Lukas, C., J. Falck, J. Bartkova, J. Bartek, and J. Lukas. 2003. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5:255-260. (Pubitemid 36322254)
23. Maison, C., and G. Almouzni. 2004. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5:296-304. (Pubitemid 38480610)
24. Maison, C., D. Bailly, A.H. Peters, J.P. Quivy, D. Roche, A. Taddei, M. Lachner, T. Jenuwein, and G. Almouzni. 2002. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30:329-334.
25. Mari, P.O., B.I. Florea, S.P. Persengiev, N.S. Verkaik, H.T. Bruggenwirth, M. Modesti, G. Giglia-Mari, K. Bezstarosti, J.A. Demmers, T.M. Luider, et al. 2006. Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc. Natl. Acad. Sci. USA. 103:18597-18602.
26. Mateescu, B., B. Bourachot, C. Rachez, V. Ogryzko, and C. Muchardt. 2008. Regulation of an inducible promoter by an HP1beta-HP1gamma switch. EMBO Rep. 9:267-272.
27. Mateos-Langerak, J., M.C. Brink, M.S. Luijsterburg, I. van der Kraan, R. van Driel, and P.J. Verschure. 2007. Pericentromeric heterochromatin domains are maintained without accumulation of HP1. Mol. Biol. Cell. 18:1464-1471. (Pubitemid 46626641)
28. Moné, M.J., M. Volker, O. Nikaido, L.H. Mullenders, A.A. van Zeeland, P.J. Verschure, E.M. Manders, and R. van Driel. 2001. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep. 2:1013-1017. (Pubitemid 33130608)
29. Moné, M.J., T. Bernas, C. Dinant, F.A. Goedvree, E.M. Manders, M. Volker, A.B. Houtsmuller, J.H. Hoeijmakers, W. Vermeulen, and R. van Driel. 2004. In vivo dynamics of chromatin-associated complex formation in mammalian nucleotide excision repair. Proc. Natl. Acad. Sci. USA. 101:15933-15937. (Pubitemid 39507905)
30. Nielsen, A.L., M. Oulad-Abdelghani, J.A. Ortiz, E. Remboutsika, P. Chambon, and R. Losson. 2001. Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. Mol. Cell. 7:729-739. (Pubitemid 32436434)
31. Nielsen, A.L., C. Sanchez, H. Ichinose, M. Cervino, T. Lerouge, P. Chambon, and R. Losson. 2002. Selective interaction between the chromatin-remodeling factor BRG1 and the heterochromatin-associated protein HP1alpha. EMBO J. 21:5797-5806. (Pubitemid 35315277)
32. O'Driscoll, M., V.L. Ruiz-Perez, C.G. Woods, P.A. Jeggo, and J.A. Goodship. 2003. A splicing mutation affecting expression of ataxia- telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 33:497-501. (Pubitemid 36390012)
33. O'Neil, N., and A. Rose. 2006. DNA repair. WormBook. 13:1-12.
34. Peters, A.H., D. O'Carroll, H. Scherthan, K. Mechtler, S. Sauer, C. Schofer, K. Weipoltshammer, M. Pagani, M. Lachner, A. Kohlmaier, et al. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell. 107:323-337. (Pubitemid 33049976)
35. Polo, S.E., D. Roche, and G. Almouzni. 2006. New histone incorporation marks sites of UV repair in human cells. Cell. 127:481-493. (Pubitemid 44647423)
36. Quivy, J.P., A. Gerard, A.J. Cook, D. Roche, and G. Almouzni. 2008. The HP1-p150/CAF-1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nat. Struct. Mol. Biol. 15:972-979.
37. Schmiedeberg, L., K. Weisshart, S. Diekmann, G. Meyer Zu Hoerste, and P. Hemmerich. 2004. High- and low-mobility populations of HP1 in heterochromatin of mammalian cells. Mol. Biol. Cell. 15:2819-2833. (Pubitemid 38691870)
38. Schott, S., V. Coustham, T. Simonet, C. Bedet, and F. Palladino. 2006. Unique and redundant functions of C. elegans HP1 proteins in post-embryonic development. Dev. Biol. 298:176-187. (Pubitemid 44414803)
39. Schotta, G., M. Lachner, K. Sarma, A. Ebert, R. Sengupta, G. Reuter, D. Reinberg, and T. Jenuwein. 2004. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18:1251-1262. (Pubitemid 38720593)
40. Solimando, L., M.S. Luijsterburg, L. Vecchio, W. Vermeulen, R. van Driel, and S. Fakan. 2009. Spatial organization of nucleotide excision repair proteins after UV-induced DNA damage in the human cell nucleus. J. Cell Sci. 122:83-91.
41. Song, K., Y. Jung, D. Jung, and I. Lee. 2001. Human Ku70 interacts with heterochromatin protein 1alpha. J. Biol. Chem. 276:8321-8327. (Pubitemid 37385642)
42. Stap, J., P.M. Krawczyk, C.H. Van Oven, G.W. Barendsen, J. Essers, R. Kanaar, and J.A. Aten. 2008. Induction of linear tracks of DNA double-strand breaks by alpha-particle irradiation of cells. Nat. Methods. 5:261-266.
43. Stergiou, L., K. Doukoumetzidis, A. Sendoel, and M.O. Hengartner. 2007. The nucleotide excision repair pathway is required for UV-C-induced apoptosis in Caenorhabditis elegans. Cell Death Differ. 14:1129-1138. (Pubitemid 46785104)
44. Syljuasen, R.G., C.S. Sorensen, J. Nylandsted, C. Lukas, J. Lukas, and J. Bartek. 2004. Inhibition of Chk1 by CEP-3891 accelerates mitotic nuclear fragmentation in response to ionizing radiation. Cancer Res. 64:9035-9040. (Pubitemid 39665514)
45. van Haaften, G., R. Romeijn, J. Pothof, W. Koole, L.H. Mullenders, A. Pastink, R.H. Plasterk, and M. Tijsterman. 2006. Identification of conserved pathways of DNA-damage response and radiation protection by genome-wide RNAi. Curr. Biol. 16:1344-1350. (Pubitemid 43975370)
46. van Hoffen, A., J. Venema, R. Meschini, A.A. van Zeeland, and L.H. Mullenders. 1995. Transcription-coupled repair removes both cyclobutane pyrimidine dimers and 6-4 photoproducts with equal efficiency and in a sequential way from transcribed DNA in xeroderma pigmentosum group C fibroblasts. EMBO J. 14:360-367.
47. Volker, M., M.J. Moné, P. Karmakar, A. van Hoffen, W. Schul, W. Vermeulen, J.H. Hoeijmakers, R. van Driel, A.A. van Zeeland, and L.H. Mullenders. 2001. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell. 8:213-224. (Pubitemid 32772919)
48. Wreggett, K.A., F. Hill, P.S. James, A. Hutchings, G.W. Butcher, and P.B. Singh. 1994. A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet. Cell Genet. 66:99-103. (Pubitemid 24042839)
49. Wyman, C., and R. Kanaar. 2006. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40:363-383.
50. Zotter, A., M.S. Luijsterburg, D.O. Warmerdam, S. Ibrahim, A. Nigg, W.A. van Cappellen, J.H. Hoeijmakers, R. van Driel, W. Vermeulen, and A.B. Houtsmuller. 2006. Recruitment of the nucleotide excision repair endonuclease XPG to sites of UV-induced DNA damage depends on functional TFIIH. Mol. Cell. Biol. 26:8868-8879.