H2AX: Tailoring histone H2A for chromatin-dependent genomic integrity

Biochemistry and Cell Biology

Volumn 83, Issue 4, 2005, Pages 505-515

  Li, Andra ^a   Eirín López, José M ^a,b   Ausió, Juan ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF A CORUÑA   (Spain)

Author keywords

DNA repair; Double stranded DNA breaks; H2AX; Phosphorylation

Indexed keywords

BIOCHEMISTRY; CHEMICAL MODIFICATION; CHEMICALS; COMPLEXATION; IONIZING RADIATION; MOLECULAR BIOLOGY; PROTEINS;

DNA REPAIR; DOUBLE-STRANDED DNA BREAKS; H2AX; PHOSPHORYLATION;

GENES;

HISTONE H2A; HISTONE H2A1; HISTONE H2AX; SERINE; UNCLASSIFIED DRUG; HISTONE;

AMINO ACID SEQUENCE; CARBOXY TERMINAL SEQUENCE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONFERENCE PAPER; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; EUKARYOTE; GENOMICS; IONIZING RADIATION; MEIOSIS; NONHUMAN; PHYLOGENY; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; ANIMAL; GENETIC TRANSCRIPTION; GENETICS; GENOMIC INSTABILITY; HUMAN; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY; REVIEW; SEQUENCE HOMOLOGY;

EUKARYOTA;

AMINO ACID SEQUENCE; ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPAIR; GENOMIC INSTABILITY; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION, GENETIC;

EID: 27744485938     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o05-114     Document Type: Conference Paper

References (66)

1. Alvelo-Ceron, D., Niu, L., and Collart, D.G. 2000. Growth regulation of human variant histone genes and acetylation of the encoded proteins. Mol. Biol. Rep. 27: 61-71.
2. Arents, G., and Moudrianakis, E.N. 1995. The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. U.S.A. 92: 11170-11174.
3. Arnaudeau, C., Lundin, C., and Helleday, T. 2001. Replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol. 307: 1235-1245.
4. Ausió, J., and Abbott, D.W. 2002. The many tales of a tail: carboxyl-terminal tail heterogeneity specializes histone H2A variants for defined chromatin function. Biochemistry, 41: 5945-5949.
5. Ausió, J., and Abbott, D.W. 2004. The role of histone variability in chromatin stability and folding. In Chromatin structure and dynamics: state-of-the-art. Edited by J. Zlatanova and S.H. Leuba. Elsevier B.V. pp. 241-290.
6. Ausió, J., Abbott, D.W., Wang, X., and Moore, S.C. 2001. Histone variants and histone modifications: a structural perspective. Biochem. Cell Biol. 79: 693-708.
7. Bakkenist, C.J., and Kastan, M.B. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature (London), 421: 499-506.
8. Balajee, A.S., and Geard, C.R. 2004. Replication protein A and γ-H2AX foci assembly is triggered by cellular response to DNA double-strand breaks. Exp. Cell Res. 300: 320-334.
9. Bassing, C.H., Chua, K.F., Sekiguchi, J., Suh, H., Whitlow, S.R., Fleming, J.C. et al. 2002. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. U.S.A. 99: 8173-8178.
10. Bird, A.W., Yu, D.Y., Pray-Grant, M.G., Qiu, Q., Harmon, K.E., Megee, P.C. et al. 2002. Acetylation of histone H4 by Esa1 is required for DNA double-strand repair. Nature (London), 419: 411-415.
11. Boudreault, A.A., Cronier, D., Selleck, W., Lacoste, N., Utley, R.T., Allard, S. et al. 2003. Yeast enhancer of polycomb defines global Esa1-dependent acetylation of chromatin. Genes Dev. 17: 1415-1428.
12. Burma, S., Chen, B.P., Murphy, M., Kurimasa, A., and Chen, D.J. 2001. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276: 42462-42467.
13. Cairns, B.R. 2004. Around the world of DNA damage INO80 days. Cell, 119: 733-735.
14. Celeste, A., Petersen, S., Romanienko, P.J., Fernandez-Capetillo, O., Chen, H.T., Sedelnikova, O. et al. 2002. Genomic instability in mice lacking histone H2AX. Science (Wash. D.C.), 296: 922-927.
15. Celeste, A., Fernandez-Capetillo, O., Kruhlak, M.J., Pilch, D.R., Staudt, D.W., Lee, A. et al. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5: 675-679.
16. Chen, H.T., Bhandoola, A., Difilippantonio, M.J., Zhu, J., Brown, M.J., Tai, X. et al. 2000. Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. Science (Wash. D.C.), 290: 1962-1965.
17. Daniel, R., Ramcharan, J., Rogakou, E., Taganov, K.D., Greger, J.G., Bonner, W.M. et al. 2004. Histone H2AX is phosphorylated at sites of retroviral DNA integration but is dispensable for postintegration repair. J. Biol. Chem. 279: 45810-45814.
18. Downs, J.A., Lowndes, N.F., and Jackson, S.P. 2000. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature (London), 408: 1001.
19. Downs, J.A., Kosmidou, E., Morgan, A., and Jackson, S.P. 2003. Suppression of homologous recombination by the Saccharomyces cerevisiae linker histone. Mol. Cell, 11: 1685-1692.
20. Downs, J.A., Allard, S., Jobin-Robitaille, O., Javaheri, A., Auger, A., Bouchard, N. et al. 2004. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell, 16: 979-990.
21. Doyon, Y., Selleck, W., Lane, W.S., Tan, S., and Cote, J. 2004. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol. Cell Biol. 24: 1884-1896.
22. Drouet, J., Delteil, C., Lefrancois, J., Concannon, P., Salles, B., and Calsou, P. 2005. DNA-PK and XRCC4/DNA ligase IV mobilization in the cell in response to DNA double-strand breaks. J. Biol. Chem. 280(8): 7060-7069.
23. Fernandez-Capetillo, O., Chen, H., Celeste, A., Ward, I., Romanienko, P.J., Morales, J.C. et al. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4: 993-997.
24. Fernandez-Capetillo, O., Liebe, B., Scherthan, H., and Nussenzweig, A. 2003a. H2AX regulates meiotic telomere clustering. J. Cell Biol. 163: 15-20.
25. Fernandez-Capetillo, O., Mahadevaiah, S.K., Celeste, A., Romanienko, P.J., Camerini-Otero, R.D., Bonner, W.M. et al. 2003b. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell, 4: 497-508.
26. Fernandez-Capetillo, O., Allis, C.D., and Nussenzweig, A. 2004a. Phosphorylation of histone H2B at DNA double-strand breaks. J. Exp. Med. 199: 1671-1677.
27. Fernandez-Capetillo, O., Lee, A., Nussenzweig, M., and Nussenzweig, A. 2004b. H2AX: the histone guardian of the genome. DNA Repair, 3(8-9): 959-967.
28. Hamer, G., Roepers-Gajadien, H.L., van Duyn-Goedhart, A., Gademan, I.S., Kal, H.B., van Buul, P.P. et al. 2003. DNA double-strand breaks and gamma-H2AX signaling in the testis. Biol. Reprod. 68: 628-634.
29. Hao, L., Strong, M.A., and Gerider, C.W. 2004. Phosphorylation of H2AX at short telmoeres in T cells and fibroblasts. J. Biol. Chem. 279: 45148-45145.
30. Harvey, A.C., and Downs, J.A. 2004. What functions do linker histones provide? Mol. Microbiol. 53: 771-775.
31. Hunter, N., Borner, G.V., Lichten, M., and Kleckner, N. 2001. Gamma-H2AX illuminates meiosis. Nat. Genet. 27: 236-238.
32. Huyen, Y., Zgheib, O., DiTullio, R.A.J., Gorgoulis, V.G., Zacharatos, P., Petty, T.J. et al. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature (London), 432: 406-411.
33. Jackson, J.D., and Gorovsky, M.A. 2000. Histone H2A.Z has a conserved function that is distinct from that of the major H2A sequence variants. Nucleic Acids Res. 28: 3811-3816.
34. Kao, G.D., McKenna, W.G., Guenther, M.G., Muschel, R.J., Lazar, M.A., and Yen, T.J. 2003. Histone deacetylase 4 interacts with 53BP1 to mediate the DNA damage response. J. Cell Biol. 160: 1017-1027.
35. Krogh, B.O., and Symington, L.S. 2004. Recombination proteins in yeast. Annu. Rev. Genet. 38: 233-271.
36. Kurimasa, A., Ouyang, H., Dong, L., Wang, S., Li, X., Cordon-Cardo, C. et al. 1999. Catalytic subunit of DNA-dependent protein kinase: impact on lymphocyte development and tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 96: 1403-1408.
37. Kusch, T., Florens, L., MacDonald, W.H., Swanson, S.K., Glaser, R.L., Yates, J.R., III. et al. 2004. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science (Wash. D.C.), 306: 2084-2087.
38. Lewis, J.D., Abbott, D.W., and Ausió J. 2003. A haploid affair: core histone transitions during spermatogenesis. Biochem. Cell Biol. 81: 131-140.
39. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. 1997. Crystal structure of the nucleosome core particle at 2.8 resolution. Nature (London), 6648: 251-260.
40. Mahadevaiah, S.K., Turner, J.M., Baudat, F., Rogakou, E.P., de Boer, P., Blanco-Rodriguez, J. et al. 2001. Recombinational DNA double strand breaks in mice precede synapsis. Nat. Genet. 27: 271-276.
41. Malik, H.S., and Henikoff, S. 2003. Phylogenomics of the nucleosome. Nat. Struct. Biol. 10: 882-891.
42. Mannironi, C., Bonner, W.M., and Hatch, C.L. 1989. H2A.X, a histone isoprotein with a conserved C-terminal sequence, is encoded by a novel mRNA with both DNA replication type and polyA 3′ processing signals. Nucleic Acids Res. 17: 9113-9126.
43. Moore, J.D., and Krebs, J.E. 2004. Histone modifications and DNA double-strand break repair. Biochem. Cell Biol. 82: 446-452.
44. Morrison, A.J., Highland, J., Krogan, N.J., Arbel-Eden, A., Greenblatt, J.F., Haber, J.E. et al. 2004. INO80 and γ-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell, 119: 767-775.
45. Nazarov, I.B., Smirnova, A.N., Krutilina, R.I., Solovjeva, L.V., Nikiforov, A.A., Oei, S.-L. et al. 2003. Dephosphorylation of histone γ-H2AX during repair of DNA double-strand breaks in mammalian cells and its inhibition by calyculin A. Radiat. Res. 160: 309-317.
46. Park, E., Chan, D.W., Park, J., Oettinger, M.A., and Kwon, J. 2003. DNA-PK is activated by nucleosomes and phosphorylates H2AX within the nucleosomes in an acetylation-dependent manner. Nucleic Acids Res. 31: 6819-6827.
47. Paull, T.T., Rogakou, E.P., Yamazaki, V., Kirchgessner, C.U., Gellert, M., and Bonner, W.M. 2000. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10: 886-895.
48. Pilch, D.R., Sedelnikova, O., Redon, C., Celeste, A., Nussenzweig, A., and Bonner, W.M. 2003. Characteristics of γ-H2AX foci at DNA double-strand breaks sites. Biochem. Cell Biol. 81: 123-129.
49. Redon, C., Pilch, D.R., Rogakou, E.P., Sedelnikova, O., Newrock, K., and Bonner, W.M. 2002. Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12: 162-169.
50. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S., and Bonner, W.M. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273: 5858-5868.
51. Rogakou, E.P., Boon, C., Redon, C., and Bonner, W.M. 1999. Megabase chromatin domains involved in DNA double-stand breaks in vivo. J. Cell Biol. 146: 905-916.
52. Rogakou, E.P., Nieves-Neira, W., Boon, C., Pommier, Y., and Bonner, W.M. 2000. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J. Biol. Chem. 275: 9390-9395.
53. Sanders, S.L., Portoso, M., Mata, J., Bahler, J., Allshire, R.C., and Kouzarides, T. 2004. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell, 119: 603-614.
54. Scherthan, H. 2003. Knockout mice provide novel insights into meiotic chromosome and telomere dynamics. Cytogenet. Genome Res. 103: 235-244.
55. Schneider, T.D., and Stephens, R.M. 1990. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 18: 6097-6100.
56. Siino, J.S., Nazarov, I.B., Svetlova, M.P., Adamson, R.H., Zalenskaya, I.A., Yau, P.M. et al. 2002. Photobleaching of GFP-labeled H2AX in chromatin: H2AX has low diffusional mobility in the nucleus. Biochem. Biophys. Res. Commun. 297: 1318-1323.
57. Stewart, G.S., Wang, B., Bignell, C.R., Taylor, A.M.R., and Elledge, S.J. 2004. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature (London), 421: 961-966.
58. Stiff, T., O'Driscoll, M., Rief, N., Iwabuchi, K., Lobrich, M., and Jeggo, P.A. 2004. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64(7): 2390-2396.
59. Taylor, A.M.R., Groom, A., and Byrd, P.J. 2004. Ataxia-telangiectasia- like disorder (ATLD)-its clinical presentation and molecular basis. DNA Repair, 3: 1219-1225.
60. Thelestam, M., and Frisan, T. 2004. Cytolethal distending toxins. Rev. Physiol. Biochem. Pharmacol. 152: 111-133.
61. van Attikum, H., Fritsch, O., Hohn, B., and Gasser, S.M. 2004. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA doublestrand break repair. Cell, 119: 777-788.
62. Ward, I.M., and Chen, J. 2001. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replication stress. J. Biol. Chem. 276: 47759-47762.
63. Ward, I.M., Minn, K., Jorda, K.G., and Chen, J. 2003. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278: 19579-19582.
64. Wyatt, H.R., Liaw, H., Green, G.R., and Lustig, A.J. 2003. Multiple roles for Saccharomyces cerevisiae histone H2A in telomere position effect, Spt phenotypes and double-strand-break repair. Genetics, 164: 47-64.
65. Xu, Y., Ashley, T., Brainerd, E.E., Bronson, R.T., Meyn, M.S., and Baltimore, D. 1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10: 2411-2422.
66. Zimmerman, E.S., Chen, J., Andersen, J.L., Ardon, O., DeHart, J.L., Blackett, J. et al. 2004. Human immunodeficiency virus type 1 Vpr-mediated G2 arrest requires Rad17 and Hus1 and induces nuclear BRCA1 and γ-H2AX focus Formation. Mol. Cell. Biol. 24: 9286-9294.