HMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells

Molecular and Cellular Biology

Volumn 25, Issue 15, 2005, Pages 6798-6810

  Taipale, Mikko ^a   Rea, Stephen ^a   Richter, Karsten ^b   Vilar, Ana ^c,d   Lichter, Peter ^b   Imhof, Axel ^c   Akhtar, Asifa ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

^d Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; HISTONE ACETYLTRANSFERASE; HISTONE H4; HISTONE H4 LYSINE K16 SPECIFIC ACETYLTRANSFERASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CELL CYCLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ASSAY; HELA CELL; HEPATOMA CELL; HUMAN; HUMAN CELL; MAMMAL CELL; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE;

ACETYLATION; ACETYLTRANSFERASES; CELL DIVISION; CELL LINE, TUMOR; CELL NUCLEUS; DNA DAMAGE; DOSAGE COMPENSATION, GENETIC; DROSOPHILA PROTEINS; G2 PHASE; HELA CELLS; HISTONE ACETYLTRANSFERASES; HISTONES; HUMANS; LYSINE; NUCLEAR PROTEINS; RECOMBINANT PROTEINS;

DROSOPHILA MELANOGASTER; MAMMALIA;

EID: 22544480772     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.15.6798-6810.2005     Document Type: Article

References (60)

1. Akhtar, A. 2003. Dosage compensation: an intertwined world of RNA and chromatin remodelling. Curr. Opin. Genet. Dev. 13:161-169.
2. Akhtar, A., and P. B. Becker. 2000. Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol. Cell 5:367-375.
3. Akhtar, A., and P. B. Becker. 2001. The histone H4 acetyltransferase MOF uses a C2HC zinc finger for substrate recognition. EMBO Rep. 2:113-118.
4. Akhtar, A., D. Zink, and P. B. Becker. 2000. Chromodomains are protein-RNA interaction modules. Nature 407:405-409.
5. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506.
6. Bonaldi, T., A. Imhof, and J. T. Regula. 2004. A combination of different mass spectroscopic techniques for the analysis of dynamic changes of histone modifications. Proteomics 4:1382-1396.
7. Bonaldi, T., J. T. Regula, and A. Imhof. 2004. The use of mass spectrometry for the analysis of histone modifications. Methods Enzymol. 377:111-130.
8. Bone, J. R., J. Lavender, R. Richman, M. J. Palmer, B. M. Turner, and M. I. Kuroda. 1994. Acetylated histone H4 on the male X chromosome is associated with dosage compensation in Drosophila. Genes Dev. 8:96-104.
9. Broers, J. L., E. A. Peeters, H. J. Kuijpers, J. Endert, C. V. Bouten, C. W. Oomens, F. P. Baaijens, and F. C. Ramaekers. 2004. Decreased mechanical stiffness in LMNA-/- cells is caused by defective nucleo-cytoskeletal integrity. Implications for the development of laminopathies. Hum. Mol. Genet. 13: 2567-2580.
10. Bulavin, D. V., S. A. Amundson, and A. J. Fornace. 2002. p38 and Chk1 kinases: different conductors for the G(2)/M checkpoint symphony. Curr. Opin. Genet. Dev. 12:92-97.
11. Buscaino, A., T. Kocher, J. H. Kind, H. Holz, M. Taipale, K. Wagner, M. Wilm, and A. Akhtar. 2003. MOF-regulated acetylation of MSL-3 in the Drosophila dosage compensation complex. Mol. Cell 11:1265-1277.
12. Carrozza, M. J., R. T. Utley, J. L. Workman, and J. Cote. 2003. The diverse functions of histone acetyltransferase complexes. Trends Genet. 19:321-329.
13. Clarke, A. S., J. E. Lowell, S. J. Jacobson, and L. Pillus. 1999. Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol. Cell. Biol. 19:2515-2526.
14. Copps, K., R. Richman, L. M. Lyman, K. A. Chang, J. Rampersad-Ammons, and M. I. Kuroda. 1998. Complex formation by the Drosophila MSL proteins: role of the MSL2 RING finger in protein complex assembly. EMBO J. 17:5409-5417.
15. Cormier, T. A., S. K. Prakash, D. B. Magner, H. Y. Zoghbi, and I. B. Van den Veyver. 2001. Analysis of Mid1, Hccs, Arhgap6, and Msl311 in X-linked polydactyly (Xpl) and Patchy-fur (Paf) mutant mice. Mamm. Genome 12: 796-798.
16. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
17. Fraga, M. F., E. Ballestar, A. Villar-Garea, M. Boix-Chornet, J. Espada, G. Schotta, T. Bonaldi, C. Haydon, S. Ropero, K. Petrie, N. G. Iyer, A. Perez-Rosado, E. Calvo, J. A. Lopez, A. Cano, M. J. Calasanz, D. Colomer, M. A. Piris, N. Ahn, A. Imhof, C. Caldas, T. Jenuwein, and M. Esteller. 2005. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 37:391-400.
18. Hagstrom, K. A., and B. J. Meyer. 2003. Condensin and cohesin: more than chromosome compactor and glue. Nat. Rev. Genet. 4:520-534.
19. Hilfiker, A., D. Hilfiker-Kleiner, A. Pannuti, and J. C. Lucchesi. 1997. mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila. EMBO J. 16:2054-2060.
20. Hoffmann, K., C. K. Dreger, A. L. Olins, D. E. Olins, L. D. Shultz, B. Lucke, H. Karl, R. Kaps, D. Muller, A. Vaya, J. Aznar, R. E. Ware, N. Sotelo Cruz, T. H. Lindner, H. Herrmann, A. Reis, and K. Sperling. 2002. Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huet anomaly). Nat. Genet. 31:410-414.
21. Huyen, Y., O. Zgheib, R. A. Ditullio, Jr., V. G. Gorgoulis, P. Zacharatos, T. J. Petty, E. A. Sheston, H. S. Meliert, E. S. Stavridi, and T. D. Halazonetis. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406-411.
22. Imai, S., C. M. Armstrong, M. Kaeberlein, and L. Guarente. 2000. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403:795-800.
23. Jazayeri, A., A. D. McAinsh, and S. P. Jackson. 2004. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 101:1644-1649.
24. Kurdistani, S. K., S. Tavazoie, and M. Grunstein. 2004. Mapping global histone acetylation patterns to gene expression. Cell 117:721-733.
25. Kusch, T., L. Florens, W. H. Macdonald, S. K. Swanson, R. L. Glaser, J. R. Yates III, S. M. Abmayr, M. P. Washburn, and J. L. Workman. 2004. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306:2084-2087.
26. Marin, I. 2003. Evolution of chromatin-remodeling complexes: comparative genomics reveals the ancient origin of "novel" compensasome genes. J. Mol. Evol. 56:527-539.
27. Marin, I., and B. S. Baker. 2000. Origin and evolution of the regulatory gene male-specific lethal-3. Mol. Biol. Evol. 17:1240-1250.
28. Marin, I., M. L. Siegal, and B. S. Baker. 2000. The evolution of dosage-compensation mechanisms. Bioessays 22:1106-1114.
29. Megee, P. C., B. A. Morgan, B. A. Mittman, and M. M. Smith. 1990. Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science 247:841-845.
30. Megee, P. C., B. A, Morgan, and M. M. Smith. 1995. Histone H4 and the maintenance of genome integrity. Genes Dev. 9:1716-1727.
31. Morales, V., T. Straub, M. F. Neumann, G. Mengus, A. Akhtar, and P. B. Becker. 2004. Functional integration of the histone acetyltransferase MOF into the dosage compensation complex. EMBO J. 23:2258-2268.
32. Munks, R. J., J. Moore, L. P. O'Neill, and B. M. Turner. 1991. Histone H4 acetylation in Drosophila. Frequency of acetylation at different sites defined by immunolabelling with site-specific antibodies. FEBS Lett. 284:245-248.
33. Nakayama, Y., and N. Yamaguchi. 2005. Multi-lobulation of the nucleus in prolonged S phase by nuclear expression of Chk tyrosine kinase. Exp. Cell Res. 304:570-581.
34. Neal, K. C., A. Pannuti, E. R. Smith, and J. C. Lucchesi. 2000. A new human member of the MYST family of histone acetyl transferases with high sequence similarity to Drosophila MOF. Biochim. Biophys. Acta 1490:170-174.
35. Otte, A. P., and T. H. Kwaks. 2003. Gene repression by Polycomb group protein complexes: a distinct complex for every occasion? Curr. Opin. Genet. Dev. 13:448-454.
36. Pardo, P. S., J. K. Leung, J. C. Lucchesi, and O. M. Pereira-Smith. 2002. MRG15, a novel chromodomain protein, is present in two distinct multiprotein complexes involved in transcriptional activation. J. Biol. Chem. 277: 50860-50866.
37. Park, E. J., D. W. Chan, J. H. Park, M. A. Oettinger, and J. Kwon. 2003. DNA-PK is activated by nucleosomes and phosphorylates H2AX within the nucleosomes in an acetylation-dependent manner. Nucleic Acids Res. 31: 6819-6827.
38. Peters, A. H., S. Kubicek, K. Mechtler, R. J. O'Sullivan, A. A. Derijck, L. Perez-Burgos, A. Kohlmaier, S. Opravil, M. Tachibana, Y. Shinkai, J. H. Martens, and T. Jenuwein. 2003. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12:1577-1589.
39. Prakash, S. K., I. B. Van den Veyver, B. Franco, M. Volta, A. Ballabio, and H. Y. Zoghbi. 1999. Characterization of a novel chromodomain gene in xp22.3 with homology to Drosophila msl-3. Genomics 59:77-84.
40. Richter, K., M. Reichenzeller, S. Gorisch, U. Schmidt, M. O. Scheuermann, H. Herrmann, and P. Lichter. 2005. Characterization of a nuclear compartment shared by nuclear bodies applying ectopic protein expression and correlative light and electron microscopy. Exp. Cell Res. 303:128-137.
41. Roth, S. Y., J. M. Denu, and C. D. Allis. 2001. Histone acetyltransferases. Annu. Rev. Biochem. 70:81-120.
42. Salina, D., P. Enarson, J. B. Rattner, and B. Burke. 2003. Nup358 integrates nuclear envelope breakdown with kinetochore assembly. J. Cell Biol. 162: 991-1001.
43. Sancar, A., L. A. Lindsey-Boltz, K. Unsal-Kaccmaz, and S. Linn. 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39-85.
44. Sanders, S. L., M. Portoso, J. Mata, J. Bahler, R. C. Allshire, and T. Kouzarides. 2004. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603-614.
45. Sanjuan, R., and I. Marin. 2001. Tracing the origin of the compensasome: evolutionary history of DEAH helicase and MYST acetyltransferase gene families. Mol. Biol. Evol. 18:330-343.
46. Sarkaria, J. N., E. C. Busby, R. S. Tibbetts, P. Roos, Y. Taya, L. M. Karnitz, and R. T. Abraham. 1999. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59:4375-4382.
47. Sarkaria, J. N., R. S. Tibbetts, E. C. Busby, A. P. Kennedy, D. E. Hill, and R. T. Abraham. 1998. Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res. 58:4375-4382.
48. Shroff, R., A. Arbel-Eden, D. Pilch, G. Ira, W. M. Bonner, J. H. Petrini, J. E. Haber, and M. Lichten. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14: 1703-1711.
49. Smith, C. M., P. R. Gafken, Z. Zhang, D. E. Gottschling, J. B. Smith, and D. L. Smith. 2003. Mass spectrometric quantification of acetylation at specific lysines within the amino-terminal tail of histone H4. Anal. Biochem. 316:23-33.
50. Smith, E. R., A. Eisen, W. Gu, M. Sattah, A. Pannuti, J. Zhou, R. G. Cook, J. C. Lucchesi, and C. D. Allis. 1998. ESA1 is a histone acetyltransferase that is essential for growth in yeast. Proc. Natl. Acad. Sci. USA 95:3561-3565.
51. Smith, E. R., A. Pannuti, W. Gu, A. Steurnagel, R. G. Cook, C. D. Allis, and J. C. Lucchesi. 2000. The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol. Cell. Biol. 20:312-318.
52. Suka, N., K. Luo, and M. Grunstein. 2002. Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of hetero-chromatin. Nat. Genet. 32:378-383.
53. Thorne, A. W., D. Kmiciek, K. Mitchelson, P. Sautiere, and C. Crane-Robinson. 1990. Patterns of histone acetylation. Eur. J. Biochem. 193:701-713.
54. Turner, B. M. 2002. Cellular memory and the histone code. Cell 111:285-291.
55. Turner, B. M., L. P. O'Neill, and I. M. Allan. 1989. Histone H4 acetylation in human cells. Frequency of acetylation at different sites defined by immunolabeling with site-specific antibodies. FEBS Lett. 253:141-145.
56. Utley, R. T., and J. Cote. 2003. The MYST family of histone acetyltransferases. Curr. Top. Microbiol. Immunol. 274:203-236.
57. Vaquero, A., M. Scher, D. Lee, H. Erdjument-Bromage, P. Tempst, and D. Reinberg. 2004. Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol. Cell 16:93-105.
58. Weinert, T. A., and L. H. Hartwell. 1988. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241: 317-322.
59. Yan, Y., N. A. Barlev, R. H. Haley, S. L. Berger, and R. Marmorstein. 2000. Crystal structure of yeast Esa1 suggests a unified mechanism for catalysis and substrate binding by histone acetyltransferases. Mol. Cell 6:1195-1205.
60. Yan, Y., S. Harper, D. W. Speicher, and R. Marmorstein. 2002. The catalytic mechanism of the ESA1 histone acetyltransferase involves a self-acetylated intermediate. Nat. Struct. Biol. 9:862-869.