A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16

Molecular and Cellular Biology

Volumn 25, Issue 21, 2005, Pages 9175-9188

  Smith, Edwin R ^a,b   Cayrou, Christelle ^c   Huang, Rong ^a   Lane, William S ^d   Côté, Jacques ^c   Lucchesi, John C ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LAVAL UNIVERSITY   (Canada)

^d HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE ACETYLTRANSFERASE; HISTONE H4; LYSINE; PROTEIN HMSL; PROTEIN HMSL1V1; PROTEIN HMSL3; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CARCINOGENESIS; CELL CYCLE; CELL CYCLE G2 PHASE; CELL STRAIN K 562; CHROMATIN; COMPLEX FORMATION; HELA CELL; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAJI CELL; RNA INTERFERENCE; TRANSCRIPTION REGULATION;

ACETYLATION; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; CELL CYCLE; CHROMATIN; DNA-BINDING PROTEINS; DROSOPHILA PROTEINS; HISTONE ACETYLTRANSFERASES; HISTONES; HOST FACTOR 1 PROTEIN; HUMANS; LYSINE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

EID: 27144546434     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.21.9175-9188.2005     Document Type: Article

References (70)

1. 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.
2. Akhtar, A., D. Zink, and P. B. Becker. 2000. Chromodomains are protein-RNA interaction modules. Nature 407:405-409.
3. Amrein, H., and R. Axel. 1997. Genes expressed in neurons of adult male Drosophila. Cell 88:459-469.
4. Belote, J. M., and J. C. Lucchesi. 1980. Control of X chromosome transcription by the maleless gene in Drosophila. Nature 285:573-575.
5. Belote, J. M., and J. C. Lucchesi. 1980. Male-specific lethal mutations of Drosophila melanogaster. Genetics 96:165-186.
6. Bertram, M. J., N. G. Beruhe, X. Hang-Swanson, Q. Ran, J. K. Leung, S. Bryce, K. Spurgers, R. J. Bick, A. Baldini, Y. Ning, L. J. Clark, E. K. Parkinson, J. C. Barrett, J. R. Smith, and O. M. Pereira-Smith. 1999. Identification of a gene that reverses the immortal phenotype of a subset of cells and is a member of a novel family of transcription factor-like genes. Mol. Cell. Biol. 19:1479-1485.
7. Bertram, M. J., and O. M. Pereira-Smith. 2001. Conservation of the MORF4 related gene family: identification of a new chromo domain subfamily and novel protein motif. Gene 266:111-121.
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. Brehm, A., K. R. Tufteland, R. Aasland, and P. B. Becker. 2004. The many colours of chromodomains. Bioessays 26:133-140.
10. Cai, Y., J. Jin, L. Florens, S. K. Swanson, T. Kusch, B. Li, J. L. Workman, M. P. Washburn, R. C. Conaway, and J. W. Conaway. 2005. The mammalian YLl protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J. Biol. Chem. 280:13665-13670.
11. Cai, Y., J. Jin, C. Tomomori-Sato, S. Sato, I. Sorokina, T. J. Parmely, R. C. Conaway, and J. W. Conaway. 2003. Identification of new subunits of the multiprotein mammalian TRRAP/TIP60-containing histone acetyltransferase complex. J. Biol. Chem. 278:42733-42736.
12. 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.
13. Corona, D. F., C. R. Clapier, P. B. Becker, and J. W. Tamkun. 2002. Modulation of ISWI function by site-specific histone acetylation. EMBO Rep. 3:242-247.
14. Cote, J., R. T. Utley, and J. L. Workman. 1995. Basic analysis of transcription factor binding to nucleosomes. Methods Mol. Genet. 6:108-128.
15. Deng, H., W. Zhang, X. Bao, J. N. Martin, J. Girton, J. Johansen, and K. M. Johansen. 29 June 2005. The JIL-1 kinase regulates the structure of Drosophila polytene chromosomes. Chromosoma 10.1007/s00412-005-0006-8.
16. Dion, M. F., S. J. Altschuler, L. F. Wu, and O. J. Rando. 2005. Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl. Acad. Sci. USA 102:5501-5506.
17. Dorigo, B., T. Schalch, K. Bystricky, and T. J. Richmond. 2003. Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J. Mol. Biol. 327:85-96.
18. Dou, Y., T. A. Milne, A. J. Tackelt, E. R. Smith, A. Fukuda, J. Wysocka, C. D. Allis, B. T. Chait, J. L. Hess, and R. G. Roeder. 2005. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121:873-885.
19. Doyon, Y., and J. Cote. 2004. The highly conserved and multifunctional NuA4 HAT complex. Curr. Opin. Genet. Dev. 14:147-154.
20. Doyon, Y., W. Selleck, W. S. Lane, S. Tan, and J. Cote. 2004. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol. Cell. Biol. 24:1884-1896.
21. Eisen, A., R. T. Utley, A. Nourani, S. Allard, P. Schmidt, W. S. Lane, J. C. Lucchesi, and J. Cote. 2001. The yeast NuA4 and Drosophila MSL complexes contain homologous subunits important for transcription regulation. J. Biol. Chem. 276:3484-3491.
22. 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.
23. Goto, H., S. Motomura, A. C. Wilson, R. N. Freiman, Y. Nakabeppu, K. Fukushima, M. Fujishima, W. Herr, and T. Nishimoto. 1997. A single-point mutation in HCF causes temperature-sensitive cell-cycle arrest and disrupts VP16 function. Genes Dev. 11:726-737.
24. Gu, W., X. Wei, A. Pannuti, and J. C. Lucchesi. 2000. Targeting the chromatin-remodeling MSL complex of Drosophila to its sites of action on the X chromosome requires both acetyl transferase and ATPase activities. EMBO J. 19:5202-5211.
25. Gupta, A., G. G. Sharma, C. S. Young, M. Agarwal, E. R. Smith, T. T. Paull, J. C. Lucchesi, K. K. Khanna, T. Ludwig, and T. K. Pandita. 2005. Involvement of human MOF in ATM function. Mol. Cell. Biol. 25:5292-5305.
26. 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.
27. Jacobs, S. A., and S. Khorasanizadeh. 2002. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295:2080-2083.
28. Jeppesen, P., and B. M. Turner. 1993. The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74:281-289.
29. Jin, Y., Y. Wang, J. Johansen, and K. M. Johansen. 2000. JIL-1, a chromosomal kinase implicated in regulation of chromatin structure, associates with the male specific lethal (MSL) dosage compensation complex. J. Cell Biol. 149:1005-1010.
30. Kelley, R. L. 2004. Path to equality strewn with roX. Dev. Biol. 269:18-25.
31. Kelley, R. L., V. H. Meller, P. R. Gordadze, G. Roman, R. L. Davis, and M. I. Kuroda. 1999. Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin. Cell 98:513-522.
32. Kimura, A., T. Umehara, and M. Horikoshi. 2002. Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat. Genet. 32:370-377.
33. Komberg, R. D., and Y. Lorch. 1999. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285-294.
34. Kurdistani, S. K., S. Tavazoie, and M. Grunstein. 2004. Mapping global histone acetylation patterns to gene expression. Cell 117:721-733.
35. Lavender, J. S., A, J. Birley, M. J. Palmer, M. I. Kuroda, and B. M. Turner. 1994. Histone H4 acetylated at lysine 16 and proteins of the Drosophila dosage compensation pathway co-localize on the male X chromosome through mitosis. Chromosome Res. 2:398-404.
36. Lembo, D., M. Donalisio, A. Hofer, M. Cornaglia, W. Brune, U. Koszinowski, L. Thelander, and S. Landolfo. 2004. The ribonucleotide reductase R1 homolog of murine cytomegalovirus is not a functional enzyme subunit but is required for pathogenesis. J. Virol. 78:4278-4288.
37. Marin, I. 2003. Evolution of chromatin-remodeling complexes: comparative genomics reveals the ancient origin of "novel" compensasome genes. J. Mol. Evol. 56:527-539.
38. McMahon, S. J., Y. Doyon, J. Cote, and P. A. Grant. 2004. Identification and analysis of native HAT complexes. Methods Enzymol. 377:154-167.
39. Meller, V. H., K. H. Wu, G. Roman, M. I. Kuroda, and R. L. Davis. 1997. roX1 RNA paints the X chromosome of male Drosophila and is regulated by the dosage compensation system. Cell 88:445-457.
40. Morales, V., C. Regnard, A. Izzo, I. Vetter, and P. B. Becker. 2005. The MRG domain mediates the functional integration of MSL3 into the dosage compensation complex. Mol. Cell. Biol. 25:5947-5954.
41. 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.
42. 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.
43. Nielsen, P. R., D. Nietlispach, A. Buscaino, R. J. Warner, A. Akhtar, A. G. Murzin, N. V. Murzina, and E. D. Laue. 2005. Structure of the chromo barrel domain from the MOF acetyl-transferase. J. Biol. Chem.
44. Ohha, R., D. J. Steger, J. E. Brownell, C. A. Mizzen, R. G. Cook, J. Cote, J. L. Workman, and C. D. Allis. 1999. A novel H2A/H4 nucleosomal histone acetyltransferase in Tetrahymena thermophila. Mol. Cell. Biol. 19:2061-2068.
45. Pannuti, A., and J. C. Lucchesi. 2000. Recycling to remodel: evolution of dosage-compensation complexes. Curr. Opin. Genet. Dev. 10:644-650.
46. 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.
47. Park, Y., G. Mengus, X. Bai, Y. Kageyama, V. H. Meller, P. B. Becker, and M. I. Kuroda. 2003. Sequence-specific targeting of Drosophila roX genes by the MSL dosage compensation complex. Mol. Cell 11:977-986.
48. Peterson, C. L., and M. A. Laniel. 2004. Histones and histone modifications. Curr. Biol. 14:R546-R551.
49. Prakash, S. K., I. B. Van den Veyver, B. Franco, M. Volta, A. Ballabio, and H. Y. Zoghbi. 1999. Characterization of a novel chromo domain gene in xp22.3 with homology to Drosophila msl-3. Genomics 59:77-84.
50. Reid, J. L., Z. Moqtaderi, and K. Struhl. 2004. Eaf3 regulates the global pattern of histone acetylation in Saccharomyces cerevisiae. Mol. Cell. Biol. 24:757-764.
51. Rice, J. C., K. Nishioka, K. Sarma, R. Steward, D. Reinberg, and C. D. Allis. 2002. Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes Dev. 16:2225-2230.
52. Richter, L., J. R. Bone, and M. I. Kuroda. 1996. RNA-dependent association of the Drosophila maleless protein with the male X chromosome. Genes Cells 1:325-336.
53. Sass, G. L., A. Pannuti, and J. C. Lucchesi. 2003. Male-specific lethal complex of Drosophila targets activated regions of the X chromosome for chromatin remodeling. Proc. Natl. Acad. Sci. USA 100:8287-8291.
54. Scott, M. J., L. L. Pan, S. B. Cleland, A. L. Knox, and J. Heinrich. 2000. MSL1 plays a central role in assembly of the MSL complex, essential for dosage compensation in Drosophila. EMBO J. 19:144-155.
55. Smith, E. R., C. D. Allis, and J. C. Lucchesi. 2001. Linking global histone acetylation to the transcription enhancement of X-chromosomal genes in Drosophila males. J. Biol. Chem. 276:31483-31486.
56. 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.
57. Sobel, R. E., R. G. Cook, and C. D. Allis. 1994. Nonrandom acetylation of histone H4 by a cytoplasmic histone acetyltransferase as determined by novel methodology. J. Biol. Chem. 269:18576-18582.
58. Strahl, B. D., P. A. Grant, S. D. Briggs, Z.W. Sun, J. R. Bone, J. A. Caldwell, S. Mollah, R. G. Cook, J. Shabanowitz, D. F. Hunt, and C. D. Allis. 2002. Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol. Cell. Biol. 22:1298-1306.
59. Suka, N., K. Luo, and M. Grunstein. 2002. Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine 16 and spreading of heterochromatin. Nat. Genet. 32:378-383.
60. Tominaga, K., J. K. Leung, P. Rookard, J. Echigo, J. R. Smith, and O. M. Pereira-Smith. 2003. MRGX is a novel transcriptional regulator that exhibits activation or repression of the B-myb promoter in a cell type-dependent manner. J. Biol. Chem. 278:49618-49624.
61. Turner, B. M., A. J. Birley, and J. Lavender. 1992. Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69:375-384.
62. Utley, R. T., and J. Cote. 2003. The MYST family of histone acetyltransferases. Curr. Top. Microbiol. Immunol. 274:203-236.
63. Wang, Y., W. Zhang, Y. Jin, J. Johansen, and K. M. Johansen. 2001. The JIL-1 tandem kinase mediates histone H3 phosphorylation and is required for maintenance of chromatin structure in Drosophila. Cell 105:433-443.
64. Wysocka, J., and W. Herr. 2003. The herpes simplex virus VP16-induced complex: the makings of a regulatory switch. Trends Biochem. Sci. 28:294-304.
65. Wysocka, J., M. P. Myers, C. D. Laherty, R. N. Eisenman, and W. Herr. 2003. Human Sin3 deacetylase and trithorax-related Set1/Ash2 histone H3-K4 methyltransferase are tethered together selectively by the cell-proliferation factor HCF-1. Genes Dev. 17:896-911.
66. 2/M checkpoints are induced by ionizing irradiation. Mol. Cell. Biol. 22:1049-1059.
67. Yochum, G. S., and D. E. Ayer. 2002. Role for the mortality factors MORF4, MRGX, and MRG15 in transcriptional repression via associations with Pf1, mSin3A, and transducin-like enhancer of split. Mol. Cell. Biol. 22:7868-7876.
68. Yokohama, A., Z. Wang, J. Wysocka, M. Sanyal, D. J. Aufiero, I. Kitabayashi, W. Herr, and M. L. Cleary. 2004. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol. Cell. Biol. 24:5639-5649.
69. Zhang, K., K. E. Williams, L. Huang, P. Yau, J. S. Siino, E. M. Bradbury, P. R. Jones, M. J. Minch, and A. L. Burlingame. 2002. Histone acetylation and deacetylation: identification of acetylation and methylation sites of HeLa histone H4 by mass spectrometry. Mol. Cell Proteomics 1:500-508.
70. Zhou, S., Y. Yang, M. J. Scott, A. Pannuti, K. C. Fehr, A. Eisen, E. V. Koonin, D. L. Fouts, R. Wrightsman, J. E. Manning, and J. C. Lucchesi. 1995. Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cysteine cluster. EMBO J. 14:2884-2895.