This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Smith, E. R.
Right arrow Articles by Lucchesi, J. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Smith, E. R.
Right arrow Articles by Lucchesi, J. C.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, January 2000, p. 312-318, Vol. 20, No. 1
0270-7306/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

The Drosophila MSL Complex Acetylates Histone H4 at Lysine 16, a Chromatin Modification Linked to Dosage Compensation

Edwin R. Smith,1,2 Antonio Pannuti,1 Weigang Gu,1 Arnd Steurnagel,1 Richard G. Cook,3 C. David Allis,2 and John C. Lucchesi1,*

Department of Biology, Emory University, Atlanta, Georgia 303221; Department of Biochemistry and Molecular Genetics, University of Virginia H.S.C., Charlottesville, Virginia 229082; and Department of Microbiology and Immunology, Baylor College of Medicine, Houston, Texas 770303

Received 30 August 1999/Returned for modification 27 September 1999/Accepted 5 October 1999

In Drosophila, dosage compensation---the equalization of most X-linked gene products in males and females---is achieved by a twofold enhancement of the level of transcription of the X chromosome in males relative to each X chromosome in females. A complex consisting of at least five gene products preferentially binds the X chromosome at numerous sites in males and results in a significant increase in the presence of a specific histone isoform, histone 4 acetylated at lysine 16. Recently, RNA transcripts (roX1 and roX2) encoded by two different genes have also been found associated with the X chromosome in males. We have partially purified a complex containing MSL1, -2, and -3, MOF, MLE, and roX2 RNA and demonstrated that it exclusively acetylates H4 at lysine 16 on nucleosomal substrates. These results demonstrate that the MSL complex is responsible for the specific chromatin modification characteristic of the X chromosome in Drosophila males.

* Corresponding author. Mailing address: Department of Biology, Emory University, 1510 Clifton Rd., Atlanta, GA 30322. Phone: (404) 727-4234. Fax: (404) 727-2880. E-mail: Lucchesi{at}biology.emory.edu.

Molecular and Cellular Biology, January 2000, p. 312-318, Vol. 20, No. 1
0270-7306/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Menon, D. U., Meller, V. H. (2009). Imprinting of the Y Chromosome Influences Dosage Compensation in roX1 roX2 Drosophila melanogaster. Genetics 183: 811-820 [Abstract] [Full Text]  
  • Gorchakov, A. A., Alekseyenko, A. A., Kharchenko, P., Park, P. J., Kuroda, M. I. (2009). Long-range spreading of dosage compensation in Drosophila captures transcribed autosomal genes inserted on X. Genes Dev. 23: 2266-2271 [Abstract] [Full Text]  
  • Gelbart, M. E., Kuroda, M. I. (2009). Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136: 1399-1410 [Abstract] [Full Text]  
  • Patalano, S., Mihailovich, M., Belacortu, Y., Paricio, N., Gebauer, F. (2009). Dual sex-specific functions of Drosophila Upstream of N-ras in the control of X chromosome dosage compensation. Development 136: 689-698 [Abstract] [Full Text]  
  • Sun, B., Hong, J., Zhang, P., Dong, X., Shen, X., Lin, D., Ding, J. (2008). Molecular Basis of the Interaction of Saccharomyces cerevisiae Eaf3 Chromo Domain with Methylated H3K36. J. Biol. Chem. 283: 36504-36512 [Abstract] [Full Text]  
  • Park, S.-W., Kuroda, M. I., Park, Y. (2008). Regulation of Histone H4 Lys16 Acetylation by Predicted Alternative Secondary Structures in roX Noncoding RNAs. Mol. Cell. Biol. 28: 4952-4962 [Abstract] [Full Text]  
  • Ganesan, G., Rao, S. M.R. (2008). A novel noncoding RNA processed by Drosha is restricted to nucleus in mouse. RNA 14: 1399-1410 [Abstract] [Full Text]  
  • Li, F., Schiemann, A. H., Scott, M. J. (2008). Incorporation of the Noncoding roX RNAs Alters the Chromatin-Binding Specificity of the Drosophila MSL1/MSL2 Complex. Mol. Cell. Biol. 28: 1252-1264 [Abstract] [Full Text]  
  • Izzo, A., Regnard, C., Morales, V., Kremmer, E., Becker, P. B. (2008). Structure-function analysis of the RNA helicase maleless. Nucleic Acids Res 36: 950-962 [Abstract] [Full Text]  
  • Morra, R., Smith, E. R., Yokoyama, R., Lucchesi, J. C. (2008). The MLE Subunit of the Drosophila MSL Complex Uses Its ATPase Activity for Dosage Compensation and Its Helicase Activity for Targeting. Mol. Cell. Biol. 28: 958-966 [Abstract] [Full Text]  
  • Smith, E. R., Lee, M. G., Winter, B., Droz, N. M., Eissenberg, J. C., Shiekhattar, R., Shilatifard, A. (2008). Drosophila UTX Is a Histone H3 Lys27 Demethylase That Colocalizes with the Elongating Form of RNA Polymerase II. Mol. Cell. Biol. 28: 1041-1046 [Abstract] [Full Text]  
  • Gupta, A., Guerin-Peyrou, T. G., Sharma, G. G., Park, C., Agarwal, M., Ganju, R. K., Pandita, S., Choi, K., Sukumar, S., Pandita, R. K., Ludwig, T., Pandita, T. K. (2008). The Mammalian Ortholog of Drosophila MOF That Acetylates Histone H4 Lysine 16 Is Essential for Embryogenesis and Oncogenesis. Mol. Cell. Biol. 28: 397-409 [Abstract] [Full Text]  
  • Worringer, K. A., Panning, B. (2007). Zinc Finger Protein Zn72D Promotes Productive Splicing of the maleless Transcript. Mol. Cell. Biol. 27: 8760-8769 [Abstract] [Full Text]  
  • Yokoyama, R., Pannuti, A., Ling, H., Smith, E. R., Lucchesi, J. C. (2007). A Plasmid Model System Shows that Drosophila Dosage Compensation Depends on the Global Acetylation of Histone H4 at Lysine 16 and Is Not Affected by Depletion of Common Transcription Elongation Chromatin Marks. Mol. Cell. Biol. 27: 7865-7870 [Abstract] [Full Text]  
  • Park, S.-W., Kang, Y. I., Sypula, J. G., Choi, J., Oh, H., Park, Y. (2007). An Evolutionarily Conserved Domain of roX2 RNA Is Sufficient for Induction of H4-Lys16 Acetylation on the Drosophila X Chromosome. Genetics 177: 1429-1437 [Abstract] [Full Text]  
  • Rodriguez, M. A., Vermaak, D., Bayes, J. J., Malik, H. S. (2007). Species-specific positive selection of the male-specific lethal complex that participates in dosage compensation in Drosophila. Proc. Natl. Acad. Sci. USA 104: 15412-15417 [Abstract] [Full Text]  
  • Gilfillan, G. D., Konig, C., Dahlsveen, I. K., Prakoura, N., Straub, T., Lamm, R., Fauth, T., Becker, P. B. (2007). Cumulative contributions of weak DNA determinants to targeting the Drosophila dosage compensation complex. Nucleic Acids Res 35: 3561-3572 [Abstract] [Full Text]  
  • Takasaki, T., Liu, Z., Habara, Y., Nishiwaki, K., Nakayama, J.-i., Inoue, K., Sakamoto, H., Strome, S. (2007). MRG-1, an autosome-associated protein, silences X-linked genes and protects germline immortality in Caenorhabditis elegans. Development 134: 757-767 [Abstract] [Full Text]  
  • Zhang, P., Du, J., Sun, B., Dong, X., Xu, G., Zhou, J., Huang, Q., Liu, Q., Hao, Q., Ding, J. (2006). Structure of human MRG15 chromo domain and its binding to Lys36-methylated histone H3. Nucleic Acids Res 34: 6621-6628 [Abstract] [Full Text]  
  • Deng, X., Meller, V. H. (2006). roX RNAs Are Required for Increased Expression of X-Linked Genes in Drosophila melanogaster Males. Genetics 174: 1859-1866 [Abstract] [Full Text]  
  • Guelman, S., Suganuma, T., Florens, L., Weake, V., Swanson, S. K., Washburn, M. P., Abmayr, S. M., Workman, J. L. (2006). The Essential Gene wda Encodes a WD40 Repeat Subunit of Drosophila SAGA Required for Histone H3 Acetylation.. Mol. Cell. Biol. 26: 7178-7189 [Abstract] [Full Text]  
  • Fukuda, H., Sano, N., Muto, S., Horikoshi, M. (2006). Simple histone acetylation plays a complex role in the regulation of gene expression.. Brief Funct Genomic Proteomic 5: 190-208 [Abstract] [Full Text]  
  • Rath, U., Ding, Y., Deng, H., Qi, H., Bao, X., Zhang, W., Girton, J., Johansen, J., Johansen, K. M. (2006). The chromodomain protein, Chromator, interacts with JIL-1 kinase and regulates the structure of Drosophila polytene chromosomes. J. Cell Sci. 119: 2332-2341 [Abstract] [Full Text]  
  • Gilfillan, G. D., Straub, T., de Wit, E., Greil, F., Lamm, R., van Steensel, B., Becker, P. B. (2006). Chromosome-wide gene-specific targeting of the Drosophila dosage compensation complex. Genes Dev. 20: 858-870 [Abstract] [Full Text]  
  • Schubeler, D. (2006). Dosage compensation in high resolution: global up-regulation through local recruitment. Genes Dev. 20: 749-753 [Full Text]  
  • Kotlikova, I. V., Demakova, O. V., Semeshin, V. F., Shloma, V. V., Boldyreva, L. V., Kuroda, M. I., Zhimulev, I. F. (2006). The Drosophila Dosage Compensation Complex Binds to Polytene Chromosomes Independently of Developmental Changes in Transcription. Genetics 172: 963-974 [Abstract] [Full Text]  
  • Kimura, A., Matsubara, K., Horikoshi, M. (2005). A Decade of Histone Acetylation: Marking Eukaryotic Chromosomes with Specific Codes. J Biochem 138: 647-662 [Abstract] [Full Text]  
  • Smith, E. R., Cayrou, C., Huang, R., Lane, W. S., Cote, J., Lucchesi, J. C. (2005). A Human Protein Complex Homologous to the Drosophila MSL Complex Is Responsible for the Majority of Histone H4 Acetylation at Lysine 16. Mol. Cell. Biol. 25: 9175-9188 [Abstract] [Full Text]  
  • Li, F., Parry, D. A. D., Scott, M. J. (2005). The Amino-Terminal Region of Drosophila MSL1 Contains Basic, Glycine-Rich, and Leucine Zipper-Like Motifs That Promote X Chromosome Binding, Self-Association, and MSL2 Binding, Respectively. Mol. Cell. Biol. 25: 8913-8924 [Abstract] [Full Text]  
  • Hamada, F. N., Park, P. J., Gordadze, P. R., Kuroda, M. I. (2005). Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster. Genes Dev. 19: 2289-2294 [Abstract] [Full Text]  
  • Nielsen, P. R., Nietlispach, D., Buscaino, A., Warner, R. J., Akhtar, A., Murzin, A. G., Murzina, N. V., Laue, E. D. (2005). Structure of the Chromo Barrel Domain from the MOF Acetyltransferase. J. Biol. Chem. 280: 32326-32331 [Abstract] [Full Text]  
  • Taipale, M., Rea, S., Richter, K., Vilar, A., Lichter, P., Imhof, A., Akhtar, A. (2005). hMOF Histone Acetyltransferase Is Required for Histone H4 Lysine 16 Acetylation in Mammalian Cells. Mol. Cell. Biol. 25: 6798-6810 [Abstract] [Full Text]  
  • Morales, V., Regnard, C., Izzo, A., Vetter, I., Becker, P. B. (2005). The MRG Domain Mediates the Functional Integration of MSL3 into the Dosage Compensation Complex. Mol. Cell. Biol. 25: 5947-5954 [Abstract] [Full Text]  
  • Gupta, A., Sharma, G. G., Young, C. S. H., Agarwal, M., Smith, E. R., Paull, T. T., Lucchesi, J. C., Khanna, K. K., Ludwig, T., Pandita, T. K. (2005). Involvement of Human MOF in ATM Function. Mol. Cell. Biol. 25: 5292-5305 [Abstract] [Full Text]  
  • Burger, J. M. S., Promislow, D. E. L. (2004). Sex-Specific Effects of Interventions That Extend Fly Life Span. Sci Aging Knowl Environ 2004: pe30-pe30 [Abstract] [Full Text]  
  • Larsson, J., Svensson, M. J., Stenberg, P., Makitalo, M. (2004). Painting of fourth in genus Drosophila suggests autosome-specific gene regulation. Proc. Natl. Acad. Sci. USA 101: 9728-9733 [Abstract] [Full Text]  
  • Rattner, B. P., Meller, V. H. (2004). Drosophila Male-Specific Lethal 2 Protein Controls Sex-Specific Expression of the roX Genes. Genetics 166: 1825-1832 [Abstract] [Full Text]  
  • OH, H., BAI, X., PARK, Y., BONE, J.R., KURODA, M.I. (2004). Targeting Dosage Compensation to the X Chromosome of Drosophila Males. Cold Spring Harb Symp Quant Biol 69: 81-88 [Abstract]  
  • Zhang, W., Jin, Y., Ji, Y., Girton, J., Johansen, J., Johansen, K. M. (2003). Genetic and Phenotypic Analysis of Alleles of the Drosophila Chromosomal JIL-1 Kinase Reveals a Functional Requirement at Multiple Developmental Stages. Genetics 165: 1341-1354 [Abstract] [Full Text]  
  • Stuckenholz, C., Meller, V. H., Kuroda, M. I. (2003). Functional Redundancy Within roX1, a Noncoding RNA Involved in Dosage Compensation in Drosophila melanogaster. Genetics 164: 1003-1014 [Abstract] [Full Text]  
  • Klisovic, D. D., Katz, S. E., Effron, D., Klisovic, M. I., Wickham, J., Parthun, M. R., Guimond, M., Marcucci, G. (2003). Depsipeptide (FR901228) Inhibits Proliferation and Induces Apoptosis in Primary and Metastatic Human Uveal Melanoma Cell Lines. IOVS 44: 2390-2398 [Abstract] [Full Text]  
  • Lachner, M., O'Sullivan, R. J., Jenuwein, T. (2003). An epigenetic road map for histone lysine methylation. J. Cell Sci. 116: 2117-2124 [Full Text]  
  • Oh, H., Park, Y., Kuroda, M. I. (2003). Local spreading of MSL complexes from roX genes on the Drosophila X chromosome. Genes Dev. 17: 1334-1339 [Abstract] [Full Text]  
  • Kusch, T., Guelman, S., Abmayr, S. M., Workman, J. L. (2003). Two Drosophila Ada2 Homologues Function in Different Multiprotein Complexes. Mol. Cell. Biol. 23: 3305-3319 [Abstract] [Full Text]  
  • Zhou, K., Choe, K.-T., Zaidi, Z., Wang, Q., Mathews, M. B., Lee, C.-G. (2003). RNA helicase A interacts with dsDNA and topoisomerase II{alpha}. Nucleic Acids Res 31: 2253-2260 [Abstract] [Full Text]  
  • Zhang, W., Wang, Y., Long, J., Girton, J., Johansen, J., Johansen, K. M. (2003). A Developmentally Regulated Splice Variant from the Complex lola Locus Encoding Multiple Different Zinc Finger Domain Proteins Interacts with the Chromosomal Kinase JIL-1. J. Biol. Chem. 278: 11696-11704 [Abstract] [Full Text]  
  • Pardo, P. S., Leung, J. K., Lucchesi, J. C., Pereira-Smith, O. M. (2002). MRG15, a Novel Chromodomain Protein, Is Present in Two Distinct Multiprotein Complexes Involved in Transcriptional Activation. J. Biol. Chem. 277: 50860-50866 [Abstract] [Full Text]  
  • Osada, S., Sutton, A., Muster, N., Brown, C. E., Yates, J. R. III, Sternglanz, R., Workman, J. L. (2001). The yeast SAS (something about silencing) protein complex contains a MYST-type putative acetyltransferase and functions with chromatin assembly factor ASF1. Genes Dev. 15: 3155-3168 [Abstract] [Full Text]  
  • Nourani, A., Doyon, Y., Utley, R. T., Allard, S., Lane, W. S., Cote, J. (2001). Role of an ING1 Growth Regulator in Transcriptional Activation and Targeted Histone Acetylation by the NuA4 Complex. Mol. Cell. Biol. 21: 7629-7640 [Abstract] [Full Text]  
  • Gregory, R. I., Randall, T. E., Johnson, C. A., Khosla, S., Hatada, I., O'Neill, L. P., Turner, B. M., Feil, R. (2001). DNA Methylation Is Linked to Deacetylation of Histone H3, but Not H4, on the Imprinted Genes Snrpn and U2af1-rs1. Mol. Cell. Biol. 21: 5426-5436 [Abstract] [Full Text]  
  • Sanjuán, R., Marín, I. (2001). Tracing the Origin of the Compensasome: Evolutionary History of DEAH Helicase and MYST Acetyltransferase Gene Families. Mol Biol Evol 18: 330-343 [Abstract] [Full Text]  
  • Nowak, S. J., Corces, V. G. (2000). Phosphorylation of histone H3 correlates with transcriptionally active loci. Genes Dev. 14: 3003-3013 [Abstract] [Full Text]  
  • Marin, I., Baker, B. S. (2000). Origin and Evolution of the Regulatory Gene male-specific lethal-3. Mol Biol Evol 17: 1240-1250 [Abstract] [Full Text]  
  • Sterner, D. E., Berger, S. L. (2000). Acetylation of Histones and Transcription-Related Factors. Microbiol. Mol. Biol. Rev. 64: 435-459 [Abstract] [Full Text]  
  • Jin, Y., Wang, Y., Johansen, J., Johansen, K. M. (2000). Jil-1, a Chromosomal Kinase Implicated in Regulation of Chromatin Structure, Associates with the Male Specific Lethal (Msl) Dosage Compensation Complex. JCB 149: 1005-1010 [Abstract] [Full Text]  
  • Smith, E. R., Allis, C. D., Lucchesi, J. C. (2001). Linking Global Histone Acetylation to the Transcription Enhancement of X-chromosomal Genes in Drosophila Males. J. Biol. Chem. 276: 31483-31486 [Abstract] [Full Text]  
  • Wang, X., Moore, S. C., Laszckzak, M., Ausio, J. (2000). Acetylation Increases the alpha -Helical Content of the Histone Tails of the Nucleosome. J. Biol. Chem. 275: 35013-35020 [Abstract] [Full Text]  
  • Eisen, A., Utley, R. T., Nourani, A., Allard, S., Schmidt, P., Lane, W. S., Lucchesi, J. C., Cote, J. (2001). The Yeast NuA4 and Drosophila MSL Complexes Contain Homologous Subunits Important for Transcription Regulation. J. Biol. Chem. 276: 3484-3491 [Abstract] [Full Text]  
  • Henry, R. A., Tews, B., Li, X., Scott, M. J. (2001). Recruitment of the Male-specific Lethal (MSL) Dosage Compensation Complex to an Autosomally Integrated roX Chromatin Entry Site Correlates with an Increased Expression of an Adjacent Reporter Gene in Male Drosophila. J. Biol. Chem. 276: 31953-31958 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»