Chromosome Research

, Volume 22, Issue 4, pp 505–515 | Cite as

A new player in X identification: the CLAMP protein is a key factor in Drosophila dosage compensation

Article

Abstract

Dosage compensation adjusts the expression levels of genes on one or both targeted sex chromosomes in heterogametic species. This process results in the normalized transcriptional output of important and essential gene families encoded on multiple chromosomes. The mechanisms of dosage compensation have been studied in many model organisms, including Drosophila melanogaster (fly), Caenorhabditis elegans (worm), and Mus musculus (mouse). Although the mechanisms of dosage compensations differ among these species, all of these processes rely on the initial discrimination of the X chromosome from autosomes. Recently, a new paradigm for how the X chromosome is targeted for regulation was identified in Drosophila. This mechanism involves a newly identified zinc finger protein, CLAMP. Here, we review important factors involved in dosage compensation across species with special focus on the fly. Understanding how the newly identified CLAMP protein is involved in X targeting in the fly could provide key insights into how the X chromosome is initially identified across species.

Keywords

dosage compensation Drosophila zinc finger protein transcription factor 

Abbreviations

H4K16ac

Histone 4 lysine 16 acetylation

RNA Pol II

RNA polymerase II

Xist

X inactive specific transcript

Enox or Jpx

Expressed neighbor of Xist

YY1

Ying yang 1

CTCF

CCCTC-binding factor

PCR2

Polycomb repressive 2

H3K27me3

Histone 3 lysine 27 tri-methylation

Tsix

Antisense to Xist

DCC

Dosage compensation complex

rex

Recruitment element on X

dox

Dependent on X

MSL

Male specific lethal complex

roX

RNA on the X

MRE

MSL recognition elements

H3K36me3

Histone 3 lysine 36 tri-methylation

CLAMP

Chromatin-linked adapter for MSL proteins

MSL1

Male specific lethal 1

MSL2

Male specific lethal 2

MSL3

Male specific lethal 3

MLE

Maleless

MOF

Males absent on the first

Sxl

Sex lethal

H2B

Histone 2B

HAT

Histone acetyl-transferase

NSL

Nonspecific lethal

JIL-1

Serine protein kinase

H3S10

Histone 3 Serine 10

NURF301

Nucleosome remodeling factor

CES

Chromatin entry sites

modENCODE

Model organism encyclopedia of DNA elements

ChIP-seq

Chromatin immunoprecipitaiton followed with next gen sequencing

GAF

GAGA factor

Notes

Acknowledgments

We are grateful to Dr. Leila Rieder for insights and critical review of the manuscript.

Conflict of interest

The author declares that they have no conflict of interest.

References

  1. Alekseyenko AA, Larschan E, Lai WR, Park PJ, Kuroda MI (2006) High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome. Genes Dev 20:848–857PubMedCentralPubMedCrossRefGoogle Scholar
  2. Alekseyenko AA, Peng S, Larschan E, Gorchakov AA, Lee OK, Kharchenko P, McGrath SD, Wang CI, Mardis ER, Park PJ et al (2008) A sequence motif within chromatin entry sites directs MSL establishment on the Drosophila X chromosome. Cell 134:599–609PubMedCentralPubMedCrossRefGoogle Scholar
  3. Alekseyenko AA, Ho JW, Peng S, Gelbart M, Tolstorukov MY, Plachetka A, Kharchenko PV, Jung YL, Gorchakov AA, Larschan E et al (2012) Sequence-specific targeting of dosage compensation in Drosophila favors an active chromatin context. PLoS Genet 8:e1002646PubMedCentralPubMedCrossRefGoogle Scholar
  4. Alekseyenko AA, Ellison CE, Gorchakov AA, Zhou Q, Kaiser VB, Toda N, Walton Z, Peng S, Park PJ, Bachtrog D et al (2013) Conservation and de novo acquisition of dosage compensation on newly evolved sex chromosomes in Drosophila. Genes Dev 27:853–858PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bai X, Alekseyenko AA, Kuroda MI (2004) Sequence-specific targeting of MSL complex regulates transcription of the roX RNA genes. EMBO J 23:2853–2861PubMedCentralPubMedCrossRefGoogle Scholar
  6. Bai X, Larschan E, Kwon SY, Badenhorst P, Kuroda MI (2007) Regional control of chromatin organization by noncoding roX RNAs and the NURF remodeling complex in Drosophila melanogaster. Genetics 176:1491–1499PubMedCentralPubMedCrossRefGoogle Scholar
  7. Beckmann K, Grskovic M, Gebauer F, Hentze MW (2005) A dual inhibitory mechanism restricts msl-2 mRNA translation for dosage compensation in Drosophila. Cell 122:529–540PubMedCrossRefGoogle Scholar
  8. Belote JM, Lucchesi JC (1980) Male-specific lethal mutations of Drosophila melanogaster. Genetics 96:165–186PubMedCentralPubMedGoogle Scholar
  9. Chao W, Huynh KD, Spencer RJ, Davidow LS, Lee JT (2002) CTCF, a candidate trans-acting factor for X-inactivation choice. Science 295:345–347PubMedCrossRefGoogle Scholar
  10. Charlesworth B (1978) Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci U S A 75:5618–5622PubMedCentralPubMedCrossRefGoogle Scholar
  11. Copps K, Richman R, Lyman LM, Chang KA, Rampersad-Ammons J, Kuroda MI (1998) Complex formation by the Drosophila MSL proteins: role of the MSL2 RING finger in protein complex assembly. EMBO J 17:5409–5417PubMedCentralPubMedCrossRefGoogle Scholar
  12. Deng X, Meller VH (2006) roX RNAs are required for increased expression of X-linked genes in Drosophila melanogaster males. Genetics 174:1859–1866PubMedCentralPubMedCrossRefGoogle Scholar
  13. Deng X, Hiatt JB, Nguyen DK, Ercan S, Sturgill D, Hillier LW, Schlesinger F, Davis CA, Reinke VJ, Gingeras TR et al (2011) Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet 43:1179–1185PubMedCentralPubMedCrossRefGoogle Scholar
  14. Deng X, Berletch JB, Ma W, Nguyen DK, Hiatt JB, Noble WS, Shendure J, Disteche CM (2013) Mammalian X upregulation is associated with enhanced transcription initiation, RNA half-life, and MOF-mediated H4K16 acetylation. Dev Cell 25:55–68PubMedCentralPubMedCrossRefGoogle Scholar
  15. Disteche CM (2012) Dosage compensation of the sex chromosomes. Annu Rev Genet 46:537–560PubMedCentralPubMedCrossRefGoogle Scholar
  16. Donohoe ME, Zhang LF, Xu N, Shi Y, Lee JT (2007) Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Mol Cell 25:43–56PubMedCrossRefGoogle Scholar
  17. Ellison CE, Bachtrog D (2013) Dosage compensation via transposable element mediated rewiring of a regulatory network. Science 342:846–850PubMedCentralPubMedCrossRefGoogle Scholar
  18. Fauth T, Muller-Planitz F, Konig C, Straub T, Becker PB (2010) The DNA binding CXC domain of MSL2 is required for faithful targeting the Dosage Compensation Complex to the X chromosome. Nucleic Acids Res 38:3209–3221PubMedCentralPubMedCrossRefGoogle Scholar
  19. Franke A, Baker BS (1999) The rox1 and rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila. Mol Cell 4:117–122PubMedCrossRefGoogle Scholar
  20. Fukunaga A, Tanaka A, Oishi K (1975) Maleless, a recessive autosomal mutant of Drosophila melanogaster that specifically kills male zygotes. Genetics 81:135–141PubMedCentralPubMedGoogle Scholar
  21. Gelbart ME, Larschan E, Peng S, Park PJ, Kuroda MI (2009) Drosophila MSL complex globally acetylates H4K16 on the male X chromosome for dosage compensation. Nat Struct Mol Biol 16:825–832PubMedCentralPubMedCrossRefGoogle Scholar
  22. Gonzalez Nelson AC, Paul KR, Petri M, Flores N, Rogge RA, Cascarina SM, Ross ED (2014) Increasing prion propensity by hydrophobic insertion. PLoS One 9:e89286PubMedCentralPubMedCrossRefGoogle Scholar
  23. Gorchakov AA, Alekseyenko AA, Kharchenko P, Park PJ, Kuroda MI (2009) Long-range spreading of dosage compensation in Drosophila captures transcribed autosomal genes inserted on X. Genes Dev 23:2266–2271PubMedCentralPubMedCrossRefGoogle Scholar
  24. Gorman M, Franke A, Baker BS (1995) Molecular characterization of the male-specific lethal-3 gene and investigations of the regulation of dosage compensation in Drosophila. Development 121:463–475PubMedGoogle Scholar
  25. Gu W, Szauter P, Lucchesi JC (1998) Targeting of MOF, a putative histone acetyl transferase, to the X chromosome of Drosophila melanogaster. Dev Genet 22:56–64PubMedCrossRefGoogle Scholar
  26. Hallacli E, Lipp M, Georgiev P, Spielman C, Cusack S, Akhtar A, Kadlec J (2012) Msl1-mediated dimerization of the dosage compensation complex is essential for male X-chromosome regulation in Drosophila. Mol Cell 48:587–600PubMedCrossRefGoogle Scholar
  27. Hilfiker A, Hilfiker-Kleiner D, Pannuti A, Lucchesi JC (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 16:2054–2060PubMedCentralPubMedCrossRefGoogle Scholar
  28. Ilik IA, Quinn JJ, Georgiev P, Tavares-Cadete F, Maticzka D, Toscano S, Wan Y, Spitale RC, Luscombe N, Backofen R et al (2013) Tandem stem-loops in roX RNAs act together to mediate X chromosome dosage compensation in Drosophila. Mol Cell 51:156–173PubMedCentralPubMedCrossRefGoogle Scholar
  29. Izzo A, Regnard C, Morales V, Kremmer E, Becker PB (2008) Structure-function analysis of the RNA helicase maleless. Nucleic Acids Res 36:950–962PubMedCentralPubMedCrossRefGoogle Scholar
  30. Jans J, Gladden JM, Ralston EJ, Pickle CS, Michel AH, Pferdehirt RR, Eisen MB, Meyer BJ (2009) A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome. Genes Dev 23:602–618PubMedCentralPubMedCrossRefGoogle Scholar
  31. Jeon Y, Lee JT (2011) YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146:119–133PubMedCentralPubMedCrossRefGoogle Scholar
  32. Jeon Y, Sarma K, Lee JT (2012) New and Xisting regulatory mechanisms of X chromosome inactivation. Curr Opin Genet Dev 22:62–71PubMedCentralPubMedCrossRefGoogle Scholar
  33. Jin Y, Wang Y, Johansen J, Johansen KM (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 149:1005–1010PubMedCentralPubMedCrossRefGoogle Scholar
  34. Jonkers I, Monkhorst K, Rentmeester E, Grootegoed JA, Grosveld F, Gribnau J (2008) Xist RNA is confined to the nuclear territory of the silenced X chromosome throughout the cell cycle. Mol Cell Biol 28:5583–5594PubMedCentralPubMedCrossRefGoogle Scholar
  35. Kadlec J, Hallacli E, Lipp M, Holz H, Sanchez-Weatherby J, Cusack S, Akhtar A (2011) Structural basis for MOF and MSL3 recruitment into the dosage compensation complex by MSL1. Nat Struct Mol Biol 18:142–149PubMedCrossRefGoogle Scholar
  36. Kato M, Han TW, Xie S, Shi K, Du X, Wu LC, Mirzaei H, Goldsmith EJ, Longgood J, Pei J et al (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149:753–767PubMedCrossRefGoogle Scholar
  37. Kelley RL, Wang J, Bell L, Kuroda MI (1997) Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 387:195–199PubMedCrossRefGoogle Scholar
  38. Kelley RL, Meller VH, Gordadze PR, Roman G, Davis RL, Kuroda MI (1999) Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin. Cell 98:513–522PubMedCrossRefGoogle Scholar
  39. Kelley RL, Lee OK, Shim YK (2008) Transcription rate of noncoding roX1 RNA controls local spreading of the Drosophila MSL chromatin remodeling complex. Mech Dev 125:1009–1019PubMedCentralPubMedCrossRefGoogle Scholar
  40. Kim D, Blus BJ, Chandra V, Huang P, Rastinejad F, Khorasanizadeh S (2010) Corecognition of DNA and a methylated histone tail by the MSL3 chromodomain. Nat Struct Mol Biol 17:1027–1029PubMedCentralPubMedCrossRefGoogle Scholar
  41. Kruesi WS, Core LJ, Waters CT, Lis JT, Meyer BJ (2013) Condensin controls recruitment of RNA polymerase II to achieve nematode X-chromosome dosage compensation. eLife 2:e00808PubMedCentralPubMedCrossRefGoogle Scholar
  42. Lam KC, Muhlpfordt F, Vaquerizas JM, Raja SJ, Holz H, Luscombe NM, Manke T, Akhtar A (2012) The NSL complex regulates housekeeping genes in Drosophila. PLoS Genet 8:e1002736PubMedCentralPubMedCrossRefGoogle Scholar
  43. Larschan E, Alekseyenko AA, Gortchakov AA, Peng S, Li B, Yang P, Workman JL, Park PJ, Kuroda MI (2007) MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism. Mol Cell 28:121–133PubMedCrossRefGoogle Scholar
  44. Larschan E, Bishop EP, Kharchenko PV, Core LJ, Lis JT, Park PJ, Kuroda MI (2011) X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature 471:115–118PubMedCentralPubMedCrossRefGoogle Scholar
  45. Larschan E, Soruco MM, Lee OK, Peng S, Bishop E, Chery J, Goebel K, Feng J, Park PJ, Kuroda MI (2012) Identification of chromatin-associated regulators of MSL complex targeting in Drosophila dosage compensation. PLoS Genet 8:e1002830PubMedCentralPubMedCrossRefGoogle Scholar
  46. Li F, Parry DA, Scott MJ (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 25:8913–8924PubMedCentralPubMedCrossRefGoogle Scholar
  47. Li F, Schiemann AH, Scott MJ (2008) Incorporation of the noncoding roX RNAs alters the chromatin-binding specificity of the Drosophila MSL1/MSL2 complex. Mol Cell Biol 28:1252–1264PubMedCentralPubMedCrossRefGoogle Scholar
  48. Lim CK, Kelley RL (2012) Autoregulation of the Drosophila noncoding roX1 RNA Gene. PLoS Genet 8:e1002564PubMedCentralPubMedCrossRefGoogle Scholar
  49. Livernois AM, Graves JA, Waters PD (2012) The origin and evolution of vertebrate sex chromosomes and dosage compensation. Heredity 108:50–58PubMedCentralPubMedCrossRefGoogle Scholar
  50. Lucchesi JC, Kelly WG, Panning B (2005) Chromatin remodeling in dosage compensation. Annu Rev Genet 39:615–651PubMedCrossRefGoogle Scholar
  51. Lyman LM, Copps K, Rastelli L, Kelley RL, Kuroda MI (1997) Drosophila male-specific lethal-2 protein: structure/function analysis and dependence on MSL-1 for chromosome association. Genetics 147:1743–1753PubMedCentralPubMedGoogle Scholar
  52. Maenner S, Muller M, Frohlich J, Langer D, Becker PB (2013) ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Mol Cell 51:174–184PubMedCrossRefGoogle Scholar
  53. Meller VH, Rattner BP (2002) The roX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex. EMBO J 21:1084–1091PubMedCentralPubMedCrossRefGoogle Scholar
  54. Meller VH, Gordadze PR, Park Y, Chu X, Stuckenholz C, Kelley RL, Kuroda MI (2000) Ordered assembly of roX RNAs into MSL complexes on the dosage-compensated X chromosome in Drosophila. Curr Biol 10:136–143PubMedCrossRefGoogle Scholar
  55. Meyer BJ (2010) Targeting X chromosomes for repression. Curr Opin Genet Dev 20:179–189PubMedCentralPubMedCrossRefGoogle Scholar
  56. Oh H, Park Y, Kuroda MI (2003) Local spreading of MSL complexes from roX genes on the Drosophila X chromosome. Genes Dev 17:1334–1339PubMedCentralPubMedCrossRefGoogle Scholar
  57. Oh H, Bone JR, Kuroda MI (2004) Multiple classes of MSL binding sites target dosage compensation to the X chromosome of Drosophila. Curr Biol 14:481–487PubMedCrossRefGoogle Scholar
  58. Park Y, Kelley RL, Oh H, Kuroda MI, Meller VH (2002) Extent of chromatin spreading determined by roX RNA recruitment of MSL proteins. Science 298:1620–1623PubMedCrossRefGoogle Scholar
  59. Park Y, Mengus G, Bai X, Kageyama Y, Meller VH, Becker PB, Kuroda MI (2003) Sequence-specific targeting of Drosophila roX genes by the MSL dosage compensation complex. Mol Cell 11:977–986PubMedCrossRefGoogle Scholar
  60. Park SW, Oh H, Lin YR, Park Y (2010) MSL cis-spreading from roX gene up-regulates the neighboring genes. Biochem Biophys Res Commun 399:227–231PubMedCrossRefGoogle Scholar
  61. Payer B, Lee JT (2008) X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 42:733–772PubMedCrossRefGoogle Scholar
  62. Pferdehirt RR, Kruesi WS, Meyer BJ (2011) An MLL/COMPASS subunit functions in the C. elegans dosage compensation complex to target X chromosomes for transcriptional regulation of gene expression. Genes Dev 25:499–515PubMedCentralPubMedCrossRefGoogle Scholar
  63. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300:131–135PubMedCrossRefGoogle Scholar
  64. Prestel M, Feller C, Straub T, Mitlohner H, Becker PB (2010) The activation potential of MOF is constrained for dosage compensation. Mol Cell 38:815–826PubMedCrossRefGoogle Scholar
  65. Reenan RA, Hanrahan CJ, Ganetzky B (2000) The mle(napts) RNA helicase mutation in Drosophila results in a splicing catastrophe of the para Na+ channel transcript in a region of RNA editing. Neuron 25:139–149PubMedCrossRefGoogle Scholar
  66. Regnard C, Straub T, Mitterweger A, Dahlsveen IK, Fabian V, Becker PB (2011) Global analysis of the relationship between JIL-1 kinase and transcription. PLoS Genet 7:e1001327PubMedCentralPubMedCrossRefGoogle Scholar
  67. Scott MJ, Pan LL, Cleland SB, Knox AL, Heinrich J (2000) MSL1 plays a central role in assembly of the MSL complex, essential for dosage compensation in Drosophila. EMBO J 19:144–155PubMedCentralPubMedCrossRefGoogle Scholar
  68. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–847PubMedCrossRefGoogle Scholar
  69. Simon MD, Pinter SF, Fang R, Sarma K, Rutenberg-Schoenberg M, Bowman SK, Kesner BA, Maier VK, Kingston RE, Lee JT (2013) High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature 504:465–469PubMedCentralPubMedCrossRefGoogle Scholar
  70. Smith ER, Pannuti A, Gu W, Steurnagel A, Cook RG, Allis CD, Lucchesi JC (2000) The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol Cell Biol 20:312–318PubMedCentralPubMedCrossRefGoogle Scholar
  71. Smith ER, Allis CD, Lucchesi JC (2001) Linking global histone acetylation to the transcription enhancement of X-chromosomal genes in Drosophila males. J Biol Chem 276:31483–31486PubMedCrossRefGoogle Scholar
  72. Soruco MM, Chery J, Bishop EP, Siggers T, Tolstorukov MY, Leydon AR, Sugden AU, Goebel K, Feng J, Xia P et al (2013) The CLAMP protein links the MSL complex to the X chromosome during Drosophila dosage compensation. Genes Dev 27:1551–1556PubMedCentralPubMedCrossRefGoogle Scholar
  73. Straub T, Grimaud C, Gilfillan GD, Mitterweger A, Becker PB (2008) The chromosomal high-affinity binding sites for the Drosophila dosage compensation complex. PLoS Genet 4:e1000302PubMedCentralPubMedCrossRefGoogle Scholar
  74. Straub T, Zabel A, Gilfillan GD, Feller C, Becker PB (2013) Different chromatin interfaces of the Drosophila dosage compensation complex revealed by high-shear ChIP-seq. Genome Res 23:473–485PubMedCentralPubMedCrossRefGoogle Scholar
  75. Sun L, Fernandez HR, Donohue RC, Li J, Cheng J, Birchler JA (2013) Male-specific lethal complex in Drosophila counteracts histone acetylation and does not mediate dosage compensation. Proc Natl Acad Sci U S A 110:E808–E817PubMedCentralPubMedCrossRefGoogle Scholar
  76. Sural TH, Peng S, Li B, Workman JL, Park PJ, Kuroda MI (2008) The MSL3 chromodomain directs a key targeting step for dosage compensation of the Drosophila melanogaster X chromosome. Nat Struct Mol Biol 15:1318–1325PubMedCentralPubMedCrossRefGoogle Scholar
  77. Tian D, Sun S, Lee JT (2010) The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143:390–403PubMedCentralPubMedCrossRefGoogle Scholar
  78. Villa R, Forne I, Muller M, Imhof A, Straub T, Becker PB (2012) MSL2 combines sensor and effector functions in homeostatic control of the Drosophila dosage compensation machinery. Mol Cell 48:647–654PubMedCrossRefGoogle Scholar
  79. Wang C, Cai W, Li Y, Deng H, Bao X, Girton J, Johansen J, Johansen KM (2011) The epigenetic H3S10 phosphorylation mark is required for counteracting heterochromatic spreading and gene silencing in Drosophila melanogaster. J Cell Sci 124:4309–4317PubMedCentralPubMedCrossRefGoogle Scholar
  80. Wang CI, Alekseyenko AA, LeRoy G, Elia AE, Gorchakov AA, Britton LM, Elledge SJ, Kharchenko PV, Garcia BA, Kuroda MI (2013) Chromatin proteins captured by ChIP-mass spectrometry are linked to dosage compensation in Drosophila. Nat Struct Mol Biol 20:202–209PubMedCentralPubMedCrossRefGoogle Scholar
  81. Wilkins RC, Lis JT (1999) DNA distortion and multimerization: novel functions of the glutamine-rich domain of GAGA factor. J Mol Biol 285:515–525PubMedCrossRefGoogle Scholar
  82. Wood AJ, Severson AF, Meyer BJ (2010) Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 11:391–404PubMedCentralPubMedCrossRefGoogle Scholar
  83. Wu L, Zee BM, Wang Y, Garcia BA, Dou Y (2011) The RING finger protein MSL2 in the MOF complex is an E3 ubiquitin ligase for H2B K34 and is involved in crosstalk with H3 K4 and K79 methylation. Mol Cell 43:132–144PubMedCentralPubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Department of Molecular Biology, Cellular Biology and BiochemistryBrown UniversityProvidenceUSA

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