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Msl1-mediated dimerization of the dosage compensation complex is essential for male X-chromosome regulation in Drosophila.

Hallacli E, Lipp M, Georgiev P, Spielman C, Cusack S, Akhtar A, Kadlec J
Mol Cell 48 587-600 (2012)
Cited: 29 times
EuropePMC logo PMID: 23084835

Abstract

The Male-Specific Lethal (MSL) complex regulates dosage compensation of the male X chromosome in Drosophila. Here, we report the crystal structure of its MSL1/MSL2 core, where two MSL2 subunits bind to a dimer formed by two molecules of MSL1. Analysis of structure-based mutants revealed that MSL2 can only interact with the MSL1 dimer, but MSL1 dimerization is MSL2 independent. We show that Msl1 is a substrate for Msl2 E3 ubiquitin ligase activity. ChIP experiments revealed that Msl1 dimerization is essential for targeting and spreading of the MSL complex on X-linked genes; however, Msl1 binding to promoters of male and female cells is independent of the dimer status and other MSL proteins. Finally, we show that loss of Msl1 dimerization leads to male-specific lethality. We propose that Msl1-mediated dimerization of the entire MSL complex is required for Msl2 binding, X chromosome recognition, and spreading along the X chromosome.

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Reviews citing this publication (9)

  1. Dosage compensation in Drosophila. Lucchesi JC, Kuroda MI. Cold Spring Harb Perspect Biol 7 a019398 (2015)
  2. Dosage Compensation of the X Chromosome: A Complex Epigenetic Assignment Involving Chromatin Regulators and Long Noncoding RNAs. Samata M, Akhtar A. Annu Rev Biochem 87 323-350 (2018)
  3. Dosage Compensation in Drosophila-a Model for the Coordinate Regulation of Transcription. Kuroda MI, Hilfiker A, Lucchesi JC. Genetics 204 435-450 (2016)
  4. The MSL complex: juggling RNA-protein interactions for dosage compensation and beyond. Keller CI, Akhtar A. Curr Opin Genet Dev 31 1-11 (2015)
  5. A new player in X identification: the CLAMP protein is a key factor in Drosophila dosage compensation. Soruco MM, Larschan E. Chromosome Res 22 505-515 (2014)
  6. X-marks the spot: X-chromosome identification during dosage compensation. Chery J, Larschan E. Biochim Biophys Acta 1839 234-240 (2014)
  7. Chemical Tools for Dissecting the Role of lncRNAs in Epigenetic Regulation. Nainar S, Feng C, Spitale RC. ACS Chem Biol 11 2091-2100 (2016)
  8. When Down Is Up: Heterochromatin, Nuclear Organization and X Upregulation. Makki R, Meller VH. Cells 10 3416 (2021)
  9. Dosage Compensation in Drosophila: Its Canonical and Non-Canonical Mechanisms. Shevelyov YY, Ulianov SV, Gelfand MS, Belyakin SN, Razin SV. Int J Mol Sci 23 10976 (2022)

Articles citing this publication (19)

  1. Tandem stem-loops in roX RNAs act together to mediate X chromosome dosage compensation in Drosophila. Ilik IA, Quinn JJ, Georgiev P, Tavares-Cadete F, Maticzka D, Toscano S, Wan Y, Spitale RC, Luscombe N, Backofen R, Chang HY, Akhtar A. Mol Cell 51 156-173 (2013)
  2. MOF-associated complexes ensure stem cell identity and Xist repression. Chelmicki T, Dündar F, Turley MJ, Khanam T, Aktas T, Ramírez F, Gendrel AV, Wright PR, Videm P, Backofen R, Heard E, Manke T, Akhtar A. Elife 3 e02024 (2014)
  3. ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Maenner S, Müller M, Fröhlich J, Langer D, Becker PB. Mol Cell 51 174-184 (2013)
  4. Structural analysis of the KANSL1/WDR5/KANSL2 complex reveals that WDR5 is required for efficient assembly and chromatin targeting of the NSL complex. Dias J, Van Nguyen N, Georgiev P, Gaub A, Brettschneider J, Cusack S, Kadlec J, Akhtar A. Genes Dev 28 929-942 (2014)
  5. PionX sites mark the X chromosome for dosage compensation. Villa R, Schauer T, Smialowski P, Straub T, Becker PB. Nature 537 244-248 (2016)
  6. Deciphering the binding between Nupr1 and MSL1 and their DNA-repairing activity. Aguado-Llera D, Hamidi T, Doménech R, Pantoja-Uceda D, Gironella M, Santoro J, Velázquez-Campoy A, Neira JL, Iovanna JL. PLoS One 8 e78101 (2013)
  7. RNA nucleation by MSL2 induces selective X chromosome compartmentalization. Valsecchi CIK, Basilicata MF, Georgiev P, Gaub A, Seyfferth J, Kulkarni T, Panhale A, Semplicio G, Manjunath V, Holz H, Dasmeh P, Akhtar A. Nature 589 137-142 (2021)
  8. Structural basis of X chromosome DNA recognition by the MSL2 CXC domain during Drosophila dosage compensation. Zheng S, Villa R, Wang J, Feng Y, Wang J, Becker PB, Ye K. Genes Dev 28 2652-2662 (2014)
  9. Factor cooperation for chromosome discrimination in Drosophila. Albig C, Tikhonova E, Krause S, Maksimenko O, Regnard C, Becker PB. Nucleic Acids Res 47 1706-1724 (2019)
  10. Functional interplay between MSL1 and CDK7 controls RNA polymerase II Ser5 phosphorylation. Chlamydas S, Holz H, Samata M, Chelmicki T, Georgiev P, Pelechano V, Dündar F, Dasmeh P, Mittler G, Cadete FT, Ramírez F, Conrad T, Wei W, Raja S, Manke T, Luscombe NM, Steinmetz LM, Akhtar A. Nat Struct Mol Biol 23 580-589 (2016)
  11. Genomic Structural Variations Within Five Continental Populations of Drosophila melanogaster. Long E, Evans C, Chaston J, Udall JA. G3 (Bethesda) 8 3247-3253 (2018)
  12. Two-step mechanism for selective incorporation of lncRNA into a chromatin modifier. Müller M, Schauer T, Krause S, Villa R, Thomae AW, Becker PB. Nucleic Acids Res 48 7483-7501 (2020)
  13. Distinct mechanisms mediate X chromosome dosage compensation in Anopheles and Drosophila. Keller Valsecchi CI, Marois E, Basilicata MF, Georgiev P, Akhtar A. Life Sci Alliance 4 e202000996 (2021)
  14. Single-nucleus transcriptomes reveal evolutionary and functional properties of cell types in the Drosophila accessory gland. Majane AC, Cridland JM, Begun DJ. Genetics 220 iyab213 (2022)
  15. Msl2 is a novel component of the vertebrate DNA damage response. Lai Z, Moravcová S, Canitrot Y, Andrzejewski LP, Walshe DM, Rea S. PLoS One 8 e68549 (2013)
  16. Two distinct males absent on the first (MOF)-containing histone acetyltransferases are involved in the epithelial-mesenchymal transition in different ways in human cells. Wei T, Liu H, Zhu H, Chen W, Wu T, Bai Y, Zhang X, Miao Y, Wang F, Cai Y, Jin J. Cell Mol Life Sci 79 238 (2022)
  17. The Males Absent on the First (MOF) Mediated Acetylation Alters the Protein Stability and Transcriptional Activity of YY1 in HCT116 Cells. Wu T, Zhao B, Cai C, Chen Y, Miao Y, Chu J, Sui Y, Li F, Chen W, Cai Y, Wang F, Jin J. Int J Mol Sci 24 8719 (2023)
  18. Physical interaction between MSL2 and CLAMP assures direct cooperativity and prevents competition at composite binding sites. Eggers N, Gkountromichos F, Krause S, Campos-Sparr A, Becker PB. Nucleic Acids Res 51 9039-9054 (2023)
  19. The identification of protein and RNA interactors of the splicing factor Caper in the adult Drosophila nervous system. Titus MB, Chang AW, Popitsch N, Ebmeier CC, Bono JM, Olesnicky EC. Front Mol Neurosci 16 1114857 (2023)


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