The Xist RNA-PRC2 complex at 20-nm resolution reveals a low Xist stoichiometry and suggests a hit-and-run mechanism in mouse cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 31, 2015, Pages E4216-E4225

  Sunwoo, Hongjae ^a,b   Wu, John Y ^a,c,d   Lee, Jeannie T ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD UNIVERSITY   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

Chromosome; Polycomb; Super resolution microscopy; X inactivation; Xist RNA

Indexed keywords

POLYCOMB REPRESSIVE COMPLEX 2; RNA; EPITOPE; EZH2 PROTEIN, MOUSE; HISTONE; LONG UNTRANSLATED RNA; LYSINE; SUZ12 PROTEIN, MOUSE; XIST NON-CODING RNA;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION; EMBRYO; EPIGENETICS; FEMALE; GENE SEQUENCE; GENOME ANALYSIS; METHYLATION; MICROSCOPY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEOSOME; OPTICAL RESOLUTION; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; STOICHIOMETRY; ANIMAL; ANIMAL EMBRYO; CHEMISTRY; CYTOLOGY; EMBRYONIC STEM CELL; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; METABOLISM; THREE DIMENSIONAL IMAGING; X CHROMOSOME; X CHROMOSOME INACTIVATION;

ANIMALS; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; EPITOPES; FEMALE; FIBROBLASTS; HISTONES; IMAGING, THREE-DIMENSIONAL; IN SITU HYBRIDIZATION, FLUORESCENCE; LYSINE; METHYLATION; MICE; POLYCOMB REPRESSIVE COMPLEX 2; RNA, LONG NONCODING; X CHROMOSOME; X CHROMOSOME INACTIVATION;

EID: 84938705162     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1503690112     Document Type: Article

References (39)

1. Starmer J, Magnuson T (2009) A new model for random X chromosome inactivation. Development 136(1):1-10.
2. Wutz A (2011) Gene silencing in X-chromosome inactivation: Advances in understanding facultative heterochromatin formation. Nat Rev Genet 12(8):542-553.
3. Disteche CM (2012) Dosage compensation of the sex chromosomes. Annu Rev Genet 46:537-560.
4. Lee JT (2011) Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat Rev Mol Cell Biol 12(12):815-826.
5. Brown CJ, et al. (1992) The human XIST gene: Analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71(3):527-542.
6. Clemson CM, McNeil JA, Willard HF, Lawrence JB (1996) XIST RNA paints the inactive X chromosome at interphase: Evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol 132(3):259-275.
7. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322(5902):750-756.
8. Jeon Y, Lee JT (2011) YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146(1):119-133.
9. Silva J, et al. (2003) Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev Cell 4(4):481-495.
10. Simon MD, et al. (2013) High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature 504(7480):465-469.
11. Pinter SF, et al. (2012) Spreading of X chromosome inactivation via a hierarchy of defined Polycomb stations. Genome Res 22(10):1864-1876.
12. Kohlmaier A, et al. (2004) A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol 2(7):E171.
13. Plath K, et al. (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300(5616):131-135.
14. Engreitz JM, et al. (2013) The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341(6147):1237973.
15. Calabrese JM, et al. (2012) Site-specific silencing of regulatory elements as a mechanism of X inactivation. Cell 151(5):951-963.
16. Duthie SM, et al. (1999) Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis. Hum Mol Genet 8(2):195-204.
17. Chadwick BP, Willard HF (2004) Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome. Proc Natl Acad Sci USA 101(50): 17450-17455.
18. Gendrel AV, et al. (2012) Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev Cell 23(2):265-279.
19. Nozawa RS, et al. (2013) Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat Struct Mol Biol 20(5):566-573.
20. Cerase A, et al. (2014) Spatial separation of Xist RNA and polycomb proteins revealed by superresolution microscopy. Proc Natl Acad Sci USA 111(6):2235-2240.
21. Smeets D, et al. (2014) Three-dimensional super-resolution microscopy of the inactive X chromosome territory reveals a collapse of its active nuclear compartment harboring distinct Xist RNA foci. Epigenetics Chromatin 7:8.
22. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3(10):793-795.
23. Dempsey GT, Vaughan JC, Chen KH, Bates M, Zhuang X (2011) Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat Methods 8(12):1027-1036.
24. Huang B, Wang W, Bates M, Zhuang X (2008) Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319(5864):810-813.
25. Buzin CH, Mann JR, Singer-Sam J (1994) Quantitative RT-PCR assays show Xist RNA levels are low in mouse female adult tissue, embryos and embryoid bodies. Development 120(12):3529-3536.
26. Sun BK, Deaton AM, Lee JT (2006) A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol Cell 21(5):617-628.
27. Femino AM, Fay FS, Fogarty K, Singer RH (1998) Visualization of single RNA transcripts in situ. Science 280(5363):585-590.
28. Wang J, et al. (2001) Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat Genet 28(4):371-375.
29. Cifuentes-Rojas C, Hernandez AJ, Sarma K, Lee JT (2014) Regulatory interactions between RNA and polycomb repressive complex 2. Mol Cell 55(2):171-185.
30. Davidovich C, et al. (2015) Toward a consensus on the binding specificity and promiscuity of PRC2 for RNA. Mol Cell 57(3):552-558.
31. Janicki SM, et al. (2004) From silencing to gene expression: Real-time analysis in single cells. Cell 116(5):683-698.
32. Simon JA, Kingston RE (2013) Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol Cell 49(5):808-824.
33. Di Croce L, Helin K (2013) Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol 20(10):1147-1155.
34. Ciferri C, et al. (2012) Molecular architecture of human polycomb repressive complex 2. eLife 1:e00005.
35. Hasegawa Y, et al. (2010) The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev Cell 19(3):469-476.
36. Sarma K, et al. (2014) ATRX directs binding of PRC2 to Xist RNA and Polycomb targets. Cell 159(4):869-883.
37. Blewitt ME, et al. (2008) SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat Genet 40(5):663-669.
38. Sarma K, Levasseur P, Aristarkhov A, Lee JT (2010) Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proc Natl Acad Sci USA 107(51):22196-22201.
39. Sunwoo H, et al. (2009) MEN epsilon/beta nuclear-retained non-coding RNAs are upregulated upon muscle differentiation and are essential components of paraspeckles. Genome Res 19(3):347-359.