Smarca4 ATPase mutations disrupt direct eviction of PRC1 from chromatin

Nature Genetics

Volumn 49, Issue 2, 2017, Pages 282-288

  Stanton, Benjamin Z ^a,b   Hodges, Courtney ^a   Calarco, Joseph P ^a   Braun, Simon M G ^a   Ku, Wai Lim ^b   Kadoch, Cigall ^c,d   Zhao, Keji ^b   Crabtree, Gerald R ^a,e  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRG1 PROTEIN; POLYCOMB GROUP PROTEIN; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CELL CYCLE PROTEIN; CHROMATIN; DNA BINDING PROTEIN; DNA HELICASE; NUCLEAR PROTEIN; SMARCA4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ARTICLE; CHROMATIN; GENE MAPPING; GENOME-WIDE ASSOCIATION STUDY; HUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECURRENT DISEASE; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETICS; MENTAL DISEASE; MOUSE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL CYCLE PROTEINS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HELICASES; DNA-BINDING PROTEINS; MICE; NEURODEVELOPMENTAL DISORDERS; NUCLEAR PROTEINS; POINT MUTATION; POLYCOMB-GROUP PROTEINS; TRANSCRIPTION FACTORS;

EID: 85003936035     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3735     Document Type: Article

References (68)

1. Clapier, C.R., Cairns, B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273-304 (2009).
2. Kennison, J.A., Tamkun, J.W. Dosage-dependent modifiers of Polycomb and antennapedia mutations in Drosophila. Proc. Natl. Acad. Sci. USA 85, 8136-8140 (1988).
3. Wilson, B.G. , et al. Epigenetic antagonism between Polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 18, 316-328 (2010).
4. Ho, L. , et al. esBAF facilitates pluripotency by conditioning the genome for LIF/STAT3 signalling and by regulating Polycomb function. Nat. Cell Biol. 13, 903-913 (2011).
5. Kadoch, C., Crabtree, G.R. Reversible disruption of mSWI/SNF (BAF) complexes by the SS18-SSX oncogenic fusion in synovial sarcoma. Cell 153, 71-85 (2013).
6. McKenna, E.S. , et al. Loss of the epigenetic tumor suppressor SNF5 leads to cancer without genomic instability. Mol. Cell. Biol. 28, 6223-6233 (2008).
7. Hodges, C., Kirkland, J.G., Crabtree, G.R. The many roles of BAF (mSWI/SNF) and PBAF complexes in cancer. Cold Spring Harb. Perspect. Med. 6, a026930 (2016).
8. Deciphering Developmental Disorders Study. Large-scale discovery of novel genetic causes of developmental disorders. Nature 519, 223-228 (2015).
9. Santen, G.W. , et al. Coffin-Siris syndrome and the BAF complex: genotype-phenotype study in 63 patients. Hum. Mutat. 34, 1519-1528 (2013).
10. Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B., Cavalli, G. Genome regulation by Polycomb and Trithorax proteins. Cell 128, 735-745 (2007).
11. O'Carroll, D. , et al. The Polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell. Biol. 21, 4330-4336 (2001).
12. Pasini, D., Bracken, A.P., Hansen, J.B., Capillo, M., Helin, K. The Polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 27, 3769-3779 (2007).
13. van der Stoop, P. , et al. Ubiquitin E3 ligase Ring1b/Rnf2 of Polycomb repressive complex 1 contributes to stable maintenance of mouse embryonic stem cells. PLoS One 3, e2235 (2008).
14. Schoenfelder, S. , et al. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat. Genet. 47, 1179-1186 (2015).
15. Jones, P.A., Baylin, S.B. The epigenomics of cancer. Cell 128, 683-692 (2007).
16. Min, J. , et al. An oncogene-tumor suppressor cascade drives metastatic prostate cancer by coordinately activating Ras and nuclear factor-B. Nat. Med. 16, 286-294 (2010).
17. Béguelin, W. , et al. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell 23, 677-692 (2013).
18. Lee, W. , et al. PRC2 is recurrently inactivated through EED or SUZ12 loss in malignant peripheral nerve sheath tumors. Nat. Genet. 46, 1227-1232 (2014).
19. Varela, I. , et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469, 539-542 (2011).
20. Wiegand, K.C. , et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 363, 1532-1543 (2010).
21. Pugh, T.J. , et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488, 106-110 (2012).
22. Taylor, M.D. , et al. Familial posterior fossa brain tumors of infancy secondary to germline mutation of the hSNF5 gene. Am. J. Hum. Genet. 66, 1403-1406 (2000).
23. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337 (2012).
24. Rodriguez-Nieto, S. , et al. Massive parallel DNA pyrosequencing analysis of the tumor suppressor BRG1/SMARCA4 in lung primary tumors. Hum. Mutat. 32, E1999-E2017 (2011).
25. Davoli, T. , et al. Cumulative haploinsufficiency and triplosensitivity drive aneuploidy patterns and shape the cancer genome. Cell 155, 948-962 (2013).
26. Son, E.Y., Crabtree, G.R. The role of BAF (mSWI/SNF) complexes in mammalian neural development. Am. J. Med. Genet. C. Semin. Med. Genet. 166C, 333-349 (2014).
27. Shi, J. , et al. Discovery of cancer drug targets by CRISPR-Cas9 screening of protein domains. Nat. Biotechnol. 33, 661-667 (2015).
28. Brookes, E. , et al. Polycomb associates genome-wide with a specific RNA polymerase II variant, and regulates metabolic genes in ESCs. Cell Stem Cell 10, 157-170 (2012).
29. Fairman-Williams, M.E., Guenther, U.P., Jankowsky, E. SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol. 20, 313-324 (2010).
30. Weinstein, J.N. , et al. The Cancer Genome Atlas Pan-Cancer analysis project. Nat. Genet. 45, 1113-1120 (2013).
31. Barretina, J. , et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603-607 (2012).
32. Smith, C.L., Peterson, C.L. A conserved Swi2/Snf2 ATPase motif couples ATP hydrolysis to chromatin remodeling. Mol. Cell. Biol. 25, 5880-5892 (2005).
33. Khavari, P.A., Peterson, C.L., Tamkun, J.W., Mendel, D.B., Crabtree, G.R. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366, 170-174 (1993).
34. Dykhuizen, E.C. , et al. BAF complexes facilitate decatenation of DNA by topoisomerase II. Nature 497, 624-627 (2013).
35. McLachlan, G. Discriminant Analysis and Statistical Pattern Recognition (John Wiley & Sons, 2004).
36. Fisher, R.A. The use of multiple measurements in taxonomic problems. Ann. Eugen. 7, 179-188 (1936).
37. Hu, D. , et al. The Mll2 branch of the COMPASS family regulates bivalent promoters in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1093-1097 (2013).
38. Tibshirani, R. Regression shrinkage and selection via the lasso. J. R. Stat. Soc. B 58, 267-288 (1996).
39. Blackledge, N.P. , et al. Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and Polycomb domain formation. Cell 157, 1445-1459 (2014).
40. Ho, L. , et al. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc. Natl. Acad. Sci. USA 106, 5181-5186 (2009).
41. Morey, L., Aloia, L., Cozzuto, L., Benitah, S.A., Di Croce, L. RYBP and Cbx7 define specific biological functions of Polycomb complexes in mouse embryonic stem cells. Cell Rep. 3, 60-69 (2013).
42. Auble, D.T. , et al. Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism. Genes Dev. 8, 1920-1934 (1994).
43. Wollmann, P. , et al. Structure and mechanism of the Swi2/Snf2 remodeller Mot1 in complex with its substrate TBP. Nature 475, 403-407 (2011).
44. Hathaway, N.A. , et al. Dynamics and memory of heterochromatin in living cells. Cell 149, 1447-1460 (2012).
45. Kadoch, C. , et al. Dynamics of BAF-Polycomb complex opposition on heterochromatin in normal and oncogenic states. Nat. Genet. http://dx.doi.org/10.1038/ng.3734 (2016).
46. Farcas, A.M. , et al. KDM2B links the Polycomb repressive complex 1 (PRC1) to recognition of CpG islands. eLife 1, e00205 (2012).
47. Lessard, J. , et al. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55, 201-215 (2007).
48. Wu, J.I. , et al. Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56, 94-108 (2007).
49. Stamatoyannopoulos, J.A. , et al. An encyclopedia of mouse DNA elements (Mouse ENCODE). Genome Biol. 13, 418 (2012).
50. Sen, M. , et al. The ClpXP protease unfolds substrates using a constant rate of pulling but different gears. Cell 155, 636-646 (2013).
51. Jin, W. , et al. Genome-wide detection of DNase I hypersensitive sites in single cells and FFPE tissue samples. Nature 528, 142-146 (2015).
52. Barski, A. , et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007).
53. Kidder, B.L., Zhao, K. Efficient library preparation for next-generation sequencing analysis of genome-wide epigenetic and transcriptional landscapes in embryonic stem cells. Methods Mol. Biol. 1150, 3-20 (2014).
54. Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
55. Zhang, Y. , et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
56. Love, M.I., Huber, W., Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
57. Pohl, A., Beato, M. bwtool: a tool for bigWig files. Bioinformatics 30, 1618-1619 (2014).
58. Hahne, F., Ivanek, R. Visualizing genomic data using Gviz and Bioconductor. Methods Mol. Biol. 1418, 335-351 (2016).
59. Quinlan, A.R., Hall, I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
60. Anders, S., Pyl, P.T., Huber, W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015).
61. Heinz, S. , et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010).
62. Fischer, J.D., Mayer, C.E., Söding, J. Prediction of protein functional residues from sequence by probability density estimation. Bioinformatics 24, 613-620 (2008).
63. Shenkin, P.S., Erman, B., Mastrandrea, L.D. Information-theoretical entropy as a measure of sequence variability. Proteins 11, 297-313 (1991).
64. Capra, J.A., Singh, M. Predicting functionally important residues from sequence conservation. Bioinformatics 23, 1875-1882 (2007).
65. Adzhubei, I.A. , et al. A method and server for predicting damaging missense mutations. Nat. Methods 7, 248-249 (2010).
66. Ramos, A.H. , et al. Oncotator: cancer variant annotation tool. Hum. Mutat. 36, E2423-E2429 (2015).
67. Ran, F.A. , et al. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308 (2013).
68. Friedman, J., Hastie, T., Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1-22 (2010).