Cell Biology: Selective targeting of the BRG/PB1 bromodomains impairs embryonic and trophoblast stem cell maintenance

Science Advances

Volumn 1, Issue 10, 2015, Pages

  Fedorov, Oleg ^a,b   Castex, Josefina ^c   Tallant, Cynthia ^a,b   Owen, Dafydd R ^d   Martin, Sarah ^a,b   Aldeghi, Matteo ^a,b   Monteiro, Octovia ^a,b   Filippakopoulos, Panagis ^b,e   Picaud, Sarah ^b   Trzupek, John D ^d   Gerstenberger, Brian S ^d   Bountra, Chas ^a,b   Willmann, Dominica ^c   Wells, Christopher ^a,b   Philpott, Martin ^a,b   Rogers, Catherine ^a,b   Biggin, Philip C ^b   Brennan, Paul E ^a,b   Bunnage, Mark E ^d   Schüle, Roland ^c,f,g   Günther, Thomas ^c   Knapp, Stefan ^a,b,h   Müller, Susanne ^a,b   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF FREIBURG   (Germany)

^d PFIZER INC   (United States)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f Deutsches Konsortium Für Translationale Krebsforschung DKTK   (Germany)

^g UNIVERSITY OF FREIBURG   (Germany)

^h GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; BINDING ENERGY; BINS; CELLS; CYTOLOGY; MAMMALS; MOLECULES; PROTEINS; SALICYLIC ACID; TRANSCRIPTION;

EMBRYONIC STEM CELLS; GENE TRANSCRIPTIONS; HIGH SPECIFICITY; INHIBITOR COMPLEX; LINEAGE SPECIFICATION; PROTEIN INTERACTION; STEM CELL DIFFERENTIATION; TRANSCRIPTIONAL REGULATOR;

STEM CELLS;

EID: 85018226503     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500723     Document Type: Article

References (54)

1. D. C. Hargreaves, G. R. Crabtree, ATP-dependent chromatin remodeling: Genetics, genomics and mechanisms. Cell Res. 21, 396-420 (2011.
2. W. Wang, Y. Xue, S. Zhou, A. Kuo, B. R. Cairns, G. R. Crabtree, Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev. 10, 2117-2130 (1996).
3. Z. Wang, W. Zhai, J. A. Richardson, E. N. Olson, J. J. Meneses, M. T. Firpo, C. Kang, W. C. Skarnes, R. Tjian, Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev. 18, 3106-3116 (2004).
4. L. Ho, J. L. Ronan, J. Wu, B. T. Staahl, L. Chen, A. Kuo, J. Lessard, A. I. Nesvizhskii, J. Ranish, G. R. Crabtree, An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc. Natl. Acad. Sci. U.S.A. 106, 5181-5186 (2009).
5. X. Zhang, B. Li, W. Li, L. Ma, D. Zheng, L. Li, W. Yang, M. Chu, W. Chen, R. B. Mailman, J. Zhu, G. Fan, T. K. Archer, Y. Wang, Transcriptional repression by the BRG1-SWI/SNF complex affects the pluripotency of human embryonic stem cells. Stem Cell Rep. 3, 460-474 (2014).
6. J. K. Kim, S.-O. Huh, H. Choi, K.-S. Lee, D. Shin, C. Lee, J.-S. Nam, H. Kim, H. Chung, H. W. Lee, S. D. Park, R. H. Seong, Srg3, a mouse homolog of yeast SWI3, is essential for early embryogenesis and involved in brain development. Mol. Cell. Biol. 21, 7787-7795 (2001).
7. S. Bultman, T. Gebuhr, D. Yee, C. La Mantia, J. Nicholson, A. Gilliam, F. Randazzo, D. Metzger, P. Chambon, G. Crabtree, T. Magnuson, A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287-1295 (2000).
8. A. Klochendler-Yeivin, L. Fiette, J. Barra, C. Muchardt, C. Babinet, M. Yaniv, The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Rep. 1, 500-506 (2000).
9. N. Singhal, D. Esch, M. Stehling, H. R. Schöler, BRG1 is required to maintain pluripotency of murine embryonic stem cells. Biores. Open Access 3, 1-8 (2014).
10. J. W. Tamkun, R. Deuring, M. P. Scott, M. Kissinger, A. M. Pattatucci, T. C. Kaufman, J. A. Kennison, brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68, 561-572 (1992).
11. P. Filippakopoulos, S. Picaud, M. Mangos, T. Keates, J.-P. Lambert, D. Barsyte-Lovejoy, I. Felletar, R. Volkmer, S. Müller, T. Pawson, A.-C. Gingras, C. H. Arrowsmith, S. Knapp, Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 149, 214-231 (2012).
12. P. Filippakopoulos, J. Qi, S. Picaud, Y. Shen, W. B. Smith, O. Fedorov, E. M. Morse, T. Keates, T. T. Hickman, I. Felletar, M. Philpott, S. Munro, M. R. McKeown, Y. Wang, A. L. Christie, N. West, M. J. Cameron, B. Schwartz, T. D. Heightman, N. La Thangue, C. A. French, O. Wiest, A. L. Kung, S. Knapp, J. E. Bradner, Selective inhibition of BET bromodomains. Nature 468, 1067-1073 (2010).
13. S. Picaud, D. Da Costa, A. Thanasopoulou, P. Filippakopoulos, P. V. Fish, M. Philpott, O. Fedorov, P. Brennan, M. E. Bunnage, D. R. Owen, J. E. Bradner, P. Taniere, B. O'Sullivan, S. Müller, J. Schwaller, T. Stankovic, S. Knapp, PFI-1, a highly selective protein interaction inhibitor, targeting BET Bromodomains. Cancer Res. 73, 3336-3346 (2013).
14. E. Nicodeme, K. L. Jeffrey, U. Schaefer, S. Beinke, S. Dewell, C.-W. Chung, R. Chandwani, I.Marazzi, P.Wilson, H. Coste, J.White, J. Kirilovsky, C. M. Rice, J.M. Lora, R. K. Prinjha, K. Lee, A. Tarakhovsky, Suppression of inflammation by a synthetic histone mimic. Nature 468, 1119-1123 (2010).
15. Y. Zhao, C.-Y. Yang, S. Wang, The making of I-BET762, a BET bromodomain inhibitor now in clinical development. J. Med. Chem. 56, 7498-7500 (2013).
16. P. Filippakopoulos, S. Knapp, Targeting bromodomains: Epigenetic readers of lysine acetylation. Nat. Rev. Drug Discov. 13, 337-356 (2014).
17. L. R. Vidler, N. Brown, S. Knapp, S. Hoelder, Druggability analysis and structural classification of bromodomain acetyl-lysine binding sites. J. Med. Chem. 55, 7346-7359 (2012).
18. L. K. Elfring, C. Daniel, O. Papoulas, R. Deuring, M. Sarte, S. Moseley, S. J. Beek, W. R. Waldrip, G. Daubresse, A. DePace, J. A. Kennison, J. W. Tamkun, Genetic analysis of brahma: The Drosophila homolog of the yeast chromatin remodeling factor SWI2/SNF2. Genetics 148, 251-265 (1998).
19. O. Fedorov, H. Lingard, C. Wells, O. P. Monteiro, S. Picaud, T. Keates, C. Yapp, M. Philpott, S. J. Martin, I. Felletar, B. D. Marsden, P. Filippakopoulos, S. Müller, S. Knapp, P. E. Brennan, [1, 2, 4]Triazolo[4, 3-a]phthalazines: Inhibitors of diverse bromodomains. J. Med. Chem. 57, 462-476 (2014).
20. O. Fedorov, F. H. Niesen, S. Knapp, Kinase inhibitor selectivity profiling using differential scanning fluorimetry. Methods Mol. Biol. 795, 109-118 (2012).
21. X.-M. Xu, L. Sansores-Garcia, X.-M. Chen, N. Matijevic-Aleksic, M. Du, K. K. Wu, Suppression of inducible cyclooxygenase 2 gene transcription by aspirin and sodium salicylate. Proc. Natl. Acad. Sci. U.S.A. 96, 5292-5297 (1999).
22. D. J. Owen, P. Ornaghi, J.-C. Yang, N. Lowe, P. R. Evans, P. Ballario, D. Neuhaus, P. Filetici, A. A. Travers, The structural basis for the recognition of acetylated histone H4 by the bromodomain of histone acetyltransferase gcn5p. EMBO J. 19, 6141-6149 (2000).
23. C. N. Nguyen, A. Cruz, M. K. Gilson, T. Kurtzman, Thermodynamics of water in an enzyme active site: Grid-based hydration analysis of coagulation factor Xa. J. Chem. Theory Comput. 10, 2769-2780 (2014).
24. M. Philpott, C. M. Rogers, C. Yapp, C. Wells, J.-P. Lambert, C. Strain-Damerell, N. A. Burgess-Brown, A.-C. Gingras, S. Knapp, S. Müller, Assessing cellular efficacy of bromodomain inhibitors using fluorescence recovery after photobleaching. Epigenetics Chromatin 7, 14 (2014).
25. J. Masliah-Planchon, I. Bièche, J.-M. Guinebretière, F. Bourdeaut, O. Delattre, SWI/SNF chromatin remodeling and human malignancies. Annu. Rev. Pathol. 10, 145-171 (2015).
26. J. Shi, W. A.Whyte, C. J. Zepeda-Mendoza, J. P. Milazzo, C. Shen, J.-S. Roe, J. L.Minder, F. Mercan, E. Wang, M. A. Eckersley-Maslin, A. E. Campbell, S. Kawaoka, S. Shareef, Z. Zhu, J. Kendall, M. Muhar, C. Haslinger, M. Yu, R. G. Roeder, M. H. Wigler, G. A. Blobel, J. Zuber, D. L. Spector, R. A. Young, C. R. Vakoc, Role of SWI/SNF in acute leukemia maintenance and enhancermediated Myc regulation. Genes Dev. 27, 2648-2662 (2013).
27. L. Ho, E. L. Miller, J. L. Ronan, W. Q. Ho, R. Jothi, G. R. Crabtree, esBAF facilitates pluripotency by conditioning the genome for LIF/STAT3 signalling and by regulating polycomb function. Nat. Cell Biol. 13, 903-913 (2011).
28. W.Qi, H. Chan, L. Teng, L. Li, S. Chuai, R. Zhang, J. Zeng, M. Li, H. Fan, Y. Lin, J. Gu, O. Ardayfio, J.-H. Zhang, X. Yan, J. Fang, Y. Mi, M. Zhang, T. Zhou, G. Feng, Z. Chen, G. Li, T. Yang, K. Zhao, X. Liu, Z. Yu, C. X. Lu, P. Atadja, E. Li, Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proc. Natl. Acad. Sci. U.S.A. 109, 21360-21365 (2012).
29. I. Versteege, N. Sévenet, J. Lange, M.-F. Rousseau-Merck, P. Ambros, R. Handgretinger, A. Aurias, O. Delattre, Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394, 203-206 (1998).
30. S. Jones, T.-L. Wang, I.-M. Shih, T.-L. Mao, K. Nakayama, R. Roden, R. Glas, D. Slamon, L. A. Diaz Jr., B. Vogelstein, K. W. Kinzler, V. E. Velculescu, N. Papadopoulos, Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330, 228-231 (2010).
31. K. C. Wiegand, S. P. Shah, O. M. Al-Agha, Y. Zhao, K. Tse, T. Zeng, J. Senz, M. K. McConechy, M. S. Anglesio, S. E. Kalloger, W. Yang, A. Heravi-Moussavi, R. Giuliany, C. Chow, J. Fee, A. Zayed, L. Prentice, N. Melnyk, G. Turashvili, A. D. Delaney, J. Madore, S. Yip, A. W. McPherson, G. Ha, L. Bell, S. Fereday, A. Tam, L. Galletta, P. N. Tonin, D. Provencher, D. Miller, S. J. Jones, R. A. Moore, G. B. Morin, A. Oloumi, N. Boyd, S. A. Aparicio, I. M. Shih, A.-M. Mes-Masson, D. D. Bowtell, M. Hirst, B. Gilks, M. A. Marra, D. G. Huntsman, ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 363, 1532-1543 (2010).
32. I. Varela, P. Tarpey, K. Raine, D. Huang, C. K. Ong, P. Stephens, H. Davies, D. Jones, M.-L. Lin, J. Teague, G. Bignell, A. Butler, J. Cho, G. L. Dalgliesh, D. Galappaththige, C. Greenman, C. Hardy, M. Jia, C. Latimer, K. W. Lau, J. Marshall, S. McLaren, A. Menzies, L. Mudie, L. Stebbings, D. A. Largaespada, L. F. A. Wessels, S. Richard, R. J. Kahnoski, J. Anema, D. A. Tuveson, P. A. Perez-Mancera, V. Mustonen, A. Fischer, D. J. Adams, A. Rust, W. Chan-on, C. Subimerb, K. Dykema, K. Furge, P. J. Campbell, B. T. Teh, M. R. Stratton, P. A. Futreal, Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469, 539-542 (2011).
33. M. Philpott, J. Yang, T. Tumber, O. Fedorov, S. Uttarkar, P. Filippakopoulos, S. Picaud, T. Keates, I. Felletar, A. Ciulli, S. Knapp, T. D. Heightman, Bromodomain-peptide displacement assays for interactome mapping and inhibitor discovery. Mol. BioSyst. 7, 2899-2908 (2011).
34. S. Tanaka, T. Kunath, A.-K. Hadjantonakis, A. Nagy, J. Rossant, Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075 (1998).
35. C. Trapnell, A. Roberts, L. Goff, G. Pertea, D. Kim, D. R. Kelley, H. Pimentel, S. L. Salzberg, J. L. Rinn, L. Pachter, Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).
36. M. D. Robinson, G. K. Smyth, Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics 9, 321-332 (2008).
37. S. Anders, W. Huber, Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
38. J. Wang, D. Duncan, Z. Shi, B. Zhang, WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): Update 2013. Nucleic Acids Res. 41, W77-W83 (2013).
39. W. Kabsch, XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
40. P. R. Evans, An introduction to data reduction: Space-group determination, scaling and intensity statistics. Acta Crystallogr. D Biol. Crystallogr. 67, 282-292 (2011).
41. A. J. McCoy, R. W. Grosse-Kunstleve, L. C. Storoni, R. J. Read, Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458-464 (2005).
42. G. Langer, S. X. Cohen, V. S. Lamzin, A. Perrakis, Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179 (2008).
43. P. Emsley, K. Cowtan, Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
44. G. N. Murshudov, A. A. Vagin, E. J. Dodson, Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
45. A. W. Schüttelkopf, D. M. F. van Aalten, PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D Biol. Crystallogr. 60, 1355-1363 (2004).
46. V. B. Chen, W. B. Arendall III, J. J. Headd, D. A. Keedy, R. M. Immormino, G. J. Kapral, L. W. Murray, J. S. Richardson, D. C. Richardson, MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
47. D. A. Case, J. T. V. Babin, R. M. Berryman, Q. Betz, D. S. Cai, T. E. Cerutti, I. Cheatham, T.A., R. E. Darden, H. Duke, A. W. Gohlke, S. Goetz, N. Gusarov, P. Homeyer, J. Janowski, I. Kaus, A. Kolossváry, T. S. Kovalenko, S. Lee, T. LeGrand, R. Luchko, B. X. W. Luo, AMBER 14 (2014).
48. D. Van Der Spoel, E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, H. J. C. Berendsen, GROMACS: Fast, flexible, and free. J. Comput. Chem. 26, 1701-1718 (2005).
49. W. L. Jorgensen, J. Chandrasekhar, J. D. Madura, R. W. Impey, M. L. Klein, Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935 (1983).
50. B. Hess, P-LINCS: A parallel linear constraint solver for molecular simulation. J. Chem. Theory Comput. 4, 116-122 (2007).
51. H. J. C. Berendsen, J. P. M. Postma, W. F. van Gunsteren, A. DiNola, J. R. Haak, Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690 (1984).
52. M. Parrinello, A. Rahman, Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys. 52, 7182-7190 (1981).
53. C. N. Nguyen, T. K. Young, M. K. Gilson, Grid inhomogeneous solvation theory: Hydration structure and thermodynamics of the miniature receptor cucurbit[7]uril. J. Chem. Phys. 137, 044101 (2012).
54. N. Michaud-Agrawal, E. J. Denning, T. B. Woolf, O. Beckstein, MDAnalysis: A toolkit for the analysis of molecular dynamics simulations. J. Comput. Chem. 32, 2319-2327 (2011).