Histone core phosphorylation regulates DNA accessibility

Journal of Biological Chemistry

Volumn 290, Issue 37, 2015, Pages 22612-22621

  Brehove, Matthew ^a   Wang, Tao ^a   North, Justin ^a   Luo, Yi ^a   Dreher, Sarah J ^a   Shimko, John C ^a,b   Ottesen, Jennifer J ^a,b   Luger, Karolin ^a,c   Poirier, Michael G ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; AMINO ACIDS; CELL DEATH; PHOSPHORYLATION; TRANSCRIPTION; TRANSPORTATION;

DNA REPLICATIONS; DNA TRANSCRIPTIONS; DNA-HISTONE INTERACTION; ENTRY EXITS; HISTONE H3; NUCLEOSOMES; REGULATORY COMPLEXES; TRANSCRIPTION REGULATIONS;

DNA;

DNA; HISTONE H3; LYSINE; LYSINE 56; THREONINE; THREONINE 45; TYROSINE; TYROSINE 41; UNCLASSIFIED DRUG; HISTONE; NUCLEOSOME;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DNA HISTONE INTERACTION; DNA TRANSCRIPTION; HISTONE PHOSPHORYLATION; MOLECULAR DYNAMICS; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; ACETYLATION; CHEMISTRY; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ACETYLATION; DNA; HISTONES; HUMANS; NUCLEOSOMES; PHOSPHORYLATION; TRANSCRIPTION, GENETIC;

EID: 84941578527     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.661363     Document Type: Article

References (62)

1. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260
2. Widom, J. (1998) Structure, dynamics, and function of chromatin in vitro. Annu. Rev. Biophys. Biomol. Struct. 27, 285-327
3. Luger, K. (2006) Dynamic nucleosomes. Chromosome Res. 14, 5-16
4. Ryan, D. P., and Owen-Hughes, T. (2011) Snf2-family proteins: chromatin remodellers for any occasion. Curr. Opin. Chem. Biol. 15, 649-656
5. Narlikar, G. J., Sundaramoorthy, R., and Owen-Hughes, T. (2013) Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154, 490-503
6. Bartholomew, B. (2014) Regulating the chromatin landscape: structural and mechanistic perspectives. Annu. Rev. Biochem. 83, 671-696
7. Loyola, A., and Almouzni, G. (2004) Histone chaperones, a supporting role in the limelight. Biochim. Biophys. Acta 1677, 3-11
8. Das, C., Tyler, J. K., and Churchill, M. E. (2010) The histone shuffle: histone chaperones in an energetic dance. Trends Biochem. Sci. 35, 476-489
9. Avvakumov, N., Nourani, A., and Côté, J. (2011) Histone chaperones: modulators of chromatin marks. Mol. Cell 41, 502-514
10. Bannister, A. J., and Kouzarides, T. (2011) Regulation of chromatin by histone modifications. Cell Res. 21, 381-395
11. Rothbart, S. B., and Strahl, B. D. (2014) Interpreting the language of histone and DNA modifications. Biochim. Biophys. Acta 1839, 627-643
12. Polach, K. J., and Widom, J. (1995) Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254, 130-149
13. Li, G., and Widom, J. (2004) Nucleosomes facilitate their own invasion. Nat. Struct. Mol. Biol. 11, 763-769
14. Bowman, G. D., and Poirier, M. G. (2015) Post-translational modifications of histones that influence nucleosome dynamics. Chem. Rev. 115, 2274-2295
15. Strahl, B. D., and Allis, C. D. (2000) The language of covalent histone modifications. Nature 403, 41-45
16. Cosgrove, M. S., Boeke, J. D., and Wolberger, C. (2004) Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 11, 1037-1043
17. Tropberger, P., and Schneider, R. (2013) Scratching the (lateral) surface of chromatin regulation by histone modifications. Nat. Struct. Mol. Biol. 20, 657-661
18. Zentner, G. E., and Henikoff, S. (2013) Regulation of nucleosome dynamics by histone modifications. Nat. Struct. Mol. Biol. 20, 259-266
19. Lo, K. A., Bauchmann, M. K., Baumann, A. P., Donahue, C. J., Thiede, M. A., Hayes, L. S., des Etages, S. A., and Fraenkel, E. (2011) Genome-wide profiling of H3K56 acetylation and transcription factor binding sites in human adipocytes. PLoS One 6, e19778
20. Tan, Y., Xue, Y., Song, C., and Grunstein, M. (2013) Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency. Proc. Natl. Acad. Sci. U. S. A. 110, 11493-11498
21. Chen, C. C., Carson, J. J., Feser, J., Tamburini, B., Zabaronick, S., Linger, J., and Tyler, J. K. (2008) Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134, 231-243
22. Li, Q., Zhou, H., Wurtele, H., Davies, B., Horazdovsky, B., Verreault, A., and Zhang, Z. (2008) Acetylation of histone H3 lysine 56 regulates replicationcoupled nucleosome assembly. Cell 134, 244-255
23. Das, C., Lucia, M. S., Hansen, K. C., and Tyler, J. K. (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459, 113-117
24. Xie, W., Song, C., Young, N. L., Sperling, A. S., Xu, F., Sridharan, R., Conway, A. E., Garcia, B. A., Plath, K., Clark, A. T., and Grunstein, M. (2009) Histone H3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol. Cell 33, 417-427
25. Xu, F., Zhang, K., and Grunstein, M. (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121, 375-385
26. Neumann, H., Hancock, S. M., Buning, R., Routh, A., Chapman, L., Somers, J., Owen-Hughes, T., van Noort, J., Rhodes, D., and Chin, J. W. (2009) A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell 36, 153-163
27. North, J. A., Shimko, J. C., Javaid, S., Mooney, A. M., Shoffner, M. A., Rose, S. D., Bundschuh, R., Fishel, R., Ottesen, J. J., and Poirier, M. G. (2012) Regulation of the nucleosome unwrapping rate controls DNA accessibility. Nucleic Acids Res. 40, 10215-10227
28. Shimko, J. C., North, J. A., Bruns, A. N., Poirier, M. G., and Ottesen, J. J. (2011) Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. J. Mol. Biol. 408, 187-204
29. Simon, M., North, J. A., Shimko, J. C., Forties, R. A., Ferdinand, M. B., Manohar, M., Zhang, M., Fishel, R., Ottesen, J. J., and Poirier, M. G. (2011) Histone fold modifications control nucleosome unwrapping and disassembly. Proc. Natl. Acad. Sci. U. S. A. 108, 12711-12716
30. Arnaudo, A. M., and Garcia, B. A. (2013) Proteomic characterization of novel histone post-translational modifications. Epigenetics Chromatin 6, 24
31. Dawson, M. A., Bannister, A. J., Göttgens, B., Foster, S. D., Bartke, T., Green, A. R., and Kouzarides, T. (2009) JAK2 phosphorylates histone H3Y41 and excludes HP1α from chromatin. Nature 461, 819-822
32. Hurd, P. J., Bannister, A. J., Halls, K., Dawson, M. A., Vermeulen, M., Olsen, J. V., Ismail, H., Somers, J., Mann, M., Owen-Hughes, T., Gout, I., and Kouzarides, T. (2009) Phosphorylation of histone H3 Thr-45 is linked to apoptosis. J. Biol. Chem. 284, 16575-16583
33. Griffiths, D. S., Li, J., Dawson, M. A., Trotter, M. W., Cheng, Y. H., Smith, A. M., Mansfield, W., Liu, P., Kouzarides, T., Nichols, J., Bannister, A. J., Green, A. R., and Göttgens, B. (2011) LIF-independent JAK signalling to chromatin in embryonic stem cells uncovered from an adult stem cell disease. Nat. Cell Biol. 13, 13-21
34. Dawson, M. A., Foster, S. D., Bannister, A. J., Robson, S. C., Hannah, R., Wang, X., Xhemalce, B., Wood, A. D., Green, A. R., Göttgens, B., and Kouzarides, T. (2012) Three distinct patterns of histone H3Y41 phosphorylation mark active genes. Cell Rep. 2, 470-477
35. Jang, S. M., Azebi, S., Soubigou, G., and Muchardt, C. (2014) DYRK1A phosphorylates histone H3 to differentially regulate the binding of HP1 isoforms and antagonize HP1-mediated transcriptional repression. EMBO Rep. 15, 686-694
36. Baker, S. P., Phillips, J., Anderson, S., Qiu, Q., Shabanowitz, J., Smith, M. M., Yates, J. R., 3rd, Hunt, D. F., and Grant, P. A. (2010) Histone H3 Thr 45 phosphorylation is a replication-associated post-translational modification in S. cerevisiae. Nat. Cell Biol. 12, 294-298
37. Casadio, F., Lu, X., Pollock, S. B., LeRoy, G., Garcia, B. A., Muir, T. W., Roeder, R. G., and Allis, C. D. (2013) H3R42me2a is a histone modification with positive transcriptional effects. Proc. Natl. Acad. Sci. U. S. A. 110, 14894-14899
38. Dyer, P. N., Edayathumangalam, R. S., White, C. L., Bao, Y., Chakravarthy, S., Muthurajan, U. M., and Luger, K. (2004) Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23-44
39. Hall, M. A., Shundrovsky, A., Bai, L., Fulbright, R. M., Lis, J. T., and Wang, M. D. (2009) High-resolution dynamic mapping of histone-DNA interactions in a nucleosome. Nat. Struct. Mol. Biol. 16, 124-129
40. Ngo, T. T., Zhang, Q., Zhou, R., Yodh, J. G., and Ha, T. (2015) Asymmetric unwrapping of nucleosomes under tension directed by DNA local flexibility. Cell 160, 1135-1144
41. Shimko, J. C., Howard, C. J., Poirier, M. G., and Ottesen, J. J. (2013) Preparing semisynthetic and fully synthetic histones H3 and H4 to modify the nucleosome core. Methods Mol. Biol. 981, 177-192
42. Mahto, S. K., Howard, C. J., Shimko, J. C., and Ottesen, J. J. (2011) A reversible protection strategy to improve Fmoc-SPPS of peptide thioesters by the N-acylurea approach. Chembiochem 12, 2488-2494
43. Little, J. W., Kim, B., Roland, K. L., Smith, M. H., Lin, L. L., and Slilaty, S. N. (1994) Cleavage of LexA repressor. Methods Enzymol. 244, 266-284
44. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J., and Svergun, D. I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
45. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
46. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-28786;
47. Correction (1999) Biophys J. 77, 2896-2896
48. Kozin, M. B., and Svergun, D. I. (2001) Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 34, 33-41
49. Volkov, V. V., and Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864
50. Yang, C., van der Woerd, M. J., Muthurajan, U. M., Hansen, J. C., and Luger, K. (2011) Biophysical analysis and small-angle X-ray scatteringderived structures of MeCP2-nucleosome complexes. Nucleic Acids Res. 39, 4122-4135
51. Guinier, A., and Fournet, G. (1955) Small-angle Scattering of x-rays. J. Polym. Sci. 19, 594, 10.1002/pol.1956.120199326
52. Clegg, R. M. (1992) Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol. 211, 353-388
53. Lowary, P. T., and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19-42
54. North, J. A., Šimon, M., Ferdinand, M. B., Shoffner, M. A., Picking, J. W., Howard, C. J., Mooney, A. M., van Noort, J., Poirier, M. G., and Ottesen, J. J. (2014) Histone H3 phosphorylation near the nucleosome dyad alters chromatin structure. Nucleic Acids Res. 42, 4922-4933
55. Schnitzler, G., Sif, S., and Kingston, R. E. (1998) Human SWI/SNF interconverts a nucleosome between its base state and a stable remodeled state. Cell 94, 17-27
56. Tachiwana, H., Kagawa, W., Shiga, T., Osakabe, A., Miya, Y., Saito, K., Hayashi-Takanaka, Y., Oda, T., Sato, M., Park, S. Y., Kimura, H., and Kurumizaka, H. (2011) Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476, 232-235
57. Dechassa, M. L., Wyns, K., Li, M., Hall, M. A., Wang, M. D., and Luger, K. (2011) Structure and Scm3-mediated assembly of budding yeast centromeric nucleosomes. Nat. Commun. 2, 313
58. Ranjith, P., Yan, J., and Marko, J. F. (2007) Nucleosome hopping and sliding kinetics determined from dynamics of single chromatin fibers in Xenopus egg extracts. Proc. Natl. Acad. Sci. U. S. A. 104, 13649-13654
59. Forties, R. A., North, J. A., Javaid, S., Tabbaa, O. P., Fishel, R., Poirier, M. G., and Bundschuh, R. (2011) A quantitative model of nucleosome dynamics. Nucleic Acids Res. 39, 8306-8313
60. Wang, X., and Hayes, J. J. (2008) Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol. Cell. Biol. 28, 227-236
61. Manohar, M., Mooney, A. M., North, J. A., Nakkula, R. J., Picking, J. W., Edon, A., Fishel, R., Poirier, M. G., and Ottesen, J. J. (2009) Acetylation of histone H3 at the nucleosome dyad alters DNA-histone binding. J. Biol. Chem. 284, 23312-23321
62. North, J. A., Javaid, S., Ferdinand, M. B., Chatterjee, N., Picking, J. W., Shoffner, M., Nakkula, R. J., Bartholomew, B., Ottesen, J. J., Fishel, R., and Poirier, M. G. (2011) Phosphorylation of histone H3 (T118) alters nucleosome dynamics and remodeling. Nucleic Acids Res. 39, 6465-6474