Abstract
Members of the ATP-dependent family of chromatin remodeling enzymes play key roles in the regulation of transcription, development, DNA repair and cell cycle control. We find that the remodeling activities of the ySWI/SNF, hSWI/SNF, xMi-2 and xACF complexes are nearly abolished by incorporation of linker histones into nucleosomal array substrates. Much of this inhibition is independent of linker histone-induced folding of the arrays. We also find that phosphorylation of the linker histone by Cdc2/Cyclin B kinase can rescue remodeling by ySWI/SNF. These results suggest that linker histones exert a global, genome-wide control over remodeling activities, implicating a new, obligatory coupling between linker histone kinases and ATP-dependent remodeling enzymes.
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Fletcher, T.M. & Hansen, J.C. Crit. Rev. Eukaryot. Gene Expr. 6, 149–188 (1996).
Carruthers, L.M., Bednar, J., Woodcock, C.L. & Hansen, J.C. Biochemistry 37, 14776–14787 (1998).
Carruthers, L.M. & Hansen, J.C. J. Biol. Chem. 275, 37285–37290 (2000).
Hansen, J.C., Tse, C. & Wolffe, A.P. Biochemistry 37, 17637–17641 (1998).
Strahl, B.D. & Allis, C.D. Nature 403, 41–45 (2000).
Vignali, M., Hassan, A.H., Neely, K.E. & Workman, J.L. Mol. Cell. Biol. 20, 1899–1910 (2000).
Peterson, C.L. & Workman, J.L. Curr. Opin. Genet. Dev. 10, 187–192 (2000).
Havas, K. et al. Cell 103, 1133–1142 (2000).
Gavin, I., Horn, P.J. & Peterson, C.L. Mol. Cell 7, 97–104 (2001).
Logie, C. & Peterson, C.L. EMBO J. 16, 6772–6782 (1997).
Carruthers, L.M., Tse, C., Walker, K.P. III & Hansen, J.C. Methods Enzymol. 304, 19–35 (1999).
Polach, K.J. & Widom, J. J. Mol. Biol. 254, 130–149 (1995).
Boyer, L.A. et al. J. Biol. Chem. 275, 18864–18870 (2000).
Garcia-Ramirez, M., Dong, F. & Ausio, J. J. Biol. Chem. 267, 19587–19595 (1992).
Fletcher, T.M. & Hansen, J.C. J. Biol. Chem. 270, 25359–25362 (1995).
Tse, C. & Hansen, J.C. Biochemistry 36, 11381–11388 (1997).
Hill, D.A. & Imbalzano, A.N. Biochemistry 39, 11649–11656 (2000).
Quinn, J., Fyrberg, A.M., Ganster, R.W., Schmidt, M.C. & Peterson, C.L. Nature 379, 844–847 (1996).
Hill, C.S., Rimmer, J.M., Green, B.N., Finch, J.T. & Thomas, J.O. EMBO J. 10, 1939–1948 (1991).
Solomon, M.J., Lee, T. & Kirschner, M.W. Mol. Biol. Cell 3, 13–27 (1992).
Varga-Weisz, P.D., Blank, T.A. & Becker, P.B. EMBO J. 14, 2209–2216 (1995).
Roth, S.Y. & Allis, C.D. Trends Biochem. Sci. 17, 93–98 (1992).
Lever, M.A., Th'ng, J.P., Sun, X. & Hendzel, M.J. Nature 408, 873–876 (2000).
Misteli, T., Gunjan, A., Hock, R., Bustin, M. & Brown, D.T. Nature 408, 877–881 (2000).
Dou, Y., Mizzen, C.A., Abrams, M., Allis, C.D. & Gorovsky, M.A. Mol. Cell 4, 641–647 (1999).
Bhattacharjee, R.N., Banks, G.C., Trotter, K.W., Lee, H.L. & Archer, T.K. Mol. Cell. Biol. 21, 5417–5425 (2001).
Shanahan, F., Seghezzi, W., Parry, D., Mahony, D. & Lees, E. Mol. Cell. Biol. 19, 1460–1469 (1999).
Logie, C. & Peterson, C.L. Methods Enzymol. 304, 726–741 (1999).
Sif, S., Stukenberg, P.T., Kirschner, M.W. & Kingston, R.E. Genes Dev. 12, 2842–2851 (1998).
Guschin, D. et al. J. Biol. Chem. 275, 35248–35255 (2000).
Wade, P.A., Jones, P.L., Vermaak, D. & Wolffe, A.P. Curr. Biol. 8, 843–846 (1998).
Acknowledgements
These studies were supported by grants from the NIH to C.L.P. and J.C.H., a NIH NRSA to P.J.H, and a PO1 from the NCI to C.L.P. and A.N.I.
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Horn, P., Carruthers, L., Logie, C. et al. Phosphorylation of linker histones regulates ATP-dependent chromatin remodeling enzymes. Nat Struct Mol Biol 9, 263–267 (2002). https://doi.org/10.1038/nsb776
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DOI: https://doi.org/10.1038/nsb776
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