Phosphorylation of the Linker Histone H1 by CDK Regulates Its Binding to HP1α

Molecular Cell

Volumn 22, Issue 5, 2006, Pages 693-699

  Hale, Tracy K ^a   Contreras, Alejandro ^a   Morrison, Ashby J ^a   Herrera, Rafael E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

CELLCYCLE; DNA

Indexed keywords

HETEROCHROMATIN PROTEIN 1;

ARTICLE; CELL CYCLE; CONTROLLED STUDY; GENETIC LINKAGE; HUMAN; HUMAN CELL; METHYLATION; PHOSPHORYLATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

BINDING SITES; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CYCLIN-DEPENDENT KINASE 2; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HISTONES; HUMANS; INTERPHASE; MICE; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; TUMOR CELLS, CULTURED;

MAMMALIA;

EID: 33744548700     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.04.016     Document Type: Article

References (34)

1. Alexandrow M.G., and Hamlin J.L. Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. J. Cell Biol. 168 (2005) 875-886
2. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., and Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 (2001) 120-124
3. Carruthers L.M., Bednar J., Woodcock C.L., and Hansen J.C. Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: mechanistic ramifications for higher-order chromatin folding. Biochemistry 37 (1998) 14776-14787
4. Contreras A., Hale T.K., Stenoien D.L., Rosen J.M., Mancini M.A., and Herrera R.E. The dynamic mobility of histone H1 is regulated by cyclin/CDK phosphorylation. Mol. Cell. Biol. 23 (2003) 8626-8636
5. Cowell I.G., Aucott R., Mahadevaiah S.K., Burgoyne P.S., Huskisson N., Bongiorni S., Prantera G., Fanti L., Pimpinelli S., Wu R., et al. Heterochromatin, HP1 and methylation at lysine 9 of histone H3 in animals. Chromosoma 111 (2002) 22-36
6. Daujat S., Zeissler U., Waldmann T., Happel N., and Schneider R. HP1 binds specifically to K26 methylated histone H1.4, whereas simultaneous S27 phosphorylation blocks HP1 binding. J. Biol. Chem. 280 (2005) 38090-38095
7. Dion M.F., Altschuler S.J., Wu L.F., and Rando O.J. Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl. Acad. Sci. USA 102 (2005) 5501-5506
8. Eissenberg J.C., and Elgin S.C. The HP1 protein family: getting a grip on chromatin. Curr. Opin. Genet. Dev. 10 (2000) 204-210
9. Fan Y., Nikitina T., Morin-Kensicki E.M., Zhao J., Magnuson T.R., Woodcock C.L., and Skoultchi A.I. H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol. Cell. Biol. 23 (2003) 4559-4572
10. Garcia B.A., Busby S.A., Barber C.M., Shabanowitz J., Allis C.D., and Hunt D.F. Characterization of phosphorylation sites on histone H1 isoforms by tandem mass spectrometry. J. Proteome Res. 3 (2004) 1219-1227
11. Hansen J.C. Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu. Rev. Biophys. Biomol. Struct. 31 (2002) 361-392
12. Henikoff S. Histone modifications: combinatorial complexity or cumulative simplicity?. Proc. Natl. Acad. Sci. USA 102 (2005) 5308-5309
13. Herrera R.E., Chen F., and Weinberg R.A. Increased histone H1 phosphorylation and relaxed chromatin structure in Rb-deficient fibroblasts. Proc. Natl. Acad. Sci. USA 93 (1996) 11510-11515
14. Hinds P.W., Mittnacht S., Dulic V., Arnold A., Reed S.I., and Weinberg R.A. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70 (1992) 993-1006
15. Jenuwein T., and Allis C.D. Translating the histone code. Science 293 (2001) 1074-1080
16. Karpova T.S., Baumann C.T., He L., Wu X., Grammer A., Lipsky P., Hager G.L., and McNally J.G. Fluorescence resonance energy transfer from cyan to yellow fluorescent protein detected by acceptor photobleaching using confocal microscopy and a single laser. J. Microsc. 209 (2003) 56-70
17. Liu C.L., Kaplan T., Kim M., Buratowski S., Schreiber S.L., Friedman N., and Rando O.J. Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3 (2005) e328 10.1371/journal.pbio.0030328
18. Maison C., and Almouzni G. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5 (2004) 296-304
19. Maison C., Bailly D., Peters A.H., Quivy J.P., Roche D., Taddei A., Lachner M., Jenuwein T., and Almouzni G. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30 (2002) 329-334
20. Meehan R.R., Kao C.F., and Pennings S. HP1 binding to native chromatin in vitro is determined by the hinge region and not by the chromodomain. EMBO J. 22 (2003) 3164-3174
21. Minc E., Allory Y., Worman H.J., Courvalin J.C., and Buendia B. Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 108 (1999) 220-234
22. Muchardt C., Guilleme M., Seeler J.S., Trouche D., Dejean A., and Yaniv M. Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep. 3 (2002) 975-981
23. Nielsen A.L., Oulad-Abdelghani M., Ortiz J.A., Remboutsika E., Chambon P., and Losson R. Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. Mol. Cell 7 (2001) 729-739
24. Ohtsubo M., Theodoras A.M., Schumacher J., Roberts J.M., and Pagano M. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell. Biol. 15 (1995) 2612-2624
25. Platero J.S., Hartnett T., and Eissenberg J.C. Functional analysis of the chromo domain of HP1. EMBO J. 14 (1995) 3977-3986
26. Powers J.A., and Eissenberg J.C. Overlapping domains of the heterochromatin-associated protein HP1 mediate nuclear localization and heterochromatin binding. J. Cell Biol. 120 (1993) 291-299
27. Roth S.Y., and Allis C.D. Chromatin condensation: does histone H1 dephosphorylation play a role?. Trends Biochem. Sci. 17 (1992) 93-98
28. Stewart M.D., Li J., and Wong J. Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment. Mol. Cell. Biol. 25 (2005) 2525-2538
29. Talasz H., Helliger W., Puschendorf B., and Lindner H. In vivo phosphorylation of histone H1 variants during the cell cycle. Biochemistry 35 (1996) 1761-1767
30. Th'ng J.P., Sung R., Ye M., and Hendzel M.J. H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. J. Biol. Chem. 280 (2005) 27809-27814
31. Truong K., and Ikura M. The use of FRET imaging microscopy to detect protein-protein interactions and protein conformational changes in vivo. Curr. Opin. Struct. Biol. 11 (2001) 573-578
32. van Holde K. Chromatin (1989), Springer-Verlag, Heidelberg, Germany
33. Vaquero A., Scher M., Lee D., Erdjument-Bromage H., Tempst P., and Reinberg D. Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol. Cell 16 (2004) 93-105
34. Zhu L., van den Heuvel S., Helin K., Fattaey A., Ewen M., Livingston D., Dyson N., and Harlow E. Inhibition of cell proliferation by p107, a relative of the retinoblastoma protein. Genes Dev. 7 (1993) 1111-1125