Signalling to chromatin through post-translational modifications of HMGN

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1799, Issue 1-2, 2010, Pages 93-100

  Pogna, Edgar A ^a   Clayton, Alison L ^a   Mahadevan, Louis C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Acetylation; HMGN; Immediate Early gene induction; Nucleocytoplasmic transport; Phosphorylation; Post translational modification

Indexed keywords

BINDING PROTEIN; HIGH MOBILITY GROUP A PROTEIN; HIGH MOBILITY GROUP B PROTEIN; HIGH MOBILITY GROUP N PROTEIN; HIGH MOBILITY GROUP N1 PROTEIN; HIGH MOBILITY GROUP N2 PROTEIN; HISTONE;

ACETYLATION; AMINO ACID SEQUENCE; CELLULAR DISTRIBUTION; CHROMATIN STRUCTURE; DNA STRUCTURE; ENZYME REGULATION; GENE ACTIVATION; GENE REGULATORY NETWORK; HUMAN; MITOSIS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CHROMATIN; CONSERVED SEQUENCE; HMGN PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 74449086311     PISSN: 18749399     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2009.11.018     Document Type: Review

References (60)

1. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 (1997) 251-260
2. Gerlitz G., Hock R., Ueda T., and Bustin M. The dynamics of HMG protein-chromatin interactions in living cells. Biochem. Cell Biol. 87 (2009) 127-137
3. Zhang Q., and Wang Y. High mobility group proteins and their post-translational modifications. Biochim. Biophys. Acta 1784 (2008) 1159-1166
4. Bianchi M.E., and Agresti A. HMG proteins: dynamic players in gene regulation and differentiation. Curr. Opin. Genet. Dev. 15 (2005) 496-506
5. Bustin M., and Reeves R. High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function. Prog. Nucleic Acid Res. Mol. Biol. 54 (1996) 35-100
6. Shirakawa H., Landsman D., Postnikov Y.V., and Bustin M. NBP-45, a novel nucleosomal binding protein with a tissue-specific and developmentally regulated expression. J. Biol. Chem. 275 (2000) 6368-6374
7. Rochman M., Postnikov Y., Correll S., Malicet C., Wincovitch S., Karpova T.S., McNally J.G., Wu X., Bubunenko N.A., Grigoryev S., and Bustin M. The interaction of NSBP1/HMGN5 with nucleosomes in euchromatin counteracts linker histone-mediated chromatin compaction and modulates transcription. Mol. Cell 35 (2009) 642-656
8. West K.L. HMGN proteins play roles in DNA repair and gene expression in mammalian cells. Biochem. Soc. Trans. 32 (2004) 918-919
9. Hock R., Furusawa T., Ueda T., and Bustin M. HMG chromosomal proteins in development and disease. Trends Cell Biol. 17 (2007) 72-79
10. Goodwin G.H., Walker J.M., and Johns E.W. In: Busch H. (Ed). The Cell Nucleus (1978), Academic Press, New York 181-219
11. Kuehl L., Salmond B., and Tran L. Concentrations of high-mobility-group proteins in the nucleus and cytoplasm of several rat tissues. J. Cell Biol. 99 (1984) 648-654
12. Boumba V.A., Seferiadis K., and Vougiouklakis T. Content of the HMG-17 chromosomal protein in porcine tissues. Protein Pept. Lett. 11 (2004) 515-519
13. Shirakawa H., Herrera J.E., Bustin M., and Postnikov Y. Targeting of high mobility group-14/-17 proteins in chromatin is independent of DNA sequence. J. Biol. Chem. 275 (2000) 37937-37944
14. Johns E.W. The HMG Chromosomal Proteins (1982), Academic Press, London, UK
15. Louie D.F., Gloor K.K., Galasinski S.C., Resing K.A., and Ahn N.G. Phosphorylation and subcellular redistribution of high mobility group proteins 14 and 17, analyzed by mass spectrometry. Protein Sci. 9 (2000) 170-179
16. Hock R., Scheer U., and Bustin M. Chromosomal proteins HMG-14 and HMG-17 are released from mitotic chromosomes and imported into the nucleus by active transport. J. Cell Biol. 143 (1998) 1427-1436
17. Prymakowska-Bosak M., Hock R., Catez F., Lim J.H., Birger Y., Shirakawa H., Lee K., and Bustin M. Mitotic phosphorylation of chromosomal protein HMGN1 inhibits nuclear import and promotes interaction with 14.3.3 proteins. Mol. Cell. Biol. 22 (2002) 6809-6819
18. Bustin M. Chromatin unfolding and activation by HMGN(*) chromosomal proteins. Trends Biochem. Sci. 26 (2001) 431-437
19. Ueda T., Catez F., Gerlitz G., and Bustin M. Delineation of the protein module that anchors HMGN proteins to nucleosomes in the chromatin of living cells. Mol. Cell. Biol. 28 (2008) 2872-2883
20. Ueda T., Postnikov Y.V., and Bustin M. Distinct domains in high mobility group N variants modulate specific chromatin modifications. J. Biol. Chem. 281 (2006) 10182-10187
21. Trieschmann L., Alfonso P.J., Crippa M.P., Wolffe A.P., and Bustin M. Incorporation of chromosomal proteins HMG-14/HMG-17 into nascent nucleosomes induces an extended chromatin conformation and enhances the utilization of active transcription complexes. EMBO J. 14 (1995) 1478-1489
22. Ding H.F., Bustin M., and Hansen U. Alleviation of histone H1-mediated transcriptional repression and chromatin compaction by the acidic activation region in chromosomal protein HMG-14. Mol. Cell. Biol. 17 (1997) 5843-5855
23. Alfonso P.J., Crippa M.P., Hayes J.J., and Bustin M. The footprint of chromosomal proteins HMG-14 and HMG-17 on chromatin subunits. J. Mol. Biol. 236 (1994) 189-198
24. Postnikov Y.V., Trieschmann L., Rickers A., and Bustin M. Homodimers of chromosomal proteins HMG-14 and HMG-17 in nucleosome cores. J. Mol. Biol. 252 (1995) 423-432
25. Phair R.D., and Misteli T. High mobility of proteins in the mammalian cell nucleus. Nature 404 (2000) 604-609
26. Phair R.D., Scaffidi P., Elbi C., Vecerova J., Dey A., Ozato K., Brown D.T., Hager G., Bustin M., and Misteli T. Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol. 24 (2004) 6393-6402
27. Sterner R., Vidali G., and Allfrey V.G. Studies of acetylation and deacetylation in high mobility group proteins. Identification of the sites of acetylation in high mobility group proteins 14 and 17. J. Biol. Chem. 256 (1981) 8892-8895
28. Bergel M., Herrera J.E., Thatcher B.J., Prymakowska-Bosak M., Vassilev A., Nakatani Y., Martin B., and Bustin M. Acetylation of novel sites in the nucleosomal binding domain of chromosomal protein HMG-14 by p300 alters its interaction with nucleosomes. J. Biol. Chem. 275 (2000) 11514-11520
29. Herrera J.E., Sakaguchi K., Bergel M., Trieschmann L., Nakatani Y., and Bustin M. Specific acetylation of chromosomal protein HMG-17 by PCAF alters its interaction with nucleosomes. Mol. Cell. Biol. 19 (1999) 3466-3473
30. Barratt M.J., Hazzalin C.A., Zhelev N., and Mahadevan L.C. A mitogen- and anisomycin-stimulated kinase phosphorylates HMG-14 in its basic amino-terminal domain in vivo and on isolated mononucleosomes. EMBO J. 13 (1994) 4524-4535
31. Thomson S., Mahadevan L.C., and Clayton A.L. MAP kinase-mediated signalling to nucleosomes and immediate-early gene induction. Semin. Cell. Dev. Biol. 10 (1999) 205-214
32. Jiang X.G., and Wang Y. Phosphorylation of human high mobility group N1 protein by protein kinase CK2. Biochem. Biophys. Res. Commun. 345 (2006) 1497-1503
33. Walton G.M., Gill G.N., Cooper E., and Spaulding S.W. Thyrotropin-stimulated phosphorylation of high mobility group protein 14 in vivo at the site catalyzed by cyclic nucleotide-dependent protein kinases in vitro. J. Biol. Chem. 259 (1984) 601-607
34. Soloaga A., Thomson S., Wiggin G.R., Rampersaud N., Dyson M.H., Hazzalin C.A., Mahadevan L.C., and Arthur J.S. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J. 22 (2003) 2788-2797
35. Lim J.H., Catez F., Birger Y., West K.L., Prymakowska-Bosak M., Postnikov Y.V., and Bustin M. Chromosomal protein HMGN1 modulates histone H3 phosphorylation. Mol. Cell 15 (2004) 573-584
36. Cooper E., Palmer R.J., and Spaulding S.W. TSH stimulates 32P-labeling of thyroid nuclear HMG 14, a protein associated with actively transcribed chromatin. Endocrinology 110 (1982) 1459-1461
37. Walton G.M., and Gill G.N. Identity of the in vivo phosphorylation site in high mobility group 14 protein in HeLa cells with the site phosphorylated by casein kinase II in vitro. J. Biol. Chem. 258 (1983) 4440-4446
38. Prymakowska-Bosak M., Misteli T., Herrera J.E., Shirakawa H., Birger Y., Garfield S., and Bustin M. Mitotic phosphorylation prevents the binding of HMGN proteins to chromatin. Mol. Cell. Biol. 21 (2001) 5169-5178
39. Phair R.D., Gorski S.A., and Misteli T. Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol. 375 (2004) 393-414
40. Walton G.M., Spiess J., and Gill G.N. Phosphorylation of high mobility group protein 14 by casein kinase II. J. Biol. Chem. 260 (1985) 4745-4750
41. Zou Y., Jiang X., and Wang Y. Identification of novel in vivo phosphorylation sites in high mobility group N1 protein from the MCF-7 human breast cancer cells. Biochemistry 43 (2004) 6322-6329
42. Cherukuri S., Hock R., Ueda T., Catez F., Rochman M., and Bustin M. Cell cycle-dependent binding of HMGN proteins to chromatin. Mol. Biol. Cell 19 (2008) 1816-1824
43. Hazzalin C.A., and Mahadevan L.C. MAPK-regulated transcription: a continuously variable gene switch?. Nat. Rev., Mol. Cell Biol. 3 (2002) 30-40
44. Clayton A.L., and Mahadevan L.C. MAP kinase-mediated phosphoacetylation of histone H3 and inducible gene regulation. FEBS Lett. 546 (2003) 51-58
45. Macdonald N., Welburn J.P., Noble M.E., Nguyen A., Yaffe M.B., Clynes D., Moggs J.G., Orphanides G., Thomson S., Edmunds J.W., Clayton A.L., Endicott J.A., and Mahadevan L.C. Molecular basis for the recognition of phosphorylated and phosphoacetylated histone H3 by 14-3-3. Mol. Cell 20 (2005) 199-211
46. Walter W., Clynes D., Tang Y., Marmorstein R., Mellor J., and Berger S.L. 14-3-3 interaction with histone H3 involves a dual modification pattern of phosphoacetylation. Mol. Cell. Biol. 28 (2008) 2840-2849
47. Winter S., Simboeck E., Fischle W., Zupkovitz G., Dohnal I., Mechtler K., Ammerer G., and Seiser C. 14-3-3 proteins recognize a histone code at histone H3 and are required for transcriptional activation. EMBO J. 27 (2008) 88-99
48. Clayton A.L., Rose S., Barratt M.J., and Mahadevan L.C. Phosphoacetylation of histone H3 on c-fos- and c-jun-associated nucleosomes upon gene activation. EMBO J. 19 (2000) 3714-3726
49. Cheung P., Tanner K.G., Cheung W.L., Sassone-Corsi P., Denu J.M., and Allis C.D. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 5 (2000) 905-915
50. Hazzalin C.A., and Mahadevan L.C. Dynamic acetylation of all lysine 4-methylated histone h3 in the mouse nucleus: analysis at c-fos and c-jun. PLoS Biol. 3 (2005) e393 10.1371/journal.pbio.0030393
51. Clayton A.L., Hazzalin C.A., and Mahadevan L.C. Enhanced histone acetylation and transcription: a dynamic perspective. Mol. Cell 23 (2006) 289-296
52. Kouzarides T. Chromatin modifications and their function. Cell 128 (2007) 693-705
53. Shahbazian M.D., and Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76 (2007) 75-100
54. Lim J.H., West K.L., Rubinstein Y., Bergel M., Postnikov Y.V., and Bustin M. Chromosomal protein HMGN1 enhances the acetylation of lysine 14 in histone H3. EMBO J. 24 (2005) 3038-3048
55. Birger Y., West K.L., Postnikov Y.V., Lim J.H., Furusawa T., Wagner J.P., Laufer C.S., Kraemer K.H., and Bustin M. Chromosomal protein HMGN1 enhances the rate of DNA repair in chromatin. EMBO J. 22 (2003) 1665-1675
56. Thomson S., Clayton A.L., and Mahadevan L.C. Independent dynamic regulation of histone phosphorylation and acetylation during immediate-early gene induction. Mol. Cell 8 (2001) 1231-1241
57. Cheung P., Allis C.D., and Sassone-Corsi P. Signaling to chromatin through histone modifications. Cell 103 (2000) 263-271
58. Hirota T., Lipp J.J., Toh B.H., and Peters J.M. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438 (2005) 1176-1180
59. Morrison D.K. The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol. 19 (2009) 16-23
60. Pallier C., Scaffidi P., Chopineau-Proust S., Agresti A., Nordmann P., Bianchi M.E., and Marechal V. Association of chromatin proteins high mobility group box (HMGB) 1 and HMGB2 with mitotic chromosomes. Mol. Biol. Cell 14 (2003) 3414-3426