Distinct properties of human HMGN5 reveal a rapidly evolving but functionally conserved nucleosome binding protein

Molecular and Cellular Biology

Volumn 31, Issue 13, 2011, Pages 2742-2755

  Malicet, Cedric ^a   Rochman, Mark ^a   Postnikov, Yuri ^a   Bustin, Michael ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; HIGH MOBILITY GROUP N PROTEIN; HIGH MOBILITY GROUP N PROTEIN 5; HISTONE H1; HISTONE H5; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CHROMATIN; CONTROLLED STUDY; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; HETEROCHROMATIN; HUMAN; HUMAN CELL; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHROMATIN; CHROMOSOMES, HUMAN, X; CONSERVED SEQUENCE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTONES; HMGN PROTEINS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RNA, SMALL INTERFERING; TRANS-ACTIVATORS;

VERTEBRATA;

EID: 79959392729     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05216-11     Document Type: Article

References (43)

1. Alfonso, P. J., M. P. Crippa, J. J. Hayes, and M. Bustin. 1994. The footprint of chromosomal proteins HMG-14 and HMG-17 on chromatin subunits. J. Mol. Biol. 236:189-198.
2. Belova, G. I., Y. V. Postnikov, T. Furusawa, Y. Birger, and M. Bustin. 2008. Chromosomal protein HMGN1 enhances the heat shock-induced remodeling of Hsp70 chromatin. J. Biol. Chem. 283:8080-8088.
3. Bianchi, M. E., and A. Agresti. 2005. HMG proteins: dynamic players in gene regulation and differentiation. Curr. Opin. Genet. Dev. 15:496-506.
4. Birger, Y., et al. 2005. Increased tumorigenicity and sensitivity to ionizing radiation upon loss of chromosomal protein HMGN1. Cancer Res. 65:6711-6718.
5. Bustin, M. 2001. Chromatin unfolding and activation by HMGN(*) chromosomal proteins. Trends Biochem. Sci. 26:431-437.
6. Bustin, M. 1999. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 19:5237-5246.
7. Bustin, M., F. Catez, and J. H. Lim. 2005. The dynamics of histone H1 function in chromatin. Mol. Cell 17:617-620.
8. Bustin, M., and R. D. Cole. 1970. Regions of high and low cationic charge in a lysine-rich histone. J. Biol. Chem. 245:1458-1466.
9. Bustin, M., and R. Reeves. 1996. High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function. Prog. Nucleic Acid Res. Mol. Biol. 54:35-100.
10. Catez, F., D. T. Brown, T. Misteli, and M. Bustin. 2002. Competition between histone H1 and HMGN proteins for chromatin binding sites. EMBO Rep. 3:760-766.
11. Catez, F., and R. Hock. 2010. Binding and interplay of HMG proteins on chromatin: lessons from live cell imaging. Biochim. Biophys. Acta 1799: 15-27.
12. Catez, F., T. Ueda, and M. Bustin. 2006. Determinants of histone H1 mobility and chromatin binding in living cells. Nat. Struct. Mol. Biol. 13:305-310.
13. Catez, F., et al. 2004. Network of dynamic interactions between histone H1 and high-mobility-group proteins in chromatin. Mol. Cell. Biol. 24:4321-4328.
14. Cato, L., K. Stott, M. Watson, and J. O. Thomas. 2008. The interaction of HMGB1 and linker histones occurs through their acidic and basic tails. J. Mol. Biol. 384:1262-1272.
15. Crippa, M. P., P. J. Alfonso, and M. Bustin. 1992. Nucleosome core binding region of chromosomal protein HMG-17 acts as an independent functional domain. J. Mol. Biol. 228:442-449.
16. Ding, H. F., S. Rimsky, S. C. Batson, M. Bustin, and U. Hansen. 1994. Stimulation of RNA polymerase II elongation by chromosomal protein HMG-14. Science 265:796-799.
17. Dunker, A. K., I. Silman, V. N. Uversky, and J. L. Sussman. 2008. Function and structure of inherently disordered proteins. Curr. Opin. Struct. Biol. 18:756-764.
18. Hofmann, K., P. Bucher, L. Falquet, and A. Bairoch. 1999. The PROSITE database, its status in 1999. Nucleic Acids Res. 27:215-219.
19. Khil, P. P., B. Oliver, and R. D. Camerini-Otero. 2005. X for intersection: retrotransposition both on and off the X chromosome is more frequent. Trends Genet. 21:3-7.
20. Kim, Y. C., et al. 2009. Activation of ATM depends on chromatin interactions occurring before induction of DNA damage. Nat. Cell Biol. 11:92-96.
21. King, L. M., and C. A. Francomano. 2001. Characterization of a human gene encoding nucleosomal binding protein NSBP1. Genomics 71:163-173.
22. Lim, J. H., et al. 2004. Chromosomal protein HMGN1 modulates histone H3 phosphorylation. Mol. Cell 15:573-584.
23. Lim, J. H., et al. 2005. Chromosomal protein HMGN1 enhances the acetylation of lysine 14 in histone H3. EMBO J. 24:3038-3048.
24. Lu, X., B. Hamkalo, M. H. Parseghian, and J. C. Hansen. 2009. Chromatin condensing functions of the linker histone C-terminal domain are mediated by specific amino acid composition and intrinsic protein disorder. Biochemistry 48:164-172.
25. Misteli, T., A. Gunjan, R. Hock, M. Bustin, and D. T. Brown. 2000. Dynamic binding of histone H1 to chromatin in living cells. Nature 408:877-881.
26. Oldfield, C. J., et al. 2008. Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. BMC Genomics 9(Suppl. 1):S1.
27. Postnikov, Y., and M. Bustin. 2010. Regulation of chromatin structure and function by HMGN proteins. Biochim. Biophys. Acta 1799:62-68.
28. Postnikov, Y. V., and M. Bustin. 1999. Reconstitution of high mobility group 14/17 proteins into nucleosomes and chromatin. Methods Enzymol. 304:133-155.
29. Postnikov, Y. V., L. Trieschmann, A. Rickers, and M. Bustin. 1995. Homodimers of chromosomal proteins HMG-14 and HMG-17 in nucleosome cores. J. Mol. Biol. 252:423-432.
30. Rattner, B. P., T. Yusufzai, and J. T. Kadonaga. 2009. HMGN proteins act in opposition to ATP-dependent chromatin remodeling factors to restrict nucleosome mobility. Mol. Cell 34:620-626.
31. Rochman, M., C. Malicet, and M. Bustin. 2010. HMGN5/NSBP1: a new member of the HMGN protein family that affects chromatin structure and function. Biochim. Biophys. Acta 1799:86-92.
32. Rochman, M., et al. 2009. The interaction of NSBP1/HMGN5 with nucleosomes in euchromatin counteracts linker histone-mediated chromatin compaction and modulates transcription. Mol. Cell 35:642-656.
33. Rochman, M., et al. Effects of HMGN variants on the cellular transcription profile. Nucleic Acids Res., in press.
34. Shirakawa, H., D. Landsman, Y. V. Postnikov, and M. Bustin. 2000. NBP-45, a novel nucleosomal binding protein with a tissue-specific and developmentally regulated expression. J. Biol. Chem. 275:6368-6374.
35. Shirakawa, H., et al. 2009. The nucleosomal binding protein NSBP1 is highly expressed in the placenta and modulates the expression of differentiation markers in placental Rcho-1 cells. J. Cell Biochem. 106:651-658.
36. Soutoglou, E., and T. Misteli. 2008. Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320:1507-1510.
37. Sprague, B. L., and J. G. McNally. 2005. FRAP analysis of binding: proper and fitting. Trends Cell Biol. 15:84-91.
38. Stasevich, T. J., F. Mueller, D. T. Brown, and J. G. McNally. 2010. Dissecting the binding mechanism of the linker histone in live cells: an integrated FRAP analysis. EMBO J. 29:1225-1234.
39. Ueda, T., F. Catez, G. Gerlitz, and M. Bustin. 2008. Delineation of the protein module that anchors HMGN proteins to nucleosomes in the chromatin of living cells. Mol. Cell. Biol. 28:2872-2883.
40. Vandepoele, K., W. De Vos, J. S. Taylor, A. Meyer, and Y. Van de Peer. 2004. Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc. Natl. Acad. Sci. U. S. A. 101:1638-1643.
41. Vestner, B., M. Bustin, and C. Gruss. 1998. Stimulation of replication efficiency of a chromatin template by chromosomal protein HMG-17. J. Biol. Chem. 273:9409-9414.
42. Woodcock, C. L., A. I. Skoultchi, and Y. Fan. 2006. Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res. 14:17-25.
43. Zhu, N., and U. Hansen. 2010. Transcriptional regulation by HMGN proteins. Biochim. Biophys. Acta 1799:74-79.