The chromatin-binding protein HMGN3 stimulates histone acetylation and transcription across the Glyt1 gene

Biochemical Journal

Volumn 442, Issue 3, 2012, Pages 495-505

  Barkess, Gráinne ^a   Postnikov, Yuri ^b   Campos, Chrisanne D ^a   Mishra, Shivam ^a   Mohan, Gokula ^a   Verma, Sakshi ^a   Bustin, Michael ^b   West, Katherine L ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Acetylation; Chromatin; Elongation; Epigenetics; HMGN; p300 CREB (cAMP response element binding protein) binding protein associated factor (PCAF)

Indexed keywords

BINDING PROTEIN; CHROMATIN BINDING PROTEIN HMGN1; CHROMATIN BINDING PROTEIN HMGN2; CHROMATIN BINDING PROTEIN HMGN3; CHROMATIN BINDING PROTEIN HMGN3A; CHROMATIN BINDING PROTEIN HMGN3B; GLYCINE TRANSPORTER 1; LYSINE; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE LOCUS; HISTONE ACETYLATION; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING;

ACETYLATION; ANIMALS; BINDING SITES; CELL LINE; CHROMATIN; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; HISTONES; HMGN PROTEINS; MICE; TRANSFECTION;

EID: 84857885406     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111502     Document Type: Article

References (58)

1. Postnikov, U. and Bustin, M. (2010) Regulation of chromatin structure and function by HMGN proteins. Biochim. Biophys. Acta 1799, 62-68
2. Rochman, M., Taher, L., Kurahashi, T., Cherukuri, S., Uversky, V. N., Landsman, D., Ovcharenko, I. and Bustin, M. (2011) Effects of HMGN variants on the cellular transcription profile. Nucleic Acids Res. 39, 1-12
3. West, K. L., Castellini, M. A., Duncan, M. K. and Bustin, M. (2004) Chromosomal proteins HMGN3a and HMGN3b regulate the expression of glycine transporter 1. Mol. Cell. Biol. 24, 3747-3756 (Pubitemid 38496154)
4. 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. (2003) Chromosomal protein HMGN1 enhances the rate of DNA repair in chromatin. EMBO J. 22, 1665-1675 (Pubitemid 36417414)
5. Vestner, B., Bustin, M. and Gruss, C. (1998) Stimulation of replication efficiency of a chromatin template by chromosomal protein HMG-17. J. Biol. Chem. 273, 9409-9414 (Pubitemid 28183021)
6. Furusawa, T.C.S. (2010) Developmental function of HMGN proteins. Biochim. Biophys. Acta 1799, 69-73
7. Bustin, M. (2001) Chromatin unfolding and activation by HMGN(*) chromosomal proteins. Trends Biochem. Sci. 26, 431-437
8. Rochman, M., Malicet, C. and Bustin, M. (2010) HMGN5/NSBP1: a new member of the HMGN protein family that affects chromatin structure and function. Biochim. Biophys. Acta 1799, 86-92
9. West, K. L., Ito, Y., Birger, Y., Postnikov, Y., Shirakawa, H. and Bustin, M. (2001) HMGN3a and HMGN3b, two protein isoforms with a tissue-specific expression pattern, expand the cellular repertoire of nucleosome-binding proteins. J. Biol. Chem. 276, 25959-25969
10. Trieschmann, L., Alfonso, P. J., Crippa, M. P., Wolffe, A. P. and Bustin, M. (1995) 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, 1478-1489
11. Ding, H. F., Bustin, M. and Hansen, U. (1997) Alleviation of histone H1-mediated transcriptional repression and chromatin compaction by the acidic activation region in chromosomal protein HMG-14. Mol. Cell. Biol. 17, 5843-5855 (Pubitemid 27411091)
12. Paranjape, S. M., Krumm, A. and Kadonaga, J. T. (1995) HMG17 is a chromatin-specific transcriptional coactivator that increases the efficiency of transcription initiation. Genes Dev. 9, 1978-1991
13. Catez, F., Brown, D. T., Misteli, T. and Bustin, M. (2002) Competition between histone H1 and HMGN proteins for chromatin binding sites. EMBO Rep. 3, 760-766. (Pubitemid 34966015)
14. Rattner, B. P., Yusufzai, T. and Kadonaga, J. T. (2009) HMGN proteins act in opposition to ATP-dependent chromatin remodeling factors to restrict nucleosome mobility. Mol. Cell 34, 620-626
15. Lim, J. H., West, K. L., Rubinstein, Y., Bergel, M., Postnikov, Y. V. and Bustin, M. (2005) Chromosomal protein HMGN1 enhances the acetylation of lysine 14 in histone H3. EMBO J. 24, 3038-3048 (Pubitemid 41486340)
16. Ueda, T., Postnikov, Y. V. and Bustin, M. (2006) Distinct domains in high mobility group N variants modulate specific chromatin modifications. J. Biol. Chem. 281, 10182-10187 (Pubitemid 43864554)
17. Lim, J. H., Catez, F., Birger, Y., West, K. L., Prymakowska-Bosak, M., Postnikov, Y. V. and Bustin, M. (2004) Chromosomal protein HMGN1 modulates histone H3 phosphorylation. Mol. Cell 15, 573-584 (Pubitemid 39141784)
18. Shimada, M., Nakadai, T., Fukuda, A. and Hisatake, K. (2010) cAMP-response element-binding protein (CREB) controls MSK1-mediated phosphorylation of histone H3 at the c-fos promoter in vitro. J. Biol. Chem. 285, 9390-9401
19. Postnikov, Y. V., Belova, G. I., Lim, J. H. and Bustin, M. (2006) Chromosomal protein HMGN1 modulates the phosphorylation of serine 1 in histone H2A. Biochemistry 45, 15092-15099 (Pubitemid 44937022)
20. Amano, T., Leu, K., Yoshizato, K. and Shi, Y. B. (2002) Thyroid hormone regulation of a transcriptional coactivator in Xenopus laevis: implication for a role in postembryonic tissue remodeling. Dev. Dyn. 223, 526-535 (Pubitemid 34273457)
21. Amen, M., Espinoza, H. M., Cox, C., Liang, X., Wang, J., Link, T. M., Brennan, R. G., Martin, J. F. and Amendt, B. A. (2008) Chromatin-associated HMG-17 is a major regulator of homeodomain transcription factor activity modulated by Wnt/β-catenin signaling. Nucleic Acids Res. 36, 462-476 (Pubitemid 351250439)
22. Zhu, N. and Hansen, U. (2007) HMGN1 modulates estrogen-mediated transcriptional activation through interactions with specific DNA-binding transcription factors. Mol. Cell. Biol. 27, 8859-8873
23. Ueda, T., Furusawa, T., Kurahashi, T., Tessarollo, L. and Bustin, M. (2009) The nucleosome binding protein HMGN3 modulates the transcription profile of pancreatic β cells and affects insulin secretion. Mol. Cell. Biol. 29, 5264-5276
24. Furusawa, T., Lim, J. H., Catez, F., Birger, Y., Mackem, S. and Bustin, M. (2006) Down-regulation of nucleosomal binding protein HMGN1 expression during embryogenesis modulates Sox9 expression in chondrocytes. Mol. Cell. Biol. 26, 592-604 (Pubitemid 43089771)
25. Belova, G. I., Postnikov, Y. V., Furusawa, T., Birger, Y. and Bustin, M. (2008) Chromosomal protein HMGN1 enhances the heat shock-induced remodeling of Hsp70 chromatin. J. Biol. Chem. 283, 8080-8088
26. Cuddapah, S., Schones, D. E., Cui, K., Roh, T. Y., Barski, A., Wei, G., Rochman, M., Bustin, M. and Zhao, K. (2011) Genomic profiling of HMGN1 reveals an association with chromatin at regulatory regions. Mol. Cell. Biol. 31, 700-709
27. Zafra, F. and Gimenez, C. (2008) Glycine transporters and synaptic function. IUBMB Life 60, 810-817
28. Kim, K. M., Kingsmore, S. F., Han, H., Yang-Feng, T. L., Godinot, N., Seldin, M. F., Caron, M. G. and Giros, B. (1994) Cloning of the human glycine transporter type 1: molecular and pharmacological characterization of novel isoform variants and chromosomal localization of the gene in the human and mouse genomes. Mol. Pharmacol. 45, 608-617 (Pubitemid 24139187)
29. Trieschmann, L., Martin, B. and Bustin, M. (1998) The chromatin unfolding domain of chromosomal protein HMG-14 targets the N-terminal tail of histone H3 in nucleosomes. Proc. Natl. Acad. Sci. U.S.A. 95, 5468-5473 (Pubitemid 28224117)
30. Crippa, M. P., Alfonso, P. J. and Bustin, M. (1992) Nucleosome core binding region of chromosomal protein HMG-17 acts as an independent functional domain. J. Mol. Biol. 228, 442-449 (Pubitemid 23007567)
31. Rada-Iglesias, A., Enroth, S., Ameur, A., Koch, C. M., Clelland, G. K., Respuela-Alonso, P., Wilcox, S., Dovey, O. M., Ellis, P. D., Langford, C. F. et al. (2007) Butyrate mediates decrease of histone acetylation centered on transcription start sites and down-regulation of associated genes. Genome Res. 17, 708-719 (Pubitemid 46919708)
32. Beedanagari, S. R., Taylor, R. T. and Hankinson, O. (2010) Differential regulation of the dioxin-induced Cyp1a1 and Cyp1b1 genes in mouse hepatoma and fibroblast cell lines. Toxicol. Lett. 194, 26-33
33. Zelko, I. N. and Folz, R. J. (2004) Sp1 and Sp3 transcription factors mediate trichostatin A-induced and basal expression of extracellular superoxide dismutase. Free Radical Biol. Med. 37, 1256-1271 (Pubitemid 39296750)
34. Duan, Z., Stamatoyannopoulos, G. and Li, Q. (2001) Role of NF-Y in in vivo regulation of the γ-globin gene. Mol. Cell. Biol. 21, 3083-3095 (Pubitemid 32298375)
35. Postnikov, Y. V., Lehn, D. A., Robinson, R. C., Friedman, F. K., Shiloach, J. and Bustin, M. (1994) The cooperative binding of chromosomal protein HMG-14 to nucleosome cores is reduced by single point mutations in the nucleosomal binding domain. Nucleic Acids Res. 22, 4520-4526 (Pubitemid 24336426)
36. Borowsky, B. and Hoffman, B. J. (1998) Analysis of a gene encoding two glycine transporter variants reveals alternative promoter usage and a novel gene structure. J. Biol. Chem. 273, 29077-29085 (Pubitemid 28507604)
37. Bustin, M., Crippa, M. P. and Pash, J. M. (1990) Immunochemical analysis of the exposure of high mobility group protein 14 and 17 surfaces in chromatin. J. Biol. Chem. 265, 20077-20080 (Pubitemid 120013975)
38. Heintzman, N. D., Hon, G. C., Hawkins, R. D., Kheradpour, P., Stark, A., Harp, L. F., Ye, Z., Lee, L. K., Stuart, R. K., Ching, C. W. et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108-112
39. Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F. et al. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858
40. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (Pubitemid 46802390)
41. Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M. and Haussler, D. (2002) The human genome browser at UCSC. Genome Res. 12, 996-1006 (Pubitemid 34662293)
42. Fujita, P. A., Rhead, B., Zweig, A. S., Hinrichs, A. S., Karolchik, D., Cline, M. S., Goldman, M., Barber, G. P., Clawson, H., Coelho, A. et al. (2011) The UCSC Genome Browser database: update 2011. Nucleic Acids Res. 39, D876-D882
43. Rosenbloom, K. R., Dreszer, T. R., Pheasant, M., Barber, G. P., Meyer, L. R., Pohl, A., Raney, B. J., Wang, T., Hinrichs, A. S., Zweig, A. S. et al. (2012) ENCODE whole-genome data in the UCSC Genome Browser: update 2012. Nucleic Acids Res. 38, D620-D625
44. Schiltz, R. L., Mizzen, C. A., Vassilev, A., Cook, R. G., Allis, C. D. and Nakatani, Y. (1999) Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J. Biol. Chem. 274, 1189-1192
45. Dhami, P., Saffrey, P., Bruce, A. W., Dillon, S. C., Chiang, K., Bonhoure, N., Koch, C. M., Bye, J., James, K., Foad, N. S. et al. (2010) Complex exon-intron marking by histone modifications is not determined solely by nucleosome distribution. PLoS ONE 5, e12339
46. Herrera, J. E., Schiltz, R. L. and Bustin, M. (2000) The accessibility of histone H3 tails in chromatin modulates their acetylation by P300/CBP-associated factor. J. Biol. Chem. 275, 12994-12999 (Pubitemid 30241458)
47. 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. (2009) The interaction of NSBP1/HMGN5 with nucleosomes in euchromatin counteracts linker histone-mediated chromatin compaction and modulates transcription. Mol. Cell 35, 642-656
48. Wittschieben, B. O., Fellows, J., Du, W., Stillman, D. J. and Svejstrup, J. Q. (2000) Overlapping roles for the histone acetyltransferase activities of SAGA and elongator in vivo. EMBO J. 19, 3060-3068 (Pubitemid 30386776)
49. Govind, C. K., Zhang, F., Qiu, H., Hofmeyer, K. and Hinnebusch, A. G. (2007) Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol. Cell 25, 31-42 (Pubitemid 46049060)
50. Kristjuhan, A. and Svejstrup, J. Q. (2004) Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 23, 4243-4252 (Pubitemid 39546162)
51. Johnsson, A., Durand-Dubief, M., Xue-Franzen, Y., Ronnerblad, M., Ekwall, K. and Wright, A. (2009) HAT-HDAC interplay modulates global histone H3K14 acetylation in gene-coding regions during stress. EMBO Rep. 10, 1009-1014
52. Winkler, G. S., Kristjuhan, A., Erdjument-Bromage, H., Tempst, P. and Svejstrup, J. Q. (2002) Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc. Natl. Acad. Sci. U.S.A. 99, 3517-3522 (Pubitemid 34252140)
53. Nagy, Z., Riss, A., Fujiyama, S., Krebs, A., Orpinell, M., Jansen, P., Cohen, A., Stunnenberg, H. G., Kato, S. and Tora, L. (2007) The metazoan ATAC and SAGA coactivator HAT complexes regulate different sets of inducible target genes. Cell. Mol. Life Sci. 67, 611-628
54. Schiltz, R. L., Mizzen, C. A., Vassilev, A., Cook, R. G., Allis, C. D. and Nakatani, Y. (1999) Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J. Biol. Chem. 274, 1189-1192
55. Hassan, A. H., Prochasson, P., Neely, K. E., Galasinski, S. C., Chandy, M., Carrozza, M. J. and Workman, J. L. (2002) Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111, 369-379 (Pubitemid 35345152)
56. Carey, M., Li, B. and Workman, J. L. (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol. Cell 24, 481-487 (Pubitemid 44647905)
57. Kasten, M., Szerlong, H., Erdjument-Bromage, H., Tempst, P., Werner, M. and Cairns, B. R. (2004) Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J. 23, 1348-1359 (Pubitemid 38525006)
58. Ding, H. F., Rimsky, S., Batson, S. C., Bustin, M. and Hansen, U. (1994) Stimulation of RNA polymerase II elongation by chromosomal protein HMG- 14. Science 265, 796-799 (Pubitemid 24266141)