HMGN1 Modulates Nucleosome Occupancy and DNase I Hypersensitivity at the CpG Island Promoters of Embryonic Stem Cells

REFERENCES

• Li M, Liu GH, Izpisua Belmonte JC. 2012. Navigating the epigenetic landscape of pluripotent stem cells. Nat. Rev. Mol. Cell Biol. 13:524–535.
   PubMedGoogle Scholar
• Mattout A, Meshorer E. 2010. Chromatin plasticity and genome organization in pluripotent embryonic stem cells. Curr. Opin. Cell Biol. 22:334–341.
   PubMedGoogle Scholar
• Shah SN, Kerr C, Cope L, Zambidis E, Liu C, Hillion J, Belton A, Huso DL, Resar LM. 2012. HMGA1 reprograms somatic cells into pluripotent stem cells by inducing stem cell transcriptional networks. PLoS One 7:e48533. doi:10.1371/journal.pone.0048533.
   PubMed Web of Science ®Google Scholar
• Young RA. 2011. Control of the embryonic stem cell state. Cell 144:940–954.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Cooke M, Panjwani S, Cao K, Krauth B, Ho PY, Medrzycki M, Berhe DT, Pan C, McDevitt TC, Fan Y. 2012. Histone h1 depletion impairs embryonic stem cell differentiation. PLoS Genet. 8:e1002691. doi:10.1371/journal.pgen.1002691.
   PubMed Web of Science ®Google Scholar
• Catez F, Hock R. 2010. Binding and interplay of HMG proteins on chromatin: lessons from live cell imaging. Biochim. Biophys. Acta 1799:15–27.
   PubMedGoogle Scholar
• Catez F, Ueda T, Bustin M. 2006. Determinants of histone H1 mobility and chromatin binding in living cells. Nat. Struct. Mol. Biol. 13:305–310.
   PubMed Web of Science ®Google Scholar
• Woodcock CL, Skoultchi AI, Fan Y. 2006. Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res. 14:17–25.
   PubMed Web of Science ®Google Scholar
• Bianchi ME, Agresti A. 2005. HMG proteins: dynamic players in gene regulation and differentiation. Curr. Opin. Genet. Dev. 15:496–506.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Rochman M, Postnikov Y, Correll S, Malicet C, Wincovitch S, Karpova TS, McNally JG, Wu X, Bubunenko NA, Grigoryev S, 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.
   PubMedGoogle Scholar
• Bustin M, Catez F, Lim JH. 2005. The dynamics of histone H1 function in chromatin. Mol. Cell 17:617–620.
   PubMed Web of Science ®Google Scholar
• Alfonso PJ, Crippa MP, Hayes JJ, Bustin M. 1994. The footprint of chromosomal proteins HMG-14 and HMG-17 on chromatin subunits. J. Mol. Biol. 236:189–198.
   PubMedGoogle Scholar
• Kato H, van Ingen H, Zhou BR, Feng H, Bustin M, Kay LE, Bai Y. 2011. Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR. Proc. Natl. Acad. Sci. U. S. A. 108:12283–12288.
   PubMedGoogle Scholar
• Pogna EA, Clayton AL, Mahadevan LC. 2010. Signalling to chromatin through post-translational modifications of HMGN. Biochim. Biophys. Acta 1799:93–100.
   PubMed Web of Science ®Google Scholar
• Weisbrod S, Weintraub H. 1979. Isolation of a subclass of nuclear proteins responsible for conferring a DNase I-sensitive structure on globin chromatin. Proc. Natl. Acad. Sci. U. S. A. 76:630–634.
   PubMed Web of Science ®Google Scholar
• Rattner BP, Yusufzai T, Kadonaga JT. 2009. HMGN proteins act in opposition to ATP-dependent chromatin remodeling factors to restrict nucleosome mobility. Mol. Cell 34:620–626.
   PubMedGoogle Scholar
• Dutta A, Workman JL. 2012. Nucleosome positioning: multiple mechanisms toward a unifying goal. Mol. Cell 48:1–2.
   PubMedGoogle Scholar
• Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF. 2012. Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149:1461–1473.
   PubMed Web of Science ®Google Scholar
• Cuddapah S, Schones DE, Cui K, Roh TY, Barski A, Wei G, Rochman M, Bustin M, Zhao K. 2011. Genomic profiling of HMGN1 reveals an association with chromatin at regulatory regions. Mol. Cell. Biol. 31:700–709.
   PubMedGoogle Scholar
• Rochman M, Taher L, Kurahashi T, Cherukuri S, Uversky VN, Landsman D, Ovcharenko I, Bustin M. 2011. Effects of HMGN variants on the cellular transcription profile. Nucleic Acids Res. 39:4076–4087.
   PubMedGoogle Scholar
• Hock R, Furusawa T, Ueda T, Bustin M. 2007. HMG chromosomal proteins in development and disease. Trends Cell Biol. 17:72–79.
   PubMed Web of Science ®Google Scholar
• Mohamed OA, Bustin M, Clarke HJ. 2001. High-mobility group proteins 14 and 17 maintain the timing of early embryonic development in the mouse. Dev. Biol. 229:237–249.
   PubMed Web of Science ®Google Scholar
• Körner U, Bustin M, Scheer U, Hock R. 2003. Developmental role of HMGN proteins in Xenopus laevis. Mech. Dev. 120:1177–1192.
   PubMedGoogle Scholar
• Fenouil R, Cauchy P, Koch F, Descostes N, Cabeza JZ, Innocenti C, Ferrier P, Spicuglia S, Gut M, Gut I, Andrau JC. 2012. CpG islands and GC content dictate nucleosome depletion in a transcription-independent manner at mammalian promoters. Genome Res. 22:2399–2408.
   PubMed Web of Science ®Google Scholar
• Sadeh R, Allis CD. 2011. Genome-wide “re”-modeling of nucleosome positions. Cell 147:263–266.
   PubMedGoogle Scholar
• Teif VB, Vainshtein Y, Caudron-Herger M, Mallm JP, Marth C, Hofer T, Rippe K. 2012. Genome-wide nucleosome positioning during embryonic stem cell development. Nat. Struct. Mol. Biol. 19:1185–1192.
   PubMed Web of Science ®Google Scholar
• Bryja V, Bonilla S, Cajanek L, Parish CL, Schwartz CM, Luo Y, Rao MS, Arenas E. 2006. An efficient method for the derivation of mouse embryonic stem cells. Stem Cells 24:844–849.
   PubMedGoogle Scholar
• Birger Y, West KL, Postnikov YV, Lim JH, Furusawa T, Wagner JP, Laufer CS, Kraemer KH, Bustin M. 2003. Chromosomal protein HMGN1 enhances the rate of DNA repair in chromatin. EMBO J. 22:1665–1675.
   PubMed Web of Science ®Google Scholar
• Cherukuri S, Hock R, Ueda T, Catez F, Rochman M, Bustin M. 2008. Cell cycle-dependent binding of HMGN proteins to chromatin. Mol. Biol. Cell 19:1816–1824.
   PubMedGoogle Scholar
• Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80. doi:10.1186/gb-2004-5-10-r80.
   PubMed Web of Science ®Google Scholar
• Gautier L, Cope L, Bolstad BM, Irizarry RA. 2004. affy—analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20:307–315.
   PubMed Web of Science ®Google Scholar
• Wilson CL, Miller CJ. 2005. Simpleaffy: a BioConductor package for Affymetrix quality control and data analysis. Bioinformatics 21:3683–3685.
   PubMed Web of Science ®Google Scholar
• Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193.
   PubMed Web of Science ®Google Scholar
• Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. doi:10.1186/gb-2009-10-3-r25.
   PubMed Web of Science ®Google Scholar
• Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W. 2009. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25:1952–1958.
   PubMed Web of Science ®Google Scholar
• Abuhatzira L, Shamir A, Schones DE, Schaffer AA, Bustin M. 2011. The chromatin-binding protein HMGN1 regulates the expression of methyl CpG-binding protein 2 (MECP2) and affects the behavior of mice. J. Biol. Chem. 286:42051–42062.
   PubMedGoogle Scholar
• Furusawa T, Cherukuri S. 2010. Developmental function of HMGN proteins. Biochim. Biophys. Acta 1799:69–73.
   PubMedGoogle Scholar
• Kim YC, Gerlitz G, Furusawa T, Catez F, Nussenzweig A, Oh KS, Kraemer KH, Shiloh Y, Bustin M. 2009. Activation of ATM depends on chromatin interactions occurring before induction of DNA damage. Nat. Cell Biol. 11:92–96.
   PubMed Web of Science ®Google Scholar
• Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44–57.
   PubMed Web of Science ®Google Scholar
• Melcer S, Hezroni H, Rand E, Nissim-Rafinia M, Skoultchi A, Stewart CL, Bustin M, Meshorer E. 2012. Histone modifications and lamin A regulate chromatin protein dynamics in early embryonic stem cell differentiation. Nat. Commun. 3:910. doi:10.1038/ncomms1915.
   PubMed Web of Science ®Google Scholar
• Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T. 2006. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 10:105–116.
   PubMed Web of Science ®Google Scholar
• Bult CJ, Eppig JT, Blake JA, Kadin JA, Richardson JE. 2013. The mouse genome database: genotypes, phenotypes, and models of human disease. Nucleic Acids Res. 41:D885–D891.
   PubMedGoogle Scholar
• Pruitt KD, Tatusova T, Brown GR, Maglott DR. 2012. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res. 40:D130–D135.
   PubMed Web of Science ®Google Scholar
• Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. 2007. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88.
   PubMed Web of Science ®Google Scholar
• Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K, Felsenfeld G. 2009. H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions. Nat. Genet. 41:941–945.
   PubMed Web of Science ®Google Scholar
• Catez F, Brown DT, Misteli T, Bustin M. 2002. Competition between histone H1 and HMGN proteins for chromatin binding sites. EMBO Rep. 3:760–766.
   PubMedGoogle Scholar
• Bustin M. 2001. Chromatin unfolding and activation by HMGN(*) chromosomal proteins. Trends Biochem. Sci. 26:431–437.
   PubMed Web of Science ®Google Scholar
• Ballaré C, Castellano G, Gaveglia L, Althammer S, Gonzalez-Vallinas J, Eyras E, Le Dily F, Zaurin R, Soronellas D, Vicent GP, Beato M. 2013. Nucleosome-driven transcription factor binding and gene regulation. Mol. Cell 49:67–79.
   PubMedGoogle Scholar
• Belova GI, Postnikov YV, Furusawa T, Birger Y, Bustin M. 2008. Chromosomal protein HMGN1 enhances the heat shock-induced remodeling of Hsp70 chromatin. J. Biol. Chem. 283:8080–8088.
   PubMedGoogle Scholar
• Lim JH, Bustin M, Ogryzko VV, Postnikov YV. 2002. Metastable macromolecular complexes containing high mobility group nucleosome-binding chromosomal proteins in HeLa nuclei. J. Biol. Chem. 277:20774–20782.
   PubMedGoogle Scholar
• Postnikov YV, Kurahashi T, Zhou M, Bustin M. 2012. The nucleosome binding protein HMGN1 interacts with PCNA and facilitates its binding to chromatin. Mol. Cell. Biol. 32:1844–1854.
   PubMedGoogle Scholar
• Masaoka A, Gassman NR, Kedar PS, Prasad R, Hou EW, Horton JK, Bustin M, Wilson SH. 2012. HMGN1 protein regulates poly(ADP-ribose) polymerase-1 (PARP-1) self-PARylation in mouse fibroblasts. J. Biol. Chem. 287:27648–27658.
   PubMedGoogle Scholar
• Ueda T, Furusawa T, Kurahashi T, Tessarollo L, Bustin M. 2009. The nucleosome binding protein HMGN3 modulates the transcription profile of pancreatic beta cells and affects insulin secretion. Mol. Cell. Biol. 29:5264–5276.
   PubMedGoogle Scholar
• Birger Y, Catez F, Furusawa T, Lim JH, Prymakowska-Bosak M, West KL, Postnikov YV, Haines DC, Bustin M. 2005. Increased tumorigenicity and sensitivity to ionizing radiation upon loss of chromosomal protein HMGN1. Cancer Res. 65:6711–6718.
   PubMedGoogle Scholar