Jeffrey_Hayes@urmc.rochester.edu

Each eukaryotic cell must execute a complex program of specific gene expression. The DNA of the genome is intimately complexed with proteins into an assembly known as chromatin. Compaction and storage of genomic DNA has long been viewed as the main function of this assembly; however, recent work has demonstrated that in some instances, chromatin structure play an important role in bringing about this pattern of specific expression, and it is likely that the structural elements of chromatin have been integrated into many transcriptional control mechanisms.

The goal of the research in this laboratory is to provide detailed structure information on the protein-DNA interactions and DNA organization within chromatin, and to correlate this information with simple functional assays of the consequences of this organization. Model chromatin complexes will be prepared in vitro and structurally analyzed with chemical approaches. In addition, cloning expression of histone proteins with specific mutations will be useful in the determination of relevant domains within these proteins while facilitating the creation of site-specific probes of protein and DNA structure with chromatin.

• Elliott GO, Murphy KJ, Hayes JJ, Thiriet C. Replication-independent nucleosome exchange is enhanced by local and specific acetylation of histone H4. Nucleic Acids Res. 2013 Feb 1; 41(4):2228-38.
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• Liu N, Hayes JJ. Preparation of Nucleosomes Containing a Specific H2A-H2A Cross-Link Forming a DNA-Constraining Loop Structure. Methods Mol Biol. 2012; 833:351-71.
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• Yang Z, Hayes JJ. The Divalent Cations Ca(2+) and Mg(2+) Play Specific Roles in Stabilizing Histone-DNA Interactions within Nucleosomes That Are Partially Redundant with the Core Histone Tail Domains. Biochemistry. 2011 Nov 22; 50(46):9973-81.
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• Fang H, Clark DJ, Hayes JJ. DNA and nucleosomes direct distinct folding of a linker histone H1 C-terminal domain. Nucleic Acids Res. 2012 Feb 1; 40(4):1475-84.
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• Liu N, Peterson CL, Hayes JJ. SWI/SNF- and RSC-catalyzed nucleosome mobilization requires internal DNA loop translocation within nucleosomes. Mol Cell Biol. 2011 Oct; 31(20):4165-75.
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• Meyer S, Becker NB, Syed SH, Goutte-Gattat D, Shukla MS, Hayes JJ, Angelov D, Bednar J, Dimitrov S, Everaers R. From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem. Nucleic Acids Res. 2011 Nov 1; 39(21):9139-54.
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• Almouzni G, Hayes JJ. Meeting report: International symposium on the physicochemical field for genetic activities. Nucleus. 2011 Jul 1; 2(4):253-7.
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• Caterino TL, Fang H, Hayes JJ. Nucleosome linker DNA contacts and induces specific folding of the intrinsically disordered H1 carboxyl-terminal domain. Mol Cell Biol. 2011 Jun; 31(11):2341-8.
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• Jagannathan I, Pepenella S, Hayes JJ. Activity of FEN1 endonuclease on nucleosome substrates is dependent upon DNA sequence but not flap orientation. J Biol Chem. 2011 May 20; 286(20):17521-9.
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• Caterino TL, Hayes JJ. Structure of the H1 C-terminal domain and function in chromatin condensation. Biochem Cell Biol. 2011 Feb; 89(1):35-44.
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• Shukla MS, Syed SH, Goutte-Gattat D, Richard JL, Montel F, Hamiche A, Travers A, Faivre-Moskalenko C, Bednar J, Hayes JJ, Angelov D, Dimitrov S. The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling. Nucleic Acids Res. 2011 Apr; 39(7):2559-70.
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• Liu N, Balliano A, Hayes JJ. Mechanism(s) of SWI/SNF-induced nucleosome mobilization. Chembiochem. 2011 Jan 24; 12(2):196-204.
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• Liu N, Hayes JJ. When push comes to shove: SWI/SNF uses a nucleosome to get rid of a nucleosome. Mol Cell. 2010 May 28; 38(4):484-6.
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• Syed SH, Goutte-Gattat D, Becker N, Meyer S, Shukla MS, Hayes JJ, Everaers R, Angelov D, Bednar J, Dimitrov S. Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome. Proc Natl Acad Sci U S A. 2010 May 25; 107(21):9620-5.
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• Cole HA, Tabor-Godwin JM, Hayes JJ. Uracil DNA glycosylase activity on nucleosomal DNA depends on rotational orientation of targets. J Biol Chem. 2010 Jan 22; 285(4):2876-85.
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• Jagannathan I, Hayes JJ. Hydroxyl radical footprinting of protein-DNA complexes. Methods Mol Biol. 2009; 543:57-71.
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• Chafin DR, Hayes JJ. Site-directed cleavage of DNA by protein-Fe(II) EDTA conjugates within model chromatin complexes. Methods Mol Biol. 2009; 543:121-38.
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• Thiriet C, Hayes JJ. Linker histone phosphorylation regulates global timing of replication origin firing. J Biol Chem. 2009 Jan 30; 284(5):2823-9.
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• Kan PY, Caterino TL, Hayes JJ. The H4 tail domain participates in intra- and internucleosome interactions with protein and DNA during folding and oligomerization of nucleosome arrays. Mol Cell Biol. 2009 Jan; 29(2):538-46.
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• Caterino TL, Hayes JJ. Chromatin structure depends on what's in the nucleosome's pocket. Nat Struct Mol Biol. 2007 Nov; 14(11):1056-8.
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• Wang X, Hayes JJ. Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol Cell Biol. 2008 Jan; 28(1):227-36.
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• Wang X, Hayes JJ. Site-specific binding affinities within the H2B tail domain indicate specific effects of lysine acetylation. J Biol Chem. 2007 Nov 9; 282(45):32867-76.
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• Kan PY, Hayes JJ. Detection of interactions between nucleosome arrays mediated by specific core histone tail domains. Methods. 2007 Mar; 41(3):278-85.
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• Kan PY, Lu X, Hansen JC, Hayes JJ. The H3 tail domain participates in multiple interactions during folding and self-association of nucleosome arrays. Mol Cell Biol. 2007 Mar; 27(6):2084-91.
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• Yang Z, Zheng C, Hayes JJ. The core histone tail domains contribute to sequence-dependent nucleosome positioning. J Biol Chem. 2007 Mar 16; 282(11):7930-8.
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• Wang X, Hayes JJ. Physical methods used to study core histone tail structures and interactions in solution. Biochem Cell Biol. 2006 Aug; 84(4):578-88.
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• Jagannathan I, Cole HA, Hayes JJ. Base excision repair in nucleosome substrates. Chromosome Res. 2006; 14(1):27-37.
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• Thiriet C, Hayes JJ. Histone dynamics during transcription: exchange of H2A/H2B dimers and H3/H4 tetramers during pol II elongation. Results Probl Cell Differ. 2006; 41:77-90.
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• Zheng C, Lu X, Hansen JC, Hayes JJ. Salt-dependent intra- and internucleosomal interactions of the H3 tail domain in a model oligonucleosomal array. J Biol Chem. 2005 Sep 30; 280(39):33552-7.
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• Owen BA, Yang Z, Lai M, Gajec M, Gajek M, Badger JD, Hayes JJ, Edelmann W, Kucherlapati R, Wilson TM, McMurray CT. (CAG)(n)-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition. Nat Struct Mol Biol. 2005 Aug; 12(8):663-70.
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• Thiriet C, Hayes JJ. Chromatin in need of a fix: phosphorylation of H2AX connects chromatin to DNA repair. Mol Cell. 2005 Jun 10; 18(6):617-22.
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• Thiriet C, Hayes JJ. Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev. 2005 Mar 15; 19(6):677-82.
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• Yang Z, Zheng C, Thiriet C, Hayes JJ. The core histone N-terminal tail domains negatively regulate binding of transcription factor IIIA to a nucleosome containing a 5S RNA gene via a novel mechanism. Mol Cell Biol. 2005 Jan; 25(1):241-9.
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• Yang Z, Hayes JJ. Large scale preparation of nucleosomes containing site-specifically chemically modified histones lacking the core histone tail domains. Methods. 2004 May; 33(1):25-32.
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• Hayes JJ. In vitro analysis of chromatin structure in model systems. Methods. 2004 May; 33(1):1-2.
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• Zheng C, Hayes JJ. Probing core histone tail-DNA interactions in a model dinucleosome system. Methods Enzymol. 2004; 375:179-93.
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• Vitolo JM, Yang Z, Basavappa R, Hayes JJ. Structural features of transcription factor IIIA bound to a nucleosome in solution. Mol Cell Biol. 2004 Jan; 24(2):697-707.
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• Yang Z, Hayes JJ. Xenopus transcription factor IIIA and the 5S nucleosome: development of a useful in vitro system. Biochem Cell Biol. 2003 Jun; 81(3):177-84.
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• Aoyagi S, Wade PA, Hayes JJ. Nucleosome sliding induced by the xMi-2 complex does not occur exclusively via a simple twist-diffusion mechanism. J Biol Chem. 2003 Aug 15; 278(33):30562-8.
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• Zheng C, Hayes JJ. Intra- and inter-nucleosomal protein-DNA interactions of the core histone tail domains in a model system. J Biol Chem. 2003 Jun 27; 278(26):24217-24.
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• Zheng C, Hayes JJ. Structures and interactions of the core histone tail domains. Biopolymers. 2003 Apr; 68(4):539-46.
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• Ye J, Yang Z, Hayes JJ, Eickbush TH. R2 retrotransposition on assembled nucleosomes depends on the translational position of the target site. EMBO J. 2002 Dec 16; 21(24):6853-64.
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• Aoyagi S, Hayes JJ. hSWI/SNF-catalyzed nucleosome sliding does not occur solely via a twist-diffusion mechanism. Mol Cell Biol. 2002 Nov; 22(21):7484-90.
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• Huggins CF, Chafin DR, Aoyagi S, Henricksen LA, Bambara RA, Hayes JJ. Flap endonuclease 1 efficiently cleaves base excision repair and DNA replication intermediates assembled into nucleosomes. Mol Cell. 2002 Nov; 10(5):1201-11.
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• Aoyagi S, Narlikar G, Zheng C, Sif S, Kingston RE, Hayes JJ. Nucleosome remodeling by the human SWI/SNF complex requires transient global disruption of histone-DNA interactions. Mol Cell Biol. 2002 Jun; 22(11):3653-62.
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• Ura K, Hayes JJ. Nucleotide excision repair and chromatin remodeling. Eur J Biochem. 2002 May; 269(9):2288-93.
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• Hayes JJ. Changing chromatin from the inside. Nat Struct Biol. 2002 Mar; 9(3):161-3.
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• Hayes JJ, Hansen JC. New insights into unwrapping DNA from the nucleosome from a single-molecule optical tweezers method. Proc Natl Acad Sci U S A. 2002 Feb 19; 99(4):1752-4.
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• Thiriet C, Hayes JJ. A novel labeling technique reveals a function for histone H2A/H2B dimer tail domains in chromatin assembly in vivo. Genes Dev. 2001 Aug 15; 15(16):2048-53.
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• Angelov D, Vitolo JM, Mutskov V, Dimitrov S, Hayes JJ. Preferential interaction of the core histone tail domains with linker DNA. Proc Natl Acad Sci U S A. 2001 Jun 5; 98(12):6599-604.
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• Vitolo JM, Thiriet C, Hayes JJ. DNase I and hydroxyl radical characterization of chromatin complexes. Curr Protoc Mol Biol. 2001 May; Chapter 21:Unit 21.4.
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• Hayes JJ, Hansen JC. Nucleosomes and the chromatin fiber. Curr Opin Genet Dev. 2001 Apr; 11(2):124-9.
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• Thiriet C, Hayes JJ. Assembly into chromatin and subtype-specific transcriptional effects of exogenous linker histones directly introduced into a living Physarum cell. J Cell Sci. 2001 Mar; 114(Pt 5):965-73.
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• Chafin DR, Hayes JJ. Site-directed cleavage of DNA by linker histone-Fe(II) EDTA conjugates. Methods Mol Biol. 2001; 148:275-90.
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• Chafin DR, Vitolo JM, Henricksen LA, Bambara RA, Hayes JJ. Human DNA ligase I efficiently seals nicks in nucleosomes. EMBO J. 2000 Oct 16; 19(20):5492-501.
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• Widlund HR, Vitolo JM, Thiriet C, Hayes JJ. DNA sequence-dependent contributions of core histone tails to nucleosome stability: differential effects of acetylation and proteolytic tail removal. Biochemistry. 2000 Apr 4; 39(13):3835-41.
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• Vitolo JM, Thiriet C, Hayes JJ. The H3-H4 N-terminal tail domains are the primary mediators of transcription factor IIIA access to 5S DNA within a nucleosome. Mol Cell Biol. 2000 Mar; 20(6):2167-75.
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• Fernández De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, Ohmori H, Woodgate R. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol. 2000 Mar; 35(6):1560-72.
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• Lee KM, Sif S, Kingston RE, Hayes JJ. hSWI/SNF disrupts interactions between the H2A N-terminal tail and nucleosomal DNA. Biochemistry. 1999 Jun 29; 38(26):8423-9.
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• Thiriet C, Hayes JJ. Chromatin remodeling by cell cycle stage-specific extracts from Physarum polycephalum. Eur J Cell Biol. 1999 Mar; 78(3):214-20.
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• Thiriet C, Hayes JJ. Histone proteins in vivo: cell-cycle-dependent physiological effects of exogenous linker histones incorporated into Physarum polycephalum. Methods. 1999 Feb; 17(2):140-50.
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• Wolffe AP, Hayes JJ. Chromatin disruption and modification. Nucleic Acids Res. 1999 Feb 1; 27(3):711-20.
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• Lee KM, Chafin DR, Hayes JJ. Targeted cross-linking and DNA cleavage within model chromatin complexes. Methods Enzymol. 1999; 304:231-51.
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• Chafin DR, Lee KM, Hayes JJ. Site-directed chemical probing of histone-DNA interactions. Methods Mol Biol. 1999; 119:27-43.
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• Thiriet C, Hayes JJ. Functionally relevant histone-DNA interactions extend beyond the classically defined nucleosome core region. J Biol Chem. 1998 Aug 14; 273(33):21352-8.
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• Lee KM, Hayes JJ. Linker DNA and H1-dependent reorganization of histone-DNA interactions within the nucleosome. Biochemistry. 1998 Jun 16; 37(24):8622-8.
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• Ehmann A, Chafin D, Lee KM, Hayes JJ. (1,4,7-trimethyl-1,4,7-triazacyclononane)iron (III)-mediated cleavage of DNA: detection of selected protein-DNA interactions. Nucleic Acids Res. 1998 May 1; 26(9):2086-91.
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• Winterling KW, Chafin D, Hayes JJ, Sun J, Levine AS, Yasbin RE, Woodgate R. The Bacillus subtilis DinR binding site: redefinition of the consensus sequence. J Bacteriol. 1998 Apr; 180(8):2201-11.
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• Lee KM, Hayes JJ. The N-terminal tail of histone H2A binds to two distinct sites within the nucleosome core. Proc Natl Acad Sci U S A. 1997 Aug 19; 94(17):8959-64.
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• Thiriet C, Hayes JJ. Antisera directed against anti-histone H4 antibodies recognize linker histones. Novel immunological probes to detect histone interactions. J Biol Chem. 1997 Jul 25; 272(30):18740-5.
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• Hayes JJ, Lee KM. In vitro reconstitution and analysis of mononucleosomes containing defined DNAs and proteins. Methods. 1997 May; 12(1):2-9.
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• Pruss D, Bartholomew B, Persinger J, Hayes J, Arents G, Moudrianakis EN, Wolffe AP. An asymmetric model for the nucleosome: a binding site for linker histones inside the DNA gyres. Science. 1996 Oct 25; 274(5287):614-7.
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• Hayes JJ, Kaplan R, Ura K, Pruss D, Wolffe A. A putative DNA binding surface in the globular domain of a linker histone is not essential for specific binding to the nucleosome. J Biol Chem. 1996 Oct 18; 271(42):25817-22.
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• Hayes JJ. Site-directed cleavage of DNA by a linker histone--Fe(II) EDTA conjugate: localization of a globular domain binding site within a nucleosome. Biochemistry. 1996 Sep 17; 35(37):11931-7.
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• Ura K, Hayes JJ, Wolffe AP. A positive role for nucleosome mobility in the transcriptional activity of chromatin templates: restriction by linker histones. EMBO J. 1995 Aug 1; 14(15):3752-65.
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• Strzelecka TE, Hayes JJ, Clore GM, Gronenborn AM. DNA binding specificity of the Mu Ner protein. Biochemistry. 1995 Mar 7; 34(9):2946-55.
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• Hayes JJ. Chemical probes of DNA structure in chromatin. Chem Biol. 1995 Mar; 2(3):127-35.
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• Pruss D, Hayes JJ, Wolffe AP. Nucleosomal anatomy--where are the histones? Bioessays. 1995 Feb; 17(2):161-70.
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• Ura K, Wolffe AP, Hayes JJ. Core histone acetylation does not block linker histone binding to a nucleosome including a Xenopus borealis 5 S rRNA gene. J Biol Chem. 1994 Nov 4; 269(44):27171-4.
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• Hayes JJ, Pruss D, Wolffe AP. Contacts of the globular domain of histone H5 and core histones with DNA in a "chromatosome". Proc Natl Acad Sci U S A. 1994 Aug 2; 91(16):7817-21.
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• Bauer WR, Hayes JJ, White JH, Wolffe AP. Nucleosome structural changes due to acetylation. J Mol Biol. 1994 Feb 25; 236(3):685-90.
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• Alfonso PJ, Crippa MP, Hayes JJ, Bustin M. The footprint of chromosomal proteins HMG-14 and HMG-17 on chromatin subunits. J Mol Biol. 1994 Feb 11; 236(1):189-98.
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• Hayes JJ, Wolffe AP. Preferential and asymmetric interaction of linker histones with 5S DNA in the nucleosome. Proc Natl Acad Sci U S A. 1993 Jul 15; 90(14):6415-9.
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• Bashkin J, Hayes JJ, Tullius TD, Wolffe AP. Structure of DNA in a nucleosome core at high salt concentration and at high temperature. Biochemistry. 1993 Mar 2; 32(8):1895-8.
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• Lee DY, Hayes JJ, Pruss D, Wolffe AP. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell. 1993 Jan 15; 72(1):73-84.
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• Wolffe AP, Almouzni G, Ura K, Pruss D, Hayes JJ. Transcription factor access to DNA in the nucleosome. Cold Spring Harb Symp Quant Biol. 1993; 58:225-35.
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• Hayes JJ, Clemens KR. Locations of contacts between individual zinc fingers of Xenopus laevis transcription factor IIIA and the internal control region of a 5S RNA gene. Biochemistry. 1992 Nov 24; 31(46):11600-5.
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• Hayes JJ, Tullius TD. Structure of the TFIIIA-5 S DNA complex. J Mol Biol. 1992 Sep 20; 227(2):407-17.
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• Hayes JJ, Wolffe AP. The interaction of transcription factors with nucleosomal DNA. Bioessays. 1992 Sep; 14(9):597-603.
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• Hayes JJ, Wolffe AP. Experimental determination of DNA helical repeats. Trends Biochem Sci. 1992 Jul; 17(7):250.
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• Hayes JJ, Wolffe AP. Histones H2A/H2B inhibit the interaction of transcription factor IIIA with the Xenopus borealis somatic 5S RNA gene in a nucleosome. Proc Natl Acad Sci U S A. 1992 Feb 15; 89(4):1229-33.
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• Hayes JJ, Bashkin J, Tullius TD, Wolffe AP. The histone core exerts a dominant constraint on the structure of DNA in a nucleosome. Biochemistry. 1991 Aug 27; 30(34):8434-40.
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• Hayes JJ, Clark DJ, Wolffe AP. Histone contributions to the structure of DNA in the nucleosome. Proc Natl Acad Sci U S A. 1991 Aug 1; 88(15):6829-33.
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• Hayes J, Scovell WM. cis-diamminedichloroplatinum (II) modified chromatin and nucleosomal core particle. Biochim Biophys Acta. 1991 Jul 23; 1089(3):377-85.
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• Hayes JJ, Scovell WM. cis-Diamminedichloroplatinum (II) modified chromatin and nucleosomal core particle probed with DNase I. Biochim Biophys Acta. 1991 Mar 26; 1088(3):413-8.
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• Dixon WJ, Hayes JJ, Levin JR, Weidner MF, Dombroski BA, Tullius TD. Hydroxyl radical footprinting. Methods Enzymol. 1991; 208:380-413.
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• Hayes JJ, Tullius TD, Wolffe AP. The structure of DNA in a nucleosome. Proc Natl Acad Sci U S A. 1990 Oct; 87(19):7405-9.
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• Churchill ME, Hayes JJ, Tullius TD. Detection of drug binding to DNA by hydroxyl radical footprinting. Relationship of distamycin binding sites to DNA structure and positioned nucleosomes on 5S RNA genes of Xenopus. Biochemistry. 1990 Jun 26; 29(25):6043-50.
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• Hayes JJ, Kam L, Tullius TD. Footprinting protein-DNA complexes with gamma-rays. Methods Enzymol. 1990; 186:545-9.
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• Hayes JJ, Tullius TD. The missing nucleoside experiment: a new technique to study recognition of DNA by protein. Biochemistry. 1989 Nov 28; 28(24):9521-7.
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• Hayes J, Tullius TD, Wolffe AP. A protein-protein interaction is essential for stable complex formation on a 5 S RNA gene. J Biol Chem. 1989 Apr 15; 264(11):6009-12.
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