Workman Lab

Workman Lab
Jerry Workman, Ph.D.
[email protected]
Workman Lab Research
Protein Complexes that Modify Chromatin and Regulate Gene Transcription.
Eukaryotic chromosomes comprise DNA that is complexed with small basic
proteins, histones, and other proteins to generate chromatin, a nucleic acid:
protein complex. The tight association of these proteins with DNA provides a level
of transcription control and contributes to epigenetic mechanisms of gene
regulation. For example, the amino-terminal tail domains of the core histone
proteins are sights of numerous post-translational modifications. In addition to
potential effects on chromatin structure, these modifications act as binding
sites/receptors for protein complexes that activate or repress gene transcription.
Thus, histone modification can be used to generate a "code" of signals on the
surface of the chromosome fiber, which provides regulatory information above that
contained in the DNA sequence. Our laboratory is focused on studying the protein
complexes that carry out these histone modifications and those that recognize the
resulting signals.
Purification and Analysis of Histone Acetyltransferase Complexes
Since the discovery of histone acetylation over three decades ago, a strong
connection has been shown between the acetylation of histone proteins and
transcriptional activity. Over the past several years, a number of the enzymes that
carry out these modifications have been identified. We have purified and
characterized the native protein HAT (histone acetyltransferase) complexes
bearing these enzymes to understand their recruitment to promoter DNA and their
function in gene regulation. Thus far we have identified and characterized six such
complexes from yeast. These include the 2-MDa SAGA (Spt-Ada-Gcn5acetyltransferase) complex, the related SLIK (SAGA-like) complex, the 0.8-MDa
ADA complex, the 1.3-MDa NuA4 (nucleosome acetyltransferase of histone H4)
complex, the 0.4-MDa NuA3 complex, and the 0.4-MDa SAS (something about
silencing) complex.
Recruitment of Histone Acetyltransferase Complexes by Transcription Activators to
Acetylate Promoter Nucleosomes
The SAGA complex comprises more than 20 different subunits, which include
several different classes of proteins implicated in transcription regulation. SAGA
contains Ada proteins, the TATA box 뻖 inding protein (TBP) group of Spt gene
products, a subset of TBP-associated factors (TAFIIs), and the 400-kDa Tra1
protein. Tra1 is related to the ataxia telangiectasia mutated (ATM) family of
phosphatidylinositol 3-kinases and is the yeast homolog of the human TRRAP
protein, which plays an essential role in cellular transformation by the c-Myc and
E2F oncogenes. Tra1 is also the largest subunit of the NuA4 complex, which also
contains a number of gene products implicated in transcriptional regulation. Its
catalytic subunit is Esa1 (essential SAS-related acetyltransferase 1).
Although SAGA primarily acetylates histone H3 and NuA4 histone H4, they
share a number of biochemical properties. Our studies have shown that both
SAGA and NuA4 interact specifically with the activation domains of promoterbinding transcription activators. When recruited to a promoter through these
interactions, either SAGA or NuA4 acetylates promoter-proximal nucleosomes,
which results in transcriptional enhancement. Through a series of biochemical and
genetic experiments, we have shown that interactions of SAGA and NuA4 with
transcription activators occur through the shared Tra1 subunit. Tra1 directs the
HAT complexes to promoters via interactions with transcription activators where
they lay down a narrow (SAGA) or wide (NuA4) patch of acetylation on histones
contained in nucleosomes (repeating histone:DNA complexes) surrounding the
promoter. In addition to characterizing the SAGA and NuA4 complexes further, we
are also investigating the function of the acetylated patches laid down by these
HATs at promoters in chromatin.
Promoter Recruitment and Retention of the SWI/SNF Chromatin Remodeling
Complex: Linking Histone Acetylation to Nucleosome Disruption
The yeast SWI/SNF complex is a 1-Mda-protein complex that is required for
the transcription of a subset of yeast genes. Mechanistic studies, by others and us,
have demonstrated that SWI/SNF uses the energy of ATP hydrolysis to alter the
structure and location of nucleosomes. Through a series of biochemical
experiments we have demonstrated that the SWI/SNF complex is also recruited to
promoters by direct interactions with the same promoter-binding transcription
activators that recruit the SAGA and NuA4 complexes. This suggests that these
complexes act in concert during chromatin remodeling, which is consistent with
genetic interactions between SAGA and SWI/SNF subunits. We have found that
after its recruitment by an activator, the retention of SWI/SNF on the promoter can
persist following loss of the activator if adjacent nucleosomes contain acetylated
histones. Indeed, prior recruitment of the SAGA or NuA4 HAT complexes to a
promoter stabilizes the subsequent binding of SWI/SNF by acetylating promoterproximal nucleosomes.
Bromodomain Function and Specificity in Anchoring Chromatin Modifying
Complexes to Promoters.
The Swi2/Snf2 subunit of the SWI/SNF complex contains a bromodomain,
which has been proposed to be an acetyl-lysine 뻖 inding domain. By purifying
and analyzing a SWI/SNF complex from which this domain has been deleted, we
have found that it is required for SWI/SNF retention on acetylated promoter
nucleosomes. Bromodomains are also found in a number of protein complexes
involved in transcriptional regulation, including the general transcription factor
TFIID and the RSC chromatin-remodeling complex. Thus, histone acetylation has
the potential to provide high-affinity interaction sites for bromodomain-containing
complexes in chromatin. The SAGA complex itself contains two bromodomains, in
the Gcn5 and Spt7 subunits, and is able to stabilize its own binding to promoter
nucleosomes by acetylation of histones. This is solely the function of the Gcn5
bromodomain. This specificity of bromodomain function is a consequence of the
subunit in which the bromodomain is found. The bromodomains of Spt7, Gcn5 or
Swi2 can all serve to anchor SAGA or SWI/SNF onto promoter nucleosomes if
placed into the Gcn5 or Swi2 proteins respectively. These studies have illustrated
the central role of bromodomains and histone acetylation in the stable binding of
chromatin modifying complexes to nucleosomes and communication between
them. These interactions are thought to form stable epigenetic marks in chromatin
and lead to ordered pathways of chromatin remodeling for transcription.
Histone Acetyltransferase Complexes That Function in Gene Silencing
While histone acetylation is most often associated with gene activation, it
also plays important roles in gene silencing. This is evidenced by the finding of
products of the SAS (Something About Silencing) genes in HAT complexes. Others
discovered the SAS genes in genetic screens for enhancers of silencing defects at
telomeres and mating-type loci in Saccharomyces cerevisiae. The SAS3 gene (a
homologue of the human MOZ proto-oncogene) encodes the catalytic subunit of
NuA3. SAS3 shares an essential function with GCN5, which results in the death of
cells when both genes are mutated. This function cannot be attributed to any of
the known Gcn5 containing HAT complexes including SAGA. However, it is clear
that the NuA3 complex is involved since deletion of genes encoding other subunits
of this complex have similar effects as SAS3 mutations.
SAS2 encodes an acetyltransferase with significant homology to SAS3 and
ESA1. We purified the protein complex containing the Sas2 protein and found that
it also contains the protein products of the SAS4 and SAS5 genes. Thus, we
simply named this the SAS complex. Surprisingly, the Sas4 component of this
complex mediates interactions of the complex with a protein known as Asf1 (antisilencing function 1). This protein is a histone chaperone/chromatin assembly
protein that can interfere with gene silencing when overexpressed in yeast cells.
We have found that deletion of ASF1 results in silencing defects similar to the loss
of SAS2. We are investigating the functions of the SAS complex and Asf1 in both
chromatin assembly and gene silencing.
Selected publications
Li B, Gogol M, Carey M, Lee D, Seidel C, Workman JL. Combined action of PHD
and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science.
2007;316:1050-1054. Abstract
Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell.
2007;128:707-719. Abstract
Gutierrez JL, Chandy M, Carrozza MJ, Workman JL. Activation domains drive
nucleosome eviction by SWI/SNF. Embo J. 2007;26:730-740. Abstract
Carey M, Li B, Workman JL. RSC Exploits Histone Acetylation to Abrogate the
Nucleosomal Block to RNA Polymerase II Elongation. Mol Cell. 2006;24:481-487.
Guelman S, Suganuma T, Florens L, Weake V, Swanson SK, Washburn MP,
Abmayr SM, Workman JL. The Essential Gene wda Encodes a WD40 Repeat
Subunit of Drosophila SAGA Required for Histone H3 Acetylation. Mol Cell Biol.
2006;26:7178-7189. Abstract
Shia WJ, Li B, Workman JL. SAS-mediated acetylation of histone H4 Lys 16 is
required for H2A.Z incorporation at subtelomeric regions in Saccharomyces
cerevisiae. Genes Dev. 2006;20:2507-2512. Abstract
Workman JL. Nucleosome displacement in transcription. Genes Dev.
2006;20:2009-2017. Abstract
Guelman S, Suganuma T, Florens L, Swanson SK, Kiesecker CL, Kusch T,
Anderson S, Yates JR, 3rd, Washburn MP, Abmayr SM, Workman JL. Host cell
factor and an uncharacterized SANT domain protein are stable components of
ATAC, a novel dAda2A/dGcn5-containing histone acetyltransferase complex in
Drosophila. Mol Cell Biol. 2006;26:871-882. Abstract
Cai Y, Jin J, Florens L, Swanson SK, Kusch T, Li B, Workman JL, Washburn MP,
Conaway RC, Conaway JW. The mammalian YL1 protein is a shared subunit of the
TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J Biol Chem.
2005;280:13665-13670. Abstract
Carrozza MJ, Florens L, Swanson SK, Shia WJ, Anderson S, Yates J, Washburn MP,
Workman JL. Stable incorporation of sequence specific repressors Ash1 and Ume6
into the Rpd3L complex. Biochim Biophys Acta. 2005;1731:77-87. Abstract
Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ,
Anderson S, Yates J, Washburn MP, Workman JL. Histone H3 methylation by Set2
directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic
transcription. Cell. 2005;123:581-592. Abstract
Ercan S, Reese JC, Workman JL, Simpson RT. Yeast recombination enhancer is
stimulated by transcription activation. Mol Cell Biol. 2005;25:7976-7987. Abstract
Jin J, Cai Y, Li B, Conaway RC, Workman JL, Conaway JW, Kusch T. In and out:
histone variant exchange in chromatin. Trends Biochem Sci. 2005;30:680-687.
Jin J, Cai Y, Yao T, Gottschalk AJ, Florens L, Swanson SK, Gutierrez JL, Coleman
MK, Workman JL, Mushegian A, Washburn MP, Conaway RC, Conaway JW. A
mammalian chromatin remodeling complex with similarities to the yeast INO80
complex. J Biol Chem. 2005;280:41207-41212. Abstract
Lee D, Ezhkova E, Li B, Pattenden SG, Tansey WP, Workman JL. The proteasome
regulatory particle alters the SAGA coactivator to enhance its interactions with
transcriptional activators. Cell. 2005;123:423-436. Abtract
Lee KK, Florens L, Swanson SK, Washburn MP, Workman JL. The deubiquitylation
activity of Ubp8 is dependent upon Sgf11 and its association with the SAGA
complex. Mol Cell Biol. 2005;25:1173-1182. Abstract
Li B, Pattenden SG, Lee D, Gutierrez J, Chen J, Seidel C, Gerton J, Workman JL.
Preferential occupancy of histone variant H2AZ at inactive promoters influences
local histone modifications and chromatin remodeling. Proc Natl Acad Sci U S A.
2005;102:18385-18390. Abstract
Li B, Ruan C, Workman JL. Histones: should I stay or should I go? Genome Biol.
2005;6:306. Abstract
Pattenden SG, Chandy MJ, Gutierrez JL, Workman JL. Chromatin dynamics rule the
genome. Genome Biol. 2005;6:355. Abstract
Prochasson P, Florens L, Swanson SK, Washburn MP, Workman JL. The HIR
corepressor complex binds to nucleosomes generating a distinct protein/DNA
complex resistant to remodeling by SWI/SNF. Genes Dev. 2005;19:2534-2539.
Ruan C, Workman JL, Simpson RT. The DNA repair protein yKu80 regulates the
function of recombination enhancer during yeast mating type switching. Mol Cell
Biol. 2005;25:8476-8485. Abstract
Shia WJ, Osada S, Florens L, Swanson SK, Washburn MP, Workman JL.
Characterization of the yeast trimeric-SAS acetyltransferase complex. J Biol Chem.
2005;280:11987-11994. Abstract
Ercan S, Carrozza MJ, Workman JL. Global nucleosome distribution and the
regulation of transcription in yeast. Genome Biol. 2004;5:243. Abstract
Jeronimo C, Langelier MF, Zeghouf M, Cojocaru M, Bergeron D, Baali D, Forget D,
Mnaimneh S, Davierwala AP, Pootoolal J, Chandy M, Canadien V, Beattie BK,
Richards DP, Workman JL, Hughes TR, Greenblatt J, Coulombe B. RPAP1, a novel
human RNA polymerase II-associated protein affinity purified with recombinant
wild-type and mutated polymerase subunits. Mol Cell Biol. 2004;24:7043-7058.
Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates JR, 3rd,
Abmayr SM, Washburn MP, Workman JL. Acetylation by Tip60 is required for
selective histone variant exchange at DNA lesions. Science. 2004;306:2084-2087.
Lee KK, Prochasson P, Florens L, Swanson SK, Washburn MP, Workman JL.
Proteomic analysis of chromatin-modifying complexes in Saccharomyces
cerevisiae identifies novel subunits. Biochem Soc Trans. 2004;32:899-903.
Robert F, Pokholok DK, Hannett NM, Rinaldi NJ, Chandy M, Rolfe A, Workman JL,
Gifford DK, Young RA. Global position and recruitment of HATs and HDACs in the
yeast genome. Mol Cell. 2004;16:199-209. Abstract
Vermeulen M, Carrozza MJ, Lasonder E, Workman JL, Logie C, Stunnenberg HG. In
vitro targeting reveals intrinsic histone tail specificity of the Sin3/histone
deacetylase and N-CoR/SMRT corepressor complexes. Mol Cell Biol.
2004;24:2364-2372. Abstract
Workman JL, Abmayr SM. Histone H3 variants and modifications on transcribed
genes. Proc Natl Acad Sci U S A. 2004;101:1429-1430. Abstract
Abmayr SM, Workman JL. Transcription factors prominently in Lasker Award to
Roeder. Cell. 2003;115:243-246. Abstract
Carrozza MJ, Hassan AH, Workman JL. Assay of activator recruitment of
chromatin-modifying complexes. Methods Enzymol. 2003;371:536-544. Abstract
Carrozza MJ, Kusch T, Workman JL. Repairing nucleosomes during transcription.
Nat Struct Biol. 2003;10:879-880. Abstract
Carrozza MJ, Utley RT, Workman JL, Cote J. The diverse functions of histone
acetyltransferase complexes. Trends Genet. 2003;19:321-329. Abstract
Kusch T, Guelman S, Abmayr SM, Workman JL. Two Drosophila Ada2 homologues
function in different multiprotein complexes. Mol Cell Biol. 2003;23:3305-3319.
Nourani A, Howe L, Pray-Grant MG, Workman JL, Grant PA, Cote J. Opposite
role of yeast ING family members in p53-dependent transcriptional activation. J
Biol Chem. 2003;278:19171-19175. Abstract
Sutton A, Shia WJ, Band D, Kaufman PD, Osada S, Workman JL, Sternglanz R.
Sas4 and Sas5 are required for the histone acetyltransferase activity of Sas2 in the
SAS complex. J Biol Chem. 2003;273:16887-16892. Abstract
Li B, Howe L, Anderson S, Yates JR III, Workman JL. The Set2 histone
methyltransferase functions through the phosphorylated carboxyl-terminal domain
of RNA polymerase II. J Biol Chem. 2003;278: 8897-8903. Abstract
Carrozza MJ, Sil AK, Hopper JE, Workman JL. Gal80 confers specificity on HAT
complex interactions with activators. J Biol Chem. 2002;277:24648-24652.
Hassan AH, Neely KE, Prochasson P, Chandy M, Workman JL. Function and
selectivity of bromodomains in anchoring chromatin-modifying complexes to
promoter nucleosomes. Cell. 2002;111:369-379. Abstract
Howe L, Kusch T, Muster N, Chaterji R, Yates JR, Workman JL. Yng1p modulates
the activity of Sas3p as a component of the yeast NuA3 histone acetyltransferase
complex. Mol Cell Biol. 2002;22:5047-5054. Abstract
Neely KE, Hassan AH, Brown CE, Howe L, Workman JL. Transcription activator
interactions with multiple SWI/SNF subunits. Mol Cell Biol. 2002;22:1615-1625.
Pray-Grant MG, Kennedy EL, Schieltz D, Cook R, Workman JL, Yates JR III, Grant
PA. The novel SLIK histone acetyltransferase complex functions in the retrograde
response pathway. Mol Cell Biol. 2002;24:;8774-8786. Abstract
Brown CE, Howe L, Sousa K, Alley SC, Tan S, Workman JL. Recruitment of HAT
complexes by direct activator interactions with the ATM-related Tra1 subunit.
Science. 2001;292:2333-2337. Abstract
Hassan AH, Neely KE, Workman JL. Histone acetyltransferase complexes stabilize
SWI/SNF binding to promoter nucleosomes. Cell. 2001;104:817-827. Abstract
Howe L, Austin D, Grant P, John S, Cook RG, Workman JL, Pillus L. Histone H3
specific HATs are essential for cell cycle progression. Genes Dev. 2001;15:31443154.
Osada S, Sutton A, Muster N, Brown CE, Yates JR, Sternglanz R, Workman JL.
The yeast SAS (something about silencing) protein complex contains a MYST-type
acetyltransferase and functions with chromatin assembly factor ASF1. Genes Dev.
2001;15:3155-3168. Abstract
John S, Howe L, Travov ST, Grant PA, Sternglanz R, Workman JL. The something
about silencing protein, SAS3, is the catalytic subunit of the NuA3 complex, a
TAF30-containing HAT complex that interacts with the Spt16 subunit of the yeast
CP (Cdc68/Pob3)/FACT complex. Genes Dev. 2000;14:1196-1208. Abstract
Lechner T, Grant PA, Eberharter A, Vannier D, Yu Y, Brosch G, Stillman DJ, Shore
D, Workman JL. Sds3 (Suppressor of defective silencing 3) is an integral
component of the yeast Sin3 / Rpd3 histone deacetylase complex and is required
for histone deacetylase activity. J Biol Chem. 2000;275:40961-40966. Abstract
Vignali M, Steger D, Neely K, Workman JL. Distribution of acetylated histones
resulting from Gal4-VP16 recruitment of SAGA and NuA4 complexes. EMBO J.
2000;19:2629-2640. Abstract
Wallberg AE, Neeley KE, Hassan AH, Gustafsson J-A, Workman JL, Wright APH.
Recruitment of the SWI-SNF chromatin remodeling complex as a mechanism of
gene activation by the glucocorticoid receptor tau1 activation domain. Mol Cell
Biol. 2000;20:2004-2013. Abstract
Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandl CJ, Pillus L, Workman JL,
Côté J. NuA4, an essential transcription adaptor/histone H4 acetyltransferase
complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J.
1999;18:5108-5119. Abstract
Bazett-Jones DP, Côté J, Landel CC, Peterson CL, Workman JL. SWI/SNF
complex creates loop domains in DNA and polynucleosome arrays and can disrupt
DNA: histone contacts within these domains. Mol Cell Biol. 1999;19:1470-1478.
Eberharter A, Sterner DE, Schieltz D, Hassan AH, Yates JR 3rd, Berger SL,
Workman JL. The ADA complex is a distinct histone acetyltransferase complex in
yeast. Mol Cell Biol. 1999;19:6621-6631. Abstract
Grant PA, Eberharter A, John S, Cook RG, Turner BM, Workman JL. Expanded
lysine acetylation specificity of Gcn5 in native complexes. J Biol Chem.
1999;274:5895-5900. Abstract
Ikeda K, Steger DJ, Eberharter A, Workman JL. Activation domain specific and
general transcription stimulation by native histone acetyltransferase complexes.
Mol Cell Biol. 1999;19:855-863. Abstract
Massari MB, Grant PA, Pray-Grant MG, Berger SL, Workman JL, Murre C. A
conserved motif present in a class of helix-loop-helix proteins activates
transcriptions by direct recruitment of the SAGA complex. Mol Cell. 1999;4:63-73.
Neely KE, Hassan AH, Wallberg AE, Steger DJ, Cairns BR, Wright APH, Workman
JL. Activation domain-mediated targeting of the SWI/SNF complex to promoters
stimulates transcription from nucleosome arrays. Mol Cell. 1999;4:649-655.
Ohba R, Steger DJ, Brownell JE, Mizzen CA, Cook RG, Côté J, Workman JL, Allis
CD. A novel H2A/H4 nucleosomal histone acetyltransferase in Tetrahymena
thermophila. Mol Cell Biol. 1999;19:2061-2068. Abstract
Sterner DE, Grant PA, Roberts SM, Duggan LJ, Belotserkovskaya R, Pacella LA,
Winston F, Workman JL, Berger SL. Functional organization of the yeast SAGA
complex: distinct components involved in structural integrity, nucleosome
acetylation, and TBP binding. Mol Cell Biol. 1999;19:86-98. Abstract
Wallberg AE, Neely KE, Gustafsson J-Å, Workman JL, Wright AP, Grant PA. HAT
complexes can mediate transcriptional activation by the major glucocorticoid
receptor activation domain. Mol Cell Biol. 1999;19:5952-5959. Abstract
Whitehouse I, Flaus A, Cairns BR, White MF, Workman JL, Owen-Hughes T.
Catalytic nucleosome mobilisation mediated by the SWI/SNF complex. Nature.
1999;400:784-787. Abstract
Côté J, Peterson CL, Workman JL. Perturbation of nucleosome structure by the
SWI/SNF complex persists following its detachment, enhancing subsequent
transcription factor binding. Proc Natl Acad Sci USA. 1998;9:4947-4952. Abstract
Grant PA, Schieltz D, Pray-Grant MG, Yates JR III, Workman JL. The ATM-related
cofactor Tra1 is a component of the purified SAGA complex. Mol Cell.
1998;2:863-867. Abstract
Grant PA, Schieltz D, Pray-Grant MG, Steger DJ, Reese JC, Yates III JR, Workman
JL. A subset of TBP-associated factors, TAFIIs, are integral components of the
SAGA complex that are required for nucleosome acetylation and transcription
stimulation. Cell. 1998;94:45-53. Abstract
Mutskov V, Gerber D, Angelov D, Ausio J, Workman JL, Dimitrov S. Persistent
interactions of the core histone tails with nucleosomal DNA following acetylattion
and transcription factor binding. Mol Cell Biol. 1998;18:6298-6304. Abstract
Steger DJ, Eberharter A, John S, Grant PA, Workman JL. Purified histone
acetyltransferase complexes stimulate HIV-1 transcription from preassembled
nucleosomal arrays. Proc Natl Acad Sci USA. 1998;95: 2924-12929. Abstract
Utley RT, Ikeda K, Grant PA, Côté J, Steger DJ, Eberharter A, John S, Workman JL.
Transcriptional activators target histone acetyltransferase complexes to
nucleosomes. Nature. 1998;394:498-502. Abstract
Grant PA, Duggan L, Côté J, Roberts SM, Brownell JE, Candau R, Ohba R, OwenHughes T, Allis CD, Winston F, Berger SL, Workman JL. Yeast Gcn5 functions in
two multisubunit complexes to acetylate nucleosomal histones: characterization of
an ADA complex and the SAGA (Spt/Ada) complex. Genes Dev. 1997;11:16401650. Abstract
Juan L-J, Utley RT, Vignali M, Bohm L, Workman JL. H1-mediated repression of
transcription factor binding to a stably positioned nucleosome. J Biol Chem.
1997;272:3635-3640. Abstract
Steger DJ, Workman JL. Stable co-occupancy of transcription factors and
histones at the HIV-1 enhancer. EMBO J. 1997;16:2463-2472. Abstract
Utley RT, Côté J, Owen-Hughes T, Workman JL. SWI/SNF stimulates the
formation of disparate activator-nucleosome complexes but is partially redundant
with cooperative binding. J Biol Chem. 1997;272:12642-12649. Abstract
Owen-Hughes TA, Utley RT, Côté J, Peterson CL, Workman JL. Persistent site
specific remodeling of a nucleosome array by transient action of the SWI/SNF
complex. Science. 1996;273:513-516. Abstract
Owen-Hughes TA, Workman JL. Remodeling the chromatin structure of a
nucleosome array by transcription factor-targeted trans-displacement of histones.
EMBO J. 1996;15:4702-4717. Abstract
Vettese-Dadey M, Grant PA, Hebbes TR, Crane-Robinson C, Allis CD, Workman JL.
Acetylation of histone H4 plays a primary role in enhancing transcription factor
binding to nucleosomal DNA in vitro. EMBO J. 1996;15:2508-2518. Abstract
Wang W, Côté J, Xue Y, Zhou S, Khavari PA, Biggar SR, Muchardt C, Kalpana GV,
Goff SP, Yaniv M, Workman JL, Crabtree GR. Purification and biochemical
heterogeneity of the mammalian SWI/SNF complex. EMBO J. 1996;15:5370-5382.