Transcriptional Elongation by RNA Polymerase II and Histone Methylation*
Mark Gerber
and
Ali Shilatifard
¶
From the
Department of Biochemistry and the
St. Louis University Cancer Center, St. Louis
University School of Medicine, St. Louis, Missouri 63104
 |
ABSTRACT
|
---|
mRNA synthesis in eukaryotic organisms is a key biological process that is
regulated at multiple levels. From the covalent modifications of chromatin by
a number of chromatin remodeling complexes during the initiation and
activation steps of transcription to the processing of mRNA transcripts, a
very large consortium of proteins and multiprotein complexes is critical for
gene expression by RNA polymerase II. The list of proteins essential for the
successful synthesis of mRNA continues to grow at a rapid pace. Recent
advances in this area of research have been focused on transcription through
chromatin. In this article, we will review the recent literature linking the
key biochemical process of transcriptional elongation by RNA polymerase II to
histone methylation by COMPASS, Dot1p, and Set2 methyltransferases.
 |
The RNA Polymerase II Elongation Factors
|
---|
RNA polymerase II transcription proceeds through multiple stages,
designated preinitiation, initiation, and elongation. Historically, efforts to
understand the elongation phase of the transcription cycle lagged behind
efforts geared toward unraveling the processes of preinitiation and
initiation. However, during the past several years an immense amount of
research has been performed to identify and characterize transcription factors
that regulate the elongation stage of mRNA synthesis by RNA polymerase II.
Although there has been significant progress in the biochemical
characterization of these factors, little is known about their physiological
role in development in multicellular organisms or at what stages of
transcription elongation they function. However, recent studies have begun to
address the roles for some of the RNA polymerase II elongation factors using
in vivo model systems.
The known elongation factors fall into at least three functional classes.
The first class is composed of factors involved in drug-induced or
sequence-dependent arrest and includes the SII (also known as TFIIS) family of
elongation factors and PTEF-b (positive transcription elongation factor b)
(1,
2). SII was the first RNA
polymerase II transcription factor to be purified and is known to promote
efficient RNA polymerase II elongation by preventing DNA sequence-dependent
premature arrest (3,
4). Furthermore, SII and its
bacterial counterparts are the only known factors that can reactivate arrested
polymerase (5). PTEF-b is a
heterodimeric factor typically composed of cyclin T and Cdk9 and has been
shown to phosphorylate the C-terminal domain
(CTD)1 of the largest
subunit of RNA polymerase II, a critical event in the transition from
initiation to elongation (6).
In vivo cross-linking studies in yeast have demonstrated that
phosphorylation of serine 5 of the pol II CTD is localized to promoter and
promoter distal regions of genes and is therefore a marker for early
elongation complexes (7).
However, phosphorylation of serine 2 of the CTD exhibits a nearly
complementary pattern of localization and is found throughout the coding
regions and nearer the 3'-end genes, suggesting that serine 2
phosphorylation is a mark for RNA polymerase engaged in the processive phases
of transcription elongation
(7).
The second class of factors functions to regulate the rate of elongation
through chromatin and includes FACT (facilitates chromatin transcription)
(8). A third class operates by
increasing the catalytic rate of elongation by altering the
Km and/or the Vmax of pol II
and includes TFIIF, the Elongins, and the ELL family of proteins
(3,
4,
914).
ELL, which is found in translocation with the MLL gene in
patients with acute myeloid leukemia, was first biochemically isolated based
on it ability to increase the catalytic rate of transcription elongation by
RNA polymerase II (13,
15). Three mammalian and one
Drosophila homologue of the ELL family have been identified and
characterized, and biochemical and genetic evidence now suggests that
(a) ELL is an essential gene, (b) ELL associates
with actively elongating RNA pol II in vivo, and (c) ELL is
required for the efficient expression of specific genes
(13,
14,
1618).
Additionally, recent observations have refuted the previously conceived notion
that elongation factors that have similar biochemical activities have
overlapping or redundant functions in cells
(18).
In Saccharomyces cerevisiae, the Paf1 complex was both genetically
and biochemically isolated and demonstrated to function at both the initiation
and elongation stages of transcription
(1924).
Most importantly, recent studies have demonstrated that the Paf1 complex is
physically associated with elongating RNA polymerase II
(2224).
However, although the Paf1 complex has been shown to associate with elongating
RNA polymerase, its exact roles in transcription elongation remained unclear
until recently.
 |
Chromosomal Modifications by Histone Methylation
|
---|
A critical step in the activation of a gene is to make the DNA near the
promoter regions more accessible to the basal transcription machinery and RNA
polymerase II. In its natural state, the two-meter long DNA is packed around a
core histone octamer (containing two copies of histones H2A, H2B, H3, and H4)
called a nucleosome (25,
26). This structure can be
further compacted with the association of histone H1, making the DNA template
inaccessible to the transcriptional machinery. Compacted chromatin must be
"loosened" for transcription and gene expression to occur. This
process is accomplished by a set of enzymes known as chromatin remodeling or
modifying complexes. These complexes function by one of two mechanisms. The
first mechanism is dependent upon ATP hydrolysis and catalyzes a shifting of
nucleosomes along DNA
(2729).
The second mechanism involves the covalent modification of the histone
proteins that make up the nucleosomes
(30,
31). These modifications
include acetylation, phosphorylation, methylation, and ubiquitination.
Although modifications of histones were identified many years ago
(32,
33), it is only recently that
concentrated research from many laboratories has begun to elucidate how they
function in regulation of gene expression. Most of these modifications such as
ubiquitination are also involved in posttranslational modification of other
components of the transcription machinery in regulation of transcription
(34).
Although histone acetylation has been actively investigated for a number of
years, histone methylation (and the enzymes that catalyze this process) is not
as thoroughly understood. Recent efforts have begun to shed light on how
methylation of histones is important in the regulation of gene expression, and
these efforts have centered around the identification and characterization of
a number of histone methyltransferase (HMT) complexes, some of which will be
described here. Histone methylation occurs at a number of residues within all
four histones in the nucleosomal core, suggesting that this type of
modification could have a significant effect on the regulation of chromatin
structure. Recently, the identification of a number of novel HMTs has
implicated histone methylation as an important event in biological processes
such as telomeric silencing, transcriptional activation, and transcriptional
repression
(3549).
SUV39 was identified in Drosophila as a suppressor of position-effect
variegation and was the first histone methyltransferase to be identified
(50). Both trithorax (trx) and
polycomb (Pc) group proteins contain a 130140-amino acid motif called
the SET domain, which is found in a variety of chromatin-associated proteins.
This domain takes its name from the Drosophila proteins
Su(var)39, Enhancer of zeste (E(z)), and
Trithorax. Searching the data base for other SET domain-containing
proteins has revealed many other potential histone methyltransferase
candidates in a phylogenetically diverse group of organisms. These SET
domain-containing proteins are involved in methylation of lysine residues of
different histones. Fig. 1
illustrates the diverse pattern of histone methylation on lysines 4, 9, and 79
of histone H3 and the localization pattern of serine 2 phospho-RNA polymerase
II on Drosophila polytene chromosomes. For example, methylation of
histone H3 on lysine 9 occurs at the fused mass of heterochromatin known as
the chromocenter and is associated with position-effect variegation and
transcriptional silencing
(51). Because the
transcriptionally active (i.e. elongating) form of RNA polymerase II
is phosphorylated on serine 2 of its CTD, a comparison of the pattern of
distribution for lysine 4 and 79 methylated histone H3 with this form of RNA
polymerase II indicates that these modifications appear to colocalize. This
observation therefore implies that lysine 4 and 79 methylation of histone H3
is associated with the transcriptionally active euchromatin.

View larger version (45K):
[in this window]
[in a new window]
|
FIG. 1. Patterns of histone methylation and localization of phospho-RNA pol II
on Drosophila polytene chromosomes. Chromosomes were prepared and
stained with antibodies against the indicated histone modifications or
phospho-pol II (A, C, E, and G) and 4',
6'-diamidino-2-phenylindole (DAPI) (B, D, F, and
H). Chromosomes were analyzed by immunofluorescence. Arrows
in panels C and D indicate the heterochromatic chromocenter.
Arrows in panels G and H indicate sites of active
transcription, as evidenced by phospho-pol II localization.
|
|
In S. cerevisiae, there are six SET domain-containing proteins. We
will focus on Set1 and Set2 in this article. Yeast Set1 was originally
purified as part of a multiprotein complex, termed COMPASS (COMplex
of Proteins ASsociated with Set1)
(42,
43,
52). Related members in this
family of proteins include those encoded by the polycomb and trithorax groups
of genes, such as the mammalian MLL gene and Drosophila TRX.
In early studies, COMPASS was implicated in telomeric silencing, as a number
of deletion strains for the various components of this complex showed defects
in silencing genes located in telomeric regions
(42,
43). COMPASS can also
methylate lysine 4 of histone H3, and this modification is linked to telomeric
silencing (42,
43,
52).
To identify proteins involved in the methylation of histone H3 by COMPASS,
we developed Global Proteome analysis of
S. cerevisiae (GPS) to test by Western blotting extracts
of each of the non-essential yeast gene deletion mutants for defects in
methylation of lysine 4 of histone H3
(47). Employing this novel
method, it was demonstrated that methylation of histone H3 by COMPASS requires
the ubiquitination of lysine 123 of histone H2B in a process involving the
ubiquitin-conjugating enzyme, Rad6
(47). Allis and colleagues
(49) also reported the same
observation independently employing a different method. Because Rad6 is an E2
ubiquitin-conjugating enzyme involved in diverse biological pathways such as
the N-end rule pathway, DNA repair, recombination, and transcription, many
laboratories have been searching to identify the specific E3 ligase that
brings Rad6 to the transcription pathway. Employing GPS, we identified the
C3HC4 ring finger protein Bre1 as the E3 ligase that is required for
ubiquitination of histone H2B
(48,
54). These observations also
help to solidify the premise that there is indeed cross-talk between pathways
used to covalently modify histone octamers.
The Set2 protein was purified and characterized based on its
nucleosome-specific HMT activity
(39). Set2 is responsible for
the methylation of the lysine 36 residue of histone H3 in S.
cerevisiae (39). Set2 has
been demonstrated to be a potent repressor of transcription, suggesting a role
for lysine 36 methylation in down-regulating gene expression
(39). However, lysine 36
methylation is observed in transcriptionally active macronuclei in
Tetrahymena, supporting an additional role for this modification in
the potentiation of transcription
(55). Recent evidence from
several laboratories has provided a clearer picture of the role of Set2 in
transcription, as will be detailed below.
The Dot1 protein was originally identified in a genetic screen for high
copy suppression of telomeric silencing
(36,
56). This effect was later
shown to require Dot1-mediated methylation of the lysine 79 residue of histone
H3, which is found within the histone globular domain rather than the tail of
the protein, where a large portion of modifications occur
(36,
40). Unlike the Set family of
proteins, Dot1 does not contain a SET domain but instead methylates proteins
via a methylase fold. Early observations of the role of lysine 79 methylation
by Dot1 demonstrated that this modification of histone H3 inhibits binding of
the Sir silencing proteins at the telomeres and therefore regulates telomeric
silencing (36,
40). By analogy, it is likely
that methylation of histone H3 on lysine 4 also inhibits binding of the Sir
silencing proteins at telomeres and hence is associated with active loci as in
other organisms. Most importantly, both histone H3 lysine 79 and lysine 4
methylation seem to occur throughout the genome, but it appears slightly
higher at the coding regions of active genes
(57,
58).
 |
A Role for Histone Methylation of Lysine 4 of Histone H3 in
Transcription Elongation
|
---|
As mentioned previously, COMPASS, the yeast Set1-containing complex, is the
HMT that catalyzes the methylation of lysine 4 of histone H3
(42,
43,
46). Employing GPS, we
recently identified several other proteins required for methylation of lysine
4 by COMPASS. Among this group of proteins are some components of the Paf1
complex that have been found to associate with the elongating form of RNA
polymerase II (59). The Paf1
complex localizes to promoters and to the body of genes and is required for
the expression of a number of genes, mainly those responding to the
Pkc1/mitogen-activated protein kinase-signaling cascade
(60). Further investigation
has revealed that the physical interaction between COMPASS and RNA polymerase
II requires the presence of some of the components of the Paf1 complex.
Although the interaction between COMPASS and RNA polymerase II requires the
Paf1 complex, the association of Paf1 with RNA polymerase II is not dependent
upon COMPASS, indicating a role for the Paf1 complex as a
"platform" for COMPASS interaction with RNA polymerase II
(59).
Biochemical studies have also demonstrated that COMPASS interacts with the
form of RNA polymerase II whose CTD is phosphorylated at serine 5, but not
serine 2, i.e. the form of RNA polymerase that is associated with the
promoter and the early elongation complexes
(59,
61). Based on the recruitment
of COMPASS to elongating RNA polymerase II at the 5' portion of active
mRNA coding regions, it was demonstrated that COMPASS association depends on
the TFIIH-associated kinase (Kin28) that phosphorylates the RNA polymerase II
CTD and mediates the transition between initiation and elongation
(61).
 |
A Role for Histone Methylation of Lysine 79 of Histone H3 in
Transcription Elongation
|
---|
As mentioned above, Dot1 methylase is the sole HMT responsible for the
methylation of lysine 79 in S. cerevisiae
(36,
40,
62). This modification has
been hypothesized exclusively to regulate repression of genes in telomeric
regions by facilitating Sir protein association with chromatin
(36,
40). However, recent reports
indicate that this modification is also found in euchromatic regions of the
genome (Fig. 1). As with lysine
4 methylation, we have also demonstrated that the components of the Paf1
complex are also required for lysine 79 methylation in S. cerevisiae
(59). Although biochemical
evidence to support an interaction between Dot1 and RNA polymerase II via the
Paf1 complex is not yet available, the striking similarities between the
regulation of Dot1-mediated lysine 79 methylation and COMPASS-mediated lysine
4 methylation suggest a similar mechanism by which Dot1 is recruited to
chromatin. These observations are also consistent with a model in which the
Paf1 complex functions as a "platform" for interaction of histone
methyltransferases with elongating RNA polymerase II.
 |
A Role for Histone Methylation of Lysine 36 of Histone H3 in
Transcription Elongation
|
---|
As previously described, the Set2 protein is the HMT required for the
methylation of lysine 36 of histone H3
(39). In efforts to understand
the role of Set2 as a transcriptional regulatory factor and to investigate its
potential targeting mechanism, we and others have recently demonstrated an
interaction between Set2 and RNA polymerase II
(6366).
Chromatin immunoprecipitation experiments have demonstrated that Set2 and
methylation of lysine 36 of histone H3 are associated with the actively
transcribed coding regions of several genes. Most interestingly, interaction
of Set2 with RNA polymerase II requires the CTD of the largest subunit of pol
II. Specifically, Set2 preferentially associates with the serine 2
phosphorylated form of pol II, indicating that it associates with both early
elongating and processively elongating RNA polymerase II. Phosphorylation of
the CTD is essential for Set2 to bind RNA polymerase II and methylate histone
H3 on lysine 36
(6466).
Work performed in several laboratories has indicated that interaction of Set2
with the elongating pol II is lost in deletion strains lacking the CTD serine
2 kinase, Ctk1 (65,
66). Interestingly, Ctk1
deletion strains are defective for lysine 36 methylation, thus revealing the
mechanism targeting Set2 to chromatin. Unlike Dot1 and COMPASS, methylation of
lysine 36 by Set2 does not require ubiquitination of lysine 123 of histone
H2B. Rather, it appears that phosphorylation is the key event leading to
lysine 36 methylation, implicating a selective pathway for this modification.
However, similar to COMPASS and Dot1, interaction of Set2 with the elongating
RNA polymerase II requires the presence of the Paf1 complex, further
supporting a role for the Paf1 complex as a "platform" for the
interaction of histone methyltransferases with the elongating RNA polymerase
II. Alternatively, it is also possible that the Paf1 complex may function as a
"platform" for other enzymatic processes during the initiation and
the elongation phase of transcription.
 |
A Role for Histone Methylation through the Elongating RNA Polymerase
II as a Mark of "Transcriptional Memory" for Recently Transcribed
Genes
|
---|
One possible role of histone methylation on the body of protein coding
genes may be to function as a molecular memory for recently transcribed genes.
Specifically, methylation of histone H3 on lysines 4, 36, and 79 and the
requirement of the Paf1 complex for this histone modification are consistent
with this idea. Several recent studies have demonstrated that lysine 4 of
histone H3 can be methylated in coding regions during the transcription of a
gene and that this histone methylation persists for a considerable time after
transcriptional inactivation and the dissociation of COMPASS
(53,
57,
59,
61). Therefore, histone
methylation on the fourth lysine of histone H3 may inform the cell that
transcription of a given gene has occurred in the recent past but is not
necessarily happening at the present time. Although it has been demonstrated
that histone methylation clearly lasts for a significant portion of an
individual cell cycle, this modification is not faithfully transmitted to all
daughter cells (61). Thus,
histone marking by lysine 4 methylation appears to provide memory for recently
transcribed genes that is mechanistically distinct from the epigenetic memory
that occurs in position-effect variegation and transcriptional silencing via
methylation on lysine 9 of histone H3.
If histone H3 lysine 4 methylation functions as a mark for recently
transcribed genes, why then do cells also use methylation of histone H3 lysine
36 and lysine 79 for the same process? One possible explanation of this
observation is that different regions of the body of a transcribed gene may be
marked with different types of methylation. For example, histone H3 lysine 4
methylation is catalyzed by COMPASS at the promoters and in early elongation
complexes, whereas histone H3 lysine 36 and lysine 79 methylation, catalyzed
by Set2 and Dot1p, respectively, occurs during the productive phase of
transcription elongation. Therefore, histone methylation at different lysines
of histone H3 may inform the cell that transcription of a given gene has
occurred and how far the RNA polymerase II has transcribed through the body of
that gene in the recent past (Fig.
2). In this model, the Paf1 complex functions as a
"platform" through which all methyltransferases mentioned above
can interact and associate with the elongating RNA polymerase II, thereby
linking transcriptional elongation to histone methylation.

View larger version (20K):
[in this window]
[in a new window]
|
FIG. 2. The process of histone modification by ubiquitination and methylation at
the promoter and during the early and processive stages of transcription
elongation. A and B, the Rad6 ubiquitin-conjugating
enzyme is recruited to the promoter by its E3 ligase Bre1 and ubiquitinates
histone H2B (48). C,
after the formation of the preinitiation complexes, the CTD of RNA polymerase
II is phosphorylated by TFIIH. D and E, the Paf1 complex
functions as a "platform" for the recruitment of COMPASS resulting
in the methylation of the fourth lysine of histone H3 at the promoter and
early elongation complexes
(59). E and
F, following the phosphorylation of the CTD by Ctk1 complex, COMPASS
departs and again the Paf1 complex functions as a "platform" for
recruitment of Set2 methyltransferase resulting in the methylation of the
lysine 36 of histone H3. GTF, general transcription factor; SAM,
s-adenosylmethionine.
|
|
 |
FOOTNOTES
|
---|
* This minireview will be reprinted in the 2003 Minireview Compendium, which
will be available in January, 2004. 
¶
To whom correspondence should be addressed: Dept. of Biochemistry, St. Louis
University School of Medicine, 1402 South Grand Blvd., St. Louis, MO 63104.
Tel.: 314-577-8137; Fax: 314-268-5737; E-mail:
shilatia{at}slu.edu.
1 The abbreviations used are: CTD, C-terminal domain; pol II, polymerase II;
HMT, histone methyltransferase. 
 |
REFERENCES
|
---|
- Reines, D., and Mote, J., Jr. (1993) Proc.
Natl. Acad. Sci. U. S. A. 90,
19171921[Abstract]
- Marshall, N. F., and Price, D. H. (1995) J.
Biol. Chem. 270,
1233512338[Abstract/Free Full Text]
- Reines, D., Conaway, J. W., and Conaway, R. C. (1996)
Trends Biochem. Sci. 21,
351355[CrossRef][Medline]
[Order article via Infotrieve]
- Conaway, J. W., and Conaway, R. C. (1999)
Annu. Rev. Biochem. 68,
301319[CrossRef][Medline]
[Order article via Infotrieve]
- Wind, M., and Reines, D. (2000)
Bioessays 22,
327336[CrossRef][Medline]
[Order article via Infotrieve]
- Marshall, N. F., Peng, J., Xie, Z., and Price, D. H.
(1996) J. Biol. Chem.
271,
2717627183[Abstract/Free Full Text]
- Komarnitsky, P., Cho, E. J., and Buratowski, S. (2000)
Genes Dev. 14,
24522460[Abstract/Free Full Text]
- Orphanides, G., LeRoy, G., Chang, C. H., Luse, D. S., and Reinberg,
D. (1998) Cell
92,
105116[Medline]
[Order article via Infotrieve]
- Price, D. H., Sluder, A. E., and Greenleaf, A. L.
(1989) Mol. Cell. Biol.
9,
14651475[Medline]
[Order article via Infotrieve]
- Bradsher, J. N., Jackson, K. W., Conaway, R. C., and Conaway, J. W.
(1993) J. Biol. Chem.
268,
2558725593[Abstract/Free Full Text]
- Garrett, K. P., Tan, S., Bradsher, J. N., Lane, W. S., Conaway, J.
W., and Conaway, R. C. (1994) Proc. Natl. Acad. Sci.
U. S. A. 91,
52375241[Abstract]
- Duan, D. R., Pause, A., Burgess, W. H., Aso, T., Chen, D. Y.,
Garrett, K. P., Conaway, R. C., Conaway, J. W., Linehan, W. M., and Klausner,
R. D. (1995) Science
269,
14021406[Medline]
[Order article via Infotrieve]
- Shilatifard, A., Lane, W. S., Jackson, K. W., Conaway, R. C., and
Conaway, J. W. (1996) Science
271,
18731876[Abstract]
- Miller, T., Williams, K., Johnstone, R. W., and Shilatifard, A.
(2000) J. Biol. Chem.
275,
3205232056[Abstract/Free Full Text]
- Thirman, M. J., Levitan, D. A., Kobayashi, H., Simon, M. C., and
Rowley, J. D. (1994) Proc. Natl. Acad. Sci. U. S.
A. 91,
1211012114[Abstract/Free Full Text]
- Shilatifard, A., Duan, D. R., Haque, D., Florence, C., Schubach, W.
H., Conaway, J. W., and Conaway, R. C. (1997) Proc.
Natl. Acad. Sci. U. S. A. 94,
36393643[Abstract/Free Full Text]
- Gerber, M., Ma, J., Dean, K., Eissenberg, J. C., and Shilatifard,
A. (2001) EMBO J.
20,
61046114[Abstract/Free Full Text]
- Eissenberg, J. C., Ma, J., Gerber, M. A., Christensen, A.,
Kennison, J. A., and Shilatifard, A. (2002) Proc.
Natl. Acad. Sci. U. S. A. 99,
98949899[Abstract/Free Full Text]
- Stolinski, L. A., Eisenmann, D. M., and Arndt, K. M.
(1997) Mol. Cell. Biol.
17,
44904500[Abstract]
- Costa, P. J., and Arndt, K. M. (2000)
Genetics 156,
535547[Abstract/Free Full Text]
- Mueller, C. L., and Jaehning, J. A. (2002)
Mol. Cell. Biol. 22,
19711980[Abstract/Free Full Text]
- Pokholok, D. K., Hannett, N. M., and Young, R. A.
(2002) Mol. Cell.
9,
799809[Medline]
[Order article via Infotrieve]
- Krogan, N. J., Kim, M., Ahn, S. H., Zhong, G., Kobor, M. S.,
Cagney, G., Emili, A., Shilatifard, A., Buratowski, S., and Greenblatt, J. F.
(2002) Mol. Cell. Biol.
22,
69796992[Abstract/Free Full Text]
- Squazzo, S. L., Costa, P. J., Lindstrom, D. L., Kumer, K. E.,
Simic, R., Jennings, J. L., Link, A. J., Arndt, K. M., and Hartzog, G. A.
(2002) EMBO J.
21,
17641774[Abstract/Free Full Text]
- Kornberg, R. D. (1974) Science
184,
868871[Medline]
[Order article via Infotrieve]
- Kornberg, R. D., and Lorch, Y. (1999)
Cell 98,
285294[Medline]
[Order article via Infotrieve]
- Workman, J. L., and Kingston, R. E. (1998)
Annu. Rev. Biochem. 67,
545579[CrossRef][Medline]
[Order article via Infotrieve]
- Gavin, I., Horn, P. J., and Peterson, C. L. (2001)
Mol. Cell 7,
97104[Medline]
[Order article via Infotrieve]
- Peterson, C. L. (2002) Mol.
Cell 9,
921922[Medline]
[Order article via Infotrieve]
- Strahl, B. D., and Allis, C. D. (2000)
Nature 403,
4145[CrossRef][Medline]
[Order article via Infotrieve]
- Kouzarides, T. (2002) Curr. Opin. Genet.
Dev. 12,
198209[CrossRef][Medline]
[Order article via Infotrieve]
- Ballal, N. R., Kang, Y. J., Olson, M. O., and Busch, H.
(1975) J. Biol. Chem.
250,
59215925[Abstract]
- Hunt, L. T., and Dayhoff, M. O. (1977)
Biochem. Biophys. Res. Commun.
74,
650655[Medline]
[Order article via Infotrieve]
- Conaway, R. C., Brower, C. S., and Conaway, J. W.
(2002) Science
296,
12541258[Abstract/Free Full Text]
- Nislow, C., Ray, E., and Pillus, L. (1997)
Mol. Biol. Cell 8,
24212436[Abstract/Free Full Text]
- Ng, H. H., Feng, Q., Wang, H., Erdjument-Bromage, H., Tempst, P.,
Zhang, Y., and Struhl, K. (2002) Genes
Dev. 16,
15181527[Abstract/Free Full Text]
- Noma, K., and Grewal, S. I. (2002) Proc.
Natl. Acad. Sci. U. S. A. 99,
1643816445[Abstract/Free Full Text]
- Strahl, B. D., Briggs, S. D., Brame, C. J., Caldwell, J. A., Koh,
S. S., Ma, H., Cook, R. G., Shabanowitz, J., Hunt, D. F., Stallcup, M. R., and
Allis, C. D. (2001) Curr. Biol.
11,
9961000[CrossRef][Medline]
[Order article via Infotrieve]
- Strahl, B. D., Grant, P. A., Briggs, S. D., Sun, Z. W., Bone, J.
R., Caldwell, J. A., Mollah, S., Cook, R. G., Shabanowitz, J., Hunt, D. F.,
and Allis, C. D. (2002) Mol. Cell. Biol.
22,
12981306[Abstract/Free Full Text]
- van Leeuwen, F., Gafken, P. R., and Gottschling, D. E.
(2002) Cell
109,
745756[Medline]
[Order article via Infotrieve]
- Wang, H., Huang, Z. Q., Xia, L., Feng, Q., Erdjument-Bromage, H.,
Strahl, B. D., Briggs, S. D., Allis, C. D., Wong, J., Tempst, P., and Zhang,
Y. (2001) Science
293,
853857[Abstract/Free Full Text]
- Miller, T., Krogan, N. J., Dover, J., Erdjument-Bromage, H.,
Tempst, P., Johnston, M., Greenblatt, J. F., and Shilatifard, A.
(2001) Proc. Natl. Acad. Sci. U. S. A.
98,
1290212907[Abstract/Free Full Text]
- Krogan, N. J., Dover, J., Khorrami, S., Greenblatt, J. F.,
Schneider, J., Johnston, M., and Shilatifard, A. (2002)
J. Biol. Chem. 277,
1075310755[Abstract/Free Full Text]
- Nagy, P. L., Griesenbeck, J., Kornberg, R. D., and Cleary, M. L.
(2002) Proc. Natl. Acad. Sci. U. S. A.
99,
9094[Abstract/Free Full Text]
- Bryk, M., Briggs, S. D., Strahl, B. D., Curcio, M. J., Allis, C.
D., and Winston, F. (2002) Curr. Biol.
12,
165170[CrossRef][Medline]
[Order article via Infotrieve]
- Briggs, S. D., Bryk, M., Strahl, B. D., Cheung, W. L., Davie, J.
K., Dent, S. Y., Winston, F., and Allis, C. D. (2001)
Genes Dev. 15,
32863295[Abstract/Free Full Text]
- Dover, J., Schneider, J., Tawiah-Boateng, M. A., Wood, A., Dean,
K., Johnston, M., and Shilatifard, A. (2002) J. Biol.
Chem. 277,
2836828371[Abstract/Free Full Text]
- Wood, A., Krogan, N. J., Dover, J., Schneider, J., Heidt, J.,
Boateng, M.-A., Dean, K., Golshani, A., Zhang, Y., Greenblatt, J., Johnston,
M., and Shilatifard, A. (2003) Mol. Cell
11,
267274[Medline]
[Order article via Infotrieve]
- Sun, Z. W., and Allis, C. D. (2002)
Nature 418,
104108[CrossRef][Medline]
[Order article via Infotrieve]
- Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B. D., Sun, Z. W.,
Schmid, M., Opravil, S., Mechtler, K., Ponting, C. P., Allis, C. D., and
Jenuwein, T. (2000) Nature
406,
593599[CrossRef][Medline]
[Order article via Infotrieve]
- Grewal, S. I., and Elgin, S. (2002) Curr.
Opin. Genet. Dev. 12,
178187[CrossRef][Medline]
[Order article via Infotrieve]
- Roguev, A., Schaft, D., Shevchenko, A., Pijnappel, W. W., Wilm, M.,
Aasland, R., and Stewart, A. F. (2001) EMBO
J. 20,
71377148[Abstract/Free Full Text]
- Santos-Rosa, H., Schneider, R., Bannister, A. J., Sherriff, J.,
Bernstein, B. E., Emre, N. C., Schreiber, S. L., Mellor, J., and Kouzarides,
T. (2002) Nature
419,
407411[CrossRef][Medline]
[Order article via Infotrieve]
- Hwang, W. W., Venkatasubrahmanyam, S., Ianculescu, A. G., Tong, A.,
Boone, C., and Madhani, H. D. (2003) Mol.
Cell 11,
261266[Medline]
[Order article via Infotrieve]
- Strahl, B. D., Ohba, R., Cook, R. G., and Allis, C. D.
(1999) Proc. Natl. Acad. Sci. U. S. A.
96,
1496714972[Abstract/Free Full Text]
- Singer, M. S., Kahana, A., Wolf, A. J., Meisinger, L. L., Peterson,
S. E., Goggin, C., Mahowald, M., and Gottschling, D. E. (1998)
Genetics 150,
613632[Abstract/Free Full Text]
- Bernstein, B. E., Humphrey, E. L., Erlich, R. L., Schneider, R.,
Bouman, P., Liu, J. S., Kouzarides, T., and Schreiber, S. L.
(2002) Proc. Natl. Acad. Sci. U. S. A.
99,
86958700[Abstract/Free Full Text]
- Ng, H. H., Ciccone, D. N., Morshead, K. B., Oettinger, M. A., and
Struhl, K. (2003) Proc. Natl. Acad. Sci. U. S.
A. 100,
18201825[Abstract/Free Full Text]
- Krogan, N. J., Dover, J., Wood, A., Schneider, J., Heidt, J.,
Boateng, M.-A., Dean, K., Ryan, O. W., Golshani, A., Johnston, M., Greenblatt,
J., and Shilatifard, A. (2003) Mol. Cell
11,
721729[Medline]
[Order article via Infotrieve]
- Porter, S. E., Washburn, T. M., Chang, M., and Jaehning, J. A.
(2002) Eukaryotic Cell
1,
830842[Abstract/Free Full Text]
- Ng, H. H., Robert, F., Young, R. A., and Struhl, K.
(2003) Mol. Cell
11,
709719[Medline]
[Order article via Infotrieve]
- Lacoste, N., Utley, R. T., Hunter, J. M., Poirier, G. G., and Cote,
J. (2002) J. Biol. Chem.
277,
3042130424[Abstract/Free Full Text]
- Li, J., Moazed, D., and Gygi, S. P. (2002)
J. Biol. Chem. 277,
4938349388[Abstract/Free Full Text]
- Li, B., Howe, L., Anderson, S., Yates, J. R., and Workman, J. L.
(2003) J. Biol. Chem.
278,
88978903[Abstract/Free Full Text]
- Xiao, T., Hall, H., Kizer, K. O., Shibata, Y., Hall, M. C.,
Borchers, C. H., and Strahl, B. D. (2003) Genes
Dev. 17,
654663[Abstract/Free Full Text]
- Krogan, N. J., Kim, M., Tong, A., Gorshani, A., Cagney, G.,
Canadien, V., Richards, D., Beattie, B., Emili, A., Boone, C., Shilatifard,
A., Buratowski, S., and Greenblatt, J. (2003) Mol.
Cell. Biol. 23,
42074218[Abstract/Free Full Text]