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First published online 16 January 2008
doi: 10.1242/dev.015362
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1 Department of Biochemistry, Biophysics, and Molecular Biology, Iowa State
University, Ames, IA 50011, USA.
2 Department of Cell and Structural Biology, University of Illinois, Urbana, IL
61801, USA.
* Author for correspondence (e-mail: kristen{at}iastate.edu)
Accepted 4 December 2007
 |
SUMMARY |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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Key words: Histone H3S10 phosphorylation, Chromatin structure remodeling, JIL-1 kinase, Drosophila
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INTRODUCTION |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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). However, these histone modifications do not occur in
isolation but rather in a combinatorial manner, leading to both synergistic
and antagonistic pathways (Allis et al.,
2007) in which the same mark may participate
(Berger, 2007). This has made
it difficult to establish a defined causative biological effect of the
addition or removal of a single mark in vivo. In Drosophila it has
recently been demonstrated that histone H3S10 phosphorylation by the JIL-1
kinase is important for maintaining chromatin structure and gene expression
(Wang et al., 2001;
Ebert et al., 2004;
Deng et al., 2005;
Zhang et al., 2006;
Bao et al., 2007). The JIL-1
histone H3S10 tandem kinase localizes specifically to euchromatic interband
regions of polytene chromosomes (Jin et
al., 1999), and analysis of a JIL-1 null allele,
JIL-1z2, has shown that JIL-1 is essential for
viability (Wang et al., 2001;
Zhang et al., 2003).
Furthermore, mutational analysis has demonstrated that a reduction in JIL-1
kinase activity leads to a global disruption of chromatin structure and that
maintaining histone H3S10 phosphorylation levels at the euchromatic regions is
necessary to counteract heterochromatization and gene silencing
(Wang et al., 2001;
Ebert et al., 2004;
Zhang et al., 2006;
Bao et al., 2007). However, we
were interested in determining whether phosphorylation of the histone H3S10
residue by the JIL-1 kinase in addition may serve as an epigenetic mark that
can play a causative role in establishing euchromatic chromatin regions. To
test this hypothesis we applied a LacI-tethering system that has previously
been used to study the effects of transcriptional activators on large-scale
chromatin structure in mammalian cells
(Tumbar et al., 1999;
Carpenter et al., 2005) as well
as the effects of ectopic HP1 on chromatin structure and gene silencing in
Drosophila (Li et al.,
2003; Danzer and Wallrath,
2004). Using this approach we show that JIL-1 mediated ectopic
histone H3S10 phosphorylation is sufficient to induce a change in higher-order
chromatin structure from a condensed heterochromatin-like state to a more open
euchromatic state during development. |
MATERIALS AND METHODS |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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)
inserted in the pUAST vector. A `kinase dead' lacI-JIL-1 was generated using
the TransformerTM Site-Directed Mutagenesis kit (Clon-Tech) to introduce
K293A and K652A substitutions in the ATP-binding loops for each kinase domain.
The fidelity of the constructs was verified by sequencing at the Iowa State
University Sequencing Facility.
Drosophila melanogaster stocks
Fly stocks were maintained according to standard protocols
(Roberts, 1998). Lac operator
insertion lines and the GFP-lacI fusion line are described in Li et al.
(Li et al., 2003) and Danzer
and Wallrath (Danzer and Wallrath,
2004). LacI-JIL-1 and LacI-JIL-1 kinase dead pUAST lines were
generated by standard P-element transformation (BestGene, Inc.) and driven
using the tub-GAL4 (P[tub>CD2>GAL4]) or
Sgs3-GAL4 drivers (obtained from the Bloomington Stock Center)
introduced by standard genetic crosses.
Immunohistochemistry
Polytene chromosome squash preparations were performed as in Kelley et al.
(Kelley et al., 1999) using
either 1 or 5 minute fixation protocols and labeled with antibody as described
in Jin et al. (Jin et al.,
1999). Primary antibodies include chicken anti-GFP (Aves Labs,
Tigard, OR), rabbit anti-H3S10ph (Epitomics), mouse anti-Pol
II0ser2 (Covance), mouse anti-Pol II0ser5 (Covance),
rabbit anti-H4K16ac (Upstate Biotechnology), rabbit anti-BRM (gift from Dr J.
Tamkun), mouse anti-lacI (Upstate Biotechnology), rabbit anti-JIL-1
(Jin et al., 1999), chicken
anti-JIL-1 (Jin et al., 2000)
and anti-JIL-1 mAb 5C9 (Jin et al.,
2000). DNA was visualized by staining with Hoechst 33258 or with
propidium iodide (Molecular Probes) in PBS. The final preparations were
mounted in 90% glycerol containing 0.5% n-propyl gallate and examined using
epifluorescence optics (40x Plan-Neofluar 1.30 NA) on a Zeiss Axioskop
microscope. Images were captured and digitized using a Spot CCD camera
(Diagnostic Instruments), imported into PhotoShop, and pseudocolored,
image-processed and merged.
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) using
extracts from third-instar salivary glands of the specified genotype. For the
quantification of immunolabeling, digital images of exposures of immunoblots
on blue X-ray film (Phenix) were analyzed using the ImageJ software as
previously described (Zhang et al.,
2006). |
RESULTS |
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SUMMARY
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MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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). A
clear example of this is found within the band-interband regions observed in
Drosophila larval polytene chromosomes
(Ananiev and Barsky, 1985;
Zhimulev et al., 2004), where
gene-active interband regions are made up of parallel 10 nm nucleosome fibrils
loosely aligned, whereas in the transcriptionally repressed banded regions the
nucleosome fibrils are folded into 30 nm chromosome fibrils that are further
compacted into dense higher-order chromatin structures
(Ananiev and Barsky, 1985;
Zhimulev et al., 2004). The
two states of chromatin can be readily distinguished in polytene squash
preparations by labeling with the fluorescent DNA dyes Hoechst 33258 or
propidium iodide, which bind stoichiometrically to DNA
(Haugland, 2002). In order to
determine whether ectopic histone H3S10 phosphorylation would be sufficient to
induce a change in higher-order chromatin structure and turn a condensed
banded chromatin region into an interband region with a more open euchromatic
chromatin structure, we applied a LacI tethering system
(Tumbar et al., 1999;
Li et al., 2003;
Danzer and Wallrath, 2004;
Carpenter et al., 2005). The
tethering system has two components: a reporter transgene containing 256
repetitive binding sites (lacO repeats) for the lac
repressor DNA-binding domain (LacI) and a transgene expressing a LacI domain
fused to the protein of interest under UAS-GAL4 promoter control. We
generated expression stocks containing two transgenes, one encoding the
LacI-binding domain fused to full-length JIL-1, and one encoding a `kinase
dead' version of JIL-1 in which the crucial lysine for catalytic activity
(Bjørbæk et al.,
1995) in each of the two kinase domains (K293 and
K652, respectively) was changed to alanine
(Fig. 1). In addition, an
expression construct containing a transgene encoding green fluorescent protein
(GFP) was used as a control (Li et al.,
2003).
Ectopic tethering of LacI-JIL-1 induces histone H3S10 phosphorylation and chromatin decondensation
We first analyzed the effect of tethering JIL-1 using line P11.3 and a
tub-Gal4 driver for LacI fusion protein expression. The
lacO-repeat-containing P-element in P11.3 is inserted into the middle
of a polytene band in region 96C1-2 (Li et
al., 2003), as verified by PCR analysis
(Li et al., 2003) as well as
by light and electron microscopy (Novikof et al., 2007). When LacI-GFP was
tethered as detected by GFP-antibody (Fig.
2A) condensed morphology of the band in polytene squash
preparations from third instar larval salivary glands remained without any
obvious subdivisions as labeled by Hoechst 33258. However, when LacI-JIL-1 was
tethered to this location as detected by either LacI
(Fig. 2B) or JIL-1 antibody
(Fig. 2C), the chromatin
attained an interband morphology and the band appeared `split in two',
reflecting a decondensation of the chromatin. This phenotype was robust and
found in at least 75% of the chromosomes examined from more than 30
independent squash preparations, and was not present in the absence of
tub-GAL4 induction (Fig.
2D). Furthermore, the tethering of the LacI-JIL-1 fusion protein
was clearly associated with distinct hyperphosphorylation of the histone H3S10
residue, as demonstrated by double labeling with H3S10ph antibody. This is in
contrast to the tethering of LacI-GFP, which did not result in ectopic or
upregulated H3S10 phosphorylation (Fig.
2A). Thus, these experiments strongly suggest that histone H3S10
phosphorylation by the JIL-1 kinase is sufficient to promote striking changes
in chromosomal packaging into a more open euchromatic state in an otherwise
condensed banded chromatin region that is normally without histone H3S10
phosphorylation.
|
), whereas
line 4D5 is inserted into an interband at region 4D5
(Danzer and Wallrath, 2004).
In the heterozygous condition only one of the paired chromatids of the
polytene chromosomes will carry the lacO repeats, with the other
chromatid being wild type. As illustrated in
Fig. 3, when LacI-JIL-1 was
targeted to such heterozygous polytene chromosome preparations morphological
changes and chromatin decondensation predominantly occurred in the chromatid
where LacI-JIL-1 was tethered. In the case of the interband and the
band-interband junction insertions, the increased accumulation of LacI-JIL-1
at the tethering site nucleated spreading of high levels of LacI-JIL-1 and
histone H3S10 phosphorylation to surrounding chromosome regions, in some cases
leading to chromatin decondensation of adjacent bands
(Fig. 3B-D). Such spreading was
also observed in P11.3/+ preparations; however, from this insertion
site the spreading was often discontinuous, resulting in small ectopic patches
of upregulated LacI-JIL-1 (Fig.
3A). In some preparations the two paired chromatids of the
polytene chromosomes were slightly separated at the insertion site, making the
LacI-JIL-1-induced changes in chromatin structure especially evident
(Fig. 3C,D). This separation
may be due to alterations in chromatid alignment caused by the changes in
chromatin structure in only one of the chromatids.
Tethering of LacI-JIL-1 `kinase dead' to lacO repeat insertion sites has a dominant-negative effect
To verify that the observed chromatin structure changes depended on JIL-1
kinase-mediated histone H3S10 phosphorylation and not on the tethering of the
LacI-JIL-1 construct itself, we examined the effects of tethering a LacI-JIL-1
`kinase dead' construct (LacI-JIL-1-kd). When this construct was expressed in
the lacO repeat line P11.3 it accumulated at higher concentrations in
the target area (Fig. 4A);
however, instead of opening up the compacted chromatin, as in the case when
wild-type LacI-JIL-1 was targeted, it induced severe chromatin structure
perturbations as well as numerous ectopic contacts between non-homologous
chromatin regions (Fig. 4B,C).
This phenotype was observed at every target site examined in more than 50
chromosome squash preparations. As illustrated in
Fig. 4B, the accumulation of
LacI-JIL-1-kd was not associated with any detectable upregulation of histone
H3S10 phosphorylation. Furthermore, immunoblot analysis of protein extracts
from third instar larval salivary glands
(Fig. 4D) showed that
endogenous JIL-1 (0.70±0.13 of wild-type levels, n=6), as well
as histone H3S10 phosphorylation levels (0.24±0.18 of wild-type levels,
n=8), were reduced when LacI-JIL-1-kd was expressed. These results
suggest that expression of LacI-JIL-1-kd had a dominant-negative effect and
that it reduced global histone H3S10 phosphorylation levels by displacing
native JIL-1 from the normal binding sites of JIL-1. That LacI-JIL-1-kd
localized to euchromatic interband regions is illustrated by LacI antibody
labeling in Fig. 4A.
Furthermore, Fig. 4A shows that
this localization often led to chromatin disruption and ectopic chromatin
associations at additional chromosome sites to that of the lacO
repeat insertion site. The chromatin structure disruption caused by
LacI-JIL-1-kd recruitment in homozygous insertion lines was too extensive to
allow for the determination of the exact location of the target site
(Fig. 4B). However, in some
cases remnants of the polytene band-interband organization was sometimes still
discernible, as shown in Fig.
4C, which further illustrates that the ectopic chromatin
connections between non-homologous chromatin regions near the target sites
were associated with high levels of LacI-JIL-1-kd.
|
; Zhimulev et
al., 2004), we performed tethering experiments with the
salivary-gland-specific Sgs3-GAL4 driver line. The onset of
expression of this driver is not before the mid-third instar larval transition
midway through the third larval instar
(Cherbas et al., 2003). As
illustrated in Fig. 5A,B we
observed similar changes in chromatin structure to those induced using the
tub-GAL4 driver line.
The LacI-JIL-1 tethering induced chromatin changes are not associated with enhanced transcriptional activity
An important issue is whether the observed changes in chromatin structure
are associated with transcriptional activation or whether the changes occur
independently of transcription. We therefore labeled the LacI-JIL-1 tethering
site in preparations homozygous for the lacO repeat line P11.3 with
antibody to the elongating form of RNA polymerase II (Pol II0ser2),
which is phosphorylated at serine 2 in the COOH-terminal domain
(Weeks et al., 1993;
Boehm et al., 2003). As
illustrated in Fig. 6A, there
is no upregulation of Pol II0ser2 labeling at the tethering site
and the labeling is several fold less than at adjacent transcriptionally
active regions, as indicated by the robust levels of Pol II0ser2 at
these sites. We also labeled the LacI-JIL-1 tethering site with antibody to
the paused form of RNA polymerase II (Pol II0ser5), which is
phosphorylated at serine 5 in the COOH-terminal domain
(Weeks et al., 1993;
Boehm et al., 2003). As shown
in Fig. 6B, the labeling was
absent or at very low levels at the tethering site compared with adjacent
interband regions. These data indicate that the chromatin structure changes
are likely to be independent of enhanced transcriptional activity.
|
|
;
Jin et al., 2000) and
therefore potentially could recruit dosage compensation proteins, leading to
local acetylation of histone H4K16. However, as illustrated in
Fig. 6C, tethering of
LacI-JIL-1 does not lead to enhanced histone H4K16 acetylation at the
lacO tethering site. Moreover, the chromatin structure changes
resulting from LacI-JIL-1 tethering occur in both male and females, suggesting
that it is highly unlikely that the MSL dosage compensation complex
contributes to these changes. Another candidate complex to mediate the
chromatin structure changes if recruited to the LacI-JIL-1 tethering sites is
the Brahma (BRM) chromatin remodeling complex, which is associated with nearly
all transcriptionally active chromatin at chromosome puffs and interband
polytene chromosome regions (Armstrong et
al., 2002). However, as shown in
Fig. 6D, levels of the BRM
protein are considerably lower at the LacI-JIL-1 tethering site in the
homozygous P11.3 lacO insertion line compared with the levels at
adjacent interband regions. |
DISCUSSION |
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DISCUSSION
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). The modifications have been broadly classified as either
repressing or activating; however, it has become clear that many of these
marks may have several complex and seemingly conflicting roles
(Berger, 2007). For this reason
it has been difficult to assign clear mechanistic functions to these histone
marks and to determine whether they represent a cause or an effect. For
example, in previous studies of histone H3S10 phosphorylation in
Drosophila using mutational analysis
(Wang et al., 2001;
Zhang et al., 2006) it could
not be resolved whether the H3S10ph mark had the capacity to induce chromatin
changes or whether it played only a reinforcing or maintenance role. Here we
demonstrate using a LacI tethering system that ectopic histone H3S10
phosphorylation by the JIL-1 kinase is sufficient to cause striking changes in
chromatin packaging from a condensed to an open state. This effect was absent
when a `kinase dead' LacI-JIL-1 construct without histone H3S10
phosphorylation activity was expressed. This indicates that the observed
chromatin structure changes depended on JIL-1-kinase-mediated histone H3S10
phosphorylation and not on the tethering of the LacI-JIL-1 construct itself.
Instead, the kinase dead construct had a dominant-negative effect, leading to
a disruption of chromatin structure that was associated with a global
repression of histone H3S10 phosphorylation levels. Interestingly, these
dominant-negative effects of LacI-JIL-1-kd on chromatin structure phenocopy
those observed in JIL-1 loss-of-function null mutants
(Wang et al., 2001;
Deng et al., 2005).
Furthermore, using a late-onset driver we show that LacI-JIL-1-induced histone
H3S10 phosphorylation can also effect changes after polytene chromosome
band/interband structure has been well established at second and early third
instar larval stages (Ananiev and Barsky,
1985; Zhimulev et al.,
2004). Thus, the changes in chromatin packaging are not likely to
depend on constitutive histone H3S10 phosphorylation or a stage-specific
developmental program.
|
;
Ivaldi et al., 2007),
suggesting the possibility that the chromatin changes resulting from ectopic
LacI-JIL-1 tethering could be associated with activation of the RNA polymerase
II machinery. However, several studies have indicated that the expanded
chromatin state during puffing in many cases precedes and/or is separable from
gene activation (Meyerowitz et al.,
1985; Tulin and Spradling,
2003). Using antibody to the elongating form of RNA polymerase II
we did not detect any indications of increased transcriptional activity at the
LacI-JIL-1 tethering sites. Similarly, there was no upregulation compared to
adjacent interband regions of the BRM chromatin remodeling complex, which has
been shown to play a general role in facilitating transcription by RNA
polymerase II in Drosophila
(Armstrong et al., 2002). Taken
together, these results indicate that the histone
H3S10-phosphorylation-induced changes observed in this study are not likely to
be a consequence of enhanced transcriptional activity. However, it should be
emphasized that a role for the BRM complex or other chromatin remodeling
complexes in mediating these changes in chromatin structure cannot be ruled
out based on the present experiments but will require more comprehensive
studies.
The above described observations suggest a model for how targeting of
LacI-JIL-1 can establish euchromatic domains in otherwise banded polytene
regions with condensed higher-order chromatin
(Fig. 7). The presence of an
extended region of lacO repeats recruits a high level of LacI-JIL-1,
which in turn hyperphosphorylates histone H3S10 at the target site as well as
at adjacent chromatin regions (Fig.
7B). The ectopic phosphorylation of histone H3S10 subsequently
induces the release of condensing factors and/or recruits euchromatic
remodeling factors (Fig. 7B).
It is unlikely that H3S10 phosphorylation would have a direct effect on
higher-order chromatin folding, as nucleosomal arrays assembled with
phosphorylated H3S10 do not behave differently from unmodified H3S10
(Fry et al., 2004). In
addition, mutational analysis has demonstrated that JIL-1-mediated maintenance
of H3S10 phosphorylation levels at euchromatic regions is necessary to
counteract heterochromatization and gene silencing
(Zhang et al., 2006).
Therefore, a plausible scenario for a molecular mechanism is that the ectopic
phosphorylation of histone H3S10 antagonizes the binding and/or activity of
condensing factors, thereby inducing a euchromatic chromatin state
(Fig. 7B). Interestingly,
phosphorylation of histone H3S10 by the Aurora B kinase during mitosis has
been shown to mediate the dissociation of HP1 proteins from heterochromatin in
a `methyl/phos switch' mechanism (Fischle
et al., 2005; Hirota et al.,
2005), although a causal relationship between this `switch' and
chromosome condensation has yet to be established. However, our data
demonstrate that during interphase H3S10 phosphorylation plays a different
role from that during mitosis and that this epigenetic modification is likely
to be a crucial factor in establishing, as well as in maintaining, euchromatic
chromatin domains during development.
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ACKNOWLEDGMENTS |
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REFERENCES |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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