1 Marie Curie Research Institute, The Chart, Oxted, Surrey RH8 0TL, UK
2 Department of Infection Biology, Institute of Basic Medical Sciences, University of Tsukuba, 1-1-1 Tennohdai, Tsukuba 305-8575, Japan
3 Department of Pharmacology, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
Correspondence
Peter O'Hare
P.OHare{at}mcri.ac.uk
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ABSTRACT |
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Published ahead of print on 12 June 2003 as DOI 10.1099/vir.0.19326-0
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INTRODUCTION |
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With the aim of understanding the functional role(s) of VP22, we wished to identify cellular proteins that interact with VP22. Previously, we used affinity chromatography on columns containing bound, purified VP22 to show that four proteins were retained specifically (van Leeuwen et al., 2002). One protein was identified as non-muscle myosin IIA (NMIIA) and we explored further the possibility that NMIIA may be involved in virus maturation. Here we report on the identity of two of the other VP22-binding proteins as template-activating factor I
and
(TAF-I
and -
), also named SETa and SETb (Adachi et al., 1994
; Nagata et al., 1995
; von Lindern et al., 1992
). TAF-I
and -
, identified originally as host factors required for adenovirus core replication, have been implicated in chromatin remodelling and were shown to promote the deposition of histones on naked DNA (Miyaji-Yamaguchi et al., 1999
; Okuwaki & Nagata, 1998
). Furthermore, a multiprotein complex containing TAF-I proteins as major subunits was shown recently to bind to histones, thereby preventing their acetylation by the cellular histone acetyltransferases p300 and PCAF (Seo et al., 2001
). Because of this histone-masking effect, the TAF-I-containing complex was named INHAT (inhibitor of acetyltransferases) (Seo et al., 2001
). TAF-I
was also identified as part of the putative oncogene associated with acute undifferentiated leukaemia when translocated to the CAN (NUP214) gene (Kraemer et al., 1994
; von Lindern et al., 1992
).
Using in vitro assays for TAF-I activity in chromatin assembly, we show that VP22 prevents nucleosome deposition on DNA by binding to TAF-I. We also observed that VP22 binds non-specifically to DNA, an activity that is blocked by recombinant TAF-I. However, VP22 had no effect on the HAT-inhibitory activity of the INHAT complex in vitro. Finally, we observed that TAF-I
overexpression appears to block the progression of HSV-1 infection. Together with the results on VP22 interaction and repression of chromatin assembly, our data indicate that modulation of TAF-I
-mediated nucleosome deposition and repression may play a role in virus infection.
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METHODS |
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Plasmids.
To construct a mammalian myc epitope-tagged TAF-I expression construct, the sequence was amplified by PCR from cDNA (Nagata et al., 1995
) using a TAF-I
-specific forward primer (5'-CGGAAGCTTAATATGGCCCCTAAACGCCAGTCTCC-3'), which contained a HindIII site, and a reverse primer (5'-GGTCTAGATCATCTTCTCCTTCATCCTCCTCTC-3'), which contained an XbaI site. The PCR product was digested with HindIII/XbaI and ligated into pCDNA3.1mychisB (Invitrogen), digested similarly with HindIII/XbaI. This resulted in the construction of an expression vector for full-length TAF-I
containing a 10 residue myc epitope tag at its C terminus. Cloning of the mammalian VP22 expression construct, pc49epB, has been described previously (Dilber et al., 1999
).
The VP22.C1.his6 bacterial expression construct was made by PCR amplification from pc49epB using VP22-specific primers containing HindIII/BamHI sites (forward primer, 5'-TCGGATCCGACCTCTCGCCGCTCCGTG-3'; reverse primer, 3'-TTAAGCTTCTCGACGGGCCGTCTGGG-3'). The PCR product was digested with HindIII/BamHI and cloned in pET24b (Novagen).
Immunofluorescence and antibodies.
COS cells seeded on glass coverslips were transfected with the appropriate expression vector and approximately 40 h later were washed twice with PBS and fixed for 20 min at -20 °C with 100 % methanol. The cells were then blocked in PBS containing 10 % calf serum for 10 min at room temperature. Primary antibodies were added in the same solution and incubated for 45 min at room temperature. Following two 5 min washes with PBS, secondary antibodies were added in blocking buffer and incubated for 15 min. After an additional two washes in PBS, the coverslips were mounted in Mowiol (Sigma) containing 2·5 % 1,4-diazabicyclo-2.2.2-octane to reduce bleaching. Antibodies used in this study and their dilutions were as follows: monoclonal antibody to the myc epitope (R950-25, diluted 1 : 200; Invitrogen) and polyclonal antibodies to VP22 (AGV30, diluted 1 : 500), as described before (Elliott & O'Hare, 1997). Polyclonal anti-TAF-I
antibody (Sp1) was a gift from T. Copeland (Adachi et al., 1994
). Secondary antibodies were FITC-conjugated anti-rabbit immunoglobulin (F1-2000, diluted 1 : 100; Vector Laboratories) and TRITC-conjugated anti-mouse (T7782, diluted 1 : 200; Sigma).
Protein purification.
VP22.C1 was purified on an Ni-NTA column as described previously (Normand et al., 2001). In order to purify VP22.C1 to homogeneity, an additional purification step on a Mono S HR 5/5 column (Pharmacia) was performed. Using a linear NaCl gradient, VP22.C1 eluted at approximately 400 mM NaCl of the Mono S column. Recombinant TAF-I
was purified similarly on an Ni-NTA column and a Mono Q HR 5/5 column. To examine direct proteinprotein interactions (see Fig. 2
), TAF-I
and -
and variants were purified as described previously (Miyaji-Yamaguchi et al., 1999
).
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Gel retardation assays.
Binding reactions were performed in 20 µl buffer containing 20 mM HEPES/KOH (pH 7·5), 1 mM EDTA, 1 mM DTT, 0·025 % Nonidet-P40, 4 % Ficoll and 0·5 nM DNA probe. The probe used was a 147 bp fragment from MspI-digested pUC19 that had been end-labelled with [-32P]dCTP using the Klenow fragment. Amounts of purified proteins used in the binding reactions are as indicated in the figures. Incubations were carried out for 60 min at 4 °C and the resulting complexes were resolved on a 5 % non-denaturing polyacrylamide gel run in 0·5x Tris/borate/EDTA.
From the known amounts of input protein and DNA, the DNA-binding constant could be calculated at approximately 1 nM [KD=(Total protein)-(DNA bound) at 50 % binding].
Nucleosome assembly assay.
Assembly and micrococcal nuclease digestion analysis were performed as described previously (Bulger & Kadonaga, 1994) using three components: (1) a core histone; (2) HuCHRAC (human chromatin accessibility complex) (Poot et al., 2000
), the ATP-dependent chromatin remodelling complex; and (3) recombinant TAF-I
(rTAF-I
), as histone chaperone. HuCHRAC (30 ng) was incubated in an ATP-containing buffer with relaxed plasmid DNA as substrate in the presence of various combinations of rTAF-I
and VP22, as indicated. After nucleosome assembly had completed on the target DNA, the DNA was digested with micrococcal nuclease. Proteins were then removed by phenol extraction and the DNA fragments were separated on agarose gels and detected by ethidium bromide staining.
HAT assay.
HAT (histone and nucleosome acetyltransferase) assays were performed as described previously (Seo et al., 2001).
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RESULTS |
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Partial amino acid sequences obtained for both the 41 and 39 kDa bands (Fig. 1, lane 3) were found to be identical (SGYRIDFYFDENPYFE). A database search of the amino acid sequence obtained revealed that the sequence corresponded precisely to human TAF-I
or -
, which have been reported to act as histone chaperone proteins (Nagata et al., 1998
). TAF-I
and -
have arisen from a gene duplication event, with TAF-I
located on chromosome 5 and TAF-I
on chromosome 17 (Nagata et al., 1995
). These genes differ from each other only in their extreme N-terminal regions (Fig. 2
B). To confirm that the peptide sequenced represents TAF-I, the eluted fraction was analysed by Western blotting, in this case using an antibody specific for the TAF-I
form. The results show that the 39 kDa protein was detected specifically by anti-TAF-I
(Fig. 1B
), and indicate that, consistent with the amino acid sequence data, the 41 kDa protein is likely to be TAF-I
.
Although the HeLa cell extract used to identify VP22-associated proteins was first pre-cleared by passing over a large Ni-NTA column, this pre-clearing step might have been inefficient, with the TAF-I proteins still binding to the VP22.C1 column by some non-specific interaction on the column. Therefore, we repeated the purification on a smaller scale, without any pre-clearing, to assay whether TAF-I bound to the Niagarose matrix at all (Fig. 1D
). HeLa cell cytoplasmic extracts were passed directly over a 100 µl NTA column or an NTA column with bound VP22.C1. Bound proteins were eluted and separated by SDS-PAGE and detected by silver staining. As expected, numerous cellular proteins remain associated with the empty column (Fig. 1D
, lane 1) but additional proteins (corresponding to those enriched in Fig. 1A
) can be seen on the VP22.C1-containing column (Fig. 1D
, lane 2, arrowheads). Western blotting showed that TAF-I
bound only to the VP22.C1-containing NTA column (Fig. 1E
, lane 2) with no non-specific binding to the control NTA column (Fig. 1E
, lane 1), confirming that the association of TAF-I
with VP22.C1 was specific (although not indicating whether the interaction was a direct or an indirect one).
To confirm the VP22.C1TAF-I/
interaction and to examine whether binding was a direct or an indirect association mediated by other bound cellular factors, we tested whether purified rTAF-I
and -
could bind and co-precipitate purified VP22.C1. Therefore, purified VP22.C1 (400 ng) was incubated alone or together with equimolar amounts of purified TAF-I
or -
proteins. Antibodies specific for TAF-I
or -
were then added and immunocomplexes isolated by the addition of protein ASepharose beads. Bound proteins were separated by SDS-PAGE and visualized by silver staining. [Note that the TAF proteins and variants are indicated by chevrons within the lanes, and VP22.C1 is indicated by the arrow to the right-hand side (Fig. 2
). Bound immunoglobulin heavy and light chains are labelled also.] Control incubations showed that no VP22.C1 was precipitated either by anti-TAF antibody in the absence of TAF-I proteins (Fig. 2
, lane 2) or when the TAF-I
-specific antibody was used in combination with the TAF-I
protein (Fig. 2
, lane 3). However, in the presence of TAF-I
together with the corresponding anti-TAF-I
antibody (Fig. 2
, lane 8), or TAF-I
together with the corresponding anti-TAF-I
antibody (Fig. 2
, lane 5), VP22 was co-precipitated efficiently (Fig. 2
, arrow). Comparison of the total input VP22.C1 for each of the test samples (Fig. 2
, lane 1) with the amount of co-precipitated VP22.C1 indicates that binding was efficient. TAF-I
and -
contain a C-terminal region of approximately 50 residues rich in acidic amino acids, which is important for chromatin remodelling activity (Miyaji-Yamaguchi et al., 1999
). We next tested whether this region was involved in the interaction with the largely basic VP22.C1 protein by incubation with variant TAF-I
(Fig. 2
,
C3) or TAF-I
(Fig. 2
,
C3 and
C5) lacking the C-terminal region (Fig. 2B
). Surprisingly, deletion of the C terminus had different effects on the VP22.C1 interaction for TAF-I
versus TAF-I
. Thus, removal of the C-terminal 54 residues of TAF-I
(
C3) had no effect on the interaction (Fig. 2
, lane 9), while the identical truncation of TAF-I
(
C3) reduced binding significantly, albeit not abolishing it completely (Fig. 2
, lane 6). A similar level of binding was observed for TAF-I
(
C5). While we do not fully understand this differential effect, which could, for example, be due to differences in the N terminus of TAF-I
and -
, the result for TAF-I
indicates that VP22.C1 binding is not due to straightforward charge interaction with the C-terminal acidic region.
Transfected TAF-I and VP22 do not co-localize on condensed chromosomes
VP22 is found both in the cytoplasm and in the nucleus, where nuclear localization represents cells that retain VP22 after nuclear envelope breakdown and division (Elliott & O'Hare, 2000). VP22 has been shown to localize to condensed chromatin during mitosis. Although TAF-I is a chaperone protein and escorts histones onto DNA through a direct interaction, it does not remain associated with condensensed chromosomes (K. Nagata, personal communication). We wished to examine the localization of VP22 and TAF-I
/
when co-expressed by transfection in COS-1 cells. An epitope-tagged (myc) version of TAF-I
was used to detect its localization by indirect immunofluorescence. VP22 was detected with the specific rabbit polyclonal antibody AGV30 (Elliott & O'Hare, 1997
). TAF-I
was found largely in the nucleus and, as described previously (Elliott & O'Hare, 2000
), transfected VP22 was found in the nucleus where nuclear localization represents cells that have divided. The nuclear staining patterns of VP22 and TAF-I
showed no obvious subnuclear localization pattern, both being excluded from the nucleoli (data not shown). However, in mitotic cells where VP22 was bound to the condensing cellular chromatin (Fig. 3
), TAF-I
was excluded from metaphase chromatin (Fig. 3
). The presence of VP22 on condensed chromosomes, therefore, does not appear to actively retain TAF-I
chromosomes, at least at detectable levels. These results were, therefore, inconclusive in attempting to substantiate an in vivo association between the two proteins, although it remains possible that a subpopulation of TAF-I
could be associated on chromatin (or viral genomes).
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VP22.C1 blocks in vitro TAF-I-dependent nucleosome reconstitution
TAF-I/
has been shown to be a member of a class of proteins involved in chromatin remodelling, reportedly by facilitating nucleosome formation via direct interactions with histones (Matsumoto et al., 1999
; Okuwaki & Nagata, 1998
). Therefore, we performed in vitro nucleosome assembly assays to examine whether VP22.C1 would have any effect on TAF-I
-dependent nucleosome assembly. Core histones (Simon & Felsenfeld, 1979
), the ATP-dependent chromatin remodelling complex HuCHRAC (Poot et al., 2000
) and rTAF-I
(as a histone chaperone) were incubated in the presence of ATP with relaxed plasmid DNA. After incubation, the DNA was digested with micrococcal nuclease, proteins were removed and the DNA was separated on an agarose gel. Preliminary experiments were performed to optimize conditions for nucleosome formation that is maximally dependent on TAF-I
as the histone chaperone. Results shown in Fig. 5
show the ability of TAF-I
to promote the appearance of 150 bp DNA fragments, corresponding to mono-nucleosomal DNA after nuclease digestion (Fig. 5
, compare lanes 1 and 7). When increasing amounts of VP22.C1 were added during the assembly reaction, nucleosome formation was lost progressively until we observed virtually complete inhibition at approximately 1 : 1 to 2 : 1 ratio of the proteins (Fig. 5
, lanes 25). At concentrations of maximum VP22.C1 inhibition (Fig. 5
, lane 5), the addition of extra TAF-I
partially restored mono-nucleosome formation (Fig. 5
, lane 6), showing a direct interdependence with TAF-I
.
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DISCUSSION |
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In this work, we show that the HSV-1 structural protein VP22 associates with a cellular histone chaperone, TAF-I. TAF-I
was shown to bind VP22 both by affinity chromatography of cell extracts on matrices containing bound VP22 and by co-precipitation of VP22 when incubated with purified TAF-I
(or TAF-I
) and immunoprecipitated with anti-TAF-I antibody. We show that interaction with VP22 inhibits the activity of TAF-I
in chromatin assembly, while, conversely, overexpression of TAF-I
suppresses HSV infection in vivo. In contrast to these observed effects, we find that the properties of the TAF-I
/
-containing INHAT complex, which blocks histone acetylation effectively by the acetylases p300/CBP and PCAF, seems unaffected by VP22 in vitro (Fig. 6
). Interestingly, the other main component of the INHAT complex, named pp32/PHAPI (Seo et al., 2002
), is extremely similar to the smallest 28 kDa VP22-binding protein we identified as APRIL/PHAPI2 (Mencinger et al., 1998
), suggesting that what we have identified as VP22-binding proteins may in fact be identical to the INHAT complex. We note that despite the lack of an effect of VP22 on INHAT activity in vitro, others have reported that acetylation of histone H4 is decreased in VP22-expressing cells (Ren et al., 2001
).
In considering the possible relevance of these findings in terms of virus replication, several considerations are noteworthy. VP22 is present in approximately 2000 molecules per virion (Leslie et al., 1996) and although the subcellular location of incoming tegument VP22 has not been reported, Morrison et al. (1998)
have reported that VP22 can be detected in the nucleus early after infection and, indeed, our preliminary studies with large-scale cell biochemical fractionation of infected cells have shown that the majority of the incoming VP22 is located in the nuclear fraction early after infection (unpublished data). In proposing, therefore, that VP22 may be involved in inhibiting nucleosome deposition, two possible, but not mutually exclusive, mechanisms could be envisaged. Assembly could be blocked by VP22 binding to TAF-I
and thus inhibiting TAF-I
binding to and chaperoning histones onto the incoming DNA, or by VP22 binding to viral DNA and subsequently preventing organized nucleosome deposition. In this latter scenario, VP22 DNA binding could itself be blocked by the presence of TAF-I
(Fig. 4
), allowing nucleosomes to access DNA. It has not proved possible to date, either by conventional immunofluorescence or in the context of GFPVP22-expressing recombinant viruses, to visualize incoming VP22 protein adequately enough to examine its association with the incoming genome. The proposal that VP22 may prevent ordered nucleosome deposition on the incoming herpesvirus DNA remains speculative until we develop more sensitive methods for visualization of the incoming particle, but additional approaches such as DNA cross-linking and immunoprecipitation may help answer this question.
We noted upon close examination of the primary amino acid sequence of VP22 that a small conserved part of VP22 has sequence similarity with the C terminus of histone H2A (Fig. 8), which forms a short
-helix and contacts the C-terminal tail of histone H4 in the nucleosome. Interestingly, NAP-1, a close homologue of TAF-I, which also appears to function as a chaperone and facilitates deposition of histones onto DNA (Ishimi & Kikuchi, 1991
; Ishimi et al., 1987
; McQuibban et al., 1998
), has been found to be associated with histone H2A in co-immunoprecipitation analysis (Chang et al., 1997
). Analysis of interactions with deletion mutants of VP22 should help define whether this region is important in the TAF-I interaction. In this context, we also note the recent observation that BHV VP22 associates with histones, as seen in Far-Western assays (Ren et al., 2001
), a result that might explain the direct association of VP22 with chromatin in mitotic cells (Fig. 3
) (Elliott & O'Hare, 2000
).
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ACKNOWLEDGEMENTS |
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Received 30 April 2003;
accepted 3 June 2003.