Introduction
Histone N-termini (tails) undergo diverse post-translational modifications,
including acetylation, phosphorylation, methylation, ubiquitination and
ADP-ribosylation (van Holde,
1988; Wolffe,
1998). The discoveries of enzymes that perform these modifications
and of chromatin-associated proteins that selectively bind to
position-specific histone modifications
(Strahl and Allis, 2000;
Jenuwein and Allis, 2001)
reveals that modified histone N-termini can significantly extend the
information potential of the genetic code. Moreover, they appear to index
chromatin regions, facilitating epigenetic control, lineage commitment and the
overall functional organisation of
chromosomes.⇓
Acetylation (Roth et al.,
2001) and arginine methylation
(Stallcup, 2001) have been
linked mainly with transcriptional stimulation. Phosphorylation
(Cheung et al., 2000a) instead
is a marker for activation of immediate early genes and a signal for mitotic
chromatin condensation. Here, we focus on histone lysine methylation. The
roles of acetylation, phosphorylation and methylation are summarized in
Table 1, and discussion of the
interplay between these distinct modifications can be found elsewhere
(Zhang and Reinberg, 2001;
Berger, 2002;
Kouzarides, 2002).
Table 1.
Histone acetylation, phosphorylation and methylation
The complexity of histone lysine methylation
At least five methylatable lysine positions exist in the N-termini of
histones H3 (K4, K9, K27, K36) and H4 (K20); another occurs in the
histone-fold domain of histone H3 (K79)
(Feng et al., 2002;
Lacoste et al., 2002;
Ng et al., 2002;
van Leeuwen et al., 2002).
For clarity, we focus on H3-K4, H3-K9 and H3-K27 methylation to illustrate the
general principles and complexities involved.
The mammalian Suv39h enzymes and their S. pombe homologue, Clr4,
were the first histone lysine methyltransferases (HMTases) identified
(Rea et al., 2000). The
conserved SET-domain of the Su(var)3-9-related HMTases catalyzes the
methylation of H3-K9, creating a high-affinity binding site for the
chromodomain of heterochromatin protein 1 (HP1) proteins
(Lachner and Jenuwein, 2002).
Other methylatable lysine positions might also be marked by position-specific
SET-domain HMTases for methyl-binding chromodomain proteins. The human and
mouse genomes each encode ≥50 predicted SET-domain proteins
(Kouzarides, 2002) and ≥30
chromodomain-containing sequences (A. Schleiffer and F. Eisenhaber, personal
communication). By contrast, S. pombe has only ∼10 putative SET
domain HMTases, and S. cerevisiae has not more than seven
(Briggs et al., 2001). Lysine
residues are mono-, di- and tri-methylated in vivo
(Paik and Kim, 1971;
van Holde, 1988;
Waterborg, 1993). A
progressive conversion towards tri-methylation could contribute to the
apparent stability of histone lysine methylation and is ideally suited to
imparting additional layers of combinatorial control, which might allow both
short-term and long-term chromatin imprints.
The poster shows the dynamic cycle of histone lysine methylation in
transcriptional stimulation or repression. `Exit routes' from this cycle
reveal more extended reprogramming of the chromatin structure – for
example, during cellular senescence, Polycomb-mediated transcriptional memory,
X chromosome inactivation and constitutive heterochromatin formation. In this
`road map', the various destinations for a chromatin region are indicated by
road signs that reflect distinct methylation positions and states.
Transcriptional regulation – going around with H3-K4 and
H3-K9
In euchromatic regions, binding of transcription factors to specific
promoter/enhancer sequences is the initiating step in altering a naive
chromatin template. If positively acting complexes prevail, promoter-proximal
nucleosomes sequentially adopt an activation-specific modification profile
(Urnov and Wolffe, 2001;
Zhang and Reinberg, 2001;
Berger, 2002;
Daujat et al., 2002). Fully
activated promoters appear to be enriched in tri-methylated H3-K4
(Santos-Rosa et al., 2002);
basal transcription correlates with H3-K4 dimethylation, although the
methylation potential of the HMTases involved needs to be defined
(Briggs et al., 2001;
Nishioka et al., 2002a;
Wang et al., 2001a;
Santos-Rosa et al., 2002).
H3-K9 methylation, by contrast, is present mainly in silenced chromatin
domains (Noma et al., 2001;
Litt et al., 2001), and the
`activated genome' of S. cerevisiae exhibits abundant H3-K4
methylation but lacks apparent H3-K9 di-methylation
(Briggs et al., 2001).
Recruitment of several H3-K9-specific HMTases induces gene repression within
euchromatin (Tachibana et al.,
2001; Nielsen et al.,
2001; Vandel et al.,
2001; Ogawa et al.,
2002; Schultz et al.,
2002; Tachibana et al.,
2002; Yang et al.,
2002). G9a and a closely related enzyme appear to be euchromatic
HMTases that form complexes with HP1γ and a subset of E2F transcription
factors (Ogawa et al., 2002).
These enzymes might, by default, repress target promoters that fail to recruit
additional activating complexes.
In proliferating cells and for G9a-mediated in vivo methylation, the
repressive signal appears to be primarily H3-K9 di-methylation
(Tachibana et al., 2002) (A.
H. Peters, S. Kubicek, L. Perez-Burgos et al., unpublished), although in vitro
G9a methylates both H3-K9 and H3-K27. Differences between H3-K9 di- and
tri-methylation patterns could underpin the more robust association of
inhibitory complexes with the promoters of several cell cycle genes, as cells
enter senescence (S. Lowe, personal communication) or have their growth
potential restricted by the tumor suppressor Rb, which could recruit
additional repressive HMTases (Nielsen et
al., 2001).
For histone lysine methylation, no `direct' demethylase has been described.
Although intermediary enzymes could destabilise the amino-methyl bond by
oxidation or radical attack (Chinenov,
2002; Falnes et al.,
2002; Trewick et al.,
2002), reversion of an engaged chromatin region to a more naive
state might instead be triggered by transcription-coupled histone replacement,
in which the histone H3.3 variant is deposited in place of modified histone H3
(Ahmad and Henikoff, 2002a).
This mechanism does not operate in transcriptionally silent domains, which
might explain turnover of methylated histones in euchromatic regions while
allowing persistence of histone methylation in constitutive heterochromatin
(Ahmad and Henikoff,
2002b).
Polycomb and trithorax – keeping on track with H3-K27 and
H3-K4
During differentiation, `transcriptional memory' maintains the expression
status of certain key regulatory genes over many cell division cycles. This
depends on the antagonistic function of polycomb (Pc-G) and trithorax (trx-G)
group proteins (Orlando and Paro,
1995; Pirrotta,
1998). The Pc-G protein enhancer of zeste [E(z)] contains a SET
domain and becomes an HMTase when complexed with another early-acting Pc-G
protein, extra sex combs (Esc). The Drosophila E(z)-Esc complex
(Czermin et al., 2002;
Müller et al., 2002) and
its mammalian Ezh-Eed counterpart (Cao et
al., 2002; Kuzmichev et al.,
2002) have an apparent preference for H3-K27 but might also target
H3-K9. Ezh/Eed-mediated nucleosome methylation increases in vitro binding of
the chromodomain protein polycomb (PC)
(Czermin et al., 2002;
Kuzmichev et al., 2002). In
E(z) mutants, methylation of H3-K27, and probably also H3-K9, is impaired–
in a manner suggesting that extended H3-K27 di- and tri-methylation
across several nucleosomes (Cao et al.,
2002) or dual tri-methylation of H3-K27 and H3-K9
[(Czermin et al., 2002) R.
Paro, personal communication] might induce stable recruitment of Pc-G
complexes. The E(z) HMTase complex could be developmentally regulated such
that a di-methylating activity prepares histones for a tri-methylating
activity, which propagates transcriptional memory. Fully defining the in vivo
methyl mark(s) involved, however, requires the development of highly specific
H3-K27 and H3-K9 antibodies.
Long-term maintenance of active transcriptional states is regulated by
trx-G proteins. The trx-G proteins Trx/MLL
(Milne et al., 2002;
Nakamura et al., 2002) and
Ash-1 each contain a SET domain and display HMTase activity. Whereas a Trx
complex performs H3-K4 di-methylation
(Czermin et al., 2002;
Milne et al., 2002;
Nakamura et al., 2002), Ash-1
can methylate H3-K4, H3-K9 and probably also H4-K20
(Beisel et al., 2002).
Ash-1-mediated methylation apparently prevents binding of the repressive PC
and HP1 proteins but facilitates association of the Brahma coactivator
(Beisel et al., 2002) –
another trx-G protein and a component of nucleosome-mobilising machines.
Indeed, H3-K4 methylation can trigger recruitment of the Brahma-related ISWI
ATPase (T. Kouzarides, personal communication). Thus, trx-G HMTases may allow
propagation of an activated chromatin state by `neutralising' repressive marks
(e.g. H3-K9 and H4-K20 methylation) (Fang
et al., 2002; Nishioka et al.,
2002b), while simultaneously coupling a positive signal (H3-K4
methylation) with chromatin remodelling.
X-inactivation – choosing an exit with H3-K9 and H3-K27
Dosage compensation in female mammals involves chromosome-wide inactivation
of one X-chromosome (Avner and Heard,
2001). H3-K9 methylation is associated with the inactive X
chromosome (Xi) (Boggs et al.,
2002; Peters et al.,
2002; Heard et al.,
2001; Mermoud et al.,
2002), but H3-K27 tri-methylation might also be a prominent, if
not the major, mark (Silva et al.,
2003; Plath et al.,
2003) (A. H. Peters, S. Kubicek, L. Perez-Burgos et al.,
unpublished). Pronounced H3-K27 tri-methylation at the Xi would be consistent
with the finding that X-inactivation is independent of Suv39h HMTases and does
not require HP1 proteins (Peters et al.,
2002). The HMTases that target the Xi, particularly for random
X-inactivation, are unidentified. A likely candidate for initiating early
methylation imprints is the Ezh-Eed complex, because both Ezh2
(Mak et al., 2002) and Eed
(Wang et al., 2001c)
accumulate at the Xi during imprinted X-inactivation. However, in contrast to
Pc-G-mediated gene silencing, there is no evidence for stable association of
PC or other Pc-G complexes at the Xi
(Silva et al., 2003).
Differences in H3-K27 and H3-K9 methylation could discriminate between
Pc-G-dependent repression (extended H3-K27 di- and tri-methylation or a
combination of H3-K9 tri- and H3-K27 tri-methylation?) and X-inactivation (a
combination of H3-K9 di- and H3-K27 tri-methylation?). Alternatively, the
Xist RNA could provide an additional signal for recruitment of other,
Xi-restricted HMTases and associated silencing complexes. This would be
similar to Xist-dependent accumulation of BRCA1
(Ganesan et al., 2002) and
preclude occupancy by the PC system and HP1 proteins. Subtle differences in
the methylation state of lysine positions might also be associated with
allele-specific imprinting (Xin et al.,
2001; Fournier et al.,
2002; Xin et al.,
2003).
Constitutive heterochromatin – a one-way street to H3-K9
tri-methylation?
Unlike euchromatin, constitutive heterochromatin lacks apparent
transcription units, and instead contains arrays of satellite repeats
(Karpen and Allshire, 1997;
Csink and Henikoff, 1998).
Such repeats appear to give rise – through the RNAi machinery – to
small heterochromatic RNAs (shRNAs)
(Volpe et al., 2002;
Hall et al., 2002;
Partridge et al., 2002;
Mochizuki et al., 2002;
Taverna et al., 2002). These
or other RNAs (Maison et al.,
2002) might pair with the underlying DNA sequences and bind to
chromodomain-like adaptor proteins (Akhtar
et al., 2000a) that could recruit Su(var)3-9-related HMTases
(Jenuwein, 2002). The H3-K9
methylation signal would then be stabilised and propagated by `interlocking'
HP1 molecules to form an extended heterochromatic domain
(Nakayama et al., 2001;
Hall et al., 2002).
Furthermore, H3-K9 methylation can trigger DNA methylation in Neurospora
crassa (Tamaru and Selker,
2001) and Arabidopsis thaliana
(Jackson et al., 2002), and a
similar pathway directs DNA methylation at pericentric satellite repeats in
mammals (B. Lehnertz, Y. Ueda, A. A. Derijck et al., unpublished). The
combination of histone- and DNA-methylation systems
(Fahrner et al., 2002;
Nguyen et al., 2002;
Fuks et al., 2003) probably
stabilises silent chromatin domains, safe-guarding gene expression programmes
and protecting genome integrity.
Pericentric heterochromatin is enriched in tri-methylated H3-K9. This
profile is selectively abolished upon disruption of Suv39h HMTases, whereas
centromeric regions display Suv39h-independent H3-K9 di-methylation (A. H.
Peters, S. Kubicek, L. Perez-Burgos et al., unpublished). Interestingly, in
Suv39h dn cells, pericentric heterochromatin exhibits significant H3-K9
mono-methylation (A. H. Peters, S. Kubicek, L. Perez-Burgos et al.,
unpublished). Suv39h HMTases are thus tri-methylating enzymes that can convert
intermediary methylation states (mono- or di-methylation) into the apparently
more stable tri-methylation end state. Regional H3-K9 tri-methylation at
transcriptionally inert chromatin domains therefore appears to be a robust
hallmark of constitutive heterochromatin.
Outlook
The above examples highlight the exquisite complexity and coding potential
of histone lysine methylation in epigenetic control. Position- and
state-specific methylation antibodies
(Santos-Rosa et al., 2002) (A.
H. Peters, S. Kubicek, L. Perez-Burgos et al., unpublished) and the solved
3D-structures of several SET domain enzymes
(Trievel et al., 2002;
Wilson et al., 2002;
Zhang et al., 2002;
Jacobs et al., 2002;
Min et al., 2002) have started
to reveal the functions of mono- (SET7/9;
Xiao et al., 2003), di- [G9a
(Tachibana et al., 2002) (A.
H. Peters, S. Kubicek, L. Perez-Burgos et al., unpublished)] and
tri-methylating HMTases [Suv39h (A. H. Peters, S. Kubicek, L. Perez-Burgos et
al., unpublished)]. Although the `rules of the road' highlighted in this
poster focused on basic mechanisms of transcriptional regulation and
chromosome organisation, histone lysine methylation probably affects most
chromatin-templated processes – from cell proliferation and
tumorigenesis (Varambally et al.,
2002) to imprinting, X-inactivation, lineage commitment
(Su et al., 2003), aging,
stem cell plasticity and the epigenetic reprogramming of the genome.
Acknowledgments
We thank David Allis, Renato Paro, Tony Kouzarides, Neil Brockdorff, Steven
Gamblin and Scott Lowe for helpful discussions and for allowing us to cite
work prior to its publication. Research in T.J.'s laboratory is supported by
the IMP through Boehringer Ingelheim and by funds from the Vienna Economy
Promotion Fund (WWFF), an EU-network grant and the Austrian GEN-AU
initiative.
- © The Company of Biologists Limited
2003
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