Post-Transcriptional Control: mRNA Translation, Localization and Turnover
Are ribosomal proteins present at transcription
sites on or off ribosomal subunits?
Sandip De and Saverio Brogna1
University of Birmingham, School of Biosciences, Edgbaston, Birmingham B15 2TT, U.K.
Abstract
RPs (ribosomal proteins) are main components of the ribosome having essential functions in its biogenesis,
function and structural integrity. Although most of the RP molecules are in the cytoplasm, being incorporated
into translating ribosomes, some RPs have non-ribosomal functions when they are off ribosomal subunits.
Notably, in eukaryotes, RPs are also present at transcription sites and some of these proteins have a
function in transcription and pre-mRNA processing of specific genes. Although the consensus is that the
proteins found at these sites are isolated RPs not assembled into ribosomal subunits, it has been proposed
that ribosomal subunits might also be present. In the present paper, we review the available evidence for
RPs at transcription sites and conclude that ribosomal subunits might be present, but additional studies will
be required to solve this important issue.
Ribosomal functions of RPs (ribosomal
proteins)
Although rRNA contributes mostly to the structure and
function of the ribosome, RPs are also important for viability
in all cell types. RPs are mostly located on the surface
of the ribosome, typically they contain an exposed Nterminal globular domain and a long C-terminal domain
extending inwards to the rRNA [1–4]. RPs shape the
rRNA into the correct tertiary structure and have essential
functions in translation [5,6]. A second important function
of RPs is in ribosome biogenesis, where they have specific
roles in rRNA maturation, export and ribosomal subunit
biogenesis [7–11]. RPs are some of the most abundant
proteins in both prokaryote and eukaryotic cells and they are
typically present stoichiometrically in the ribosome. These
proteins are evolutionarily well conserved: approx. 30% of
Escherichia coli RPs have orthologues in higher eukaryotes
and archaea; archaeal ribosomes have an additional 30%
RPs in common with eukaryotes [12,13]. Most RP genes
in Saccharomyces cerevisiae and Schizosaccharomyces pombe
are duplicated; the protein paralogues are either identical
or very similar, yet deletions on the two paralogues have
different phenotypes in S. cerevisiae [14]. It has been
suggested that there are different ribosome subtypes in
the cell, distinguishable by the RP paralogues they carry
[14]. An alternative explanation for the different phenotypes
is that one of the RP paralogues might have evolved a
specific extra ribosomal function. In Drosophila and other
multicellular organisms, heterozygous mutations in RP genes
often lead to developmental irregularities [15,16]. Although
these phenotypes can be explained by an insufficient level
Key words: ribosomal protein, ribosome, splicing, transcription, translation.
Abbreviations used: DFC, dense fibrillar component; Nus, N-utilization substance; RP, ribosomal
protein; UTR, untranslated region.
1
To whom correspondence should be addressed (email [email protected]).
Biochem. Soc. Trans. (2010) 38, 1543–1547; doi:10.1042/BST0381543
of ribosomes, in some instances they might also be due to
extraribosomal functions [17–19].
In eukaryotes, newly synthesized RPs are rapidly imported
into the nucleus and incorporated into pre-ribosomal
subunits at the nucleolus, where they bind to the rRNA
co-transcriptionally [20]. The nucleolus is divided into three
morphologically distinct subcompartments: transcription,
early processing and rRNA modifications occur within the
innermost FC (fibrillar component) and the surrounding
DFC (dense fibrillar component), and RPs bind the rRNA
either in the DFC or in the outer GC (granular component)
layer [21,22]. A previous study shows that RPs accumulate
in the nucleolus much more rapidly than other nucleolar
proteins [23]. However, the rate at which RPs are imported in
the nucleus is higher than the rate at which they are exported
back to the cytoplasm (presumably as ribosomal subunits)
[23]; it appears that a large fraction of RPs is destroyed by the
proteasome in the nucleus [23]. Yet some RPs must escape
degradation because many RPs are found to be associated
with pre-mRNAs and proteins in the nucleus.
Non-ribosomal functions of RPs
Besides their main role in ribosome function and biogenesis,
extraribosomal functions for RPs have been reported across
organisms, from prokaryotes to eukaryotes [17–19]. There are
several reports of RPs that bind their own mRNAs or premRNAs and negatively autoregulate their own expression
by affecting translation, splicing or transcription [17–19].
For example, RpS13 in mammalian cells represses its own
gene expression by inhibiting splicing; RpS13 binds its own
pre-mRNA close to the splice sites of the first intron
and probably prevents spliceosome assembly (Figure 1,
upper left panel) [24]. Similar regulatory mechanisms have
been reported for other RPs in both humans and yeast
[25–28]. Notably, in mammalian cells, there is also evidence
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Figure 1 RPs function at transcription sites
Upper left panel: free RpS13, off subunit, binds to splice sites of its own pre-mRNA and inhibits splicing. Upper right panel:
RpS13 binds the splice sites while associated with the ribosomal subunit, possibly pre-40S subunit. Lower left panel: free
RpL11, off subunit, interacts with c-Myc and represses transcription. Lower right panel: RpL11 interacts with c-Myc while still
associated with a complex, either as part of the 5S rRNA complex or as a pre-60S particle. Pol II, RNA polymerase II.
of RPs that regulate genes other than their own, by
binding directly to specific transcription factors. RpL11, for
instance, associates with a defined domain of the oncoprotein
c-Myc and inhibits transcription activation of c-Myc target
genes (Figure 1, lower left panel); the effect appears to
be specific for RpL11 since other RPs did not show
similar activities [29,30]. Similarly, it has also been reported
that RpS3 specifically associates with the NF-κB (nuclear
factor κB) DNA-binding protein complex and stabilizes the
association of this transcription factor to its target sites [31].
Interestingly, RpS3 functions also as a DNA glycosylase and
interacts with OGG1 (8-oxoguanine DNA glycosylase 1), an
enzyme involved in oxidative-stress-associated DNA repair
[32–35]. In summary, there is abundant evidence for RPs
not assembled into ribosomes having additional functions
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Authors Journal compilation unrelated to the role of the ribosome in translation. In the
present paper, we focus on examples of RPs with additional
functions in the nucleus; however, there are also reports of
RPs which bind mRNAs and affect translation. Classical
demonstrations of extraribosomal functions in translation
are RPs that bind specific RNA structures in the 5 -UTR
(untranslated region) and suppress their own translation.
This mechanism is widespread in E. coli, but there are also
examples in eukaryotes. These repressor functions create
negative-regulatory loops that synchronize synthesis of RPs
with that of rRNA, preventing accumulation of free RPs in
the cell [36]. In prokaryotes, the RNA structure in the
5 -UTR typically resembles that of the rRNA domain that
the RP binds on the ribosome [37,38]. Another welldocumented case of an RP functioning as a translation
Post-Transcriptional Control: mRNA Translation, Localization and Turnover
repressor is RpL13a; in human cells during inflammation,
RpL13a is phosphorylated at a specific residue and released
from the ribosome, and as a free protein is incorporated into
a complex that binds the mRNA 3 -UTR of inflammatory
genes and represses translation [39,40].
Figure 2 RpS30 associates with transcription sites
Indirect immunofluorescence of RpS30. (A) Single-channel showing the
typical banding pattern produced by anti-RpS30 detected with a Cy3
(indocarbocyanine)-labelled secondary antibody. (B) Same chromosome
squash as above, showing the DAPI (4 ,6-diamidino-2-phenylindole)
signal (blue) to visualize DNA; note that the Cy3 signal (red)
highlights a decondensed region of the chromosomes (interbands),
which correspond to transcription sites.
Are ribosomal subunits present at
chromosomal sites?
As described above, the current understanding is that free
proteins not assembled into ribosomal subunits mediate
extraribosomal functions of RPs in the nucleus. RPs are often
found together in biochemical preparations of complexes
involved in transcription and pre-mRNA processing [41–
43]; however, the presence of RPs in these complexes is
typically dismissed as a contamination with proteins that
associate after cell lysis [41]. The observation that the full
complement of 40S or 60S RPs is never found in these
complexes also suggests that the RPs are contaminants. The
caveat of this argument is that RPs or whole complexes might
have been lost during the purification. For instance, in the
study referred to above [29], RpL11, but not other RPs,
associates with c-Myc. While finding only RpL11 is a strong
argument for the interaction with c-Myc being specific, it is
still possible that RpL11 was recruited to c-Myc as a complex
rather than as an individual protein (Figure 1, lower right
panel). Most of the RpL11 in the cell is probably bound
to 5S rRNA together with RpL5; most of the 5S rRNA is
probably associated with the 60 S subunits, but a substantial
fraction is not and might have a non-ribosomal function [44].
Several factors may have released RpL11 from the 5S rRNA
during the biochemical purification procedure. For example,
the solutions used by Dai et al. [29] contained EDTA, which
is known to disassociate the ribosome and release RPs from
the subunits; in particular, addition of EDTA readily releases
the 5S rRNA and associated proteins from the 60S subunits
[44,45]. Using a similar argument, we could speculate that
RpS13 is recruited to the splice sites as part of the 40 S subunit,
but the rest of the subunit and associated RPs are lost during
the purification (Figure 1, upper right panel) [24].
It has also been reported that at least 20 RPs and
rRNA are present at many transcription sites in Drosophila
melanogaster polytene chromosomes; the kinetics of the
recruitment to the transcription site and RNA sensitivity
suggested that the RPs are associated with nascent Pol II
(RNA polymerase II) transcripts [46]; Figure 2 shows
polytene chromosomes immunostained for RpS30. This
study demonstrates that RPs are present at most transcription
sites; in addition, the concurrent presence of many RPs and
rRNA seems to be a good indication that these proteins are
probably recruited as components of ribosomal subunits. Yet
it has been speculated that some of the antibodies used in
the polytene study are not sufficiently specific and might
cross-react with common components of transcription sites
[47]. Although some of the antibodies recognized multiple
bands on Western blot of whole-protein extracts, our view
is that it is unlikely that the 20 antibodies could produce a
similar polytene banding pattern by non-specific binding. In
a later study, it was reported that RpS7b, RpL7b, RpL26a
and RpL34b associate with genes also in S. cerevisiae [48].
Although this finding confirms that RPs are present at
transcription sites also in budding yeast, Schroder and Moore
[48] found that the RPs associate both to coding and noncoding genes and it was concluded that the association is
probably with free proteins rather than ribosomal subunits.
Many studies clearly demonstrate that RPs are present
at transcription sites and have important functions in
transcription and RNA processing. The association of RPs
with transcription sites is probably a general cellular feature;
an important issue is whether these proteins are recruited to
transcription sites as individual RPs or ribosomal subunits,
as indicated by the polytene study [46]. The consensus is
that the extraribosomal functions are always mediated by
free RPs; however, future studies might change this view.
For example, in E. coli, the RP S10 is a classic example of a
protein moonlighting. During lytic growth of bacteriophage
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λ on E. coli, the λ N gene product modifies host RNA
polymerase molecules that are transcribing certain λ genes
so they cannot be prematurely terminated by the host. To do
this, N protein forms a complex with several host proteins,
known as Nus (N-utilization substance) factors, and one
of these is the free S10 RP (also known as NusE) [17,49].
Another of these Nus factors is NusG, a well-characterized
bacterial transcription elongation factor, which forms a
bridge between NusE and transcribing RNA polymerase
[50]. Interestingly, in non-infected E. coli, NusG associates
with most elongating RNA polymerase molecules [51] and
appears to contact the NusE (S10) protein in the small subunit
of the first ribosome that loads on the nascent transcript
[50]. This interaction thus couples bacterial transcription to
translation, and this is critical for minimizing transcriptional
polarity and counteracting RNA polymerase pausing [52].
In summary, similarly to S10 in E. coli, it might be that in
eukaryotes, individual RPs can affect transcription on and
off the ribosome, depending on the specific gene. Ribosomal
subunits are clearly present in the nucleus; they are assembled
in the nucleolus during ribosome biogenesis [53]. Although
these ribosomal subunits might not be able to join together
to form translation competent 80S ribosomes before
export to the cytoplasm, they can still have a nuclear function;
this perhaps is independent of translation and it could only
be that of tethering RPs which have non-ribosomal roles
in transcription or pre-mRNA processing of specific genes.
Future studies should investigate these important open issues.
Acknowledgements
We thank Steve Busby for critically reading the paper.
Funding
S.D. is supported by a Darwin Trust scholarship and S.B. is supported
by a Royal Society University Research Fellowship.
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Received 7 June 2010
doi:10.1042/BST0381543
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