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From the
DNA helicases are a class of enzymes able to
unwind the two complementary DNA strands in a reaction dependent on
energy derived from nucleoside 5'-triphosphate hydrolysis. Their action
is required in fundamental cellular processes such as DNA replication,
repair, recombination, and transcription. From the known crystal
structures it appears that the enzymatic machinery of DNA helicases has
been highly conserved; nevertheless their functions can be
distinguished by co-factor utilization, substrate preference,
directionality of unwinding, processivity, and interaction with other
proteins. These aspects of DNA helicase biochemistry have recently been reviewed (1-4). Unrepaired DNA lesions can affect the outcome of DNA
replication, repair, recombination, and transcription. Thus, because
DNA helicases are among the first proteins that would encounter DNA
damage during these processes, a complete understanding of the
metabolism of damaged DNA requires a biochemical analysis of the
interaction between helicases and lesions. Clearly, chemical or
physical cross-links between opposite DNA strands (interstrand lesions)
will represent a mechanical block to DNA helicase action. However,
in vivo the functions of DNA helicases are also expected to
be severely impaired by bulky, helix-distorting intrastrand DNA lesions
like those produced by ultraviolet irradiation or by chemical agents
such as cisplatin, acetylaminofluorene, and benzopyrene. (For a general
description of DNA lesions, see Ref. 5.). Although helicases unwind
duplex DNA, most known helicases associate and translocate
unidirectionally along one strand of the DNA. Accordingly, except for
interstrand lesions, the position of a lesion may differentially
influence the action of a DNA helicase, depending on whether it is
located on the DNA strand along which the enzyme translocates or on the
opposite one.
In this minireview we will focus mainly on in vitro studies
aimed at investigating the effects of helix-distorting DNA lesions on
the action of DNA helicases implicated in DNA repair, recombination, and replication; the possible biological consequences of these interactions will also be discussed. To facilitate organization of this
review, helicases have been categorized depending on whether they
function in repair, recombination, or replication. However, the reader
should be aware that there is substantial overlap between these processes.
To overcome the deleterious effects of DNA lesions, a variety of
DNA repair systems is present in all living organisms (5). Nucleotide
excision repair (NER)1 is one
of the most versatile systems and shows remarkable similarities in both prokaryotes and eukaryotes (for review see Refs. 6 and 7).
Among the six proteins necessary for NER in Escherichia coli, the UvrA2B protein complex and the UvrD protein
have been shown to possess DNA helicase activities. The 5' to 3'
helicase activity of UvrA2B is thought to allow limited
ATP-dependent scanning of DNA to detect damaged bases. For
example, UV-induced lesions have been shown to inhibit translocation of
UvrA2B, suggesting that arrest of the helicase may be a
signal for repair (8). Subsequently, a preincision complex is formed,
and incision occurs on both sides of the lesion. UvrD then loads onto
the free 3' end of the damaged oligonucleotide and displaces it using
its intrinsic 3' to 5' helicase activity (6). The recent determination of the crystal structure of UvrB suggests that formation of the preincision complex requires unwinding of the DNA by UvrA2B
(9). It was postulated that stalling of the UvrA2B complex
upon encountering a lesion triggers dissociation of the complex. In
another study (10), it was found that the presence of the
2-(acetylamino)fluorene lesion in either DNA strand stimulated the
activity of UvrA2B, leading the authors to suggest that the
strand-separating activity of UvrA2B may not play a major
role in lesion recognition.
The function of UvrD helicase (helicase II) in E. coli NER
is in the excision of damage-containing oligonucleotides. The helicase activity of UvrD was found to be only moderately sensitive to ultraviolet radiation damage and intrastrand cisplatin adducts, whereas
it was exquisitively sensitive to intercalators that position in the
major groove of DNA (11, 12). However, in one study (11) but not in the
other (12), UvrD helicase action was found to be affected by distamycin
A, an intercalator binding to the minor grove of DNA. Generally
speaking, it is possible that UV-induced lesions or other
helix-distorting intrastrand adducts are better tolerated by DNA
helicases than those produced by intercalating agents, which can either
totally disrupt the continuity of what a helicase normally recognizes
or increase the thermodynamic stability of the DNA duplex in such a way
that it resists helicase action (13). In the same study (11), the
activity of UvrD helicase on damaged DNA was compared with the product
of the yeast Saccharomyces cerevisiae rad3
gene, a helicase that is absolutely required for yeast NER. The
5' to 3' helicase activity of the Rad3 protein was found to be
profoundly inhibited by UV damage and intrastrand cisplatin adducts
located on the strand along which the enzyme translocates, whereas
lesions on the opposite strand had no effect. Blockage of Rad3 by a
lesion results in the formation of an abnormally stable protein-DNA
complex (14). These results indicate that the DNA helicase activity of
Rad3 protein may have been adopted by the yeast NER machinery to locate
and determine the strand specificity of DNA damage, thus establishing
some functional relationship with E. coli
UvrA2B. It has long been known that the
recognition-incision step of NER in human cells requires ATP (15), and
the recent reconstitution of NER with recombinant human proteins now
provides an interesting tool to study the role of the different factors involved in this process (16). Eukaryotic TFIIH is a multisubunit protein complex involved in RNA polymerase II transcription and nucleotide excision repair, which contains two demonstrated DNA helicases, named Rad3 and Rad25 in yeast and XPB and XPD in mammals (17). Interestingly, TFIIH containing a mutant XPD with impaired DNA
helicase activity was shown to be defective in incisions around the
lesion (18). Consistent with the role of the yeast homologue of XPD,
Rad3, these results support previous models that suggest a role for the
DNA helicases of TFIIH in the identification of the damaged strand and
the correct localization of the incisions (6, 19). The strand-specific
stalling of either the 5' to 3' XPD helicase or the 3' to 5' XPB
helicase could result in the distortion of the DNA-TFIIH complex,
leading to the identification of the damaged strand and to the
formation of a fully opened preincision complex. A schematic
representation of the putative roles of complexes containing
prokaryotic UvrA2B and eukaryotic TFIIH in DNA damage recognition is presented in Fig. 1.
Calf thymus DNA helicase E is a moderately processive 3' to 5' helicase
active on nicked DNA that has been proposed to play a role in DNA
repair (20). In vitro, helicase E can displace a primer
containing an internal GpG intrastrand cross-link, the major DNA lesion
generated by the antitumor drug cisplatin (Pt-d(GpG)). If the lesion
was placed on the strand to which it binds, helicase E was inhibited
only if the adduct was in the single strand part of the template but
not if it was within the annealed region, suggesting that, in the
latter case, it did not represent an absolute stop to helicase
progression (21). Subsequent work has shown that a protein which
recognizes and binds cisplatin-damaged DNA, the high mobility group 1 protein (HMG-1), reduced DNA unwinding of a platinated substrate by
helicase E (22). HMG-1 protein has also been reported to inhibit NER of
cisplatin lesions catalyzed by either cell extract or purified proteins
by shielding the lesions from repair proteins (23).
DNA recombination assures exchange of information between DNA
chains and contributes to the repair of DNA damage and to restart DNA
replication (for review see Refs. 24-26). Double strand DNA break
repair by homologous recombination in E. coli is initiated by the RecBCD enzyme, which unwinds and simultaneously degrades DNA
from a double-stranded DNA end (27). Early studies on RecBCD enzyme
showed that the enzyme could translocate through DNA duplexes that
contain UV adducts, although, as expected, progression of the enzyme
was arrested by interstrand lesions (28). Of the three subunits, RecB
is the sole one that possesses 3' to 5' helicase activity (29). The
effect of a Pt-d(GpG) adduct, in the context of partially duplex
synthetic oligonucleotides, on the helicase activity of RecB was
examined in vitro. Both strand-separating and
DNA-dependent ATPase activities of the RecB protein were
inhibited by the adduct when located on the template strand (30).
Although further studies are required, these results suggest that
subunit interactions within RecBCD enzyme allow the enzyme to traverse regions of DNA damage whereas RecB alone is inhibited. Another protein
that plays a key role in recombination in E. coli is RecA protein (24). RecA catalyzes DNA strand exchange in vitro
and has been shown to possess ATP-dependent DNA unwinding
activity that is limited to the unwinding of short duplexes (31). The capacity of RecA to unwind a damaged template identical to the one used
for the RecB helicase was examined in the same study. Contrary to RecB,
it was found that neither the strand-separating nor the ATPase
activities of RecA were inhibited by the Pt-d(GpG) adduct (30).
Previous work had shown that RecA protein was able to bypass UV
pyrimidine dimers during strand exchange in vitro (32). Ku
autoantigen is a DNA end binding protein that has been shown to act as
a regulator of a DNA-dependent protein kinase (DNA-PK),
which plays essential roles in DNA repair and recombination (for review
see Ref. 33). Ku protein has been identified as human DNA helicase II
(HDH II), an enzyme that preferentially unwinds partially duplex DNA
proceeding in the 3' to 5' direction (34). It was found that
intercalating agents such as actinomycin, daunorubicin, or nogalamycin
severely inhibited the unwinding activity of the HDH II/Ku enzyme
(35).
The familiar structure of a replication fork, a site where the two
strands of a duplex DNA are separated to reveal the single strands of
opposite polarity, is generated through the action of replicative DNA
helicases (36). In eukaryotes, although many helicases have been
characterized biochemically, their precise roles in vivo
remain difficult to establish. Thus, despite the existence of several
candidates, no eukaryotic DNA helicase has yet been unambiguously shown
to be essential for the progression of the replication fork during
chromosomal replication (37-39). Such is not the case for bacteria and
related phages or for eukaryotic viruses, where replicative DNA
helicases have been identified and characterized (40). T7 gene 4 protein acts both as a primase and a helicase. The gene 4 protein has
been shown to translocate along single-stranded DNA in the 5' to 3'
direction, and this movement was found to be arrested in
vitro by bulky DNA adducts formed by the chemical carcinogen
benzo[a]pyrene. The inhibitory effects of these adducts
are strand-specific in that they blocked the DNA helicase activity of
gene 4 protein only if they are located on the strand along which the
helicase translocates. In addition, the data presented indicate that
gene 4 protein was sequestered at the site of the adduct (41, 42). In
Herpes simplex virus type 1 (HSV-1) DNA replication, two
helicases are required for viral origin-specific DNA replication (43).
The first of the two helicases is the product of the UL9 gene, a 3'-5'
helicase that together with the viral single-stranded DNA binding
protein, ICP8, can specifically unwind the HSV-1 origins of replication (44). It was found that a Pt-d(GpG) adduct significantly reduced, but
did not abolish, the helicase activity of the UL9 protein but only when
it was present on the strand along which the protein translocated (45).
However, addition of ICP8 greatly stimulated the capacity of the
helicase to unwind platinated DNA. Furthermore, the stimulation
appeared to be the result of the functional and physical interaction
that is known to exist between UL9 and ICP8 and not because of a
preferential binding of ICP8 at the site of the adduct. Results from a
subsequent study showed that ICP8 stimulated the DNA helicase activity
of UL9 protein by increasing its processivity, thus facilitating its
translocation along DNA and through regions of secondary structure
(46). Based on the finding of this study it is tempting to speculate
that ICP8 enables the UL9 protein to bypass the cisplatin Pt-d(GpG)
lesion by tethering it to the DNA substrate, thereby preventing its
dissociation. The second HSV-1 replicative DNA helicase is the product
of the UL5, UL8, and UL52 genes. This heterotrimeric 5' to 3' helicase is also endowed with DNA-primase activity and is responsible for concomitant DNA unwinding and primer synthesis at the viral replication fork (44).
Addition of ICP8 specifically stimulated unwinding of platinated DNA by
the helicase-primase, but at variance to what was found for UL9,
stimulation by ICP8 appeared to enable bypass of the cisplatin
intrastrand cross-link by recruiting the enzyme to the DNA rather than
by increasing its processivity (47). Thus, these studies (45, 47)
suggest that specific protein-protein interactions between a
single-stranded DNA binding protein and two replicative DNA helicases
allow substantial unwinding of substrates containing a bulky
intrastrand DNA lesion.
In the case of simian virus 40 (SV40), the only viral protein required
for viral replication is large T antigen. This protein has an intrinsic
3' to 5' DNA helicase activity and binds specifically to the origin,
allowing it to initiate replication and functions as the replicative
helicase at the fork (48). The impact of intrastrand DNA lesions on the
unwinding activity of SV40 T antigen protein was recently examined
in vitro (49). Using synthetic forklike substrates
containing either single UV photoproducts or a specific
2-(acetylamino)fluorene adduct, it was shown that T antigen helicase
activity was not affected by the presence of the lesions on either the
strand on which the enzyme translocates or on the opposite one. The
capacity of T antigen to displace UV-irradiated DNA was also observed
in a previous work (50). However, T antigen helicase was found to be
blocked by DNA-intercalating drugs in vitro (51).
In general, intrastrand DNA lesions seem to affect DNA helicase
activity in vitro only when placed on the strand to which the protein translocates. Many of the DNA helicases mentioned here act
as multimers (52). Replicative helicases in particular appear to exist
as hexameric rings. A model for hexameric helicase action has been
proposed where one strand of the DNA passes through the central channel
of the helicase while the second strand is displaced outside the ring
(53). This model is consistent with the observed strand specificity if
one assumes that any bulky DNA lesion will have an inhibitory role when
placed on the strand encircled by the helicase and no effect on the
strand outside the ring, as recently suggested (54). However, in
apparent contradiction of this view, the unwinding activity of proteins
capable of forming oligomeric structures, such as SV40 T antigen or
RecA, does not appear to be impaired in vitro by intrastrand
DNA lesions on either strand (30, 49). Perhaps the capacity of these
proteins to oligomerize into large complexes can contribute to their
ability to unwind past a lesion. HSV-1 UL9 helicase, whose action has been shown to be impeded but not blocked by a cisplatin lesion (45),
may also belong to this category. Indeed, UL9 helicase action appears
to be stoichiometric, requiring a DNA-dependent assembly of
multimeric UL9 protein complex (43). The molecular mechanism(s) leading
to DNA helicase inhibition by bulky DNA lesions have been investigated
in some instances. It was found that S. cerevisiae Rad3 and
T7 gene 4 helicases were sequestered on single-stranded DNA at the
sites of damage, forming stable protein-DNA complexes (14, 41), whereas
calf thymus DNA helicase E was not (21). Whether or not these distinct
in vitro characteristics are the reflection of different
roles played by enzymes in vivo remains to be seen. HSV-1
ICP8 has been shown to interact with the HSV-1 UL9 helicase and with
the UL8 subunit of the HSV-1 UL5/52/8 helicase-primase (43). ICP8 was
found to specifically stimulate unwinding of platinated DNA substrates
by both helicases, although the mechanisms of stimulation appear to be
different for the two enzymes (45, 47). The effect of ICP8 appeared to
be the result of its interaction with the helicases and not a
consequence of its preferential binding to the cisplatin adduct
Pt-d(GpG). On the contrary, addition of the HMG-1 protein, which
strongly binds the Pt-d(GpG) adducts, was found to inhibit the activity
of calf thymus helicase E (22). These data point out how the
interaction of helicases with damaged DNA can be modulated by other proteins.
Many DNA helicases are active in the cell, and their wide range of
functions probably explains why organisms have so many helicase genes
(55). The molecular mechanism governing the interaction of a given DNA
helicase with damaged DNA may be dictated, at least in part, by its
cellular functions. For instance, DNA helicases implicated in the
initial steps of NER have been proposed to check DNA for the presence
of repairable DNA lesions and might be expected to be exquisitely
sensitive to DNA damage whereas DNA helicases involved in the
subsequent removal of the damaged DNA could be less affected. In
vitro studies with UvrA2B, Rad3, or XPD helicases on
one hand and UvrD helicase on the other hand roughly support this view.
The sensitivity of various DNA helicases to DNA-damaging agents may
also be influenced by their mechanism of translocation along DNA. For
instance, it was recently shown that the RecBC DNA helicase is able to
"step across" single-stranded DNA gaps, enabling it to unwind
nicked or gapped duplexes (56). However, bulky intrastrand DNA lesions
can still inhibit RecB activity (30).
Specific protein-protein interactions have been demonstrated for DNA
helicases involved in DNA replication. Examples include: interactions of SV40 T antigen helicase with the eukaryotic
single-stranded binding protein RP-A and DNA polymerase Current models dealing with replication of damaged DNA postulate the
initial dissociation of replicative DNA polymerases when encountering
sites of DNA damage. Replication can then restart beyond lesions, or
DNA polymerases specialized in translesion synthesis (TLS) can
temporarily replace replicative polymerases to synthesize across the
lesion; replicative enzymes will then take over again (for review see
Refs. 61-63, and references therein).
On the other hand, if interactions between components of the replisome
are maintained, the bypass capacity of a helicase may drive some TLS by
the replicative polymerases, possibly by increasing their dwell time at
the lesion and/or by modifying the conformation of their active sites.
Fig. 2 gives a simplified view of some of
the possible molecular events following the interaction between a
complex formed by a 5' to 3' DNA helicase, a replicative DNA polymerase, and a single-stranded binding protein with the site of DNA
damage located at the replication fork. However, it should be stressed
that the helicase-mediated bypass hypothesis remains purely speculative
at the present time.
MINIREVIEW
Interactions of DNA Helicases with Damaged DNA: Possible
Biological Consequences*
§ and¶
Institut de Pharmacologie et de Biologie
Structurale, CNRS, 205 route de Narbonne 31077 Toulouse Cedex, France
and ¶ Department of Biochemistry and Molecular Biology, University
of Miami School of Medicine, Miami, Florida 33101-6219
INTRODUCTION
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INTRODUCTION
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Effects of DNA Lesions on DNA Helicases Involved in DNA
Repair
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View larger version (14K):
[in a new window]
Fig. 1.
Hypothetical roles for DNA helicases
associated with NER complexes of prokaryotes (A) or
eukaryotes (B) in DNA damage recognition. In
B only the interaction of the 5' to 3' helicase with a
lesion is shown. This representation is derived from models previously
presented in Refs. 6 and 17, respectively. See text for further
details. Gray triangle, intrastrand DNA lesion; red
oval, UvrA; blue oval, UvrB; small yellow and
orange spheres on large green sphere, TFIII (both 3' to 5'
(orange sphere) and 5' to 3' (yellow sphere)
helicases are represented).
Effects of DNA Lesions on DNA Helicases Involved in DNA
Recombination
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Effects of DNA Lesions on DNA Helicases Involved in DNA
Replication
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Tentative Conclusions from in Vitro Studies
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Possible Biological Consequences of the Interaction of DNA
Helicases with Damaged DNA
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(57); HSV-1
helicase-primase with HSV-1 single-stranded binding protein ICP8 and
HSV-1 DNA polymerase UL30/42 complex (43); T7 gene 4 helicase-primase with T7 single- stranded binding protein and T7 DNA polymerase (58);
E. coli DnaB helicase with E. coli DNA polymerase
III (59). In the latter case contact between DnaB and DNA polymerase increases the unwinding rate more than 10-fold (59) and imparts increased processivity to the leading strand polymerase of the DNA
polymerase III holoenzyme dimer (60). When a DNA lesion is encountered
during replication, the helicase will be at the forefront of the
replication complex, and its initial interaction with the damage may
influence the behavior of the DNA polymerase it contacts. Therefore, a
stalled helicase could lead to the stalling of the whole replication
complex whereas its capacity to unwind DNA past a lesion could promote
replication bypass.
View larger version (20K):
[in a new window]
Fig. 2.
Possible consequences of the interaction of a
DNA helicase/DNA polymerase/single-stranded DNA binding protein complex
with a site of damage at the replication fork. Only interactions
with a lesion positioned on the leading strand template are
represented. For simplicity, the subsequent replacement of the TLS
polymerase by the replicative polymerase following TLS
polymerase-mediated bypass is not represented. See text for
further explanations. Inverted gray triangle, intrastrand
DNA lesion; red sphere cluster, 5' to 3' hexameric DNA
helicase; yellow oval, SSB protein; blue oval,
replicative DNA polymerase; green sphere, specialized TLS
DNA polymerase; dashed arrow, direction of
replication.
A further example of the potential importance of protein-protein interactions affecting a DNA helicase activity is given in the case of Werner's syndrome. The Werner's syndrome (WRN) gene encodes a polypeptide containing domains homologous to the RecQ family of DNA helicases, and mutations in these genes result in genomic instability and premature aging disorders (for review see Refs. 3 and 64). WRN protein (WRNp) has been purified and shown to possess a 3' to 5' helicase activity (65). In vitro, WRN helicase activity requires a 3' single-stranded tail, and its capacity to unwind small stretches of DNA is greatly stimulated by the single-stranded DNA binding protein RP-A (66, 67). In addition to the capacity to unwind DNA, WRNp also possesses a 3'- to 5'-exonuclease activity (68, 69). Several lines of evidence suggest that WRNp could play a role in DNA replication. (i) Werner cells exhibit a reduced rate of DNA replication and a prolonged S phase; (ii) a Xenopus laevis WRN homologue, FFA-1, has been shown to be present in replication foci (39); and (iii) WRNp copurifies with DNA replication complex and interacts with proliferating cellular antigen, RP-A, and topoisomerase I (67, 70). Furthermore, a role for WRNp in DNA repair is also likely because (i) Werner's syndrome cells are sensitive to 4-nitroquinoline-1-oxide, an agent that produces bulky guanine and adenine adducts and oxidative DNA damage and (ii) WRNp interacts with p53 (71, 72) and Ku autoantigen (73). However, in vitro WRNp shows no increased affinity for various types of intrastrand DNA damage, including adducts formed during 4-nitroquinoline-1-oxide treatment (74) but is potently inhibited by the structurally related minor groove binders distamycin A and neotropsin (75). Addition of RP-A did not alleviate this inhibition. Finally, the capacity of WRNp to partially suppress the hyper-recombination phenotype of mutants of its yeast homologue Sgs1 points to a role of WRNp in regulating homologous recombination (76). Thus, the roles of WRN protein in the cell appear to be multifaceted.
A recent finding may uncover a molecular link between the putative
roles of WRNp in replication, repair, and recombination processes (77).
In this study it is shown that WRNp, in the absence of proliferating
cellular antigen, specifically interacts with the 32-kDa subunit of
S. cerevisiae DNA polymerase 
, a key DNA polymerase in
replication and repair, and increases the rate of nucleotide
incorporation. The authors suggest that one function of WRNp would be
to play a role in replication reinitiation at forks blocked by DNA
damage or unusual secondary structures that arise during
replication/recombination processes and from which the normal
replication machinery has dissociated, a role previously envisaged for
E. coli RecQ (78).
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ACKNOWLEDGEMENT |
|---|
We are deeply grateful to Dr. P. E. Boehmer for invaluable help in preparing this article.
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FOOTNOTES |
|---|
* This minireview will be reprinted in the 2000 Minireview Compendium, which will be available in December, 2000. The work of the authors is supported by Grant 9584 from the Association pour la Recherche sur le Cancer (to G. V.) and National Institutes of Health Grant GM62643 and American Heart Association Grant 0050973B (to P. E. Boehmer).
§ To whom correspondence should be addressed. Tel.: 33-0561175955; Fax: 33-0561175994; E-mail: villani@ipbs.fr.
Published, JBC Papers in Press, August 22, 2000, DOI 10.1074/jbc.R000011200
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ABBREVIATIONS |
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The abbreviations used are: NER, nucleotide excision repair; HMG, high mobility group; HDH, human DNA helicase; HSV, Herpes simplex virus; TLS, translesion synthesis; WRN, Werner's syndrome.
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