Department of Microbial Biotechnology, Centro
Nacional de Biotecnología, CSIC, Campus Universidad
Autónoma de Madrid, Cantoblanco, 28049 Madrid,
Spain,1 and INRA-Génétique
Microbienne, 78352 Jouy-en-Josas Cedex, France2
 |
TEXT |
Genetic analysis using
chromosomal and plasmid transformation allows the classification of
Bacillus subtilis Rec
strains, other
than recA strains, within five different epistatic groups
(
, 
, 
, 
, and 
groups) (6, 12). Unless
otherwise stated, the indicated genes and products are of B. subtilis origin. The epistatic group activity requires the
recF, recL, recO, recR, and
recN genes (3-5). The recF,
recL, recO, and recR strains and the
Escherichia coli recF
(recFEco),
recOEco, and
recREco strains have similar phenotypes
and share indirect suppressors (e.g., a special type of recA
mutant) (2, 10). It was assumed therefore that RecFLOR has
its counterpart in the RecFOREco complex
(6, 13). The epistatic group activity is dependent on
the addA and addB genes (3). The
addA and addB genes encode different subunits of
the nuclease-helicase AddAB (also termed exonuclease V or
RecBCDEco for E. coli)
(8, 9, 16). The epistatic group activity requires the
recP and recH genes (6). The epistatic group activity requires the recB, recD,
and recU genes (4), and the group is
dependent on recS, a gene sharing homology with
recQ of both B. subtilis and E. coli origin (12). The function whose mutants were
classified within the , , and epistatic groups does not seem
to have a counterpart in E. coli (6, 14).
Identification of the helD gene.
DNA helicases
are involved in both the generation of the recombinogenic
substrates and branch migration of synapsed Holliday junctions
(16). RecBCDEco and the
recQEco,
uvrDEco, and
helDEco gene products have been implicated
in the RecBCDEco and
RecFEco recombination pathways,
respectively. The RecBCD DNA helicase is implicated in the presynaptic
stage of recombination. Furthermore, it has been suggested that
the presence of RecQEco,
UvrDEco, or E. coli
helicase IV (helD gene product, a 3' to 5' DNA helicase) is
required for efficient recombination and repair in a
recBCEco
sbcB(C)Eco
background (21, 23). The B. subtilis pcrA,
addAB, and yvgS genes encode a DNA helicase or
have a high degree of identity with bona fide DNA helicases of the SF1
family (8, 9, 16, 24, 25), and the recS and
recQ gene products have identity with DNA helicases of the
SF2 family, according to the nomenclature of Gorbalenya and Koonin
(15). No UvrDEco,
RepEco, or
HelEco counterparts have been described
for B. subtilis (17, 24).
Helicases of the SF1 family share seven conserved motives scattered
along the protein sequence. Structural analysis has shown that these
motives come close together in the folded protein, bind ATP, and
correspond to the translocating domain of these helicases, allowing the
tracking of single-stranded DNA through the protein. The seven motives
delimit four domains in the primary sequence of the SF1 helicases, an
N-terminal domain preceding the first motive, a 1B domain between the
second and third motives, a 2B domain between the fifth and sixth
motives, and a C-terminal (C-t) domain after the last motive (Fig.
1). An analysis of the length of these
four domains in any helicase of the SF1 family allows their
classification into one of the three following groups: (i) the PcrA
subfamily, helicases with a fixed 1B and 2B length (~134 and 220 to
240 residues, respectively); (ii) the
HelDEco subfamily, helicases with a long
C-t and a short 2B domain; and (iii) the AddA subfamily, helicases with
a long C-t domain. The four helicases of the SF1 family in B. subtilis and in E. coli were classified accordingly, as
shown Fig. 1. PcrA and YjcD belonged to the first group, together with
UvrDEco and
RepEco. The YvgS protein belonged to the
second group, together with HelDEco or
E. coli helicase IV. We therefore propose to name the YvgS protein HelD. It should be noted, however, that the overall level of
similarity between HelD and HelDEco is low
(22% identity). AddA and RecBEco belonged
to the third group. Again, these last two proteins have only 21.7%
identity, but they have been shown to be functionally equivalent
(8, 9).
View larger version (18K):
[in this window]
[in a new window]
|
FIG. 1.
Classification of DNA helicases of the SF1 family from
B. subtilis and E. coli into three
subfamilies. The seven conserved motives are shown with boxes separated
by the four domains, called N-t (N-terminal), 1B, 2B, and C-t
(C-terminal). The distances (in amino acid residues) separating the
different clusters of motives are reported on the right part of the
figure. See the text for details.
|
|
PcrA, which is able to suppress the UV sensitivity defect of a
uvrDEco mutant, is an essential DNA
helicase (24). A defect in RecS decreases plasmid
transformation ~100-fold when present in an otherwise
Rec+ strain (12). The AddAB protein
has its counterpart in the RecBCDEco enzyme (8, 9, 16). Nothing is known about the role of RecQ
and helicase IV (helD gene product) in recombination and DNA
repair. Here, we report the genetic analysis of a helD null allele (
helD) in combination with rec
function, classified within the , , , , and epistatic
groups. We show that the loss of helicase IV stabilized recombination
repair intermediates formed in the absence of recFLOR and
rendered recFLOR, addAB, and recH cells impaired in plasmid transformation. Furthermore, the fact that
the helD mutation is a common partial suppressor of the recFLOR mutations further supported the classification of
the recFLOR genes within the epistatic group.
Disruption of the helD gene by use of a selectable
marker.
It has been shown previously that (i) E. coli
helicase IV is a DNA helicase (26), (ii) it shares several
biochemical properties with the E. coli helicase II and Rep
proteins (27), (iii) double helicase II
(uvrDEco)-helicase IV
(helDEco) deletion mutants are defective
in DNA recombination and repair (20), (iv) B. subtilis possesses two genes homologous to the
uvrDEco-repEco
tandem, the pcrA and yjcD genes
(reference 24; also see above), (v) PcrA, which suppresses
the UV sensitivity defect of a uvrDEco
mutant, is an essential helicase of B. subtilis, whereas a
yjcD mutant does not exhibit a UV-sensitive phenotype
(24). To learn whether the helD gene is
involved in recombinational DNA repair, we have constructed a
helD deletion strain. The helD gene was
disrupted using the plasmid pMUTIN2 (details of the mutant
construction are available on the Micado site
[http://locus.jouy.inra.fr/cgi-bin/genmic/madbase/progs/madbase.operl]). As a result, the helD gene is disrupted starting 139 bp
downstream from the start codon. The helD mutant allele
was transferred into the B. subtilis chromosome of the wild
type (YB886) and its isogenic rec-deficient derivatives of
groups (recF15 [BG129], recL16 [BG107],
recO [BG439], and recR13
[BG127]) and (addA5 addB72 [BG189]), (recH342 [BG119]), (recU
[BG427]), and (recS [BG425]) listed in Table
1, by a double crossing-over event as
previously described (5). The presence of the desired replacement was confirmed by PCR amplification and nucleotide sequence
analysis (data not shown).
Interaction between helD and the functions
classified within the , , , , and epistatic
groups.
To understand the role of the helD gene product
in homologous recombination, we investigated the genetic interaction
between helD and the following mutant genes:
recF, addA addB (addAB), recH, recU, and recS, which were
selected as representatives of the five different epistatic groups
(, , , , and , respectively). B. subtilis
(rec+) and its isogenic rec-deficient
derivative strains (listed in Table 1) were exposed to the killing
action of DNA-damaging agents as previously described (1).
The removal of lesions from Sn2-type simple alkylating agents, such as
methyl methanesulfonate (MMS), could be carried out to a different
degree by adaptive response and recombination repair (1).
As revealed in Fig. 2, various degrees of
increased sensitivity to 10 mM MMS were observed. The helD and recS cells are slightly sensitive,
the addAB and recH cells are moderately
sensitive, and the recF and recU cells are very sensitive to the killing action of MMS compared to the
rec+ control (1, 5, 12, 13)
(Fig. 2).
View larger version (21K):
[in this window]
[in a new window]
|
FIG. 2.
Survival of B. subtilis strains following
exposure to 10 mM MMS. Survival of rec+
(filled circles) and helD1 strains (empty circles) is
shown. (A) Survival of recF15 cells (empty squares) and
helD1 recF15 cells (filled squares). (B)
Survival of addA5 addB72 cells (empty
squares) and helD1 addA5
addB72 cells (filled squares). (C) Survival of
recH342 cells (empty squares) and helD1
recH342 cells (filled squares). (D) Survival of
recU1 cells (empty squares) and helD1
recU1 cells (filled squares). (E) Survival of
recS1 cells (empty squares) and helD1
recS1 cells (filled squares). The chemical treatment of
DNA repair-deficient mutant strains was performed essentially as
previously described (1).
|
|
The helD mutant allele increases the MMS sensitivity of
addAB, recU, and recS cells but
does not affect the survival rate of recH cells (Fig. 2B to
E). Previously we have shown that the recS null allele
partially suppressed the sensitivity of addAB cells to MMS
(12). Since helD slightly increases the
sensitivity of addAB and recS cells, we have
to assume that helicase IV operates at a different stage than the AddAB
and RecS DNA helicases. Furthermore, if a helicase is needed at the
presynaptic stage in the RecF pathway, as suggested by some experiments
with E. coli (21), the fact that helD
addAB and helD recS cells are more
proficient in recombinational DNA repair than recF and/or
recU cells (Fig. 2) suggests that helicase IV is not the
only helicase responsible for presenting the DNA substrate to RecA. An
alternative DNA helicase (e.g., PcrA, YjcD, RecQ, RecG or
RuvAB), alone or in concerted action with a nuclease, could
generate the recombinogenic substrate. Because the pcrA gene
product is essential (24), the double mutant pcrA
helD could not be tested. Whether any of the remaining putative
helicases, encoded by yjcD, recG,
recQ, or ruvAB, is involved at this stage remains
to be determined.
The helDEco cells do not exhibit a
UV-sensitive phenotype (21). In B. subtilis the
removal of purine adducts produced by 4-nitroquinoline-1-oxide
(4NQO) has been reported to involve nucleotide excision repair
and recombination repair (1). To analyze and interpret the
involvement of the helD allele in recombinational repair,
we have exposed the helD recF strain to the killing
action of 100 µM 4NQO. helD cells are slightly sensitive
to 4NQO (Fig. 3), but when the
helD recF strain was exposed to the killing action of
4NQO a suppression of the recF defect was observed (Fig. 3).
View larger version (21K):
[in this window]
[in a new window]
|
FIG. 3.
Survival of B. subtilis strains following
exposure to 100 µM 4NQO. Survival of rec+
cells (filled circles), helD1 cells (empty circles),
recF15 cells (empty squares), and helD1
recF15 cells (filled squares) is shown.
|
|
From these data we can infer that (i) helD renders cells
slightly sensitive to DNA-damaging agents, (ii) the helD
gene product (helicase IV) contributed to different extents to the
removal of DNA damage in addAB (group ), recH
(group ), recU (group ), and recS
(group ) cells, and (iii) the absence of helicase IV partially
suppressed the recombinational repair deficiency of recF cells.
helD partially suppresses the DNA repair defects
of the recF, recL, recO,
and recR mutants.
Previously we have shown that
suppressors of the recF defect (e.g., recA73
mutant, overexpression of ssb product) also suppressed the
recL, recO, and recR defects (2,
13). To address whether the helD allele also
suppressed the defect of the recL, recO, and
recR mutations, the respective double mutant strains have been constructed (Table 1).
Unlike the case with recBCEco
sbcB(C)Eco cells, which show a
synergistic interaction between the
helDEco gene and the
recFEco or
recOEco gene for the repair of MMS-damaged
DNA (23), the helD allele suppressed the
recombinational repair defect of recF, recL,
recR, and recO cells (Fig. 2A, 3, and
4). Similar results were observed when
the mutant cells were challenged with 100 µM 4NQO (Fig. 3 and data
not shown).
View larger version (13K):
[in this window]
[in a new window]
|
FIG. 4.
Survival of B. subtilis strains following
exposure to 10 mM MMS. Survival of rec+
(filled circles) and helD1 (empty circles) strains is
analyzed. (A) Survival of recL16 cells (empty squares)
and helD1 recL16 cells (filled squares).
(B) Survival of recO1 cells (empty squares) and
helD1 recO1 cells (filled squares). (C)
Survival of recR13 cells (empty squares) and
helD1 recR13 cells (filled squares).
|
|
The introduction of a plasmid-borne helD gene in the
helD recF background resulted in a phenotype
indistinguishable from that of recF cells (data not
shown). It is likely, therefore, that helD is a bona fide
suppressor of the recFLOR mutants and that the absence of
helicase IV redirects recombinational repair into an avenue different
from the RecFLOR complex.
Effect of helD on genetic recombination.
To
study the effect of the helD mutation on homologous DNA
recombination, we analyzed the requirement of the helD
function in natural transformational recombination. Natural
transformation in B. subtilis involves the transfer of naked
double-stranded DNA from the media, with the subsequent degradation of
one of the exogenous DNA strands by a set of competence
(com) genes (11, 18, 19). Under these
conditions, the level of expression of the recA and
addAB genes is also increased. The recipient competent uninucleated cell takes up the other DNA strand in a linear
single-stranded form (see references 11, 18, and
19 for reviews). Therefore, by the activity of the
com genes, the donor single-stranded DNA is presented to the
recombinational machinery in a form that it is ready for a homology
search on the parental molecule. Hence, in our analysis we are studying
the late presynaptic, synaptic, and postsynaptic stages but neglect the
involvement of rec functions in the presentation of the
substrate (early presynaptic stage) (14).
Except in recA cells where chromosomal transformation is
blocked (~104-fold reduction), chromosomal
transformation did not change more than fourfold relative to the
wild-type value when present in an otherwise wild-type strain (1, Table
2). The effect of double or triple
mutations in some cases, however, is drastic. A recFLOR (epistatic group ) mutation blocks (>1,000-fold reduction)
chromosomal transformation of addAB (group ) and
recH (group ) cells and reduces (>20-fold) that of
recU (group ) or recS (group ) cells
(2, 6, 12, 13). A recH mutation blocks
(>1,000-fold) chromosomal transformation of addAB cells and
reduces (>200-fold) that of recS cells, but it does not
affect chromosomal transformation of recU cells more than
fourfold (5, 6, 12, 13).
View this table:
[in this window]
[in a new window]
|
TABLE 2.
Effect of the helD mutation on homologous
recombination as measured by transformation of chromosomal and
plasmid DNAa
|
|
Plasmid establishment on transformation of B. subtilis
competent cells is dependent on the degree of oligomerization of the plasmid genome and requires the RecU, RecO, and RecS products (7,
12, 13) but is independent of the RecA activity (12, 18,
19). Except in the recO, recU, and
recS strains (50-fold reduction), the frequency of
plasmid transformation did not change more than twofold relative to the
wild-type value (12, 13). A recFLOR mutation
blocks (>100-fold) plasmid transformation of addAB (group
) and recH (group ) cells and reduces (>15-fold) that
of recU or recS cells (5, 6, 12,
13). A recH mutation reduced plasmid transformation
of recU and recS cells about 10-fold
(12). Altogether those data indicate that the gene
products classified with the , , , , and epistatic groups provide overlapping activities that compensate for the effects of a single mutation.
By measuring both chromosomal (intermolecular recombination) and
plasmid (intramolecular recombination) transformation we can examine
different types of events. B. subtilis competent cells were
transformed with 1 µg of homologous chromosomal DNA or plasmid DNA/ml
to determine the transformation frequency of the
Rec mutant strains. The frequency of appearance
of met+ transformants in the single Rec
strains and in certain double Rec strains has been previously
reported (1). Here, however, the experiments were
performed in parallel for comparison with other strains (Table 2). We
show here that helD deletion did not affect more than
threefold chromosomal transformation of recF, addAB, recH, recU, and
recS cells (Table 2).
The helD deletion did not affect more than twofold
plasmid transformation of the highly impaired recU and
recS cells, and it reduced three- to sevenfold plasmid
transformation of recF, addAB, and
recH cells (Table 2).
What is the role for helicase IV in DNA recombination?
The
AddAB, PcrA, helicase IV, RecS, and RecQ helicases are the orthologs of
the presynaptic RecBCDEco,
UvrDEco, E. coli
helicase IV, and RecQEco DNA
helicases, respectively. However, genetic studies on mutants of these
various helicases start to uncover some differences in terms of their
respective roles in repair and recombination in the two hosts. PcrA is
essential in B. subtilis, whereas
UvrDEco is not essential under laboratory growth conditions (24). It has been shown that
RecQEco is required for conjugational
recombination and DNA repair in a
recBCEco
sbcB(C)Eco background
(22), whereas the RecS helicase partially suppressed the
DNA repair defect of addAB cells and was required for
plasmid transformation and DNA repair in an otherwise Rec+
background (12). The
uvrDEco,
helDEco,
recQEco, and helD
cells were recombination and repair proficient when present in
otherwise Rec+ cells (21, 22, this work). A
helDEco mutation, which has no effect
on repair and recombination in an
recBCEco sbcB(C)Eco background,
interacts synergistically with recFEco
and recOEco in the repair of
MMS-damaged DNA (21), but we show here that
helD partially suppresses the DNA repair defect of
recFLOR cells.
A possible way to reconcile these contrasting observations is to
consider that in B. subtilis recombinational repair takes place mostly through the functions classified within the (recFLOR) and (recB,
recU, and recD) epistatic groups. To illustrate
this point, one should compare the steepness of MMS curves for a
recF or a recU mutant to the modest effect of MMS
on survival of an addAB mutant. Furthermore, genetic studies
are made possible in a RecF
Add+ background in B. subtilis which
are prevented in E. coli given the preponderance of the
RecBCD pathway, hiding all possible effect of mutations on the RecF
pathway. Taking these data into account, we propose that in a
recF background, helicase IV extends the number of gaps
created upon injury to DNA, which results in a severe sensitivity to
genotoxic agents. When it is absent, fewer gaps are created, which are
taken in charge by the functions classified within the (RecB, RecU,
and RecD) and (AddAB) epistatic groups, and this results in the
partial suppression of the repair defect. Such an effect cannot be
observed in E. coli for the above-mentioned reasons (work in
a recBC sbcBC background). Still, one observation made for E. coli could be reminiscent of such a role for
helicase IV. It was found that the double
recQEco uvrDEco
mutant could not be constructed in a
recBCEco sbcBCEco
background, whereas the triple recQEco
uvrDEco helDEco mutant
was successfully constructed, albeit with difficulty (22).
This suggests that somehow the absence of helicase IV in this mutant
had a positive effect, possibly by reducing the amount of
substrate that RecFOR had to deal with. A similar and
symmetrical argument can be drawn in the case of recS
(12). In conclusion, studies on recombination in B. subtilis are instructive and stimulating for the broadening of our
view on recombination mechanisms in bacteria at large.
| 1.
|
Alonso, J. C.,
R. H. Tailor, and G. Lüder.
1988.
Characterization of recombination-deficient mutants of Bacillus subtilis.
J. Bacteriol.
170:3001-3007[Abstract/Free Full Text].
|
| 2.
|
Alonso, J. C., and G. Lüder.
1991.
Characterization of recF suppressors in Bacillus subtilis.
Biochimie
73:277-280[Medline].
|
| 3.
|
Alonso, J. C.,
G. Lüder, and R. H. Tailor.
1991.
Characterization of the Bacillus subtilis recombinational pathways.
J. Bacteriol.
173:3977-3980[Abstract/Free Full Text].
|
| 4.
|
Alonso, J. C.,
G. Lüder, and T. A. Trautner.
1992.
Intramolecular homologous recombination in Bacillus subtilis 168.
Mol. Gen. Genet.
236:60-64[Medline].
|
| 5.
|
Alonso, J. C.,
A. C. Stiege, and G. Lüder.
1993.
Molecular analysis of the Bacillus subtilis recF function.
Mol. Gen. Genet.
239:129-136[CrossRef][Medline].
|
| 6.
|
Alonso, J. C.,
S. Ayora, and F. Rojo.
1996.
Recombinación Genética en Bacillus subtilis,, p. 229-240.
In
J. Casadesús (ed.), Microbiología y genética molecular. Publicaciones Universidad de Huelva, Huelva, Spain.
|
| 7.
|
Canosi, U.,
A. Iglesias, and T. A. Trautner.
1981.
Plasmid transformation in Bacillus subtilis: effects of insertion of Bacillus subtilis DNA into plasmid pC194.
Mol. Gen. Genet.
181:434-440[CrossRef][Medline].
|
| 8.
|
Chédin, F.,
P. Noirot,
V. Biaudet, and S. D. Ehrlich.
1998.
A five-nucleotide sequence protects DNA from exonucleolytic degradation by AddAB, the RecBCD analogue of Bacillus subtilis.
Mol. Microbiol.
29:1369-1377[CrossRef][Medline].
|
| 9.
|
Chédin, F.,
S. D. Ehrlich, and S. C. Kowalczykowsky.
2000.
The Bacillus subtilis AddAB helicase/exonuclease is regulated by its cognate Chi sequence in vitro.
J. Mol. Biol.
298:7-20[CrossRef][Medline].
|
| 10.
|
Clark, A. J., and S. J. Sandler.
1994.
Homologous genetic recombination: the pieces begin to fall into place.
Crit. Rev. Microbiol.
20:125-142[Medline].
|
| 11.
|
Dubnau, D.
1993.
Genetic exchange and homologous recombination, p. 555-584.
In
A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria. American Society for Microbiology, Washington, D.C.
|
| 12.
|
Fernández, S.,
A. Sorokin, and J. C. Alonso.
1998.
Genetic recombination in Bacillus subtilis 168: effects of recU and recS on DNA repair and homologous recombination.
J. Bacteriol.
180:3405-3409[Abstract/Free Full Text].
|
| 13.
|
Fernández, S.,
Y. Kobayashi,
N. Ogasawara, and J. C. Alonso.
1999.
Analysis of the Bacillus subtilis recO gene: RecO is part of RecFLOR function.
Mol. Gen. Genet.
261:567-573[CrossRef][Medline].
|
| 14.
|
Fernández, S.,
S. Ayora, and J. C. Alonso.
2000.
Bacillus subtilis homologous recombination gene and products.
Res. Microbiol.
151:481-486[Medline].
|
| 15.
|
Gorbalenya, A. E., and E. V. Koonin.
1993.
Helicases: amino acid sequence comparisons and structure-function relationships.
Curr. Opin. Struct. Biol.
3:419-429.
|
| 16.
|
Kooistra, J., and G. Venema.
1991.
Cloning, sequencing and expression of Bacillus subtilis genes involved in ATP-dependent nuclease synthesis.
J. Bacteriol.
173:3644-3655[Abstract/Free Full Text].
|
| 17.
|
Kunst, F.,
N. Ogasawara,
I. Moszer,
A. M. G. Albertini,
Alloni,
V. M. G. Azevedo,
Bestero, et al.
1997.
The complete genome sequence of the Gram-positive model organism Bacillus subtilis.
Nature
390:249-256[CrossRef][Medline].
|
| 18.
|
Lacks, S. A.
1988.
Mechanisms of genetic recombination in gram-positive bacteria, p. 43-86.
In
R. Kucherlapati, and G. R. Smith (ed.), Genetic recombination. American Society for Microbiology, Washington, D.C.
|
| 19.
|
Lorenz, M. G., and W. Wackernagel.
1994.
Bacterial gene transfer by natural genetic transformation in the environment.
Microbiol. Rev.
58:563-602[Abstract/Free Full Text].
|
| 20.
|
Matson, S. W.
1989.
Escherichia coli DNA helicase II (uvrD gene product) catalyzes the unwinding of DNA-RNA hybrids in vitro.
Proc. Natl. Acad. Sci. USA
86:4430-4434[Abstract/Free Full Text].
|
| 21.
|
Mendonca, V. M.,
K. Kaiser-Rogers, and S. W. Matson.
1993.
Double helicase II (uvrD)-helicase IV (helD) deletion mutants are defective in the recombination pathways of Escherichia coli.
J. Bacteriol.
175:4641-4651[Abstract/Free Full Text].
|
| 22.
|
Mendonca, V. M.,
H. D. Klepin, and S. W. Matson.
1995.
DNA helicases in recombination and repair: construction of a uvrD helD recQ mutant deficient in recombination and repair.
J. Bacteriol.
177:1326-1335[Abstract/Free Full Text].
|
| 23.
|
Mendonca, V. M., and S. W. Matson.
1995.
Genetic analysis of helD and uvrD mutation in combination with other genes in the RecF recombination pathways in Escherichia coli: suppression of a ruvB mutation by a uvrD deletion.
Genetics
141:443-452[Abstract].
|
| 24.
|
Petit, M. A.,
E. Dervyn,
K. D. Entian,
S. McGovern,
S. D. Ehrlich, and C. Bruan.
1998.
PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling circle replication.
Mol. Microbiol.
29:261-273[CrossRef][Medline].
|
| 25.
|
Subramanya, H. S.,
L. E. Bird,
J. A. Brannigan, and D. B. Wigle.
1996.
Crystal structure of the Dexx box DNA helicase.
Nature
384:379-383[CrossRef][Medline].
|
| 26.
|
Wood, E. R., and S. W. Matson.
1989.
The molecular cloning of the gene encoding the Escherichia coli 75-kDa helicase and the determination of its nucleotide sequence and genetic map position.
J. Biol. Chem.
264:8297-8303[Abstract/Free Full Text].
|
| 27.
|
Yancey-Wrona, J. E.,
E. R. Wood,
J. W. George,
K. R. Smith, and S. W. Matson.
1992.
Escherichia coli Rep protein and helicase IV. Distributive single-stranded DNA-dependent ATPases that catalyze a limited unwinding reaction in vitro.
Eur. J. Biochem.
207:479-485[Medline].
|
![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
helD on DNA Repair
and Homologous Recombination
Top
Abstract
Text
