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300 a.a.
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(+ 0 more)
239 a.a.
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* Residue conservation analysis
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Embo J
22:4566-4576
(2003)
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PubMed id:
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Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2.
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D.S.Shin,
L.Pellegrini,
D.S.Daniels,
B.Yelent,
L.Craig,
D.Bates,
D.S.Yu,
M.K.Shivji,
C.Hitomi,
A.S.Arvai,
N.Volkmann,
H.Tsuruta,
T.L.Blundell,
A.R.Venkitaraman,
J.A.Tainer.
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ABSTRACT
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To clarify RAD51 interactions controlling homologous recombination, we report
here the crystal structure of the full-length RAD51 homolog from Pyrococcus
furiosus. The structure reveals how RAD51 proteins assemble into inactive
heptameric rings and active DNA-bound filaments matching three-dimensional
electron microscopy reconstructions. A polymerization motif (RAD51-PM) tethers
individual subunits together to form assemblies. Subunit interactions support an
allosteric 'switch' promoting ATPase activity and DNA binding roles for the
N-terminal domain helix-hairpin-helix (HhH) motif. Structural and mutational
results characterize RAD51 interactions with the breast cancer susceptibility
protein BRCA2 in higher eukaryotes. A designed P.furiosus RAD51 mutant binds BRC
repeats and forms BRCA2-dependent nuclear foci in human cells in response to
gamma-irradiation-induced DNA damage, similar to human RAD51. These results show
that BRCA2 repeats mimic the RAD51-PM and imply analogous RAD51 interactions
with RAD52 and RAD54. Both BRCA2 and RAD54 may act as antagonists and chaperones
for RAD51 filament assembly by coupling RAD51 interface exchanges with DNA
binding. Together, these structural and mutational results support an interface
exchange hypothesis for coordinated protein interactions in homologous
recombination.
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Literature references that cite this PDB file's key reference
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PubMed id
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Reference
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J.A.Grasby,
and
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Human flap endonuclease structures, DNA double-base flipping, and a unified understanding of the FEN1 superfamily.
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Cell,
145,
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PDB codes:
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A.L.Forget,
and
S.C.Kowalczykowski
(2010).
Single-molecule imaging brings Rad51 nucleoprotein filaments into focus.
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Trends Cell Biol,
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Two modules in the BRC repeats of BRCA2 mediate structural and functional interactions with the RAD51 recombinase.
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and
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Mutation of the RAD51C gene in a Fanconi anemia-like disorder.
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Nat Genet,
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L.Zou
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DNA repair: A protein giant in its entirety.
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Nature,
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Software for the high-throughput collection of SAXS data using an enhanced Blu-Ice/DCS control system.
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J Synchrotron Radiat,
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T.Thorslund,
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S.A.Compton,
S.Lekomtsev,
M.Petronczki,
J.D.Griffith,
and
S.C.West
(2010).
The breast cancer tumor suppressor BRCA2 promotes the specific targeting of RAD51 to single-stranded DNA.
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Nat Struct Mol Biol,
17,
1263-1265.
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W.Kagawa,
and
H.Kurumizaka
(2010).
From meiosis to postmeiotic events: uncovering the molecular roles of the meiosis-specific recombinase Dmc1.
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FEBS J,
277,
590-598.
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Y.Savir,
and
T.Tlusty
(2010).
RecA-mediated homology search as a nearly optimal signal detection system.
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| |
Mol Cell,
40,
388-396.
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A.A.Grigorescu,
J.H.Vissers,
D.Ristic,
Y.Z.Pigli,
T.W.Lynch,
C.Wyman,
and
P.A.Rice
(2009).
Inter-subunit interactions that coordinate Rad51's activities.
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| |
Nucleic Acids Res,
37,
557-567.
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A.Carreira,
J.Hilario,
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R.J.Baskin,
M.K.Shivji,
A.R.Venkitaraman,
and
S.C.Kowalczykowski
(2009).
The BRC repeats of BRCA2 modulate the DNA-binding selectivity of RAD51.
|
| |
Cell,
136,
1032-1043.
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A.R.Venkitaraman
(2009).
Linking the cellular functions of BRCA genes to cancer pathogenesis and treatment.
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Annu Rev Pathol,
4,
461-487.
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A.Reymer,
K.Frykholm,
K.Morimatsu,
M.Takahashi,
and
B.Nordén
(2009).
Structure of human Rad51 protein filament from molecular modeling and site-specific linear dichroism spectroscopy.
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Proc Natl Acad Sci U S A,
106,
13248-13253.
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C.A.Haseltine,
and
S.C.Kowalczykowski
(2009).
An archaeal Rad54 protein remodels DNA and stimulates DNA strand exchange by RadA.
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| |
Nucleic Acids Res,
37,
2757-2770.
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C.D.Lee,
and
T.F.Wang
(2009).
The N-terminal domain of Escherichia coli RecA have multiple functions in promoting homologous recombination.
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J Biomed Sci,
16,
37.
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D.Lucarelli,
Y.A.Wang,
V.E.Galkin,
X.Yu,
D.B.Wigley,
and
E.H.Egelman
(2009).
The RecB nuclease domain binds to RecA-DNA filaments: implications for filament loading.
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J Mol Biol,
391,
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D.S.Shin,
M.Didonato,
D.P.Barondeau,
G.L.Hura,
C.Hitomi,
J.A.Berglund,
E.D.Getzoff,
S.C.Cary,
and
J.A.Tainer
(2009).
Superoxide dismutase from the eukaryotic thermophile Alvinella pompejana: structures, stability, mechanism, and insights into amyotrophic lateral sclerosis.
|
| |
J Mol Biol,
385,
1534-1555.
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PDB codes:
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E.V.Mladenov,
P.S.Kalev,
and
B.B.Anachkova
(2009).
Nuclear matrix binding site in the Rad51 recombinase.
|
| |
J Cell Physiol,
219,
202-208.
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J.Hikiba,
Y.Takizawa,
S.Ikawa,
T.Shibata,
and
H.Kurumizaka
(2009).
Biochemical analysis of the human DMC1-I37N polymorphism.
|
| |
FEBS J,
276,
457-465.
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J.J.Perry,
R.M.Harris,
D.Moiani,
A.J.Olson,
and
J.A.Tainer
(2009).
p38alpha MAP kinase C-terminal domain binding pocket characterized by crystallographic and computational analyses.
|
| |
J Mol Biol,
391,
1.
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PDB code:
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M.Frankenberg-Schwager,
A.Gebauer,
C.Koppe,
H.Wolf,
E.Pralle,
and
D.Frankenberg
(2009).
Single-strand annealing, conservative homologous recombination, nonhomologous DNA end joining, and the cell cycle-dependent repair of DNA double-strand breaks induced by sparsely or densely ionizing radiation.
|
| |
Radiat Res,
171,
265-273.
|
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R.B.Robertson,
D.N.Moses,
Y.Kwon,
P.Chan,
W.Zhao,
P.Chi,
H.Klein,
P.Sung,
and
E.C.Greene
(2009).
Visualizing the disassembly of S. cerevisiae Rad51 nucleoprotein filaments.
|
| |
J Mol Biol,
388,
703-720.
|
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|
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R.S.Williams,
G.E.Dodson,
O.Limbo,
Y.Yamada,
J.S.Williams,
G.Guenther,
S.Classen,
J.N.Glover,
H.Iwasaki,
P.Russell,
and
J.A.Tainer
(2009).
Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair.
|
| |
Cell,
139,
87-99.
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PDB codes:
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S.Delmas,
L.Shunburne,
H.P.Ngo,
and
T.Allers
(2009).
Mre11-Rad50 promotes rapid repair of DNA damage in the polyploid archaeon Haloferax volcanii by restraining homologous recombination.
|
| |
PLoS Genet,
5,
e1000552.
|
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|
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S.Kojima,
K.Imada,
M.Sakuma,
Y.Sudo,
C.Kojima,
T.Minamino,
M.Homma,
and
K.Namba
(2009).
Stator assembly and activation mechanism of the flagellar motor by the periplasmic region of MotB.
|
| |
Mol Microbiol,
73,
710-718.
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PDB codes:
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T.Ishida,
Y.Takizawa,
T.Kainuma,
J.Inoue,
T.Mikawa,
T.Shibata,
H.Suzuki,
S.Tashiro,
and
H.Kurumizaka
(2009).
DIDS, a chemical compound that inhibits RAD51-mediated homologous pairing and strand exchange.
|
| |
Nucleic Acids Res,
37,
3367-3376.
|
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|
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Y.Morozumi,
Y.Takizawa,
M.Takaku,
and
H.Kurumizaka
(2009).
Human PSF binds to RAD51 and modulates its homologous-pairing and strand-exchange activities.
|
| |
Nucleic Acids Res,
37,
4296-4307.
|
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|
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Y.W.Chang,
T.P.Ko,
C.D.Lee,
Y.C.Chang,
K.A.Lin,
C.S.Chang,
A.H.Wang,
and
T.F.Wang
(2009).
Three new structures of left-handed RADA helical filaments: structural flexibility of N-terminal domain is critical for recombinase activity.
|
| |
PLoS ONE,
4,
e4890.
|
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PDB codes:
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C.L.Hartley,
and
R.McCulloch
(2008).
Trypanosoma brucei BRCA2 acts in antigenic variation and has undergone a recent expansion in BRC repeat number that is important during homologous recombination.
|
| |
Mol Microbiol,
68,
1237-1251.
|
|
|
|
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|
|
D.Sheng,
M.Li,
J.Jiao,
J.Ni,
and
Y.Shen
(2008).
Co-expression with RadA and the characterization of stRad55B, a RadA paralog from the hyperthermophilic crenarchaea Sulfolobus tokodaii.
|
| |
Sci China C Life Sci,
51,
60-65.
|
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|
|
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|
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J.Hikiba,
K.Hirota,
W.Kagawa,
S.Ikawa,
T.Kinebuchi,
I.Sakane,
Y.Takizawa,
S.Yokoyama,
B.Mandon-Pépin,
A.Nicolas,
T.Shibata,
K.Ohta,
and
H.Kurumizaka
(2008).
Structural and functional analyses of the DMC1-M200V polymorphism found in the human population.
|
| |
Nucleic Acids Res,
36,
4181-4190.
|
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PDB code:
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J.San Filippo,
P.Sung,
and
H.Klein
(2008).
Mechanism of eukaryotic homologous recombination.
|
| |
Annu Rev Biochem,
77,
229-257.
|
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|
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|
|
J.T.Holt,
W.P.Toole,
V.R.Patel,
H.Hwang,
and
E.T.Brown
(2008).
Restoration of CAPAN-1 cells with functional BRCA2 provides insight into the DNA repair activity of individuals who are heterozygous for BRCA2 mutations.
|
| |
Cancer Genet Cytogenet,
186,
85-94.
|
|
|
|
|
|
|
M.Frankenberg-Schwager,
M.Becker,
I.Garg,
E.Pralle,
H.Wolf,
and
D.Frankenberg
(2008).
The role of nonhomologous DNA end joining, conservative homologous recombination, and single-strand annealing in the cell cycle-dependent repair of DNA double-strand breaks induced by H(2)O(2) in mammalian cells.
|
| |
Radiat Res,
170,
784-793.
|
|
|
|
|
|
|
M.López-Casamichana,
E.Orozco,
L.A.Marchat,
and
C.López-Camarillo
(2008).
Transcriptional profile of the homologous recombination machinery and characterization of the EhRAD51 recombinase in response to DNA damage in Entamoeba histolytica.
|
| |
BMC Mol Biol,
9,
35.
|
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|
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M.Nowacka-Zawisza,
M.Brys,
H.Romanowicz-Makowska,
A.Kulig,
and
W.M.Krajewska
(2008).
Dinucleotide repeat polymorphisms of RAD51, BRCA1, BRCA2 gene regions in breast cancer.
|
| |
Pathol Int,
58,
275-281.
|
|
|
|
|
|
|
R.A.Edwards,
M.S.Lee,
S.E.Tsutakawa,
R.S.Williams,
J.A.Tainer,
and
J.N.Glover
(2008).
The BARD1 C-terminal domain structure and interactions with polyadenylation factor CstF-50.
|
| |
Biochemistry,
47,
11446-11456.
|
|
|
|
|
|
|
R.Kanaar,
C.Wyman,
and
R.Rothstein
(2008).
Quality control of DNA break metabolism: in the 'end', it's a good thing.
|
| |
EMBO J,
27,
581-588.
|
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|
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|
|
A.Yamagata,
and
J.A.Tainer
(2007).
Hexameric structures of the archaeal secretion ATPase GspE and implications for a universal secretion mechanism.
|
| |
EMBO J,
26,
878-890.
|
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|
PDB codes:
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C.D.Putnam,
M.Hammel,
G.L.Hura,
and
J.A.Tainer
(2007).
X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution.
|
| |
Q Rev Biophys,
40,
191-285.
|
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|
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|
|
F.Esashi,
V.E.Galkin,
X.Yu,
E.H.Egelman,
and
S.C.West
(2007).
Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2.
|
| |
Nat Struct Mol Biol,
14,
468-474.
|
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|
|
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|
|
J.J.Perry,
L.Fan,
and
J.A.Tainer
(2007).
Developing master keys to brain pathology, cancer and aging from the structural biology of proteins controlling reactive oxygen species and DNA repair.
|
| |
Neuroscience,
145,
1280-1299.
|
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|
|
L.T.Chen,
T.P.Ko,
Y.C.Chang,
K.A.Lin,
C.S.Chang,
A.H.Wang,
and
T.F.Wang
(2007).
Crystal structure of the left-handed archaeal RadA helical filament: identification of a functional motif for controlling quaternary structures and enzymatic functions of RecA family proteins.
|
| |
Nucleic Acids Res,
35,
1787-1801.
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PDB code:
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|
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L.T.Chen,
T.P.Ko,
Y.W.Chang,
K.A.Lin,
A.H.Wang,
and
T.F.Wang
(2007).
Structural and functional analyses of five conserved positively charged residues in the L1 and N-terminal DNA binding motifs of archaeal RADA protein.
|
| |
PLoS ONE,
2,
e858.
|
|
|
PDB code:
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|
O.R.Davies,
and
L.Pellegrini
(2007).
Interaction with the BRCA2 C terminus protects RAD51-DNA filaments from disassembly by BRC repeats.
|
| |
Nat Struct Mol Biol,
14,
475-483.
|
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|
|
|
|
|
Q.Zhou,
M.Kojic,
Z.Cao,
M.Lisby,
N.A.Mazloum,
and
W.K.Holloman
(2007).
Dss1 interaction with Brh2 as a regulatory mechanism for recombinational repair.
|
| |
Mol Cell Biol,
27,
2512-2526.
|
|
|
|
|
|
|
R.S.Williams,
J.S.Williams,
and
J.A.Tainer
(2007).
Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template.
|
| |
Biochem Cell Biol,
85,
509-520.
|
|
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|
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|
|
S.Vijayakumar,
B.R.Chapados,
K.H.Schmidt,
R.D.Kolodner,
J.A.Tainer,
and
A.E.Tomkinson
(2007).
The C-terminal domain of yeast PCNA is required for physical and functional interactions with Cdc9 DNA ligase.
|
| |
Nucleic Acids Res,
35,
1624-1637.
|
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|
PDB code:
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|
|
T.Thorslund,
and
S.C.West
(2007).
BRCA2: a universal recombinase regulator.
|
| |
Oncogene,
26,
7720-7730.
|
|
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|
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|
|
T.van der Heijden,
R.Seidel,
M.Modesti,
R.Kanaar,
C.Wyman,
and
C.Dekker
(2007).
Real-time assembly and disassembly of human RAD51 filaments on individual DNA molecules.
|
| |
Nucleic Acids Res,
35,
5646-5657.
|
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|
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|
|
A.Granéli,
C.C.Yeykal,
R.B.Robertson,
and
E.C.Greene
(2006).
Long-distance lateral diffusion of human Rad51 on double-stranded DNA.
|
| |
Proc Natl Acad Sci U S A,
103,
1221-1226.
|
|
|
|
|
|
|
C.Wiese,
J.M.Hinz,
R.S.Tebbs,
P.B.Nham,
S.S.Urbin,
D.W.Collins,
L.H.Thompson,
and
D.Schild
(2006).
Disparate requirements for the Walker A and B ATPase motifs of human RAD51D in homologous recombination.
|
| |
Nucleic Acids Res,
34,
2833-2843.
|
|
|
|
|
|
|
J.M.Pascal,
O.V.Tsodikov,
G.L.Hura,
W.Song,
E.A.Cotner,
S.Classen,
A.E.Tomkinson,
J.A.Tainer,
and
T.Ellenberger
(2006).
A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA.
|
| |
Mol Cell,
24,
279-291.
|
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|
PDB codes:
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|
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Conserved XPB core structure and motifs for DNA unwinding: implications for pathway selection of transcription or excision repair.
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Mol Cell,
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PDB codes:
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M.Kojic,
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M.Lisby,
and
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Rec2 interplay with both Brh2 and Rad51 balances recombinational repair in Ustilago maydis.
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Mol Cell Biol,
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M.Spies,
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The RecA binding locus of RecBCD is a general domain for recruitment of DNA strand exchange proteins.
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Mol Cell,
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N.Sarai,
W.Kagawa,
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H.Kurumizaka,
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(2006).
Stimulation of Dmc1-mediated DNA strand exchange by the human Rad54B protein.
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Nucleic Acids Res,
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Nat Rev Mol Cell Biol,
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Cells expressing murine RAD52 splice variants favor sister chromatid repair.
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Mol Cell Biol,
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V.E.Galkin,
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The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity.
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Structure,
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PDB code:
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V.M.Navadgi,
A.Shukla,
R.K.Vempati,
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DNA mediated disassembly of hRad51 and hRad52 proteins and recruitment of hRad51 to ssDNA by hRad52.
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FEBS J,
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Roles of the human Rad51 L1 and L2 loops in DNA binding.
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FEBS J,
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Conformational flexibility revealed by the crystal structure of a crenarchaeal RadA.
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Nucleic Acids Res,
33,
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PDB code:
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A.Friedler,
D.B.Veprintsev,
T.Rutherford,
K.I.von Glos,
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Binding of Rad51 and other peptide sequences to a promiscuous, highly electrostatic binding site in p53.
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J Biol Chem,
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A.Hatanaka,
M.Yamazoe,
J.E.Sale,
M.Takata,
K.Yamamoto,
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E.Sonoda,
K.Kikuchi,
Y.Yonetani,
and
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(2005).
Similar effects of Brca2 truncation and Rad51 paralog deficiency on immunoglobulin V gene diversification in DT40 cells support an early role for Rad51 paralogs in homologous recombination.
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Mol Cell Biol,
25,
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C.E.Bell
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Structure and mechanism of Escherichia coli RecA ATPase.
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Mol Microbiol,
58,
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C.Proudfoot,
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Distinct roles for two RAD51-related genes in Trypanosoma brucei antigenic variation.
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Nucleic Acids Res,
33,
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D.Ristic,
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C.Dekker,
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Human Rad51 filaments on double- and single-stranded DNA: correlating regular and irregular forms with recombination function.
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Nucleic Acids Res,
33,
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K.Usui,
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C.Ogawa,
C.Kai,
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J.Kawai,
T.Arakawa,
P.Carninci,
M.Itoh,
K.Takio,
M.Miyano,
S.Kidoaki,
T.Matsuda,
Y.Hayashizaki,
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Protein-protein interactions of the hyperthermophilic archaeon Pyrococcus horikoshii OT3.
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Genome Biol,
6,
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P.Sung
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Mediating repair.
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Nat Struct Mol Biol,
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T.Akiba,
N.Ishii,
N.Rashid,
M.Morikawa,
T.Imanaka,
and
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(2005).
Structure of RadB recombinase from a hyperthermophilic archaeon, Thermococcus kodakaraensis KOD1: an implication for the formation of a near-7-fold helical assembly.
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Nucleic Acids Res,
33,
3412-3423.
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PDB codes:
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T.Allers,
and
M.Mevarech
(2005).
Archaeal genetics - the third way.
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Nat Rev Genet,
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T.Kinebuchi,
W.Kagawa,
H.Kurumizaka,
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Role of the N-terminal domain of the human DMC1 protein in octamer formation and DNA binding.
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J Biol Chem,
280,
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V.E.Galkin,
F.Esashi,
X.Yu,
S.Yang,
S.C.West,
and
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(2005).
BRCA2 BRC motifs bind RAD51-DNA filaments.
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Proc Natl Acad Sci U S A,
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X.P.Zhang,
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K.Kiianitsa,
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Gly-103 in the N-terminal domain of Saccharomyces cerevisiae Rad51 protein is critical for DNA binding.
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J Biol Chem,
280,
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Y.V.Kil,
E.A.Glazunov,
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Characteristic thermodependence of the RadA recombinase from the hyperthermophilic archaeon Desulfurococcus amylolyticus.
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J Bacteriol,
187,
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Y.Wu,
X.Qian,
Y.He,
I.A.Moya,
and
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(2005).
Crystal structure of an ATPase-active form of Rad51 homolog from Methanococcus voltae. Insights into potassium dependence.
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J Biol Chem,
280,
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PDB code:
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Y.Yoshikawa,
M.Morimatsu,
K.Ochiai,
M.Nagano,
Y.Yamane,
N.Tomizawa,
N.Sasaki,
and
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(2005).
Insertion/deletion polymorphism in the BRCA2 nuclear localization signal.
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Biomed Res,
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A.B.Conway,
T.W.Lynch,
Y.Zhang,
G.S.Fortin,
C.W.Fung,
L.S.Symington,
and
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Crystal structure of a Rad51 filament.
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Nat Struct Mol Biol,
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791-796.
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PDB code:
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A.R.Venkitaraman
(2004).
Tracing the network connecting BRCA and Fanconi anaemia proteins.
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Nat Rev Cancer,
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Recombination proteins in yeast.
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Annu Rev Genet,
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Homologous recombination: down to the wire.
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Curr Biol,
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Identifying DNA-binding proteins using structural motifs and the electrostatic potential.
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Nucleic Acids Res,
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J.Oh,
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Genetic steps of mammalian homologous repair with distinct mutagenic consequences.
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Mol Cell Biol,
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K.A.Miller,
D.Sawicka,
D.Barsky,
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Domain mapping of the Rad51 paralog protein complexes.
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Nucleic Acids Res,
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Physical interaction between replication protein A and Rad51 promotes exchange on single-stranded DNA.
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J Biol Chem,
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M.E.Stauffer,
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Structural mechanisms of DNA replication, repair, and recombination.
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J Biol Chem,
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N.A.Yamada,
J.M.Hinz,
V.L.Kopf,
K.D.Segalle,
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XRCC3 ATPase activity is required for normal XRCC3-Rad51C complex dynamics and homologous recombination.
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J Biol Chem,
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N.Siaud,
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I.Gy,
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Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1.
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EMBO J,
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D.Korkin,
M.Pichaud,
M.Topf,
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A structural perspective on protein-protein interactions.
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Curr Opin Struct Biol,
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T.Kinebuchi,
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H.Yagi,
T.Shibata,
H.Kurumizaka,
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Positive role of the mammalian TBPIP/HOP2 protein in DMC1-mediated homologous pairing.
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J Biol Chem,
279,
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W.D.Heyer,
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Recombination mechanisms; fortieth anniversary meeting of the Holliday model.
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Mol Cell,
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Y.Takizawa,
T.Kinebuchi,
W.Kagawa,
S.Yokoyama,
T.Shibata,
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H.Kurumizaka
(2004).
Mutational analyses of the human Rad51-Tyr315 residue, a site for phosphorylation in leukaemia cells.
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Genes Cells,
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781-790.
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The most recent references are shown first.
Citation data come partly from CiteXplore and partly
from an automated harvesting procedure. Note that this is likely to be
only a partial list as not all journals are covered by
either method. However, we are continually building up the citation data
so more and more references will be included with time.
Where a reference describes a PDB structure, the PDB
codes are
shown on the right.
|
 |
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