Current Biology, Vol. 14, 1778–1782, October 5, 2004, 2004 Elsevier Ltd. All rights reserved.
0 4 4
Structural Biochemistry of ATP-Driven
Dimerization and DNA-Stimulated
Activation of SMC ATPases
Alfred Lammens, Alexandra Schele,
and Karl-Peter Hopfner*
Gene Center and Institute of Biochemistry
University of Munich
Feodor-Lynen-Straße 25
81377 Munich
Germany
Summary
Structural maintenance of chromosome (SMC) pro-
teins play a central role in higher-order chromosome
structure in all kingdoms of life [1–5]. SMC proteins
consist of a long coiled-coil domain that joins an ATP
binding cassette (ABC) ATPase domain on one side
and a dimerization domain on the other side [6]. SMC
proteins require ATP binding or hydrolysis to promote
cohesion and condensation, which is suggested to
proceed via formation of SMC rings or assemblies
[7–11]. To learn more about the role of ATP in the
architecture of SMC proteins, we report crystal struc-
tures of nucleotide-free and ATP bound P. furiosus
SMC ATPase domains. ATP dimerizes two SMC ATP-
ase domains by binding to opposing Walker A and
signature motifs, indicating that ATP binding can di-
rectly assemble SMC proteins. DNA stimulates ATP
hydrolysis in the engaged SMC ABC domains, sug-
gesting that ATP hydrolysis can be allosterically regu-
lated. Structural and mutagenesis data identify an
SMC protein conserved-arginine finger that is required
for DNA stimulation of the ATPase activity and directly
connects a putative DNA interaction site to ATP. Our
results suggest that stimulation of the SMC ATPase
activity may be a specific feature to regulate the ATP-
driven assembly and disassembly of SMC proteins.
Results and Discussion
Structure of the ATP Bound SMC ATPase
Domain Dimer
To help understand the role of ATP binding and hydroly-
sis by the ATP binding cassette (ABC) domain in promot-
ing higher-order structure of structural maintenance of
chromosome (SMC) proteins, we crystallized the cata-
lytic ABC domain of the Pyrococcus furiosus SMC pro-
tein (pfSMCcd) and determined its crystal structure in
the presence of ATP. For crystallization of a stable ATP
bound complex, it was necessary to introduce the
Walker B motif mutation E1098Q, which traps the ATP
complex of SMC proteins [12, 13]. SMCcd-E1098Q
forms dimers in the presence of ATP in solution, as
judged from the increased hydrodynamic radius in gel
*Correspondence: hopfner@lmb.uni-muenchen.de
DOI 10.1016/j .c ub . 20 04 . 09 .
filtration (Figure 1A). Dimer formation was also observed
for wtSMCcd in the presence of the slowly hydrolysable
ATP analog ATP␥S (data not shown). wtSMCcd did not
form stable dimers during gel filtration in the presence
of ATP, probably because of more rapid ATP hydrolysis.
We determined the ATP bound crystal structure of
pfSMCcd-E1098Q to 2.5 Å resolution by a single-wave-
length anomalous dispersion experiment (see the Sup-
plemental Data available with this article online). Inspec-
tion of the crystal packing revealed that an ATP bound
SMCcd-SMCcd homodimer with sandwiched Mg2⫹-ATP
molecules assembled along the 2-fold symmetry axis
of the crystal lattice (Figure 1C). The SMCcd domains
are arranged to face each other, creating two composite
ATPase active sites in the dimer interface. The compos-
ite active sites contain Walker A/B motifs from one
SMCcd subunit and the signature motif from the oppos-
ing SMCcd subunit. The roots of the two coiled-coil
domains protrude from the same side of the SMCcd
dimer surface, well in accordance with electron-micro-
scopic data of cohesin/condensin complexes [6, 14, 15].
Thus, the structure supports a mechanism in which ATP
binding to and hydrolysis by the SMC ABC domains
control formation and disruption of SMC protein rings
or assemblies (Figure 1D).
ATP Bound Active Site and Dimerization Interface
Two ATP molecules are tightly sandwiched in the
SMCcd dimer interface, each bound via ␣ and ␤ phos-
phates to Walker A motifs to one subunit and via the ␥
phosphate to the signature motif of the opposing subunit
(Figures 1B and 2). ATP:protein contacts (1800 Å2 buried
surface) contribute a similar amount of buried surface
area to the ABC-ABC dimer interface as protein:protein
contacts (2600 Å2 buried surface) do. Thus, ATP binding
and hydrolysis is a major driving force for opening and
closing SMC protein rings. The adenine moieties are
specifically recognized by three main-chain hydrogen
bonds to residues 71 and 72 (Figure 2). The ␣ and ␤
phosphates are bound by the P loop. ␤ and ␥ phos-
phates bind the active-site magnesium ion, which is
additionally coordinated by residues S40, D1097 (via a
water molecule), and Q145. From the opposing subunit,
ATP is bound by hydrogen bonds of K1064 and K1061
to the ribose 2⬘-OH and 3⬘-OH, respectively, and by two
hydrogen bonds from the signature motif S1070-O␥ and
G1072-N to the ATP ␥ phosphate (Figure 2). Besides
these ATP-mediated contacts, several protein-protein
interactions contribute to the SMCcd dimer. At the cen-
ter of the dimer interface, the major interaction is medi-
ated by the D loop (Figure 2). The conserved DA box,
which has long been recognized as an important motif
in SMC proteins [16], forms the central dimerization ele-
ment whereby A1101 hydrophobically interacts with
A1101 from the opposing subunit.
A crystallographically observed water molecule is
poised for collinear attack on the scissile P␥-O bond
(Figure 2). This likely nucleophile for ATP hydrolysis is
SMC ATPase Crystal Structure
1779

Figure 1. Structural Biochemistry of ATP-Driven SMC Dimerization

(A) Gel filtration elution profiles of SMCcd-E1098Q with indicated molecular weight standards (in kDa). In the absence of ATP (continuous
line), SMCcd elutes as a monomer. In the presence of ATP (dashed line), the majority of SMCcd elutes with the hydrodynamic radius
corresponding to a dimer, indicating that ATP promotes engagement of two SMC ABC domains.
(B) SAD and 2Fo ⫺ Fc electron densities (1␴ contour) at the ATP moiety are shown superimposed with the refined model (color-coded sticks).
(C) Two orthogonal views of a ribbon model of the ATP bound SMC ATPase dimer with highlighted and annotated secondary structure. One
subunit is shown in yellow, the other subunit, representing the 2-fold symmetry-related molecule in the crystal, is shown in green. Two ATP
molecules (color-coded sticks with cyan carbons, red oxygens, blue nitrogens, and white phosphor atoms) and two Mg2⫹ ions (magenta
spheres) are sandwiched in the dimer interface and are bound to opposing P loop (red) and signature (magenta) motifs. The two coiled-coil
domains (indicated by dotted lines) protrude from the same face of the dimer, consistent with electron microscopy studies of multisubunit
SMC protein rings. A C-terminal helix (red) reaches across the dimer interface and could be a specific interaction point for other subunits
that control assembly of SMC protein rings.
(D) Model of the closed SMC ring. Two SMC proteins (yellow/green) form a large ring by stable association via dimerization domains on one
side of the coiled coil and ATP-driven association of ABC ATPase domains on the other side of the coiled coil. Additional subunits (orange)
interact with the ABC domain and can further control assembly.

optimally positioned and activated by hydrogen bonds
to E1098 (Walker B, mutated to Q) and the backbone
carbonyl oxygen of H1102 from the opposing subunit.
The contributions to positioning of the nucleophile from
both subunits suggest that ATP hydrolysis only takes
place in the engaged form of the ABC dimer. These
findings are supported by mutagenesis data showing
that an S1070R mutation that disengages ABC:ABC in-
teractions abolishes ATP hydrolysis of SMCcd (see
below).
Conformational Flexibility and ATP-Induced
Structural Switches
In many ABC enzymes, including ABC transporter and
the DNA repair enzyme Rad50, ATP binding induces
a conformational change within the ABC domain; this
change has been linked to a “power stroke” [17]. To
directly visualize ATP-driven structural changes in the
SMC ABC domain, we crystallized wtSMCcd in the ab-
sence of ATP and determined the structure to 2.0 Å
resolution (Figure 3A; Supplemental Data). Comparison
of ATP bound and nucleotide-free SMCcd revealed very
similar overall conformations, indicating that SMC pro-
teins do not possess a “power stroke.” Thus, the role
of ATP binding and hydrolysis of SMC proteins seems
to be limited to the formation and disruption of SMC
protein rings or higher-order assemblies.
Nevertheless, two regions of SMCcd were markedly
altered by ATP binding. The C-terminal helix rotates
away from the ABC domain and binds to the opposing
subunit (Figure 3B). This conformational transition indi-
cates that the C-terminal helix is a good candidate for
the control of SMCcd association and ATPase activity
by additional subunits [12]. A second conformational
change is observed in a surface loop in the vicinity of
the ATPase active site (R loop). In the presence of ATP,
R59 binds to the ATP ␣ phosphate. In the absence of
ATP, the R loop is partially disordered and rearranged
(Figure 3C). The R loop is located in the center of a
positively charged surface patch at the concave side of
the SMCcd dimer on Lobe I (Figure 3D). An equivalent
positively charged molecular surface has been impli-
cated in DNA binding by Rad50 [18]. The ATP-driven
conformational variability and the location in the center
of a positively charged surface region suggest that the
R loop is a good candidate for the stimulation of the
ATPase activity of SMC proteins by DNA.
Current Biology
1780
DNA-Stimulated ATPase Activity
Recent data suggest that ATP hydrolysis by SMC protein
complexes is involved in the stable association of cohe-
sion with DNA in vivo and for the generation of DNA
gyres by condensin in vitro [8, 9, 11]. To test whether
DNA can directly activate the ATPase activity of SMCcd,
we performed thin-layer chromatography assays of
wild-type and mutant SMCcd in the absence or in the
presence of a dsDNA oligonucleotide. We found that
the ATPase activity of P. furiosus SMCcd is slow in the
absence of DNA but strongly stimulated in the presence
of dsDNA (Figure 4A). A similar DNA-dependent stimula-
tion of ATPase activity was observed for both bacterial
(D) Solvent-accessible surface of the ATP bound SMCcd dimer with electrostatic potential (⫹7 kT/e⫺ [blue] to ⫺7 kT/e⫺ [red]). The central
region of the composite DNA binding site is formed by the R loop, which is involved in DNA-stimulated activation of ATP hydrolysis. The
circled areas represent the location of the coiled-coil domains.
Figure 2. ATP Bound Active Site
Stereo view of the ATP bound active site,
shown as ball-and-stick model with the color
code of Figure 1C. Only one out of two sym-
metrically related composite active sites in
the dimer interface is shown. One subunit is
depicted in yellow, the other in green. Key
side chains are labeled (see text for details),
and notable hydrogen bonds are shown as
dashed lines. The major dimerization con-
tacts are hydrogen bonds to the ATP ␥ phos-
phate from the signature motif and to the ri-
bose 2⬘- and 3⬘-OH from K1064 and K1061,
respectively. Additional contacts are contri-
buted from the SMC conserved DA box
(A1101), which forms a hydrophobic interac-
tion core at the center of the dimerization
interface. A water molecule (red sphere) is
positioned for collinear attack on the ␥ phos-
phate (arrow) by E1098 (mutated to Q in the
crystal structure) and the backbone carbonyl
of H1102, suggesting that ATP hydrolysis re-
quires the fully engaged ABC dimer.
and eukaryotic multisubunit SMC protein complexes,
suggesting that this DNA-stimulated ATPase activity di-
rectly acts on the ABC domains in full SMC complexes
as well [19, 20]. Mutations in the Walker A motif (K39A)
and the signature motif (S1070R) abolished ATP hydroly-
sis. The latter has been shown to prevent ATP-induced
ABC domain engagement [21]. This indicates that ATP
hydrolysis specifically occurs in the SMCcd dimer, con-
sistent with the structural results indicating that both
subunits position the putative attacking water molecule
(Figure 2). The Walker B mutation (E1098Q) strongly
reduces ATPase and DNA-stimulated ATPase activity.
The residual activity is consistent with our observation
Figure 3. ATP-Induced Conformational
Changes
(A) MAD and 2Fo ⫺ Fc electron densities (1␴
contour) of a portion of the nucleotide free
SMCcd crystal structure along with the re-
fined model (color-coded sticks).
(B) Superposition of the backbone traces of
nucleotide-free (green) and ATP bound (yel-
low) SMCcd shows that only minor intrado-
main conformational changes are induced by
ATP. The largest conformational changes are
observed for the R loop, which is implicated
in DNA-stimulated control of ATP hydrolysis,
and the C helix, which rotates away to avoid
steric clash with the opposing subunit (not
shown) and to participate in ABC-ABC inter-
action. Thus, the predominant role of ATP is
probably to control engagement/disengage-
ment of two SMC ABC domains.
(C) Detailed view of the R loop (red) of super-
imposed ATP bound (yellow) and nucleotide-
free (gray) SMCcd (shown as backbone
worms). R59 (arginine finger) directly hydro-
gen bonds to the ATP ␣ phosphate (ball-and-
stick model). R59 could participate in ATP
hydrolysis by compensating the negative
charge on the transition state phosphates.
SMC ATPase Crystal Structure
1781
Figure 4A. The arginine finger mutation R59A specifically abolishes DNA stimulation of the SMCcd:ScpA complex as well.
(D) Sequence alignment showing that the arginine finger (highlighted) in the R loop is highly conserved among SMC proteins. This conservation
suggests that the role of the arginine finger in coupling ATP hydrolysis to DNA binding is a more general element of SMC proteins. The
following abbreviations were used: Pf, Pyrococcus furiosus; Tm, Thermatoga maritima; Bs, Bacillus subtilis; hu, human; and Sc, Saccharomyces
cerevisiae.
that crystals of ATP:SMCcd-E1098Q dissolved after a
few days, indicating that the observed crystal structure
nevertheless shows an active site that is capable of ATP
hydrolysis.
Conserved Arginine Finger
Because the R loop showed a substantial rearrangement
in response to ATP binding, we tested the effect of
the arginine finger (R59) on the DNA-stimulated ATPase
activity. We mutated R59 to alanine and performed ATP-
ase activity assays in the presence and absence of DNA.
R59A does not affect the basal ATPase activity of
SMCcd, but it completely abolishes its stimulation by
DNA (Figure 4A). To test whether R59A and other mu-
tants still bind ATP, we performed filter binding assays
(Figure 4B). wtSMCcd, as well as SMCcd-R59A, E1098Q,
and S1070R, retained ATP binding. On the other hand,
the Walker A mutation SMCcd-K39A is defective in ATP
binding. This is consistent with a model stating that
R59A abolishes only the DNA stimulation of the ATPase
activity and that S1070R specifically prevents SMCcd
dimer formation but does not interfere with ATP binding
to Walker A motifs. We also tested the effect of the
non-SMC subunit ScpA on the role of R59 in the DNA-
stimulated ATPase activity. ScpA has no significant ef-
fect on the ATPase activity of pfSMCcd (data not shown)
although it moderately reduces ATPase activity of Bacil-
lus subtilis SMC [12]. In any case, the ScpA:SMCcd
complex also showed pronounced DNA-stimulated
ATPase activity, which was specifically abolished by
R59A (Figure 4C). Thus, the DNA stimulation of the ATP-
ase activity of SMCcd appears to be independent of its
association with ScpA.
Figure 4. Structural and Mechanist Role of
the Arginine Finger
(A) Thin-layer chromatography ATPase activity
assays in the absence (white) and presence
(black) of DNA show that wtSMCcd has DNA-
stimulated ATPase activity. Walker A (K39A)
and Walker B (E1098Q) mutations abolish or
strongly reduce ATPase activity, respectively.
The signature motif mutant S1070R abolishes
ATPase activity, suggesting that ATP hydroly-
sis requires SMCcd:SMCcd engagement. The
R loop mutation (R59A) does not affect the
basal ATPase activity but abolishes DNA
stimulation. Data represent means of tripli-
cate assays (error bars).
(B) ATP binding assays (nitrocellulose filter
binding) of wild-type and mutant SMCcd. All
mutations except Walker A motif K39A show
qualitatively unperturbed ATP binding. This
indicates that ATPase defects are predomi-
nantly associated with ATP hydrolysis rather
than ATP binding. Experiments represent
triplicates (error bars) with subtracted low-
background ATP binding.
(C) Relative stimulation of the ATPase activity
of SMCcd (white) and SMCcd:ScpA (black)
by DNA. Experiments were performed as in
The arginine finger is among the most conserved resi-
dues in SMC proteins (Figure 4D). This exceptional con-
servation indicates that the interaction of the arginine
finger with ATP is a key mechanism in the molecular
function of SMC proteins. The structure and mechanistic
role of arginine fingers on the DNA-stimulated activation
of the SMCcd ATPase activity shows a remarkable anal-
ogy to the allosteric activation of small GTPases by
GTPase-activating proteins (GAPs). GAPs insert into the
active site of G proteins an arginine finger that both
binds GTP and stimulates GTP hydrolysis [22]. R59 most
likely counterbalances the developing negative charge
during ATP hydrolysis. The location of the R loop within
the positively charged molecular surface of SMCcd sug-
gests that DNA binding could directly modify the confor-
mational properties of the R loop; this would lead to a
stable binding of R59 to ATP.
Mechanistic Implications and Conclusions
Recent results indicate that ATP binding to SMC pro-
teins is a major driving force in condensation of DNA
by E. coli MukBEF in vitro. ATP binding was also found
to be important for cohesin ring assembly in vivo [7, 9,
11]. As suggested by the crystal structure, these higher-
order structures are probably mediated by stable ATP
bound SMCcd-SMCcd dimers (Figure 1B). The poor
basal ATPase activity, further regulated by non-SMC
subunits, could result in fairly stable SMC complex/DNA
structures in both cohesion and condensation [12]. Nev-
ertheless, these structures must be eventually disas-
sembled for various reasons; for example, to allow trans-
port of DNA into cohesin rings or to decondensate DNA
after cell division. Activation of SMC protein ATPase
Current Biology
1782
activity by DNA or additional factors would be both a
feasible and a likely mechanism to allow stable ATP-
driven association of SMC protein complexes on one
side, and then a rapid disassembly or decondensation at
specific time points on the other side. Such an allosteric
control, suggested by the striking conservation of the
arginine finger, could be a more general feature of SMC
protein complexes. The activation could be driven sim-
ply by changes in DNA structure in the dividing bacterial
cell or by the presence of additional factors that promote
the interaction of DNA with the SMC ABC domains.
Regulators include DNA, at least for bacterial complexes
and eukaryotic condensin ([20, 23], this study), but in
principle could also involve protein factors, such as the
possible cohesin loading factor Scc2/4 [24, 25].
Supplemental Data
Detailed Experimental Procedures and a supplemental table are
available at www.current-biology.com/cgi/content/full/14/19/1778/
DC1/.
Acknowledgments
We thank Frank Uhlmann for communicating unpublished observa-
tions. We thank Jan Löwe and Kim Nasmyth for exchanging manu-
scripts prior to publication. We thank Toni Meinhart and the staffs
at the Swiss Light Source and European Synchrotron Radiation
Facility for help with data collection. We thank Harald Dürr for help
with data processing and phasing. We thank members of the
Hopfner lab for discussion. K.P.H. is supported by grant HO2489/
1-1 from the Deutsche Forschungsgemeinschaft and by the Young
Investigator Award from the European Molecular Biology Organi-
zation.
Received: August 23, 2004
Revised: August 23, 2004
Accepted: August 23, 2004
Published online: September 30, 2004
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Accession Numbers
Coordinates for the nucleotide-free and ATP bound SMC ABC do-
mains have been deposited at the Protein Data Bank (http://www.
rcsb.org/pdb/) under ID codes 1XEW and 1XEX, respectively.