NMR Structure of the Thrombin-Binding
DNA Aptamer Stabilized by Sr
2+
http://www.jbsdonline.com
Abstract
The structure of thrombin-binding DNA aptamer complexed with a single Sr
2+
ion
(Sr
2+
:TBA complex) has been determined using NMR spectroscopy and restrained
molecular dynamics simulations. The quadruplex structure for the Sr
2+
:TBA complex is
similar in topology, but distinct in structure, from that previously reported for the
K
+
:TBA complex. The inter-tetrad distance of the Sr
2+
:TBA complex is 3.8 Å, or 0.7 Å
larger than in the K
+
:TBA complex. This substantial difference can be attributed to a dif-
ferent binding site for Sr
2+
in the Sr
2+
:TBA complex than for K
+
in the K
+
:TBA com-
plex. The Sr
2+
:TBA complex assumes a 1:1 stoichiometry, and it is very likely that the
Sr
2+
ion simultaneously interacts with the eight O6 atoms of the two G-tetrads. The
results indicate that quadruplex DNA structures are highly sensitive to the presence of
specific metal ions. The binding of specific metal ions may modulate the biological
activity of quadruplex DNA structures in vivo.
Introduction
The thrombin-binding DNA aptamer (TBA) is a 15mer DNA sequence that was
identified using the SELEX procedure as a DNA sequence that binds tightly to
thrombin (1). Aptamers are relatively short sequences of DNA (or RNA) that fold
into three-dimensional structures that have high affinity for a particular molecular
target (e.g., thrombin) (2, 3). Thrombin is an important protein that is involved in
the enzymatic cascade that results in blood clot formation. Inhibitors of thrombin,
such as the TBA, have potential therapeutic value (4). Folded structures of DNA
aptamers are essential for their biological activity. Therefore, structural studies are
important for understanding how DNA aptamers bind to their molecular targets.
NMR spectroscopy (5-11) and X-ray crystallography (12-14) have each been used
to determine the structure of the TBA. These studies have shown that the TBA
adopts an intramolecular quadruplex DNA structure in which eight of the nine dG
nucleotides form two G-tetrads that stack on one another (Figure 1).
DNA quadruplex structures are important components in cell biology where they
play an important role in the regulation of proto-oncogene transcription (15, 16)
and in the maintenance of DNA telomeres (17-21). Several studies have shown
that the biological function of DNA quadruplex structures is remarkably sensitive
to the presence of particular cations in solution. Thus, the NHE
III
element from the
c-myc proto-oncogene serves as a repressor of gene transcription by adopting a
quadruplex DNA structure in the presence of K
+
(15, 16). Model DNA telomere
sequences may form either intramolecular or intermolecular G-quadruplex struc-
tures depending on the presence of K
+
and/or Na
+
in the solution (22, 23). The
propensity for particular cations to stabilize G-quadruplex structures has been
attributed to the interior cavity of the G-quadruplex being preferentially occupied
Journal of Biomolecular Structure &
Dynamics, ISSN 0739-1102
Volume 22, Issue Number 1, (2004)
©Adenine Press (2004)
Xi-an Mao
1,§
Luis A. Marky
2
William H. Gmeiner
1,*
1
Department of Biochemistry
Wake Forest University School of Medicine
Winston-Salem, NC 27157-1016
2
Department of Pharmaceutical Sciences
University of Nebraska Medical Center
Omaha, NE 68198
§Present address
Cleveland Clinic
Cleveland, Ohio
(Mailing Address?)
1
*
Email: bgmeiner@wfubmc.edu