487
Acta Cryst. (1996). B52, 487-499
Hydrogen-Bond Patterns in 1,4-Dihydro-2,3-quinoxalinediones: Ligands for the Giycine
Modulatory Site on the NMDA Receptor
MACIEJ KUBICKI,t TERESAW. KINDOPP, MARIO V. CAPPARELLI~AND PENELOPEW. CODDING*
Departments of Chemistry and of Pharmacology and Therapeutics, University of Calgary, Calgary, Alberta, Canada
T2N 1N4
(Received 10 Januar 3' 1994; accepted 25 August 1995)
Abstract
The crystal structures of five 1,4-dihydro-2,3-quinoxali-
nediones, antagonists of the NMDA modulatory glycine
binding site on the excitary amino acid (EAA) receptor
complex, have been determined: (I) 6,7-dinitro-l,4-
dihydro-2,3-quinoxalinedione (DNQX); (II) 5,7-dinitro-
1,4-dihydro-2,3-quinoxalinedione (MNQX); (III) 6-nitro-
1,4-dihydro-2,3-quinoxalinedione hydrate; (IV) 6,7-di-
chloro-l,4-dihydro-2,3-quinoxalinedione; (V) 5,7-di-
chloro- 1,4-dihydro-2,3-quinoxalinedione dimethylform-
amide. The crystal structure of the most active
compound (II) contains a unique intramolecular
N--H...O(NO2) hydrogen bond, which may be impor-
tant for activity, as semiempirical calculations show that
this bond is stable over a wide range of dihedral angles
between the planes of the molecule and of the nitro
group. In the other compounds the intermolecular
hydrogen bonds connect molecules into three-dimen-
sional networks. In compounds (I), (III) and (IV) head-
to-tail :r-stacking is found between molecules connected
by a center of symmetry. The geometries of the
hydrogen-bonded --NH--C--O fragments show
evidence of zr-cooperativity or resonance-assisted
hydrogen bonding. Graph-set analysis of the hydrogen-
bond patterns of quinoxalinedione derivatives shows a
tendency to form two types of hydrogen-bonding motifs:
a centrosymmetric dimeric ring and an infinite chain.
Even though this pattern may be modified by the
presence of additional hydrogen-bond acceptors and/or
donors, as well as by solvent molecules, general
similarities have been found. Comparison of all quinox-
alinedione structures suggests that the hydrogen-bonding
pattern necessary for the biological activity at the glycine
binding site contains one donor and two acceptors.
1. Introduction
Quinoxalinedione (QD) derivatives have been found to
be highly potent antagonists in the excitary amino acid
(EAA) neurotransmission system and to act by binding to
tOn leave from Department of Chemistry, Adam Mickiewicz
UniversiW, 60-780 Poznafi, Poland.
~:Present address: Escuela de Quimica, Universidad Central de
Venezuela, Caracas 1051. Venezuela.
© 1996 Intemational Union of Crystallography
Printed in Great Britain - all rights reserved
the glycine modulatory site of the NMDA (N-methyl-D-
aspartic acid) receptor, as well as to other excitatory
receptor subtypes (Honor6 et al., 1988; Randle et al.,
1992). EAA receptors are part of a supramolecular
complex that forms a ligand-gated ion channel. The
NMDA receptor requires both glutamate and glycine for
activity; agonists and antagonists for these two sites are
potential therapies for epilepsy, learning disorders and
ischemic damage (Kemp & Lesson, 1993; Reynolds &
Miller, 1990). For this reason, extensive structural studies
of the QD derivatives have been performed. Structural
analysis identifies three important features for biological
action: the hydrogen-bonding pattern, the distribution of
charge throughout the molecule and steric factors
(Kubicki & Codding, 1993; Kubicki, Kindopp,
Capparelli & Codding, 1992). To obtain further insight
into these features, we have extended the studies to three
nitro and two chloro derivatives. The nitro derivatives are
important, because a small structural change from
6,7-dinitro-QD (DNQX; hereinafter the basic molecule,
1,4-dihydro-2,3-quinoxalinedione, will be referred to as
QD) to 5,7-dinitro-QD (MNQX) reduces the affinity of
the compounds for the nonNMDA receptors fourfold, but
increases the antagonistic activity at the glycine site 30-
fold (Watkins, Krogsgaard-Larsen & Honorr, 1989;
Randle et al., 1992). IC50 values measure the concentra-
tion required to inhibit the binding of the natural ligand,
glycine, by 50%. The IC50 value for (I) is ca 4.5 ~tM, for
(II) is 0.14 I.tM, for (III) is ca 27 l.tM, and for (IV) and (V)
is 4 l.tM (Pullan, 1991 ). Thus, (II) is the most active of the
RI
15 i
R2 ' ~ O3
R 3 7 g "~ N 0 2
8 I.l
H
(I) R2 = R 3 = NO 2, R I = H
(II) R 1 =R 3 =NO,,,R 2=H
(III) R 2 = NO 2, R t = R 3 = H
(IV) R 2=R 3 =CI, R 1 =H
(W) R t = R 3 = CI, R 2 = H
Acta CrystallographicaSection B
ISSN 0108-7681 © 1996