Molecular Diversity, 7: 15–23.
KLUWER/ESCOM
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
15
Full paper
Normal coordinate structural decomposition of the heme distortions of
hemoglobin in various quaternary states and bound to allosteric effectors
Monique Laberge
1
, Takashi Yonetani
2
& Judit Fidy
1*
1
Institute of Biophysics and Radiation Biology, Semmelweis University, Puskin u. 9, Budapest H-1088, Hungary;
2
Department of Biochemistry and Biophysics, Johnson Research Foundation, University of Pennsylvania,
Philadelphia, PA 19104–6059
(
*
Author for correspondence, E-mail: judit@puskin.sote.hu, phone: 36-1-267-6261, fax: 36-1-266-6656)
Received 20 March 2003; Accepted 29 May 2003
Key words: allosteric effectors, cooperativity, hemoglobin, normal coordinate structural decomposition
Summary
The distortions of the α
1
, α
2
, β
1
, and β
2
hemes of human hemoglobin (HbA) in various quaternary states and
as affected by the presence of allosteric effectors was investigated by subjecting CHARMM energy-minimized
models to normal coordinate structural decomposition (NSD) analysis. NSD was applied to the individual hemes
extracted from the R, T, and R2-state models of HbA and to HbA bound to DPG and to IHP. Overall, NSD results
are indicative of characteristic distortions, not only for the hemes of the different HbA quaternary states, but also
for the hemes of the HbA models bound to allosteric effectors. Comparing the distortions of the inequivalent α and
β hemes in T-state HbA, we show good correlation between NSD and the experimentally observed low-frequency
ν
52
(E
g
) and γ
7
(A
2u
) modes reported in the literature for α and β HbA hemes while noting substantial differences
between these types for B
2u
and B
1u
distortions. For the R2 hemes, NSD yields heme distortions that are more
comparable to those of the R-state, especially in magnitude. However, the R2 hemes do not exhibit inequivalence of
α and β heme distortions, a result that may contribute to an understanding of the functional importance of this state.
Relative to T-state heme distortions, NSD results on the effector-bound hemes show that tertiary changes induced
in T-state HbA as a result of binding DPG and IHP drastically affect heme distortions. In the α hemes extracted
from the HbA-DPG model, most noteworthy are the increased wav(x) and wav(y) distortions and enhancement of
ruf and dom deformations. In the β hemes, the wav(y) is the most affected distortion with increase in sad. The NSD
results are also different for the hemes of the HbA-IHP model, in that the β sad and ruf deformations are more
enhanced with increase of doming in the α hemes. Our results describe the effect of the subtle protein-induced
changes on the nonplanarity of the HbA hemes that may play a role in the regulation of their oxygen affinity.
Abbreviations: DPG, 2,3-diphosphoglycerate; EM, energy minimization; HbA, human adult hemoglobin; IHP,
inositol hexaphosphate; ip, in-plane; NMA, normal coordinate analysis; NSD, normal structural decomposition;
oop, out-of-plane
Introduction
Human adult hemoglobin (HbA) is a tetrameric hemo-
globin consisting of two α-subunits and two β -
subunits arranged as symmetrical αβ dimers. Each
dimer consists of an α-chain with 141 residues and
a β -chain with 146 residues, with one heme group
per subunit. The hemes are located between the E
and F helices of each monomer and stabilized by an
H-bonding network [1]. In the T-state, the iron is five-
coordinate with ligation to four porphyrin N-atoms
and to the N of an F-helix histidine located on the
proximal side of the heme. In the R-state, oxygen
binds on the distal side as a 6th ligand to the iron.