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Acta Cryst. (1992). B48, 281-285
The Sensitivity of the Synchrotron Laue Method to Small Structural Changes:
Binding Studies of Human Carbonic Anhydrase II (HCAII)
BY M. LXNDAHL AND A. LILJAS
Department of Molecular Biophysics, Chemical Center, University of Lund, Box 124, S 221 00 Lund, Sweden
J. HABASH AND S. HARROP
Department of Chemistry, University of Manchester, Manchester M13 9PL, England
AND J. R. HELLIWELL
Department of Chemistry, University of Manchester, Manchester M13 9PL, England, and
SERC Daresbury Laboratory, Daresbury, Warrington WA4 4AD, England
(Received 16 January 1991; accepted 18 November 1991)
Abstract
Human carbonic anhydrase II has been studied using
Laue crystallography and short exposure times
(3-20 s) at the Daresbury Synchrotron Radiation
Source (SRS). Two types of crystals were investi-
gated, the enzyme in complex with the inhibitor
bisulfite and the enzyme at pH 6.0. A bisulfite ion
and a water molecule, respectively, are bound with
tetrahedral coordination to the zinc ion. These
results have been subsequently confirmed by mono-
chromatic methods. Synchrotron Laue crystallogra-
phy is evidently able to characterize minor structural
differences.
Introduction
The zinc enzyme carbonic anhydrase is widely spread
among living organisms and at least seven genetically
distinct isoenzymes are known in mammals (Tashian,
1989). The isoenzyme II is a high activity form, the
structure of which is known (Liljas et al., 1972) and
well refined (Eriksson, Jones & Liljas, 1988). The
enzyme is inhibited by a number of inorganic ions as
well as by sulfonamides (Lindskog et al., 1984).
Extensive spectroscopic investigations of Co 2÷-
substituted carbonic anhydrases and crystallo-
graphic studies of the native enzyme have indicated
that the coordination of the metal varies depending
on the pH and the type of ligand (Lindskog, 1963;
Bertini & Luchinat, 1982; Eriksson, Jones & Liljas,
1988; Vidgren, Liljas & Walker, 1990). This is in
agreement with EXAFS studies of the Co 2÷ enzyme
(Yachandra, Powers & Spiro, 1983). The cobalt elec-
tronic absorption spectrum of the enzyme when
inhibited by thiocyanate is interpreted as originating
from a penta-coordinated metal (Bertini & Luchinat,
1982). This has been confirmed by crystallographic
0108-7681/92/030281-05506.00
methods on the zinc enzyme (Eriksson, Kylsten,
Jones & Liljas, 1988). In addition to the three histi-
dine ligands the inhibitor occupies a fourth and a
water molecule a fifth coordination position.
We wanted to extend these studies of penta-
coordinated zinc in carbonic anhydrase in order to
further elucidate the structure and function of the
enzyme. At the same time we wanted to test the
potential of Laue crystallography to observe small
details in electron density which is a prerequisite to
time-resolved protein crystallography. In contrast to
the spectroscopic observations of the Co 2÷ enzyme
we have observed that the zinc ion of the crystallized
enzyme is tetra-coordinated in complex with bisulfite
as well as at pH 6.0 where a water molecule is
situated at the fourth coordination site. Interestingly,
EXAFS studies of Zn 2+ carbonic anhydrase found
that the average coordination number seems
independent of pH, or of inhibitor binding, and is
judged to be four (Yachandra et al., 1983).
Experimental
Crystals of human carbonic anhydrase II with space
group P21, cell parameters a = 42.7, b--41.7, c =
73.0~, fl = 104.6 °, were grown, complexed with
Hg 2+, in 2.3M (NH4)2SO4 at pH 8.5. Soaking
experiments with the crystals are summarized in
Table 1. Diffraction data were collected at 293 K on
experimental stations 9.6 and 9.7 at the Daresbury
Synchrotron Radiation Source (SRS), using poly-
chromatic (Laue) radiation in the interval 0.40-2.6 )~
on stations 9.6 and 9.7. Data were extended to a
resolution of 2.2 A and were sampled with a com-
pleteness of 55-70% (Table 2).
The crystals were elongated plates in morphology
and were mounted with the a axis approximately
© 1992 International Union of Crystallography