The enzyme carbonic anhydrase (CA) (EC 4.2.2.1.) is a
catalyst of the reversible hydration of carbon dioxide to
bicarbonate ions and protons (Maren, 1967). Carbonic
anhydrase isozymes exhibit distinct differences in activity,
tissue specificity and cellular localisation (Sly and Hu, 1995).
Intraerythrocytic CA I and especially CA II are known to play
an important role in the transport of CO
2
by blood (Klocke,
1988). Discussion continues as to whether CA IV, a
membrane-bound carbonic anhydrase isozyme which, among
other localizations, is present on the plasma face of vascular
endothelium (Sender et al., 1998), significantly accelerates
the efflux of CO
2
from tissue, e.g. from working skeletal
muscle (Geers et al., 1997; Geers and Gros, 2000; Henry et
al., 1997b) and, therefore, contributes to CO
2
transport within
the body. Thus, it seems puzzling that both the plasma and
serum of diverse vertebrate species including mammals, but
not man and birds, have been shown to have an inhibitory
effect on carbonic anhydrase (Booth, 1938; Haswell and
Randall, 1976; Haswell et al., 1983; Henry et al., 1997a;
Hill, 1986; Leiner et al., 1962; Maetz, 1956; Rispens et al.,
1985).
We aimed to identify any inhibitor of carbonic anhydrase
present in the plasma of the European flounder Platichthys
flesus and to determine its inhibitory properties and its
molecular mass. A major purpose of the study was to
investigate whether the serum of the flounder reduces the
catalytic activity of carbonic anhydrase while the enzyme is
enclosed in red blood cells.
Materials and methods
European flounder (Platichthys flesus) with a mean body
mass of 200 g were caught in the Baltic Sea off Eckernfoerde,
Germany. Live fish were brought to shore on the day of catch.
Blood used for the preparation of serum and haemolysate was
collected the same day, and red blood cell suspensions were
prepared from blood samples taken from flounders that had
been transported to our institute and kept in tanks filled with
aerated artificial sea water. The continuously purified water
had a temperature of 12–14 °C. The photoperiod was 12 h:12 h
light:dark. The captive fish refused food. They were kept in the
tanks for a maximum of 6 weeks before blood samples were
taken.
Fish were anaesthetised in a solution of 0.02 % (w/v)
metacaine (3-aminobenzoic acid ethyl ester-methanesulphonate,
Sigma) in sea water. Subsequently, each fish was given an
intraperitoneal injection of 500 i.u. of heparin (Liquemin,
Roche) and was then returned to the metacaine solution. After
some minutes, animals were taken out again, sponged dry and
bled by cutting off the caudal fin. One flounder yielded
approximately 3 ml of blood.
Blood was collected in 1.5 ml Eppendorf tubes containing
3003 The Journal of Experimental Biology 203, 3003–3009 (2000)
Printed in Great Britain © The Company of Biologists Limited 2000
JEB2846
The blood serum of the European flounder Platichthys
flesus strongly inhibits soluble erythrocytic carbonic
anhydrase from the same species. The inhibition is of the
uncompetitive type. Hence, the mechanism of the carbonic
anhydrase inhibition is different from that of all other
known carbonic anhydrase inhibitors. The serum showed
no inhibitory effect on carbonic anhydrase from human
and bovine red blood cells. By applying the
18
O exchange
reaction, it could be demonstrated that the presence of the
carbonic anhydrase inhibitor in the extracellular fluid has
no effect on carbonic anhydrase in intact red blood cells.
Thus, this carbonic anhydrase inhibitor seems to act
only within the plasma space of the circulatory system.
However, the carbonic anhydrase inhibitor does appear to
reduce the bicarbonate permeability of flounder red cells
to approximately one-quarter of normal levels as measured
by the
18
O exchange reaction. The 28 kDa carbonic
anhydrase inhibitor was isolated from the serum by gel
filtration. The isolated inhibitor was detected in acrylamide
gels as a single band representing a 7 kDa protein. The
denaturing conditions used in electrophoresis presumably
led to a dissociation of the native protein into subunits.
Key words: blood CO2 transport, fish, uncompetitive enzyme
inhibition, red blood cell,
18
O exchange reaction, European flounder,
Platichthys flesus.
Summary
Introduction
PROPERTIES OF A CARBONIC ANHYDRASE INHIBITOR PROTEIN IN
FLOUNDER SERUM
THOMAS PETERS*, FRAUKE PAPADOPOULOS, HANS-PETER KUBIS AND GEROLF GROS
Zentrum Physiologie, Medizinische Hochschule Hannover, Carl-Neuberg-Strasse 1, D-30623 Hannover, Germany
*e-mail: Peters.Thomas@mh-hannover.de
Accepted 11 July; published on WWW 7 September 2000