The bicarbonate permeability of the plasma membrane of intact hagfish (Myxine glutinosa) red blood cells and the intracellular carbonic anhydrase activity of these cells were determined by applying the (18)O exchange reaction using a special mass spectrometric technique. When the macromolecular carbonic anhydrase inhibitor Prontosil-Dextran was used to suppress any extracellular carbonic anhydrase activity, the mean intracellular acceleration of the CO(2) hydration/HCO(3)(−) dehydration reaction over the uncatalyzed reaction (referred to as intracellular carbonic anhydrase activity A(i)) was 21 320+/−3000 at 10 degrees C (mean +/− s.d., N=9). The mean bicarbonate permeability of the red blood cell membrane (P(HCO3)-) was indistinguishable from zero. It can be concluded that CO(2) transport within hagfish blood does not follow the classical scheme of CO(2) transport in vertebrate blood. It is suggested that the combination of considerable intraerythrocytic carbonic anhydrase activity and low P(HCO3)- may serve to enhance O(2) delivery to the tissue in the exceptionally hypoxia-tolerant hagfish.

Brill
S. R.
,
Musch
M. W.
,
Goldstein
L.
(
1992
).
Taurine efflux, band 3 and erythrocyte volume of the hagfish (Myxine glutinosa) and lamprey (Petromyzon marinus)
.
J. Exp. Zool
264
,
19
–.
Carlsson
U.
,
Kjellström
B.
,
Antonsson
B.
(
1980
).
Purification and properties of cyclostome carbonic anhydrase from erythrocytes of hagfish
.
Biochim. Biophys. Acta
612
,
160
–.
Ellory
J. C.
,
Wolowyk
M. W.
,
Young
J. D.
(
1987
).
Hagfish (Eptatretus stouti) erythrocytes show minimal chloride transport activity
.
J. Exp. Biol
129
,
377
–.
Fago
A.
,
Malte
H.
,
Dohn
N.
(
1999
).
Bicarbonate binding to hemoglobin links oxygen and carbon dioxide transport in hagfish
.
Respir. Physiol
115
,
309
–.
Forster
M. E.
(
1990
).
Confirmation of the low metabolic rate of hagfish
.
Comp. Biochem. Physiol
96
,
113
–.
Geers
C.
,
Gros
G.
,
Gärtner
A.
(
1985
).
Extracellular carbonic anhydrase of skeletal muscle associated sarcolemma
.
J. Appl. Physiol
59
,
548
–.
Glomski
C. A.
,
Tamburlin
J.
,
Chainani
M.
(
1992
).
The phylogenetic odyssey of the erythrocyte. III. Fish, the lower vertebrate experience
.
Histol. Histopath
7
,
501
–.
Gros
G.
,
Moll
W.
(
1971
).
The diffusion of carbon dioxide in erythrocytes and hemoglobin solutions
.
Pflugers Arch
324
,
249
–.
Harned
H. S.
,
Bonner
F. T.
(
1945
).
The first ionization of carbonic acid in aqueous solution of sodium chloride
.
J. Am. Chem. Soc
67
,
1026
–.
Hastings
A. B.
,
Sendroy
J.
(
1925
).
The effect of variation in ionic strength on the apparent first and second dissociation constant of carbonic acid
.
J. Biol. Chem
65
,
445
–.
Ho
C.
,
Sturtevant
J. M.
(
1963
).
The kinetics of the hydration of carbon dioxide at 25deg
.
J. Biol. Chem
238
,
3499
–.
Itada
N.
,
Forster
R. E.
(
1977
).
Carbonic anhydrase activity in intact red blood cells measured with 18O exchange
.
J. Biol. Chem
252
,
3881
–.
Maren
T. H.
,
Friedland
B. R.
,
Rittmaster
R. S.
(
1980
).
Kinetic properties of primitive vertebrate carbonic anhydrases
.
Comp. Biochem. Physiol
67
,
69
–.
Mills
G. A.
,
Urey
H. C.
(
1940
).
The kinetics of isotopic exchange between carbon dioxide, bicarbonate ion, carbonate ion and water
.
J. Am. Chem. Soc
62
,
1019
–.
Munz
F. W.
,
Morris
R. W.
(
1965
).
Metabolic rate of the hagfish, Eptatretus stoutii
.
Comp. Biochem. Physiol
16
,
1
–.
Norris
F. A.
,
Powell
G. L.
(
1992
).
Characterization of CO2/carbonic acid mediated proton flux through phosphatidylcholine vesicles as model membranes
.
Biochim. Biophys. Acta
1111
,
17
–.
Sanyal
G.
,
Maren
T. H.
(
1981
).
Thermodynamics of carbonic anhydrase catalysis
.
J. Biol. Chem
256
,
608
–.
Smith
K. L.
,
Hessler
R. R.
(
1974
).
Respiration of benthopelagic fishes: in situ measurements at 1230m
.
Science
184
,
72
–.
Tufts
B. L.
,
Boutilier
R. G.
(
1990
).
CO2transport in agnathanblood: evidence of erythrocyte Cl/HCO3 exchange limitations
.
Respir. Physiol
80
,
335
–.
Tufts
B. L.
,
Boutilier
R. G.
(
1990
).
CO2transport properties of a primitive vertebrate, Myxine glutinosa (L.)
.
Exp. Biol
48
,
341
–.
Tufts
B. L.
,
Vincent
C. J.
,
Currie
S.
(
1998
).
Different red blood cell characteristics in a primitive agnathan (M. glutinosa) and a more recent teleost (O. mykiss) influence their strategies forblood CO2transport
.
Comp. Biochem. Physiol
119
,
533
–.
Wells
R. M. G.
,
Forster
M. E.
,
Davidson
W.
,
Taylor
H. H.
(
1986
).
Blood oxygen transport in the free swimming hagfish, Eptatretus cirrhatus
.
J. Exp. Biol
123
,
43
–.
Wissbrun
K. F.
,
French
D. M.
,
Patterson
A.
Jr.
(
1954
).
The true ionization constant of carbonic acid in aqueous solution from 5 to 45deg
.
J. Phys. Chem
58
,
693
–.
This content is only available via PDF.