Summary
We review here the membrane transport studies that have appeared for the red cells of hagfishes Myxine glutinosa and Eptatretus stoutii. In the first part the transport of substrates of energy metabolism across the red blood cell membrane is considered. Hagfish red cells possess highly efficient transport systems for glucose, pyruvate and several amino acids. In the case of glucose, this property may be related to the animal’s hypoxia tolerance and its capacity for anaerobic glycolysis. Transport systems for small inorganic ions include the Na+, K+-ATPase and a K+-C1- symport requiring the presence of Na+. A striking feature is the absence of a Cl--HCO3 --exchanger, which constitutes in almost all red cells, except those of hagfishes and lampreys, the major pathway for Cl- and for HCO3 -. Consequently, Cl- permeability in hagfish red cells is orders of magnitude lower than in mammalian and most other red cells. We report our mass spectrometric determinations of hagfish red blood cell permeability for HCO3 - and find its value to be not significantly different from zero. This implies that CO2 transport in hagfish blood operates quite differently from that in the blood of most other species. Hagfish red cells, due to the presence of intracellular haemoglobin and carbonic anhydrase, can rapidly convert the CO2 taken up to HCO3 - and H+, but they cannot transfer most of the HCO3 - to the plasma, as red cells of most species do.
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References
Albers, C. and Goetz, K.G. (1985) H+ and Cl- ion equilibrium across the red cell membrane in the carp. Respiration Physiology, 61(2), 209–219.
Bauer, C., Engels, U. and Paleus, S. (1975) Oxygen binding to haemoglobins of the primitive vertebrate Myxine glutinosa L. Nature, 256(5512), 66–68.
Berglund, L., Carlsson, U. and Kjellstroem, B. (1980) Cyclostome carbonic anhydrase. Purification and some properties of the enzyme from erythrocytes of lamprey. Acta Chemica Scandinavica, Series B: Organic Chemistry and Biochemistry, 34(3), 227–228.
Boutilier, R.G. and Ferguson, R.A. (1989) Nucleated red cell function: metabolism and pH regulation. Canadian Journal of Zoology, 67, 2986–2993.
Brahm, J. (1977) Temperature-dependent changes of chloride transport kinetics in human red cells. Journal of General Physiology, 70, 283–306.
Brill, S.R., Musch, M.W. and Goldstein, L. (1992) Taurine efflux, band 3, and erythrocyte volume of the hagfish (Myxine glutinosa) and lamprey (Petromyzon marinus). Journal of Experimental Zoology, 264, 19–25.
Carlsson, U., Kjellström, B. and Antonsson, B. (1980) Purification and properties of cyclostome carbonic anhydrase from erythrocytes of hagfish. Biochimica et Biophysica Acta, 612, 160–170.
Cholette, C. and Gagnon, A. (1973) Isosmotic adaptation in Myxine glutinosa L. — II. Variations of the free arnino acids, trimethylamine oxide and potassium of the blood and muscle cells. Comparative Biochemistry and Physiology A —Comparative Physiology, 45A(4), 1009–1021.
Deuticke, B., Rickert, I. and Beyer, E. (1978) Stereoselective, SH-dependent transfer of lactate in mammalian erythrocytes. Biochimica et Biophysica Acta, 507, 137–155.
Ellory, J.C. and Wolowyk, M.W. (1991) Evidence for bumetanide-sensitive, Na+-dependent, partial Na-K-Cl co-transport in red blood cells of a primitive fish. Canadian Journal of Physiology and Pharmacology, 69, 588–591.
Ellory, J.C., Wolowyk, M.W., and Young, J.D. (1987) Hagfish (Eptatretus stoutii) erythrocytes show minimal chloride transport activity. Journal of Experimental Biology, 129, 377–383.
Evans, D.H. (1984) Gill Na+/H+ and Cl-/HCO3-exchange systems evolved before the vertebrates entered fresh water. Journal of Experimental Biology, 113, 465–469.
Fincham, D.A., Wolowyk, M.W. and Young, J.D. (1990) Characterisation of amino acid transport in red blood cells of a primitive vertebrate, the Pacific hagfish (Eptatretus stoutii). Journal of Experimental Biology, 154, 355–370.
Fincham, D.A., Wolowyk, M.W. and Young, J.D. (1991) Nucleoside uptake by red blood cells from a primitive vertebrate, the Pacific hagfish (Eptatretus stoutii), is mediated by a nitrobenzylthioinosine-insensitive transport system. Biochimica et Biophysica Acta, 1069(1), 123–126.
Gorkin, A.A. (1970) In-vitro uptake of amino-acids by erthrocytes of the hagfish Eptatretus stoutii. Physiologist, 13(3), 210.
Gros, G. (1991) Mechanisms of CO2 transport in vertebrates. Verhandlungen der Deutschen Zoologischen Gesellschaft, 84, 213–230.
Heming, T.A., Randall, D.J., Boutilier, R.G. et al. (1986) Ionic equilibria in red blood cells of rainbow trout (Salmo gairdneri): Cl-, HCO3 - and H+. Respiration Physiology, 65, 223–234.
Ingermann, R.L., Hall, R.E., Bissonette et al. (1984) Monosaccharide transport into erythrocytes of the Pacific hagfish Eptatretus stoutii. Molecular Physiology, 6(5-6), 311–320.
Ingermann, R.L., Bissonnette, J.M. and Hall, R.E. (1985) Sugar uptake by red blood cells, in Circulation, Respiration, and Metabolism. Current Comparative Approaches (ed. R. Gilles), Springer-Verlag, Berlin, Heidelberg, New York, Tokyo, pp. 290–300.
Itada, N. and Forster, R.E. (1977) Carbonic anhydrase activity in intact red blood cells measured with 18O exchange. Journal of Biological Chemistry, 252(11), 3881–3890.
Jacobs, M.H. and Stewart, D.R. (1942) The role of carbonic anhydrase in certain ion exchanges involving the erythrocyte. Journal of General Physiology, 25, 539–552.
Kaplan, M.A., Hays, L. and Hays, R.M. (1974) Evolution of a facilitated diffusion pathway for amides in the erythrocyte. American Journal of Physiology, 226, 1327–1332.
Macey, R.I. and Yousef, L.W. (1988) Osmotic stability of red cells in renal circulation requires rapid urea transport. American Journal of Physiology, 254, C669–74.
Mannuzzu, L.M., Moronne, M.M. and Macey, R.I. (1993) Estimate of the number of urea transport sites in erythrocyte ghosts using a hydrophobic mercurial. Journal of Membrane Biology, 133, 85–97.
Maren, T.H., Friedland, B.R. and Rittmaster, R.S. (1980) Kinetic properties of primitive vertebrate carbonic anhydrases. Comparative Biochemistry and Physiology B — Comparative Biochemistry, 67B, 69–74.
Nikinmaa, M. (1986) Red cell pH of lamprey Lampetra-fluviatilis is actively regulated. Journal of Comparative Physiology B — Biochemical Systemic and Environmental Physiology, 156(5), 747–750.
Nikinmaa, M. and Railo, E. (1987) Anion movements across lamprey (Lampetra fluviatilis) red cell membrane. Biochimica et Biophysica Acta, 899(1), 134–136.
Nikinmaa, M. and Tiihonen, K. (1994) Substrate transport and utilization in fish erythrocytes. Acta Physiologica Scandinavica, 152, 183–189.
Obaid, A.L., Critz, A.M. and Crandall, E.D. (1979) Kinetics of bicarbonate/chloride exchange in dogfish erythrocytes. American journal of Physiology, 273(3), R132–8.
Olives, B., Mattel, M.-G., Huet, M. et al. (1995) Kidd blood group and urea transport function of human erythrocytes are carried by the same protein. Journal of Biological Chemistry, 270, 15607–10.
Ohnishi, S.T. and Asai, H. (1985) Lamprey erythrocytes lack glycoproteins and anion transport. Comparative Biochemistry and Physiology B — Comparative Biochemistry, 81B(2), 405–408.
Sands, J.M., Gargus, J.J., Fröhlich, O. et al. (1992) Urinary concentrating ability in patients with Jk(a-b-) blood type who lack carrier-mediated urea transport. Journal of the American Society of Nephrology, 2, 1689–1696.
Tiihonen, K. and Nikinmaa, M. (1991) D-glucose permeability in river lamprey (Lampetra fluviatilis) and carp (Cyprinus carpio) erythrocytes. Comparative Biochemistry and Physiology, 100(3), 581–584.
Tiihonen, K. and Nikinmaa, M. (1993) Membrane permeability and utilization of L-lactate and pyruvate in carp red blood cells. Journal of Experimental Biology, 178, 161–172.
Tiihonen, K., Yao, S.Y.M., Nikinmaa, M. et al. (1993) Erythrocytes from the Pacific hagfish (Eptatretus stoutii) transport pyruvate by a concentrative Na+-dependent mechanism insensitive to inhibition by alpha-cyano-4-hydrox-ycinnamate. Biochemistry and Cell Biology, 71, Axv.
Tufts, B.L. and Boutilier, R.G. (1989) The absence of rapid chloride-bicarbonate exchange in lamprey erythrocytes: Implications for carbon dioxide transport and ion distribution between plasma and erythrocytes in the blood of Petromyzon marinus. Journal of Experimental Biology, 144, 565–576.
Tufts, B.L. and Boutilier, R.G. (1990a) CO2 transport in agnathan blood: evidence of erythrocyte Cl-/HCO3 - exchange limitations. Respiration Physiology, 80, 335–347.
Tufts, B.L. and Boutilier, R.G. (1990b) CO2 transport properties of the blood of a primitive vertebrate, Myxine glutinosa (L.). Experimental Biology, 48(6), 341–347.
Young, J.D., Yao, S.Y.-M., Tse, C.M. et al. (1994) Functional and molecular characteristics of a primitive vertebrate glucose transporter: studies of glucose transport by erythrocytes from the Pacific hagfish (Eptatretus stoutii). Journal of Experimental Biology, 186, 24–41.
Zhang, Z.H. and Solomon, A.K. (1992) Effect of pCMBS on anion transport in human red cell membranes. Biochimica et Biophysica Acta, 1106, 31–39.
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Peters, T., Gros, G. (1998). Transport of Bicarbonate, other Ions and Substrates Across the Red Blood Cell Membrane of Hagfishes. In: The Biology of Hagfishes. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5834-3_20
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DOI: https://doi.org/10.1007/978-94-011-5834-3_20
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