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Facilitation of maternal-fetal oxygen transfer in fishes: Anatomical and molecular specializations

  • Chapter
Respiration and metabolism of embryonic vertebrates

Part of the book series: Perspectives in vertebrate science ((PIVS,volume 3))

Abstract

Oxygen transfer in viviparous vertebrates is facilitated by the close proximity of fetal and maternal circulatory systems. Among the fishes, facilitation is accomplished by a remarkable diversity of maternal-fetal anatomical specializations. Maternal-fetal O2 transfer is further enhanced by a fetal blood which has a higher O2 affinity than that of the adult. The diversity of anatomical specializations suggests that there may be a similar variety of molecular specializations as well to ensure a relatively high fetal blood O2 affinity. Study of adult and fetal bloods of the seaperch, Embiotoca lateralis have shown that fetal blood has a higher O2 affinity than that of the adult. It appears that the E. lateralis fetus utilizes a different hemoglobin and a lower organic phosphate concentration to ensure this higher blood O2 affinity; a lower mean corpuscular hemoglobin concentration may contribute to the higher O2. affinity as well. A higher fetal than adult O2 affinity of whole blood exists in at least some sharks. The molecular basis for such affinity differences also appears to involve different fetal and adult hemoglobins; different intraerythrocytic organic phosphate concentrations may contribute as well. However, further studies are required to clarify the molecular basis of the facilitation of maternal-fetal O2 transfer in the fishes.

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References

  • Amoroso, E.C. (1960). Viviparity in Fishes. Symp. Zool. Soc. (Land.) 1: 153–181.

    Google Scholar 

  • Bard, H. and Teasdale, F. (1979). Red cell oxygen affinity. hemoglobin type, 2,3-diphosphoglycerate, and pH as a function of fetal development. Pediatrics 64: 483–487.

    PubMed  CAS  Google Scholar 

  • Bartlett, G.R. (1978). Water-soluble phosphates of fish red cells. Can. J. Zool. 56: 870–877.

    Article  CAS  Google Scholar 

  • Bartlett, G.R. (1980). Phosphate compounds in vertebrate red blood cells. Am. Zool. 20: 103–114.

    CAS  Google Scholar 

  • Bartlett, G.R. (1982). Phosphate compounds in red cells of two dogfish sharks: Squalus acanthias and - Mustelus cants. Comp. Biochem. Physiol. 73A: 135–140.

    Article  Google Scholar 

  • Bauer, C., Ludwig, I. and Ludwig, M. (1968). Different effects of 2,3-diphosphoglycerate and adenosine triphosphate on the oxygen affinity of adult and fetal human haemoglobin. Life Sci. 7: 1339–1343.

    Article  CAS  Google Scholar 

  • Bauer, C., Jelkmann, W. and Moll, W. (1981). High oxygen affinity of maternal blood reduces fetal weight in rats. Respir. Physiol. 43: 169–178.

    Article  PubMed  CAS  Google Scholar 

  • Baumann, R. Bauer, C. and Ratschlag-Schaefer, A.M. (1972). Causes of the postnatal decrease of blood oxygen affinity in lambs. Respir. Physiol. 15: 151–158.

    Article  PubMed  CAS  Google Scholar 

  • Bellingham, A.J., Detter. J.C. and Lenfant, C. (1971). Regulatory mechanisms of hemoglobin oxygen affinity in acidosis and alkalosis. J. Clin. Invest. 50: 700–706.

    Article  PubMed  CAS  Google Scholar 

  • Benesch. R. and Benesch. R.E. (1967). The effect of organic phosphates from the human erythrocyte on the allosteric properties of hemoglobin. Biochem. Biophys. Res. Comm. 26: 162–167.

    Article  PubMed  CAS  Google Scholar 

  • Benesch, R. and Benesch. R.E. (1969). Intracellular organic phosphates as regulators of oxygen release by haemoglobin. Nature 221: 618–622.

    Article  PubMed  CAS  Google Scholar 

  • Blake, J. (1867). On the nourishment of the foetus in embiotocid fishes. Proc. Calif. Acad. Nat. Sci. 3: 314–317.

    Google Scholar 

  • Blunt, M.II., Kitchen, J.L.. Mayson, S.M. and Huisman, T.H.J. (1971). Red cell 2,3-diphosphoglycerate and oxygen affinity in newborn goats and sheep. Proc. Soc. Exp. Biol. Med. 138: 800–803.

    PubMed  CAS  Google Scholar 

  • Bunn, H.F. and Kitchen, H. (1973). Hemoglobin function in the horse: the role of 2,3-diphospho-glycerate in modifying the oxygen affinity of maternal and fetal blood. Blood 42: 471–479.

    PubMed  CAS  Google Scholar 

  • Chanutin, A. and Curnish. R.R. (1967). Effect of organic and inorganic phosphates on the oxygen equilibrium of human erythrocytes. Arch. Biochem. Biophys. 121: 96–102.

    Article  PubMed  CAS  Google Scholar 

  • Coates, M.L. (1975). hemoglobin function in the vertebrates: an evolutionary model J. Mol. Evol. 6: 285–307.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, D. and Wourms, J.F. (1976). Microhrotula randalli, a new viviparous Ophidioid fish from Samoa and New Hebrides, whose embryos hear trophotaeniae Proc. Biol. Soc. Wash. 86: 339–350.

    Google Scholar 

  • De Simone, J and Mueller, A.L. (1979). Fetal hemoglobin (HbF) synthesis in baboons, Papio cvnocephalus. Analysis of fetal and adult hemoglobin synthesis during fetal development, Blood, 53: 19–27.

    PubMed  Google Scholar 

  • De Verdier, C.H. and Garhy, L. (1969). Low binding of 2,3-diphosphoglycerate to haemoglobin F. A contribution to the knowledge of the binding site and an explanation for the high oxygen affinity of foetal blood. Scand. J. Clin. L.ah. Invest. 23: 149–151.

    Article  Google Scholar 

  • Dhindsa, D.S., Hoversland, A.S. and Templeton, J.W. (1972). Postnatal changes in oxygen affinity and concentration of 2.3-diphosphoglycerate in dog blood. Biol. Neonate 20: 226–235.

    Article  PubMed  CAS  Google Scholar 

  • Duhm,.I. (1971). Effects of 2.3-diphosphoglycerate and other organic phosphate compounds on oxygen affinity and intracellular pH of human erythrocytes. Pflügers Arch. 326: 341–356.

    Article  PubMed  CAS  Google Scholar 

  • Duhm, J. (1976). Dual effect of 2.3-diphosphoglycerate on the Bohr effects of human blood. Pflügers Arch. 363: 55–60.

    Article  PubMed  CAS  Google Scholar 

  • Eigenmann, C.H. (1982). Cymatogaster aggregatus Gibbons. A contribution to the ontogeny of viviparous fishes. Bull. U.S. Fish. Comm. 12: 401–478.

    Google Scholar 

  • Forster, R.E. (1972). The effects of dilution in saline on the oxygen affinity of human hemoglobin. In: Oxygen Affinity of Hemoglobin and Red Cell Acid Base Status, M. Rorth and P. Astrup, eds., Alfred Benzon Symposium IV-Copenhagen, 1971. Academic Press, New York, pp. 162–165.

    Google Scholar 

  • Fyhn, U.E.H. and Sullivan, B. (1975). Elasmobranch hemoglobins: dimerization and polymerization in various species. Comp. Biochem. Physiol. 50B: 119–129.

    Google Scholar 

  • Garlick, R.L., Davis, B.J., Farmer, F. Fyhn, H.J., Fyhn, U.E.H., Noble, R.W. Powers D.A., Riggs, A. and Weber, R.E. (1979). A fetal-maternal shift in the oxygen equilibrium of hemoglobin from the viviparous caecilian. Tv’phlonectes compressicuuda. Comp. Biochem. Physiol. 62A: 239–244.

    CAS  Google Scholar 

  • Gilbert, P.W. and Schlernitzauer. D.A. (1966). The placenta and gravid uterus of Carcharhinus falciformis. Copeia 1966: 451–457.

    Article  Google Scholar 

  • Gillen, R.G. and Riggs, A. (1971). The hemoglobins of a freshwater teleost Cichlasoma cyanoquttatum: The effects of phosphorylated organic compounds upon oxygen equilibria. Comp. Biochem. Physiol. 38B: 585–595.

    Google Scholar 

  • Grigg, G.C. and Harlow, P. (1981). A fetal-maternal shift of blood oxygen affinity in an Australian viviparous lizard. Sphenoniorphus quoyü (Reptilia, Scincidae). J. Comp. Physiol. 142: 495–499.

    CAS  Google Scholar 

  • Hart, J.L. (1973). Pacific Fishes of Canada. Bulletin 180, Fisheries Research Board of Canada, Ottawa.

    Google Scholar 

  • Hjorth, J.P. (1974). Genetics of Zoarces populations. VII. Fetal and adult hemoglobins and a polymorphism common to both. Hereditas 78: 69–72.

    Article  PubMed  CAS  Google Scholar 

  • Hoar, W.S. (1969). Reproduction. In: Fish Physiology. Vol. 3. W.S. Hoar and D.J. Randall, eds., Academic Press, New York. pp. 1–72.

    Google Scholar 

  • Hoffmann, E.K. (1977). Control of cell volume. In: Transport of Ions and Water in Animals. B.L. Gupta, R.B. Moreton, J.L. Oxchman and B.J. Wall, eds., Academic Press, London, pp. 285–332.

    Google Scholar 

  • Ingermann, R.L. and Terwilliger. R.C. (1981a). Oxygen affinities of maternal and fetal hemoglobins of the viviparous seaperch, Embiotoca lateralis. J. Comp. Physiol.142: 523–531.

    CAS  Google Scholar 

  • Ingermann, R.L. and Terwilliger, R.C. (1981b). Intraerythrocytic organic phosphates of fetal and adult seaperch (Embiotoca lateralis): their role in maternal-fetal oxygen transport. J. Comp. Physiol. 144: 253–259.

    CAS  Google Scholar 

  • Ingermann, R.L. and Terwilliger, R.C. (1982). Blood parameters and facilitation of maternal-fetal oxygen transfer in a viviparous fish (Embiotoca lateralis). Comp. Biochem. Physiol. 73A: 497–501.

    Article  Google Scholar 

  • Ingermann, R.L., Terwilliger. R.C. and Roberts. M.S. (1984). Foetal and adult blood oxygen affinities of the viviparous seaperch, Embiotoca lateralis. J. Exp. Biol. In press.

    Google Scholar 

  • Kitchen, H. and Brett, I. (1974). Embryonic and fetal hemoglobin in animals. Ann. N.Y. Acad. Sci. 241: 653–671.

    Article  PubMed  CAS  Google Scholar 

  • Kristofferson, R., Broberg, S. and Pekkarinen, M. (1973). Histology and physiology of embryotrophe formation, embryonic nutrition and growth in the eel pout. Zoarces viviparus (L.). Ann. Zool. Fennici 10: 467–477.

    Google Scholar 

  • Laver, M.B., Jackson, E., Scherperel, M.. ‘Tung, C., Tung, W. and Radford, E.P. (1977). Hemoglobin-O affinity regulation: DPG, monovalent anions, and hemoglobin concentration. J. Appl. Physiol.: Respir. Environ. Exercise Physiol. 43: 632–642.

    CAS  Google Scholar 

  • Leray. C. (1979). Patterns of purine nucleotides in fish erythrocytes. Comp. Biochem. Physiol. 64B: 77–82.

    CAS  Google Scholar 

  • MacKnight, A.D.C. and Leaf, A. (1977). Regulation of cellular volume. Physiol. Rev., 57: 510–573.

    PubMed  CAS  Google Scholar 

  • Manwell, C. (1958a). A ‘fetal-maternal shift’ in the ovoviviparous spiny dogfish Squalus suckleyi (Girard). Physiol. Zool. 31: 93–100.

    Google Scholar 

  • Manwell, C. (1958b). Ontogeny of hemoglobin in the skate Raja binoculata. Science 128: 419–420.

    CAS  Google Scholar 

  • Manwell, C. (1963). Fetal and adult hemoglobins of the spiny dogfish Squalus suckleyi. Arch. Biochem. Biophys. 101: 504–511.

    Article  CAS  Google Scholar 

  • Manwell, C. and Baker. C.M.A. (1970). Molecular Biology and the Origin of Species. University of Washington Press, Seattle.

    Google Scholar 

  • McCutcheon, F.H. (1947). Specific oxygen affinity of hemoglobin in elasmobranchs and turtles. J. Cell. Comp. Physiol. 29: 333–344.

    Article  CAS  Google Scholar 

  • McMenamin, J. W. (1979). Functional morphology of sheathed blood vessels in the ovarian curtains of embiotocid fishes. Am. Zool. 19: 947 (abst).

    Google Scholar 

  • Meschia, G. (1978). Evolution of thinking in fetal respiratory physiology. Am. J. Obstet. Gynecol. 132: 806–813.

    PubMed  CAS  Google Scholar 

  • Novy. M.J. and Parer, J.T. (1969). Absence of high blood oxygen affinity in the fetal cat. Respir. Physiol. 6: 144–150.

    Article  PubMed  CAS  Google Scholar 

  • Pennelly. R.R., Noble, R.W. and Riggs. A. (1975). Equilibria and ligand binding kinetics of hemoglobins from the sharks. Prionace glauca and Carcharhinus milberti. Comp. Biochem. Physiol. 52B: 83–87.

    Article  Google Scholar 

  • Perutz, M.F. (1970). Stereochemistry of cooperative effects in haemoglobin. Nature 228: 726–739.

    Article  PubMed  CAS  Google Scholar 

  • Perutz, M.F. and Brunori. M. (1982). Stereochemistry of cooperative effects in fish and amphibian haemoglobins. Nature 299: 421–426.

    Article  PubMed  CAS  Google Scholar 

  • Ramsey. E.M. (1982). The Placenta: Human and Animal. Praeger Publi., New York.

    Google Scholar 

  • Schlernitzauer, D.A. and Gilbert. P.W. (1966). Placentation and associated aspects of gestation in the bonnethead shark. Sphvrna tiburo. J. Morphol. 120: 219–232.

    Article  CAS  Google Scholar 

  • Sinet, M., Joubin, C. Lachia, L. and Pocidalo. J.J. (1976). Effect of osmotic changes on intracellular pH and haemoglobin oxygen affinity of human erythrocytes. Biomedicine 25: 66–69.

    PubMed  CAS  Google Scholar 

  • Takenaka, O. and Morimoto. H. (1976). Oxygen equilibrium characteristics of adult and fetal hemoglobin of japanese monkey I Macaca fuscata). Biochim. Biophys. Acta 446: 457–462.

    PubMed  CAS  Google Scholar 

  • Turner, C.L. (1936). The absorptive processes in the embryos of Parabrotula dentiens, a viviparous, deep-sea brotulid fish. J. Morphol. 59: 313–325.

    Article  Google Scholar 

  • Turner, C.L. (1937). The trophotaeniae of the Goodeidae, a family of viviparous cyprinodont fishes. J. Morphol. 61: 495–523.

    Article  Google Scholar 

  • Turner, C.L. (1938). Histological and cytological changes in the ovary of Cymatogaster aggregatus during gestation. J. Morphol. 62: 351–373.

    Article  Google Scholar 

  • Turner. C.L. (1940a). Pseudoamnion, pscudochorion, and follicular pseudoplacenta of poeciliid fishes. J. Morphol. 67: 59–89.

    Article  Google Scholar 

  • “Turner, C.L. (1940b). Follicular pseudoplacenta and gut modifications in anablepid fishes. J. Morphol. 67: 91–105.

    Article  Google Scholar 

  • Turner, C.L. (1940c). Pericardial sac. trophotaeniae, and alimentary tract in embryos of goodeid fishes. J. Morphol. 67: 271–289.

    Article  Google Scholar 

  • Turner, C.L. (1940d). Adaptations for viviparity in jenynsiid fishes. J. Morphol 67: 291–297.

    Article  Google Scholar 

  • Turner, C.L. (1952). An accessory respiratory device in embryos of the embiotocid fish, Cymatogaser aggregata, during gestation. Copeia 1952: 146–147.

    Article  Google Scholar 

  • Tweeddale, P.M. (1973). DPG and the oxygen affinity of maternal and foetal pigblood and hemoglobins. Respir. Physiol. 19: 12 - I8.

    Article  PubMed  Google Scholar 

  • Tyuma, I. and Shimizu, K. (1969). Different response to organic phosphates of human fetal blood and adult hemoglobins. Arch. Biochem. Biophys. 129: 404–405.

    Article  PubMed  CAS  Google Scholar 

  • Veith, W.J. (1980). Viviparity and embryonic adaptations in the teleost Clinus superciliosus. Can. J. Zool. 58: 1–12.

    Article  Google Scholar 

  • Webb, P.W. and Brett, J.R. (1972a). Respiratory adaptations of prenatal young in the ovary of two species of viviparous seaperch, Rhacochilus vacca and Embiotoca lateralis. J. Fish. Res. Board Can. 29: 1525–1542.

    Article  Google Scholar 

  • Webb, P.W. and Brett, J.R. (1972b). Oxygen consumption of embryos and parents, and oxygen transfer characteristics within the ovary of two species of viviparous seaperch, Rhacochilus vacca and Embiotoca lateralis. J. Fish. Res. Board Can. 29: 1543–1553.

    Article  CAS  Google Scholar 

  • Weber, RE., Wells, R.M.G. and Rossetti, J.E. (1983a). Allosteric interactions governing oxygen equilibria in the haemoglobin system of the spiny dogfish, Squalus acanthias. J. Exp. Biol. 103: 109–120.

    CAS  Google Scholar 

  • Weber, R.E., Wells, R.M.G. and Tougaard, S. (1983b). Antagonistic effect of urea on oxygenation-linked binding of ATP in an elasmobranch hemoglobin. Life Sci. 32: 2157–2161.

    Article  CAS  Google Scholar 

  • Wells, R.M.G. (1979). Haemoglobin-oxygen affinity in developing embryonic cells of the mouse. J. Comp. Physiol. 129: 333–338.

    CAS  Google Scholar 

  • Wells, R.M.G. and Weber, R.E. (1983). Oxygenation properties and phosphorylated metabolic intermediates in blood and erythrocytes of the dogfish. Squalus acanthias. J. Exp. Biol. 103: 95–108.

    PubMed  CAS  Google Scholar 

  • Wood, S.C. and Johansen. K. (1972). Adaptation to hypoxia by increased HbO affinity and decreased red cell ATP concentration. Nature 237: 278–279.

    CAS  Google Scholar 

  • Wood-Mason, J. and Alcock. A. (1891). On the uterine villiform papillae of Pteroplatea micrura, and their relation to the embryo. Proc. R. Soc. (London) 49: 359–367.

    Google Scholar 

  • Wourms, J.P. (1981). Viviparity: the maternal-fetal relationship in fishes. Am. Zool. 21: 473–515.

    Google Scholar 

  • Wourms, J.P. and Cohen. D. (1975). Trophotaeniae. embryonic adaptations in the viviparous ophidioid fish, Oligopus longhursti: A study of museum specimens. J. Morphol. 147: 385–401.

    Article  Google Scholar 

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Authors and Affiliations

  1. Obstetrics and Gynecology Research, L458, Oregon Health Sciences University, Portland, Oregon, 97201, USA

    Rolf L. Ingermann

  2. Oregon Institute of Marine Biology, University of Oregon, Charleston, Oregon, 97420, USA

    Robert C. Terwilliger

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  1. Rolf L. Ingermann
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  2. Robert C. Terwilliger
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  1. Department of Zoology, University of Adelaide, G.P.O. Box 498, 5001, Adelaide, S.A., Australia

    Roger S. Seymour

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Ingermann, R.L., Terwilliger, R.C. (1984). Facilitation of maternal-fetal oxygen transfer in fishes: Anatomical and molecular specializations. In: Seymour, R.S. (eds) Respiration and metabolism of embryonic vertebrates. Perspectives in vertebrate science, vol 3. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-6536-2_1

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  • DOI: https://doi.org/10.1007/978-94-009-6536-2_1

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