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Adaptations for Oxygen Transport: Lessons from Fish Hemoglobins

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Hemoglobin Function in Vertebrates

Abstract

Hemoglobin (Hb) is a prototype of macromolecules whose functional properties are controlled by ionic effectors and a paradigm for study of the structure, function and allosteric interactions of proteins. By virtue of its well-defined roles in transporting O2 from the respiratory surfaces to the tissues and metabolic end-products such as CO2, protons, heat in the opposite direction, and its implication in regulating other processes in red cells, it forms an ideal model for probing the mechanisms of molecular adaptations to environmental conditions and physiological demands [[16], [62]].

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References

  1. Bauer C, Forster M, Gros G, Mosca A, Perrella M, Rollema HS, Vogel D (1981) Analysis of bicarbonate binding to crocodilian hemoglobin. J Biol Chem 256:8429–8435

    PubMed  CAS  Google Scholar 

  2. Bonaventura C, Bonaventura J (1978) Anionic control of hemoglobin function. In: Caughey WS (ed) Biochemical and clinical aspects of hemoglobin abnormalities. Academic, New York, pp 647–663

    Google Scholar 

  3. Brittain T (1987) The Root effect. Comp Biochem Physiol 86B:473–481

    CAS  Google Scholar 

  4. Brunori M, Coletta M, Giardina B, Wyman J (1978) A macromolecular transducer as illustrated by trout hemoglobin IV. Proc Natl Acad Sci USA 75:4310–4312

    Article  PubMed  CAS  Google Scholar 

  5. Bunn HF, Ransil BJ, Chao A (1971) The interaction between erythrocyte organic phosphates, magnesium ion, and hemoglobin. J Biol Chem 246:5273–5279

    PubMed  CAS  Google Scholar 

  6. Chétrite G, Cassoly R, Chetrite G (1985) Affinity of hemoglobin for the cytoplasmic fragment of human erythrocyte membrane band 3. Equilibrium measurements at physiological pH using matrix-bound proteins: the effects of ionic strength, deoxygenation and of 2,3-diphosphoglycerate. J Mol Biol 185:639–644

    Article  PubMed  Google Scholar 

  7. Chien JCW, Mayo KH (1980) Carp hemoglobin. I. Precise oxygen equilibrium and analysis according to the models of Adair and of Monod, Wyman, and Changeux. J Biol Chem 255:9790–9799

    PubMed  CAS  Google Scholar 

  8. Davie PS, Wells RMG, Tetens V (1986) Effects of sustained swimming on rainbow trout muscle structure, blood oxygen transport, and lactate dehydrogenase isozymes: evidence for increased aerobic capacity of white muscle. J Exp Zool 237:159–171

    Article  PubMed  CAS  Google Scholar 

  9. Davis BJ (1991) Developmental changes in the blood oxygen transport system of Kemp’s ridley sea turtle, Lepidochelys kempi. Can J Zool 69:2660–2666

    Article  CAS  Google Scholar 

  10. di Prisco G, Tamburrini M (1992) The hemoglobins of marine and freshwater fish: The search for correlations with physiological adaptation. Comp Biochem Physiol [B] 102:661–671

    Google Scholar 

  11. Fago A, Carratore V, di Prisco G, Feuerlein RJ, Sottrup-Jensen L, Weber RE (1995) The cathodic hemoglobin of Anguilla anguilla. Amino acid sequence and oxygen equilibria of a reverse Bohr effect hemoglobin with high oxygen affinity and high phosphate sensitivity. J Biol Chem 270:18897–18902

    Article  PubMed  CAS  Google Scholar 

  12. Fago A, Bendixen E, Malte H, Weber RE (1997) The anodic hemoglobin of Anguilla anguilla. Molecular base for allosteric effects in a Root-effect hemoglobin. J Biol Chem 272:15628–15635

    Article  PubMed  CAS  Google Scholar 

  13. Fago A, Malte H, Dohn N (1999) Bicarbonate binding to hemoglobin links oxygen and carbon dioxide transport in hagfish. Respir Physiol 115:309–315

    Article  PubMed  CAS  Google Scholar 

  14. Feuerlein RJ, Weber RE (1996) Oxygen equilibria of cathodic eel hemoglobin analysed in terms of the MWC model and Adair’s successive oxygenation theory. J Comp Physiol 165:597–606

    CAS  Google Scholar 

  15. Garlick RL, Bunn HF, Fyhn HJ, Fyhn UEH, Martin JP, Noble RW, Powers D (1979) Functional studies on the separated hemoglobin components of an air-breathing catfish, Hoplosternum littorate (Hancock). Comp Biochem Physiol 62A:219–226

    CAS  Google Scholar 

  16. Giardina B, Messana I, Scatena R, Castagnola M (1995) The multiple functions of hemoglobin. Crit Rev Biochem Mol Biol 30:165–196

    Article  PubMed  CAS  Google Scholar 

  17. Giles MA, Rystephanuk DM (1989) Ontogenetic variation in the multiple hemoglobins of Arctic charr, Salvelinus alpinus. Can J Fish Aquat Sci 46:804–809

    Article  Google Scholar 

  18. Gillen RG, Riggs A (1973) Structure and function of the isolated hemoglobins of the American eel, Anguilla rostrata. J Biol Chem 248:1961–1969

    PubMed  CAS  Google Scholar 

  19. Gronenborn AM, Clore GM, Brunori M, Giardina B, Falcioni G, Perutz MF (1984) Stereochemistry of ATP and GTP bound to fish haemoglobins. A transferred nuclear overhauser enhancement, 31P-Nuclear Magnetic Resonance, oxygen equilibrium and molecular modelling study. J Mol Biol 178:731–742

    Article  PubMed  CAS  Google Scholar 

  20. Imai K (1982) Allosteric effects in haemoglobin. Cambridge University Press, Cambridge

    Google Scholar 

  21. Ingermann RL, Terwilliger RC (1981) Intraerythrocytic organic phosphates of fetal and adult seaperch (Embiotoca lateralis): their role in maternal-fetal oxygen transport. J Comp Physiol [B] 144:253–259

    Article  CAS  Google Scholar 

  22. Isaacks RE, Kim HD, Harkness DR (1978) Relationship between phosphorylated metabolic intermediates and whole blood oxygen affinity in some air-breathing and water-breathing teleosts. Can J Zool 56:887–890

    Article  CAS  Google Scholar 

  23. Jensen FB, Weber RE (1982) Respiratory properties of tench blood and hemoglobin. Adaptation to hypoxic-hypercapnic water. Molec Physiol 2:235–250

    CAS  Google Scholar 

  24. Jensen FB, Weber RE (1987) Internal hypoxia-hypercapnia in tench exposed to aluminium in acid water: effects on blood gas transport, acid-base status and electrolyte composition in arterial blood. J Exp Biol 127:427–442

    CAS  Google Scholar 

  25. Jensen FB, Andersen NA, Heisler N (1990) Interrelationships between red cell nucleoside triphosphate content, and blood pH, 02-tension and haemoglobin concentration in carp, Cyprinus carpio. Fish Physiol Biochem 8:459–464

    Article  CAS  Google Scholar 

  26. Jensen FB, Fago A, Weber RE (1998) Hemoglobin structure and function. In: Perry SF, Tufts BL (eds) Fish respiration. Academic, San Diego, pp 1–40

    Google Scholar 

  27. Jensen FB, Jakobsen MH, Weber RE (1998) Interaction between haemoglobin and synthetic peptides of the N-terminal cytoplasmic Interaction between haemoglobin and synthetic peptides of the N-terminal cytoplasmic fragment of trout band 3 (AE1) protein. J Exp Biol 201:2685–2690

    PubMed  CAS  Google Scholar 

  28. Johansen K, Lykkeboe G, Weber RE, Maloiy GMO (1976) Respiratory properties of blood in awake and estivating lungfish, Protopterus amphibius. Respir Physiol 27:335345

    Google Scholar 

  29. Johansen K, Mangum CP, Weber RE (1978) Reduced blood 02 affinity associated with air breathing in osteoglossid fishes. Can J Zool 56:891–897

    Article  CAS  Google Scholar 

  30. Kleinschmidt T, Sgouros JG (1987) Hemoglobin sequences. Biol Chem Hoppe-Seyler 368:579–615

    Article  PubMed  CAS  Google Scholar 

  31. Lane HC, Rolfe AE, Nelson JR (1981) Changes in the nucleoside triphosphate/haemoglobin and nucleoside triphosphate/red cell ratios of rainbow trout, Salmo gairdneri Richardson, subjected to prolonged starvation and bleeding. J Fish Biol 18:661–668

    Article  CAS  Google Scholar 

  32. Leray C (1979) Patterns of purine necleotides in fish erythrocytes. Comp Biochem Physiol [B] 64B:77–82

    CAS  Google Scholar 

  33. Leray C (1982) Patterns of purine nucleotides in North Sea fish erythrocytes. Comp Biochem Physiol 71B:77–81

    CAS  Google Scholar 

  34. Low PS (1986) Structure and function of the cytoplasmic domain of band 3: center of erythrocyte membrane-peripheral protein interactions. Biochim Biophys Acta 864:145–167

    Article  PubMed  CAS  Google Scholar 

  35. Luisi BF, Nagai K, Perutz M, Perutz MF (1987) X-ray crystallographic and functional studies of human haemoglobin mutants produced in Escherichia coli. Acta Haematol 78:85–89

    Article  PubMed  CAS  Google Scholar 

  36. Lykkeboe G, Johansen K, Maloiy GMO (1975) Functional properties of hemoglobins in the teleost Tilapia grahami. J Comp Physiol 104:1–11

    CAS  Google Scholar 

  37. Martin JP, Bonaventura J, Brunori M, Fyhn HJ, Fyhn UEH, Garlick RL, Powers DA, Wilson MT (1979) The isolation and characterization of the hemoglobin components of Mylossoma sp., an Amazonian teleost. Comp Biochem Physiol 62A:155–162

    CAS  Google Scholar 

  38. Messana I, Orlando M, Cassiano L, Pennacchietti L, Zuppi C, Castagnola M, Giardina B (1996) Human erythrocyte metabolism is modulated by the 02-linked transition of hemoglobin. FEBS Lett 390:25–28

    Article  PubMed  CAS  Google Scholar 

  39. Moyle PB, Cech JJ Jr (1996) Fishes: an introduction to ichthyology, 3rd edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  40. Mylvaganam SE, Bonaventura C, Bonaventura J, Getzoff ED (1996) Structural basis for the Root effect in haemoglobin. Nature Struct Biol 3:275–283

    Article  PubMed  CAS  Google Scholar 

  41. Nagai K, Perutz MF, Poyart C (1985) Oxygen binding properties of human mutant hemoglobins synthesized in Escherichia coli. Proc Natl Acad Sci USA 82:7252–7255

    Article  PubMed  CAS  Google Scholar 

  42. Nikinmaa M (1992) Membrane transport and control of hemoglobin-oxygen affinity in nucleated erythrocytes. Physiol Rev 72:301–321

    PubMed  CAS  Google Scholar 

  43. Nikinmaa M, Salama A (1998) Oxygen transport in fish. In: Perry SF, Tufts BL (eds) Fish respiration. Academic, San Diego, pp 141–184

    Google Scholar 

  44. Noble RW, Kwiatkowski LD, De Young A, Davis BJ, Haedrich RL, Tam LT, Riggs AF, Tam LT (1986) Functional properties of hemoglobins from deep-sea fish: correlations with depth distribution and presence of a swimbladder. Biochim Biophys Acta 870:552–563

    Article  PubMed  CAS  Google Scholar 

  45. Perutz MF (1970) Stereochemistry of cooperative effects in haemoglobin. Haemhaem interaction and the problem of allostery. Nature 228:726–734

    Article  PubMed  CAS  Google Scholar 

  46. Perutz MF (1983) Species adaptation in a protein molecule. Mol Biol Evol 1(1):1–28

    PubMed  CAS  Google Scholar 

  47. Perutz MF (1986) A bacterial haemoglobin. Nature 322:405

    Article  Google Scholar 

  48. Perutz MF, Brunori M (1982) Stereochemistry of cooperative effects in fish and amphibian haemoglobins. Nature 299(5882):421–426

    Article  PubMed  CAS  Google Scholar 

  49. Perutz MF, Fermi G, Poyart C, Pagnier J, Kister J (1993) A novel allosteric mechanism in haemoglobin. Structure of bovine deoxyhaemoglobin, absence of specific chloride-binding sites and origin of the chloride-linked Bohr effect in bovine and human haemoglobin. J Mol Biol 233:536–545

    Article  PubMed  CAS  Google Scholar 

  50. Samuelsen EN, Imsland AK, Brix 0 (1999) Oxygen binding properties of three different hemoglobin genotypes in turbot (Scophthalmus maximus Rafinesque): effect of temperature and pH. Fish Physiol Biochem 20:135–141

    Article  CAS  Google Scholar 

  51. Sayare M, Fikiet M (1981) Cross-linking of hemoglobin to the cytoplasmic surface of human erythrocyte membranes. Identification of band 3 as a site for hemoglobin binding in Cu2+-o-phenanthroline catalyzed cross-linking. J Biol Chem 256:13152–13158

    PubMed  CAS  Google Scholar 

  52. Val AL (1993) Adaptations of fishes to extreme conditions in fresh waters. In: Bicudo JEPW (ed) The vertebrate gas transport cascade. Adaptations to environment and mode of life. CRC Press, Boca Raton, pp 43–53

    Google Scholar 

  53. Val AL, Schwantes AR, Almeida-Val VMF (1986) Biological aspects of Amazonian fishes VI. Hemoglobins and whole blood properties of Semaprochilodus species (Prochilodontidae) at two phases of migration. Comp Biochem Physiol 83B:659–667

    CAS  Google Scholar 

  54. Val AL, Affonso EG, Souza RHS, Almeida-Val VMF, Moura MAF (1992) Inositol pentaphosphate in the erythrocytes of an Amazonian fish, the pirarucu (Arapaima gigas). Can J Zool 70:852–855

    Article  CAS  Google Scholar 

  55. Vorger P, Ristori M-T (1985) Effects of experimental anemia on the ATP content and the oxygen affinity of the blood in the rainbow trout (Salmo gairdnerii). Comp Biochem Physiol A 82A:221–224

    Article  CAS  Google Scholar 

  56. Walder JA, Chatterjee R, Steck TL, Low PS, Musso GF, Kaiser ET, Rogers PH, Arnone A (1984) The interaction of hemoglobin with the cytoplasmic domain of Band 3 of the human erythrocyte membrane. J Biol Chem 259:10238–10246

    PubMed  CAS  Google Scholar 

  57. Weber RE (1982) Intraspecific adaptation of hemoglobin function in fish to oxygen availability. In: Addink ADF, Spronk N (eds) Exogenous and endogenous influences on metabolic and neural control, vol 1. Pergamon, Oxford, pp 87–102

    Google Scholar 

  58. Weber RE (1990) Functional significance and structural basis of multiple hemoglobins with special reference to ectothermic vertebrates. In: Truchot JP, Lahlou B (eds) Animal nutrition and transport processes. 2. Transport, respiration and excretion: comparative and environmental aspects. Comparative physiology, vol 6, Basel, Karger, pp 58–75

    Google Scholar 

  59. Weber RE (1994) Hemoglobin-based 02 transfer in viviparous animals. Isr J Zool 40:541–550

    Google Scholar 

  60. Weber RE (1996) Hemoglobin adaptations in Amazonian and temperate fish with special reference to hypoxia, allosteric effectors and functional heterogeneity. In: Val AL, Almeida-Val VMF, Randall DJ (eds) Physiology and biochemistry of the fishes of the Amazon. INPA, Brazil, pp 75–90

    Google Scholar 

  61. Weber RE, Hartvig M (1984) Specific fetal hemoglobin underlies the fetal-maternal shift in blood oxygen affinity in a viviparous teleost. Molec Physiol 6:27–32

    CAS  Google Scholar 

  62. Weber RE, Jensen FB (1988) Functional adaptations in hemoglobins from ectothermic vertebrates. Annu Rev Physiol 50:161–179

    Article  PubMed  CAS  Google Scholar 

  63. Weber RE, Lykkeboe G (1978) Respiratory adaptations in carp blood. Influences of hypoxia, red cell organic phosphates, divalent cations and CO2 on hemoglobin-oxygen affinity. J Comp Physiol 128B:127–137

    Google Scholar 

  64. Weber RE, Wood SC (1979) Effects of erythrocytic nucleoside triphosphates on oxygen equilibria of composite and fractionated hemoglobins from the facultative air-breathing Amazonian catfish, Hypostomus and Pterygoplichthys. Comp Biochem Physiol 62A:179–183

    CAS  Google Scholar 

  65. Weber RE, Lykkeboe G, Johansen K (1976) Physiological properties of eel haemoglobin: Hypoxic acclimation, phosphate effects and multiplicity. J Exp Biol 64:75–88

    PubMed  CAS  Google Scholar 

  66. Weber RE, Wood SC, Davis BJ (1979) Acclimation to hypoxic water in facultative air-breathing fish: Blood oxygen affinity and allosteric effectors. Comp Biochem Physiol 62A:125–129

    CAS  Google Scholar 

  67. Weber RE, Jensen FB, Cox RP (1987) Analysis of teleost hemoglobin by Adair and Monod-Wyman-Changeux models. Effects of nucleoside triphosphates and pH on oxygenation of tench hemoglobin. J Comp Physiol 157B:145–152

    Google Scholar 

  68. Weber RE, Fago A, Val AL, Bang A, Van Hauwaert M-L, Dewilde S, Zal F, Moens L (2000) Isohemoglobin differentiation in the bimodal-breathing Amazon catfish Hoplosternum littorale. J Biol Chem, in press

    Google Scholar 

  69. Wells RMG, Weber RE (1990) The spleen in hypoxic and exercised rainbow trout. J Exp Biol 150:461–466

    Google Scholar 

  70. Wilhelm Filho D, Marcon JL, Caprario FX, Correa Nollis A (1992) Erythrocytic nucleoside triphosphates in marine fish. Comp Biochem Physiol A 102A:323–331

    Article  CAS  Google Scholar 

  71. Wilkins NP (1985) Ontogeny and evolution of salmonid hemoglobins. Int Rev Cytol 94:269–298

    Article  PubMed  CAS  Google Scholar 

  72. Wood SC, Johansen K (1972) Adaptation to hypoxia by increased HbO2 affinity and decreased red cell ATP concentration. Nat New Biol 237:278–279

    PubMed  CAS  Google Scholar 

  73. Wood SC, Johansen K (1973) Blood oxygen transport and acid-base balance in eels during hypoxia. Am J Physiol 225:849–851

    PubMed  CAS  Google Scholar 

  74. Wood SC, Johansen K (1973) Organic phosphate metabolism in nucleated red cells: influence of hypoxia on eel HbO2 affinity. Neth J Sea Res 7:328–338

    Article  CAS  Google Scholar 

  75. Yamamoto KI (1988) Contraction of spleen in exercised freshwater teleost. Comp Biochem Physiol A 89:65–66

    Article  Google Scholar 

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Weber, R.E. (2000). Adaptations for Oxygen Transport: Lessons from Fish Hemoglobins. In: Hemoglobin Function in Vertebrates. Springer, Milano. https://doi.org/10.1007/978-88-470-2111-2_2

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  • DOI: https://doi.org/10.1007/978-88-470-2111-2_2

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