Skip to main content
SpringerLink
Log in
Book cover

Respiratory Pigments in Animals pp 21–34Cite as

Physiological Adaptations and Subunit Diversity in Hemocyanins

  • Conference paper

Abstract

One may question the degree to which physiological adaptations of multisubunit oxygen carrying proteins to the requirements of diverse organisms are based on the existence of structurally and functionally distinct types of subunits. This question can be most easily addressed through studies of the hemocyanins, where multiple types of subunits can self-assemble into truly giant molecules with highly developed allosteric properties. A consideration of our present knowledge concerning subunit differences leads rather directly to the conclusion that both the assembly of the high molecular weight aggregates found in vivo and their physiological function may be directly related to the types of subunits present. Much of our present understanding has come from study of the structure, function and assembly of the chelicerate hemocyanins, present in the horseshoe crabs, scorpions, and spiders. Only recently has it been possible to perform comparable experiments with crustacean hemocyanins. One crustacean hemocyanin, that of the lobster Panulirus interrupts, has proven to be a good model system for studies of subunit diversity. We find that in this system the diverse subunits differ in their ability to self-assemble, in their relative sensitivities to calcium and magnesium, and, of particular physiological importance, in the extent to which an organic cofactor can modulate their oxygen binding properties. Studies with hemocyanin of the garden snail, Helix pomatia and of the sea snail, Murex fulvescens, can be cited as evidence for the presence of diverse subunits that contribute significantly to the assembly and function of molluscan hemocyanins.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Bannister JV, Galdes A, Bannister WH (1977) The oxygen equilibrium of Murex trunculus haemocyanin. In: Bannister JV (ed) Structure and Function of Haemocyanin. Springer-Verlag, Berlin, New York, pp. 193–205

    Google Scholar 

  • Bijlholt MMC, van Brüggen EFJ, Bonaventura J (1979) Dissociation and reassembly of Limulus poiyphemus hemocyanin. Eur. J. Biochem. 95: 399–405

    Google Scholar 

  • Bonaventura C, Bonaventura J (1981) Kinetics of oxygen binding by hemocyanins. In: Lamy J, Lamy J (eds) Invertebrate Oxygen Binding Proteins: Structure, Active Site, and Function. Marcel Dekker, New York, pp. 693–701

    Google Scholar 

  • Bonaventura C, Bonaventura J (1983) Respiratory pigments: structure and function. In: Wilbur K (ed) The Mollusca, Vol. 2, Academic Press, New York, pp. 1–50

    Google Scholar 

  • Bonaventura C, Sullivan B, Bonaventura J, Bourne S (1974) CO binding by hemocyanins of Limulus poiyphemus, Busycon carica, and Callinectes sapidus. Biochemistry 13: 4784–4789

    Article  PubMed  CAS  Google Scholar 

  • Bonaventura J, Bonaventura C, Sullivan B (1977) Properties of the oxygen-binding domains isolated from subtilisin digests of six molluscan hemocyanins. In: Bannister JV (ed) Structure and Function of Haemocyanin. Springer-Verlag, Berlin, New York, pp. 206–216.

    Google Scholar 

  • Bonaventura C, Sullivan B, Bonaventura J, Brunori M (1977) Hemocyanin of the horseshoe crab, Limulus poiyphemus. A temperature-jump study of the oxygen kinetics of the isolated components. In: Bannister JV (ed) Structure and Function of Haemocyanin. Springer-Verlag, Berlin, New York, pp. 265–270

    Google Scholar 

  • Bonaventura C, Bonaventura J, Miller KI, van Holde KE (1981) Hemocyanin of the chambered Nautilus: structure-function relationships. Arch. Biochem. Biophys. 211: 589–598

    Google Scholar 

  • Brenowitz M (1982) The Role of Structurally Distinct Subunits in the Function and Assembly Limulus poiyphemus Hemocyanin, PhD Thesis, Duke University

    Google Scholar 

  • Brenowitz M, Bonaventura C, Bonaventura J, Gianazza E (1981) Subunit composition of a high molecular weight oligomer: Limulus polyphemus hemocyanin. Arch. Biochem. Biophys. 210 (2): 748–761

    Article  PubMed  CAS  Google Scholar 

  • Brenowitz M, Bonaventura C, Bonaventura J (1984) Self-association and oxygen-binding characteristics of the isolated subunits of Limulus polyphemus hemocyanin. Arch. Biochem. Biophys. 230 (1): 238–249

    Article  PubMed  CAS  Google Scholar 

  • Brouwer M (1975) Structural Domains in Helix pomatia Alpha Hemocyanin, Ph.D Thesis, University of Groningen

    Google Scholar 

  • Brouwer M, Kuiper HA (1973) Molecular-weight analysis of Helix pomatia α-hemocyanin in guanidine hydrochloride, urea and sodium dodecyl-sulfate. Eur. J. Biochem. 35: 428–435

    Google Scholar 

  • Brouwer M, Wolters M, van Brüggen EFJ (1976) Proteolytic fragmentation of Helix pomatia alpha hemocyanin: structural domains in the polypeptide chain. Biochemistry 15: 18–23

    Article  Google Scholar 

  • Brouwer M, Ryan M, Bonaventura J, Bonaventura C (1978) Functional and structural properties of Murex fulvescens hemocyanin: isolation of two different subunits required for reassociation of a molluscan hemocyanin. Biochemistry 17: 2810–2815

    Article  PubMed  CAS  Google Scholar 

  • Brouwer M, Bonaventura C, Bonaventura J (1983) Metal ion interactions with Limulus poiyphemus and Callinectes sapidus hemocyanin: stoichiometry and structural and functional consequences of calcium (II), cadmium (II), zinc (II), and mercury ( II) binding. Biochemistry 22: 4713–4723

    Google Scholar 

  • Brunori M, Kuiper HA, Antonini E, Bonaventura C, Bonaventura J (1977) Kinetics of oxygen binding by hemocyanins. In: Lamy J, Lamy J (eds) Invertebrate Oxygen-Binding Proteins: Structure, Active Site, and Function. Marcel Dekker, New York, pp. 693–702

    Google Scholar 

  • Ellerton HD, Ellerton NF, Robinson HA (1983) Hemocyanin-A current perspective. Progr. Biophys. Molec. Biol. 41: 143–248

    Google Scholar 

  • Felsenfeld G, Printz MP (1959) Specific reactions of hydrogen peroxide with the active site of hemocyanin. The formation of “methemocyanin”. J. Amer. Chem. Soc. 81: 6259–6264

    Google Scholar 

  • Folkerts A, van Eerd JP (1981) Immunological relatedness of five hemocyanin subunits from the spiny lobster Panulirus interruptus. In: Lamy J, Lamy J (eds) Invertebrate Oxygen Binding Proteins: Structure, Active, Site, and Function. Marcel Dekker, New York, pp. 215–225

    Google Scholar 

  • Gaykema WPJ, Hoi WGJ, Vereijken JM, Soeter NM, Bäk HJ, Beintema JJ (1984) 3.2 Å structure of the copper-containing, oxygen-carryin protein Panulirus interrruptus haemocyanin. Nature 309: 23–29

    Google Scholar 

  • Gielens C, Préaux G, Lontie R (1975) Limited trypsinolysis of ß-haemocyanin of Helix pomatia: Characterization of the fragments and heterogeneity of the copper groups by circular dichroism. Eur. J. Biochem. 60: 271–280

    Google Scholar 

  • Gielens C, Préaux G, Lontie R (1977) Structural investigations of ß-haemocyanin of Helix pomatia by limited proteolysis. In: Bannister JV (ed) Structure and Function of Haemo-cyanin. Springer-Verlag, Berlin, New York, pp. 85–94

    Google Scholar 

  • Hoylaerts M, Préaux G, Witters R, Lontie R (1979) Immunological heterogeneity of the subunits of Limulus polyphemus hemocyanin. Arch. Intern. Physiol. Biochem. 87: 417–418

    Google Scholar 

  • Johnson B (1984) Allosteric Interactions of L-Lactate and Inorganic Ions with structurally Distinct Crustacean hemocyanins, Ph.D Thesis, Duke University

    Google Scholar 

  • Johnson B, Bonaventura C, Bonaventura J (1984) Allosteric modulation of Callinectes sapidus hemocyanin by binding of L-lactate. Biochemistry 23: 872–878

    Article  CAS  Google Scholar 

  • Joliès J, Jollès P, Lamy J, Lamy J (1981) N-terminal sequences and antigenic purity of isolated subunits from Androctonus australis hemocyanin. In: Lamy J, Lamy J (eds) Invertebrate Oxygen-Binding Proteins: Structure, Active Site, and Function. Marcel Dekker, New York, pp. 305–310

    Google Scholar 

  • Konings WN, Dijk J, Wichertjes T, Beuvery EC, Gruber M (1969) Structure and properties of hemocyanins. IV. Dissociation of Helix pomatia hemocyanin by succinylation into functional subunits. Biochim. Biophys. Acta 188: 43–54

    Google Scholar 

  • Lamy J, Lamy J, Weill J, Bonaventura J, Bonaventura C, Brenowitz M (1979) Immunological correlates between the multiple subunits of Limulus polyphemus and Tachypleus tridentatus. Arch. Biochem. Biophys. 196: 324–339

    Google Scholar 

  • Lamy J, Lamy J, Bonaventura J, Bonaventura C (1980) Structure, function and assembly in the hemocyanin system of the scorpion Androctonus australis. Biochemistry 19: 3033–3039

    Article  PubMed  CAS  Google Scholar 

  • Lontie R, Witters R (1973) Hemocyanin. In: Eichorn GL (ed) Inorganic Biochemistry. Elsevier, Amsterdam, pp. 344–358

    Google Scholar 

  • Lontie R, Gielens C, Groeseneken D, Verplaetse J, Witters R (1982) Comparison of the active sites of molluscan and arthropodan hemocyanins. In: King TE, Mason HS, Morrison M (eds) Oxidases and related Redox Systems. Pergamon Press, Oxford, New York, pp. 245–261

    Google Scholar 

  • Mangum CP (1983) On the distribution of lactate sensitivity among the hemocyanins. Mar. Biol. Lett. 4: 139–150

    CAS  Google Scholar 

  • Markl J, Hofer A, Bauer G, Markl A, Kempter B, Brenzinger M, Linzen B (1979) Subunit heterogeneity in arthropod hemocyanins. II. Crustacea. J. Comp. Physiol. 133: 167–175

    Google Scholar 

  • Markl J, Decker H, Savel A, Linzen B (1981) Homogeneity, subunit heterogeneity, and quaternary structure of Eurypelma hemocyanin. In: Lamy J, Lamy J (eds) Invertebrate Oxygen-Binding Proteins: Structure, Active Site, and Function. Marcel Dekker, New York, pp. 445–454

    Google Scholar 

  • Senozan NM, Landrum J, Bonaventura J, Bonaventura C (1981) Hemocyanin of the giant keyhole limpet, Meqathura crenulata. In: Lamy J, Lamy J (eds) Invertebate Oxygen-Binding Proteins: Structure, Active Site, and Function. Marcel Dekker, New York, pp. 703–717

    Google Scholar 

  • Siezen RJ, van Driel R (1973) Structure and properties of hemocyanins. VIII. Microheteroge-neity of α-hemocyanin of Helix pomatia. Biochim. Biophys. Acta 295: 131–139

    PubMed  CAS  Google Scholar 

  • Siezen RJ, van Brüggen EFJ (1974) Structure and properties of hemocyanin. XII. Electron microscopy of Helix pomatia a-hemocyanins quaternary structure. J. Mol. Biol. 90: 77–89

    Article  PubMed  CAS  Google Scholar 

  • Snyder GK, Mangum CP (1982) The relationship between the capacity for oxygen transport, size, shape, and aggregation state of an extracellular oxygen carrier. In: Bonaventura J, Bonaventura C, Tesh S (eds) Physiology and Biology of Horseshoe Crabs. A.R. Liss Inc., New York, pp. 173–188

    Google Scholar 

  • Solomon EI, Eickman NC, Himmelwright RS, Hwang YT, Plön SE, Wilcox DE (1982) The nature of the binuclear copper site in Limulus and other hemocyanins. In: Bonaventura J, Bonaventura C, Tesh S (eds) Physiology and Biology of Horseshoe Crabs. A.R. Liss Inc., New York, pp. 189–230

    Google Scholar 

  • Sullivan B, Bonaventura J, Bonaventura C (1974) Functional difference in the multiple hemocyanins of the hors shoe crab, Limulus polyphemus L. Proc. Natl. Acad. Sci. USA 71: 2558–2562

    Google Scholar 

  • Sullivan B, Bonaventura J, Bonaventura C, Godette G (1976) Hemocyanin of the horseshoe crab Limulus polyphemus. Structural differentiation of the isolated components. J. Biol. Chem. 251: 7644–7648

    Google Scholar 

  • Svedberg T, Hedenius A (1934) The sedimentation constants of the respiratory proteins. Biol. Bull. ( Woods Hole, Mass. ) 66: 191–223

    Google Scholar 

  • Svedberg T, Petersen KO (1940) The Ultracentrifuge. Oxford University Press, London and New York

    Google Scholar 

  • van Brüggen EFJ, Bijlholt MMC, Schütter WG, Wichertjes T, Bonaventura J, Bonaventura C, Lamy J, Lamy J, Ledere M, Schneider HJ, Markl J, Linzen B (1980) The role of structurally diverse subunits in the assembly of three cheliceratan hemocyanins. FEBS Lett. 116: 207–210

    Article  Google Scholar 

  • van Eerd JP, Folkerts A (1981) Isolation and characterization of five subunits of the hemocyanin from the spiny lobster Panulirus interruptus. In: Lamy J, Lamy J (eds) Invertebrate Oxygen-Binding Proteins: Structure, Active Site, and Function. Marcel Dekker, New York, pp. 139–149

    Google Scholar 

  • van Holde KE, Miller KI (1982) Hemocyanins. Quart. Rev. Biophys. 15: 1–129

    Google Scholar 

  • Witters R, van Rossen-Usé L, Lontie R (1974) The regeneration with cysteine of gastropod haemocyanin mediated by hydrogen peroxide. Arch. Intern. Physiol. Biochim. 82: 917–924

    Google Scholar 

Download references

Authors
  1. J. Bonaventura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Bonaventura
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Laboratory of Biochemistry, University of Francois-Rabelais, 2, Boulevard Tonnellé, F-37032, Tours Cedex, France

    Jean Lamy (Scientific Editor) (Scientific Editor)

  2. Department of Pharmaceutical Science, University of Francois-Rabelais, 2, Boulevard Tonnellé, F-37032, Tours Cedex, France

    Jean Lamy (Scientific Editor) (Scientific Editor)

  3. Laboratory of Neurobiology and Compared Physiology, University of Bordeaux I, Place du Dr. Bertrand Peyneau, F-33120, Arcachon Cedex, France

    Jean-Paul Truchot (Scientific Editor) (Scientific Editor)

  4. Laboratory of Biochemistry, University of Liège, 22, Quai Van Benden, B-4020, Liège, Belgium

    Raymond Gilles (Coordinating Editor) (Coordinating Editor)

Rights and permissions

Reprints and permissions

Copyright information

© 1985 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Bonaventura, J., Bonaventura, C. (1985). Physiological Adaptations and Subunit Diversity in Hemocyanins. In: Lamy, J., Truchot, JP., Gilles, R. (eds) Respiratory Pigments in Animals. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-70616-5_3

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-70616-5_3

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-540-15629-1

  • Online ISBN: 978-3-642-70616-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation