Whale Rider: The Co-occurrence of Haemoglobin and Haemocyanin in Cyamus scammoni

  • Nora Terwilliger
Part of the Protein Reviews book series (PRON, volume 9)


Beatrice and Jonathan Wittenberg have inspired generations of scientists to explore the mysteries of heme proteins. Their papers on the high-affinity haemoglobins of Ascaris, a parasite living in the gut of a mammal, prompted discussions among Bob Terwilliger, Bob Garlick and the author in the 1970s, and led to investigations on numerous invertebrate myoglobins and haemoglobins in the Terwilliger laboratory. In this chapter, I review the structure and function of several of the outstanding molecules and their source organisms, including the haemoglobin and haemocyanin from Cyamus scammoni, the crustacean amphi-pod that rides on a whale. The presence of a high M w extracellular haemoglobin in this arthropod is the first report of haemoglobin expression in the more advanced crustaceans. The co-occurrence of haemoglobin and haemocyanin is also extremely unusual and unprecedented in the Arthropoda.


Heme Protein Ascaris Lumbricoides Grey Whale Phenoloxidase Activity Parasite Living 
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  1. Arellano, S., and Terwilliger, N. 2004. Hemocyanin, cryptocyanin and phenoloxidase in deep sea (Bathynomus giganteus) and intertidal (Cirolana harfordi) isopods. Integr. Comp. Biol. 43:961A.Google Scholar
  2. Decker, H., and Jaenicke, E. 2004. Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins. Devel. Comp. Immun. 28:673–687.CrossRefGoogle Scholar
  3. Fox, H. 1953. Hemoglobin and biliverdin in parasitic cirripede Crustacea. Nature 171:162–163.PubMedCrossRefGoogle Scholar
  4. Kusche, K., Ruhberg, H., and Burmester, T. 2002. A hemocyanin from the Onychophora and the emergence of respiratory proteins. Proc. Natl. Acad. Sci. U.S.A. 98:10545–10548.CrossRefGoogle Scholar
  5. Leung, Y. 1967. An illustrated key to the species of whale-lice (Amphipoda, Cyamidae), ectoparasites of cetacea, with a guide to the literature. Crustaceana 12:279–291.CrossRefGoogle Scholar
  6. Lieb, B., Dimitrova, K., Kang, H., Braun, S., Gebauer, W., Martin, A., Hanelt, B., Saenz, S., Adema, C., and Markl, J. 2006. Red blood with blue-blood ancestry: Intriguing structure of a snail hemoglobin. Proc. Natl. Acad. Sci. U.S.A. 103:12011–12016.PubMedCrossRefGoogle Scholar
  7. Okazaki, T. and Wittenberg, J. B. 1965. The hemoglobin of Ascaris perienteric fluid. III. Equilibria with oxygen and carbon monoxide. Biochim. Biophy. Acta 111:503–511.Google Scholar
  8. Okazaki, T., Briehl, R., Wittenberg, J., and Wittenberg, B. 1965. The hemoglobin of Ascaris perienteric fluid. II. Molecular weight and subunits. Biochim. Biophys. Acta 111:496–502.PubMedGoogle Scholar
  9. Okazaki, T., Wittenberg, B., Briehl, R., and Wittenberg, J. 1967. The hemoglobin of Ascaris body walls. Biochim. Biophys. Acta 140:258–265.PubMedGoogle Scholar
  10. Parkinson, N., Smith, I., Weaver, R., and Edwards, J. 2001. A new form of arthropod phenoloxidase is abundant in venom of the parasitoid wasp Pimpla hypochondriaca. Insect Biochem. Mol. Biol. 31:57–63.PubMedCrossRefGoogle Scholar
  11. Pless, D., Aguilar, M., Falcon, A., Lozano-Alvarez, E., and Heimer de la Cotera, E. 2003. Latent phenoloxidase activity and N-terminal amino acid sequence of hemocyanin from Bathynomus giganteus, a primitive crustacean. Arch. Biochem. Biophys. 409:402–410.PubMedCrossRefGoogle Scholar
  12. Terwilliger, N. B. 1991. Arthropod (Cyamus scammoni, Amphipoda) hemoglobin structure and function. In Structure and Function of Invertebrate Oxygen Carriers, eds. S. Vinogradov and O. Kapp, pp. 59–63. Berlin, Heidelberg, New York: Springer.Google Scholar
  13. Terwilliger, N. B. 1998. Functional adaptations of oxygen-transport proteins. J. Exp. Biol. 201:1085–1098.PubMedGoogle Scholar
  14. Terwilliger, N. B. 2007. Hemocyanins and the immune response: Defense against the dark arts. Integr. Comp. Biol. 47:662–665.CrossRefGoogle Scholar
  15. Terwilliger, N. B. and Ryan, M. 2001. Ontogeny of crustacean respiratory proteins. Am. Zool. 41:1057–1067.CrossRefGoogle Scholar
  16. Terwilliger, N. B. and Ryan, M. 2006. Functional and phylogenetic analyses of phenolox-idases from brachyuran (Cancer magister) and branchiopod (Artemia franciscana, Triops longicaudatus) crustaceans. Biol. Bull. 210:38–50.PubMedCrossRefGoogle Scholar
  17. Terwilliger, R. C., Terwilliger, N. B., and Schabtach, E. 1986. Hemoglobin from the parasitic barnacle, Briarosaccus callosus. In Invertebrate Oxygen Carriers, ed. B. Linzen, pp. 125–127. New York: Springer.Google Scholar
  18. Weber, R. and Vinogradov, S. 2001. Nonvertebrate hemoglobins: Functions and molecular adaptations. Physiol. Rev. 81:569–628.PubMedGoogle Scholar
  19. Wittenberg, B., Okazaki, T., and Wittenberg, J. 1965. The hemoglobin of Ascaris perienteric fluid. I. Purification and spectra. Biochim. Biophys. Acta 111:485–495.PubMedGoogle Scholar
  20. Wittenberg, J. and Stein, J. 1995. Hemoglobin in the symbiotic-harboring gill of the marine gastropod Alviniconcha hessleri. Biol. Bull. 188:5–7.PubMedCrossRefGoogle Scholar

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© Springer-Verlag Italia 2008

Authors and Affiliations

  • Nora Terwilliger
    • 1
  1. 1.Oregon Institute of Marine BiologyUniversity of OregonCharlestonUSA

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