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3.2 Å structure of the copper-containing, oxygen-carrying protein Panulirus interruptus haemocyanin

Nature volume 309, pages 23–29 (1984)Cite this article

Abstract

For the first time, the three-dimensional structure of a member of the copper-containing class of oxygen-carrying proteins—the haemocyanins—has been determined. The structure of Panulirus interruptus haemocyanin at 3.2 Å resolution shows that each subunit of the 450,000-molecular weight hexamer is folded into three domains, and that the binuclear copper site is situated in the centre of the second domain. Amino acid sequence comparisons suggest that the polypeptide fold of P. interruptus haemocyanin is common to all arthropod haemocyanins.

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References

  1. Perutz, M. F., Muirhead, H., Cox, J. M. & Goaman, L. C. G. Nature 219, 131–139 (1968).

    Article  ADS  CAS  Google Scholar 

  2. Steigemann, W. & Weber, E. J. molec. Biol. 127, 309–338 (1979).

    Article  CAS  Google Scholar 

  3. Dickerson, R. E. & Geis, I., Hemoglobin: Structure, Function, Evolution and Pathology (Cummings, Menlo Park, 1983).

    Google Scholar 

  4. Garlick, R. L. & Riggs, A. F. J. biol. Chem. 257, 9005–9015 (1982).

    CAS  PubMed  Google Scholar 

  5. Hendrickson, W. A. & Ward, K. B. J. biol. Chem. 252, 3012–3018 (1977).

    CAS  Google Scholar 

  6. Stenkamp, R. E., Sieker, L. C., Jensen, L. H. & McQueen, J. E. Biochemistry 17, 2499–2504 (1978).

    Article  CAS  Google Scholar 

  7. Smith, J. L., Hendrickson, W. A. & Addison, A. W. Nature 303, 86–88 (1983).

    Article  ADS  CAS  Google Scholar 

  8. Nemoto, T. & Takagi, T. Life Chem. Rep. 1, Suppl. 1, 89–92 (1983).

    CAS  Google Scholar 

  9. Yokota, E., Moore, M. D., Behrens, P. Q. & Riggs, A. F. Life Chem. Rep. 1, Suppl. 1, 75–80 (1983).

    CAS  Google Scholar 

  10. Moore, M. D. & Riggs, A. F. Life Chem. Rep. 1, Suppl. 1, 93–97 (1983).

    CAS  Google Scholar 

  11. Schneider, H. J. et al. Hoppe-Seyler's Z. physiol Chem. 364, 1357–1381 (1983).

    Article  CAS  Google Scholar 

  12. Schartau, W. et al. Hoppe-Seyler's Z. physiol. Chem. 364, 1383–1409 (1983).

    Article  CAS  Google Scholar 

  13. Van Eerd, J. P. & Folkerts, A. in Invertebrate Oxygen-Binding Proteins (eds Lamy, J. & Lamy, J.) 139–149 (Marcel Dekker, New York, 1981).

    Google Scholar 

  14. Vereijken, J. M., Schwander, E. H., Soeter, N. M. & Beintema, J. J. Eur. J. Biochem. 123, 283–289 (1982).

    Article  CAS  Google Scholar 

  15. Vereijken, J. M. Life Chem. Rep. 1, Suppl. 1, 99–100 (1983).

    Google Scholar 

  16. Soeter, N. M. & Beintema, J. J. Life Chem. Rep. 1, Suppl. 1, 101–102 (1983).

    Google Scholar 

  17. Schwander, E. H. & Vereijken, J. M. Life Chem. Rep. 1, Suppl. 1, 103–106 (1983).

    CAS  Google Scholar 

  18. Jollès, J., Jollès, P., Lamy, J. & Lamy, J. FEBS Lett. 106, 289–291 (1979).

    Article  Google Scholar 

  19. Schneider, H.-J. et al. Hoppe-Seyler's Z. physiol. Chem. 363, 487–492 (1982).

    Article  CAS  Google Scholar 

  20. Fernändez-Morän, H., Van Bruggen, E. F. J. & Ohtsuki, M. J. molec. Biol. 16, 191–207 (1966).

    Article  Google Scholar 

  21. Mellema, J. E. & Klug, A. Nature 239, 146–150 (1972).

    Article  ADS  CAS  Google Scholar 

  22. Van Bruggen, E. F. J. et al. in Electron Miscroscopy of Proteins Vol. 1 (ed. Harris, M.) 1–38 (Academic, New York, 1981).

    Google Scholar 

  23. Lamy, J., Bijlholt, M. M. C., Sizaret, P.-Y., Lamy, J. & van Bruggen, E. F. J. Biochemistry 20, 1849–1856 (1981).

    Article  CAS  Google Scholar 

  24. Bijlholt, M. C., Van Heel, M. G. & Van Bruggen, E. F. J. J. molec. Biol. 161, 139–153 (1982).

    Article  CAS  Google Scholar 

  25. Van Holde, K. E. & Miller, K. I. Q. Rev. Biophys. 15, 1–129 (1982).

    Article  CAS  Google Scholar 

  26. Himmelwright, R. S., Eickman, N. C., LuBien, C. D. & Solomon, E. I. J. Am. chem. Soc. 102, 5378–5388 (1980).

    Article  CAS  Google Scholar 

  27. Torensma, R. & Phillips, J. C. FEBS Lett. 130, 314–316 (1981).

    Article  CAS  Google Scholar 

  28. Schoot Uiterkamp, A. J. M. & Mason, H. S. Proc. natn. Acad. Sci. U.S.A. 70, 993–996 (1973).

    Article  ADS  CAS  Google Scholar 

  29. Eickman, N. C., Solomon, E. I., Larrabee, J. A., Spiro, Th. G. & Lerch, K. J. Am. chem. Soc. 100, 6529–6531 (1978).

    Article  CAS  Google Scholar 

  30. Himmelwright, R. S., Eickman, N. C., LuBien, C. D., Lerch, K. & Solomon, E. I. J. Am. chem. Soc. 102, 7339–7344 (1980).

    Article  CAS  Google Scholar 

  31. Urbach, F. L. in Metal Ions in Biological Systems Vol. 13 (ed. Sigel, H.) 73–115 (Marcel Dekker, New York, 1981).

    Google Scholar 

  32. Rydén, L. Proc. natn. Acad. Sci. U.S.A. 79, 6767–6771 (1982).

    Article  ADS  Google Scholar 

  33. Takahashi, N. et al. Proc. natn. Acad. Sci. U.S.A. 80, 115–119 (1983).

    Article  ADS  CAS  Google Scholar 

  34. Kuiper, H. A. et al. J. molec. Biol. 99, 619–629 (1975).

    Article  CAS  Google Scholar 

  35. Kuiper, H. A., Antonini, E. & Brunori, M. J. molec. Biol. 116, 569–576 (1977).

    Article  CAS  Google Scholar 

  36. Kuiper, H. A. et al. Biochemistry 18, 5849–5854 (1979).

    Article  CAS  Google Scholar 

  37. Antonini, E., Brunori, M., Colosimo, A., Kuiper, H. A. & Zolla, L. Biophys. Chem. 18, 117–124 (1983).

    Article  CAS  Google Scholar 

  38. Folkerts, A. & Van Eerd, J. P. in Invertebrate Oxygen-Binding Proteins (eds Lamy, J. & Lamy, J.) 215–225 (Marcel Dekker, New York, 1981).

    Google Scholar 

  39. van Schaick, E. J. M., Schutter, W. G., Gaykema, W. P. J., Schepman, A. M. H. & Hol, W. G. J. J. molec. Biol. 158, 457–485 (1982).

    Article  CAS  Google Scholar 

  40. Dickerson, R. E., Weinzierl, J. E. & Palmer, R. A. Acta crystallogr. B24, 997–1003 (1968).

    Article  CAS  Google Scholar 

  41. Blow, D. M. & Crick, F. H. C. Acta crystallogr. 12, 794–802 (1959).

    Article  CAS  Google Scholar 

  42. Bricogne, G. Acta crystallogr. A32, 832–847 (1976).

    Article  Google Scholar 

  43. Gaykema, W. P. J., Van Schaick, E. J. M., Schutter, W. & Hol, W. G. J. Chemica Scripta 21, 19–23 (1983).

    CAS  Google Scholar 

  44. Van den Berg, A. A., Gaastra, W. & Kuiper, H. A. in Structure and Function of Haemocyanin (ed. Bannister, J. V.) 6–12 (Springer, Berlin, 1977).

    Book  Google Scholar 

  45. Deisenhofer, J. Biochemistry 20, 2361–2370 (1981).

    Article  CAS  Google Scholar 

  46. Wilson, I. A., Skehel, J. J. & Wiley, D. C. Nature 289, 366–373 (1981).

    Article  ADS  CAS  Google Scholar 

  47. Varghese, J. N., Laver, W. G. & Colman, P. M. Nature 303, 35–40 (1983).

    Article  ADS  CAS  Google Scholar 

  48. Kuiper, H. A., Coletta, M., Zolla, L., Chiancone, E. & Brunori, M. Biochim. biophys. Acta 626, 412–416 (1980).

    Article  CAS  Google Scholar 

  49. Ringe, D., Petsko, G. A., Yamakura, F., Suzuki, K. & Ohmori, D. Proc. natn. Acad. Sci. U.S.A. 80, 3879–3883 (1983).

    Article  ADS  CAS  Google Scholar 

  50. Stalling, W. C., Powers, T. B., Pattridge, K. A., Fee, J. A. & Ludwig, M. L. Proc. natn. Acad. Sci. U.S.A. 80, 3884–3888 (1983).

    Article  ADS  Google Scholar 

  51. Brown, J. M., Powers, L., Kincaid, B., Larrabee, J. A. & Spiro, T. G. J. Am. chem. Soc. 102, 4210–4216 (1980).

    Article  CAS  Google Scholar 

  52. Larrabee, J. A. & Spiro, Th. G. J. Am. chem. Soc. 102, 4217–4223 (1980).

    Article  CAS  Google Scholar 

  53. Co, M. S., Hodgson, K. O., Eccles, Th. K. & Lontie, R. J. Am. chem. Soc. 103, 984–986 (1981).

    Article  CAS  Google Scholar 

  54. Lerch, K. Proc. natn. Acad. Sci. U.S.A. 75, 3635–3639 (1978).

    Article  ADS  CAS  Google Scholar 

  55. Briving, C. thesis, Univ. Göteborg (1975).

  56. Briving, C., Gandvik, E.-K. & Nyman, P. O. Biochem. biophys. Res. Commun. 93, 454–461 (1980).

    Article  CAS  Google Scholar 

  57. Brouwer, M., Wolters, M. & Van Bruggen, E. F. J. Biochemistry 15, 2618–2623 (1976).

    Article  CAS  Google Scholar 

  58. Siezen, R. J. & Van Bruggen, E. F. J. J. molec. Biol. 90, 77–89 (1974).

    Article  CAS  Google Scholar 

  59. Gielens, C., Verschueren, L. J., Préaux, G. & Lontie, R. Eur. J. Biochem. 103, 463–470 (1980).

    Article  CAS  Google Scholar 

  60. Van Holde, K. E. Life Chem. Rep. l, Suppl. 1, 403–412 (1983).

    Google Scholar 

  61. Richardson, J. S., Richardson, D. C., Thomas, K. A., Silverton, E. W. & Davies, D. R. J. molec. Biol. 102, 221–225 (1976).

    Article  CAS  Google Scholar 

  62. Tainer, J. A., Getzoff, E. D., Beem, K. M., Richardson, J. S. & Richardson, D. C. J. molec. Biol. 160, 181–217 (1982).

    Article  CAS  Google Scholar 

  63. Epp. O. et al. Eur. J. Biochem. 45, 513–524 (1974).

    Article  CAS  Google Scholar 

  64. Magnus, K. A. & Love, W. E. J. molec. Biol. 116, 171–173 (1977).

    Article  CAS  Google Scholar 

  65. Magnus, K. A. & Love, W. E. Life Chem. Rep. 1, Suppl. 1, 61–64 (1983).

    CAS  Google Scholar 

  66. Sim, G. A. Acta crystallogr. 12, 813–815 (1959).

    Article  CAS  Google Scholar 

  67. Bernstein, F. C. et al. J. molec. Biol. 112, 535–542 (1977).

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Biomolecular Study Centre (BIOS), University of Groningen, Nijenborgh 16, 9747 AG, Groningen, The Netherlands

    W. P. J. Gaykema, W. G. J. Hol, J. M. Vereijken, N. M. Soeter, H. J. Bak & J. J. Beintema

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Gaykema, W., Hol, W., Vereijken, J. et al. 3.2 Å structure of the copper-containing, oxygen-carrying protein Panulirus interruptus haemocyanin. Nature 309, 23–29 (1984). https://doi.org/10.1038/309023a0

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