Quaternary structure of the European spiny lobster (Palinurus elephas) 1 × 6-mer hemocyanin from cryoEM and amino acid sequence data

Journal of Molecular Biology

Volumn 325, Issue 1, 2003, Pages 99-109

  Meissner, Ulrich ^a   Stohr, Michael ^a   Kusche, Kristina ^a   Burmester, Thorsten ^a   Stark, Holger ^b   Harris, J Robin ^a   Orlova, Elena V ^c   Markl, Jürgen ^a   Baumeister, W ^d  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d NONE

Author keywords

3D reconstruction; 3D EM, cryoelectron microscopy (cryoEM); Crustacea; Hemocyanin; Quaternary structure

Indexed keywords

HEMOCYANIN; PROTEIN SUBUNIT;

ALPHA HELIX; AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DENSITY; ELECTRON MICROSCOPY; EUROPE; LOBSTER; MOLECULAR WEIGHT; NONHUMAN; PARTICULATE MATTER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; RELIABILITY; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; X RAY ANALYSIS;

ARTHROPODA; CRUSTACEA; ELEPHAS; PALINURUS ELEPHAS; PALINURUS INTERRUPTUS; PALINURUS VULGARIS; PANULIRUS INTERRUPTUS; PONTOPHILUS SPINOSUS; SPINY;

EID: 0037255448     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01173-7     Document Type: Article

References (52)

1. Markl, J. & Decker, H. (1992). Molecular structure of the arthropod hemocyanins. In Advances in Comparative and Environmental Physiology (Mangum, C. P., ed.), vol. 13, pp. 325-376, Springer, Berlin.
2. van Holde, K. E. & Miller, K. I. (1995). Hemocyanins Advances in Protein Chemistry, vol. 47, Academic Press, San Diego pp. 1-81.
3. Meissner, U., Dube, P., Harris, J. R., Stark, H. & Markl, J. (2000). Structure of a molluscan hemocyanin didecamer (HtH1 from Haliotis tuberculata) at 12 Å resolution by cryoelectron microscopy. J. Mol. Biol. 298, 21-34.
4. Markl, J., Stöcker, W., Runzler, R. & Precht, E. (1986). Immunological correspondences between the hemocyanin subunits of 86 arthropods: Evolution of a multigene protein family. In Invertebrate Oxigen Carriers (Linzen, B., ed.), pp. 281-292, Springer, Berlin.
5. Savel-Niemann, A., Markl, J. & Linzen, B. (1988). Hemocyanins in spiders XXII. Range of allosteric interaction in a four-hexamer hemocyanin. Cooperativity and Bohr effect in dissociation intermediates. J. Mol. Biol. 204, 385-395.
6. Robert, C. H., Decker, H., Richey, B., Gill, S. J. & Wyman, J. (1987). Nesting: Hierarchies of allosteric interactions. Proc. Natl. Acad. Sci. USA, 84, 1891-1895.
7. Leidescher, T. & Decker, H. (1990). Conformational changes of tarantula (Eurypelma californicum) hemocyanin detected with a fluorescent probe, 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole. Eur. J. Biochem. 187, 617-625.
8. Sterner, R., Bardehle, K., Paul, R. & Decker, H. (1994). Tris - An allosteric effector of tarantula hemocyanin. FEBS Letters, 339, 37-39.
9. Burmester, T. (2001). Molecular evolution of the arthropod hemocyanin superfamily. Mol. Biol. Evol. 18, 184-195.
10. Burmester, T. (2002). Origin and evolution of arthropod hemocyanins and related proteins. J. Comp. Physiol. [B], 172, 95-117.
11. Gaykema, W. P., Hol, W. G., Vereijken, J. M., Soeter, N. M., Bak, H. J. & Beintema, J. J. (1984). 3.2 Å structure of the copper-containing, oxygen-carrying protein Panulirus interruptus hemocyanin. Nature, 309, 23-29.
12. Hazes, B., Magnus, K. A., Bonaventura, C., Bonaventura, J., Dauter, Z., Kalk, K. H. & Hol, W. G. (1993). Crystal structure of deoxygenated Limulus polyphemus subunit II hemocyanin at 2.18 Å resolution: Clues for a mechanism for allosteric regulation. Protein Sci. 2, 597-619.
13. Gaykema, W. P., Volbeda, A. & Hol, W. G. (1986). Structure determination of Panulirus interruptus hemocyanin at 3.2 Å resolution. Successful phase extension by sixfold density averaging. J. Mol. Biol. 187, 255-275.
14. Volbeda, A. & Hol, W. G. (1989). Crystal structure of hexameric hemocyanin from Panulirus interruptus refined at 3.2 Å resolution. J. Mol. Biol. 209, 249-279.
15. Boisset, N., Radermacher, M., Grassucci, R., Taveau, J. C., Liu, W. P., Lamy, J. et al. (1993). 3-Dimensional immunoelectron microscopy of scorpion hemocyanin labeled with a monoclonal Fab fragment. J. Struct. Biol. 111, 234-244.
16. Boisset, N., Penczek, P., Taveau, J. C., Lamy, J. & Frank, J. (1995). Three-dimensional reconstruction of Androctonus australis hemocyanin labeled with a monoclonal Fab fragment. J. Struct. Biol. 115, 16-29.
17. de Haas, F., Bijlholt, M. & van Bruggen, E. F. (1991). An electron microscopic study of two-hexameric hemocyanins from the crab Cancer pagurus and the tarantula Eurypelma californicum: Determination of their quaternary structure using image processing and simulation models based on X-ray diffraction data. J. Struct. Biol. 107, 86-94.
18. de Haas, F. (1993). Electron Microscopic Studies on Structure and Function of Arthropod Hemocyanins. Thesis. University of Groningen.
19. Taveau, J. C., Boisset, N., Lamy, J., Lambert, O. & Lamy, J. N. (1997). Three-dimensional reconstruction of Limulus polyphemus hemocyanin from cryoelectron microscopy. J. Mol. Biol. 266, 1002-1015.
20. van Heel, M. & Dube, P. (1994). Quaternary structure of multihexameric arthropod hemocyanins. Micron, 25, 387-418.
21. Boisset, N., Taveau, J. C. & Lamy, J. N. (1990). An approach to the architecture of Scutigera coleoptrata hemocyanin by electron microscopy and image processing. Biol. Cell, 68, 73-84.
22. van Heel, M., Gowen, B., Matadeen, R., Orlova, E. V., Finn, R., Pape, T. et al. (2000). Single-particle electron cryo-microscopy: Towards atomic resolution. Quart. Rev. Biophys. 33, 307-369.
23. Harris, J. R., Schroder, E., Isupov, M. N., Scheffler, D., Kristensen, P., Littlechild, J. A. et al. (2001). Comparison of the decameric structure of peroxiredoxin-II by transmission electron microscopy and X-ray crystallography. Biochim. Biophys. Acta, 1547, 221-234.
24. Ludtke, S. J., Jakana, J., Song, J. L., Chuang, D. T. & Chiu, W. (2001). A 11.5 Å single particle reconstruction of GroEL using EMAN. J. Mol. Biol. 314, 253-262.
25. Ranson, N. A., Farr, G. W., Roseman, A. M., Gowen, B., Fenton, W. A., Horwich, A. L. & Saibil, H. R. (2001). ATP-bound states of GroEL captured by cryo-electron microscopy. Cell, 107, 869-879.
26. Bak, H. J. & Beintema, J. J. (1987). Panulirus interruptus hemocyanin. The elucidation of the complete amino acid sequence of subunit a. FEBS Letters, 204, 141-144.
27. Jekel, P. A., Bak, H. J., Soeter, N. M., Vereijken, J. M. & Beintema, J. J. (1988). Panulirus interruptus hemocyanin. The amino acid sequence of subunit b and anomalous behaviour of subunits a and b on poly-acrylamide gel electrophoresis in the presence of SDS. Eur. J. Biochem. 178, 403-412.
28. Kusche, K. & Burmester, T. (2001). Molecular cloning and evolution of lobster hemocyanin. Biochem. Biophys. Res. Commun. 282, 887-892.
29. Orlova, E. V., Dube, P., Harris, J. R., Beckman, E., Zemlin, F., Markl, J. & van Heel, M. (1997). Structure of keyhole limpet hemocyanin type 1 (KLH1) at 15 Å resolution by electron cryo-microscopy and angular reconstitution. J. Mol. Biol. 271, 417-437.
30. Neuteboom, B., Jekel, P. A. & Beintema, J. J. (1992). Primary structure of hemocyanin subunit c from Panulirus interruptus. Eur. J. Biochem. 206, 243-249.
31. Grimes, J. M., Fuller, S. D. & Stewart, D. I. (1999). Complementing crystallography: The role of cryo-electron microscopy in structural biology. Acta Crystallog. Sect. D, 55, 1742-1749.
32. de Haas, F., van Breemen, J. F., Boekema, E. J., Keegstra, W. & van Bruggen, E. F. (1993). Comperative electron microscopy and image analysis of oxy- and deoxy-hemocyanin from the spiny lobster Panulirus interruptus. Ultramicroscopy, 49, 426-435.
33. Burmester, T. (1999). Evolution and function of the insect hexamerins. Eur. J. Entomol. 96, 213-225.
34. Telfer, W. H. & Kunkel, J. G. (1991). The function and evolution of insect storage hexamers. Annu. Rev. Entomol. 36, 205-228.
35. Decker, H., Ryan, M., Jaenicke, E. & Terwilliger, N. (2001). SDS-induced phenoloxidase activity of hemocyanins from Limulus polyphemus, Eurypelma californicum, and Cancer magister. J. Biol. Chem. 276, 17796-17799.
36. Chirgwin, J. M., Przbyla, A. E., MacDonald, R. J. & Rutter, W. J. (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry, 18, 5294.
37. Adrian, M., Dubrochet, J., Lepault, J. & McDowall, A. W. (1984). Cryo-electron microscopy of viruses. Nature, 308, 32-36.
38. van Heel, M., Harauz, G., Orlova, E. V., Schmidt, R. & Schatz, M. (1996). A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24.
39. Zhou, Z. H., Hardt, S., Wang, B., Sherman, M. B., Jakana, J. & Chiu, W. (1996). CTF determination of images of ice-embedded single particles using a graphics interface. J. Struct. Biol. 116, 216-222.
40. Dube, P., Tavares, P., Lurz, R. & van Heel, M. (1993). The portal protein of bacteriophage SPP1: A DNA pump with 13-fold symmetry. EMBO J. 12, 1303-1309.
41. van Heel, M., Winkler, H., Orlova, E. & Schatz, M. (1992). Structure analysis of ice-embedded single particles. Scanning Microsc. Suppl. 6, 23-42.
42. Serysheva, I. I., Orlova, E. V., Chiu, W., Sherman, M. B., Hamilton, S. L. & van Heel, M. (1995). Electron cryomicroscopy and angular reconstitution used to visualize the skeletal muscle calcium release channel. Nature Struct. Biol. 2, 18-24.
43. Harauz, G., Borland, L., Bahr, G. F., Zeitler, E. & van Heel, M. (1987). Three-dimensional reconstruction of a human metaphase chromosome from electron micrographs. Chromosoma, 95, 366-374.
44. Orlova, E. V. (2000). Structural analysis of non-crystalline macromolecules: The ribosome. Acta Crystallog. Sect. D, 56, 1253-1258.
45. Peitsch, M. C. (1996). ProMod and swiss-model: Internet-based tools for automated comparative protein modelling. J. Struct. Biol. 136, 190-200.
46. Guex, N. & Peitsch, M. C. (1997). Swiss-model and the Swiss-Pdb viewer: An environment for comparative protein modelling. Electrophoresis, 18, 2714-2723.
47. Peitsch, M. C. (1995). Protein modelling by E-mail. Bio/Technology, 13, 658-660.
48. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. Sect. A, 47, 110-119.
49. Vagin, A. A. & Isupov, M. N. (2001). Spherically averaged phased translation function and its application to the search for molecules and fragments in electron-density maps. Acta Crystallog., Sect. D, 57, 1451-1456.
50. Crowther, R. A. (1972). The fast rotation function. In The Molecular Replacement Method (Rossmann, M. G., ed.), pp. 173-178, Gordon & Breach, New York.
51. Bentley, G. A. (1997). Phase transfer function. Methods Enzymol. 276, 611-619.
52. Linzen, B., Soeter, N. M., Riggs, A. F., Schneider, H. J., Schartau, W., Moore, M. D. et al. (1985). The structure of arthropod hemocyanins. Science, 229, 519-524.