Synchrotron SAXS studies on the structural stability of Carcinus aestuarii hemocyanin in solution

Biophysical Journal

Volumn 85, Issue 4, 2003, Pages 2661-2672

  Spinozzi, Francesco ^a   Maccioni, Elisabetta ^a   Teixeira, Cilâine Verônica ^a,e   Amenitsch, Heinz ^b   Favilla, Roberto ^c   Goldoni, Matteo ^c   Di Muro, Paolo ^d   Salvato, Benedetto ^d   Mariani, Paolo ^a   Beltramini, Mariano ^d  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b Institute of Biophysics and X ray Structure   (Austria)

^c UNIVERSITY OF PARMA   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOCYANIN; MONOMER; PROTEIN CAESS2; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CALCULATION; CARCINUS AESTUARII; CONCENTRATION RESPONSE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRAB; MOLECULAR MODEL; MOLECULAR STABILITY; NONHUMAN; OLIGOMERIZATION; PROTEIN AGGREGATION; PROTEIN DENATURATION; PROTEIN STABILITY; RADIATION; STRUCTURE ANALYSIS; SYNCHROTRON; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ANIMALIA; CARCINUS; CARCINUS AESTUARII; DECAPODA (CRUSTACEA); INVERTEBRATA;

EID: 12444272581     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74689-X     Document Type: Article

References (60)

1. Ashton, A. W., M. K. Boehm, J. R. Gallimore, M. B. Pepys, and S. J. Perkins. 1997. Pentameric and decameric structures in solution of serum amyloid P component by x-ray and neutron scattering and molecular modelling analyses. J. Mol. Biol. 272:408-422.
2. Beltramini, M., E. Borghi, P. Di Muro, A. Magaldi, A. La Monaca, B. Salvato, C. Santini, and G. Tognon. 1993. SAXS on invertebrate dioxygen carriers. J. Phys. IV. C8 3:249-252.
3. Beltramini, M., E. Borghi, P. Di Muro, A. La Monaca, B. Salvato, and C. Santini. 1996. The use of SAXS in the study of quaternary organisation of giant proteins. J. Mol. Struct. 383:231-236.
4. Beltramini, M., P. Di Muro, R. Favilla, A. La Monaca, P. Mariani, A. Sabatucci, B. Salvato, and P. L. Solari. 1999. SAXS investigations on the temperature dependence of the conformation of 5S hemocyanin subunit of Carcinus aestuarii. J. Mol. Struct. 475:73-82.
5. Bonafe, C. F. S., J. R. V. Araujo, and J. L. Silva. 1994. Intermediate states of assembly in the dissociation of gastropod hemocyanin by hydrostatic pressure. Biochemistry. 33:2651-2660.
6. Bubacco, L., R. S. Magliozzo, M. Beltramini, B. Salvato, and J. Peisach. 1992. Preparation and spectroscopic characterization of a coupled binuclear center in Co(II) substituted hemocyanin. Biochemistry. 31:9294-9303.
7. Calmettes, P., D. Durand, P. Minard, M. Desmadril, V. Receveur, and J. C. Smith. 1994. How random is a highly denatured protein? Biophy. Chem. 53:105-114.
8. Cinelli, S., F. Spinozzi, R. Itri, F. Carsughi, G. Onori, and P. Mariani. 2001. Structural characterisation of the pH-denatured states of ferricytochromec by synchrotron small angle x-ray scattering. Biophys. J. 81:3522-3533.
9. Dainese, E., P. Di Muro, M. Beltramini, B. Salvato, and H. Decker. 1998. Subunits composition and allosteric control in Carcinus aesturarii hemocyanin. Eur. J. Biochem. 256:350-358.
10. Debye, P. 1947. Molecular-weight determination by light scattering. J. Phys. Coll. Chem. 51:18-32.
11. Debye, P., and E. Hückel. 1923. Zur Theorie der Elektrolyte. I. Gefrierpunktserniedrigung und verwandte Erscheinungen. 24:185-206.
12. Decker, H., H. Hartmann, R. Stemer, E. Schwarz, and I. Pilz. 1996. Small-angle x-ray scattering reveals differences between the quatemary structures of oxygenated and deoxygenated tarantula hemocyanin. FEBS Lett. 393:226-230.
13. Dill, K. A., and D. Shortle. 1991. Denatured states of proteins. Annu. Rev. Biochem. 60:795-825.
14. Durstewitz, G., and N. B. Terwilliger. 1997. cDNA cloning of a developmentally regulated hemocyanin subunit in the crustacean Cancer magister and phylogenetic analysis of the hemocyanin gene family. Mol. Biol. Evol. 14:266-276.
15. Favilla, R., M. Goldoni, A. Mazzini, P. Di Muro, B. Salvato, and M. Beltramini. 2002a. Guanidinium chloride induced unfolding of a hemocyanin subunit from Carcinus aestuarii. I. Apo form. Biochim. Biophys. Acta. 1597:42-50.
16. Favilla, R., M. Goldoni, F. Del Signore, P. Di Muro, B. Salvato, and M. Beltramini. 2002b. Guanidinium chloride induced unfolding of a hemocyanin subunit from Carcinus aestuarii. II. Holo form. Biochim. Biophys. Acta. 1597:51-59.
17. Feigin, L. A., and D. I. Svergun. 1987. Structure analysis by small-angle x-ray and neutron scattering. New York, Plenum Press.
18. Flory, P. 1971. Principles of Polymer Chemistry. Cornell University Press, Ithaca, NY.
19. Gaykema, W. P. J., W. G. J. Hol., J. M. Vereijken, N. M. Soeter, H. J. Bak, and J. J. Beintema. 1984. A structure of the copper-containing oxygen-carrying protein Palinurus interruptus hemocyanin. Nature. 309:23-29.
20. Grossmann, J. G., S. A. Ali, A. Abbasi, Z. Zaidi, S. Stoeva, W. Voelter, and S. S. Hasnain. 2000. Low-resolution molecular structures of isolated functional units from arthropodan and molluscan hemocyanin. Biophys. J. 78:977-981.
21. Guinier, A., and G. Fournet. 1955. Small Angle Scattering of X-Rays. Wiley, New York.
22. Hansen, S. 1990. Calculation of small-angle scattering profiles using Monte Carlo simulation. J. Appl. Crystallogr. 23:344-346.
23. Hartmann, H., and H. Decker. 2002. All hierarchical levels are involved in conformational transitions of the 4 × 6-meric tarantula hemocyanin upon oxygenation. Biochim. Biophys. Acta. 1601:132-137.
24. Hartmann, H., B. Lohkamp, N. Hellmann, and H. Decker. 2001. The allosteric effector L-lactate induces a conformational change of 2 × 6-meric lobster hemocyanin in the oxy state as revealed by small angle x-ray scattering. J. Biol. Chem. 276:19954-19958.
25. Hazes, B., K. A. Magnus, C. Bonaventura, J. Bonaventura, Z. Dauter, K. H. Kalk, and W. G. Hol. 1993. Crystal structure of deoxygenated Limulus polyphemus subunit II hemocyanin at 2.18 Ångstroms resolution: clues for a mechanism for allosteric regulation. Protein Sci. 2:597-619.
26. Henderson, S. J. 1996. Monte Carlo modelling of small-angle scattering data from non-interacting homogeneous and heterogeneous particles in solution. Biophys. J. 70:1618-1627.
27. Herskovits, T. T., M. W. Russell, and S. E. Carberry. 1984. Light-scattering investigation of the subunit structure and sequential dissociation of Homarus americanus hemocyanin. Biochemistry. 23:1875-1881.
28. Hübler, R., B. Fertl, N. Hellmann, and H. Decker. 1998. On the stability of the 24-meric hemocyanin from Eurypelma californicum. Biochim. Biophys. Acta. 1383:327-339.
29. Jacrot, B. 1976. The study of biological structures by neutron scattering from solution. Rep. Prog. Phys. 39:911-953.
30. Jacrot, B., and G. Zaccai. 1981. Determination of molecular weight by neutron scattering. Biopolymers. 20:2413-2426.
31. Kataoka, M., I. Nishii, T. Fujisawa, T. Ueki, F. Tokunaga, and Y. Goto. 1995. Structural characterization of molten globule and native states of apomyoglobin by solution x-ray scattering. J. Mol. Biol. 249:215-228.
32. Kataoka, M., Y. Hagihara, K. Mihara, and Y. Goto. 1993. Molten globule of cytochrome c studied by the small angle x-ray scattering. J. Mol. Biol. 229:591-596.
33. Kozin, M. B., V. V. Volkov, and D. I. Svergun. 1997. ASSA-a program for three-dimensional rendering in solution scattering from biopolymers. J. Appl. Crystallogr. 30:811-815.
34. Kratky, O., and G. Porod. 1949. Röntgenuntersuchung gelöster fadenmoleküle. Rec. Trav. Chim. Pays-Bas. 68:1106-1123.
35. Linzen, B., N. M. Soeter, A. F. Riggs, H. J. Schneider, W. Schartau, M. D. Moore, E. Yokota, P. Q. Behrens, H. Nakashima, T. Takagi, T. Nemoto, J. M. Vereijken, H. J. Bak, J. J. Beintema, A. Voldeba, W. P. J. Gaykema, and W. G. J. Hol. 1985. The structure of arthropod hemocyanins. Science. 229:519-524.
36. Magnus, K. A., E. E. Lattman, A. Volbeda, and W. G. J. Hol. 1991. Hexamers of subunit II from Limulus hemocyanin (a 48-mer) have the same quaternary structure as whole Panulirus hemocyanin molecules. Proteins Strucr. Funct. Gen. 9:240-247.
37. Mangum, C. P., J. Greaves, and J. S Rainer. 1991. Oligomer composition and oxygen binding of the hemocyanin of the blue crab Callinectes sapidus. Biol. Bull. 181:453-458.
38. Mariani, P., F. Carsughi, F. Spinozzi, S. Romanzetti, G. Meier, R. Casadio, and C. M. Bergamini. 2000. Ligand-induced conformational changes in tissue transglutaminase: Monte Carlo analysis of small-angle scattering data. Biophys. J. 78:3240-3251.
39. Markl, J., A. Hofer, G. Bauer, A. Markl, B. Kempter, M. Brenzinger, and B. Linzen. 1979a. Subunit heterogeneity in arthropod hemocyanin: crustacea. J. Comp. Physiol. 133:167-175.
40. Markl, J., A. Markl, W. Schartau, and B. Linzen. 1979b. Subunit heterogeneity in arthropod hemocyanin: chelicerata. J. Comp. Physiol. 130:283-292.
41. Markl, J., and H. Decker. 1992. Molecular structure of the arthropod hemocyanins. In Advances of Environmental Biochemistry and Physiology. C.P. Mangum, editor. Springer-Verlag, Berlin, Germany. pp.325-376.
42. Molon, A., P. Di Muro, L. Bubacco, V. Vasilyev, B. Salvato, M. Beltramini, W. Conze, N. Hellmann, and H. Decker. 2000. Molecular heterogeneity of the hemocyanin isolated from the king crab Paralithodes camtschaticae. Eur. J. Biochem. 267:7046-7057.
43. Pedersen, J. S., and P. Schurtenberger. 1996. Scattering functions of semiflexible polymers with and without excluded volume effects. Macromolecules. 29:7602-7612.
44. Miller, K. I., and K. E. van Holde. 1974. Oxygen binding by Callianassa californiensis hemocyanin. Biochemistry. 13:1668-1674.
45. Pérez, J., P. Vachette, D. Russo, M. Desmadril, and D. Durand. 2001. Heat-induced unfolding of neocarzinostatin, a small all-protein investigated by small-angle x-ray scattering. J. Mol. Biol. 308:721-743.
46. Pilz, I., K. Goral, M. Hoylaerts, R. Witters, and R. Lontie. 1980. Studies by small-angle x-ray scattering of the quaternary structure of the 24-S component of the haemocyanin of Astacus leptodactylus in solution. Eur. J. Biochem. 105:539-543.
47. Pollack, L., M. W. Tate, N. C. Darnton, J. B. Knight, S. M. Gruner, W. A. Eaton, and R. H. Austin. 1999. Compactness of the denatured state of a fast-folding protein measured by submillisecond small angle x-ray scattering. Proc. Natl. Acad. Sci. USA. 96:10115-10117.
48. Salvato, B., and M. Beltramini. 1990. Hemocyanins: molecular architecture, structure and reactivity of the binuclear copper active site. Life Chem. Rep. 8:1-47.
49. Semisotnov, G. V., H. Kihara, N. V. Kotova, K. Kimura, Y. Amemiya, K. Wakabayashi, I. N. Serdyuk, A. A. Timchenko, K. Chiba, K. Nikaido, T. Ikura, and K. Kuwajima. 1996. Protein globularization during folding. A study by synchrotron small-angle x-ray scattering. J. Mol. Biol. 262:559-574.
50. Spinozzi, F., F. Carsughi, and P. Mariani. 1998. Particle shape reconstruction by small-angle scattering. Integration of group theory and maximum entropy to multipole expansion method. J. Chem. Phys. 109:10148-10158.
51. Sterner, R., T. Vogl, H. J. Hinz, F. Penz, R. Hoff, R. Foll, and H. Decker. 1995. Extreme thermostability of tarantula hemocyanin. FEBS Lett. 364:9-12.
52. Svergun, D. I. 1997. Restoring three-dimensional structure of biopolymers from solution scattering. J. Appl. Crystallogr. 30:792-797.
53. Svergun, D., C. Barberato, and M. H. J. Koch. 1995. CRYSOL - a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28:768-773.
54. Taveau, J. C., N. Boisset, J. Lamy, O. Lambert, and J. N. Lamy. 1997. Three-dimensional reconstruction of Limulus polyphemus hemocyanin from cryoelectron microscopy. J. Mol. Biol. 266:1002-1015.
55. Trewhella, J. 1997. Insights into biomolecular function from small-angle scattering. Curr. Opin. Struct. Biol. 7:702-708.
56. van Holde, K. E., and K. I. Miller. 1995. Hemocyanins. Adv. Prot Chem. 47:1-81.
57. Voit, R., G. Feldmaier-Fuchs, T. Schweikardt, H. Decker, and T. Burmester. 2000. Complete sequence of the 24-mer hemocyanin of the tarantula Europlema californicum. J. Biol. Chem. 275:39339-39344.
58. Volbeda, A., and W. G. J. Hol. 1989a. Crystal structure of hexameric hemocyanin from Panulirus interruptus refined at 3.2 Å resolution. J. Mol. Biol. 209:249-279.
59. Volbeda, A., and W. G. J. Hol. 1989b. Pseudo twofold symmetry in the copper-binding domain of arthropodan haemocyanins. J. Mol. Biol. 206:531-546.
60. Zlateva, T., P. Di Muro, B. Salvato. and M. Beltramini. 1996. The o-diphenol oxidase activity of arthropod hemocyanin. FEBS Lett. 384:251-254.