Solution structures of 2×6-meric and 4×6-meric hemocyanins of crustaceans Carcinus aestuarii, Squilla mantis and Upogebia pusilla

Journal of Structural Biology

Volumn 171, Issue 1, 2010, Pages 1-10

  Mičetić, Ivan ^a   Losasso, Carmen ^b   Muro, Paolo Di ^a   Tognon, Giuseppe ^a   Benedetti, Piero ^a   Beltramini, Mariano ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b REFERRAL CANCER CENTER OF BASILICATA   (Italy)

Author keywords

Hemocyanin; Oligomeric proteins; Quaternary structure; Solution scattering

Indexed keywords

HEMOCYANIN; OXYGEN;

ARTHROPOD; ARTICLE; BINDING KINETICS; BINDING SITE; CRAB; CRUSTACEA; ELECTRON MICROSCOPY; IMAGE ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN QUATERNARY STRUCTURE; RADIATION SCATTERING; SHRIMP;

ANIMALS; BINDING SITES; CRUSTACEA; HEMOCYANIN; MODELS, MOLECULAR; OXYGEN; PROTEIN STRUCTURE, QUATERNARY; SCATTERING, SMALL ANGLE; X-RAY DIFFRACTION;

ARTHROPODA; CARCINUS AESTUARII; CRUSTACEA; DECAPODA (CRUSTACEA); PORTUNIDAE; SQUILLA MANTIS; STOMATOPODA; THALASSINIDAE; UPOGEBIA PUSILLA;

EID: 77953611541     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.03.012     Document Type: Article

References (43)

1. Bijlholt M., van Bruggen E. A model for the architecture of the hemocyanin from the arthropod Squilla mantis (Crustacea, Stomatopoda). Eur. J. Biochem. 1986, 155:339-344.
2. Bijlholt M., van Heel M., van Bruggen M. Comparison of 4×6-meric hemocyanins from three different arthropods using computer alignment and correspondence analysis. J. Mol. Biol. 1982, 161:139-153.
3. Bruneaux M., Terrier P., Leize E., Mary J., Lallier F., Zal F. Structural study of Carcinus maenas hemocyanin by native ESI-MS: interaction with l-lactate and divalent cations. Proteins 2009, 77:589-601.
4. Bubacco L., Magliozzo R.S., Beltramini M., Salvato B., Peisach J. Preparation and spectroscopic characterization of a coupled binuclear center in cobalt(II)-substituted hemocyanin. Biochemistry 1992, 31:9294-9303.
5. Burmester T. Origin and evolution of arthropod hemocyanins and related proteins. J. Comp. Physiol. B. 2002, 172:95-107.
6. Cavellec A., Boisset N., Taveau J.C., Lamy J.N. Image processing of electron-microscopic views of Callianassa californiensis hemocyanin. Invertebrate Dioxygen Carriers 1989, 271-274. Leuven University Press, Louvain. G. Préaux, R. Lontie (Eds.).
7. Cong Y., et al. Structural mechanism of SDS-induced enzyme activity of scorpion hemocyanin revealed by electron cryomicroscopy. Structure 2009, 17:749-758.
8. Corbett K.D., Benedetti P., Berger J.M. Holoenzyme assembly and ATP-mediated conformational dynamics of topoisomerase VI. Nat. Struct. Mol. Biol. 2007, 14:611-619.
9. Dainese E., Di Muro P., Beltramini M., Salvato B., Decker H. Subunits composition and allosteric control in Carcinus aestuarii hemocyanin. Eur. J. Biochem. 1998, 256:350-358.
10. De Haas F., van Bruggen E. The interhexameric contacts in the four-hexameric hemocyanin from the tarantula Eurypelma californicum. A tentative mechanism for cooperative behavior. J. Mol. Biol. 1994, 237:464-478.
11. De Haas F., Bijlholt M., van Bruggen E. 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. 1991, 107:86-94.
12. Decker H., Savel-Niemann A., Körschenhausen D., Eckerskorn E., Markl J. Allosteric oxygen-binding properties of reassembled tarantula (Eurypelma californicum) hemocyanin with incorporated apo- or met-subunits. Biol. Chem. Hoppe Seyler 1989, 370:511-523.
13. Decker H., Hartmann H., Sterner R., Schwarz E., Pilz I. Small-angle X-ray scattering reveals differences between the quaternary structures of oxygenated and deoxygenated tarantula hemocyanin. FEBS Lett. 1996, 393:226-230.
14. Dolashka-Angelova P., et al. Structure of hemocyanin subunit CaeSS2 of the crustacean Mediterranean crab Carcinus aestuarii. J. Biochem. 2005, 138:303-312.
15. Frank J., Radermacher M., Penczek P.A., Zhu J., Li Y., Ladjadj M., Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 1996, 116:190-199.
16. Hartmann H., Decker H. All hierarchical levels are involved in conformational transitions of the 4×6-meric tarantula hemocyanin upon oxygenation. Biochim. Biophys. Acta 2002, 1601:132-137.
17. Hartmann H., Decker H. Small-angle scattering techniques for analyzing conformational transitions in hemocyanins. Methods Enzymol. 2004, 379:81-106.
18. Hartmann H., Lohkamp B., Hellmann N., Decker H. 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. 2001, 276:19954-19958.
19. Hazes B., Magnus K.A., Bonaventura C., Bonaventura J., Dauter Z., Kalk K.H., Hol W.G. Crystal structure of deoxygenated Limulus polyphemus subunit II hemocyanin at 2.18Å resolution: clues for a mechanism for allosteric regulation. Protein Sci. 1993, 2:597-619.
20. Kozin M., Svergun D.I. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 2001, 34:33-41.
21. Kusche K., Hembach A., Hagner-Holler S., Gebauer W., Burmester T. Complete subunit sequences, structure and evolution of the 6×6-mer hemocyanin from the common house centipede, Scutigera coleoptrata. Eur. J. Biochem. 2003, 270:2860-2868.
22. Li Y., Wang Y., Jiang H., Deng J. Crystal structure of Manduca sexta prophenoloxidase provides insights into the mechanism of type 3 copper enzymes. Proc. Natl Acad. Sci. USA 2009, 106:17002-17006.
23. Linzen B., et al. The structure of arthropod hemocyanins. Science 1985, 229:519-524.
24. Ludtke S.J., Baldwin P.R., Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 1999, 128:82-97.
25. Magnus K.A., Hazes B., Ton-That H., Bonaventura C., Bonaventura J., Hol W.G. Crystallographic analysis of oxygenated and deoxygenated states of arthropod hemocyanin shows unusual differences. Proteins 1994, 19:302-309.
26. Markl J., Decker H. Molecular structure of the arthropod hemocyanins. Advances in Comparative and Environmental Physiology 1992, 325-376. Springer-Verlag, Berlin Heidelberg. C.P. Mangum (Ed.).
27. Markl J., Moeller A., Martin A., Rheinbay J., Gebauer W., Depoix F. Ten-Angstrom CryoEM structure and molecular model of the myriapod (Scutigera) 6×6mer hemocyanin: understanding a giant oxygen transport protein. J. Mol. Biol 2009, 392:362-380.
28. Martin A.G., et al. Limulus polyphemus hemocyanin: 10Å cryo-EM structure, sequence analysis, molecular modelling and rigid-body fitting reveal the interfaces between the eight hexamers. J. Mol. Biol. 2007, 366:1332-1350.
29. Meissner U., Stohr M., Kusche K., Burmester T., Stark H., Harris R., Orlova E.V., Markl J. Quaternary structure of the European spiny lobster (Palinurus elephas) 1×6-mer hemocyanin from cryoEM and amino acid sequence data. J. Mol. Biol. 2003, 325:99-109.
30. Narayanan T., Diat O., Bösecke P. SAXS and USAXS on the high brilliance beamline at the ESRF. Nucl. Instrum. Methods A 2001, 467:1005-1009.
31. Ohi M., Li Y., Cheng Y., Walz T. Negative staining and image classification - powerful tools in modern electron microscopy. Biol. Proced. Online 2004, 6:23-34.
32. Paoli M., Giomi F., Hellmann N., Jaenicke E., Di Muro P., Beltramini M. The molecular heterogeneity of hemocyanin: Structural and functional properties of the 4×6-meric protein of Upogebia pusilla (Crustacea). Gene 2007, 398:177-182.
33. Petoukhov M.V., Svergun D.I. Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys. J. 2005, 89:1237-1250.
34. Salvato B., Beltramini M. Hemocyanins: molecular architecture, structure and reactivity of the binuclear copper active site. Life Chem. Rep. 1990, 8:1-47.
35. Svergun D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 1992, 25:495-503.
36. Svergun D.I., Semenyuk A., Feigin L. Small-angle-scattering-data treatment by the regularization method. Acta Crystallogr. A 1988, 44:244-250.
37. Svergun D.I., Barberato C., Koch M.H.J. CRYSOL - a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 1995, 28:768-773.
38. Taveau J.C., Boisset N., Lamy J., Lambert O., Lamy J.N. Three-dimensional reconstruction of Limulus polyphemus hemocyanin from cryoelectron microscopy. J. Mol. Biol. 1997, 266:1002-1015.
39. van Heel M., Dube P. Quaternary structure of multihexameric arthropod hemocyanins. Micron 1994, 25:387-418.
40. Voit R., Feldmaier-Fuchs G., Schweikardt T., Decker H., Burmester T. Complete sequence of the 24-mer hemocyanin of the tarantula Eurypelma californicum. Structure and intramolecular evolution of the subunits. J. Biol. Chem. 2000, 275:39339-39344.
41. Volbeda A., Hol W.G. Crystal structure of hexameric haemocyanin from Panulirus interruptus refined at 3.2Å resolution. J. Mol. Biol. 1989, 209:249-279.
42. Volkov V.V., Svergun D.I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 2003, 36:860-864.
43. Wriggers W., Chacon P. Using situs for the registration of protein structures with low-resolution bead models from X-ray solution scattering. J. Appl. Crystallogr. 2001, 34:773-776.