Structural basis of the ferrous iron specificity of the yeast ferroxidase, Fet3p

Biochemistry

Volumn 45, Issue 42, 2006, Pages 12741-12749

  Stoj, Christopher S ^a,c   Augustine, Anthony J ^b   Zeigler, Lynn ^a   Solomon, Edward I ^b   Kosman, Daniel J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b STANFORD UNIVERSITY   (United States)

^c NIAGARA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ELECTRON TRANSITIONS; IRON; OXIDATION; SUBSTRATES; YEAST;

FUNGAL LACCASE; HISTIDINE LIGANDS; MULTICOPPER OXIDASE (MCO); MUTANTS;

ENZYME KINETICS;

CERULOPLASMIN; FERROXIDASE FET3P; FUNGAL PROTEIN; HEPHAESTIN; IRON PERMEASE; LACCASE; MULTICOPPER OXIDASE; PROTEIN FTR1P; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; BINDING SITE; CARBOXYLATION; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; HYDROGEN BOND; IRON METABOLISM; NONHUMAN; OXIDATION; PRIORITY JOURNAL; REDUCTION; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS;

AMINO ACID SUBSTITUTION; CERULOPLASMIN; IRON; KINETICS; POTENTIOMETRY; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROPHOTOMETRY; SUBSTRATE SPECIFICITY;

EID: 33750310022     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061543+     Document Type: Article

References (40)

1. Solomon, E. I., Sundaram, U. M., and Machonkin, T. E. (1996) Multicopper oxidases and oxygenases, Chem. Rev. 96, 2563-2605.
2. Stoj, C. S., and Kosman, D. J. (2005) Copper Oxidases, in Encyclopedia of Inorganic Chemistry (King, R. B., Ed.) pp 1134-1159, John Wiley, New York.
3. Stoj, C., and Kosman, D. J. (2003) Cuprous oxidase activity of yeast Fet3p and human ceruloplasmin: Implication for function, FEBS Lett. 554, 422-426.
4. Kosman, D. J. (2002) Fet3p, ceruloplasmin, and the role of copper in iron metabolism, in Advances in Protein Chemistry (Valentine, J. S., and Gralla, E., Eds.) pp 221-269, Elsevier, New York.
5. Hellman, N. E., and Gitlin, J. D. (2002) Ceruloplasmin metabolism and function, Annu. Rev. Nutr. 22, 439-458.
6. Osaki, S., Johnson, D. A., and Frieden, E. (1966) The possible significance of the ferrous oxidase activity of ceruloplasmin in normal human serum, J. Biol. Chem. 241, 2746-2751.
7. Griffiths, T. A. M., Mauk, A. G., and MacGillivray, R. T. A. (2005) Recombinant expression and functional characterization of human hephaestin: A multicopper oxidase with ferroxidase activity, Biochemistry 44, 14725-14731.
8. Vulpe, C. D., Kuo, Y. M., Murphy, T. L., Cowley, L., Askwith, C., Libina, N., Gitschier, J., and Anderson, G. J. (1999) Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse, Nat. Genet. 21, 195-199.
9. Askwith, C., Eide, D., Van Ho, A., Bernard, P. S., Li, L., Davis-Kaplan, S., Sipe, D. M., and Kaplan, J. (1994) The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake, Cell 76, 403-410.
10. Hassett, R. F., Yuan, D. S., and Kosman, D. J. (1998) Spectral and kinetic properties of the Fet3 protein from Saccharomyces cerevisiae, a multinuclear copper ferroxidase enzyme, J. Biol. Chem. 273, 23274-23282.
11. Urbanowski, J. L., and Piper, R. C. (1999) The iron transporter Fth1p forms a complex with the Fet5 iron oxidase and resides on the vacuolar membrane, J. Biol. Chem. 274, 38061-38070.
12. Chidambaram, M. V., Barnes, G., and Frieden, E. (1983) Ceruloplasmin and the reactions forming diferric transferrin, FEBS Lett. 159, 137-140.
13. Stearman, R., Yuan, D. S., Yamaguchi-Iwai, Y., Klausner, R. D., and Dancis, A. (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast, Science 271, 1552-1557.
14. Quintanar, L., Gebhard, M., Wang, T. P., Kosman, D. J., and Solomon, E. I. (2004) Ferrous binding to the multicopper oxidases Saccharomyces cerevisiae Fet3p and human ceruloplasmin: Contributions to ferroxidase activity, J. Am. Chem. Soc. 126, 6579-6589.
15. Wang, T. P., Quintanar, L., Severance, S., Solomon, E. I., and Kosman, D. J. (2003) Targeted suppression of the ferroxidase and iron trafficking activities of the multicopper oxidase Fet3p from Saccharomyces cerevisiae, J. Biol. Inorg. Chem. 8, 611-620.
16. Ducros, V., Brzozowski, A. M., Wilson, K. S., Brown, S. H., Ostergaard, P., Schneider, P., Yaver, D. S., Pedersen, A. H., and Davies, G. J. (1998) Crystal structure of the type 2 Cu depleted laccase from Coprinus cinereus at 2.2 Å resolution, Nat. Struct. Biol. 5, 310-316.
17. Machonkin, T. E., Quintanar, L., Palmer, A. E., Hassett, R., Severance, S., Kosman, D. J., and Solomon, E. I. (2001) Spectroscopy and reactivity of the type 1 copper site in Fet3p from Saccharomyces cerevisiae: Correlation of structure with reactivity in the multicopper oxidases, J. Am. Chem. Soc. 123, 5507-5517.
18. Machonkin, T. E., and Solomon, E. I. (2000) The thermodynamics, kinetics, and molecular mechanism of intramolecular electron transfer in human ceruloplasmin, J. Am. Chem. Soc. 122, 12547-12560.
19. Taylor, A. B., Stoj, C. S., Ziegler, L., Kosman, D. J., and Hart, P. J. (2005) The copper-iron connection in biology: Structure of the metallo-oxidase Fet3p, Proc. Natl. Acad. Sci. U.S.A. 102, 15459-15464.
20. Singh, A., Severance, S., Kaur, N., Wiltsie, W., and Kosman, D. J. (2006) Assembly, activation and trafficking of the Fet3p, Ftr1p high affinity iron permease complex in Saccharomyces cerevisiae, J. Biol. Chem. 281, 13355-13564.
21. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
22. Felsenfeld, G. (1960) The determination of cuprous ion in copper proteins, Arch. Biochem. Biophys. 87, 247-251.
23. Xu, F., Palmer, A. E., Yaver, D. S., Berka, R. M., Gambetta, G. A., Brown, S. H., and Solomon, E. I. (1999) Targeted mutations in a Trametes villosa laccase. Axial perturbations of the T1 copper, J. Biol. Chem. 274, 12372-12375.
24. Yanagisawa, S., and Dennison, C. (2005) Reduction potential tuning at a type 1 copper site does not compromise electron transfer reactivity, J. Am. Chem. Soc. 127, 16453-16459.
25. 2 reactivity of the trinuclear Cu cluster of mutants of the multicopper oxidase Fet3p, Biochemistry 41, 6438-6448.
26. Quintanar, L., Stoj, C., Wang, T. P., Kosman, D. J., and Solomon, E. I. (2005) Role of aspartate 94 in the decay of the peroxide intermediate in the multicopper oxidase Fet3p, Biochemistry 44, 6081-6091.
27. Kwok, E. Y., Severance, S., and Kosman, D. J. (2006) Evidence for iron channeling in the Fet3p-Ftr1p high-affinity iron uptake complex in the yeast plasma membrane, Biochemistry 45, 6317-6327.
28. Zaitseva, I., Zaitsev, V., Card, G., Moshkov, K., Bax, B., Ralph, A., and Lindley, P. (1996) The X-ray structure of human ceruloplasmin at 3.1 Å: Nature of the copper centres, J. Biol. Inorg. Chem. 1, 15-23.
29. Lindley, P. F., Card, G., Zaitseva, I., Zaitsev, V., Reinhammar, B., Selin-Lindgren, E., and Yoshida, K. (1997) An X-ray structural study of human ceruloplasmin in relation to ferroxidase activity, J. Biol. Inorg. Chem. 2, 454-463.
30. Bonaccorsi di Patti, M. C., Pascarella, S., Catalucci, D., and Calabrese, L. (1999) Homology modeling of the multicopper oxidase Fet3 gives new insights in the mechanism of iron transport in yeast, Protein Eng. 12, 895-897.
31. Bonaccorsi di Patti, M. C., Felice, M. R., Camuti, A. P., Lania, A., and Musci, G. (2000) The essential role of Glu-185 and Tyr-354 residues in the ferroxidase activity of Saccharomyces cerevisiae Fet3, FEBS Lett. 472, 283-286.
32. Ackers, G. K., and Smith, F. R. (1985) Effects of site-specific amino acid modification on protein interactions and biological function, Annu. Rev. Biochem. 54, 597-629.
33. Wells, J. A. (1990) Additivity of mutational effects in proteins, Biochemistry 29, 8509-8517.
34. Marcus, R. A., and Sutin, N. (1985) Electron transfer in chemistry and biology, Biochim. Biophys. Acta 811, 265-322.
35. DeBeer George, S., Basumallick, L., Szilagyi, R. K., Randall, D. W., Hill, M. G., Nersissian, A. M., Valentine, J. S., Hedman, B., Hodgson, K. O., and Solomon, E. I. (2003) Spectroscopic investigation of stellacyanin mutants: Axial ligand interactions at the blue copper site, J. Am. Chem. Soc. 125, 11314-11328.
36. Olsson, M. H., Ryde, U., and Roos, B. O. (1998) Quantum chemical calculations of the reorganization energy of blue-copper proteins, Protein Sci. 7, 2659-2668.
37. Betts, J. N., Beratan, D. N., and Onuchic, J. N. (1992) Mapping electron tunneling pathways: An algorithm that finds the "minimum length"/maximum coupling pathway between electron donors and acceptors in proteins, J. Am. Chem. Soc. 114, 4063-4046.
38. Roberts, S. A., Wildner, G. F., Grass, G., Weichsel, A., Ambrus, A., Rensing, C., and Montfort, W. R. (2003) A labile regulatory copper ion lies near the T1 copper site in the multicopper oxidase CueO, J. Biol. Chem. 278, 31958-31963.
39. Bertrand, T., Jolivalt, C., Briozzo, P., Caminade, E., Joly, N., Madzak, C., and Mougin, C. (2002) Crystal structure of a four-copper laccase complexed with an arylamine: Insights into substrate recognition and correlation with kinetics, Biochemistry 41, 7325-7333.
40. Reinhammar, B. R. (1972) Oxidation-reduction potentials of the electron acceptors in laccases and stellacyanin, Biochim. Biophys. Acta 275, 245-259.