Evidence for iron channeling in the Fet3p-Ftr1p high-affinity iron uptake complex in the yeast plasma membrane

Biochemistry

Volumn 45, Issue 20, 2006, Pages 6317-6327

  Kwok, Ernest Y ^a   Severance, Scott ^a   Kosman, Daniel J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; COPPER; DIMERS; IRON; PROTEINS; YEAST;

FET3P-FTR1P HIGH-AFFINITY IRON UPTAKE COMPLEX; IRON CHANNELING; YEAST PLASMA MEMBRANE;

ENZYME KINETICS;

FERRIC ION; FERROUS ION; ION CHANNEL; IRON; IRON 59; OXIDOREDUCTASE;

ARTICLE; CELL MEMBRANE; FLUORESCENCE; IRON TRANSPORT; KINETICS; NONHUMAN; OXIDATION; PLASMID; PRIORITY JOURNAL; PROTEIN LOCALIZATION; YEAST CELL;

BIOLOGICAL TRANSPORT; CELL MEMBRANE; CERULOPLASMIN; CHELATING AGENTS; CITRIC ACID; DOSE-RESPONSE RELATIONSHIP, DRUG; FERRIC COMPOUNDS; IRON; KINETICS; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; MUTATION; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; THERMODYNAMICS;

SACCHAROMYCES CEREVISIAE;

EID: 33646893459     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052173c     Document Type: Article

References (56)

1. Andrews, N. C., Fleming, M. D., and Gunshin, H. (1999) Iron transport across biologic membranes, Nutr. Rev. 57, 114-123.
2. Frieden, E., and Osaki, S. (1974) Ferroxidases and ferrireductases: their role in iron metabolism, Adv. Exp. Med. Biol. 48, 235-265.
3. Kosman, D. J. (2003) The molecular mechanisms of iron uptake in fungi, Mol. Microbiol. 47, 1185-1197.
4. Bondy, S. C., Guo-Ross, S. X., and Truong, A. T. (1998) Promotion of transition metal-induced reactive oxygen species formation by β-amyloid, Brain Res. 799, 91-96.
5. Pierre, J. L., and Fontecave, M. (1999) Iron and activated oxygen species in biology: the basic chemistry, BioMetals 12, 195-199.
6. Martins, L. J., Jensen, L. T., Simon, J. R., Keller, G. L., and Winge, D. R. (1998) Metalloregulation of FRE1 and FRE2 homologs in Saccharomyces cerevisiae, J. Biol. Chem. 273, 23716-23721.
7. Dancis, A., Roman, D. G., Anderson, G. J., Hinnebusch, A. G., and Klausner, R. D. (1992) Ferric reductase of Saccharomyces cerevisiae: Molecular characterization, role in iron uptake and transcriptional control by iron, Proc. Natl. Acad. Sci. U.S.A. 89, 3869-3873.
8. Georgatsou, E., and Alexandraki, D. (1999) Regulated expression of the Saccharomyces cerevisiae Fre1p/Fre2p Fe/Cu reductase related genes, Yeast 15, 573-584.
9. Hassett, R., and Kosman, D. J. (1995) Evidence for Cu(II) reduction as a component of copper uptake by Saccharomyces cerevisiae, J. Biol. Chem. 270, 128-134.
10. de Silva, D. M., Askwith, C. C., Eide, D., and Kaplan, J. (1995) The FET3 gene product required for high affinity iron transport in yeast is a cell surface ferroxidase, J. Biol. Chem. 270, 1098-1101.
11. 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.
12. Yuan, D. S., Dancis, A., and Klausner, R. D. (1997) Restriction of copper export in Saccharomyces cerevisiae to a late Golgi or post-Golgi compartment in the secretory pathway, J. Biol. Chem. 272, 25787-25793.
13. Severance, S., Chakraborty, S., and Kosman, D. J. (2004) Structure and function in the Ftr1 protein from Saccharomyces cerevisiae: orientation, topology and iron permeation residues, Biochem. J. 380, 487-496.
14. Solomon, E. I., Sundaram, U. M., and Machonkin, T. E. (1996) Multicopper oxidases and oxygenases, Chem. Rev. 96, 2563-2605.
15. 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.
16. Harris, Z. L., Durley, A. P., Man, T. K., and Gitlin, J. D. (1999) Targeted gene disruption reveals an essential role for ceruloplasmin in cellular iron efflux, Proc. Natl. Acad. Sci. U.S.A. 96, 10812-10817.
17. 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.
18. de Silva, D., Davis-Kaplan, S., Fergestad, J., and Kaplan, J. (1997) Purification and characterization of Fet3 protein, a yeast homologue of ceruloplasmin, J. Biol. Chem. 272, 14208-14213.
19. 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.
20. Blackburn, N. J., Ralle, M., Hassett, R., and Kosman, D. J. (2000) Spectroscopic analysis of the trinuclear cluster in the Fet3 protein from yeast, a multinuclear copper oxidase, Biochemistry 39, 2316-2324.
21. 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.
22. 2 reactivity of the trinuclear cluster of mutants of the multicopper oxidase Fet3p, Biochemistry 41, 6438-6448.
23. Dix, D., Bridgham, J., Broderius, M., and Eide, D. (1997) Characterization of the FET4 protein of yeast. Evidence for a direct role in the transport of iron, J. Biol. Chem. 272, 11770-11777.
24. Yamaguchi-Iwai, Y., Stearman, R., Dancis, A., and Klausner, R. D. (1996) Iron-regulated DNA binding by the AFT1 protein controls the iron regulon in yeast, EMBO J. 15, 3377-3384.
25. 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.
26. Segel, I. (1975) Enzyme Kinetics, pp 203-206, Wiley-Interscience, New York.
27. Bonaccorsi di Patti, M. C., Paronetto, M. P., Dolci, V., Felice, M. R., Lania, A., and Musci, G. (2001) Mutational analysis of the iron binding site of Saccharomyces cerevisiae ferroxidase Fet3. An in vivo study, FEBS Lett. 508, 475-478.
28. 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 yeast metallo-oxidase, Fet3p, Proc. Natl. Acad. Sci. U.S.A. 102, 15459-15464.
29. 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.
30. Fersht, A. R. (1999) in Structure and Mechanism in Protein Science, pp 350-355, W. H. Freeman, New York.
31. 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.
32. Jencks, W. P. (1981) On the attribution and additivity of binding energies, Proc. Natl. Acad. Sci. U.S.A. 78, 4046-4050.
33. Mildvan, A. S., Weber, D. J., and Kuliopulos, A. (1992) Quantitative interpretation of double mutations of enzymes, Arch. Biochem. Biophys. 294, 327-340.
34. Wells, J. A. (1990) Additivity of mutational effects in proteins, Biochemistry 29, 8509-8517.
35. Anderson, K. S. (1999) Fundamental mechanisms of substrate channeling, Methods Enzymol. 308, 111-145.
36. Spivey, H. O., and Ovadi, J. (1999) Substrate channeling, Methods 19, 306-321.
37. Martell, A. E., and Motekaitis, R. J. (1992) Determination and Use of Stability Constants, 2nd ed., John Wiley & Sons, New York.
38. 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.
39. Miles, E. W., Rhee, S., and Davies, D. R. (1999) The molecular basis of substrate channeling, J. Biol. Chem. 274, 12193-12196.
40. Ovadi, J., and Saks, V. (2004) On the origin of intracellular compartmentation and organized metabolic systems, Mol. Cell. Biochem. 256-257, 5-12.
41. Rakus, D., Pasek, M., Krotkiewski, H., and Dzugaj, A. (2004) Interaction between muscle aldolase and muscle fructose 1,6-bisphosphatase results in the substrate channeling, Biochemistry 43, 14948-14957.
42. Huang, X., Holden, H. M., and Raushel, F. M. (2001) Channeling of substrates and intermediates in enzyme-catalyzed reactions, Annu. Rev. Biochem. 70, 149-180.
43. Olsson, U., Billberg, A., Sjovall, S., Al-Karadaghi, S., and Hansson, M. (2002) In vivo and in vitro studies of Bacillus subtilis ferrochelatase mutants suggest substrate channeling in the heme biosynthesis pathway, J. Bacteriol. 184, 4018-4024.
44. Seifert, G. J., Barber, C., Wells, B., Dolan, L., and Roberts, K. (2002) Galactose biosynthesis in Arabidopsis: genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers, Curr. Biol. 12, 1840-1845.
45. Licata, V. J., and Ackers, G. K. (1995) Long-range, small magnitude nonadditivity of mutational effects in proteins, Biochemistry 34, 3133-3139.
46. Huffman, D. L., and O'Halloran, T. V. (2001) Function, structure, and mechanism of intracellular copper trafficking proteins, Annu. Rev. Biochem. 70, 677-701.
47. Xiao, Z., Loughlin, F., George, G. N., Howlett, G. J., and Wedd, A. G. (2004) C-terminal domain of the membrane copper transporter Ctr1 from Saccharomyces cerevisiae binds four Cu(I) ions as a cuprous-thiolate polynuclear cluster: sub-femtomolar Cu(I) affinity of three proteins involved in copper trafficking, J. Am. Chem. Soc. 126, 3081-3090.
48. Xiao, Z., and Wedd, A. G. (2002) A C-terminal domain of the membrane copper pump Ctr1 exchanges copper(I) with the copper chaperone Atxl, Chem. Commun., 588-589.
49. Huffman, D. L., and O'Halloran, T. V. (2000) Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2, J. Biol. Chem. 275, 18611-18614.
50. Rae, T. D., Schmidt, P. J., Pufahl, R. A., Culotta, V. C., and O'Halloran, T. V. (1999) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase, Science 284, 805-808.
51. Milani, M., Pesce, A., Bolognesi, M., Bocedi, A., and Ascenzi, P. (2003) Substrate channeling: molecular bases, Biochem. Mol. Biol. Educ. 31, 228-233.
52. Maynard, E. L., and Lindahl, P. A. (2001) Catalytic coupling of the active sites in acetyl-CoA synthase, a bifunctional CO-channeling enzyme, Biochemistry 40, 13262-13267.
53. Dobbek, H., Svetlitchnyi, V. Gremer, L., Huber, R. and Neyer, Ol. (2001) Crystal structure of a corbon monoxide dehydrogenase reveals a [Ni4Fe-5S] cluster, Science 293, 1281-1285.
54. Treffry, A., Bauminger, E. R., Hechel, D., Hodson, N. W., Nowik, I., Yewdall, S. J., and Harrison, P. M. (1993) Defining the roles of the threefold channels in iron uptake, iron oxidation and iron-core formation in ferritin: a study aided by site-directed mutagenesis, Biochem. J. 296, 721-728.
55. Santambrogio, P., Levi, S., Cozzi, A., Corsi, B., and Arosio, P. (1996) Evidence that the specificity of iron incorporation into homopolymers of human ferritin L- and H-chains is conferred by the nucleation and ferroxidase centres, Biochem. J. 314, 139-144.
56. Liu, X., and Theil, E. C. (2004) Ferritin reactions: direct identification of the site for the diferric peroxide reaction intermediate, Proc. Natl. Acad. Sci. U.S.A. 101, 8557-8562.