Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli

Journal of Molecular Biology

Volumn 341, Issue 2, 2004, Pages 605-615

  Bou Abdallah, Fadi ^a   Adinolfi, Salvatore ^b   Pastore, Annalisa ^b   Laue, Thomas M ^c   Dennis Chasteen, N ^a  

^a Univ of New Hampshire   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c UNIVERSITY OF NEW HAMPSHIRE   (United States)

Author keywords

CyaY, bacterial frataxin; Dps, DNA binding protein from starved cells; DTPA, diethylenetriamine pentaacetic acid; EcBFR, E. coli bacterioferritin; frataxin; IAA, iodoacetamide; iron metabolism; iron toxicity; isothermal titration calorimetry; radicals

Indexed keywords

BINDING PROTEIN; FRATAXIN; HYDROGEN PEROXIDE; HYDROXYL RADICAL; IRON; MONOMER; TETRAMER;

ARTICLE; CALORIMETRY; CATALYSIS; ELECTRON SPIN RESONANCE; ESCHERICHIA COLI; KINETICS; MEASUREMENT; MITOCHONDRION; NONHUMAN; OXIDATION; OXIDATION KINETICS; PRIORITY JOURNAL; PROTEIN FUNCTION; STOICHIOMETRY; TITRIMETRY; ULTRACENTRIFUGATION; ULTRAVIOLET RADIATION; ULTRAVIOLET SPECTROSCOPY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 3342981572     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.05.072     Document Type: Article

References (43)

1. Muhlenhoff U., Lill R. Biogenesis of iron-sulfur proteins in eukaryotes: a novel task of mitochondria that is inherited from bacteria. Biochim. Biophys. Acta. 1459:2000;370-382
2. Patel P.I., Isaya G. Friedrich's ataxia: from GAA triplet-repeat expansion to frataxin deficiency. Am. J. Hum. Genet. 69:2001;15-24
3. Flatmark T., Romslo I. Energy-dependent accumulation of iron by isolated rat liver mitochondria. Requirement of reducing equivalents and evidence for a unidirectional flux of Fe(II) across the inner membrane. J. Biol. Chem. 250:1975;6433-6438
4. Kispal G., Csere P., Guiard B., Lill R. The ABC transporter Atm1p is required for mitochondrial iron homeostasis. FEBS Letters. 418:1997;346-350
5. Knight S.A.B., Sepuri N.B.V., Pain D., Dancis A. Mt-Hsp70 homolog, Ssc2p, required for maturation of yeast frataxin and mitochondrial iron homeostasis. J. Biol. Chem. 273:1998;18389-18393
6. Lange H., Kispal G., Lill R. Mechanism of iron transport to the site of heme synthesis inside yeast mitochondria. J. Biol. Chem. 274:1999;18989-18996
7. Gibson T.J., Koonin E.V., Musco G., Pastore A., Bork P. Friedreich's ataxia protein: phylogenetic evidence for mitochondrial dysfunction. Trends Neurosci. 19:1996;465-468
8. Cavadini P., Gellera C., Patel P.I., Isaya G. Human frataxin maintains mitochondrial iron homeostasis in Saccharomyces cerevisiae. Hum. Mol. Genet. 9:2000;2523-2530
9. Radisky D.C., Babcock M.C., Kaplan J. The yeast frataxin homologue mediates mitochondrial iron efflux. Evidence for a mitochondrial iron cycle. J. Biol. Chem. 274:1999;4497-4499
10. Wong A., Yang J., Cavadini P., Gellera C., Lonnerdal B., Taroni F., Cortopassi G. The Friedreich's ataxia mutation confers cellular sensitivity to oxidant stress which is rescued by chelators of iron and calcium and inhibitors of apoptosis. Hum. Mol. Genet. 8:1999;425-430
11. Campuzano V., Montermini L., Molto M.D., Pianese L., Cossee M., Cavalcanti F., et al. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science. 271:1996;1423-1427
12. Pandolfo M. Iron metabolism and mitochondrial abnormalities in Friedreich ataxia. Blood Cells Mol. Dis. 29:2002;536-547
13. Koutnikova H., Campuzano V., Foury F., Dolle P., Cazzalini O., Koenig M. Studies of human, mouse and yeast homologues indicate a mitochondrial function for frataxin. Nature Genet. 16:1997;345-351
14. Becker E., Richardson D.R. Frataxin: its role in iron metabolism and the pathogenesis of Friedreich's ataxia. Int. J. Biochem. Cell Biol. 33:2001;1-10
15. Park S., Gakh O., Mooney S.M., Isaya G. The ferroxidase activity of yeast frataxin. J. Biol. Chem. 277:2002;38589-38595
16. Cavadini P., O'Neill H.A., Benada O., Isaya G. Assembly and iron-binding properties of human frataxin, the protein deficient in Friedreich ataxia. Hum. Mol. Genet. 11:2002;217-227
17. Nichol H., Gakh O., O'Neill H.A., Pickering I.J., Isaya G., George G.N. Structure of frataxin iron cores: an x-ray absorption spectroscopic study. Biochemistry. 42:2003;5971-5976
18. Gakh O., Adamec J., Gacy A.M., Twesten R.D., Owen W.G., Isaya G. Physical evidence that yeast frataxin is an iron storage protein. Biochemistry. 41:2002;6798-6804
19. Adamec J., Rusnak F., Owen W.G., Naylor S., Benson L.M., Gacy A.M., Isaya G. Iron-dependent self-assembly of recombinant yeast frataxin: implications for Friedreich ataxia. Am. J. Hum. Genet. 67:2000;549-562
20. Ramazzotti A., Vanmansart V., Foury F. Mitochondrial functional interactions between frataxin and Isu1p, the iron-sulfur cluster scaffold protein, in Saccharomyces cerevisiae. FEBS Letters. 557:2004;215-220
21. Duby G., Foury F., Ramazzotti A., Herrmann J., Lutz T. A non-essential function for yeast frataxin in iron-sulfur cluster assembly. Hum. Mol. Genet. 11:2002;2635-2643
22. Gerber J., Muehlenhoff U., Lill R. An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Reports. 4:2003;906-911
23. Yoon T., Cowan J.A. Iron-sulfur cluster biosynthesis. Characterization of Frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins. J. Am. Chem. Soc. 125:2003;6078-6084
24. Yoon T., Cowan J.A. Frataxin-mediated iron delivery to ferrochelatase is the final step of heme biosynthesis. J. Biol. Chem. 279:2004;25943-25946
25. Park S., Gakh O., O'Neill H.A., Mangravita A., Nichol H., Ferreira J.C., Isaya G. Yeast frataxin sequentially chaperones and stores iron by coupling protein assembly with iron oxidation. J. Biol. Chem. 278:2003;31340-31351
26. Adinolfi S., Trifuoggi M., Politou A., Martin S., Pastore A. A structural approach to understanding the iron-binding properties of phylogenetically different frataxins. Hum. Mol. Genet. 11:2002;1865-1877
27. Zhao G., Ceci P., Ilari A., Giangiacomo L., Laue T.M., Chiancone E., Chasteen N.D. Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells: a ferritin-like DNA-binding protein of Escherichia coli. J. Biol. Chem. 277:2002;27689-27696
28. Bou-Abdallah F., Lewin A.C., Le Brun N.E., Moore G.R., Chasteen N.D. Iron detoxification properties of Escherichia coli bacterioferritin. J. Biol. Chem. 277:2002;37064-37069
29. Zhao G., Bou-Abdallah F., Yang X., Arosio P., Chasteen N.D. Is hydrogen peroxide produced during iron(II) oxidation in mammalian apoferritins? Biochemistry. 40:2001;10832-10838
30. Yang X., Le brun N.E., Thomson A.J., Moore G.R., Chasteen N.D. The iron oxidation and hydrolysis chemistry of Escherichia coli bacterioferritin. Biochemistry. 39:2000;4915-4923
31. Yang X., Chen-Barrett Y., Arosio P., Chasteen N.D. Reaction paths of iron oxidation and hydrolysis in horse spleen and recombinant human ferritins. Biochemistry. 37:1998;9743-9750
32. Babcock M., de silva D., Oaks R., Davis-Kaplan S., Jiralerspong S., Montermini L., et al. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science. 276:1997;1709-1712
33. Karthikeyan G., Santos J.H., Graziewicz M.A., Copeland W.C., Isaya G., Van Houten B., Resnick M.A. Reduction in frataxin causes progressive accumulation of mitochondrial damage. Hum. Mol. Genet. 12:2003;3331-3342
34. Karthikeyan G., Lewis L.K., Resnick M.A. The mitochondrial protein frataxin prevents nuclear damage. Hum. Mol. Genet. 11:2002;1351-1362
35. Bou-Abdallah F., Arosio P., Santambrogio P., Yang X., Janus-Chandler C., Chasteen N.D. Ferrous ion binding to recombinant human H-chain ferritin. An isothermal titration calorimetry study. Biochemistry. 41:2002;11184-11191
36. Bou-Abdallah F., Arosio P., Levi S., Janus-Chandler C., Chasteen N.D. Defining metal ion inhibitor interactions with recombinant human H- and L-chain ferritins and site-directed variants: an isothermal titration calorimetry study. J. Biol. Inorg. Chem. 8:2003;489-497
37. Foury F., Talibi D. Mitochondrial control of iron homeostasis. A genome wide analysis of gene expression in a yeast frataxin-deficient strain. J. Biol. Chem. 276:2001;7762-7768
38. Branda S.S., Yang Z.Y., Chew A., Isaya G. Mitochondrial intermediate peptidase and the yeast frataxin homolog together maintain mitochondrial iron homeostasis in Saccharomyces cerevisiae. Hum. Mol. Genet. 8:1999;1099-1110
39. Huynen M.A., Snel B., Bork P., Gibson T.J. The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum. Mol. Genet. 10:2001;2463-2468
40. Cossee M., Puccio H., Gansmuller A., Koutnikova H., Dierich A., LeMeur M., et al. Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation. Hum. Mol. Genet. 9:2000;1219-1226
41. Schuck P., Perugini M.A., Gonzales N.R., Howlett G.J., Schubert D. Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys. J. 82:2002;1096-1111
42. Percival M.D. Human 5-lipoxygenase contains an essential iron. J. Biol. Chem. 266:1991;10058-10061
43. Cowart R.E., Singleton F.L., Hind J.S. A comparison of bathophenanthroline-disulfonic acid and Ferrozine as chelators of iron(II) in reduction reactions. Anal. Biochem. 211:1993;151-155