Understanding the binding properties of an unusual metal-binding protein - A study of bacterial frataxin

FEBS Journal

Volumn 274, Issue 16, 2007, Pages 4199-4210

  Pastore, Chiara ^a   Franzese, Marisa ^b   Sica, Filomena ^b,c   Temussi, Pierandrea ^a,b   Pastore, Annalisa ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c CNR   (Italy)

Author keywords

CyaY; Friedreich's ataxia; Iron binding; NMR; X ray

Indexed keywords

ASPARTIC ACID; CATION; CYAY PROTEIN; CYSTEINE; FRATAXIN; GLUTAMIC ACID; HISTIDINE; IRON BINDING PROTEIN; METAL; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; ELECTRICITY; IRON CHELATION; METAL BINDING; NUCLEAR MAGNETIC RESONANCE; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BINDING, COMPETITIVE; COBALT; CRYSTALLOGRAPHY, X-RAY; GADOLINIUM; IRON; IRON-BINDING PROTEINS; IRON-SULFUR PROTEINS; LANTHANOID SERIES ELEMENTS; LUTETIUM; MAGNESIUM; MAGNETIC RESONANCE SPECTROSCOPY; METALS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; ZINC;

BACTERIA (MICROORGANISMS);

EID: 34547760795     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05946.x     Document Type: Article

References (46)

1. Campuzano V, Montermini L, Molto MD, Pianese L, Cossée M, Cavalcanti F, Monros E, Rodius F, Duclos F, Monticelli A et al. (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271, 1423 1427.
2. Cossee M, Puccio H, Gansmuller A, Koutnikova H, Dierich A, LeMeur M, Fischbeck K, Dolle P Koenig M (2000) Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation. Hum Mol Genet 9, 1219 1226.
3. Yoon T Cowan JA (2003) 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, 6078 6084.
4. Yoon T Cowan JA (2004) Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J Biol Chem 279, 25943 25946.
5. Bulteau AL, O'Neill HA, Kennedy MC, Ikeda-Saito M, Isaya G Szweda LI (2004) Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science 305, 242 245.
6. Gerber J, Muhlenhoff U Lill R (2003) An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Reports 4, 906 911.
7. Park S, Gakh O, O'Neill HA, Mangravita A, Nichol H, Ferreira GC Isaya G (2003) Yeast frataxin sequentially chaperones and stores iron by coupling protein assembly with iron oxidation. J Biol Chem 278, 31340 31351.
8. Park S, Gakh O, Mooney SM Isaya G (2002) The ferroxidase activity of yeast frataxin. J Biol Chem 277, 38589 38595.
9. Cavadini P, O'Neill HA, Benada O Isaya G (2002) Assembly and iron-binding properties of human frataxin, the protein deficient in Friedreich's ataxia. Hum Mol Genet 11, 217 227.
10. Delatycki MB, Williamson R Forrest SM (2000) Freidreich's ataxia: an overview. J Med Genet 37, 1 8.
11. Huynen MA, Snel B, Bork P Gibson TJ (2001) The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum Mol Genet 10, 2463 2468.
12. Muhlenhoff U, Richhardt N, Ristow M, Kispal G Lill R (2002) The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum Mol Genet 11, 2025 2036.
13. Stehling O, Elsasser H-P, Bruckel B, Muhlenhoff U Lill R (2004) Iron-sulfur protein maturation in human cells: evidence for a function of frataxin. Hum Mol Genet 13, 3007 3015.
14. Wong A, Yang J, Cavadini P, Gellera C, Lonnerdal B, Taroni F Cortopassi G (1999) 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, 425 430.
15. Ristow M, Pfister MF, Yee AJ, Schubert M, Michael L, Zhang C-Y, Ueki K, Michael MD 2nd, Lowell BB Kahn CR (2000) Frataxin activates mitochondrial energy conversion and oxidative phosphorylation. Proc Natl Acad Sci USA 97, 12239 12243.
16. Tan G, Napoli E, Taroni F Cortopassi G (2003) Decreased expression of genes involved in sulfur amino acid metabolism in frataxin-deficient cells. Hum Mol Genet 12, 1699 1711.
17. Lesuisse E, Santos R, Matzanke BF, Knight SAB, Camadro J-M Dancis A (2003) Iron use for heme synthesis is under control of the yeast frataxin homologue (Yfh1). Hum Mol Genet 12, 879 889.
18. Radisky DC, Babcock MC Kaplan J (1999) The yeast frataxin homologue mediates mitochondrial iron efflux: evidence for a mitochondrial iron cycle. J Biol Chem 274, 4497 4499.
19. Foury F Talibi D (2001) Mitochondrial control of iron homeostasis. A genome wide analysis of gene expression in a yeast frataxin-deficient strain. J Biol Chem 276, 7762 7768.
20. Que L Jr. Ho RY (1996) Dioxygen activation by enzymes with mononuclear non-heme iron active sites. Chem Rev 96, 2607 2624.
21. Musco G, Stier G, Kolmerer B, Adinolfi S, Martin S, Frenkiel T, Gibson T Pastore A (2000) Towards a structural understanding of Friedreich's ataxia: the olution structure of frataxin. Structure 8, 695 707.
22. Dhe-Paganon S, Shigeta R, Chi Y-I, Ristow M Shoelson SE (2000) Crystal structure of human frataxin. J Biol Chem 275, 30753 30756.
23. Cho SJ, Lee MG, Yang JY, Song HK Suh SW (2000) Crystal structure of Escherichia coli CyaY reveals a previously unidentified fold for the evolutionary conserved frataxin family. Proc Natl Acad Sci USA 97, 8932 8937.
24. Nair M, Adinolfi S, Pastore C, Kelly G, Temussi P Pastore A (2004) Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites. Structure (Camb) 12, 2037 2048.
25. He Y, Alam SL, Proteasa SV, Zhang Y, Lesuisse E, Dancis A Stemmler TL (2004) Yeast frataxin solution structure, iron binding and ferrochelatase interaction. Biochemistry 43, 16254 16262.
26. Bou-Abdallah F, Adinolfi S, Pastore A, Laue TM Chasteen DN (2004) Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli. J Mol Biol 341, 605 615.
27. Adinolfi S, Trifuoggi M, Politou AS, Martin S Pastore A (2002) A structural approach to understanding the iron-binding properties of phylogenetically different frataxins. Hum Mol Genet 11, 1865 1877.
28. Adinolfi S, Nair M, Politou A, Bayer E, Martin S, Temussi P Pastore A (2004) The factors governing the thermal stability of frataxin orthologues: how to increase a protein's stability. Biochemistry 43, 6511 6518.
29. Butchard CG, Dwek RA, Ferguson SJ, Kent PW, Williams RJP Xavier AV (1972) Mapping of the binding site of N-fluoroacetyl-d-glucosamine and analogues in hen egg lysozyme by 1H and 19F-NMR techniques with Gd(III) and Mn(II) as paramagnetic probes. FEBS Lett 25, 91 93.
30. Bertini I Luchinat C (1996) NMR of paramagnetic substances. Coord Chem Rev 150, 1.
31. Saito T, Wormald MR Williams RJ (1991) Some structural features of the iron-uptake regulation protein. Eur J Biochem 197, 29 38.
32. Evans CH (1990) Biochemistry of the Lanthanides. Plenum Press, New York, NY.
33. Carter CW Jr. Sweet RM (1997) Macromolecular crystallography. Part A. Methods Enzymol 276, 530 538.
34. Karlberg T, Schagerlof U, Gakh O, Park S, Ryde U, Lindahl M, Leath K, Garman E, Isaya G Al-Karadaghi S (2006) The structures of frataxin oligomers reveal the mechanism for the delivery and detoxification of iron. Structure 14, 1535 1546.
35. Foury F, Pastore A Trincal M (2007) Acidic residues of yeast frataxin have an essential role in Fe-S cluster assembly. EMBO Report 8, 194 199.
36. Delaglio F, Grzesiek S, Vuister G, Zhu G, Pfeifer J Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277 293.
37. Bartels Ch, Xia T-H, Billeter M, Güntert P Wüthrich K (1995) The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J Biomol NMR 5, 1 10.
38. Otwinowski Z Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276, 307 326.
39. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewki JJ, Nilges M, Pannu NS et al. (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr 54D, 905 921.
40. Schneider TR Sheldrick GM (2002) Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 58, 1772 1779.
41. Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760 763.
42. Jones TA, Zou JY, Cowan SW Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A47, 110 119.
43. Laskowski RA, MacArthur MW, Moss DS Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structure. J Appl Crystallogr 26, 283 291.
44. Hooft RW, Vriend GS Abola EE (1996) Errors in protein structures. Nature 381, 272.
45. Koradi R, Billeter M Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structure. J Mol Graph 14, 51 55.
46. Esnouf RM (1999) Further additions to Molscript, Version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr D55, 938 940.