Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS

Nature Structural and Molecular Biology

Volumn 16, Issue 4, 2009, Pages 390-396

  Adinolfi, Salvatore ^a   Iannuzzi, Clara ^a,b   Prischi, Filippo ^a,c   Pastore, Chiara ^a,e   Iametti, Stefania ^d   Martin, Stephen R ^a   Bonomi, Franco ^d   Pastore, Annalisa ^a,f  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF SIENA   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e Och Spine at New York Presbyterian Hospitals   (United States)

^f CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FRATAXIN; GLUTATHIONE TRANSFERASE; IRON SULFUR PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN CYAY; PROTEIN ISCS; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; GEL FILTRATION; GENE CLUSTER; INHIBITION KINETICS; IRON BINDING CAPACITY; IRON KINETICS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN INTERACTION;

BACTERIAL PROTEINS; CARBON-SULFUR LYASES; CHROMATOGRAPHY, GEL; ESCHERICHIA COLI; IRON; IRON-BINDING PROTEINS; KINETICS; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING;

BACTERIA (MICROORGANISMS); PYRONIA TITHONUS;

EID: 64049116040     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1579     Document Type: Article

References (37)

1. Pandolfo, M. Iron and Friedreich's ataxia. J. Neural Transm. Suppl. 70, 143-146 (2006).
2. Campuzano, V. et al. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271, 1423-1427 (1996).
3. Koutnikova, H. et al. Studies of human, mouse and yeast homologues indicate a mitochondrial function for frataxin. Nat. Genet. 16, 345-351 (1997).
4. Adinolfi, S., Trifuoggi, M., Politou, A.S., Martin, S. & Pastore, A. A structural approach to understanding the iron-binding properties of phylogenetically different frataxins. Hum. Mol. Genet. 11, 1865-1877 (2002).
5. He, Y. et al. Yeast frataxin solution structure, iron binding & ferrochelatase interaction. Biochemistry 43, 16254-16262 (2004).
6. Nair, M. et al. Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites. Structure 12, 2037-2048 (2004).
7. Cook, J.D. et al. Monomeric yeast frataxin is an iron-binding protein. Biochemistry 45, 7767-7777 (2006).
8. Foury, F. & Cazzalini, O. Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett. 411, 373-377 (1997).
9. Lesuisse, E. et al. Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1). Hum. Mol. Genet. 12, 879-889 (2003).
10. Yoon, T. & Cowan, J.P. Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J. Biol. Chem. 279, 25943-25946 (2004).
11. Gerber, J., Muhlenhoff, U. & Lill, R. An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep. 4, 906-911 (2003).
12. Ramazzotti, A., Vanmansart, V. & Foury, F. Mitochondrial functional interactions between frataxin and Isu1p, the iron-sulfur cluster scaffold protein, in Saccharomyces cerevisiae. FEBS Lett. 557, 215-220 (2004).
13. Layer, G., Ollagnier-de Choudens, S., Sanakis, Y. & Fontecave, M. Iron-sulfur cluster biosynthesis: characterization of Escherichia coli CYaY as an iron donor for the assembly of [2Fe-2S] clusters in the scaffold IscU. J. Biol. Chem. 281, 16256-16263 (2006).
14. 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, 6078-6084 (2003).
15. Adamec, J. et al. Iron-dependent self-assembly of recombinant yeast frataxin: implications for Friedreich ataxia. Am. J. Hum. Genet. 67, 549-562 (2000).
16. Johnson, D.C., Dean, D.R., Smith, A.D. & Johnson, M.K. Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 74, 247-281 (2005).
17. 2+ cluster core in IscU proteins. J. Am. Chem. Soc. 124, 8774-8775 (2002).
18. Agar, J.N., Krebs, C., Frazzon, J., Hanh Huynh, B. & Dean, D.R. IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. Biochemistry 39, 7856-7862 (2000).
19. Yuvaniyama, P., Agar, J.N., Cash, V.L., Johnson, M.K. & Dean, D.R. NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc. Natl. Acad. Sci. USA 97, 599-604 (2000).
20. Urbina, H.D., Silberg, J.J., Hoff, K.G. & Vickery, L.E. Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J. Biol. Chem. 276, 44521-44526 (2001).
21. Mansy, S.S. Wu, G., Surerus, K.K. & Cowan, J.A. Iron-sulfur cluster biosynthesis. Thermatoga maritima IscU is a structured iron-sulfur cluster assembly protein. J. Biol. Chem. 277, 21397-21404 (2002).
22. Bou-Abdallah, F., Adinolfi, S., Pastore, A., Laue, T.M. & Chasteen, D.N. Iron binding & oxidation kinetics in frataxin CyaY of Escherichia coli. J. Mol. Biol. 341, 605-615 (2004).
23. Bonomi, F., Pagani, S. & Kurtz, D.M. Jr. Enzymatic synthesis of the 4Fe-4S clusters of Clostridium pasteurianum ferredoxin. Eur. J. Biochem. 148, 67-73 (1985).
24. Bonomi, F., Iametti, S., Ta, D. & Vickery, L.E. Multiple turnover transfer of [2Fe2S] clusters by the iron-sulfur cluster assembly scaffold proteins IscU and IscA. J. Biol. Chem. 280, 29513-29518 (2005).
25. Musco, G. et al. Towards a structural understanding of Friedreich's ataxia: the solution structure of frataxin. Structure 8, 695-707 (2000).
26. Pastore, C., Franzese, M., Sica, F., Temussi, P. & Pastore, A. Understanding the binding properties of an unusual metal binding protein: a study of bacterial frataxin. FEBS J. 274, 4199-4210 (2007).
27. Foury, F., Pastore, A. & Trincal, M. Acidic residues of yeast frataxin have an essential role in Fe-S cluster assembly. EMBO Rep. 8, 194-199 (2007).
28. Labuda, M., Poirier, J. & Pandolfo, M. A missense mutation (W155R) in an American patient with Friedreich Ataxia. Hum. Mutat. 13, 506-509 (1999).
29. Correia, A.R., Adinolfi, S., Pastore, A. & Gomes, C. Conformational stability of human frataxin and effect of Friedreich's ataxia related mutations on protein folding. Biochem. J. 398, 605-611 (2006).
30. Bedekovics, T., Gajdos, G.B., Kispal, G. & Isaya, G. Partial conservation of functions between eukaryotic frataxin and the Escherichia coli frataxin homolog CyaY. FEMS Yeast Res. 7, 1276-1284 (2007).
31. Cavadini, P., Gellera, C., Patel, P.I. & Isaya, G. Human frataxin maintains mitochondrial iron homeostasis in Saccharomyces cerevisiae. Hum. Mol. Genet. 9, 2523-2530 (2000).
32. Huang, J., Dizin, E. & Cowan, J.A. Mapping iron binding sites on human frataxin: implications for cluster assembly on the ISU Fe-S cluster scaffold protein. J. Biol. Inorg. Chem. 13, 825-836 (2008).
33. Schwartz, C.J. et al. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc. Natl. Acad. Sci. USA 98, 14895-14900 (2001).
34. Cossee, M. et al. Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation. Hum. Mol. Genet. 9, 1219-1226 (2000).
35. Leidgens, S. The function of yeast frataxin in iron-sulfur cluster biogenesis: a systematic mutagenesis of the solvent-exposed side chains of the beta-sheet platform. PhD thesis Louvain la Neuf (Belgium) (2008).
36. Levi, S. et al. A human mitochondrial ferritin encoded by an intronless gene. J. Biol. Chem. 276, 24437-24440 (2001).
37. Aloria, K., Schilke, B., Andrew, A. & Craig, E.A. Iron-induced oligomerization of yeast frataxin homologue Yfh1 is dispensable in vivo. EMBO Rep. 5, 1096-1101 (2004).