Frataxin interacts with Isu1 through a conserved tryptophan in its β-sheet

Human Molecular Genetics

Volumn 19, Issue 2, 2009, Pages 276-286

  Leidgens, Sébastien ^a,b   de Smet, Sébastien ^a   Foury, Françoise ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; FRATAXIN; PROTEIN ISU1; SCAFFOLD PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG; IRON BINDING PROTEIN; ISU1 PROTEIN, S CEREVISIAE; MITOCHONDRIAL PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BETA SHEET; BIOSYNTHESIS; CELL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; FRIEDREICH ATAXIA; GENE CLUSTER; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; IMMUNOPRECIPITATION; NONHUMAN; OLIGOMERIZATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SEQUENCE ALIGNMENT; YEAST; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CHEMISTRY; CONFORMATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; FRIEDREICH ATAXIA; HUMANS; IRON-BINDING PROTEINS; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; TRYPTOPHAN;

EID: 77949440735     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp495     Document Type: Article

References (62)

1. Harding, A.E. (1981) Friedreich's ataxia: a clinical and genetic study of 90 families with an analysis of early diagnostic criteria and intrafamilial clustering of clinical features. Brain, 104, 589-620.
2. Cossée, M., Schmitt, M., Campuzano, V., Reutenauer, L., Moutou, C., Mandel, J.L. and Koenig, M. (1997) Evolution of the Friedreich's ataxia trinucleotide repeat expansion: founder effect and premutations. Proc. Natl. Acad. Sci. USA, 94, 7452-7457.
3. Campuzano, V., Montermini, L., Molto, M.D., Pianese, L., Cossee, 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.
4. Rötig, A., de Lonlay, P., Chretien, D., Foury, F., Koenig, M., Sidi, D., Munnich, A. and Rustin, P. (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet., 17, 215-217.
5. Wong, A., Yang, J., Cavadini, P., Gellera, C., Lonnerdal, B., Taroni, F. and 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.
6. Delatycki, M.B., Camakaris, J., Brooks, H., Evans-Whipp, T., Thorburn, D.R., Williamson, R. and Forrest, S.M. (1999) Direct evidence that mitochondrial iron accumulation occurs in Friedreich ataxia. Ann. Neurol., 45, 673-675.
7. Bradley, J.L., Blake, J.C., Chamberlain, S., Thomas, P.K., Cooper, J.M. and Schapira, A.H. (2000) Clinical, biochemical and molecular genetic correlations in Friedreich's ataxia. Hum. Mol. Genet., 9, 275-282.
8. Lodi, R., Cooper, J.M., Bradley, J.L., Manners, D., Styles, P., Taylor, D.J. and Schapira, A.H. (1999) Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia. Proc. Natl. Acad. Sci. USA, 96, 11492-11495.
9. Waldvogel, D., van Gelderen, P. and Hallett, M. (1999) Increased iron in the dentate nucleus of patients with Friedrich's ataxia. Ann. Neurol., 46, 123-125.
10. Cossée, M., Dürr, A., Schmitt, M., Dahl, N., Trouillas, P., Allinson, P., Kostrzewa, M., Nivelon-Chevallier, A., Gustavson, K.H., Kohlschütter, A. et al. (1999) Friedreich's ataxia: point mutations and clinical presentation of compound heterozygotes. Ann. Neurol., 45, 200-206.
11. Filla, A., De Michele, G., Cavalcanti, F., Pianese, L., Monticelli, A., Campanella, G. and Cocozza, S. (1996) The relationship between trinucleotide (GAA) repeat length and clinical features in Friedreich ataxia. Am. J. Hum. Genet., 59, 554-560.
12. Dürr, A., Cossee, M., Agid, Y., Campuzano, V., Mignard, C., Penet, C., Mandel, J.L., Brice, A. and Koenig, M. (1996) Clinical and genetic abnormalities in patients with Friedreich's ataxia. N. Engl. J. Med., 335, 1169-1175.
13. Foury, F. (1999) Low iron concentration and aconitase deficiency in a yeast frataxin homologue deficient strain. FEBS Lett., 456, 281-284.
14. Mühlenhoff, U., Richhardt, N., Ristow, M., Kispal, G. and 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.
15. Chen, O.S., Hemenway, S. and Kaplan, J. (2002) Inhibition of Fe-S cluster biosynthesis decreases mitochondrial iron export: evidence that Yfh1p affects Fe-S cluster synthesis. Proc. Natl. Acad. Sci. USA, 99, 12321-12326.
16. Lesuisse, E., Santos, R., Matzanke, B.F., Knight, S.A.B., Camadro, J.-M. and Dancis, A. (2003) Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1). Hum. Mol. Genet., 12, 879-889.
17. Wilson, R.B. and Roof, D.M. (1997) Respiratory deficiency due to loss of mitochondrial DNA in yeast lacking the frataxin homologue. Nat. Genet., 16, 352-357.
18. Radisky, D.C., Babcock, M.C. and Kaplan, J. (1999) The yeast frataxin homologue mediates mitochondrial iron efflux. Evidence for a mitochondrial iron cycle. J. Biol. Chem., 274, 4497-4499.
19. Babcock, M., de Silva, D., Oaks, R., Davis-Kaplan, S., Jiralerspong, S., Montermini, L., Pandolfo, M. and Kaplan, J. (1997) Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science, 276, 1709-1712.
20. Karthikeyan, G., Lewis, L.K. and Resnick, M.A. (2002) The mitochondrial protein frataxin prevents nuclear damage. Hum. Mol. Genet., 11, 1351-1362.
21. Karthikeyan, G., Santos, J.H., Graziewicz, M.A., Copeland, W.C., Isaya, G., Van Houten, B. and Resnick, M.A. (2003) Reduction in frataxin causes progressive accumulation of mitochondrial damage. Hum. Mol. Genet., 12, 3331-3342.
22. Kispal, G., Csere, P., Prohl, C. and Lill, R. (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J., 18, 3981-3989.
23. Adam, A.C., Bornhövd, C., Prokisch, H., Neupert, W. and Hell, K. (2006) The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria. EMBO J., 25, 174-183.
24. Wiedemann, N., Urzica, E., Guiard, B., Müller, H., Lohaus, C., Meyer, H.E., Ryan, M.T., Meisinger, C., Mühlenhoff, U., Lill, R. et al. (2006) Essential role of Isd11 in mitochondrial iron-sulfur cluster synthesis on Isu scaffold proteins. EMBO J., 25, 184-195.
25. Adinolfi, S., Iannuzzi, C., Prischi, F., Pastore, C., Iametti, S., Martin, S.R., Bonomi, F. and Pastore, A. (2009) Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS. Nat. Struct. Mol. Biol., 16, 390-396.
26. Duby, G., Foury, F., Ramazzotti, A., Herrmann, J. and Lutz, T. (2002) A non-essential function for yeast frataxin in iron-sulfur cluster assembly. Hum. Mol. Genet., 11, 2635-2643.
27. Dhe-Paganon, S., Shigeta, R., Chi, Y.I., Ristow, M. and Shoelson, S.E. (2000) Crystal structure of human frataxin. J. Biol. Chem., 275, 30753-30756.
28. Musco, G., Stier, G., Kolmerer, B., Adinolfi, S., Martin, S., Frenkiel, T., Gibson, T. and Pastore, A. (2000) Towards a structural understanding of Friedreich's ataxia: the solution structure of frataxin. Structure, 8, 695-707.
29. Cho, S.J., Lee, M.G., Yang, J.K., Lee, J.Y., Song, H.K. and Suh, S.W. (2000) Crystal structure of Escherichia coli CyaY protein reveals a previously unidentified fold for the evolutionarily conserved frataxin family. Proc. Natl. Acad. Sci. USA, 97, 8932-8937.
30. He, Y., Alam, S.L., Proteasa, S.V., Zhang, Y., Lesuisse, E., Dancis, A. and Stemmler, T.L. (2004) Yeast frataxin solution structure, iron binding, and ferrochelatase interaction. Biochemistry, 43, 16254-16262.
31. Kondapalli, K.C., Kok, N.M., Dancis, A. and Stemmler, T.L. (2008) Drosophila frataxin: an iron chaperone during cellular Fe-S cluster bioassembly. Biochemistry, 47, 6917-6927.
32. Bou-Abdallah, F., Adinolfi, S., Pastore, A., Laue, T.M. and Chasteen, N.D. (2004) Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli. J. Mol. Biol., 341, 605-615.
33. Huang, J., Dizin, E. and Cowan, J.A. (2008) 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.
34. Nair, M., Adinolfi, S., Pastore, C., Kelly, G., Temussi, P. and Pastore, A. (2004) Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites. Structure, 12, 2037-2048.
35. Cook, J.D., Bencze, K.Z., Jankovic, A.D., Crater, A.K., Busch, C.N., Bradley, P.B., Stemmler, A.J., Spaller, M.R. and Stemmler, T.L. (2006) Monomeric yeast frataxin is an iron-binding protein. Biochemistry, 45, 7767-7777.
36. Yoon, T. and Cowan, J.A. (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.
37. Adamec, J., Rusnak, F., Owen, W.G., Naylor, S., Benson, L.M., Gacy, A.M. and Isaya, G. (2000) Iron-dependent self-assembly of recombinant yeast frataxin: implications for Friedreich ataxia. Am. J. Hum. Genet., 67, 549-562.
38. Cavadini, P., O'Neill, H.A., Benada, O. and Isaya, G. (2002) Assembly and iron-binding properties of human frataxin, the protein deficient in Friedreich ataxia. Hum. Mol. Genet., 11, 217-227.
39. Gakh, O., Adamec, J., Gacy, A.M., Twesten, R.D., Owen, W.G. and Isaya, G. (2002) Physical evidence that yeast frataxin is an iron storage protein. Biochemistry, 41, 6798-6804.
40. Karlberg, T., Schagerlöf, U., Gakh, O., Park, S., Ryde, U., Lindahl, M., Leath, K., Garman, E., Isaya, G. and Al-Karadaghi, S. (2006) The structures of frataxin oligomers reveal the mechanism for the delivery and detoxification of iron. Structure, 14, 1535-1546.
41. Schagerlöf, U., Elmlund, H., Gakh, O., Nordlund, G., Hebert, H., Lindahl, M., Isaya, G. and Al-Karadaghi, S. (2008) Structural basis of the iron storage function of frataxin from single-particle reconstruction of the iron-loaded oligomer. Biochemistry, 47, 4948-4954.
42. Aloria, K., Schilke, B., Andrew, A. and Craig, E.A. (2004) Iron-induced oligomerization of yeast frataxin homologue Yfh1 is dispensable in vivo. EMBO Rep., 5, 1096-1101.
43. Gakh, O., Smith, D.Y.t. and Isaya, G. (2008) Assembly of the iron-binding protein frataxin in Saccharomyces cerevisiae responds to dynamic changes in mitochondrial iron influx and stress level. J. Biol. Chem., 283, 31500-31510.
44. Gerber, J., Mühlenhoff, U. and Lill, R. (2003) An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep., 4, 906-911.
45. Ramazzotti, A., Vanmansart, V. and Foury, F. (2004) Mitochondrial functional interactions between frataxin and Isu1p, the iron-sulfur cluster scaffold protein, in Saccharomyces cerevisiae. FEBS Lett., 557, 215-220.
46. Foury, F., Pastore, A. and Trincal, M. (2007) Acidic residues of yeast frataxin have an essential role in Fe-S cluster assembly. EMBO Rep., 8, 194-199.
47. Yoon, T. and Cowan, J.A. (2004) Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J. Biol. Chem., 279, 25943-25946.
48. Wang, T. and Craig, E.A. (2008) Binding of yeast frataxin to the scaffold for Fe-S cluster biogenesis, isu. J. Biol. Chem., 283, 12674-12679.
49. Foury, F. and Cazzalini, O. (1997) Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett., 411, 373-377.
50. Bota, D.A. and Davies, K.J. (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol., 4, 674-680.
51. Lutz, T., Westermann, B., Neupert, W. and Herrmann, J.M. (2001) The mitochondrial proteins Ssq1 and Jac1 are required for the assembly of iron sulfur clusters in mitochondria. J. Mol. Biol., 307, 815-825.
52. Adinolfi, S., Nair, M., Politou, A., Bayer, E., Martin, S., Temussi, P. and Pastore, A. (2004) The factors governing the thermal stability of frataxin orthologues: how to increase a protein's stability. Biochemistry, 43, 6511-6518.
53. Van Dyck, L. and Langer, T. (1999) ATP-dependent proteases controlling mitochondrial function in the yeast Saccharomyces cerevisiae. Cell. Mol. Life. Sci., 56, 825-842.
54. Shan, Y., Napoli, E. and Cortopassi, G. (2007) Mitochondrial frataxin interacts with ISD11 of the NFS1/ISCU complex and multiple mitochondrial chaperones. Hum. Mol. Genet., 16, 929-941.
55. Layer, G., Ollagnier-de Choudens, S., Sanakis, Y. and Fontecave, M. (2006) 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.
56. Lill, R. and Mühlenhoff, U. (2008) Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu. Rev. Biochem., 77, 669-700.
57. Labuda, M., Poirier, J. and Pandolfo, M. (1999) A missense mutation (W155R) in an American patient with Friedreich Ataxia. Hum. Mutat., 13, 506.
58. Correia, A.R., Adinolfi, S., Pastore, A. and Gomes, C.M. (2006) Conformational stability of human frataxin and effect of Friedreich's ataxia-related mutations on protein folding. Biochem. J., 398, 605-611.
59. Ma, B., Elkayam, T., Wolfson, H. and Nussinov, R. (2003) Protein-protein interactions: structurally conserved residues distinguish between binding sites and exposed protein surfaces. Proc. Natl. Acad. Sci. USA, 100, 5772-5777.
60. Daum, G., Bohni, P.C. and Schatz, G. (1982) Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Biol. Chem., 257, 13028-13033.
61. Clamp, M., Cuff, J., Searle, S.M. and Barton, G.J. (2004) The Jalview Java alignment editor. Bioinformatics, 20, 426-427.
62. Leibrecht, I. and Kessler, D. (1997) A novel L-cysteine/cystine C-S-lyase directing [2Fe-2S] cluster formation of Synechocystis ferredoxin. J. Biol. Chem., 272, 10442-10447.