His86 from the N-terminus of frataxin coordinates iron and is required for Fe-S cluster synthesis

Biochemistry

Volumn 52, Issue 35, 2013, Pages 6085-6096

  Gentry, Leslie E ^a   Thacker, Matthew A ^a   Doughty, Reece ^a,b   Timkovich, Russell ^a   Busenlehner, Laura S ^a  

^a UNIVERSITY OF ALABAMA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS PATHWAYS; CHAPERONE FUNCTIONS; CLUSTER SYNTHESIS; CYSTEINE DESULFURASE; FRIEDREICH'S ATAXIAS; PROTEIN-PROTEIN INTERACTIONS; QUATERNARY COMPLEXES; STRUCTURAL APPROACH;

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; COORDINATION REACTIONS; IRON; MACHINERY; NEURODEGENERATIVE DISEASES; PROTEINS;

IRON COMPOUNDS;

ASPARTIC ACID; CHAPERONE; FRATAXIN; GLUTAMIC ACID; HISTIDINE; IRON; SULFUR;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; FLUORESCENCE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MITOCHONDRION; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STOICHIOMETRY; SYNTHESIS;

HISTIDINE; HUMANS; IRON; IRON-BINDING PROTEINS; IRON-SULFUR PROTEINS; MODELS, MOLECULAR; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR;

EID: 84883480177     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400443n     Document Type: Article

References (43)

1. Campuzano, V., Montermini, L., Molto, M. D., Pianese, L., Cossee, M., Cavalcanti, F., Monros, E., Rodius, F., Duclos, F., Monticelli, A., Zara, F., Canizares, J., Koutnikova, H., Bidichandani, S. I., Gellera, C., Brice, A., Trouillas, P., De Michele, G., Filla, A., De Frutos, R., Palau, F., Patel, P. I., Di Donato, S., Mandel, J. L., Cocozza, S., Koenig, M., and Pandolfo, M. (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion Science 271, 1423-1427
2. Schmucker, S. and Puccio, H. (2010) Understanding the molecular mechanisms of Friedreich's ataxia to develop therapeutic approaches Hum. Mol. Genet. 19, R103-110
3. Gonzalez-Cabo, P., Llorens, J. V., Palau, F., and Molto, M. D. (2009) Friedreich ataxia: an update on animal models, frataxin function and therapies Adv. Exp. Med. Biol. 652, 247-261
4. Rouault, T. A. and Tong, W. H. (2008) Iron-sulfur cluster biogenesis and human disease Trends Genet. 24, 398-407
5. Ye, H. and Rouault, T. A. (2010) Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease Biochemistry 49, 4945-4956
6. Muhlenhoff, 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
7. 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
8. Watson, H. M., Gentry, L. E., Asuru, A. P., Wang, Y., Marcus, S., and Busenlehner, L. S. (2012) Heterotrifunctional chemical cross-linking mass spectrometry confirms physical interaction between human frataxin and ISU Biochemistry 51, 6889-6891
9. Schmucker, S., Martelli, A., Colin, F., Page, A., Wattenhofer-Donze, M., Reutenauer, L., and Puccio, H. (2011) Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 iron-sulfur assembly complex PLoS One 6, e16199
10. Colin, F., Martelli, A., Clemancey, M., Latour, J. M., Gambarelli, S., Zeppieri, L., Birck, C., Page, A., Puccio, H., and Ollagnier de Choudens, S. (2013) Mammalian Frataxin Controls Sulfur Production and Iron Entry during de Novo Fe(4)S(4) Cluster Assembly J. Am. Chem. Soc. 135, 733-740
11. Pandolfo, M. and Pastore, A. (2009) The pathogenesis of Friedreich ataxia and the structure and function of frataxin J. Neurol. 256 (Suppl 1) 9-17
12. 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
13. 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
14. 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
15. 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
16. Lane, D. J. and Richardson, D. R. (2010) Frataxin, a molecule of mystery: trading stability for function in its iron-binding site Biochem. J. 426, e1-3
17. Huang, J., Dizin, E., and Cowan, J. (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
18. Pastore, C., Franzese, M., Sica, F., Temussi, P., and Pastore, A. (2007) Understanding the binding properties of an unusual metal-binding protein - a study of bacterial frataxin FEBS. J. 274, 4199-4210
19. Maret, W. and Vallee, B. L. (1993) Cobalt as probe and label of proteins Methods Enzymol. 226, 52-71
20. Thompsen, J. C. and Mottola, H. A. (1984) Kinetics of the Complexation of Iron(II) with Ferrozine Anal. Chem. 56, 755-757
21. van de Weert, M. (2010) Fluorescence quenching to study protein-ligand binding: common errors J. Fluoresc. 20, 625-629
22. Musco, G., de Tommasi, T., Stier, G., Kolmerer, B., Bottomley, M., Adinolfi, S., Muskett, F. W., Gibson, T. J., Frenkiel, T. A., and Pastore, A. (1999) Assignment of the 1H, 15N, and 13C resonances of the C-terminal domain of frataxin, the protein responsible for Friedreich ataxia J. Biomol. NMR 15, 87-88
23. Kay, L., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 114, 10663-10665
24. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRpipe: A multidimensional spectral processing system based on Unix pipes J. Biomol. NMR 6, 227-293
25. Grzesiek, S., Stahl, S. J., Wingfield, P. T., and Bax, A. (1996) The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR Biochemistry 35, 10256-10261
26. Ma, B., Zhang, K., Hendrie, C., Liang, C., Li, M., Doherty-Kirby, A., and Lajoie, G. (2003) PEAKS: powerful software for peptide de novo sequencing by tandem mass spectrometry Rapid Commun. Mass Spectrom. 17, 2337-2342
27. Engen, J. R. and Smith, D. L. (2001) Investigating protein structure and dynamics by hydrogen exchange MS Anal. Chem. 73, 256A-265A
28. Busenlehner, L. S. and Armstrong, R. N. (2005) Insights into enzyme structure and dynamics elucidated by amide H/D exchange mass spectrometry Arch. Biochem. Biophys. 433, 34-46
29. Tong, W. H. and Rouault, T. A. (2006) Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis Cell Metab. 3, 199-210
30. Solomon, E. I., Brunold, T. C., Davis, M. I., Kemsley, J. N., Lee, S. K., Lehnert, N., Neese, F., Skulan, A. J., Yang, Y. S., and Zhou, J. (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes Chem. Rev. 100, 235-350
31. Krezel, A., Lesniak, W., Jezowska-Bojczuk, M., Mlynarz, P., Brasuñ, J., Kozlowski, H., and Bal, W. (2001) Coordination of heavy metals by dithiothreitol, a commonly used thiol group protectant J. Inorg. Biochem. 84, 77-88
32. Bertini, I. and Luchinat, C. (1984) High spin cobalt(II) as a probe for the investigation of metalloproteins Adv. Inorg. Biochem. 6, 71-111
33. Dian, C., Vitale, S., Leonard, G. A., Bahlawane, C., Fauquant, C., Leduc, D., Muller, C., de Reuse, H., Michaud-Soret, I., and Terradot, L. (2011) The structure of the Helicobacter pylori ferric uptake regulator Fur reveals three functional metal binding sites Mol. Microbiol. 79, 1260-1275
34. Otting, G. (2010) Protein NMR using paramagnetic ions Annu. Rev. Biophys. 39, 387-405
35. Li, H., Gakh, O., Smith, D. Y. t., and Isaya, G. (2009) Oligomeric yeast frataxin drives assembly of core machinery for mitochondrial iron-sulfur cluster synthesis J. Biol. Chem. 284, 21971-21980
36. Gakh, O., Bedekovics, T., Duncan, S. F., Smith, D. Y. t., Berkholz, D. S., and Isaya, G. (2010) Normal and Friedreich ataxia cells express different isoforms of frataxin with complementary roles in iron-sulfur cluster assembly J. Biol. Chem. 285, 38486-38501
37. 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
38. Pearson, R. G. (1968) Hard and Soft Acids and Bases HSAB 1. Fundamental Principles J. Chem. Educ. 45, 581
39. Asuru, A. P. and Busenlehner, L. S. (2011) Analysis of human ferrochelatase iron binding via amide hydrogen/deuterium exchange mass spectrometry Intl. J. Mass Spectrom. 302, 76-84
40. Cavadini, P., Adamec, J., Taroni, F., Gakh, O., and Isaya, G. (2000) Two-step processing of human frataxin by mitochondrial processing peptidase. Precursor and intermediate forms are cleaved at different rates J. Biol. Chem. 275, 41469-41475
41. Yoon, T., Dizin, E., and Cowan, J. A. (2007) N-terminal iron-mediated self-cleavage of human frataxin: regulation of iron binding and complex formation with target proteins J. Biol. Inorg. Chem. 12, 535-542
42. 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
43. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0 Bioinformatics 23, 2947-2948