The yeast iron regulatory proteins Grx3/4 and Fra2 form heterodimeric complexes containing a [2Fe-2S] cluster with cysteinyl and histidyl ligation

Biochemistry

Volumn 48, Issue 40, 2009, Pages 9569-9581

  Li, Haoran ^a   Mapolelo, Daphne T ^b   Dingra, Nin N ^a   Naik, Sunil G ^c   Lees, Nicholas S ^d   Hoffman, Brian M ^d   Riggs Gelasco, Pamela J ^e   Boi, Hanh Huynh ^c   Johnson, Michael K ^b   Outten, Caryn E ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c EMORY UNIVERSITY   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e Department of Teacher Education and Department of Sociology and Anthropology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CLUSTER STABILITY; CO-EXPRESSION; COORDINATION ENVIRONMENT; CYTOSOLIC; EXAFS STUDIES; GLUTATHIONES; HETERODIMERIC COMPLEXES; HETERODIMERS; HISTIDINE RESIDUES; HOMODIMERS; IN-VITRO; IRON REGULATORY PROTEINS; IRON REGULON; IRON UPTAKE; MONOTHIOL; NUCLEO-CYTOPLASMIC SHUTTLING; RESONANCE RAMAN; SACCHAROMYCES CEREVISIAE; SIGNALING PATHWAYS; UV-VISIBLE ABSORPTION;

BIOCHEMISTRY; COORDINATION REACTIONS; ESCHERICHIA COLI; MOLYBDENUM COMPOUNDS; SIGNALING; TRANSCRIPTION; TRANSCRIPTION FACTORS; YEAST;

IRON COMPOUNDS;

IRON REGULATORY FACTOR; IRON SULFUR PROTEIN; PROTEIN GRX3; PROTEIN GRX4; TRANSCRIPTION FACTOR FRA 2; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; ELECTRON NUCLEAR DOUBLE RESONANCE; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ESCHERICHIA COLI; MOSSBAUER SPECTROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RAMAN SPECTROMETRY; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; ULTRAVIOLET SPECTROSCOPY;

CYSTEINE; DIMERIZATION; ENZYME STABILITY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; GLUTAREDOXINS; HISTIDINE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; IRON-SULFUR PROTEINS; LIGANDS; MULTIPROTEIN COMPLEXES; MUTAGENESIS, SITE-DIRECTED; OXIDOREDUCTASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 70350070125     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901182w     Document Type: Article

References (71)

1. Stohs, S. J., and Bagchi, D. (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radical Biol. Med. 18, 321-336.
2. Yamaguchi-Iwai, Y., Dancis, A., and Klausner, R. D. (1995) AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J. 14, 1231-1239.
3. Yamaguchi-Iwai, Y., Stearman, R., Dancis, A., and Klausner, R. D. (1996) Iron-regulated DNA binding by the AFT1 protein controls the iron regulon in yeast. EMBO J. 15, 3377-3384. (Pubitemid 26231944)
4. Yamaguchi-Iwai, Y., Ueta, R., Fukunaka, A., and Sasaki, R. (2002) Subcellular localization of Aft1 transcription factor responds to iron status in Saccharomyces cerevisiae. J. Biol. Chem. 277, 18914-18918.
5. Casas, C., Aldea, M., Espinet, C., Gallego, C., Gil, R., and Herrero, E. (1997) The AFT1 transcriptional factor is differentially required for expression of high-affinity iron uptake genes in Saccharomyces cerevisiae. Yeast 13, 621-637. (Pubitemid 27232465)
6. Foury, F., and 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.
7. Protchenko, O., Ferea, T., Rashford, J., Tiedeman, J., Brown, P. O., Botstein, D., and Philpott, C. C. (2001) Three cell wall mannoproteins facilitate the uptake of iron in Saccharomyces cerevisiae. J. Biol. Chem. 276, 49244-49250.
8. Kumanovics, A., Chen, O. S., Li, L., Bagley, D., Adkins, E. M., Lin, H., Dingra, N. N., Outten, C. E., Keller, G., Winge, D., Ward, D. M., and Kaplan, J. (2008) Identification of FRA1 and FRA2 as genes involved in regulating the yeast iron regulon in response to decreased mitochondrial iron-sulfur cluster synthesis. J. Biol. Chem. 283, 10276-10286.
9. Ojeda, L., Keller, G., Muhlenhoff, U., Rutherford, J. C., Lill, R., and Winge, D. R. (2006) Role of glutaredoxin-3 and glutaredoxin-4 in the iron regulation of the Aft1 transcriptional activator in Saccharomyces cerevisiae. J. Biol. Chem. 281, 17661-17669.
10. Pujol-Carrion, N., Belli, G., Herrero, E., Nogues, A., and de la Torre-Ruiz, M. A. (2006) Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J. Cell Sci. 119, 4554-4564. (Pubitemid 44830654)
11. Rutherford, J. C., Ojeda, L., Balk, J., Muhlenhoff, U., Lill, R., and Winge, D. R. (2005) Activation of the iron regulon by the yeast Aft1/Aft2 transcription factors depends on mitochondrial but not cytosolic iron-sulfur protein biogenesis. J. Biol. Chem. 280, 10135-10140.
12. Ueta, R., Fujiwara, N., Iwai, K., and Yamaguchi-Iwai, Y. (2007) Mechanism underlying the iron-dependent nuclear export of the ironresponsive transcription factor Aft1p in Saccharomyces cerevisiae. Mol. Biol. Cell 18, 2980-2990.
13. Herrero, E., and de la Torre-Ruiz, M. A. (2007) Monothiol glutaredoxins: a common domain for multiple functions. Cell. Mol. Life Sci. 64, 1518-1530.
14. Muhlenhoff, U., Gerber, J., Richhardt, N., and Lill, R. (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J. 22, 4815-4825. (Pubitemid 37162917)
15. Rodriguez-Manzaneque, M. T., Tamarit, J., Belli, G., Ros, J., and Herrero, E. (2002) Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol. Biol. Cell 13, 1109-1121.
16. Witte, S., Villalba, M., Bi, K., Liu, Y., Isakov, N., and Altman, A. (2000) Inhibition of the c-Jun N-terminal kinase/AP-1 and NFkappaB pathways by PICOT, a novel protein kinase C-interacting protein with a thioredoxin homology domain. J. Biol. Chem. 275, 1902-1909.
17. Jeong, D., Kim, J. M., Cha, H., Oh, J. G., Park, J., Yun, S. H., Ju, E. S., Jeon, E. S., Hajjar, R. J., and Park, W. J. (2008) PICOT attenuates cardiac hypertrophy by disrupting calcineurin-NFAT signaling. Circ. Res. 102, 711-719.
18. Lillig, C. H., Berndt, C., and Holmgren, A. (2008) Glutaredoxin systems. Biochim. Biophys. Acta 1780, 1304-1317.
19. Bandyopadhyay, S., Gama, F., Molina-Navarro, M. M., Gualberto, J. M., Claxton, R., Naik, S. G., Huynh, B. H., Herrero, E., Jacquot, J. P., Johnson, M. K., and Rouhier, N. (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J. 27, 1122-1133.
20. Picciocchi, A., Saguez, C., Boussac, A., Cassier-Chauvat, C., and Chauvat, F. (2007) CGFS-type monothiol glutaredoxins from the cyanobacterium Synechocystis PCC6803 and other evolutionary distant model organisms possess a glutathione-ligated [2Fe-2S] cluster. Biochemistry 46, 15018-15026. (Pubitemid 350308893)
21. Iwema, T., Picciocchi, A., Traore, D. A., Ferrer, J. L., Chauvat, F., and Jacquamet, L. (2009) Structural basis for delivery of the intact [Fe2S2] cluster by monothiol glutaredoxin. Biochemistry 48, 6041-6043.
22. Franco, R., Schoneveld, O. J., Pappa, A., and Panayiotidis, M. I. (2007) The central role of glutathione in the pathophysiology of human diseases. Arch. Physiol. Biochem. 113, 234-258.
23. Johansson, C., Kavanagh, K. L., Gileadi, O., and Oppermann, U. (2007) Reversible sequestration of active site cysteines in a 2Fe-2S-bridged dimer provides a mechanism for glutaredoxin 2 regulation in human mitochondria. J. Biol. Chem. 282, 3077-3082.
24. Rouhier, N., Unno, H., Bandyopadhyay, S., Masip, L., Kim, S. K., Hirasawa, M., Gualberto, J. M., Lattard, V., Kusunoki, M., Knaff, D. B., Georgiou, G., Hase, T., Johnson, M. K., and Jacquot, J. P. (2007) Functional, structural, and spectroscopic characterization of a glutathione-ligated [2Fe-2S] cluster in poplar glutaredoxin C1. Proc. Natl. Acad. Sci. U.S.A. 104, 7379-7384.
25. Huynen, M. A., Spronk, C. A., Gabaldon, T., and Snel, B. (2005) Combining data from genomes, Y2H and 3D structure indicates that BolA is a reductase interacting with a glutaredoxin. FEBS Lett. 579, 591-596.
26. Aldea, M., Hernandez-Chico, C., de la Campa, A. G., Kushner, S. R., and Vicente, M. (1988) Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli. J. Bacteriol. 170, 5169-5176.
27. Giot, L., Bader, J. S., Brouwer, C., Chaudhuri, A., Kuang, B., Li, Y., Hao, Y. L., Ooi, C. E., Godwin, B., Vitols, E., Vijayadamodar, G., Pochart, P., Machineni, H., Welsh, M., Kong, Y., Zerhusen, B., Malcolm, R., Varrone, Z., Collis, A., Minto, M., Burgess, S., McDaniel, L., Stimpson, E., Spriggs, F., Williams, J., Neurath, K., Ioime, N., Agee, M., Voss, E., Furtak, K., Renzulli, R., Aanensen, N., Carrolla, S., Bickelhaupt, E., Lazovatsky, Y., DaSilva, A., Zhong, J., Stanyon, C. A., Finley, R. L. Jr., White, K. P., Braverman, M., Jarvie, T., Gold, S., Leach, M., Knight, J., Shimkets, R. A., McKenna, M. P., Chant, J., and Rothberg, J. M. (2003) A protein interaction map of Drosophila melanogaster. Science 302, 1727-1736. (Pubitemid 37505730)
28. Ito, T., Tashiro, K., Muta, S., Ozawa, R., Chiba, T., Nishizawa, M., Yamamoto, K., Kuhara, S., and Sakaki, Y. (2000) Toward a protein-protein interaction map of the budding yeast: A comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. Proc. Natl. Acad. Sci. U.S.A. 97, 1143-1147.
29. Ho, Y., Gruhler, A., Heilbut, A., Bader, G. D., Moore, L., Adams, S. L., Millar, A., Taylor, P., Bennett, K., Boutilier, K., Yang, L., Wolting, C., Donaldson, I., Schandorff, S., Shewnarane, J., Vo, M., Taggart, J., Goudreault, M., Muskat, B., Alfarano, C., Dewar, D., Lin, Z., Michalickova, K., Willems, A. R., Sassi, H., Nielsen, P. A., Rasmussen, K. J., Andersen, J. R., Johansen, L. E., Hansen, L. H., Jespersen, H., Podtelejnikov, A., Nielsen, E., Crawford, J., Poulsen, V., Sorensen, B. D., Matthiesen, J., Hendrickson, R. C., Gleeson, F., Pawson, T., Moran, M. F., Durocher, D., Mann, M., Hogue, C. W., Figeys, D., and Tyers, M. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183. (Pubitemid 34059520)
30. Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A. P., Punna, T., Peregrin-Alvarez, J. M., Shales, M., Zhang, X., Davey, M., Robinson, M. D., Paccanaro, A., Bray, J. E., Sheung, A., Beattie, B., Richards, D. P., Canadien, V., Lalev, A., Mena, F., Wong, P., Starostine, A., Canete, M. M., Vlasblom, J., Wu, S., Orsi, C., Collins, S. R., Chandran, S., Haw, R., Rilstone, J. J., Gandi, K., Thompson, N. J., Musso, G.St, Onge, P., Ghanny, S., Lam, M. H., Butland, G., Altaf-Ul, A. M., Kanaya, S., Shilatifard, A., O'Shea, E., Weissman, J. S., Ingles, C. J., Hughes, T. R., Parkinson, J., Gerstein, M., Wodak, S. J., Emili, A., and Greenblatt, J. F. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643.
31. Butland, G., Peregrin-Alvarez, J. M., Li, J., Yang, W., Yang, X., Canadien, V., Starostine, A., Richards, D., Beattie, B., Krogan, N., Davey, M., Parkinson, J., Greenblatt, J., and Emili, A. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433, 531-537. (Pubitemid 40204311)
32. Couturier, J., Jacquot, J. P., and Rouhier, N. (2009) Evolution and diversity of glutaredoxins in photosynthetic organisms. Cell. Mol. Life Sci. 66, 2539-2557.
33. Gibson, L. M., Dingra, N. N., Outten, C. E., and Lebioda, L. (2008) Structure of the thioredoxin-like domain of yeast glutaredoxin 3. Acta Crystallogr., Sect. D: Biol. Crystallogr. 64, 927-932.
34. Lillig, C. H., Berndt, C., Vergnolle, O., Lonn, M. E., Hudemann, C., Bill, E., and Holmgren, A. (2005) Characterization of human glutaredoxin 2 as iron-sulfur protein: a possible role as redox sensor. Proc. Natl. Acad. Sci. U.S.A. 102, 8168-8173.
35. Riemer, J., Hoepken, H. H., Czerwinska, H., Robinson, S. R., and Dringen, R. (2004) Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal. Biochem. 331, 370-375.
36. Beinert, H. (1983) Semi-micro methods for analysis of labile sulfide and of labile sulfide plus sulfane sulfur in unusually stable iron-sulfur proteins. Anal. Biochem. 131, 373-378.
37. Broderick, J. B., Henshaw, T. F., Cheek, J., Wojtuszewski, K., Smith, S. R., Trojan, M. R., McGhan, R. M., Kopf, A., Kibbey, M., and Broderick, W. E. (2000) Pyruvate formate-lyase-activating enzyme: strictly anaerobic isolation yields active enzyme containing a [3Fe- 4S](+) cluster. Biochem. Biophys. Res. Commun. 269, 451-456. (Pubitemid 30440321)
38. Outten, C. E., and Culotta, V. C. (2004) Alternative start sites in the Saccharomyces cerevisiae GLR1 gene are responsible for mitochondrial and cytosolic isoforms of glutathione reductase. J. Biol. Chem. 279, 7785-7791.
39. Cosper, M. M., Jameson, G. N., Hernandez, H. L., Krebs, C., Huynh, B. H., and Johnson, M. K. (2004) Characterization of the cofactor composition of Escherichia coli biotin synthase. Biochemistry 43, 2007-2021. (Pubitemid 38233263)
40. Werst, M. M., Davoust, C. E., and Hoffman, B. M. (1991) Ligand spin-densities in blue copper proteins by Q-band H-1 and N-14 ENDOR spectroscopy. J. Am. Chem. Soc. 113, 1533-1538.
41. Ravi, N., Bollinger, J. M., Huynh, B. H., Edmondson, D. E., and Stubbe, J. (1994) Mechanism of assembly of the tyrosyl radicaldiiron(III) cofactor of Escherichia coli ribonucleotide reductase. 1. Mossbauer characterization of the diferric radical precursor. J. Am. Chem. Soc. 116, 8007-8014.
42. Dailey, H. A., Finnegan, M. G., and Johnson, M. K. (1994) Human ferrochelatase is an iron-sulfur protein. Biochemistry 33, 403-407.
43. Stephens, P. J., Thomson, A. J., Dunn, J. B. R., Keiderling, T. A., Rawlings, J., Rao, K. K., and Hall, D. O. (1978) Circular-dichroism and magnetic circular-dichroism of iron-sulfur proteins. Biochemistry 17, 4770-4778.
44. Fu, W., Drozdzewski, P. M., Davies, M. D., Sligar, S. G., and Johnson, M. K. (1992) Resonance Raman and magnetic circular dichroism studies of reduced [2Fe-2S] proteins. J. Biol. Chem. 267, 15502-15510.
45. Han, S., Czernuszewicz, R. S., Kimura, T., Adams, M. W. W., and Spiro, T. G. (1989) Fe2S2 protein resonance Raman-spectra revisited; Structural variations among adrenodoxin, ferredoxin, and red paramagnetic protein. J. Am. Chem. Soc. 111, 3505-3511.
46. Iwasaki, T., Kounosu, A., Kolling, D. R. J., Crofts, A. R., Dikanov, S. A., Jin, A., Imai, T., and Urushiyama, A. (2004) Characterization of the pH-dependent resonance Raman transitions of archaeal and bacterial Rieske [2Fe-2S] proteins. J. Am. Chem. Soc. 126, 4788-4789.
47. Kounosu, A., Li, Z. R., Cosper, N. J., Shokes, J. E., Scott, R. A., Imai, T., Urushiyama, A., and Iwasaki, T. (2004) Engineering a threecysteine, one-histidine ligand environment into a new hyperthermophilic archaeal Rieske-type [2Fe-2S] ferredoxin from Sulfolobus solfataricus. J. Biol. Chem. 279, 12519-12528.
48. Kuila, D., Schoonover, J. R., Dyer, R. B., Batie, C. J., Ballou, D. P., Fee, J. A., and Woodruff, W. H. (1992) Resonance Raman studies of Rieske-type proteins. Biochim. Biophys. Acta 1140, 175-183.
49. Rotsaert, F. A. J., Pikus, J. D., Fox, B. G., Markley, J. L., and Sanders-Loehr, J. (2003) N-isotope effects on the Raman spectra of Fe2S2 ferredoxin and Rieske ferredoxin: evidence for structural rigidity of metal sites. J. Biol. Inorg. Chem. 8, 318-326.
50. Tirrell, T. F., Paddock, M. L., Conlan, A. R., Smoll, E. J. Jr., Nechushtai, R., Jennings, P. A., and Kim, J. E. (2009) Resonance Raman studies of the (His)(Cys)(3) 2Fe-2S cluster of MitoNEET: comparison to the (Cys)(4) mutant and implications of the effects of pH on the labile metal center. Biochemistry 48, 4747-4752.
51. Meyer, J., Fujinaga, J., Gaillard, J., and Lutz, M. (1994) Mutated forms of the [2Fe-2S] ferredoxin from Clostridium pasteurianum with noncysteinyl ligands to the iron-sulfur cluster. Biochemistry 33, 13642-13650. (Pubitemid 24381924)
52. Moulis, J. M., Davasse, V., Golinelli, M. P., Meyer, J., and Quinkal, I. (1996) The coordination sphere of iron-sulfur clusters: lessons from site-directed mutagenesis experiments. J. Biol. Inorg. Chem. 1, 2-14.
53. Fee, J. A., Findling, K. L., Yoshida, T., Hille, R., Tarr, G. E., Hearshen, D. O., Dunham, W. R., Day, E. P., Kent, T. A., and Munck, E. (1984) Purification and characterization of the Rieske iron-sulfur protein from Thermus thermophilus. Evidence for a [2Fe- 2S] cluster having non-cysteine ligands. J. Biol. Chem. 259, 124-133.
54. Bertrand, P., Guigliarelli, B., Gayda, J. P., Beardwood, P., and Gibson, J. F. (1985) A ligand-field model to describe a new class of 2Fe-2S clusters in proteins and their synthetic analogs. Biochim. Biophys. Acta 831, 261-266.
55. Guigliarelli, B., and Bertrand, P. (1999) Application of EPR spectroscopy to the structural and functional study of iron-sulfur proteins, Adv. Inorg. Chem. 47, 421-497.
56. 15N-enriched phthalate dioxygenase from Pseudomonas cepacia proves that two histidines are coordinated to the [2Fe-2S] Rieske-type clusters. Biochemistry 28, 4861-4871.
57. Gurbiel, R. J., Doan, P. E., Gassner, G. T., Macke, T. J., Case, D. A., Ohnishi, T., Fee, J. A., Ballou, D. P., and Hoffman, B. M. (1996) Active site structure of Rieske-type proteins: electron nuclear double resonance studies of isotopically labeled phthalate dioxygenase from Pseudomonas cepacia and Rieske protein from Rhodobacter capsulatus and molecular modeling studies of a Rieske center. Biochemistry 35, 7834-7845. (Pubitemid 26202522)
58. Clark-Baldwin, K., Tierney, D. L., Govindaswamy, N., Gruff, E. S., Kim, C., Berg, J., Koch, S. A., and Penner-Hahn, J. E. (1998) The limitations of X-ray absorption spectroscopy for determining the structure of zinc sites in proteins. When is a tetrathiolate not a tetrathiolate? J. Am. Chem. Soc. 120, 8401-8409.
59. Stemmler, T. L., Sossong, T. M. Jr., Goldstein, J. I., Ash, D. E., Elgren, T. E., Kurtz, D. M. Jr., and Penner-Hahn, J. E. (1997) EXAFS comparison of the dimanganese core structures of manganese catalase, arginase, and manganese-substituted ribonucleotide reductase and hemerythrin. Biochemistry 36, 9847-9858.
60. Hunsicker-Wang, L. M., Heine, A., Chen, Y., Luna, E. P., Todaro, T., Zhang, Y. M., Williams, P. A., McRee, D. E., Hirst, J., Stout, C. D., and Fee, J. A. (2003) High-resolution structure of the soluble, respiratory-type Rieske protein from Thermus thermophilus: analysis and comparison. Biochemistry 42, 7303-7317. (Pubitemid 36735809)
61. Kolling, D. J., Brunzelle, J. S., Lhee, S., Crofts, A. R., and Nair, S. K. (2007) Atomic resolution structures of Rieske iron-sulfur protein: role of hydrogen bonds in tuning the redox potential of iron-sulfur clusters. Structure 15, 29-38. (Pubitemid 46091746)
62. Cosper, N. J., Eby, D. M., Kounosu, A., Kurosawa, N., Neidle, E. L., Kurtz, D. M. Jr., Iwasaki, T., and Scott, R. A. (2002) Redox-dependent structural changes in archaeal and bacterial Rieske-type [2Fe-2S] clusters. Protein Sci. 11, 2969-2973. (Pubitemid 35365262)
63. Tsang, H. T., Batie, C. J., Ballou, D. P., and Penner-Hahn, J. E. (1989) X-ray absorption spectroscopy of the [2Fe-2S] Rieske cluster in Pseudomonas cepacia phthalate dioxygenase. Determination of core dimensions and iron ligation. Biochemistry 28, 7233-7240.
64. Hou, X., Liu, R., Ross, S., Smart, E. J., Zhu, H., and Gong, W. (2007) Crystallographic studies of human MitoNEET. J. Biol. Chem. 282, 33242-33246.
65. Lin, J., Zhou, T., Ye, K., and Wang, J. (2007) Crystal structure of human mitoNEET reveals distinct groups of iron sulfur proteins. Proc. Natl. Acad. Sci. U.S.A. 104, 14640-14645.
66. Paddock, M. L., Wiley, S. E., Axelrod, H. L., Cohen, A. E., Roy, M., Abresch, E. C., Capraro, D., Murphy, A. N., Nechushtai, R., Dixon, J. E., and Jennings, P. A. (2007) MitoNEET is a uniquely folded 2Fe 2S outer mitochondrial membrane protein stabilized by pioglitazone. Proc. Natl. Acad. Sci. U.S.A. 104, 14342-14347.
67. Agar, J. N., Krebs, C., Frazzon, J., Huynh, B. H., Dean, D. R., and Johnson, M. K. (2000) IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. Biochemistry 39, 7856-7862. (Pubitemid 30452357)
68. Netz, D. J., Pierik, A. J., Stumpfig, M., Muhlenhoff, U., and Lill, R. (2007) The Cfd1-Nbp35 complex acts as a scaffold for iron-sulfur protein assembly in the yeast cytosol. Nat. Chem. Biol. 3, 278-286.
69. Yuvaniyama, P., Agar, J. N., Cash, V. L., Johnson, M. K., and Dean, D. R. (2000) NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc. Natl. Acad. Sci. U.S.A. 97, 599-604.
70. Bonomi, F., Iametti, S., Ta, D., and Vickery, L. E. (2005) Multiple turnover transfer of [2Fe2S] clusters by the iron-sulfur cluster assembly scaffold proteins IscU and IscA. J. Biol. Chem. 280, 29513-29518.
71. Raulfs, E. C., O'Carroll, I. P., Dos Santos, P. C., Unciuleac, M. C., and Dean, D. R. (2008) In vivo iron-sulfur cluster formation. Proc. Natl. Acad. Sci. U.S.A. 105, 8591-8596.