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Applied Microbiology and Biotechnology

, Volume 91, Issue 1, pp 47–61 | Cite as

Bacterial cysteine desulfurases: versatile key players in biosynthetic pathways of sulfur-containing biofactors

  • Ryota Hidese
  • Hisaaki Mihara
  • Nobuyoshi EsakiEmail author
Mini-Review

Abstract

Cysteine desulfurases are pyridoxal 5′-phosphate-dependent homodimeric enzymes that catalyze the conversion of L-cysteine to L-alanine and sulfane sulfur via the formation of a protein-bound cysteine persulfide intermediate on a conserved cysteine residue. The enzymes are capable of donating the persulfide sulfur atoms to a variety of biosynthetic pathways for sulfur-containing biofactors, such as iron–sulfur clusters, thiamin, transfer RNA thionucleosides, biotin, and lipoic acid. The enormous advances in biochemical and structural studies of these biosynthetic pathways over the past decades provide an opportunity for detailed understanding of the nature of the excellent sulfur transfer mechanism of cysteine desulfurases.

Keywords

Cysteine desulfurase Sulfur transfer Sulfur-containing biofactors Biosynthetic pathways A persulfide intermediate 

References

  1. Adam AC, Bornhövd C, Prokisch H, Neupert W, Hell K (2006) The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria. EMBO J 25:174–183CrossRefGoogle Scholar
  2. Adinolfi S, Iannuzzi C, Prischi F, Pastore C, Iametti S, Martin SR, Bonomi F, Pastore A (2009) Bacterial frataxin CyaY is the gatekeeper of iron–sulfur cluster formation catalyzed by IscS. Nat Struct Mol Biol 16:390–396CrossRefGoogle Scholar
  3. Agar JN, Krebs C, Frazzon J, Huynh BH, Dean DR, Johnson MK (2000) IscU as a scaffold for iron–sulfur cluster biosynthesis: sequential assembly of [2Fe–2S] and [4Fe–4S] clusters in IscU. Biochemistry 39:7856–7862CrossRefGoogle Scholar
  4. Albrecht AG, Netz DJ, Miethke M, Pierik AJ, Burghaus O, Peuckert F, Lill R, Marahiel MA (2010) SufU is an essential iron–sulfur cluster scaffold protein in Bacillus subtilis. J Bacteriol 192:1643–1651CrossRefGoogle Scholar
  5. Angelini S, Gerez C, Ollagnier-de Choudens S, Sanakis Y, Fontecave M, Barras F, Py B (2008) NfuA, a new factor required for maturing Fe/S proteins in Escherichia coli under oxidative stress and iron starvation conditions. J Biol Chem 283:14084–14091CrossRefGoogle Scholar
  6. Balk J, Pilon M (2011) Ancient and essential: the assembly of iron–sulfur clusters in plants. Trends Plant Sci 16:218–226. doi: 10.1016/j.tplants.2010.12.006 CrossRefGoogle Scholar
  7. Bandyopadhyay S, Naik SG, O'Carroll IP, Huynh BH, Dean DR, Johnson MK, Dos Santos PC (2008) A proposed role for the Azotobacter vinelandii NfuA protein as an intermediate iron–sulfur cluster carrier. J Biol Chem 283:14092–14099CrossRefGoogle Scholar
  8. Begley TP, Downs DM, Ealick SE, McLafferty FW, Van Loon AP, Taylor S, Campobasso N, Chiu HJ, Kinsland C, Reddick JJ, Xi J (1999) Thiamin biosynthesis in prokaryotes. Arch Microbiol 171:293–300CrossRefGoogle Scholar
  9. Behshad E, Parkin SE, Bollinger JM Jr (2004) Mechanism of cysteine desulfurase Slr0387 from Synechocystis sp. PCC 6803: kinetic analysis of cleavage of the persulfide intermediate by chemical reductants. Biochemistry 43:12220–12226CrossRefGoogle Scholar
  10. Behshad E, Bollinger JM Jr (2009) Kinetic analysis of cysteine desulfurase CD0387 from Synechocystis sp. PCC 6803: formation of the persulfide intermediate. Biochemistry 48:12014–12023CrossRefGoogle Scholar
  11. Beinert H (2000) Iron–sulfur proteins: ancient structures, still full of surprises. J Biol Inorg Chem 5:2–15CrossRefGoogle Scholar
  12. Bergstrom DE, Leonard NJ (1972) Structure of the borohydride reduction product of photolinked 4-thiouracil and cytosine. Fluorescent probe of transfer ribonucleic acid tertiary structure. J Am Chem Soc 94:6178–6182CrossRefGoogle Scholar
  13. Berkovitch F, Nicolet Y, Wan JT, Jarrett JT, Drennan CL (2004) Crystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme. Science 303:76–79CrossRefGoogle Scholar
  14. Beynon J, Ally A, Cannon M, Cannon F, Jacobson M, Cash V, Dean D (1987) Comparative organization of nitrogen fixation-specific genes from Azotobacter vinelandii and Klebsiella pneumoniae: DNA sequence of the nifUSV genes. J Bacteriol 169:4024–4029Google Scholar
  15. Biederbick A, Stehling O, Rosser R, Niggemeyer B, Nakai Y, Elsässer HP, Lill R (2006) Role of human mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Mol Cell Biol 26:5675–5687CrossRefGoogle Scholar
  16. Bonomi F, Iametti S, Ta D, Vickery LE (2005) Multiple turnover transfer of [2Fe2S] clusters by the iron–sulfur cluster assembly scaffold proteins IscU and IscA. J Biol Chem 280:29513–29518CrossRefGoogle Scholar
  17. Bonomi F, Iametti S, Morleo A, Ta D, Vickery LE (2008) Studies on the mechanism of catalysis of iron–sulfur cluster transfer from IscU[2Fe2S] by HscA/HscB chaperones. Biochemistry 47:12795–12801CrossRefGoogle Scholar
  18. Broach RB, Jarrett JT (2006) Role of the [2Fe-2S]2+ cluster in biotin synthase: mutagenesis of the atypical metal ligand arginine 260. Biochemistry 45:14166–14174CrossRefGoogle Scholar
  19. Cavazza C, Contreras-Martel C, Pieulle L, Chabrière E, Hatchikian EC, Fontecilla-Camps JC (2006) Flexibility of thiamine diphosphate revealed by kinetic crystallographic studies of the reaction of pyruvate-ferredoxin oxidoreductase with pyruvate. Structure 14:217–224CrossRefGoogle Scholar
  20. Chahal HK, Dai Y, Saini A, Ayala-Castro C, Outten FW (2009) The SufBCD Fe–S scaffold complex interacts with SufA for Fe–S cluster transfer. Biochemistry 48:10644–10653CrossRefGoogle Scholar
  21. Challand MR, Martins FT, Roach PL (2010) Catalytic activity of the anaerobic tyrosine lyase required for thiamine biosynthesis in Escherichia coli. J Biol Chem 285:5240–5248CrossRefGoogle Scholar
  22. Chandramouli K, Johnson MK (2006) HscA and HscB stimulate [2Fe–2S] cluster transfer from IscU to apoferredoxin in an ATP-dependent reaction. Biochemistry 45:11087–11095CrossRefGoogle Scholar
  23. Chandramouli K, Unciuleac MC, Naik S, Dean DR, Huynh BH, Johnson MK (2007) Formation and properties of [4Fe–4S] clusters on the IscU scaffold protein. Biochemistry 46:6804–6811CrossRefGoogle Scholar
  24. Chatterjee A, Han X, McLafferty FW, Begley TP (2006) Biosynthesis of thiamin thiazole: determination of the regiochemistry of the S/O acyl shift by using 1,4-dideoxy-D-xylulose-5-phosphate. Angew Chem Int Ed Engl 45:3507–3510CrossRefGoogle Scholar
  25. Cicchillo RM, Lee KH, Baleanu-Gogonea C, Nesbitt NM, Krebs C, Booker SJ (2004) Escherichia coli lipoyl synthase binds two distinct [4Fe–4S] clusters per polypeptide. Biochemistry 43:11770–11781CrossRefGoogle Scholar
  26. Cicchillo RM, Booker SJ (2005) Mechanistic investigations of lipoic acid biosynthesis in Escherichia coli: both sulfur atoms in lipoic acid are contributed by the same lipoyl synthase polypeptide. J Am Chem Soc 127:2860–2861CrossRefGoogle Scholar
  27. Cupp-Vickery JR, Urbina H, Vickery LE (2003) Crystal structure of IscS, a cysteine desulfurase from Escherichia coli. J Mol Biol 330:1049–1059CrossRefGoogle Scholar
  28. Cupp-Vickery JR, Peterson JC, Ta DT, Vickery LE (2004) Crystal structure of the molecular chaperone HscA substrate binding domain complexed with the IscU recognition peptide ELPPVKIHC. J Mol Biol 342:1265–1278CrossRefGoogle Scholar
  29. Desnoyers G, Morissette A, Prévost K, Massé E (2009) Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J 28:1551–1561CrossRefGoogle Scholar
  30. Dos Santos PC, Johnson DC, Ragle BE, Unciuleac MC, Dean DR (2007) Controlled expression of nif and isc iron–sulfur protein maturation components reveals target specificity and limited functional replacement between the two systems. J Bacteriol 189:2854–2862CrossRefGoogle Scholar
  31. Dos Santos PC, Dean DR (2008) A newly discovered role for iron–sulfur clusters. Proc Natl Acad Sci USA 105:11589–11590CrossRefGoogle Scholar
  32. Douglas P, Kriek M, Bryant P, Roach PL (2006) Lipoyl synthase inserts sulfur atoms into an octanoyl substrate in a stepwise manner. Angew Chem Int Ed Engl 45:5197–5199CrossRefGoogle Scholar
  33. Drennan CL, Peters JW (2003) Surprising cofactors in metalloenzymes. Curr Opin Struct Biol 13:220–226CrossRefGoogle Scholar
  34. Eccleston JF, Petrovic A, Davis CT, Rangachari K, Wilson RJ (2006) The kinetic mechanism of the SufC ATPase: the cleavage step is accelerated by SufB. J Biol Chem 281:8371–8378CrossRefGoogle Scholar
  35. Esaki N, Nakamura T, Tanaka H, Soda K (1982) Selenocysteine lyase, a novel enzyme that specifically acts on selenocysteine. Mammalian distribution and purification and properties of pig liver enzyme. J Biol Chem 257:4386–4391Google Scholar
  36. Favre A, Yaniv M, Michelson AM (1969) The photochemistry of 4-thiouridine in Escherichia coli t-RNA 1Val. Biochem Biophys Res Commun 37:266–271CrossRefGoogle Scholar
  37. Favre A, Michelson AM, Yaniv M (1971) Photochemistry of 4-thiouridine in Escherichia coli transfer RNA1Val. J Mol Biol 58:367–379CrossRefGoogle Scholar
  38. Flint DH (1996) Escherichia coli contains a protein that is homologous in function and N-terminal sequence to the protein encoded by the nifS gene of Azotobacter vinelandii and that can participate in the synthesis of the Fe–S cluster of dihydroxy-acid dehydratase. J Biol Chem 271:16068–16074Google Scholar
  39. Frey PA, Hegeman AD, Ruzicka FJ (2008) The Radical SAM Superfamily. Crit Rev Biochem Mol Biol 43:63–88CrossRefGoogle Scholar
  40. Fuezery AK, Oh JJ, Ta DT, Vickery LE, Markley JL (2011) Three hydrophobic amino acids in Escherichia coli HscB make the greatest contribution to the stability of the HscB-IscU complex. BMC Biochem 12:3CrossRefGoogle Scholar
  41. Giel JL, Rodionov D, Liu M, Blattner FR, Kiley PJ (2006) IscR-dependent gene expression links iron–sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol Microbiol 60:1058–1075CrossRefGoogle Scholar
  42. Grishin NV, Phillips MA, Goldsmith EJ (1995) Modeling of the spatial structure of eukaryotic ornithine decarboxylases. Protein Sci 4:1291–1304CrossRefGoogle Scholar
  43. Gupta V, Sendra M, Naik SG, Chahal HK, Huynh BH, Outten FW, Fontecave M, Ollagnier de Choudens S (2009) Native Escherichia coli SufA, coexpressed with SufBCDSE, purifies as a [2Fe–2S] protein and acts as an Fe–S transporter to Fe–S target enzymes. J Am Chem Soc 131:6149–6153CrossRefGoogle Scholar
  44. Hernández HL, Pierrel F, Elleingand E, Garcia-Serres R, Huynh BH, Johnson MK, Fontecave M, Atta M (2007) MiaB, a bifunctional radical-S-adenosylmethionine enzyme involved in the thiolation and methylation of tRNA, contains two essential [4Fe-4S] clusters. Biochemistry 46:5140–5147CrossRefGoogle Scholar
  45. Hille R (2002) Molybdenum and tungsten in biology. Trends Biochem Sci 27:360–367CrossRefGoogle Scholar
  46. Hoff KG, Ta DT, Tapley TL, Silberg JJ, Vickery LE (2002) Hsc66 substrate specificity is directed toward a discrete region of the iron–sulfur cluster template protein IscU. J Biol Chem 277:27353–27359CrossRefGoogle Scholar
  47. Hoff KG, Cupp-Vickery JR, Vickery LE (2003) Contributions of the LPPVK motif of the iron–sulfur template protein IscU to interactions with the Hsc66-Hsc20 chaperone system. J Biol Chem 278:37582–37589CrossRefGoogle Scholar
  48. Ikeuchi Y, Shigi N, Kato J, Nishimura A, Suzuki T (2006) Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol Cell 21:97–108CrossRefGoogle Scholar
  49. Jacobson MR, Cash VL, Weiss MC, Laird NF, Newton WE, Dean DR (1989) Biochemical and genetic analysis of the nifUSVWZM cluster from Azotobacter vinelandii. Mol Gen Genet 219:49–57CrossRefGoogle Scholar
  50. Jameson GN, Cosper MM, Hernández HL, Johnson MK, Huynh BH (2004) Role of the [2Fe–2S] cluster in recombinant Escherichia coli biotin synthase. Biochemistry 43:2022–2031CrossRefGoogle Scholar
  51. Jang S, Imlay JA (2010) Hydrogen peroxide inactivates the Escherichia coli Isc iron–sulphur assembly system, and OxyR induces the Suf system to compensate. Mol Microbiol 78:1448–1467CrossRefGoogle Scholar
  52. Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron–sulfur clusters. Annu Rev Biochem 74:247–281CrossRefGoogle Scholar
  53. Johnson DC, Unciuleac MC, Dean DR (2006) Controlled expression and functional analysis of iron–sulfur cluster biosynthetic components within Azotobacter vinelandii. J Bacteriol 188:7551–7561CrossRefGoogle Scholar
  54. Kaiser JT, Clausen T, Bourenkow GP, Bartunik HD, Steinbacher S, Huber R (2000) Crystal structure of a NifS-like protein from Thermotoga maritima: implications for iron sulphur cluster assembly. J Mol Biol 297:451–464CrossRefGoogle Scholar
  55. Kakuta Y, Horio T, Takahashi Y, Fukuyama K (2001) Crystal structure of Escherichia coli Fdx, an adrenodoxin-type ferredoxin involved in the assembly of iron–sulfur clusters. Biochemistry 40:11007–11012CrossRefGoogle Scholar
  56. Kambampati R, Lauhon CT (2000) Evidence for the transfer of sulfane sulfur from IscS to ThiI during the in vitro biosynthesis of 4-thiouridine in Escherichia coli tRNA. J Biol Chem 275:10727–10730CrossRefGoogle Scholar
  57. Kambampati R, Lauhon CT (2003) MnmA and IscS are required for in vitro 2-thiouridine biosynthesis in Escherichia coli. Biochemistry 42:1109–1117CrossRefGoogle Scholar
  58. Kato S, Mihara H, Kurihara T, Yoshimura T, Esaki N (2000) Gene cloning, purification, and characterization of two cyanobacterial NifS homologs driving iron–sulfur cluster formation. Biosci Biotechnol Biochem 64:2412–2419CrossRefGoogle Scholar
  59. Kato S, Mihara H, Kurihara T, Takahashi Y, Tokumoto U, Yoshimura T, Esaki N (2002) Cys-328 of IscS and Cys-63 of IscU are the sites of disulfide bridge formation in a covalently bound IscS/IscU complex: implications for the mechanism of iron–sulfur cluster assembly. Proc Natl Acad Sci USA 99:5948–5952CrossRefGoogle Scholar
  60. Kim JH, Füzéry AK, Tonelli M, Ta DT, Westler WM, Vickery LE, Markley JL (2009) Structure and dynamics of the iron-sulfur cluster assembly scaffold protein IscU and its interaction with the cochaperone HscB. Biochemistry 48:6062–6071CrossRefGoogle Scholar
  61. Kirby J, Wright F, Flint HJ (1998) A cysteine desulphurase gene from the cellulolytic rumen anaerobe Ruminococcus flavefaciens. Biochim Biophys Acta 1386:233–237CrossRefGoogle Scholar
  62. Kessler D, Papenbrock J (2005) Iron–sulfur cluster biosynthesis in photosynthetic organisms. Photosynth Res 86:391–407CrossRefGoogle Scholar
  63. Kitaoka S, Wada K, Hasegawa Y, Minami Y, Fukuyama K, Takahashi Y (2006) Crystal structure of Escherichia coli SufC, an ABC-type ATPase component of the SUF iron–sulfur cluster assembly machinery. FEBS Lett 580:137–143CrossRefGoogle Scholar
  64. Kolman C, Söll D (1993) SPL1-1, a Saccharomyces cerevisiae mutation affecting tRNA splicing. J Bacteriol 175:1433–1442Google Scholar
  65. Kramer GF, Baker JC, Ames BN (1988) Near-UV stress in Salmonella typhimurium: 4-thiouridine in tRNA, ppGpp, and ApppGpp as components of an adaptive response. J Bacteriol 170:2344–2351Google Scholar
  66. Krebs C, Agar JN, Smith AD, Frazzon J, Dean DR, Huynh BH, Johnson MK (2001) IscA, an alternate scaffold for Fe–S cluster biosynthesis. Biochemistry 40:14069–14080CrossRefGoogle Scholar
  67. Kriek M, Martins F, Challand MR, Croft A, Roach PL (2007a) Thiamine biosynthesis in Escherichia coli: identification of the intermediate and by-product derived from tyrosine. Angew Chem Int Ed Engl 46:9223–9226CrossRefGoogle Scholar
  68. Kriek M, Martins F, Leonardi R, Fairhurst SA, Lowe DJ, Roach PL (2007b) Thiazole synthase from Escherichia coli: an investigation of the substrates and purified proteins required for activity in vitro. J Biol Chem 282:17413–17423CrossRefGoogle Scholar
  69. Kurihara T, Mihara H, Kato S, Yoshimura T, Esaki N (2003) Assembly of iron–sulfur clusters mediated by cysteine desulfurases, IscS, CsdB and CSD, from Escherichia coli. Biochim Biophys Acta 1647:303–309Google Scholar
  70. Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Van Montagu M (2001) A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100CrossRefGoogle Scholar
  71. Land T, Rouault TA (1998) Targeting of a human iron–sulfur cluster assembly enzyme, nifs, to different subcellular compartments is regulated through alternative AUG utilization. Mol Cell 2:807–815CrossRefGoogle Scholar
  72. Lauhon CT, Kambampati R (2000) The iscS gene in Escherichia coli is required for the biosynthesis of 4-thiouridine, thiamin, and NAD. J Biol Chem 275:20096–20103CrossRefGoogle Scholar
  73. Layer G, Ollagnier-de Choudens S, Sanakis Y, 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 281:16256–16263CrossRefGoogle Scholar
  74. Layer G, Gaddam SA, Ayala-Castro CN, Ollagnier-de Choudens S, Lascoux D, Fontecave M, Outten FW (2007) SufE transfers sulfur from SufS to SufB for iron–sulfur cluster assembly. J Biol Chem 282:13342–13350CrossRefGoogle Scholar
  75. Lee JH, Yeo WS, Roe JH (2004) Induction of the sufA operon encoding Fe–S assembly proteins by superoxide generators and hydrogen peroxide: involvement of OxyR, IHF and an unidentified oxidant-responsive factor. Mol Microbiol 51:1745–1755CrossRefGoogle Scholar
  76. Lee KC, Yeo WS, Roe JH (2008) Oxidant-responsive induction of the suf operon, encoding a Fe–S assembly system, through Fur and IscR in Escherichia coli. J Bacteriol 190:8244–8247CrossRefGoogle Scholar
  77. Leimkühler S, Rajagopalan KV (2001) A sulfurtransferase is required in the transfer of cysteine sulfur in the in vitro synthesis of molybdopterin from precursor Z in Escherichia coli. J Biol Chem 276:22024–22031CrossRefGoogle Scholar
  78. Léon S, Touraine B, Briat JF, Lobréaux S (2002) The AtNFS2 gene from Arabidopsis thaliana encodes a NifS-like plastidial cysteine desulphurase. Biochem J 366:557–564CrossRefGoogle Scholar
  79. Leonardi R, Roach PL (2004) Thiamine biosynthesis in Escherichia coli: in vitro reconstitution of the thiazole synthase activity. J Biol Chem 279:17054–17062CrossRefGoogle Scholar
  80. Leong-Morgenthaler P, Oliver SG, Hottinger H, Söll D (1994) A Lactobacillus nifS-like gene suppresses an Escherichia coli transaminase B mutation. Biochimie 76:45–49CrossRefGoogle Scholar
  81. Li K, Tong WH, Hughes RM, Rouault TA (2006) Roles of the mammalian cytosolic cysteine desulfurase, ISCS, and scaffold protein, ISCU, in iron–sulfur cluster assembly. J Biol Chem 281:12344–12351CrossRefGoogle Scholar
  82. Lill R, Mühlenhoff U (2008) Maturation of iron–sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77:669–700CrossRefGoogle Scholar
  83. Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831–838CrossRefGoogle Scholar
  84. Loiseau L, Ollagnier-de Choudens S, Lascoux D, Forest E, Fontecave M, Barras F (2005) Analysis of the heteromeric CsdA–CsdE cysteine desulfurase, assisting Fe–S cluster biogenesis in Escherichia coli. J Biol Chem 280:26760–26769CrossRefGoogle Scholar
  85. Loiseau L, Gerez C, Bekker M, Ollagnier-de Choudens S, Py B, Sanakis Y, Teixeira de Mattos J, Fontecave M, Barras F (2007) ErpA, an iron sulfur (Fe S) protein of the A-type essential for respiratory metabolism in Escherichia coli. Proc Natl Acad Sci USA 104:13626–13631CrossRefGoogle Scholar
  86. Marelja Z, Stöcklein W, Nimtz M, Leimkühler S (2008) A novel role for human Nfs1 in the cytoplasm: Nfs1 acts as a sulfur donor for MOCS3, a protein involved in molybdenum cofactor biosynthesis. J Biol Chem 283:25178–25185CrossRefGoogle Scholar
  87. Mendel RR, Bittner F (2006) Cell biology of molybdenum. Biochim Biophys Acta 1763:621–635CrossRefGoogle Scholar
  88. Mihara H, Kurihara T, Yoshimura T, Soda K, Esaki N (1997) Cysteine sulfinate desulfinase, a NIFS-like protein of Escherichia coli with selenocysteine lyase and cysteine desulfurase activities. Gene cloning, purification, and characterization of a novel pyridoxal enzyme. J Biol Chem 272:22417–22424CrossRefGoogle Scholar
  89. Mihara H, Maeda M, Fujii T, Kurihara T, Hata Y, Esaki N (1999) A nifS-like gene, csdB, encodes an Escherichia coli counterpart of mammalian selenocysteine lyase. Gene cloning, purification, characterization and preliminary x-ray crystallographic studies. J Biol Chem 274:14768–14772CrossRefGoogle Scholar
  90. Mihara H, Kurihara T, Yoshimura T, Esaki N (2000a) Kinetic and mutational studies of three NifS homologs from Escherichia coli: mechanistic difference between L-cysteine desulfurase and L-selenocysteine lyase reactions. J Biochem 127:559–567Google Scholar
  91. Mihara H, Kurihara T, Watanabe T, Yoshimura T, Esaki N (2000b) cDNA cloning, purification, and characterization of mouse liver selenocysteine lyase. Candidate for selenium delivery protein in selenoprotein synthesis. J Biol Chem 275:6195–6200CrossRefGoogle Scholar
  92. Mihara H, Esaki N (2002) Bacterial cysteine desulfurases: their function and mechanisms. Appl Microbiol Biotechnol 60:12–23CrossRefGoogle Scholar
  93. Mihara H, Fujii T, Kato S, Kurihara T, Hata Y, Esaki N (2002) Structure of external aldimine of Escherichia coli CsdB, an IscS/NifS homolog: implications for its specificity toward selenocysteine. J Biochem 131:679–685Google Scholar
  94. Morimoto K, Yamashita E, Kondou Y, Lee SJ, Arisaka F, Tsukihara T, Nakai M (2006) The asymmetric IscA homodimer with an exposed [2Fe–2S] cluster suggests the structural basis of the Fe–S cluster biosynthetic scaffold. J Mol Biol 360:117–132CrossRefGoogle Scholar
  95. Mueller EG, Palenchar PM, Buck CJ (2001) The role of the cysteine residues of ThiI in the generation of 4-thiouridine in tRNA. J Biol Chem 276:33588–33595CrossRefGoogle Scholar
  96. Mueller EG (2006) Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nat Chem Biol 2:185–194CrossRefGoogle Scholar
  97. Mühlenhoff U, Balk J, Richhardt N, Kaiser JT, Sipos K, Kispal G, Lill R (2004) Functional characterization of the eukaryotic cysteine desulfurase Nfs1p from Saccharomyces cerevisiae. J Biol Chem 279:36906–36915CrossRefGoogle Scholar
  98. Mulligan ME, Haselkorn R (1989) Nitrogen fixation (nif) genes of the cyanobacterium Anabaena species strain PCC 7120. The nifB-fdxN-nifS-nifU operon. J Biol Chem 264:19200–19207Google Scholar
  99. Naamati A, Regev-Rudzki N, Galperin S, Lill R, Pines O (2009) Dual targeting of Nfs1 and discovery of its novel processing enzyme, Icp55. J Biol Chem 284:30200–30208CrossRefGoogle Scholar
  100. Nakai Y, Nakai M, Lill R, Suzuki T, Hayashi H (2007) Thio modification of yeast cytosolic tRNA is an iron–sulfur protein-dependent pathway. Mol Cell Biol 27:2841–2847CrossRefGoogle Scholar
  101. Nakai Y, Nakai M, Hayashi H (2008) Thio-modification of yeast cytosolic tRNA requires a ubiquitin-related system that resembles bacterial sulfur transfer systems. J Biol Chem 283:27469–27476CrossRefGoogle Scholar
  102. Nakamura M, Saeki K, Takahashi Y (1999) Hyperproduction of recombinant ferredoxins in Escherichia coli by coexpression of the ORF1-ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster. J Biochem 126:10–18Google Scholar
  103. Neumann M, Stöcklein W, Walburger A, Magalon A, Leimkühler S (2007) Identification of a Rhodobacter capsulatus L-cysteine desulfurase that sulfurates the molybdenum cofactor when bound to XdhC and before its insertion into xanthine dehydrogenase. Biochemistry 46:9586–9595CrossRefGoogle Scholar
  104. Numata T, Fukai S, Ikeuchi Y, Suzuki T, Nureki O (2006a) Structural basis for sulfur relay to RNA mediated by heterohexameric TusBCD complex. Structure 14:357–366CrossRefGoogle Scholar
  105. Numata T, Ikeuchi Y, Fukai S, Suzuki T, Nureki O (2006b) Snapshots of tRNA sulphuration via an adenylated intermediate. Nature 442:419–424CrossRefGoogle Scholar
  106. Ollagnier-de-Choudens S, Sanakis Y, Fontecave M (2004) SufA/IscA: reactivity studies of a class of scaffold proteins involved in [Fe–S] cluster assembly. J Biol Inorg Chem 9:828–838CrossRefGoogle Scholar
  107. Olson JW, Agar JN, Johnson MK, Maier RJ (2000) Characterization of the NifU and NifS Fe–S cluster formation proteins essential for viability in Helicobacter pylori. Biochemistry 39:16213–16219CrossRefGoogle Scholar
  108. Omi R, Kurokawa S, Mihara H, Hayashi H, Goto M, Miyahara I, Kurihara T, Hirotsu K, Esaki N (2010) Reaction mechanism and molecular basis for selenium/sulfur discrimination of selenocysteine lyase. J Biol Chem 285:12133–12139CrossRefGoogle Scholar
  109. Outten FW, Wood MJ, Muñoz FM, Storz G (2003) The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe-S cluster assembly in Escherichia coli. J Biol Chem 278:45713–45719CrossRefGoogle Scholar
  110. Outten FW, Djaman O, Storz G (2004) A suf operon requirement for Fe–S cluster assembly during iron starvation in Escherichia coli. Mol Microbiol 52:861–872CrossRefGoogle Scholar
  111. Palenchar PM, Buck CJ, Cheng H, Larson TJ, Mueller EG (2000) Evidence that ThiI, an enzyme shared between thiamin and 4-thiouridine biosynthesis, may be a sulfurtransferase that proceeds through a persulfide intermediate. J Biol Chem 275:8283–8286CrossRefGoogle Scholar
  112. Pastore C, Adinolfi S, Huynen MA, Rybin V, Martin S, Mayer M, Bukau B, Pastore A (2006) YfhJ, a molecular adaptor in iron–sulfur cluster formation or a frataxin-like protein? Structure 14:857–867CrossRefGoogle Scholar
  113. Patzer SI, Hantke K (1999) SufS is a NifS-like protein, and SufD is necessary for stability of the [2Fe–2S] FhuF protein in Escherichia coli. J Bacteriol 181:3307–3309Google Scholar
  114. Petrovic A, Davis CT, Rangachari K, Clough B, Wilson RJ, Eccleston JF (2008) Hydrodynamic characterization of the SufBC and SufCD complexes and their interaction with fluorescent adenosine nucleotides. Protein Sci 17:1264–1274CrossRefGoogle Scholar
  115. Pierrel F, Björk GR, Fontecave M, Atta M (2002) Enzymatic modification of tRNAs: MiaB is an iron–sulfur protein. J Biol Chem 277:13367–13370CrossRefGoogle Scholar
  116. Pierrel F, Douki T, Fontecave M, Atta M (2004) MiaB protein is a bifunctional radical-S-adenosylmethionine enzyme involved in thiolation and methylation of tRNA. J Biol Chem 279:47555–47563CrossRefGoogle Scholar
  117. Pilon-Smits EA, Garifullina GF, Abdel-Ghany S, Kato S, Mihara H, Hale KL, Burkhead JL, Esaki N, Kurihara T, Pilon M (2002) Characterization of a NifS-like chloroplast protein from Arabidopsis. Implications for its role in sulfur and selenium metabolism. Plant Physiol 130:1309–1318CrossRefGoogle Scholar
  118. Pohl M, Sprenger GA, Müller M (2004) A new perspective on thiamine catalysis. Curr Opin Biotechnol 15:335–342CrossRefGoogle Scholar
  119. Py B, Barras F (2010) Building Fe–S proteins: bacterial strategies. Nat Rev Microbiol 8:436–446CrossRefGoogle Scholar
  120. Raulfs EC, O'Carroll IP, Dos Santos PC, Unciuleac MC, Dean DR (2008) In vivo iron–sulfur cluster formation. Proc Natl Acad Sci USA 105:8591–8596CrossRefGoogle Scholar
  121. Rees DC (2002) Great metalloclusters in enzymology. Annu Rev Biochem 71:221–246CrossRefGoogle Scholar
  122. Reyda MR, Dippold R, Dotson ME, Jarrett JT (2008) Loss of iron–sulfur clusters from biotin synthase as a result of catalysis promotes unfolding and degradation. Arch Biochem Biophys 471:32–41CrossRefGoogle Scholar
  123. Reyda MR, Fugate CJ, Jarrett JT (2009) A complex between biotin synthase and the iron–sulfur cluster assembly chaperone HscA that enhances in vivo cluster assembly. Biochemistry 48:10782–10792CrossRefGoogle Scholar
  124. Rudolph MJ, Wuebbens MM, Rajagopalan KV, Schindelin H (2001) Crystal structure of molybdopterin synthase and its evolutionary relationship to ubiquitin activation. Nat Struct Biol 8:42–46CrossRefGoogle Scholar
  125. Ruiz M, Bettache A, Janicki A, Vinella D, Zhang CC, Latifi A (2010) The alr2505 (osiS) gene from Anabaena sp. strain PCC7120 encodes a cysteine desulfurase induced by oxidative stress. FEBS J 277:3715–3725CrossRefGoogle Scholar
  126. Schilke B, Voisine C, Beinert H, Craig E (1999) Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 96:10206–10211CrossRefGoogle Scholar
  127. Schwartz CJ, Djaman O, Imlay JA, Kiley PJ (2000) The cysteine desulfurase, IscS, has a major role in in vivo Fe–S cluster formation in Escherichia coli. Proc Natl Acad Sci USA 97:9009–9014CrossRefGoogle Scholar
  128. Schwartz CJ, Giel JL, Patschkowski T, Luther C, Ruzicka FJ, Beinert H, Kiley PJ (2001) 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 98:14895–14900CrossRefGoogle Scholar
  129. Schwarz G, Mendel RR (2006) Molybdenum cofactor biosynthesis and molybdenum enzymes. Annu Rev Plant Biol 57:623–647CrossRefGoogle Scholar
  130. Selbach B, Earles E, Dos Santos PC (2010) Kinetic analysis of the bisubstrate cysteine desulfurase SufS from Bacillus subtilis. Biochemistry 49:8794–8802CrossRefGoogle Scholar
  131. Shi R, Proteau A, Villarroya M, Moukadiri I, Zhang L, Trempe JF, Matte A, Armengod ME, Cygler M (2010) Structural basis for Fe–S cluster assembly and tRNA thiolation mediated by IscS protein–protein interactions. PLoS Biol 8:e1000354CrossRefGoogle Scholar
  132. Shimomura Y, Takahashi Y, Kakuta Y, Fukuyama K (2005) Crystal structure of Escherichia coli YfhJ protein, a member of the ISC machinery involved in assembly of iron–sulfur clusters. Proteins 60:566–569CrossRefGoogle Scholar
  133. Silberg JJ, Tapley TL, Hoff KG, Vickery LE (2004) Regulation of the HscA ATPase reaction cycle by the co-chaperone HscB and the iron–sulfur cluster assembly protein IscU. J Biol Chem 279:53924–53931CrossRefGoogle Scholar
  134. Smith AD, Agar JN, Johnson KA, Frazzon J, Amster IJ, Dean DR, Johnson MK (2001) Sulfur transfer from IscS to IscU: the first step in iron–sulfur cluster biosynthesis. J Am Chem Soc 123:11103–11104CrossRefGoogle Scholar
  135. Smith AD, Frazzon J, Dean DR, Johnson MK (2005a) Role of conserved cysteines in mediating sulfur transfer from IscS to IscU. FEBS Lett 579:5236–5240CrossRefGoogle Scholar
  136. Smith AD, Jameson GN, Dos Santos PC, Agar JN, Naik S, Krebs C, Frazzon J, Dean DR, Huynh BH, Johnson MK (2005b) NifS-mediated assembly of [4Fe–4S] clusters in the N- and C-terminal domains of the NifU scaffold protein. Biochemistry 44:12955–12969CrossRefGoogle Scholar
  137. Sullivan MA, Cannon JF, Webb FH, Bock RM (1985) Antisuppressor mutation in Escherichia coli defective in biosynthesis of 5-methylaminomethyl-2-thiouridine. J Bacteriol 161:368–376Google Scholar
  138. Sun D, Setlow P (1993) Cloning, nucleotide sequence, and regulation of the Bacillus subtilis nadB gene and a nifS-like gene, both of which are essential for NAD biosynthesis. J Bacteriol 175:1423–1432Google Scholar
  139. Takahashi Y, Nakamura M (1999) Functional assignment of the ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster involved in the assembly of Fe-S clusters in Escherichia coli. J Biochem 126:917–926Google Scholar
  140. Takahashi Y, Tokumoto U (2002) A third bacterial system for the assembly of iron–sulfur clusters with homologs in archaea and plastids. J Biol Chem 277:28380–28383CrossRefGoogle Scholar
  141. Tan G, Lu J, Bitoun JP, Huang H, Ding H (2009) IscA/SufA paralogues are required for the [4Fe–4S] cluster assembly in enzymes of multiple physiological pathways in Escherichia coli under aerobic growth conditions. Biochem J 420:463–472CrossRefGoogle Scholar
  142. Tapley TL, Vickery LE (2004) Preferential substrate binding orientation by the molecular chaperone HscA. J Biol Chem 279:28435–28442CrossRefGoogle Scholar
  143. Taylor SV, Kelleher NL, Kinsland C, Chiu HJ, Costello CA, Backstrom AD, McLafferty FW, Begley TP (1998) Thiamin biosynthesis in Escherichia coli. Identification of ThiS thiocarboxylate as the immediate sulfur donor in the thiazole formation. J Biol Chem 273:16555–16560CrossRefGoogle Scholar
  144. Thomas G, Favre A (1975) 4-Thiouridine as the target for near-ultraviolet light induced growth delay in Escherichia coli. Biochem Biophys Res Commun 66:1454–1461CrossRefGoogle Scholar
  145. Tirupati B, Vey JL, Drennan CL, Bollinger JM Jr (2004) Kinetic and structural characterization of Slr0077/SufS, the essential cysteine desulfurase from Synechocystis sp. PCC 6803. Biochemistry 43:12210–12219CrossRefGoogle Scholar
  146. Tokumoto U, Takahashi Y (2001) Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron–sulfur proteins. J Biochem 130:63–71Google Scholar
  147. Tokumoto U, Kitamura S, Fukuyama K, Takahashi Y (2004) Interchangeability and distinct properties of bacterial Fe–S cluster assembly systems: functional replacement of the isc and suf operons in Escherichia coli with the nifSU-like operon from Helicobacter pylori. J Biochem 136:199–209CrossRefGoogle Scholar
  148. Trotter V, Vinella D, Loiseau L, Ollagnier de Choudens S, Fontecave M, Barras F (2009) The CsdA cysteine desulphurase promotes Fe/S biogenesis by recruiting Suf components and participates to a new sulphur transfer pathway by recruiting CsdL (ex-YgdL), a ubiquitin-modifying-like protein. Mol Microbiol 74:1527–1542CrossRefGoogle Scholar
  149. Unciuleac MC, Chandramouli K, Naik S, Mayer S, Huynh BH, Johnson MK, Dean DR (2007) In vitro activation of apo-aconitase using a [4Fe–4S] cluster-loaded form of the IscU [Fe–S] cluster scaffolding protein. Biochemistry 46:6812–6821CrossRefGoogle Scholar
  150. Urbina HD, Silberg JJ, Hoff KG, Vickery LE (2001) Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J Biol Chem 276:44521–44526CrossRefGoogle Scholar
  151. Urbonavicius J, Qian Q, Durand JM, Hagervall TG, Björk GR (2001) Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J 20:4863–4873CrossRefGoogle Scholar
  152. Van Hoewyk D, Abdel-Ghany SE, Cohu CM, Herbert SK, Kugrens P, Pilon M, Pilon-Smits EA (2007) Chloroplast iron-sulfur cluster protein maturation requires the essential cysteine desulfurase CpNifS. Proc Natl Acad Sci U S A 104:5686–5691CrossRefGoogle Scholar
  153. Vickery LE, Cupp-Vickery JR (2007) Molecular chaperones HscA/Ssq1 and HscB/Jac1 and their roles in iron–sulfur protein maturation. Crit Rev Biochem Mol Biol 42:95–111CrossRefGoogle Scholar
  154. Vinella D, Brochier-Armanet C, Loiseau L, Talla E, Barras F (2009) Iron–sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers. PLoS Genet 5:e1000497CrossRefGoogle Scholar
  155. Wang W, Huang H, Tan G, Si F, Liu M, Landry AP, Lu J, Ding H (2010) In vivo evidence for the iron-binding activity of an iron–sulfur cluster assembly protein IscA in Escherichia coli. Biochem J 432:429–436CrossRefGoogle Scholar
  156. Waterman DG, Ortiz-Lombardia M, Fogg MJ, Koonin EV, Antson AA (2006) Crystal structure of Bacillus anthracis ThiI, a tRNA-modifying enzyme containing the predicted RNA-binding THUMP domain. J Mol Biol 356:97–110CrossRefGoogle Scholar
  157. Webb E, Claas K, Downs DM (1997) Characterization of thiI, a new gene involved in thiazole biosynthesis in Salmonella typhimurium. J Bacteriol 179:4399–4402Google Scholar
  158. Wollers S, Layer G, Garcia-Serres R, Signor L, Clemancey M, Latour JM, Fontecave M, Ollagnier de Choudens S (2010) Iron–sulfur (Fe–S) cluster assembly: the SufBCD complex is a new type of Fe–S scaffold with a flavin redox cofactor. J Biol Chem 285:23331–23341CrossRefGoogle Scholar
  159. Wuebbens MM, Rajagopalan KV (2003) Mechanistic and mutational studies of Escherichia coli molybdopterin synthase clarify the final step of molybdopterin biosynthesis. J Biol Chem 278:14523–14532CrossRefGoogle Scholar
  160. Xi J, Ge Y, Kinsland C, McLafferty FW, Begley TP (2001) Biosynthesis of the thiazole moiety of thiamin in Escherichia coli: identification of an acyldisulfide-linked protein-protein conjugate that is functionally analogous to the ubiquitin/E1 complex. Proc Natl Acad Sci USA 98:8513–8518CrossRefGoogle Scholar
  161. Yang J, Bitoun JP, Ding H (2006) Interplay of IscA and IscU in biogenesis of iron–sulfur clusters. J Biol Chem 281:27956–27963CrossRefGoogle Scholar
  162. Yeo WS, Lee JH, Lee KC, Roe JH (2006) IscR acts as an activator in response to oxidative stress for the suf operon encoding Fe–S assembly proteins. Mol Microbiol 61:206–218CrossRefGoogle Scholar
  163. Zafrilla B, Martínez-Espinosa RM, Esclapez J, Pérez-Pomares F, Bonete MJ (2010) SufS protein from Haloferax volcanii involved in Fe–S cluster assembly in haloarchaea. Biochim Biophys Acta 1804:1476–1482Google Scholar
  164. Zhang W, Urban A, Mihara H, Leimkühler S, Kurihara T, Esaki N (2010) IscS functions as a primary sulfur-donating enzyme by interacting specifically with MoeB and MoaD in the biosynthesis of molybdopterin in Escherichia coli. J Biol Chem 285:2302–2308CrossRefGoogle Scholar
  165. Zheng L, White RH, Cash VL, Jack RF, Dean DR (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc Natl Acad Sci USA 90:2754–2758CrossRefGoogle Scholar
  166. Zheng L, White RH, Cash VL, Dean DR (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33:4714–4720CrossRefGoogle Scholar
  167. Zheng L, Cash VL, Flint DH, Dean DR (1998) Assembly of iron–sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273:13264–13272CrossRefGoogle Scholar

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© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Institute for Chemical ResearchKyoto UniversityUjiJapan
  2. 2.Department of Biotechnology, Institute of Science and Engineering, College of Life SciencesRitsumeikan UniversityKusatsuJapan

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