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Annual Review of Microbiology

Volume 69, 2015

How Is Fe-S Cluster Formation Regulated?

Abstract

Iron-sulfur (Fe-S) clusters are fundamental to numerous biological processes in most organisms, but these protein cofactors can be prone to damage by various oxidants (e.g., O, reactive oxygen species, and reactive nitrogen species) and toxic levels of certain metals (e.g., cobalt and copper). Furthermore, their synthesis can also be directly influenced by the level of available iron in the environment. Consequently, the cellular need for Fe-S cluster biogenesis varies with fluctuating growth conditions. To accommodate changes in Fe-S demand, microorganisms employ diverse regulatory strategies to tailor Fe-S cluster biogenesis according to their surroundings. Here, we review the mechanisms that regulate Fe-S cluster formation in bacteria, primarily focusing on control of the Isc and Suf Fe-S cluster biogenesis systems in the model bacterium .

Keyword(s): Fe-S, homeostasis, iron-sulfur cluster, Isc pathway, regulation, Suf pathway
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2015-10-15
2024-05-23
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Literature Cited

  1. Adinolfi S, Iannuzzi C, Prischi F, Pastore C, Iametti S. 1.  et al. 2009. Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS. Nat. Struct. Mol. Biol. 16:390–96 [Google Scholar]
  2. Andrew AJ, Song JY, Schilke B, Craig EA. 2.  2008. Posttranslational regulation of the scaffold for Fe-S cluster biogenesis, Isu. Mol. Biol. Cell 19:5259–66 [Google Scholar]
  3. Angelini S, Gerez C, Ollagnier-de Choudens S, Sanakis Y, Fontecave M. 3.  et al. 2008. NfuA, a new factor required for maturing Fe/S proteins in Escherichia coli under oxidative stress and iron starvation conditions. J. Biol. Chem. 283:14084–91 [Google Scholar]
  4. Arifuzzaman M, Maeda M, Itoh A, Nishikata K, Takita C. 4.  et al. 2006. Large-scale identification of protein-protein interaction of Escherichia coli K-12. Genome Res. 16:686–91 [Google Scholar]
  5. Babu M, Arnold R, Bundalovic-Torma C, Gagarinova A, Wong KS. 5.  et al. 2014. Quantitative genome-wide genetic interaction screens reveal global epistatic relationships of protein complexes in Escherichia coli. PLOS Genet. 10:e1004120 [Google Scholar]
  6. Beinert H. 6.  2000. Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5:2–15 [Google Scholar]
  7. Bhubhanil S, Niamyim P, Sukchawalit R, Mongkolsuk S. 7.  2014. Cysteine desulphurase-encoding gene sufS2 is required for the repressor function of RirA and oxidative resistance in Agrobacterium tumefaciens. Microbiology 160:79–90 [Google Scholar]
  8. Bitoun JP, Wu G, Ding H. 8.  2008. Escherichia coli FtnA acts as an iron buffer for re-assembly of iron-sulfur clusters in response to hydrogen peroxide stress. Biometals 21:693–703 [Google Scholar]
  9. Blanc B, Clemancey M, Latour JM, Fontecave M, Ollagnier de Choudens S. 9.  2014. Molecular investigation of iron-sulfur cluster assembly scaffolds under stress. Biochemistry 53:7867–69 [Google Scholar]
  10. Blanc B, Gerez C, Ollagnier de Choudens S. 10.  2015. Assembly of Fe/S proteins in bacterial systems: biochemistry of the bacterial ISC system. Biochim. Biophys. Acta 1853:1436–47 [Google Scholar]
  11. Blanchard JL, Wholey WY, Conlon EM, Pomposiello PJ. 11.  2007. Rapid changes in gene expression dynamics in response to superoxide reveal SoxRS-dependent and independent transcriptional networks. PLOS ONE 2:e1186 [Google Scholar]
  12. Bodenmiller DM, Spiro S. 12.  2006. The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J. Bacteriol. 188:874–81 [Google Scholar]
  13. Bou-Abdallah F, Adinolfi S, Pastore A, Laue TM, Dennis Chasteen N. 13.  2004. Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli. J. Mol. Biol. 341:605–15 [Google Scholar]
  14. Boutigny S, Saini A, Baidoo EE, Yeung N, Keasling JD, Butland G. 14.  2013. Physical and functional interactions of a monothiol glutaredoxin and an iron sulfur cluster carrier protein with the sulfur-donating radical S-adenosyl-l-methionine enzyme MiaB. J. Biol. Chem. 288:14200–11 [Google Scholar]
  15. Boyd ES, Thomas KM, Dai Y, Boyd JM, Outten FW. 15.  2014. Interplay between oxygen and Fe-S cluster biogenesis: insights from the Suf pathway. Biochemistry 53:5834–47 [Google Scholar]
  16. Boyd JM, Lewis JA, Escalante-Semerena JC, Downs DM. 16.  2008. Salmonella enterica requires ApbC function for growth on tricarballylate: evidence of functional redundancy between ApbC and IscU. J. Bacteriol. 190:4596–602 [Google Scholar]
  17. Boyd JM, Pierik AJ, Netz DJ, Lill R, Downs DM. 17.  2008. Bacterial ApbC can bind and effectively transfer iron-sulfur clusters. Biochemistry 47:8195–202 [Google Scholar]
  18. Boyd JM, Sondelski JL, Downs DM. 18.  2009. Bacterial ApbC protein has two biochemical activities that are required for in vivo function. J. Biol. Chem. 284:110–18 [Google Scholar]
  19. Bridwell-Rabb J, Fox NG, Tsai C, Winn AM, Barondeau DP. 19.  2014. Human frataxin activates Fe-S cluster biosynthesis by facilitating sulfur transfer chemistry. Biochemistry 53:4904–13 [Google Scholar]
  20. Bridwell-Rabb J, Iannuzzi C, Pastore A, Barondeau DP. 20.  2012. Effector role reversal during evolution: the case of frataxin in Fe-S cluster biosynthesis. Biochemistry 51:2506–14 [Google Scholar]
  21. Butland G, Babu M, Diaz-Mejia JJ, Bohdana F, Phanse S. 21.  et al. 2008. eSGA: E. coli synthetic genetic array analysis. Nat. Methods 5:789–95 [Google Scholar]
  22. Butland G, Peregrin-Alvarez JM, Li J, Yang W, Yang X. 22.  et al. 2005. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433:531–37 [Google Scholar]
  23. Campuzano V, Montermini L, Molto MD, Pianese L, Cossee M. 23.  et al. 1996. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271:1423–27 [Google Scholar]
  24. Chamberlain S, Shaw J, Rowland A, Wallis J, South S. 24.  et al. 1988. Mapping of mutation causing Fried-reich's ataxia to human chromosome 9. Nature 334:248–50 [Google Scholar]
  25. Colin F, Martelli A, Clemancey M, Latour JM, Gambarelli S. 25.  et al. 2013. Mammalian frataxin controls sulfur production and iron entry during de novo Fe4S4 cluster assembly. J. Am. Chem. Soc. 135:733–40 [Google Scholar]
  26. Couturier J, Przybyla-Toscano J, Roret T, Didierjean C, Rouhier N. 26.  2015. The roles of glutaredoxins ligating Fe-S clusters: sensing, transfer or repair functions?. Biochim. Biophys. Acta 1853:1513–27 [Google Scholar]
  27. Crack JC, Green J, Thomson AJ, Le Brun NE. 27.  2014. Iron-sulfur clusters as biological sensors: the chemistry of reactions with molecular oxygen and nitric oxide. Acc. Chem. Res. 47:3196–205 [Google Scholar]
  28. Crawford MJ, Goldberg DE. 28.  1998. Regulation of the Salmonella typhimurium flavohemoglobin gene. A new pathway for bacterial gene expression in response to nitric oxide. J. Biol. Chem. 273:34028–32 [Google Scholar]
  29. D'Autreaux B, Touati D, Bersch B, Latour JM, Michaud-Soret I. 29.  2002. Direct inhibition by nitric oxide of the transcriptional ferric uptake regulation protein via nitrosylation of the iron. PNAS 99:16619–24 [Google Scholar]
  30. Dahl JU, Urban A, Bolte A, Sriyabhaya P, Donahue JL. 30.  et al. 2011. The identification of a novel protein involved in molybdenum cofactor biosynthesis in Escherichia coli. J. Biol. Chem. 286:35801–12 [Google Scholar]
  31. Dai Y, Outten FW. 31.  2012. The E. coli SufS-SufE sulfur transfer system is more resistant to oxidative stress than IscS-IscU. FEBS Lett. 586:4016–22 [Google Scholar]
  32. Desnoyers G, Morissette A, Prevost K, Masse E. 32.  2009. Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J. 28:1551–61 [Google Scholar]
  33. Ding B, Smith ES, Ding H. 33.  2005. Mobilization of the iron centre in IscA for the iron-sulphur cluster assembly in IscU. Biochem. J. 389:797–802 [Google Scholar]
  34. Ding H, Clark RJ. 34.  2004. Characterization of iron binding in IscA, an ancient iron-sulphur cluster assembly protein. Biochem. J. 379:433–40 [Google Scholar]
  35. Ding H, Harrison K, Lu J. 35.  2005. Thioredoxin reductase system mediates iron binding in IscA and iron delivery for the iron-sulfur cluster assembly in IscU. J. Biol. Chem. 280:30432–37 [Google Scholar]
  36. Expert D, Boughammoura A, Franza T. 36.  2008. Siderophore-controlled iron assimilation in the enterobacterium Erwinia chrysanthemi: evidence for the involvement of bacterioferritin and the Suf iron-sulfur cluster assembly machinery. J. Biol. Chem. 283:36564–72 [Google Scholar]
  37. Ezraty B, Vergnes A, Banzhaf M, Duverger Y, Huguenot A. 37.  et al. 2013. Fe-S cluster biosynthesis controls uptake of aminoglycosides in a ROS-less death pathway. Science 340:1583–87 [Google Scholar]
  38. Fantino JR, Py B, Fontecave M, Barras F. 38.  2010. A genetic analysis of the response of Escherichia coli to cobalt stress. Environ. Microbiol. 12:2846–57 [Google Scholar]
  39. Fleischhacker AS, Stubna A, Hsueh KL, Guo Y, Teter SJ. 39.  et al. 2012. Characterization of the [2Fe-2S] cluster of Escherichia coli transcription factor IscR. Biochemistry 51:4453–62 [Google Scholar]
  40. Flynn JM, Neher SB, Kim YI, Sauer RT, Baker TA. 40.  2003. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell 11:671–83 [Google Scholar]
  41. Fontecave M. 41.  2006. Iron-sulfur clusters: ever-expanding roles. Nat. Chem. Biol. 2:171–74 [Google Scholar]
  42. Gardner PR, Fridovich I. 42.  1993. Effect of glutathione on aconitase in Escherichia coli. Arch. Biochem. Biophys. 301:98–102 [Google Scholar]
  43. Giel JL. 43.  2007. Role of IscR in regulation of iron-sulfur biogenesis in Escherichia coli: identification of the IscR regulon and mechanisms of autoregulation Ph.D. thesis. University of Wisconsin-Madison
  44. Giel JL, Nesbit AD, Mettert EL, Fleischhacker AS, Wanta BT, Kiley PJ. 44.  2013. Regulation of iron-sulphur cluster homeostasis through transcriptional control of the Isc pathway by [2Fe-2S]-IscR in Escherichia coli. Mol. Microbiol. 87:478–92 [Google Scholar]
  45. Giel JL, Rodionov D, Liu M, Blattner FR, Kiley PJ. 45.  2006. IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol. Microbiol. 60:1058–75 [Google Scholar]
  46. Gralnick J, Downs D. 46.  2001. Protection from superoxide damage associated with an increased level of the YggX protein in Salmonella enterica. PNAS 98:8030–35 [Google Scholar]
  47. Gu M, Imlay JA. 47.  2013. Superoxide poisons mononuclear iron enzymes by causing mismetallation. Mol. Microbiol. 89:123–34 [Google Scholar]
  48. Hidese R, Mihara H, Esaki N. 48.  2011. Bacterial cysteine desulfurases: versatile key players in biosynthetic pathways of sulfur-containing biofactors. Appl. Microbiol. Biotechnol. 91:47–61 [Google Scholar]
  49. Hidese R, Mihara H, Kurihara T, Esaki N. 49.  2014. Global identification of genes affecting iron-sulfur cluster biogenesis and iron homeostasis. J. Bacteriol. 196:1238–49 [Google Scholar]
  50. Hoff KG, Silberg JJ, Vickery LE. 50.  2000. Interaction of the iron-sulfur cluster assembly protein IscU with the Hsc66/Hsc20 molecular chaperone system of Escherichia coli. PNAS 97:7790–95 [Google Scholar]
  51. Huynen MA, Snel B, Bork P, Gibson TJ. 51.  2001. The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum. Mol. Genet. 10:2463–68 [Google Scholar]
  52. Iannuzzi C, Adinolfi S, Howes BD, Garcia-Serres R, Clemancey M. 52.  et al. 2011. The role of CyaY in iron sulfur cluster assembly on the E. coli IscU scaffold protein. PLOS ONE 6:e21992 [Google Scholar]
  53. Imlay JA. 53.  2006. Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol. 59:1073–82 [Google Scholar]
  54. Imlay JA. 54.  2008. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77:755–76 [Google Scholar]
  55. Imlay JA. 55.  2013. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11:443–54 [Google Scholar]
  56. Jang S, Imlay JA. 56.  2010. Hydrogen peroxide inactivates the Escherichia coli Isc iron-sulphur assembly system, and OxyR induces the Suf system to compensate. Mol. Microbiol. 78:1448–67 [Google Scholar]
  57. Justino MC, Almeida CC, Goncalves VL, Teixeira M, Saraiva LM. 57.  2006. Escherichia coli YtfE is a di-iron protein with an important function in assembly of iron-sulphur clusters. FEMS Microbiol. Lett. 257:278–84 [Google Scholar]
  58. Justino MC, Almeida CC, Teixeira M, Saraiva LM. 58.  2007. Escherichia coli di-iron YtfE protein is necessary for the repair of stress-damaged iron-sulfur clusters. J. Biol. Chem. 282:10352–59 [Google Scholar]
  59. Justino MC, Vicente JB, Teixeira M, Saraiva LM. 59.  2005. New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide. J. Biol. Chem. 280:2636–43 [Google Scholar]
  60. Keyer K, Imlay JA. 60.  1997. Inactivation of dehydratase [4Fe-4S] clusters and disruption of iron homeostasis upon cell exposure to peroxynitrite. J. Biol. Chem. 272:27652–59 [Google Scholar]
  61. Kiley PJ, Beinert H. 61.  2003. The role of Fe-S proteins in sensing and regulation in bacteria. Curr. Opin. Microbiol. 6:181–85 [Google Scholar]
  62. Kim JH, Bothe JR, Frederick RO, Holder JC, Markley JL. 62.  2014. Role of IscX in iron-sulfur cluster biogenesis in Escherichia coli. J. Am. Chem. Soc. 136:7933–42 [Google Scholar]
  63. Kim JH, Frederick RO, Reinen NM, Troupis AT, Markley JL. 63.  2013. [2Fe-2S]-ferredoxin binds directly to cysteine desulfurase and supplies an electron for iron-sulfur cluster assembly but is displaced by the scaffold protein or bacterial frataxin. J. Am. Chem. Soc. 135:8117–20 [Google Scholar]
  64. Layer G, Ollagnier-de Choudens S, Sanakis Y, Fontecave M. 64.  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. 281:16256–63 [Google Scholar]
  65. Lee J, Yeo W, Roe J. 65.  2003. Regulation of the sufABCDSE operon by Fur. J. Microbiol. 41:109–14 [Google Scholar]
  66. Lee JH, Yeo WS, Roe JH. 66.  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. 51:1745–55 [Google Scholar]
  67. Lee KC, Yeo WS, Roe JH. 67.  2008. Oxidant-responsive induction of the suf operon, encoding a Fe-S assembly system, through Fur and IscR in Escherichia coli. J. Bacteriol. 190:8244–47 [Google Scholar]
  68. Li DS, Ohshima K, Jiralerspong S, Bojanowski MW, Pandolfo M. 68.  1999. Knock-out of the cyaY gene in Escherichia coli does not affect cellular iron content and sensitivity to oxidants. FEBS Lett. 456:13–16 [Google Scholar]
  69. Li GW, Burkhardt D, Gross C, Weissman JS. 69.  2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:624–35 [Google Scholar]
  70. Loiseau L, Gerez C, Bekker M, Ollagnier-de Choudens S, Py B. 70.  et al. 2007. ErpA, an iron sulfur (Fe S) protein of the A-type essential for respiratory metabolism in Escherichia coli. PNAS 104:13626–31 [Google Scholar]
  71. Lu J, Yang J, Tan G, Ding H. 71.  2008. Complementary roles of SufA and IscA in the biogenesis of iron-sulfur clusters in Escherichia coli. Biochem. J. 409:535–43 [Google Scholar]
  72. Macomber L, Imlay JA. 72.  2009. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. PNAS 106:8344–49 [Google Scholar]
  73. Martinez-Argudo I, Little R, Shearer N, Johnson P, Dixon R. 73.  2005. Nitrogen fixation: key genetic regulatory mechanisms. Biochem. Soc. Trans. 33:152–56 [Google Scholar]
  74. Masse E, Gottesman S. 74.  2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. PNAS 99:4620–25 [Google Scholar]
  75. Maynard ND, Birch EW, Sanghvi JC, Chen L, Gutschow MV, Covert MW. 75.  2010. A forward-genetic screen and dynamic analysis of lambda phage host-dependencies reveals an extensive interaction network and a new anti-viral strategy. PLOS Genet. 6:e1001017 [Google Scholar]
  76. Maynard ND, Macklin DN, Kirkegaard K, Covert MW. 76.  2012. Competing pathways control host resistance to virus via tRNA modification and programmed ribosomal frameshifting. Mol. Syst. Biol. 8:567 [Google Scholar]
  77. Mettert EL, Kiley PJ. 77.  2014. Coordinate regulation of the Suf and Isc Fe-S cluster biogenesis pathways by IscR is essential for viability of Escherichia coli. J. Bacteriol. 196:4315–23 [Google Scholar]
  78. Mettert EL, Outten FW, Wanta B, Kiley PJ. 78.  2008. The impact of O2 on the Fe-S cluster biogenesis requirements of Escherichia coli FNR. J. Mol. Biol. 384:798–811 [Google Scholar]
  79. Mettert EL, Perna NT, Kiley PJ. 79.  2014. Sensing the cellular Fe-S cluster demand: a structural, functional, and phylogenetic overview of Escherichia coli IscR. Iron-Sulfur Clusters in Chemistry and Biology TA Rouault 326–45 Berlin: Walter de Gruyter GmbH [Google Scholar]
  80. Muhlenhoff U, Richhardt N, Ristow M, Kispal G, Lill R. 80.  2002. The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet. 11:2025–36 [Google Scholar]
  81. Nair M, Adinolfi S, Pastore C, Kelly G, Temussi P, Pastore A. 81.  2004. Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites. Structure 12:2037–48 [Google Scholar]
  82. Nesbit AD, Giel JL, Rose JC, Kiley PJ. 82.  2009. Sequence-specific binding to a subset of IscR-regulated promoters does not require IscR Fe-S cluster ligation. J. Mol. Biol. 387:28–41 [Google Scholar]
  83. Netz DJ, Mascarenhas J, Stehling O, Pierik AJ, Lill R. 83.  2014. Maturation of cytosolic and nuclear iron-sulfur proteins. Trends Cell Biol. 24:303–12 [Google Scholar]
  84. Nobre LS, Garcia-Serres R, Todorovic S, Hildebrandt P, Teixeira M. 84.  et al. 2014. Escherichia coli RIC is able to donate iron to iron-sulfur clusters. PLOS ONE 9:e95222 [Google Scholar]
  85. Outten FW. 85.  2015. Recent advances in the Suf Fe-S cluster biogenesis pathway: beyond the Proteobacteria. Biochim. Biophys. Acta 1853:1464–69 [Google Scholar]
  86. Outten FW, Djaman O, Storz G. 86.  2004. A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol. Microbiol. 52:861–72 [Google Scholar]
  87. Pandey A, Gordon DM, Pain J, Stemmler TL, Dancis A, Pain D. 87.  2013. Frataxin directly stimulates mitochondrial cysteine desulfurase by exposing substrate-binding sites, and a mutant Fe-S cluster scaffold protein with frataxin-bypassing ability acts similarly. J. Biol. Chem. 288:36773–86 [Google Scholar]
  88. Pandolfo M. 88.  1999. Molecular pathogenesis of Friedreich ataxia. Arch. Neurol. 56:1201–8 [Google Scholar]
  89. Pandolfo M, Pastore A. 89.  2009. The pathogenesis of Friedreich ataxia and the structure and function of frataxin. J. Neurol. 256:Suppl. 19–17 [Google Scholar]
  90. Parent A, Elduque X, Cornu D, Belot L, Le Caer JP. 90.  et al. 2015. Mammalian frataxin directly enhances sulfur transfer of NFS1 persulfide to both ISCU and free thiols. Nat. Commun. 6:5686 [Google Scholar]
  91. Partridge JD, Bodenmiller DM, Humphrys MS, Spiro S. 91.  2009. NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility. Mol. Microbiol. 73:680–94 [Google Scholar]
  92. Pastore A, Puccio H. 92.  2013. Frataxin: a protein in search for a function. J. Neurochem. 126:Suppl. 143–52 [Google Scholar]
  93. Pastore C, Adinolfi S, Huynen MA, Rybin V, Martin S. 93.  et al. 2006. YfhJ, a molecular adaptor in iron-sulfur cluster formation or a frataxin-like protein?. Structure 14:857–67 [Google Scholar]
  94. Pastore C, Franzese M, Sica F, Temussi P, Pastore A. 94.  2007. Understanding the binding properties of an unusual metal-binding protein—a study of bacterial frataxin. FEBS J. 274:4199–210 [Google Scholar]
  95. Patzer SI, Hantke K. 95.  1999. SufS is a NifS-like protein, and SufD is necessary for stability of the [2Fe-2S] FhuF protein in Escherichia coli. J. Bacteriol. 181:3307–9 [Google Scholar]
  96. Pohl T, Walter J, Stolpe S, Soufo JH, Grauman PL, Friedrich T. 96.  2007. Effects of the deletion of the Escherichia coli frataxin homologue CyaY on the respiratory NADH:ubiquinone oxidoreductase. BMC Biochem. 8:13 [Google Scholar]
  97. Poor CB, Wegner SV, Li H, Dlouhy AC, Schuermann JP. 97.  et al. 2014. Molecular mechanism and structure of the Saccharomyces cerevisiae iron regulator Aft2. PNAS 111:4043–48 [Google Scholar]
  98. Prischi F, Konarev PV, Iannuzzi C, Pastore C, Adinolfi S. 98.  et al. 2010. Structural bases for the interaction of frataxin with the central components of iron-sulphur cluster assembly. Nat. Commun. 1:95 [Google Scholar]
  99. Pullan ST, Gidley MD, Jones RA, Barrett J, Stevanin TM. 99.  et al. 2007. Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S nitrosation. J. Bacteriol. 189:1845–55 [Google Scholar]
  100. Py B, Barras F. 100.  2010. Building Fe-S proteins: bacterial strategies. Nat. Rev. Microbiol. 8:436–46 [Google Scholar]
  101. Py B, Gerez C, Angelini S, Planel R, Vinella D. 101.  et al. 2012. Molecular organization, biochemical function, cellular role and evolution of NfuA, an atypical Fe-S carrier. Mol. Microbiol. 86:155–71 [Google Scholar]
  102. Py B, Moreau PL, Barras F. 102.  2011. Fe-S clusters, fragile sentinels of the cell. Curr. Opin. Microbiol. 14:218–23 [Google Scholar]
  103. Rajagopalan S, Teter SJ, Zwart PH, Brennan RG, Phillips KJ, Kiley PJ. 103.  2013. Studies of IscR reveal a unique mechanism for metal-dependent regulation of DNA binding specificity. Nat. Struct. Mol. Biol. 20:740–47 [Google Scholar]
  104. Ranquet C, Ollagnier-de-Choudens S, Loiseau L, Barras F, Fontecave M. 104.  2007. Cobalt stress in Escherichia coli: the effect on the iron-sulfur proteins. J. Biol. Chem. 282:30442–51 [Google Scholar]
  105. Roche B, Agrebi R, Huguenot A, Ollagnier de Choudens S, Barras F, Py B. 105.  2015. Turning Escherichia coli into a frataxin dependent organism. PLOS Genetics 11:5e1005134 [Google Scholar]
  106. Roche B, Aussel L, Ezraty B, Mandin P, Py B, Barras F. 106.  2013. Iron/sulfur proteins biogenesis in prokaryotes: formation, regulation and diversity. Biochim. Biophys. Acta 1827:455–69 [Google Scholar]
  107. Roche B, Huguenot A, Barras F, Py B. 107.  2015. The iron-binding CyaY and IscX proteins assist the ISC-catalyzed Fe-S biogenesis in Escherichia coli. Mol. Microbiol. 95:605–23 [Google Scholar]
  108. Saini A, Mapolelo DT, Chahal HK, Johnson MK, Outten FW. 108.  2010. SufD and SufC ATPase activity are required for iron acquisition during in vivo Fe-S cluster formation on SufB. Biochemistry 49:9402–12 [Google Scholar]
  109. Schwartz CJ, Giel JL, Patschkowski T, Luther C, Ruzicka FJ. 109.  et al. 2001. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. PNAS 98:14895–900 [Google Scholar]
  110. Seki A, Nakano T, Takahashi H, Matsumoto K, Ikeuchi M, Tanaka K. 110.  2006. Light-responsive transcriptional regulation of the suf promoters involved in cyanobacterium Synechocystis sp. PCC 6803 Fe-S cluster biogenesis. FEBS Lett. 580:5044–48 [Google Scholar]
  111. Shen G, Balasubramanian R, Wang T, Wu Y, Hoffart LM. 111.  et al. 2007. SufR coordinates two [4Fe-4S]2+,1+ clusters and functions as a transcriptional repressor of the sufBCDS operon and an autoregulator of sufR in cyanobacteria. J. Biol. Chem. 282:31909–19 [Google Scholar]
  112. Shi R, Proteau A, Villarroya M, Moukadiri I, Zhang L. 112.  et al. 2010. Structural basis for Fe-S cluster assembly and tRNA thiolation mediated by IscS protein-protein interactions. PLOS Biol. 8:e1000354 [Google Scholar]
  113. Skovran E, Downs DM. 113.  2003. Lack of the ApbC or ApbE protein results in a defect in Fe-S cluster metabolism in Salmonella enterica serovar Typhimurium. J. Bacteriol. 185:98–106 [Google Scholar]
  114. Skovran E, Lauhon CT, Downs DM. 114.  2004. Lack of YggX results in chronic oxidative stress and uncovers subtle defects in Fe-S cluster metabolism in Salmonella enterica. J. Bacteriol. 186:7626–34 [Google Scholar]
  115. Song JY, Marszalek J, Craig EA. 115.  2012. Cysteine desulfurase Nfs1 and Pim1 protease control levels of Isu, the Fe-S cluster biogenesis scaffold. PNAS 109:10370–75 [Google Scholar]
  116. Takahashi Y, Tokumoto U. 116.  2002. A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J. Biol. Chem. 277:28380–83 [Google Scholar]
  117. Thorgersen MP, Downs DM. 117.  2008. Analysis of yggX and gshA mutants provides insights into the labile iron pool in Salmonella enterica. J. Bacteriol. 190:7608–13 [Google Scholar]
  118. Thorgersen MP, Downs DM. 118.  2009. Oxidative stress and disruption of labile iron generate specific auxotrophic requirements in Salmonella enterica. Microbiology 155:295–304 [Google Scholar]
  119. Tokumoto U, Nomura S, Minami Y, Mihara H, Kato S. 119.  et al. 2002. Network of protein-protein interactions among iron-sulfur cluster assembly proteins in Escherichia coli. J. Biochem. 131:713–19 [Google Scholar]
  120. Tokumoto U, Takahashi Y. 120.  2001. Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron-sulfur proteins. J. Biochem. 130:63–71 [Google Scholar]
  121. Trotter V, Vinella D, Loiseau L, Ollagnier de Choudens S, Fontecave M, Barras F. 121.  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. 74:1527–42 [Google Scholar]
  122. Tsai CL, Barondeau DP. 122.  2010. Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex. Biochemistry 49:9132–39 [Google Scholar]
  123. Varghese S, Wu A, Park S, Imlay KR, Imlay JA. 123.  2007. Submicromolar hydrogen peroxide disrupts the ability of Fur protein to control free-iron levels in Escherichia coli. Mol. Microbiol. 64:822–30 [Google Scholar]
  124. Velayudhan J, Castor M, Richardson A, Main-Hester KL, Fang FC. 124.  2007. The role of ferritins in the physiology of Salmonella enterica sv. Typhimurium: a unique role for ferritin B in iron-sulphur cluster repair and virulence. Mol. Microbiol. 63:1495–507 [Google Scholar]
  125. Velayudhan J, Karlinsey JE, Frawley ER, Becker LA, Nartea M, Fang FC. 125.  2014. Distinct roles of the Salmonella enterica serovar Typhimurium CyaY and YggX proteins in the biosynthesis and repair of iron-sulfur clusters. Infect. Immun. 82:1390–401 [Google Scholar]
  126. Vickery LE, Silberg JJ, Ta DT. 126.  1997. Hsc66 and Hsc20, a new heat shock cognate molecular chaperone system from Escherichia coli. Protein Sci. 6:1047–56 [Google Scholar]
  127. Vinella D, Brochier-Armanet C, Loiseau L, Talla E, Barras F. 127.  2009. Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers. PLOS Genet. 5:e1000497 [Google Scholar]
  128. Vinella D, Loiseau L, Ollagnier de Choudens S, Fontecave M, Barras F. 128.  2013. In vivo [Fe-S] cluster acquisition by IscR and NsrR, two stress regulators in Escherichia coli. Mol. Microbiol. 87:493–508 [Google Scholar]
  129. Vivas E, Skovran E, Downs DM. 129.  2006. Salmonella enterica strains lacking the frataxin homolog CyaY show defects in Fe-S cluster metabolism in vivo. J. Bacteriol. 188:1175–79 [Google Scholar]
  130. Waller JC, Alvarez S, Naponelli V, Lara-Nunez A, Blaby IK. 130.  et al. 2010. A role for tetrahydrofolates in the metabolism of iron-sulfur clusters in all domains of life. PNAS 107:10412–17 [Google Scholar]
  131. Wang T, Shen G, Balasubramanian R, McIntosh L, Bryant DA, Golbeck JH. 131.  2004. The sufR gene (sll0088 in Synechocystis sp. strain PCC 6803) functions as a repressor of the sufBCDS operon in iron-sulfur cluster biogenesis in cyanobacteria. J. Bacteriol. 186:956–67 [Google Scholar]
  132. Westphal K, Langklotz S, Thomanek N, Narberhaus F. 132.  2012. A trapping approach reveals novel substrates and physiological functions of the essential protease FtsH in Escherichia coli. J. Biol. Chem. 287:42962–71 [Google Scholar]
  133. Wollers S, Layer G, Garcia-Serres R, Signor L, Clemancey M. 133.  et al. 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. 285:23331–41 [Google Scholar]
  134. Yan R, Konarev PV, Iannuzzi C, Adinolfi S, Roche B. 134.  et al. 2013. Ferredoxin competes with bacterial frataxin in binding to the desulfurase IscS. J. Biol. Chem. 288:24777–87 [Google Scholar]
  135. Yang J, Bitoun JP, Ding H. 135.  2006. Interplay of IscA and IscU in biogenesis of iron-sulfur clusters. J. Biol. Chem. 281:27956–63 [Google Scholar]
  136. Yeo WS, Lee JH, Lee KC, Roe JH. 136.  2006. IscR acts as an activator in response to oxidative stress for the suf operon encoding Fe-S assembly proteins. Mol. Microbiol. 61:206–18 [Google Scholar]
  137. Yeung N, Gold B, Liu NL, Prathapam R, Sterling HJ. 137.  et al. 2011. The E. coli monothiol glutaredoxin GrxD forms homodimeric and heterodimeric FeS cluster containing complexes. Biochemistry 50:8957–69 [Google Scholar]
  138. Yoon H, Golla R, Lesuisse E, Pain J, Donald JE. 138.  et al. 2012. Mutation in the Fe-S scaffold protein Isu bypasses frataxin deletion. Biochem. J. 441:473–80 [Google Scholar]
  139. Yoon H, Knight SA, Pandey A, Pain J, Zhang Y. 139.  et al. 2014. Frataxin-bypassing Isu1: characterization of the bypass activity in cells and mitochondria. Biochem. J. 459:71–81 [Google Scholar]
  140. Yoon H, Knight SAB, Pandey A, Pain J, Turkarslan S. 140.  et al. 2015. Turning Saccharomyces cerevisiae into a frataxin-independent organism. PLOS Genetics 11:5e1005135 [Google Scholar]
  141. Zheng M, Doan B, Schneider TD, Storz G. 141.  1999. OxyR and SoxRS regulation of fur. J. Bacteriol. 181:4639–43 [Google Scholar]
  142. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G. 142.  2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183:4562–70 [Google Scholar]
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How Is Fe-S Cluster Formation Regulated?
Annual Review of Microbiology 69, 505 (2015); https://doi.org/10.1146/annurev-micro-091014-104457
/content/journals/10.1146/annurev-micro-091014-104457
/content/journals/10.1146/annurev-micro-091014-104457
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