Turning Escherichia coli into a Frataxin-Dependent Organism

PLoS Genetics

Volumn 11, Issue 5, 2015, Pages

  Roche, Béatrice ^a   Agrebi, Rym ^b   Huguenot, Allison ^a   Ollagnier de Choudens, Sandrine ^c   Barras, Frédéric ^a   Py, Béatrice ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b DE DUVE INSTITUTE   (Belgium)

^c CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FRATAXIN; IRON SULFUR PROTEIN; PROTEIN CYAY; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SUCCINATE DEHYDROGENASE; UNCLASSIFIED DRUG; CYAY PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; IRON BINDING PROTEIN; ISCU PROTEIN, E COLI;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PHYLOGENETIC TREE; PHYLOGENY; PROKARYOTE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SEQUENCE ALIGNMENT; BIOLOGY; GENE DELETION; GENETICS; METABOLISM; MICROBIAL VIABILITY; MUTATION;

ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA; RICKETTSIACEAE;

COMPUTATIONAL BIOLOGY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; IRON-BINDING PROTEINS; IRON-SULFUR PROTEINS; MICROBIAL VIABILITY; MUTATION; PHYLOGENY; SUCCINATE DEHYDROGENASE;

EID: 84930788102     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005134     Document Type: Article

References (85)

1. Py B, Barras F, Building Fe-S proteins: bacterial strategies. Nat Rev Microbiol. 2010;8: 436–446. doi: 10.1038/nrmicro2356 20467446
2. Crack JC, Green J, Thomson AJ, Le Brun NE, Iron-sulfur cluster sensor-regulators. Curr Opin Chem Biol. 2012;16: 35–44. doi: 10.1016/j.cbpa.2012.02.009 22387135
3. Balk J, Schaedler TA, Iron cofactor assembly in plants. Annu Rev Plant Biol. 2014;65: 125–53. doi: 10.1146/annurev-arplant-050213-035759 24498975
4. Roche B, Aussel L, Ezraty B, Mandin P, Py B, Barras F, Iron/sulfur proteins biogenesis in prokaryotes: formation, regulation and diversity. Biochim Biophys Acta. 2013;1827: 923–937. doi: 10.1016/j.bbabio.2013.05.001 23660107
5. Stehling O, Lill R, The role of mitochondria in cellular iron-sulfur protein biogenesis: mechanisms, connected processes, and diseases. Cold Spring Harb Perspect Med. 2013;3: 1–17. 23986915
6. Schilke B, Williams B, Knieszner H, Pukszta S, D’Silva P, Craig EA, et al. Evolution of mitochondrial chaperones utilized in Fe-S cluster biogenesis. Curr Biol. 2006;16: 1660–1665. 16920629
7. Vickery LE, Cupp-Vickery JR, Molecular chaperones HscA/Ssq1 and HscB/Jac1 and their roles in iron-sulfur protein maturation. Crit Rev Biochem Mol Biol. 2007;42: 95–111. 17453917
8. Bandyopadhyay S, Chandramouli K, Johnson MK, Iron-sulfur cluster biosynthesis. Biochem Soc Trans. 2008;36: 1112–1119. doi: 10.1042/BST0361112 19021507
9. Bonomi F, Iametti S, Morleo A, Ta D, Vickery LE, Facilitated transfer of IscU-[2Fe-2S] clusters by chaperone-mediated ligand exchange. Biochem. 2011;50: 9641–9650.
10. Marinoni EN, de Oliveira JS, Nicolet Y, Raulfs EC, Amara P, Dean DR, et al. (IscS-IscU)2 complex structures provide insights into Fe2S2 biogenesis and transfer. Angew Chem Int Ed. 2012;51: 5439–5442. doi: 10.1002/anie.201201708 22511353
11. Zheng L, White RH, Cash VL, Jack RF, Dean DR, Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc Natl Acad Sci USA. 1993;90: 2754–2758. 8464885
12. Kispal G, Csere P, Prohl C, Lill R, The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J. 1999;18: 3981–3989. 10406803
13. Li J, Kogan M, Knight SA, Pain D, Dancis A, Yeast mitochondrial protein, Nfs1p, coordinately regulated iron-sulfur cluster proteins, cellular iron uptake, and iron distribution. J Biol Chem. 1999;274: 33025–33034. 10551871
14. Schwartz CJ, Djaman O, Imaly JA, Kiley PJ, The cysteine desulfurase, IscS, has a major role in vivo Fe-S cluster formation in Escherichia coli. Proc Natl Acad Sci USA. 2000;97: 9009–9014. 10908675
15. Hidese R, Mihara H, Esaki N, Bacterial cysteine desulfurases: versatile key players in biosynthetic pathways of sulfur-containing biofactors. Appl Microbiol Biotechnol. 2011;91: 47–61. doi: 10.1007/s00253-011-3336-x 21603932
16. Smith AD, Agar JN, Johnson KA, Frazzon J, Amster IJ, Dean DR, et al. Sulfur transfer from IscS to IscU: the first step in iron-sulfur cluster biosynthesis. J Am Chem Soc. 2001;123: 11103–11104. 11686732
17. Smith AD, Frazzon J, Dean DR, Johnson MK, Role of conserved cysteines in mediating sulfur transfer from IscS to IscU. FEBS Lett. 2005;579: 5236–5240. 16165131
18. Urbina HD, Silberg JJ, Hoff KG, Vickery LE, Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J Biol Chem. 2001;276: 44521–44526. 11577100
19. Gibson TJ, Koonin EV, Musco G, Pastore A, Bork P, Friedreich’s ataxia protein: phylogenetic evidence for mitochondrial dysfunction. Trends Neurosci. 1996;19: 465–468. 8931268
20. Gerber J, Mühlenhoff U, Lill R, An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep. 2003;4: 906–911. 12947415
21. Wang T, Craig EA, Binding of yeast frataxin to the scaffold for Fe-S cluster biogenesis, Isu. J Biol Chem. 2008;283: 12674–12679. doi: 10.1074/jbc.M800399200 18319250
22. Adinolfi S, Iannuzzi C, Prischi F, Pastore C, Iametti S, Martin SR, et al. Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS. Nat Struct Mol Biol. 2009;16: 390–396. doi: 10.1038/nsmb.1579 19305405
23. Shi R, Proteau A, Villarroya M, Moukadiri I, Zhang L, Trempe JF, et al. Structural basis for Fe-S cluster assembly and tRNA thiolation mediated by IscS protein-protein interactions. PLoS Biol. 2010;8: e1000354. doi: 10.1371/journal.pbio.1000354 20404999
24. Prischi F, Konarev PV, Iannuzzi C, Pastore C, Adinolfi S, Martin SR, et al. Structural bases for the interaction of frataxin with the central components of iron-sulfur cluster assembly. Nat Commun. 2010;1: 95. doi: 10.1038/ncomms1097 20981023
25. Tsai CL, Barondeau DP, Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex. Biochemistry. 2010;49: 9132–9139. doi: 10.1021/bi1013062 20873749
26. Schmucker S, Martelli A, Colin F, Page A, Wattenhofer-Donzé M, Reutenauer L, et al. Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 iron-sulfur assembly complex. PLoS One. 2011;6: e16199. doi: 10.1371/journal.pone.0016199 21298097
27. Tokumoto U, Takahashi Y, Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron-sulfur proteins. J Biochem. 2001;130: 63–71. 11432781
28. Li K, Tong WH, Hughes RM, Rouault TA, Roles of the mammalian cytosolic cysteine desulfurase, ISCS, and scaffold protein, ISCU, in iron-sulfur cluster assembly. J Biol Chem. 2006;281: 12344–12351. 16527810
29. Rouault TA, Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease. Dis Model Mech. 2012;5: 155–164. doi: 10.1242/dmm.009019 22382365
30. Babcock M, de Silva D, Oaks R, Davis-Kaplan S, Jiralerspong S, Montermini L, et al. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science. 1997;276: 1709–1712. 9180083
31. Foury F, Cazzalini O, Deletion of the yeast homologue of the human gene associated with Friedreich’s ataxia elicits iron accumulation in mitochondria. FEBS Lett. 1997;11: 373–377.
32. Foury F, Low iron concentration and aconitase deficiency in a yeast frataxin homologue deficient strain. FEBS Lett. 1999;456: 281–284. 10456324
33. Lesuisse E, Santos R, Matzanke BF, Knight SA, Camadro JM, Dancis A, Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1). Hum Mol Genet. 2003;12: 879–889. 12668611
34. Pastore A, Puccio H, Frataxin: a protein in search for a function. J Neurochem. 2013;1: 43–52.
35. Campuzano V, Montermini L, Molto MD, Pianese L, Cossée M, Cavalcanti F, et al. Freidreich’s ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science. 1996;271: 1423–1427. 8596916
36. Rötig A, de Lonlay P, Chretien D, Foury F, Koenig M, Sidi D, et al. Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat Genet. 1997;17: 215–217. 9326946
37. Stehling O, Elsässer HP, Brückel B, Mühlenhoff U, Lill R, Iron-sulfur protein maturation in human cells: evidence for a function of frataxine. Hum Mol Genet. 2004;13: 3007–3015. 15509595
38. Pandolfo M, Pastore A, The pathogenesis of Friedreich ataxia and the structure and function of frataxin. J Neurol. 2009;256: 9–17. doi: 10.1007/s00415-009-1003-2 19283345
39. Santos R, Lefevre S, Sliwa D, Seguin A, Camadro JM, Lesuisse E, Friedreich ataxia: molecular mechanisms, redox considerations, and therapeutic opportunities. Antioxid Redox Signal. 2010;13: 651–690. doi: 10.1089/ars.2009.3015 20156111
40. Li DS, Ohshima K, Jiralerspong S, Bojanowski MW, Pandolfo M, Knock-out of the cyaY gene in Escherichia coli does not affect cellular iron content and sensitivity to oxidants. FEBS. 1999;456:13–16. 10452520
41. Vivas E, Skovran E, Downs DM, Salmonella enterica strains lacking the frataxin homolog CyaY show defects in Fe-S cluster metabolism in vivo. J Bacteriol. 2006;188: 1175–1179. 16428423
42. Pohl T, Walter J, Stolpe S, Soufo JH, Grauman PL, Friedrich T, Effects of the deletion of the Escherichia coli frataxin homologue CyaY on the respiratory NADH: ubiquinone oxidoreductase. BMC Biochem. 2007;8: 13. doi: 10.1186/1471-2091-8-13 17650323
43. Velayudhan J, Karlinsev JE, Frawley ER, Becker LA, Nartea M, Fang FC, Distinct roles of the Salmonella enterica serovar Typhimurium CyaY and YggX proteins in the biosynthesis and repair of iron-sulfur clusters. Infect Immun. 2014;82: 1390–1401. doi: 10.1128/IAI.01022-13 24421039
44. Roche B, Huguenot A, Barras F, Py B, The iron-binding CyaY and IscX proteins assist the ISC-catalyzed Fe-S biogenesis in Escherichia coli. Mol Microbiol. 2015;4: 605–623. doi: 10.1111/mmi.12888 25430730
45. Yoon H, Golla R, Lesuisse E, Pain J, Donald JE, Lyver ER, et al. Mutation in the Fe-S scaffold protein Isu bypasses frataxin deletion. Biochem J. 2012;441: 473–480. doi: 10.1042/BJ20111637 21936771
46. Ezraty B, Vergnes A, Banzhaf M, Duverger Y, Huguenot A, Brochado AR, et al. Fe-S cluster biosynthesis controls uptake of aminoglycosides in a ROS-less death pathway. Science. 2013;340: 1583–1587. doi: 10.1126/science.1238328 23812717
47. Dailey HA, Finnegan MG, Johnson MK, Human ferrochelatase is an iron-sulfur protein. Biochemistry. 1994;33: 403–407. 8286370
48. Agar JN, Krebs C, Frazzon J, Huynh BH, Dean DR, Johnson MK, IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. Biochemistry. 2000;39: 7856–7862. 10891064
49. Adinolfi S, Rizzo F, Masino L, Nair M, Martin SR, Pastore A, et al. Bacterial IscU is a well folded and functional single domain protein. Eur J Biochem. 2004;271: 2093–2100. 15153099
50. Loiseau L, Gerez C, Bekker M, Ollagnier-de Choudens S, Py B, Sanakis Y, et al. ErpA, an iron sulfur (Fe-S) protein of the A-type essential for respiratory metabolism in Escherichia coli. Proc Natl Acad Sci USA. 2007;104: 13626–13631. 17698959
51. Vinella D, Loiseau L, Ollagnier-de-Choudens S, Fontecave M, Barras F, In vivo [Fe-S] cluster acquisition by IscR and NsrR, two stress regulators in Escherichia coli. Mol Microbiol. 2013;3: 493–508. doi: 10.1111/mmi.12135 23320508
52. Adam AC, Bornhövd C, Prokisch H, Neupert W, Hell K, The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria. EMBO J. 2006;25:174–183. 16341090
53. Wiedemann N, Urzica E, Guiard B, Müller H, Lohaus C, Meyer HE, et al. Essential role of Isd11 in mitochondrial iron-sulfur cluster synthesis on Isu scaffold proteins. EMBO J. 2006;25: 184–195. 16341089
54. Richards TA, van der Giezen M, Evolution of the Isd11-IscS complex reveals a single alpha-proteobacterial endosymbiosis for all eukaryotes. Mol Biol Evol. 2006;23: 1341–1344. 16648156
55. Pandey A, Golla R, Yoon H, Dancis A, Pain D, Persulfide formation on mitochondrial cysteine desulfurase: enzyme activation by a eukaryote-specific interacting protein and Fe-S cluster synthesis. Biochem J. 2012;448: 171–187. doi: 10.1042/BJ20120951 22928949
56. Lim SC, Friemel M, Marum JE, Tucker EJ, Bruno DL, Riley LG, et al. Mutations in LYRM4, encoding iron-sulfur cluster biogenesis factor ISD11, cause deficiency of multiple respiratory chain complexes. Hum Mol Genet. 2013;22: 4460–4473. doi: 10.1093/hmg/ddt295 23814038
57. Pandey A, Gordon DM, Pain J, Stemmler TL, Dancis A, Pain D, 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. 2013;288: 36773–36786. doi: 10.1074/jbc.M113.525857 24217246
58. Parent A, Elduque X, Cornu D, Belot L, Le Caer JP, Grandas A, et al. Mammalian frataxin directly enhances sulfur transfer of NFS1 persulfide to both ISCU and free thiols. Nat Commun. 2015;6: 5686. doi: 10.1038/ncomms6686 25597503
59. Yoon H, Knight SA, Pandey A, Pain J, Zhang Y, Pain D, et al. Frataxin-bypassing Isu1: characterization of the bypass activity in cells and mitochondria. Biochem J. 2014;459: 71–81. doi: 10.1042/BJ20131273 24433162
60. Seguin A, Bayot A, Dancis A, Rogowska-Wrzesinska A, Auchère F, Camadro JM, et al. Overexpression of the yeast frataxin homolog (Yfh1): contrasting effects on iron-sulfur cluster assembly, heme synthesis and resistance to oxidative stress. Mitochondrion. 2009;9: 130–138. doi: 10.1016/j.mito.2009.01.007 19460301
61. Lefevre S, Sliwa D, Rustin P, Camadro JM, Santos R, Oxidative stress induces mitochondrial fragmentation in frataxin-deficient cells. Biochem Biophys Res Commun. 2012;418: 336–341. doi: 10.1016/j.bbrc.2012.01.022 22274609
62. Iannuzzi C, Adinolfi S, Howes BD, Garcia-Serres R, Cemancey M, Latour JM, et al. The role of CyaY in iron-sulfur cluster assembly on the E. coli IscU scaffold protein. PLoS One. 2011;6: e21992. doi: 10.1371/journal.pone.0021992 21799759
63. Bridwell-Rabb J, Iannuzzi C, Pastore A, Barondeau DP, Effector role reversal during evolution: the case of frataxin in Fe-S cluster biosynthesis. Biochemistry. 2012;51: 2506–2514. doi: 10.1021/bi201628j 22352884
64. Huynen MA, Snel B, Bork P, Gibson TJ, The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum Mol Genet. 2001;10: 2463–2468. 11689493
65. Vinella D, Brochier-Armanet C, Loiseau L, Talla E, Barras F, Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers. PLoS Genet. 2009;5: e1000497. doi: 10.1371/journal.pgen.1000497 19478995
66. Py B, Gerez C, Angelini S, Planel R, Vinella D, Loiseau L, et al. Molecular organization, biochemical function, cellular role and evolution of NfuA, an atypical Fe-S carrier. Mol Microbiol. 2012;86: 155–171. doi: 10.1111/j.1365-2958.2012.08181.x 22966982
67. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the KEIO collection. Mol Syst Biol. 2006;2: 2006.0008. 16738554
68. Mandin P, Gottesman S, A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA/DpiB two-component system. Mol Microbiol. 2009;72: 551–565. doi: 10.1111/j.1365-2958.2009.06665.x 19426207
69. Layer G, Ollagnier-de-Choudens S, Sanakis Y, Fontecave M, Iron-sulfur cluster biosynthesis. J Biol Chem. 2006;281: 16256–16263. 16603772
70. Miller J.H, Experiments in molecular genetics. Cold Spring Harbor Laboratory Press. Cold Sppring Harbor, NY;1972.
71. Seaver LC, Imlay JA, Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J Biol Chem. 2004;279: 48742–48750. 15361522
72. Kolaj-Robin O, O’Kane SR, Nitschke W, Léger C, Baymann F, Soulimane T, Biochemical and biophysical characterization of succinate: quinone reductase from Thermus thermophilus. Biochim Biophys Acta. 2011;1807: 68–79. doi: 10.1016/j.bbabio.2010.10.009 20951673
73. Zhao Z, Rothery RA, Weiner JH, Effects of site-directed mutations on heme reduction in Escherichia coli nitrate reductase A by menaquinol: a stopped-flow study. Biochemistry. 2003;42: 14225–14233. 14640690
74. Tokumoto U, Nomura S, Minami Y, Mihara H, Kato S, Kurihara T, et al. Network of protein-protein interactions among iron-sulfur assembly proteins in Escherichia coli. J Biochem. 2002;131: 713–719. 11983079
75. Finn RD, Clements J, Eddy SR, HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39: 29–37.
76. Qi W, Cowan JA, A structural and functional homolog supports a general role for frataxin in cellular iron chemistry. Chem Commun (Camb). 2010;46: 719–721. doi: 10.1039/b911975b 20087498
77. Albrecht AG, Landmann H, Nette D, Burghaus O, Peuckert F, Seubert A, et al. The frataxin homologue Fra plays a key role in intracellular iron channeling in Bacillus subtilis. Chembiochem. 2011;12: 2052–2061. doi: 10.1002/cbic.201100190 21744456
78. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25: 3389–3402. 9254694
79. Overmars L, Kerkhoven R, Siezen RJ, Francke C, MGcV: the microbial genomic context viewer for comparative genome analysis. BMC Genomics. 2013;14: 209. doi: 10.1186/1471-2164-14-209 23547764
80. Katoh K, Standley DM, MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30: 772–780. doi: 10.1093/molbev/mst010 23329690
81. Philippe H, MUST, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res. 1993;21: 5264–5272. 8255784
82. Criscuolo A, Gribaldo S, BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol. 2010;10: 210. doi: 10.1186/1471-2148-10-210 20626897
83. Huelsenbeck JP, Ronquist F, MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17: 754–755. 11524383
84. Shih AC, Lee DT, Peng CL, Wu YW, Phylo-mLogo: an interactive and hierarchical multiple-logo visualization tool for alignment of many sequences. BMC Bioinformatics. 2007;8: 63. doi: 10.1186/1471-2105-8-63 17319966
85. Cho SJ, Lee MG, Yang JK, Lee JY, Song HK, Suh SW, Crystal structure of Escherichia coli CyaY protein reveals a previously unidentified fold for the evolutionarily conserved frataxin family. Proc Natl Acad Sci USA. 2000;97: 8932–8937. 10908679