Effects of the deletion of the Escherichia coli frataxin homologue CyaY on the respiratory NADH:ubiquinone oxidoreductase

BMC Biochemistry

Volumn 8, Issue , 2007, Pages

  Pohl, Thomas ^a   Walter, Julia ^a   Stolpe, Stefan ^a   Soufo, Joel H Defeu ^a   Grauman, Peter L ^a   Friedrich, Thorsten ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYAY PROTEIN; FRATAXIN; IRON SULFUR PROTEIN; MUTANT PROTEIN; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UBIQUINONE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYAY PROTEIN, E COLI; IRON BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; BACTERIAL STRAIN; CELL MEMBRANE; CELL STRUCTURE; CYTOPLASM; ENZYME ACTIVATION; ESCHERICHIA COLI; GENE ACTIVITY; GENE DELETION; GENE FUNCTION; GENETIC ENGINEERING; MITOCHONDRIAL RESPIRATION; NONHUMAN; WESTERN BLOTTING; CATALYSIS; CHEMISTRY; CYTOLOGY; ELECTRON SPIN RESONANCE; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL VIABILITY; OXYGEN CONSUMPTION; PROTEIN BINDING;

ESCHERICHIA COLI; THERMUS THERMOPHILUS;

BACTERIAL PROTEINS; CATALYSIS; CELL MEMBRANE; CYTOPLASM; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; GENE DELETION; IRON-BINDING PROTEINS; MICROBIAL VIABILITY; NAD; OXIDOREDUCTASES; OXYGEN CONSUMPTION; PROTEIN BINDING; UBIQUINONE;

EID: 34548363856     PISSN: None     EISSN: 14712091     Source Type: Journal    
DOI: 10.1186/1471-2091-8-13     Document Type: Article

References (56)

1. The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. JE Walker, Q Rev Biophys 1992 25 253 324 1470679
2. The respiratory-chain NADH dehydrogenase (complex I) of mitochondria. H Weiss T Friedrich G Hofhaus D Preis, Eur J Biochem 1991 197 563 576 10.1111/j.1432-1033.1991.tb15945.x 2029890
3. Iron-sulfur clusters/semiquinones in complex I. T Ohnishi, Biochim Biophys Acta 1998 1364 186 206 10.1016/S0005-2728(98)00027-9 9593887
4. Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism? U Brandt S Kerscher S Dröse K Zwicker V Zickermann, FEBS Lett 2003 545 9 17 10.1016/S0014-5793(03)00387-9 12788486
5. The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. T Yagi A Matsuno-Yagi, Biochemistry 2003 42 2266 2274 10.1021/bi027158b 12600193
6. The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. T Friedrich K Steinmüller H Weiss, FEBS Lett 1995 367 107 111 10.1016/0014-5793(95)00548-N 7796904
7. The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. T Friedrich D Scheide, FEBS Lett 2000 479 1 5 10.1016/S0014-5793(00)01867-6 10940377
8. Complex I: a chimaera of a redox and conformation-driven proton pump? T Friedrich, J Bioenerg Biomembr 2001 33 169 177 10.1023/A:1010722717257 11695826
9. Procaryotic complex I (NDH-1), an overview. T Yagi T Yano S Di Bernado A Matsuno-Yagi, Biochim Biophys Acta 1998 1364 125 133 10.1016/S0005-2728(98) 00023-1 9593856
10. The NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli. T Friedrich, Biochim Biophys Acta 1998 1364 134 146 10.1016/S0005-2728(98)00024-3 9593861
11. Structure of the respiratory NADH:ubiquinone oxidoreductase (complex I). N Grigorieff, Curr Opin Struct Biol 1999 9 476 483 10.1016/S0959-440X(99)80067-0 10449365
12. The gross structure of the respiratory complex I: a Lego System. T Friedrich B Böttcher, Biochim Biophys Acta 2004 1608 1 9 10.1016/j.bbabio.2003.10.002 14741580
13. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. LA Sazanov P Hinchliffe, Science 2006 311 1430 1436 10.1126/science.1123809 16469879
14. Identification of a novel subunit of respiratory complex I from Thermus thermophilus. P Hinchliffe J Carroll LA Sazanov, Biochemistry 2006 45 4413 4420 10.1021/bi0600998 16584177
15. Crystal structure of Escherichia coli CyaY protein reveals a previously unidentified fold for the evolutionarily conserved frataxin family. SJ Cho MG Lee JK Yang JY Lee HK Song SW Suh, Proc Natl Acad Sci USA 2000 97 8932 8937 10908679 10.1073/pnas.160270897
16. Mapping of mutation causing Friedreich's ataxia to human chromosome 9. S Chamberlain J Shaw A Rowland J Wallis S South Y Nakamura GA von M Farrall R Williamson, Nature 1988 334 248 250 10.1038/334248a0 2899844
17. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. V Campuzano L Montermini MD Molto L Pianese M Cossee F Cavalcanti E Monros F Rodius F Duclos A Monticelli F Zara J Canizares H Koutnikova SI Bidichandani C Gellera A Brice P Trouillas G De Michele A Filla R De Frutos F Palau PI Patel S Di Donato JL Mandel S Cocozza M Koenig M Pandolfo, Science 1996 271 1423 1427 10.1126/science.271.5254.1423 8596916
18. Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. V Campuzano L Montermini Y Lutz L Cova C Hindelang S Jiralerspong Y Trottier SJ Kish B Faucheux P Trouillas FJ Authier A Durr JL Mandel A Vescovi M Pandolfo M Koenig, Hum Mol Genet 1997 6 1771 1780 10.1093/hmg/6.11.1771 9302253
19. The molecular basis of Friedreich ataxia. M Pandolfo, Adv Exp Med Biol 2002 516 99 118 12611437
20. Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli. F Bou-Abdallah S Adinolfi A Pastore TM Laue CN Dennis, J Mol Biol 2004 341 605 615 10.1016/j.jmb.2004.05.072 15276847
21. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. M Babcock D de Silva R Oaks S Davis-Kaplan S Jiralerspong L Montermini M Pandolfo J Kaplan, Science 1997 276 1709 1712 10.1126/science.276. 5319.1709 9180083
22. A non-essential function for yeast frataxin in iron-sulfur cluster assembly. G Duby F Foury A Ramazzotti J Herrmann T Lutz, Hum Mol Genet 2002 11 2635 2643 10.1093/hmg/11.21.2635 12354789
23. An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. J Gerber U Mühlenhoff R Lill, EMBO Rep 2003 4 906 911 12947415 10.1038/sj.embor.embor918
24. Iron-sulfur cluster biosynthesis: characterization of Escherichia coli CYaY as an iron donor for the assembly of [2Fe-2S] clusters in the scaffold IscU. G Layer S Ollagnier-de Choudens Y Sanakis M Fontecave, J Biol Chem 2006 281 16256 16263 10.1074/jbc.M513569200 16603772
25. Knock-out of the cyaY gene in Escherichia coli does not affect cellular iron content and sensitivity to oxidants. DS Li K Ohshima S Jiralerspong MW Bojanowski M Pandolfo, FEBS Lett 1999 456 13 16 10.1016/S0014-5793(99)00896-0 10452520
26. Salmonella enterica strains lacking the frataxin homolog CyaY show defects in Fe-S cluster metabolism in vivo. E Vivas E Skovran DM Downs, J Bacteriol 2006 188 1175 1179 16428423 10.1128/JB.188.3.1175-1179.2006
27. Two binding sites of inhibitors in NADH: ubiquinone oxidoreductase (complex I). Relationship of one site with the ubiquinone-binding site of bacterial glucose:ubiquinone oxidoreductase. T Friedrich P van Heek H Leif T Ohnishi E Forche B Kunze R Jansen W Trowitzsch-Kienast G Höfle H Reichenbach H Weiss, Eur J Biochem 1994 219 691 698 10.1111/j.1432-1033.1994. tb19985.x 8307034
28. NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain. K Matsushita T Ohnishi HR Kaback, Biochemistry 1987 26 7732 7737 10.1021/bi00398a029 3122832
29. Involvement of tyrosines 114 and 139 of subunit NuoB in the proton pathway around cluster N2 in Escherichia coli NADH:ubiquinone oxidoreductase. D Flemming P Hellwig T Friedrich, J Biol Chem 2003 278 3055 3062 10.1074/jbc.M208849200 12446673
30. Isolation and characterization of the proton-translocating NADH: ubiquinone oxidoreductase from Escherichia coli. H Leif VD Sled T Ohnishi H Weiss T Friedrich, Eur J Biochem 1995 230 538 548 10.1111/j.1432-1033.1995. tb20594.x 7607227
31. Overexpression of the Escherichia coli nuo-operon and isolation of the overproduced NADH:ubiquinone oxidoreductase (complex I). V Spehr A Schlitt D Scheide V Guénebaut T Friedrich, Biochemistry 1999 38 16261 16267 10.1021/bi9919605 10587449
32. Characterization of the overproduced NADH dehydrogenase fragment of the NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli. M Braun S Bungert T Friedrich, Biochemistry 1998 37 1861 1867 10.1021/bi971176p 9485311
33. The Escherichia coli NADH:ubiquinone oxidoreductase (complex I) is a primary proton pump but may be capable of secondary sodium antiport. S Stolpe T Friedrich, J Biol Chem 2004 279 18377 18383 10.1074/jbc.M311242200 14970214
34. A role for native lipids in the stabilization and two-dimensional crystallization of the Escherichia coli NADH-ubiquinone oxidoreductase (complex I). LA Sazanov J Carroll P Holt L Toime IM Fearnley, J Biol Chem 2003 278 19483 19491 10.1074/jbc.M208959200 12637579
35. The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. MA Huynen B Snel P Bork TJ Gibson, Hum Mol Genet 2001 10 2463 2468 10.1093/hmg/10.21.2463 11689493
36. A structural approach to understanding the iron-binding properties of phylogenetically different frataxins. S Adinolfi M Trifuoggi AS Politou S Martin A Pastore, Hum Mol Genet 2002 11 1865 1877 10.1093/hmg/11.16.1865 12140189
37. Structure-function studies of iron-sulfur clusters and semiquinones in the NADH-Q oxidoreductase segment of the respiratory chain. T Ohnishi VD Sled T Yano T Yagi DS Burbaev AD Vinogradov, Biochim Biophys Acta 1998 1365 301 308 10.1016/S0005-2728(98)00082-6 9693742
38. EPR signals assigned to Fe/S cluster N1c of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I) derive from cluster N1a. M Uhlmann T Friedrich, Biochemistry 2005 44 1653 1658 10.1021/bi048136n 15683249
39. The complex I from Rhodobacter capsulatus. A Dupuis M Chevallet E Darrouzet H Duborjal J Lunardi JP Issartel, Biochim Biophys Acta 1998 1364 147 165 10.1016/S0005-2728(98)00025-5 9593868
40. Distinct Iron Binding Property of Two Putative Iron Donors for the Iron-Sulfur Cluster Assembly. H Ding J Yang LC Coleman S Yeung, J Biol Chem 2007 282 7997 8004 10.1074/jbc.M609665200 17244611
41. Iron-sulfur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins. T Yoon JA Cowan, J Am Chem Soc 2003 125 6078 6084 10.1021/ja027967i 12785837
42. Iron-sulfur-protein biogenesis in eukaryotes. R Lill U Mühlenhoff, Trends Biochem Sci 2005 30 133 141 10.1016/j.tibs.2005.01.006 15752985
43. Structure, function, and formation of biological iron-sulfur clusters. DC Johnson DR Dean AD Smith MK Johnson, Annu Rev Biochem 2005 74 247 281 10.1146/annurev.biochem.74.082803.133518 15952888
44. IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. JN Agar C Krebs J Frazzon BH Huynh DR Dean MK Johnson, Biochemistry 2000 39 7856 7862 10.1021/bi000931n 10891064
45. Supramolecular assemblies of human frataxin are formed via subunit-subunit interactions mediated by a non-conserved amino-terminal region. HA O'Neill O Gakh G Isaya, J Mol Biol 2005 345 433 439 10.1016/j.jmb.2004.10.074 15581888
46. Iron-induced oligomerization of yeast frataxin homologue Yfh1 is dispensable in vivo. K Aloria B Schilke A Andrew EA Craig, EMBO Rep 2004 5 1096 1101 15472712 10.1038/sj.embor.7400272
47. Monomeric yeast frataxin is an iron-binding protein. JD Cook KZ Bencze AD Jankovic AK Crater CN Busch PB Bradley AJ Stemmler MR Spaller TL Stemmler, Biochemistry 2006 45 7767 7777 10.1021/bi060424r 16784228
48. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. T Baba T Ara M Hasegawa Y Takai Y Okumura M Baba KA Datsenko M Tomita BL Wanner H Mori, Mol Syst Biol 2006 2 2006 10.1038/msb4100050
49. Complete set of ORF clones of Escherichia coli ASKA library (A Complete Set of E. coli K-12 ORF Archive): Unique Resources for Biological Research. M Kitagawa T Ara M Arifuzzaman T Ioka-Nakamichi E Inamoto H Toyonaga H Mori, DNA Res 2005 12 291 299 10.1093/dnares/dsi012 16769691
50. Experimentally based topology models for E. coli inner membrane proteins. M Rapp D Drew DO Daley J Nilsson T Carvalho K Melen JW De Gier G Von Heijne, Protein Sci 2004 13 937 945 10.1110/ps.03553804 15044727
51. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. LM Guzman D Belin MJ Carson J Beckwith, J Bacteriol 1995 177 4121 4130 7608087
52. Comparison of catalytic activity and inhibitors of quinone reactions of succinate dehydrogenase (succinate-ubiquinone oxidoreductase) and fumarate reductase (menaquinol-fumarate oxidoreductase) from Escherichia coli. E Maklashina G Cecchini, Arch Biochem Biophys 1999 369 223 232 10.1006/abbi.1999.1359 10486141
53. Human 5-lipoxygenase contains an essential iron. MD Percival, J Biol Chem 1991 266 10058 10061 2037564
54. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. MM Bradford, Anal Biochem 1976 72 248 254 10.1016/0003-2697(76)90527-3 942051
55. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. H Schägger G von Jagow, Anal Biochem 1987 166 368 379 10.1016/0003-2697(87)90587-2 2449095
56. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. H Towbin T Staehelin J Gordon, Proc Natl Acad Sci USA 1979 76 4350 4354 388439 10.1073/pnas.76.9.4350