Salmonella enterica strains lacking the frataxin homolog cyaY show defects in Fe-S cluster metabolism in vivo

Journal of Bacteriology

Volumn 188, Issue 3, 2006, Pages 1175-1179

  Vivas, E ^a   Skovran, E ^a,b   Downs, D M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRATAXIN; IRON SULFUR PROTEIN; THIAMINE;

ARTICLE; AUXOTROPHY; BACTERIAL GENE; CYAY GENE; GENE LOCUS; GENE MUTATION; GENOTYPE; IRON METABOLISM; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; STRAIN DIFFERENCE;

BACTERIAL PROTEINS; IRON-BINDING PROTEINS; IRON-SULFUR PROTEINS; SALMONELLA ENTERICA;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA;

EID: 31344438920     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.3.1175-1179.2006     Document Type: Article

References (40)

1. Babcock, M., D. de Silva, R. Oaks, S. Davis-Kaplan, S. Jiralerspong, L. Montermini, M. Pandolfo, and J. Kaplan. 1997. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 276:1709-1712.
2. Bou-Abdallah, F., S. Adinolfi, A. Pastore, T. M. Laue, and N. D. Chasteen. 2004. Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli. J. Mol. Biol. 341:605-615.
3. Braun, V. 2003. Iron uptake in Escherichia coli Front. Biosci. 8:s1409-s1421.
4. Bulteau, A. L., H. A. O'Neill, M. C. Kennedy, M. Ikeda-Saito, G. Isaya, and L. I. Szweda. 2004. Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science 305:242-245.
5. Campuzano, V., L. Montermini, Y. Lutz, L. Cova, C. Hindelang, S. Jiralerspong, Y. Trottier, S. J. Kish, B. Faucheux, P. Trouillas, F. J. Authier, A. Durr, J. L. Mandel, A. Vescovi, M. Pandolfo, and M. Koenig. 1997. Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum. Mol. Genet. 6:1771-1780.
6. Campuzano, V., L. Montermini, M. D. Molto, L. Pianese, M. Cossee, F. Cavalcanti, E. Monros, F. Rodius, F. Duclos, A. Monticelli, F. Zara, J. Canizares, H. Koutnikova, S. I. Bidichandani, C. Gellera, A. Brice, P. Trouillas, G. De Michele, A. Filla, R. De Frutos, F. Palau, P. I. Patel, S. Di Donato, J. L. Mandel, S. Cocozza, M. Koenig, and M. Pandolfo. 1996. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271:1423-1427.
7. Chamberlain, S., M. Koenig, A. Richter, F. Palau, and M. Pandolfo. 1993. Molecular analysis of the Friedreich's ataxia locus. Adv. Neurol. 61:193-204.
8. Chamberlain, S., J. Shaw, A. Rowland, J. Wallis, S. South, Y. Nakamura, A. von Gabain, M. Farrall, and R. Williamson. 1988. Mapping of mutation causing Friedreich's ataxia to human chromosome 9. Nature 334:248-250.
9. Claas, K., S. Weber, and D. M. Downs. 2000. Lesions in the nuo operon, encoding NADH dehydrogenase complex I, prevent PurF-independent thiamine synthesis and reduce flux through the oxidative pentose phosphate pathway in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182:228-232.
10. Cui, Q., M. P. Thorgersen, W. M. Westler, J. L. Markley, and D. M. Downs. Solution structure of YggX: a prokaryotic protein involved in Fe(II) trafficking. Proteins, in press.
11. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
12. Duby, G., F. Foury, A. Ramazzotti, J. Herrmann, and T. Lutz. 2002. A non-essential function for yeast frataxin in iron-sulfur cluster assembly. Hum. Mol. Genet. 11:2635-2643.
13. Falk-Krzesinski, H. J., and A. J. Wolfe. 1998. Genetic analysis of the nuo locus, which encodes the proton-translocating NADH dehydrogenase in Escherichia coli. J. Bacteriol. 180:1174-1184.
14. Flint, D. H. 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. 271:16068-6074.
15. Flint, D. H., and R. M. Allen. 1996. Iron-sulfur proteins with nonredox functions. Chem. Rev. 96:2315-2334.
16. Foury, F. 1999. Low iron concentration and aconitase deficiency in a yeast frataxin homologue deficient strain. FEBS Lett. 456:281-284.
17. Frazzon, J., and D. R. Dean. 2003. Formation of iron-sulfur clusters in bacteria: an emerging field in bioinorganic chemistry. Curr. Opin. Chem. Biol. 7:166-173.
18. Friedrich, T., and B. Böttcher. 2004. The gross structure of the respiratory complex I: a Lego system. Biochim. Biophys. Acta 1608:1-9.
19. Gralnick, J., E. Webb, B. Beck, and D. Downs. 2000. Lesions in gshA (encoding γ-L-glutamyl-L-cysteine synthetase) prevent aerobic synthesis of thiamine in Salmonella enterica serovar typhimurium LT2. J. Bacteriol. 182:5180-5187.
20. Gralnick, J. A., and D. M. Downs. 2003. The YggX protein of Salmonella enterica is involved in Fe(II) trafficking and minimizes the DNA damage caused by hydroxyl radicals: residue CYS-7 is essential for YggX function. J. Biol. Chem. 278:20708-20715.
21. Hinchliffe, P., and L. A. Sazanov. 2005. Organization of iron-sulfur clusters in respiratory complex I. Science 309:771-774.
22. Huynen, M. A., B. Snel, P. Bork, and T. J. Gibson. 2001. The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum. Mol. Genet. 10:2463-2468.
23. Lezhneva, L., K. Amann, and J. Meurer. 2004. The universally conserved HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J. 37:174-185.
24. Li, D. S., K. Ohshima, S. Jiralerspong, M. W. Bojanowski, and M. Pandolfo. 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.
25. Mansy, S. S., and J. A. Cowan. 2004. Iron-sulfur cluster biosynthesis: toward an understanding of cellular machinery and molecular mechanism. Acc. Chem. Res. 37:719-725.
26. Nair, M., S. Adinolfi, C. Pastore, G. Kelly, P. Temussi, and A. Pastore. 2004. Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites. Structure (Cambridge) 12:2037-2048.
27. Pandolfo, M. 2002. The molecular basis of Friedreich ataxia. Adv. Exp. Med. Biol. 516:99-118.
28. Park, S., O. Gakh, H. A. O'Neill, A. Mangravita, H. Nichol, G. C. Ferreira, and G. Isaya. 2003. Yeast frataxin sequentially chaperones and stores iron by coupling protein assembly with iron oxidation. J. Biol. Chem. 278:31340-31351.
29. Petersen, L. A., and D. M. Downs. 1997. Identification and characterization of an operon in Salmonella typhimurium involved in thiamine biosynthesis. J. Bacteriol. 179:4894-4900.
30. Prub, B. M., J. M. Nelms, C. Park, and A. J. Wolfe. 1994. Mutations in NADH:ubiquinone oxidoreductase of Escherichia coli affect growth on mixed amino acids. J. Bacteriol. 176:2143-2150.
31. Roy, A., N. Solodovnikova, T. Nicholson, W. Antholine, and W. E. Walden. 2003. A novel eukaryotic factor for cytosolic Fe-S cluster assembly. EMBO J. 22:4826-4835.
32. Schwartz, C. J., O. Djaman, J. A. Imlay, and P. J. Kiley. 2000. The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. Proc. Natl. Acad. Sci. USA 97:9009-9014.
33. Skovran, E., and D. M. Downs. 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.
34. Skovran, E., and D. M. Downs. 2000. Metabolic defects caused by mutations in the isc gene cluster in Salmonella enterica serovar Typhimurium: implications for thiamine synthesis. J. Bacteriol. 182:3896-3903.
35. Skovran, E., C. T. Lauhon, and D. M. Downs. 2004. Lack of YggX results in chronic oxidative stress and uncovers subtle defects in Fe-S cluster metabolism in Salmonella enterica. J. Bacteriol. 186:7626-7634.
36. Wong, A., J. Yang, P. Cavadini, C. Gellera, B. Lonnerdal, F. Taroni, and G. Cortopassi. 1999. The Friedreich's ataxia mutation confers cellular sensitivity to oxidant stress which is rescued by chelators of iron and calcium and inhibitors of apoptosis. Hum. Mol. Genet. 8:425-430.
37. Yoon, T., and J. A. Cowan. 2004. Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J. Biol. Chem. 279:25943-25946.
38. Yoon, T., and J. A. Cowan. 2003. Iron-sulfur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins. J. Am. Chem. Soc. 125:6078-6084.
39. Zambrano, M. M., and R. Kolter. 1993. Escherichia coli mutants lacking NADH dehydrogenase I have a competitive disadvantage in stationary phase. J. Bacteriol. 175:5642-5647.
40. Zheng, L., V. L. Cash, D. H. Flint, and D. R. Dean. 1998. Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J. Biol. Chem. 273:13264-13272.