Distinct roles of the Salmonella enterica serovar typhimurium CyaY and YggX proteins in the biosynthesis and repair of iron-sulfur clusters

Infection and Immunity

Volumn 82, Issue 4, 2014, Pages 1390-1401

  Velayudhan, Jyoti ^a,b   Karlinsey, Joyce E ^a   Frawley, Elaine R ^a   Becker, Lynne A ^a,c   Nartea, Margaret ^a,d   Fang, Ferric C ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b AMGEN INC   (United States)

^c SEATTLE CANCER CARE ALLIANCE   (United States)

^d WEYERHAEUSER COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; CATALASE; CYAY PROTEIN; DEAMINASE; FRATAXIN; HYDROGEN PEROXIDE; HYDROLYASE; IRON SULFUR PROTEIN; PHOSPHOGLUCONATE DEHYDRATASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE I; SERINE DEAMINASE; UNCLASSIFIED DRUG; YGGX PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATOMIC EMISSION SPECTROMETRY; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM CULTURE; CELL DENSITY; COLONY FORMING UNIT; CONTROLLED STUDY; DNA SEQUENCE; EFFUSION; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME REACTIVATION; ESCHERICHIA COLI; FEMALE; GENE CLUSTER; GENE INACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC SUSCEPTIBILITY; GENOTYPE; HYPOTHESIS; IN VITRO STUDY; IN VIVO STUDY; IRON OVERLOAD; IRON TRANSPORT; MICROPLATE READER; MOUSE; NITROSATIVE STRESS; NONHUMAN; OPEN READING FRAME; ORTHOLOGY; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PHAGOCYTE; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN SYNTHESIS; SALMONELLA TYPHIMURIUM;

ACONITATE HYDRATASE; ANIMALS; BACTERIAL PROTEINS; CARBON-SULFUR LYASES; CATALASE; CELL PROLIFERATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; FEMALE; HYDROGEN PEROXIDE; IRON; IRON-SULFUR PROTEINS; MICE; MICE, INBRED C3H; MODELS, CHEMICAL; MUTATION; NAD; NITRIC OXIDE; OXIDATIVE STRESS; OXYGEN; PLASMIDS; REACTIVE OXYGEN SPECIES; SALMONELLA TYPHI; SULFUR; TYPHOID FEVER; VIRULENCE;

EID: 84896460464     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01022-13     Document Type: Article

References (52)

1. Johnson MK. 1998. Iron-sulfur proteins: new roles for old clusters. Curr. Opin. Chem. Biol. 2:173-181. http://dx.doi.org/10.1016/S1367-5931(98) 80058-6.
2. 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. U. S. A. 97:9009-9014. http://dx.doi.org/10.1073/pnas.160261497.
3. Chandramouli K, Johnson MK. 2006. HscA and HscB stimulate [2Fe-2S] cluster transfer from IscU to apoferredoxin in an ATP-dependent reaction. Biochemistry 45:11087-11095. http://dx.doi.org/10.1021/bi061237w.
4. Ding H, Yang J, Coleman LC, Yeung S. 2007. Distinct iron binding property of two putative iron donors for the iron-sulfur cluster assembly: IscA and the bacterial frataxin ortholog CyaY under physiological and oxidative stress conditions. J. Biol. Chem. 282:7997-8004. http://dx.doi.org/10.1074/jbc.M609665200.
5. 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. 283:14092-14099. http://dx.doi.org/10.1074/jbc.M709161200.
6. Outten FW, Djaman O, Storz G. 2004. A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol. Microbiol. 52:861-872. http://dx.doi.org/10.1111/j.1365-2958.2004.04025.x.
7. Keyer K, Imlay JA. 1997. Inactivation of dehydratase [4Fe-4S] clusters and disruption of iron homeostasis upon cell exposure to peroxynitrite. J. Biol. Chem. 272:27652-27659. http://dx.doi.org/10.1074/jbc.272.44.27652.
8. Flint DH, Tuminello JF, Emptage MH. 1993. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J. Biol. Chem. 268:22369-22376.
9. Varghese S, Tang Y, Imlay JA. 2003. Contrasting sensitivities of Escherichia coli aconitases A and B to oxidation and iron depletion. J. Bacteriol. 185:221-230. http://dx.doi.org/10.1128/JB.185.1.221-230.2003.
10. Djaman O, Outten FW, Imlay JA. 2004. Repair of oxidized iron-sulfur clusters in Escherichia coli. J. Biol. Chem. 279:44590-44599. http://dx.doi.org/10.1074/jbc.M406487200.
11. Gardner PR, Fridovich I. 1992. Inactivation-reactivation of aconitase in Escherichia coli. A sensitive measure of superoxide radical. J. Biol. Chem. 267:8757-8763.
12. Layer G, Ollagnier-de Choudens S, Sanakis Y, Fontecave M. 2006. Ironsulfur 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. 281:16256-16263. http://dx.doi.org/10.1074/jbc.M513569200.
13. Vivas E, Skovran E, Downs DM. 2006. Salmonella enterica strains lacking the frataxin homolog CyaY show defects in Fe-S cluster metabolism in vivo. J. Bacteriol. 188:1175-1179. http://dx.doi.org/10.1128/JB.188.3.1175-1179.2006.
14. Babcock M, de Silva D, Oaks R, Davis-Kaplan S, Jiralerspong S, Montermini L, Pandolfo M, Kaplan J. 1997. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 276: 1709-1712. http://dx.doi.org/10.1126/science.276.5319.1709.
15. Huynen MA, Snel B, Bork P, Gibson TJ. 2001. The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum. Mol. Genet. 10:2463-2468. http://dx.doi.org/10.1093/hmg/10.21.2463.
16. Bulteau AL, O'Neill HA, Kennedy MC, Ikeda-Saito M, Isaya G, Szweda LI. 2004. Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science 305:242-245. http://dx.doi.org/10.1126/science.1098991.
17. Bou-Abdallah F, Adinolfi S, Pastore A, Laue TM, Dennis Chasteen N. 2004. Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli. J. Mol. Biol. 341:605-615. http://dx.doi.org/10.1016/j.jmb.2004.05.072.
18. Nair M, Adinolfi S, Pastore C, Kelly G, Temussi P, Pastore A. 2004. Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites. Structure 12:2037-2048. http://dx.doi.org/10.1016/j.str.2004.08.012.
19. Yoon T, Cowan JA. 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. http://dx.doi.org/10.1021/ja027967i.
20. 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. 16:390-396. http://dx.doi.org/10.1038/nsmb.1579.
21. Iannuzzi C, Adinolfi S, Howes BD, Garcia-Serres R, Clemancey M, Latour JM, Smulevich G, Pastore A. 2011. The role of CyaY in iron sulfur cluster assembly on the E. coli IscU scaffold protein. PLoS One 6:e21992. http://dx.doi.org/10.1371/journal.pone.0021992.
22. 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:e1000354. http://dx.doi.org/10.1371/journal.pbio.1000354.
23. Bedekovics T, Gajdos GB, Kispal G, Isaya G. 2007. Partial conservation of functions between eukaryotic frataxin and the Escherichia coli frataxin homolog CyaY. FEMS Yeast Res. 7:1276-1284. http://dx.doi.org/10.1111/j.1567-1364.2007.00296.x.
24. Li DS, Ohshima K, Jiralerspong S, Bojanowski MW, Pandolfo M. 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. http://dx.doi.org/10.1016/S0014-5793(99)00896-0.
25. Thorgersen MP, Downs DM. 2009. Oxidative stress and disruption of labile iron generate specific auxotrophic requirements in Salmonella enterica. Microbiology 155:295-304. http://dx.doi.org/10.1099/mic.0.020727-0.
26. Skovran E, Downs DM. 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. http://dx.doi.org/10.1128/JB.185.1.98-106.2003.
27. Pomposiello PJ, Koutsolioutsou A, Carrasco D, Demple B. 2003. SoxRS-regulated expression and genetic analysis of the yggX gene of Escherichia coli. J. Bacteriol. 185:6624-6632. http://dx.doi.org/10.1128/JB.185.22.6624-6632.2003.
28. Cui Q, Thorgersen MP, Westler WM, Markley JL, Downs DM. 2006. Solution structure of YggX: a prokaryotic protein involved in Fe(II) trafficking. Proteins 62:578-586. http://dx.doi.org/10.1002/prot.20781.
29. Gralnick J, Downs D. 2001. Protection from superoxide damage associated with an increased level of the YggX protein in Salmonella enterica. Proc. Natl. Acad. Sci. U. S. A. 98:8030-8035. http://dx.doi.org/10.1073/pnas.151243198.
30. Skovran E, Lauhon CT, Downs DM. 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. http://dx.doi.org/10.1128/JB.186.22.7626-7634.2004.
31. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
32. Velayudhan J, Castor M, Richardson A, Main-Hester KL, Fang FC. 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. 63:1495-1507. http://dx.doi.org/10.1111/j.1365-2958.2007.05600.x.
33. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
34. Horton RM. 1995. PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes. Mol. Biotechnol. 3:93-99.
35. Berggren RE, Wunderlich A, Ziegler E, Schleicher M, Duke RC, Looney D, Fang FC. 1995. HIV gp120-specific cell-mediated immune responses in mice after oral immunization with recombinant Salmonella. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 10:489-495. http://dx.doi.org/10.1097/00042560-199512050-00001.
36. Woodmansee AN, Imlay JA. 2002. Quantitation of intracellular free iron by electron paramagnetic resonance spectroscopy. Methods Enzymol. 349:3-9. http://dx.doi.org/10.1016/S0076-6879(02)49316-0.
37. Visick JE, Clarke S. 1997. RpoS-and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J. Bacteriol. 179:4158-4163.
38. Aparicio O, Geisberg JV, Sekinger E, Yang A, Moqtaderi Z, Struhl K. 2005. Chromatin immunoprecipitation for determining the association of proteins with specific genomic sequences in vivo. Curr. Protoc. Mol. Biol. Chapter 21:Unit 21.3. http://dx.doi.org/10.1002/0471142727.mb2103s69.
39. Bridges KR, Cudkowicz A. 1984. Effect of iron chelators on the transferrin receptor in K562 cells. J. Biol. Chem. 259:12970-12977.
40. Gardner PR. 2002. Aconitase: sensitive target and measure of superoxide. Methods Enzymol. 349:9-23. http://dx.doi.org/10.1016/S0076-6879(02)49317-2.
41. Wong A, Yang J, Cavadini P, Gellera C, Lonnerdal B, Taroni F, Cortopassi G. 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. http://dx.doi.org/10.1093/hmg/8.3.425.
42. Keyer K, Imlay JA. 1996. Superoxide accelerates DNA damage by elevating free-iron levels. Proc. Natl. Acad. Sci. U. S. A. 93:13635-13640. http://dx.doi.org/10.1073/pnas.93.24.13635.
43. Frawley ER, Crouch ML, Bingham-Ramos LK, Robbins HF, Wang W, Wright GD, Fang FC. 2013. Iron and citrate export by a major facilitator superfamily pump regulates metabolism and stress resistance in Salmonella Typhimurium. Proc. Natl. Acad. Sci. U. S. A. 110:12054-12059. http://dx.doi.org/10.1073/pnas.1218274110.
44. Lu J, Yang J, Tan G, Ding H. 2008. Complementary roles of SufA and IscA in the biogenesis of iron-sulfur clusters in Escherichia coli. Biochem. J. 409:535-543. http://dx.doi.org/10.1042/BJ20071166.
45. Peekhaus N, Conway T. 1998. What's for dinner?: Entner-Doudoroff metabolism in Escherichia coli. J. Bacteriol. 180:3495-3502.
46. Gardner PR, Fridovich I. 1991. Superoxide sensitivity of the Escherichia coli 6-phosphogluconate dehydratase. J. Biol. Chem. 266:1478-1483.
47. Fang FC. 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2:820-832. http://dx.doi.org/10.1038/nrmicro1004.
48. Imlay JA. 2006. Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol. 59:1073-1082. http://dx.doi.org/10.1111/j.1365-2958.2006.05028.x.
49. Seaver LC, Imlay JA. 2001. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J. Bacteriol. 183:7182-7189. http://dx.doi.org/10.1128/JB.183.24.7182-7189.2001.
50. Bridwell-Rabb J, Iannuzzi C, Pastore A, Barondeau DP. 2012. Effector role reversal during evolution: the case of frataxin in Fe-S cluster biosynthesis. Biochemistry 51:2506-2514. http://dx.doi.org/10.1021/bi201628j.
51. Woodmansee AN, Imlay JA. 2003. A mechanism by which nitric oxide accelerates the rate of oxidative DNA damage in Escherichia coli. Mol. Microbiol. 49:11-22. http://dx.doi.org/10.1046/j.1365-2958.2003.03530.x.
52. Justino MC, Almeida CC, Teixeira M, Saraiva LM. 2007. Escherichia coli di-iron YtfE protein is necessary for the repair of stress-damaged ironsulfur clusters. J. Biol. Chem. 282:10352-10359. http://dx.doi.org/10.1074/jbc.M610656200.