Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes

FEMS Microbiology Reviews

Volumn 30, Issue 6, 2006, Pages 825-840

  Kessler, Dorothea ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cystine lyase; Desulfurase; Persulfide; Prokaryotic sulfur metabolism; Sulfurtransferase; Ubiquitin

Indexed keywords

BIOTIN; COENZYME A; CYSTEINE; IRON SULFUR PROTEIN; METHIONINE; MOLYBDOPTERIN; PROTEIN; PROTEIN ISCS; PROTEIN SUFS; SULFIDE; SULFUR; THIAMINE; THIOCTIC ACID; THIOL; TRANSFER RNA; UNCLASSIFIED DRUG;

BIOCATALYST; BIOSYNTHESIS; CHEMICAL ANALYSIS; CHEMICAL REACTION; ENZYME ACTIVATION; ENZYME DEGRADATION; ESCHERICHIA COLI; NONHUMAN; PROKARYOTE; REVIEW;

BACTERIAL PROTEINS; BINDING SITES; COENZYMES; CYSTEINE; ENZYME PRECURSORS; LYASES; MODELS, MOLECULAR; NITROGEN; NITROGEN FIXATION; PROKARYOTIC CELLS; PYRIDOXAL PHOSPHATE; SULFUR; SULFUR COMPOUNDS; THIAZOLES; UBIQUITIN; VITAMINS;

PROKARYOTA;

EID: 33750083296     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2006.00036.x     Document Type: Review

References (108)

1. Adams H, Teertstra W, Koster M & Tommassen J (2002) PspE (phage-shock protein E) of Escherichia coli is a rhodanese. FEBS Lett 518: 173-176.
2. Ali V, Shigeta Y, Tokumoto U, Takahashi Y & Nozaki T (2004) An intestinal parasitic protist, Entamoeba histolytica, possesses a non-redundant nitrogen fixation-like system for iron-sulfur cluster assembly under anaerobic conditions. J Biol Chem 279: 16863-16874.
3. Bartsch RG, Newton GL, Sherrill C & Fahey RC (1996) Glutathione amide and its perthiol in anaerobic sulfur bacteria. J Bacteriol 178: 4742-4746.
4. Begley TP, Downs DM, Ealick SE et al. (1999) Thiamin biosynthesis in prokaryotes. Arch Microbiol 171: 293-300.
5. Behshad E, Parkin SE & Bollinger JM (2004) Mechanism of cysteine desulfurase Slr0387 from Synechocystis sp. PCC 6803: kinetic analysis for cleavage of the persulfide intermediate by chemical reductants. Biochemistry 43: 12220-12226.
6. Beinert H (2000a) A tribute to sulfur. Eur J Biochem 267: 5657-5664.
7. Beinert H (2000b) Iron-sulfur proteins: ancient structures, still full of surprises. J Biol Inorg Chem 5: 2-15.
8. Bordo D & Bork P (2002) The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations. EMBO Reports 3: 741-746.
9. Burns KE, Baumgart S, Dorrestein PC, Zhai H, McLafferty FW & Begley TP (2005) Reconstitution of a new cysteine biosynthetic pathway in Mycobacterium tuberculosis. J Am Chem Soc 127: 11602-11603.
10. Cavallini D, De Marco C, Mondovi B & Mori BG (1960) The cleavage of cystine by cystathionase and the transulfuration of hypotaurine. Enzymologia 22: 161-173.
11. Cavallini D, Federici G & Barboni E (1970) Interaction of proteins with sulfide. Eur J Biochem 14: 169-174.
12. Cerletti P (1986) Seeking a better job for an under-employed enzyme: rhodanese. Trends Biochem Sci 11: 369-372.
13. Cianci M, Gliubich F, Zanotti G & Berni R (2000) Specific interaction of lipoate at the active site of rhodanese. Biochim Biophys Acta 1481: 103-108.
14. Cicchillo RM & Booker SJ (2005) Mechanistic investigations of lipoic acid biosynthesis in Escherichia coli: both sulfur atoms in lipoic acid are contributed by the same lipoyl synthase polypeptide. J Am Chem Soc 127: 2860-2861.
15. Cicchillo RM, Iwig DF, Jones AD, Nesbitt NM, Baleanu-Gogonea C, Souder MG, Tu L & Booker SJ (2004) Lipoyl synthase requires two equivalents of S-adenosyl-L-methionine to synthesize one equivalent of lipoic acid. Biochemistry 43: 6378-6386.
16. Clausen T, Kaiser JT, Steegborn C, Huber R & Kessler D (2000) Crystal structure of the cystine C-S lyase from Synechocystis: Stabilization of cysteine persulfide for FeS cluster biosynthesis. Proc Natl Acad Sci USA 97: 3856-3861.
17. Cupp-Vickery JR, Urbina H & Vickery LE (2003) Crystal structure of IscS, a cysteine desulfurase from Escherichia coli. J Mol Biol 330: 1049-1059.
18. Delavier-Klutchko C & Flavin M (1965) Role of a bacterial cystathionine β-cleavage enzyme in disulfide decomposition. Biochim Biophys Acta 99: 375-377.
19. Ding H, Harrison K & Lu J (2005) Thioredoxin reductase system mediates iron binding in IscA and iron delivery for the ironsulfur cluster assembly in IscU. J Biol Chem 280: 30432-30437.
20. Donadio S, Shafiee A & Hutchinson CR (1990) Disruption of a rhodaneselike gene results in cysteine auxotrophy in Saccharopolyspora erythraea. J Bacteriol 172: 350-360.
21. Ellis KES, Clough B, Saldanha JW & Wilson RJM (2001) Nifs and Sufs in malaria. Mol Microbiol 41: 973-981.
22. Everett SA & Wardman P (1995) Perthiols as antioxidants: radical-scavenging and prooxidative mechanisms. Meth Enzymol 251: 55-69.
23. Flavin M (1962) Microbial transsulfuration: the mechanism of an enzymatic disulfide elimination reaction. J Biol Chem 237: 768-777.
24. Flint DH, Tuminello JF & Miller TJ (1996) Studies on the synthesis of the Fe-S cluster of dihydroxy-acid dehydratase in Escherichia coli crude extract. Isolation of O-acetylserine sulfhydrylases A and B and β-cystathionase based on their ability to mobilize sulfur from cysteine and to participate in Fe-S cluster synthesis. J Biol Chem 271: 16053-16067.
25. Florentin D, Tse Sum Bui B, Marquet A, Ohshiro T & Izumi Y (1994) On the mechanism of biotin synthase of Bacillus sphaericus. CR Acad Sci Paris Life Sci 317: 485-488.
26. Fontecave M, Ollagnier-de-Choudens S, Py B & Barras F (2005) Mechanisms of iron-sulfur cluster assembly: the SUF machinery. J Biol Inorg Chem 10: 713-721.
27. Fujii T, Maeda M, Mihara H, Kurihara T, Esaki N & Hata Y (2000) Structure of a NifS homologue: X-ray structure analysis of CsdB, an Escherichia coli counterpart of mammalian selenocysteine lyase. Biochemistry 39: 1263-1273.
28. Gentry-Weeks CR, Keith JM & Thompson J (1993) Toxicity of Bordetella avium β-cystathionase toward MC3T3-E1 osteogenic cells. J Biol Chem 268: 7298-7314.
29. Goldsmith-Fischman S, Kuzin A, Edstrom WC, Benach J, Shastry R, Xiao R, Acton TB, Honig B, Montelione GT & Hunt JF (2004) The SufE sulfur-acceptor protein contains a conserved core structure that mediates interdomain interactions in a variety of redox protein complexes. J Mol Biol 344: 549-565.
30. Graham DE & White RH (2002) Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics. Nat Prod Rep 19: 133-147.
31. Hand CE & Honek JF (2005) Biological chemistry of naturally occurring thiols of microbial and marine origin. J Nat Prod 68: 293-308.
32. Hille R (2002) Molybdenum and tungsten in biology. Trends Biochem Sci 27: 360-367.
33. Huet G, Daffé M & Saves I (2005) Identification of the Mycobacterium tuberculosis SUF machinery as the exclusive mycobacterial system of [Fe-S] cluster assembly: evidence for its implication in the pathogen's survival. J Bacteriol 187: 6137-6146.
34. Ikeuchi Y, Shigi N, Kato J, Nishimura A & Suzuki T (2006) Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol Cell 21: 97-108.
35. Jarabak R & Westley J (1980) 3-Mercaptopyruvate sulfurtransferase: rapid equilibrium-ordered mechanism with cyanide as the acceptor substrate. Biochemistry 19: 900-904.
36. Jarrett JT (2005) The novel structure and chemistry of iron-sulfur clusters in the adenosylmethionine-dependent radical enzyme biotin synthase. Arch Biochem Biophys 433: 312-321.
37. Johnson D, Dean DR, Smith AD & Johnson MK (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74: 247-281.
38. Kaiser JT, Clausen T, Bourenkow GP, Bartunik H-D, Steinbacher S & Huber R (2000) Crystal structure of a NifS-like protein from Thermotoga maritima: implications for iron sulphur cluster assembly. J Mol Biol 297: 451-464.
39. Kaiser JT, Bruno S, Clausen T, Huber R, Schiaretti F, Mozzarelli A & Kessler D (2003) Snapshots of the cystine lyase C-DES during catalysis. Studies in solution and in the crystalline state. J Biol Chem 278: 357-365.
40. Kambampati R & Lauhon CT (2003) MnmA and IscS are required for in vitro 2-thiouridine biosynthesis in Escherichia coli. Biochemistry 42: 1109-1117.
41. Kessler D (2004) Slr0077 of Synechocystis has cysteine desulfurase as well as cystine lyase activity. Biochem Biophys Res Commun 320: 571-577.
42. Kleerebezem M, Crielaard W & Tommassen J (1996) Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J 15: 162-171.
43. Krupka HI, Huber R, Holt SC & Clausen T (2000) Crystal structure of cystalysin from Treponema denticola: a pyridoxal 5′-phosphate-dependent protein acting as a haemolytic enzyme. EMBO J 19: 3168-3178.
44. Lake MW, Wuebbens MM, Rajagopalan KV & Schindelin H (2001) Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB-MoaD complex. Nature 414: 325-329.
45. Lang T & Kessler D (1999) Evidence for cysteine persulfide as reaction product of L-cyst(e)ine C-S-lyase (C-DES) from Synechocystis. Analyses using cystine analogues and recombinant C-DES. J Biol Chem 274: 189-195.
46. Lauhon CT (2002) Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli. J Bacteriol 184: 6820-6829.
47. Lauhon C & Kambampati R (2000) The iscS gene in Escherichia coli is required for the biosynthesis of 4-thiouridine, thiamin, and NAD. J Biol Chem 275: 20096-20103.
48. Lauhon CT, Skovran E, Urbina HD, Downs DM & Vickery LE (2004) Substitutions in an active site loop of Escherichia coli IscS result in specific defects in Fe-S cluster and thionucleoside biosynthesis in vivo. J Biol Chem 279: 19551-19558.
49. Lee J-H, Yeo W-S & Roe J-H (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: 1745-1755.
50. Leibrecht I & Kessler D (1997) A novel L-cysteine/cystine C-S lyase directing[2Fe-2S] cluster formation of Synechocystis ferredoxin. J Biol Chem 272: 10442-10447.
51. Leimkühler S & Rajagopalan KV (2001) A sulfurtransferase is required in the transfer of cysteine sulfur in the in vitro synthesis of molybdopterin from precursor Z in Escherichia coli. J Biol Chem 276: 22024-22031.
52. Leipuviene R, Qian Q & Bjork GR (2004) Formation of thiolated nucleosides present in tRNA from Salmonella enterica serovar Typhimurium occurs in two principally distinct pathways. J Bacteriol 186: 758-766.
53. 4-dechlorination agent pyridine-2,6-bis(thiocarboxylic acid). Environ Microbiol 2: 407-416.
54. Lill R & M̈uhlenhoff U (2005) Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30: 133-141.
55. Lima CD (2002) Analysis of the E. coli NifS CsdB protein at 2.0 Å reveals the structural basis for perselenide and persulfide intermediate formation. J Mol Biol 315: 1199-1208.
56. Loiseau L, Ollagnier-de-Choudens S, Nachin L, Fontecave M & Barras F (2003) Biogenesis of Fe-S cluster by the bacterial Suf system. SufS and SufE form a new type of cysteine desulfurase. J Biol Chem 278: 38352-38359.
57. Loiseau L, Ollagnier-de-Choudens S, Lascoux D, Forest E, Fontecave M & Barras F (2005) Analysis of the heteromeric CsdA-CsdE cysteine desulfurase, assisting Fe-S cluster biogenesis in Escherichia coli. J Biol Chem 280: 26760-26769.
58. Lotierzo M, Tse Sum Bui B, Florentin D, Escalettes F & Marquet A (2005) Biotin synthase mechanism: an overview. Biochem Soc Trans 33: 820-823.
59. Matthies A, Rajagopalan KV, Mendel RR & Leimkühler S (2004) Evidence for the physiological role of a rhodanese-like protein for the biosynthesis of the molybdenum cofactor in humans. Proc Natl Acad Sci USA 101: 5946-5951.
60. Matthijs S, Baysse C, Koedam N et al. (2004) The Pseudomonas siderophore quinolobactin is synthesized from xanthurenic acid, an intermediate of the kynurenine pathway. Mol Microbiol 52: 371-384.
61. Mihara H, Kurihara T, Yoshimura T, Soda K & Esaki N (1997) Cysteine sulfinate desulfinase, a NIFS-like protein of Escherichia coli with selenocysteine lyase and cysteine desulfurase activities. Gene cloning, purification, and characterization of a novel pyridoxal enzyme. J Biol Chem 272: 22417-22424.
62. Mihara H, Maeda M, Fujii T, Kurihara T, Hata Y & Esaki N (1999) A nifS-like gene, csdB, encodes an Escherichia coli counterpart of mammalian selenocysteine lyase. Gene cloning, purification, characterization and preliminary X-ray crystallographic studies. J Biol Chem 274: 14768-14772.
63. Miller JR, Busby RW, Jordan SW, Cheek J, Henshaw TF, Ashley GW, Broderick JB, Cronan JE Jr & Marletta MA (2000) Escherichia coli LipA is a lipoyl synthase: "in vitro biosynthesis of lipoylated pyruvate dehydrogenase complex from octanoylacyl carrier protein. Biochemistry 39: 15166-15178.
64. Newton GL & Javor B (1985) γ-Glutamylcysteine and thiosulfate are the major low-molecular weight thiols in Halobacteria. J Bacteriol 161: 438-441.
65. Ollagnier-de-Choudens S, Sanakis Y, Hewitson KS, Roach P, Baldwin JE, Münck E & Fontecave M (2000) Iron-sulfur center of biotin synthase and lipoate synthase. Biochemistry 39: 4165-4173.
66. Ollagnier-de-Choudens S, Lascoux D, Loiseau L, Barras F, Forest E & Fontecave M (2003) Mechanistic studies of the SufS-SufE cysteine desulfurase: evidence for sulfur transfer from SufS to SufE. FEBS Lett 555: 263-267.
67. Olson JW, Agar JN, Johnson MK & Maier RJ (2000) Characterization of the NifU and NifS Fe-S cluster formation proteins essential for viability in Helicobacter pylori. Biochemistry 39: 16213-16219.
68. Outten FW, Wood MJ, Muñoz M & Storz G (2003) The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe-S cluster assembly in Escherichia coli. J Biol Chem 278: 45713-45719.
69. 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.
70. Palenchar PM, Buck CJ, Cheng H, Larson TJ & Mueller EG (2000) Evidence that ThiI, an enzyme shared between thiamin and 4-thiouridine biosynthesis, may be a sulfurtransferase that proceeds through a persulfide intermediate. J Biol Chem 275: 8283-8286.
71. Park J-H, Dorrestein PC, Zhai H, Kinsland C, McLafferty FW & Begley TP (2003) Biosynthesis of the thiazole moiety of thiamin pyrophosphate (vitamin B1). Biochemistry 42: 12430-12438.
72. Park S & Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J Bacteriol 185: 1942-1950.
73. Patzer SI & Hantke K (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: 3307-3309.
74. Pierrel F, Douki T, Fontecave M & Atta M (2004) MiaB protein is a bifunctional radical-S-adenosylmethionine enzyme involved in thiolation and methylation of tRNA. J Biol Chem 279: 47555-47563.
75. Rajagopalan KV (1997) Biosynthesis and processing of the molybdenum cofactors. Biochem Soc Trans 25: 757-761.
76. Ravot G, Casalot L, Ollivier B, Loison G & Magot M (2005) rdlA, a new gene encoding a rhodanese-like protein in Halanerobium congolense and other thiosulfate-reducing anaerobes. Res Microbiol 156: 1031-1038.
77. Ray WK, Zeng G, Potters MB, Mansuri AM & Larson TJ (2000) Characterization of a 12-kilodalton rhodanese encoded by glpE of Escherichia coli and its interaction with thioredoxin. J Bacteriol 182: 2277-2284.
78. Rohwerder T & Sand W (2003) The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp.. Microbiology 149: 1699-1709.
79. Sauerwald A, Zhu W, Major TA, Roy H, Palioura S, Jahn D, Whitman WB, Yates JR III, Ibba M & Söll D (2005) RNA-dependent cysteine biosynthesis in Archaea. Science 307: 1969-1972.
80. Schmidt A & Jäger K (1992) Open questions about sulfur metabolism in plants. Annu Rev Plant Physiol Plant Mol Biol 43: 325-349.
81. Settembre EC, Dorrestein PC, Zhai H, Chatterjee A, McLafferty FW, Begley TP & Ealick SE (2004) Thiamin biosynthesis in Bacillus subtilis: structure of the thiazole synthase/sulfur carrier protein complex. Biochemistry 43: 11647-11657.
82. Skovran E & Downs DM (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.
83. Smith AD, Jameson GNL, DosSantos PC, Agar JN, Naik S, Krebs C, Frazzon J, Dean DR, Huynh BH & Johnson MK (2005) NifS-mediated assembly of[4Fe-4S] clusters in the N- and C-terminal domains of the NifU scaffold protein. Biochemistry 44: 12955-12969.
84. Spallarossa A, Forlani F, Carpen A, Armirotti A, Pagani S, Bolognesi M & Bordo D (2004) The 'rhodanese' fold and catalytic mechanism of 3-mercaptopyruvate sulfurtransferase: crystal structure of SseA from Escherichia coli. J Mol Biol 335: 583-593.
85. Steegborn C, Clausen T, Sondermann P, Jacob U, Worbs M, Marinkovic S, Huber R & Wahl MC (1999) Kinetics and inhibition of recombinant human cystathionine γ-lyase. Toward the rational control of transsulfuration. J Biol Chem 274: 12675-12684.
86. Streit WR & Entcheva P (2003) Biotin in microbes, the genes involved in its biosynthesis, its biochemical role and perspectives for biotechnological production. Appl Microbiol Biotechnol 61: 21-31.
87. Tachezy J, Sánchez LB & Müller M (2001) Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol Biol Evol 18: 1919-1928.
88. Takahashi Y & Tokumoto U (2002) A third bacterial system for the assembly of iron-sulfur clusters with homologs in Archaea and plastids. J Biol Chem 277: 28380-28383.
89. Taylor SV, Kelleher NL, Kinsland C, Chiu H-J, Costello CA, Backstrom AD, McLafferty FW & Begley TP (1998) Thiamin biosynthesis in Escherichia coli. Identification of ThiS thiocarboxylate as the immediate sulfur donor in the thiazole formation. J Biol Chem 273: 16555-16560.
90. Tchong S, Xu H & White RH (2005) L-Cysteine desulfidase: an [4Fe-4S] enzyme isolated from Methanocaldococcus jannaschii that catalyzes the breakdown of L-cysteine into pyruvate, ammonia and sulfide. Biochemistry 44: 1659-1670.
91. Theissen U, Hoffmeister M, Grieshaber M & Martin W (2003) Single eubacterial origin of eukaryotic sulfide: uinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol Biol Evol 20: 1564-1574.
92. Tirupati B, Vey JL, Drennan CL & Bollinger JM (2004) Kinetic and structural characterization of Slr0077/SufS, the essential cysteine desulfurase from Synechocystis sp. PCC 6803. Biochemistry 43: 12210-12219.
93. Toohey JI (1989) Sulphane sulphur in biological systems: a possible regulatory role. Biochem J 264: 625-632.
94. Tovar J, León-Avila G, Sánchez LB, Sutak R, Tachezy J, van der Giezen M, Hernández M, Müller M & Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in ironsulphur protein maturation. Nature 426: 172-176.
95. Ugulava NB, Sacanell CJ & Jarrett JT (2001) Spectroscopic changes during a single turnover of biotin synthase: destruction of a [2Fe-2S] cluster accompanies sulfur insertion. Biochemistry 40: 8352-8358.
96. Vamvakas S, Berthold K, Dekant W & Henschler D (1988) Bacterial cysteine conjugate beta-lyase and the metabolism of cysteine-S-conjugates: structural requirements for the cleavage of S-conjugates and the formation of reactive intermediates. Chem Biol Interact 65: 59-71.
97. 2S be the third endogenous gaseous transmitter? FASEB J 16: 1792-1798.
98. Webb E, Claas K & Downs DM (1997) Characterization of thiI, a new gene involved in thiazole biosynthesis in Salmonella typhimurium. J Bacteriol 179: 4399-4402.
99. Wolfe MD, Ahmed F, Lacourciere GM, Lauhon CT, Stadtman TC & Larson TJ (2004) Functional diversity of the rhodanese homology domain: the Escherichia coli ybbB gene encodes a selenophosphate-dependent tRNA 2-selenouridine synthase. J Biol Chem 279: 1801-1809.
100. Wood JL (1987) Sulfane sulfur. Meth Enzymol 143: 25-29.
101. Wuebbens MM & Rajagopalan KV (2003) Mechanistic and mutational studies of Escherichia coli molybdopterin synthase clarify the final step of molybdopterin biosynthesis. J Biol Chem 278: 14523-14532.
102. Xi J, Ge Y, Kinsland C, McLafferty FW & Begley TP (2001) Biosynthesis of the thiazole moiety of thiamin in Escherichia coli: identification of an acyldisulfide-linked protein-protein conjugate that is functionally analogous to the ubiquitin/E1 complex. Proc Natl Acad Sci USA 98: 8513-8518.
103. Zdych E, Peist R, Reidl J & Boos W (1995) MalY of Escherichia coli is an enzyme with the activity of a βC-S lyase (cystathionase). J Bacteriol 177: 5035-5039.
104. Zhao S, Miller JR, Jiang Y, Marletta MA & Cronan JE Jr (2003) Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem Biol 10: 1293-1302.
105. Zheng L, White RH, Cash VL, Jack RF & Dean DR (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc Natl Acad Sci USA 90: 2754-2758.
106. Zheng L, White RH, Cash VL & Dean DR (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33: 4714-4720.
107. Zheng L, Cash VL, Flint DH & Dean DR (1998) Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273: 13264-13272.
108. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA & Storz G (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562-4570.