Biochemical and Structural Characterization of a Novel Family of Cystathionine β-Synthase Domain Proteins Fused to a Zn Ribbon-Like Domain

Journal of Molecular Biology

Volumn 375, Issue 1, 2008, Pages 301-315

  Proudfoot, Michael ^a   Sanders, Stephen A ^a   Singer, Alex ^a   Zhang, Rongguang ^b   Brown, Greg ^a   Binkowski, Andrew ^b   Xu, Linda ^a   Lukin, Jonathan A ^c   Murzin, Alexey G ^d   Joachimiak, Andrzej ^b   Arrowsmith, Cheryl H ^c   Edwards, Aled M ^a   Savchenko, Alexei V ^a   Yakunin, Alexander F ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b Biosciences Division   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d MRC CENTRE FOR PROTEIN ENGINEERING   (United Kingdom)

Author keywords

crystal structure; cystathionine beta synthase domain; electron transfer; rubredoxin; zinc ribbon domain

Indexed keywords

ASCORBIC ACID; BACTERIAL PROTEIN; CYSTATHIONINE BETA SYNTHASE; CYTOCHROME C; DITHIONITE; IRON; MERCURY; PROTEIN KTI11; PROTEIN TA0289; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RUBREDOXIN; UNCLASSIFIED DRUG; ZINC;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DIMERIZATION; ELECTRON TRANSPORT; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS;

EQUIDAE; ESCHERICHIA COLI; PYROCOCCUS FURIOSUS; PYROCOCCUS HORIKOSHII; SACCHAROMYCES CEREVISIAE; THERMOPLASMA ACIDOPHILUM; THERMOPLASMA VOLCANIUM;

EID: 36448989752     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.10.060     Document Type: Article

References (74)

1. Bateman A. The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem. Sci. 22 (1997) 12-13
2. Ignoul S., and Eggermont J. CBS domains: structure, function, and pathology in human proteins. Am. J. Physiol.: Cell Physiol. 289 (2005) C1369-C1378
3. Scott J.W., Hawley S.A., Green K.A., Anis M., Stewart G., Scullion G.A., et al. CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J. Clin. Invest. 113 (2004) 274-284
4. Bennetts B., Rychkov G.Y., Ng H.L., Morton C.J., Stapleton D., Parker M.W., and Cromer B.A. Cytoplasmic ATP-sensing domains regulate gating of skeletal muscle ClC-1 chloride channels. J. Biol. Chem. 280 (2005) 32452-32458
5. Biemans-Oldehinkel E., Mahmood N.A., and Poolman B. A sensor for intracellular ionic strength. Proc. Natl Acad. Sci. USA 103 (2006) 10624-10629
6. Miller M.D., Schwarzenbacher R., von Delft F., Abdubek P., Ambing E., Biorac T., et al. Crystal structure of a tandem cystathionine-beta-synthase (CBS) domain protein (TM0935) from Thermotoga maritima at 1.87 Å resolution. Proteins 57 (2004) 213-217
7. Meyer S., and Dutzler R. Crystal structure of the cytoplasmic domain of the chloride channel ClC-0. Structure 14 (2006) 299-307
8. Jhee K.H., McPhie P., and Miles E.W. Domain architecture of the heme-independent yeast cystathionine beta-synthase provides insights into mechanisms of catalysis and regulation. Biochemistry 39 (2000) 10548-10556
9. Zhang R., Evans G., Rotella F.J., Westbrook E.M., Beno D., Huberman E., et al. Characteristics and crystal structure of bacterial inosine-5′-monophosphate dehydrogenase. Biochemistry 38 (1999) 4691-4700
10. Rudolph M.J., Amodeo G.A., Iram S.H., Hong S.P., Pirino G., Carlson M., and Tong L. Structure of the Bateman2 domain of yeast Snf4: dimeric association and relevance for AMP binding. Structure 15 (2007) 65-74
11. Meyer S., Savaresi S., Forster I.C., and Dutzler R. Nucleotide recognition by the cytoplasmic domain of the human chloride transporter ClC-5. Nat. Struct. Mol. Biol. 14 (2007) 60-67
12. Day P., Sharff A., Parra L., Cleasby A., Williams M., Horer S., et al. Structure of a CBS-domain pair from the regulatory gamma1 subunit of human AMPK in complex with AMP and ZMP. Acta Crystallogr., Sect. D: Biol. Crystallogr. 63 (2007) 587-596
13. Townley R., and Shapiro L. Crystal structures of the adenylate sensor from fission yeast AMP-activated protein kinase. Science 315 (2007) 1726-1729
14. Krishna S.S., Majumdar I., and Grishin N.V. Structural classification of zinc fingers: survey and summary. Nucleic Acids Res. 31 (2003) 532-550
15. Laity J.H., Lee B.M., and Wright P.E. Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11 (2001) 39-46
16. Ravasi T., Huber T., Zavolan M., Forrest A., Gaasterland T., Grimmond S., and Hume D.A. Systematic characterization of the zinc-finger-containing proteins in the mouse transcriptome. Genome Res. 13 (2003) 1430-1442
17. Zhu W., Zeng Q., Colangelo C.M., Lewis M., Summers M.F., and Scott R.A. The N-terminal domain of TFIIB from Pyrococcus furiosus forms a zinc ribbon. Nat. Struct. Biol. 3 (1996) 122-124
18. Qian X., Gozani S.N., Yoon H., Jeon C.J., Agarwal K., and Weiss M.A. Novel zinc finger motif in the basal transcriptional machinery: three-dimensional NMR studies of the nucleic acid binding domain of transcriptional elongation factor TFIIS. Biochemistry 32 (1993) 9944-9959
19. 4 and ferritin-like diiron domains. Nat. Struct. Biol. 3 (1996) 539-546
20. Gomes C.M., Vicente J.B., Wasserfallen A., and Teixeira M. Spectroscopic studies and characterization of a novel electron-transfer chain from Escherichia coli involving a flavorubredoxin and its flavoprotein reductase partner. Biochemistry 39 (2000) 16230-16237
21. Gomes C.M., Silva G., Oliveira S., LeGall J., Liu M.Y., Xavier A.V., et al. Studies on the redox centers of the terminal oxidase from Desulfovibrio gigas and evidence for its interaction with rubredoxin. J. Biol. Chem. 272 (1997) 22502-22508
22. da Costa P.N., Romao C.V., LeGall J., Xavier A.V., Melo E., Teixeira M., and Saraiva L.M. The genetic organization of Desulfovibrio desulfuricans ATCC 27774 bacterioferritin and rubredoxin-2 genes: involvement of rubredoxin in iron metabolism. Mol. Microbiol. 41 (2001) 217-227
23. McKenna E.J., and Coon M.J. Enzymatic omega-oxidation. IV. Purification and properties of the omega-hydroxylase of Pseudomonas oleovorans. J. Biol. Chem. 245 (1970) 3882-3889
24. Shen G., Antonkine M.L., van der Est A., Vassiliev I.R., Brettel K., Bittl R., et al. Assembly of photosystem I. II. Rubredoxin is required for the in vivo assembly of F(X) in Synechococcus sp. PCC 7002 as shown by optical and EPR spectroscopy. J. Biol. Chem. 277 (2002) 20355-20366
25. Wang X., Lee H.S., Sugar F.J., Jenney Jr. F.E., Adams M.W., and Prestegard J.H. PF0610, a novel winged helix-turn-helix variant possessing a rubredoxin-like Zn ribbon motif from the hyperthermophilic archaeon, Pyrococcus furiosus. Biochemistry 46 (2007) 752-761
26. LeGall J., Liu M.Y., Gomes C.M., Braga V., Pacheco I., Regalla M., et al. Characterisation of a new rubredoxin isolated from Desulfovibrio desulfuricans 27774: definition of a new family of rubredoxins. FEBS Lett. 429 (1998) 295-298
27. Grishin N.V. C-terminal domains of Escherichia coli topoisomerase I belong to the zinc-ribbon superfamily. J. Mol. Biol. 299 (2000) 1165-1177
28. Yan Y., and Moult J. Detection of operons. Proteins 64 (2006) 615-628
29. Lovenberg W., and Sobel B.E. Rubredoxin: a new electron transfer protein from Clostridium pasteurianum. Proc. Natl Acad. Sci. USA 54 (1965) 193-199
30. Ragsdale S.W., and Ljungdahl L.G. Characterization of ferredoxin, flavodoxin, and rubredoxin from Clostridium formicoaceticum grown in media with high and low iron contents. J. Bacteriol. 157 (1984) 1-6
31. Jenney Jr. F.E., and Adams M.W. Rubredoxin from Pyrococcus furiosus. Methods Enzymol. 334 (2001) 45-55
32. Weinberg M.V., Jenney Jr. F.E., Cui X., and Adams M.W. Rubrerythrin from the hyperthermophilic archaeon Pyrococcus furiosus is a rubredoxin-dependent, iron-containing peroxidase. J. Bacteriol. 186 (2004) 7888-7895
33. Blake P.R., Park J.B., Bryant F.O., Aono S., Magnuson J.K., Eccleston E., et al. Determinants of protein hyperthermostability: purification and amino acid sequence of rubredoxin from the hyperthermophilic archaebacterium Pyrococcus furiosus and secondary structure of the zinc adduct by NMR. Biochemistry 30 (1991) 10885-10895
34. 4 coordination unit in a protein. Proc. Natl Acad. Sci. USA 93 (1996) 8836-8840
35. Eidsness M.K., O'Dell S.E., Kurtz Jr. D.M., Robson R.L., and Scott R.A. Expression of a synthetic gene coding for the amino acid sequence of Clostridium pasteurianum rubredoxin. Protein Eng. 5 (1992) 367-371
36. Mathieu I., Meyer J., and Moulis J.M. Cloning, sequencing and expression in Escherichia coli of the rubredoxin gene from Clostridium pasteurianum. Biochem. J. 285 (1992) 255-262
37. Maher M., Cross M., Wilce M.C., Guss J.M., and Wedd A.G. Metal-substituted derivatives of the rubredoxin from Clostridium pasteurianum. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 298-303
38. Blake P.R., Day M.W., Hsu B.T., Joshua-Tor L., Park J.B., Hare D.R., et al. Comparison of the X-ray structure of native rubredoxin from Pyrococcus furiosus with the NMR structure of the zinc-substituted protein. Protein Sci. 1 (1992) 1522-1525
39. 2- site of rubredoxin. J. Biol. Inorg. Chem. 3 (1998) 595-605
40. Mayhew S.G. The redox potential of dithionite and SO-2 from equilibrium reactions with flavodoxins, methyl viologen and hydrogen plus hydrogenase. Eur. J. Biochem. 85 (1978) 535-547
41. Moura I., Moura J.J., Santos M.H., Xavier A.V., and Le Gall J. Redox studies on rubredoxins from sulphate and sulphur reducing bacteria. FEBS Lett. 107 (1979) 419-421
42. Gomes C.M., Giuffre A., Forte E., Vicente J.B., Saraiva L.M., Brunori M., and Teixeira M. A novel type of nitric-oxide reductase, Escherichia coli flavorubredoxin. J. Biol. Chem. 277 (2002) 25273-25276
43. Gardner A.M., Gessner C.R., and Gardner P.R. Regulation of the nitric oxide reduction operon (norRVW) in Escherichia coli. Role of NorR and sigma54 in the nitric oxide stress response. J. Biol. Chem. 278 (2003) 10081-10086
44. Lode E.T., and Coon M.J. Enzymatic omega-oxidation. V. Forms of Pseudomonas oleovorans rubredoxin containing one or two iron atoms: structure and function in omega-hydroxylation. J. Biol. Chem. 246 (1971) 791-802
45. Chen L., Liu M.Y., LeGall J., Fareleira P., Santos H., and Xavier A.V. Rubredoxin oxidase, a new flavo-hemo-protein, is the site of oxygen reduction to water by the "strict anaerobe" Desulfovibrio gigas. Biochem. Biophys. Res. Commun. 193 (1993) 100-105
46. Lee H.J., Basran J., and Scrutton N.S. Electron transfer from flavin to iron in the Pseudomonas oleovorans rubredoxin reductase-rubredoxin electron transfer complex. Biochemistry 37 (1998) 15513-15522
47. Ueda T., Lode E.T., and Coon M.J. Enzymatic omega-oxidation. VI. Isolation of homogeneous reduced diphosphopyridine nucleotide-rubredoxin reductase. J. Biol. Chem. 247 (1972) 2109-2116
48. Petitdemange H., Marczak R., Blusson H., and Gay R. Isolation and properties of reduced nicotinamide adenine dinucleotiderubredoxin oxidoreductase of Clostridium acetobutylicum. Biochem. Biophys. Res. Commun. 91 (1979) 1258-1265
49. Perry A., Lian L.Y., and Scrutton N.S. Two-iron rubredoxin of Pseudomonas oleovorans: production, stability and characterization of the individual iron-binding domains by optical, CD and NMR spectroscopies. Biochem. J. 354 (2001) 89-98
50. Claus R., Asperger O., and Kleber H.P. Properties of rubredoxin reductase from the alkane-assimilating bacterium Acinetobacter calcoaceticus. Z. Allg. Mikrobiol. 19 (1979) 695-704
51. Grunden A.M., Jenney Jr. F.E., Ma K., Ji M., Weinberg M.V., and Adams M.W. In vitro reconstitution of an NADPH-dependent superoxide reduction pathway from Pyrococcus furiosus. Appl. Environ. Microbiol. 71 (2005) 1522-1530
52. Meier M., Janosik M., Kery V., Kraus J.P., and Burkhard P. Structure of human cystathionine beta-synthase: a unique pyridoxal 5′-phosphate-dependent heme protein. EMBO J. 20 (2001) 3910-3916
53. Blake P.R., Park J.B., Zhou Z.H., Hare D.R., Adams M.W., and Summers M.F. Solution-state structure by NMR of zinc-substituted rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus. Protein Sci. 1 (1992) 1508-1521
54. Blake P.R., Lee B., Summers M.F., Adams M.W., Park J.B., Zhou Z.H., and Bax A. Quantitative measurement of small through-hydrogen-bond and 'through-space' 1H-113Cd and 1H-199Hg J couplings in metal-substituted rubredoxin from Pyrococcus furiosus. J. Biomol. NMR 2 (1992) 527-533
55. Day M.W., Hsu B.T., Joshua-Tor L., Park J.B., Zhou Z.H., Adams M.W., and Rees D.C. X-ray crystal structures of the oxidized and reduced forms of the rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus. Protein Sci. 1 (1992) 1494-1507
56. Bau R., Rees D.C., Kurtz D.M., Scott R.A., Huang H.S., Adams M.W.W., and Eidsness M.K. Crystal structure of rubredoxin from Pyrococcus furiosus at 0.95 angstrom resolution, and the structures of N-terminal methionine and formylmethionine variants of Pf Rd. Contributions of N-terminal interactions to thermostability. J. Biol. Inorg. Chem. 3 (1998) 484-493
57. Page C.C., Moser C.C., Chen X., and Dutton P.L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402 (1999) 47-52
58. Archer M., Huber R., Tavares P., Moura I., Moura J.J., Carrondo M.A., et al. Crystal structure of desulforedoxin from Desulfovibrio gigas determined at 1.8 Å resolution: a novel non-heme iron protein structure. J. Mol. Biol. 251 (1995) 690-702
59. Liu S., and Leppla S.H. Retroviral insertional mutagenesis identifies a small protein required for synthesis of diphthamide, the target of bacterial ADP-ribosylating toxins. Mol. Cell 12 (2003) 603-613
60. Kummerle R., Zhuang-Jackson H., Gaillard J., and Moulis J.M. Site-directed mutagenesis of rubredoxin reveals the molecular basis of its electron transfer properties. Biochemistry 36 (1997) 15983-15991
61. Cross M., Xiao Z., Maes E.M., Czernuszewicz R.S., Drew S.C., Pilbrow J.R., et al. Removal of a cysteine ligand from rubredoxin: assembly of Fe(2)S(2) and Fe(S-Cys)(3)(OH) centres. J. Biol. Inorg. Chem. 7 (2002) 781-790
62. Sieker L.C., Stenkamp R.E., and LeGall J. Rubredoxin in crystalline state. Methods Enzymol. 243 (1994) 203-216
63. Logan D.T., Mulliez E., Larsson K.M., Bodevin S., Atta M., Garnaud P.E., et al. A metal-binding site in the catalytic subunit of anaerobic ribonucleotide reductase. Proc. Natl Acad. Sci. USA 100 (2003) 3826-3831
64. Treich I., Riva M., and Sentenac A. Zinc-binding subunits of yeast RNA polymerases. J. Biol. Chem. 266 (1991) 21971-21976
65. Carles C., Treich I., Bouet F., Riva M., and Sentenac A. Two additional common subunits, ABC10 alpha and ABC10 beta, are shared by yeast RNA polymerases. J. Biol. Chem. 266 (1991) 24092-24096
66. Zhang R.G., Skarina T., Katz J.E., Beasley S., Khachatryan A., Vyas S., et al. Structure of Thermotoga maritima stationary phase survival protein SurE: a novel acid phosphatase. Structure 9 (2001) 1095-1106
67. Neidhardt F.C., Bloch P.L., and Smith D.F. Culture medium for enterobacteria. J. Bacteriol. 119 (1974) 736-747
68. Hogbom M., Ericsson U.B., Lam R., Bakali H.M., Kuznetsova E., Nordlund P., and Zamble D.B. A high throughput method for the detection of metalloproteins on a microgram scale. Mol. Cell. Proteomics 4 (2005) 827-834
69. Minnaert K. Measurement of the equilibrium constant of the reaction between cytochrome c and cytochrome a. Biochim. Biophys. Acta 110 (1965) 42-56
70. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
71. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
72. Perrakis A., Morris R., and Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6 (1999) 458-463
73. Oldfield T.J., and Hubbard R.E. Analysis of C alpha geometry in protein structures. Proteins 18 (1994) 324-337
74. Laskowski R.A., Macarthur M.W., Moss D.S., and Thornton J.M. Procheck-a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291