Active sites of transition-metal enzymes with a focus on nickel

Current Opinion in Structural Biology

Volumn 8, Issue 6, 1998, Pages 749-758

  Ermler, Ulrich ^a   Grabarse, Wolfgang ^a,b   Shima, Seigo ^b   Goubeaud, Marcel ^b   Thauer, Rudolf K ^b  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A SYNTHETASE; CARBON MONOXIDE DEHYDROGENASE; COBALT; COPPER; ENZYME; HYDROGENASE; IRON; MANGANESE; MOLYBDENUM; NICKEL; OXIDOREDUCTASE; SUPEROXIDE DISMUTASE; TUNGSTEN; UREASE; VANADIUM;

CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; PRIORITY JOURNAL; REVIEW;

EID: 0032435658     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(98)80095-X     Document Type: Article

References (99)

1. 1. Cammack R, van Vliet P: Catalysis by nickel in biological systems. In Bioinorganic Catalysis, edn 2. Edited by Reedijk J, Bouernans L. New York: Marcel Dekker Inc.; 1998:231-268.
2. 2. Maroney MJ, Davidson G, Allan CB, Figlar J: The structure and function of nickel sites in metalloproteins. Structure and Bonding 1998, 92:1-66.
3. 3. Ragsdale SW: Nickel biochemistry. Curr Opin Chem Biol 1998, 2:208-215.
4. 4. Hausinger RP: Metallocenter assembly in nickel-containing enzymes. J Biol Inorg Chem 1997, 2:279-286.
5. 5. Fontecilla-Camps JC: Biological nickel. Structure and Bonding 1997, 91:1-30.
6. 6. Thauer RK: Biochemistry of methanogenesis. A tribute to Majory Stephenson. Microbiology 1998, 144:2377-2406.
7. 430. In Bioinorganic Chemistry: Trace Element Evolution from Anaerobes to Aerobes, vol 91. Edited by Williams RJP. Heidelberg: Springer Verlag; 1998:31-63.
8. 8. Shima S, Goubeaud M, Vinzenz D, Thauer RK, Ermler U: Crystallization and preliminary X-ray diffraction studies of methyl-coenzyme M reductase from Methanobacterium thermoautotrophicum. J Biochem 1997, 121:8 29-830.
9. 430, M and B. In a second enzyme state, the protein contains the heterodisulfide of coenzymes M and B. An enzymatic mechanism was proposed that includes a Ni-methyl intermediate.
10. 430 is reduced to the nickel(I) oxidation state by titanium(III) citrate. Eur J Biochem 1997, 243:110-114. The described activation procedure opens the possibility of obtaining the active form of methyl-CoM reductase after purification.
11. 11. Rouviére PE, Wolfe RS: Component A3 of the methylcoenzyme M methylreductase system of Methanobacterium thermoautotrophicum AH: resolution into two components. J Bacteriol 1989, 161:4556-4562.
12. 12. Becker DF, Ragsdale SW: Activation of methyl-SCoM reductase to high specific activity after treatment of whole cells with sodium sulfide. Biochemistry 1998, 37:2639-2647.
13. 430. In Metal Ions in Biological Systems, vol 29. Edited by Sigel H, Sigel A. New York: Marcel Dekker Inc.; 1993:287-337.
14. 14. Moncrief MBC, Hausinger RP: Characterization of UreG, identification of a UreD-UreF-UreG complex, and evidence suggesting that a nucleotide-binding site in UreG is required for in vivo metallocenter assembly of Klebsiella aerogenes urease. J Bacteriol 1997, 179:4081-4086.
15. 15. Jabri E, Carr MB, Hausinger RP, Karplus PA: The crystal structure of urease from Klebsiella aerogenes. Science 1995, 268:998-1004.
16. 16. Karplus PA, Pearson MA, Hausinger RP: 70 years of crystalline urease: what have we learned? Accounts Chem Res 1997, 30:330-337. This excellent review summarizes present knowledge of the urease reaction. The role of the nickel ions and the catalytically relevant amino acids are examined comprehensively, The proposed mechanism was connected to more general aspects of enzymatic catalysis in a stimulating manner.
17. 17. Jabri E, Karplus PA: Structures of the Klebsiella aerogenes urease apoenzyme and two active-site mutants. Biochemistry 1996, 35:10616-10626.
18. 18. Pearson MA, Michel LO, Hausinger RP, Karplus PA: Structures of Cys319 variants and acetohydroxamate-inhibited Klebsiella aerogenes urease. Biochemistry 1997, 36:8164-8172.
19. 19. Park I-S, Hausinger RP: Requirement of carbon dioxide for in vitro assembly of the urease nickel metallocenter. Science 1995, 267:1156-1158.
20. 20. Yamagushi K, Hausinger RP: Substitution of the urease active site carbamate by dithiocarbonate and vanadate. Biochemistry 1997, 36:15118-15122.
21. 21. Park IS, Michel LO, Pearson MA, Jabri E, Karplus PA, Wang SK, Dong J, Scott RA, Koehler BP, Johnson MK, Hausinger RP: Characterization of the mononickel metallocenter in H134A mutant urease. J Biol Chem 1996, 271:18632-18637.
22. 22. Thauer RK, Klein AR, Hartmann GC: Reactions with molecular hydrogen in microorganisms. Evidence for a purely organic hydrogenation catalyst. Chem Rev 1996, 96:3031-3042.
23. 23. Frey M: Nickel-iron hydrogenases: structural and functional properties. Structure and Bonding 1998, 90:97-126.
24. 24. Künkel A, Vorholt JA, Thauer RK, Hedderich R: An Escherichia coli hydrogenase-3-type hydrogenase in methanogenic archaea. Eur J Biochem 1998, 252:467-476.
25. 25. Lenz O, Strack A, Tran-Betcke A, Friedrich B: A hydrogen-sensing system in transcriptional regulation of hydrogenase gene expression in Alcaligenes species. J Bacteriol 1997, 179:1655-1663.
26. 26. Drapal N, Bȯck A: Interaction of the hydrogenase accessory protein hypC, the large subunit of Escherichia coli hydrogenase 3 during enzyme maturation. Biochemistry 1998, 37:2941-2948.
27. 27. Volbeda A, Charon M-H, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC: Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 1995, 373:580-587.
28. 28. Volbeda A, Garcia E, Piras C, de Lacey AL, Fernandez VM, Hatchikian EC, Frey M, Fontecilla-Camps JC: Structure of the [NiFe] hydrogenase active site - evidence for biologically uncommon Fe ligands. J Am Chem Soc 1996, 118:12989-12996.
29. 29. Higuchi Y, Yagi T, Yasuoka N: Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis. Structure 1997, 5:1671-1680.
30. 30. Van Dam PJ, Reijerse EJ, Hagen WR: Identification of a putative histidine base and of a non-protein nitrogen ligand in the active site of Fe-hydrogenases by one-dimensional and two-dimensional electron spin-echo envelope-modulation spectroscopy. Eur J Biochem 1997, 248:355-361.
31. 31. Van der Spek TM, Arendsen AF, Happe RP, Yun S, Bagley JA, Stufkens DJ, Hagen WR, Albracht SRJ: Similarities in the architecture of the active sites of Ni-hydrogenases and Fe-hydrogenases detected by means of infrared spectroscopy. Eur J Biochem 1996, 237:629-634.
32. 32. Montet Y, Amara P, Volbeda A, Vernede X, Hatchikian EC, Field MJ, Frey M, Fontecilla-Camps JC: Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics. Nat Struct Biol 1997, 4:523-526.
33. 33. Gu Z, Dong J, Allan CB, Choudhury SB, Franco R, Moura JJG, Moura I, LeGall J, Przybyla AE, Roseboom W et al.: Structure of the Ni sites in hydrogenases by X-ray absorption spectroscopy. Species variation and the effects of redox poise. J Am Chem Soc 1996, 118:11155-11165.
34. 34. Sorgenfrei O, Duin EC, Klein A, Albracht SPJ: Changes in the electronic structure around Ni in oxidized and reduced selenium-containing hydrogenases from Methanococcus voltae. Eur J Biochem 1997, 247:681-687.
35. 35. Dole F, Fournel A, Magro V, Hatchikian EC, Bertrand P, Guigliarelli B: Nature-end electronic structure of the Ni-X dinuclear center of Desulfovibrio gigas hydrogenase. Implications for the enzymatic mechanism. Biochemistry 1997, 36:7847-7854.
36. 57Fe Q-band pulsed ENDOR of the hetero-dinuclear site of nickel hydrogenases: comparison of the NiA, NiB, and NiC states. J Am Chem Soc 1997, 119:9291-9292.
37. 13C labeled Ni-Fe hydrogenase in order to elucidate the nature of the unexpected diatomic iron ligands as carbon monoxide and cyanide.
38. 38. De Lacey AL, Hatchikian EC, Volbeda A, Frey M, Fontecilla-Camps JC, Fernandez VM: Infrared-spectroelectrochemical characterization of the [NiFe] hydrogenase of Desulfovibrio gigas. J Am Chem Soc 1997, 119:7181-7189.
39. 2] structural unit in Ni-Fe hydrogenase enyzmes. J Am Chem Soc 1997, 119:8371-8372.
40. 40. Pavlov M, Siegbahn PEM, Blomberg MRA, Crabtree RH: Mechanism of H-H activation by nickel-iron hydrogenase. J Am Chem Soc 1998, 120:548-555.
41. 41. Hänzelmann P, Meyer O: Effect of molybdate and tungstate on the biosynthesis of carbon monoxide dehydrogenase and the molybdopterin cytosine dinucleotide type of molybdenum in Hydrogenophaga pseudoflava. Eur J Biochem 1998, 255:755-765.
42. 42. Ragsdale SW, Kumar M: Nickel-containing carbon monoxide dehydrogenase/acetyl-CoA synthase. Chem Rev 1996, 96:2515-2539.
43. 43. Grahame DA, DeMoll E: Partial reactions catalyzed by protein components of the acetyl-CoA decarboxylase synthase enzyme complex from Methanosarcina barkeri. J Biol Chem 1996, 271:8352-8358.
44. 44. Kerby RL, Ludden PW, Roberts GP: In vivo nickel insertion into the carbon monoxide dehydrogenase of Rhodospirillum rubrum: molecular and physiological characterization of cooCTJ. J Bacteriol 1997, 179:2259-2266.
45. 45. Watt RK, Ludden PW: The identification, purification and characterization of CooJ. J Biol Chem 1998, 273:10019-10025.
46. 46. Xia J, Sinclair JF, Baldwin TO, Lindahl PA: Carbon monoxide dehydrogenase from Clostridium thermoaceticum: quarternary structure and stoichiometry of its SDS-induced dissociation. Biochemistry 1996, 35:1965-1971.
47. 47. Seravalli J, Kumar M, Lu W-P, Ragsdale SW: Mechanism of carbon monoxide oxidation by the carbon monoxide dehydrogenase/acetyl-CoA synthase from Clostridium thermoaceticum: kinetic characterization of the intermediates. Biochemistry 1997, 36:11241-11251.
48. 48. Hu Z, Spangler NJ, Anderson ME, Xia J, Ludden PW, Lindahl PA, Münck E: The nature of the C-cluster in Ni-containing carbon monoxide dehydrogenases. J Am Chem Soc 1996, 118:830-845.
49. 49. Spangler NJ, Meyers MR, Gierke KL, Kerby RL, Roberts GP, Ludden PW: Substitution of valine for histidine 265 in carbon monoxide dehydrogenase from Rhodospirillum rubrum affects activity and spectroscopic states. J Biol Chem 1998, 273:4059-4064.
50. 4] center. J Am Chem Soc 1998, 120:8764-8776.
51. 2. Biochemistry 1998, 37:10016-10026.
52. 52. Menon S, Ragsdale SW: Evidence that carbon monoxide is an obligatory intermediate in anaerobic acetyl-CoA synthesis. Biochemistry 1996, 35:12119-12125.
53. 53. Xia J, Hu Z, Popescu CV, Lindahl PA, Münck E: Mössbauer and EPR study of the Ni-activated α-subunit of carbon monoxide dehydrogenase from Clostridium thermoaceticum. J Am Chem Soc 1997, 119:8301-8312. The described experimental results have significant implications for the structure and oxidation states of the A cluster, as well as for the enzymatic mechanism of the carbon monoxide dehydrogenase-acetyl-CoA synthase complex.
54. 54. Barondeau DP, Lindahl PA: Methylation of carbon monoxide dehydrogenase from Clostridium thermoaceticum and mechanism of acetyl coenzyme A synthesis. J Am Chem Soc 1997, 119:3959-3970.
55. 55. Russell WK, Stålhandske CMV, Xia J, Scott R, Lindahl PA: Spectroscopic, redox and structural characterization of the Ni-labile and nonlabile forms of the acetyl-CoA synthase active site of carbon monoxide dehydrogenase. J Am Chem Soc 1998, 120:7502-7510.
56. 56. Menon S, Ragsdale SW: Role of the [4Fe-4S] cluster in reductive activation of the cobalt center of the corrinoid iron-sulfur protein from Clostridium thermoaceticum during acetate biosynthesis. Biochemistry 1998, 37:5689-5698. This important work shows how a methyl group is transferred from a corrinoid Fe-S protein to the carbon monoxide dehydrogenase-acetyl-CoA synthase complex.
57. 57. Spiro TG: Resonance Raman results: retraction. Science 1997, 278:21.
58. 58. Lim J-H, Yu YG, Man YS, Cho S-J, Ahn B-Y, Kim S-H, Cho Y: The crystal structure of an Fe-superoxide dismutase from the hyperthermophilic Aquifex pyrophilus at 1.9 Å resolution: structural basis for thermostability. J Mol Biol 1997, 270:259-274.
59. 59. Edwards RA, Baker HM, Whittaker MM, Whittaker JW, Jameson GB, Baker EN: Crystal structure of Escherichia coli manganese superoxide dismutase at 2.1-Ångstrom resolution. J Biol Inorg Chem 1998, 3:161-171.
60. 60. Pesce A, Capasso C, Battistoni A, Folcareili A, Rotilio G, Desideri A, Bolognesi M: Unique structural features of the monomeric Cu,Zn superoxide dismutase from Escherichia coli, revealed by X-ray crystallography. J Mol Biol 1997, 274:408-420.
61. 61. Murphy LM, Strange RW, Hasnain SS: A critical assessment of the evidence from XAFS and crystallography for the breakage of the imidazolate bridge during catalysis in CuZn superoxide dismutase. Structure 1997, 5:371-379.
62. 62. Youn H-D, Kim E-J, Roe J-H, Hah YC, Kang S-O: A novel nickel-containing superoxide dismutase from Streptomyces spp. Biochem J 1996, 318:889-896.
63. 63. Youn H-D, Youn H, Lee J-W, Yim Y-I, Lee JK, Hah YC, Kang S-O: Unique isozymes of superoxide dismutase in Streptomyces grieseu. Arch Biochem Biophys 1996, 334:341-348.
64. 2+. After the deletion of the 14 N-terminal amino acids, active NiSOD was produced, indicating the necessity of N-terminal processing.
65. 65. Kim E-J, Kim H-P, Hah YC, Roe J-H: Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor. Eur J Biochem 1996, 241:178-185.
66. 66. Wang ZM, Quiocho FA: Complexes of adenosine deaminase with two potent inhibitors - X-ray structures in four independent molecules at pH of maximum activity. Biochemistry 1998, 37:8314-8324.
67. 67. Vanhooke JL, Benning MM, Raushel FM, Holden HM: Three-dimensional structure of the zinc-containing phosphotriesterase with the bound substrate analog diethyl 4-methylbenzyl-phosphonate. Biochemistry 1996, 35:6020-6025.
68. 68. Holm L, Sander C: An evolutionary treasure: unification of a broad set of amidohydrolases related to urease. Proteins 1997, 28:72-82.
69. 69. Kanyo ZF, Scolnick LR, Ash DE, Christianson DW: Structure of a unique binuclear manganese cluster in arginase. Nature 1996, 383:554-557.
70. 70. Das AK, Helps NR, Cohen PTW, Barford D: Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 Å resolution. EMBO J 1996, 15:6798-6809.
71. 71. Sträter N, Klabunde T, Tucker P, Witzel H, Krebs B: Crystal structure of a purple acid phosphatase containing a dinuclear Fe(III)-Zn(II) active site. Science 1995, 268:1489-1492.
72. 72. Lindquist Y, Huang W, Schneider G, Shanklin J: Crystal structure of Δ9 stearoyl-acyl carrier protein desaturase from castor seed and its relationship to other di-iron proteins. EMBO J 1996, 15:4081-4092.
73. 73. Nordlund P, Eklund H: Di-iron-carboxylate proteins. Curr Opin Struct Biol 1995, 5:758-766.
74. 74. Michel H, Behr J, Harrenga A, Kannt A: Cytochrome c oxidase -structure and spectroscopy. Annu Rev Biophys Biomol Struct 1998, 27:329-356.
75. 75. Yoshikawa S, Shinzawa-Itoh K, Nakashina R, Yaono R, Yamashita E, Inoue N, Yao M, Fei MJ, Libeu CP, Mizushima T et al.: Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 1998, 280:1723-1729.
76. 76. Crane BR, Siegel LM, Getzoff ED: Probing the catalytic mechanism of sulfite reductase by X-ray crystallography: structures of the Escherichia coli hemoprotein in complex with substrates, inhibitors, intermediates and products. Biochemistry 1997, 36:12120-12137.
77. 77. Gillmor SA, Villasenor A, Fletterick R, Sigal E, Browner M: The structure of mammalian 15-lipoxygenase reveals similarities to the lipases and the determinants of substrate specificity. Nat Struct Biol 1997, 4:1003-1009. Mammalian 15-lipoxygenase contains a nonheme catalytic iron. The Fe(III) ion serves as Lewis acid that enhances the nucleophilicity of a water molecule acting as general base.
78. 78. Reynolds MP, Baron AJ, Wilmot CM, Vinecombe E, Stevens C, Phillips SEV, Knowles PF, McPherson MJ. Structure and mechanism of galactose oxidase - catalytic role of tyrosine 495. J Biol Inorg Chem 1997, 2:327-335.
79. 12-dependent enzymes. Annu Rev Biochem 1997, 66:269-313.
80. 80. Crane BR, Arvai AS, Ghosh DK, Wu C, Getzoff WD, Stuehr DJ, Tainer JA: Structure of nitric oxide synthase oxygenase dimer with pterin and substrate. Science 1998, 279:2121-2126. The structure of the nitric oxide synthase oxygenase domain revealed an unusual fold for heme binding. The binding of the arginine substrate and the pterin cofactor allowed an enzymatic mechanism for nitric oxide biosynthesis to be proposed.
81. 1 complex (80% complete) and the position of the metal centers.
82. 1 and Rieske subunits. The conformational change of the Rieske extrinsic domain in different structures is interpreted as a key feature of electron transfer.
83. 1 complex confirms an electron transfer mechanism based on a domain movement and provides an answer as to how mitochondrial targeting presequences are recognized.
84. 84. Messerschmidt A: Metal sites in blue copper proteins, blue copper oxidases and vanadium-containing enzymes. Structure and Bonding 1998, 90:37-68.
85. 85. Romao MJ, Rösch N, Huber R: The molybdenum site in the xanthine-related aldehyde oxidoreductase from Desulfobibrio gigas and a catalytic mechanism for this class of enzymes. J Biol Inorg Chem 1997, 2:782-785.
86. 86. Schindelin H, Kisker C, Hilton J, Rajagoplan KV, Rees DC: Crystal structure of DMSO reductase: redox-linked changes in molybdopterin coordination. Science 1996, 272:1615-1621.
87. 4 cluster. Science 1997, 275:1305-1308. A reaction mechanism was derived from the crystal structure of formate dehydrogenase H complexed with nitrite. The mechanism involves a two-electron transfer through the oxygen of formate to MoVI, forming MoIV. The specific role of selenium is discussed.
88. 88. Kisker C, Schindel in H, Pacheco A, Wehbi WA1 Garrett RM, Rajagoplan KV, Enemark JH, Rees DC: Molecular basis of sulfite oxidase deficiency from the structure of sulfite oxidase. Cell 1997, 91:973-983. The structure of chicken sulfite oxidase is the prototype of a group of molybdopterin-containing enzymes. Nitrate reductase also belongs to this group. An enzymatic mechanism is proposed, whereby oxygen transfer between a hydroxide ligand coordinated to molybdenum and sulfite takes place.
89. - and interpreted with respect to the coupling of ATP hydrolysis and electron transfer.
90. 90. Kisker C, Schindelin H, Rees DC: Molybdenum-cofactor-containing enzymes: structure and mechanism. Annu Rev Biochem 1997, 66:233-267.
91. 91. Goodwill KE, Sabatier C, Marks C, Raag R, Fitzpatrick PF, Stevens RC: Crystal structure of tyrosine hydroxylase at 2.3 Å and its implications for inherited neurodegenerative diseases. Nat Struct Biol 1997, 4:578-585.
92. 92. Roach PL, Clifton IJ, Charles MH, Hensgens MH, Shibata N, Schofield CJ, Hajdu J, Baldwin JE: Structure of isopenicillin N synthase complexed with substrate and the mechanism of penicillin formation. Nature 1997, 387:825-830. The convincing structure-based mechanism described in this paper involves a nonheme iron in oxidation states I, II and III.
93. 93. Huang W, Jia J, Cummings J, Nelson M, Schneider G, Lindqvist Y: Crystal structure of nitrile nydratase reveals a novel iron centre in a novel fold. Structure 1997, 5:691-699.
94. 94. Tsujimura M, Dohmae N, Odaka M, Chijimatsu M, Takio K, Yohda M, Hoshino M, Nagashima S, Endo I: Structure of the photo-reactive iron center of the nitrile hydratase from Rhodococcus sp. N-771 -evidence of a novel post-translational modification in the cysteine ligand. J Biol Chem 1997, 272:29454-29459.
95. 95. Arendsen AF, Hadden J, Card G, McAlpine AS, Bailey S, Zaitsev V, Duke EHM, Lindley PF, Kröckel M, Trautwein AX: The 'prismane' protein resolved: X-ray structure at 1.7 Å and multiple spectroscopy of two novel 4Fe clusters. J Biol Inorg Chem 1998, 3:81-95.
96. 96. Park S-Y, Shimizu H, Adachi S-i, Nakagawa A, Tanaka I, Nakahara K, Shoun H, Obayashi E, Nakamura H, IizukaT, Shiro Y: Crystal structure of nitric oxide reductase from denitrifying fungus Fusarium oxysporum. Nat Struct Biol 1997, 4:827-832
97. 97. Mancia F, Evans PR: Conformational changes on substrate binding to methylmalonyl CoA mutase and new insights into the free radical mechanism. Structure 1998, 6:711-720.
98. 98. Lindley PF, Card G, Zaitseva I, Zaitsev V, Reinhammer B, Selin-Lindgren E, Yoshida K: An X-ray structural study of human ceruloplasmin in relation to ferroxidase activity. J Biol Inorg Chem 1997, 2:454-463. Human ceruloplasmin belongs to the class of blue-copper oxidases (see also [84]) and it contains three mononuclear copper atoms (type I) and one trinuclear copper (type II and III) complex, the potential dioxygen reducing site. The crystal structure supports the role of ceruloplasmin as a ferroxidase.
99. 99. Prigge ST, Kolhekar AS, Eipper EA, Mains RE, Amzel LM: Amidation of bioactive peptides: the structure of peptidylglycine α-hydroxylating monoxygenase. Science 1997, 278:1300-1305. The structure of rat peptidylglycine α-hydroxylating monoxygenase represents the prototype of a class of physiologically important copper-containing monoxygenases. The two copper ions (11 Å apart) cycle through Cu(I) and Cu(II) oxidation states, each donating one electron for oxygen cleavage.