Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b

Protein Science

Volumn 6, Issue 3, 1997, Pages 556-568

  Elango, Natesan ^a   Radhakrishnan, Ramaswamy ^a,b   Froland, Wayne A ^a,c   Wallar, Bradley J ^a   Earhart, Cathleen A ^a   Lipscomb, John D ^a   Ohlendorf, Douglas H ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

dinuclear iron cluster; methane oxidation; methanotroph; oxygen activation; X ray crystallography

Indexed keywords

METHANE; OXYGENASE;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; OXIDATION; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

METHYLOCOCCUS; METHYLOCOCCUS CAPSULATUS STR. BATH; METHYLOCYSTACEAE; METHYLOSINUS TRICHOSPORIUM; TRICHOSPORIUM;

EID: 0030943755     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560060305     Document Type: Article

References (70)

1. Andersson KK, Froland WA, Lee SK, Lipscomb JD. 1991. Dioxygen independent oxygenation of hydrocarbons by methane monooxygenase hydroxylase component. New J Chem 15:411-415.
2. Anthony C. 1982. The biochemistry of the methylotrophs. London, UK: Academic Press.
3. +. J Am Chem Soc 106:4632-4633.
4. Borer L, Thalken L, Ceccarrelli C, Glick M, Zhang JH, Reiff WM. 1983. Synthesis and characterization of a hydroxyl-bridged iron(III) dimer of N,N'-ethylenebis(salicylamine). Inorg Chem 22:1719-1724.
5. Brünger AT. 1992. XPLOR, version 3.1. A system for X-ray crystallography and NMR. New Haven, Connecticut: Yale University Press.
6. Cardy DLN, Laidler V, Salmond GPC, Murrell JC. 1991a. The methane monooxygenase gene cluster of Methylosinus trichosporium: Cloning and sequencing of mmoC gene. Arch Microbiol 156:477-483.
7. Cardy DLN, Laidler V, Salmond GPC, Murrell JC. 1991b. Molecular analysis of the methane monooxygenase (MMO) gene cluster of Methylosinus trichosporium OB3b. Mol Microbiol 5:335-342.
8. Colby J, Stirling DI, Dalton H. 1977. The soluble methane monooxygenase of Methylococcus capsulatus Bath: Its ability to oxygenate n-alkanes, n-alkenes, ethers and alicyclic, aromatic and heterocyclic compounds. Biochem J 165:395-402.
9. Dalton H. 1980. Oxidation of hydrocarbons by methane monooxygenases from a variety of microbes. Adv Appl Microbiol 26:71-87.
10. Dalton H. 1991. Structure and mechanism of action of the enzymes involved in methane oxidation. In: Kelly JW, Baldwin T, eds. Applications of enzyme biotechnology. New York: Plenum. pp 55-68.
11. DeRose VJ, Liu KE, Kurtz DM Jr, Hoffman BM, Lippard SJ. 1993. Proton ENDOR identification of bridging hydroxide ligands in mixed-valent diiron centers of proteins: Methane monooxygenase and semimet azidohemerythrin. J Am Chem Soc 115:6440-6441.
12. DeWitt JG, Bentsen JG, Rosenzweig AC, Hedman B, Green J, Pilkington S, Papaefthymiou GC, Dalton H, Hodgson KO, Lippard SJ. 1991. X-ray absorption, Mossbauer, and EPR studies of the dinuclear iron center in the hydroxylase component of methane monooxygenase. J Am Chem Soc 113:9219-9235.
13. 3. J Am Chem Soc 117:2778-2792.
14. III sites relevance to cluster X of Escherichia coli ribonucleotide reductase. J Am Chem Soc 117:11377-11378.
15. Evans SV. 1993. SETOR: Hardware lighted three-dimensional solid model representations of macromolecules. J Mol Graphics 11:134-138.
16. Feig AL, Lippard SJ. 1994. Reactions of non-heme iron(II) centers with dioxygen in biology and chemistry. Chem Rev 94:759-805.
17. Fox BG, Borneman JG, Wackett LP, Lipscomb JD. 1990b. Haloalkene oxidation by the soluble methane monooxygenase from Methylosinus trichosporium OB3b: Mechanistic and environmental implications. Biochemistry 29:6419-6427.
18. Fox BG, Froland WA, Dege J, Lipscomb JD. 1989. Methane monooxygenase from Methylosinus trichosporium OB3b: Purification and properties of a three component system with high specific activity from a type II methanotroph. J Biol Chem 264:10023-10233.
19. Fox BG, Froland WA, Jollie DR, Lipscomb JD. 1990a. Methane monooxygenase from Methylosinus trichosporium OB3b. Methods Enzymol 188:191-202.
20. Fox BG, Hendrich MP, Surerus KK, Andersson KK, Froland WA, Lipscomb JD, Münck E. 1993. Mossbauer, EPR, and ENDOR studies of the hydroxylase and reductase components of methane monooxygenase from Methylosinus trichosporium OB3b. J Am Chem Soc 115:3688-3701.
21. Fox BG, Liu Y, Dege, JE Lipscomb JD. 1991. Complex formation between the protein components of methane monooxygenase from Methylosinus trichosporium OB3b. Identification of sites of component interaction. J Biol Chem 266:540-550.
22. Fox BG, Shanklin J, Ai J, Loehr TM, Sanders-Loehr J. 1994. Resonance Raman evidence for an Fe-O-Fe center in stearoyl-ACP desaturase. Primary sequence identity with other diiron-oxo proteins. Biochemistry 33:12776-12786.
23. Fox BG, Surerus KK, Münck E, Lipscomb JD. 1988. Evidence for a μ-oxo-bridged binuclear iron cluster in the hydroxylase component of methane monooxygenase. J Biol Chem 263:10553-10556.
24. Froland WA, Andersson KK, Lee SK, Liu Y, Lipscomb JD. 1992. Methane monooxygenase component B and reductase alter the regioselectivity of the hydroxylase component-catalyzed reactions. A novel role for protein-protein interactions in an oxygenase mechanism. J Biol Chem 267:17588-17597.
25. Froland WA, Dyer DH, Radhakrishnan R, Earhart CA, Lipscomb JD, Ohlendorf DH. 1994. Preliminary crystallographic analysis of methane monooxygenase hydroxylase from Methylosinus trichosporium OB3b. J Mol Biol 236:379-381.
26. Green J, Dalton H. 1989. Substrate specificity of soluble methane monooxygenase: Mechanistic implications. J Biol Chem 264:17698-17703.
27. Hagen KS, Lachicotte R. 1992. Diiron(II) μ-aqua bis(μ-carboxylato) models of reduced dinuclear non-heme iron sites in proteins. J Am Chem Soc 114:8741-8742.
28. Higgins IJ, Best DJ, Hammond RC. 1980. New findings in methane-utilizing bacteria highlight their importance in the biosphere and their commercial potential. Nature 286:561-564.
29. CAM monooxygenase reaction by a single mutation, threonine-252 to alanine or valine: Possible role of the hydroxy amino acid in oxygen activation. Proc Natl Acad Sci USA 86:7823-7827.
30. Jones TA. 1978. A graphics model building and refinement system for macromolecules. J Appl Crystallogr 11:268-272.
31. Kim K, Lippard SJ. 1996. Structure and Mossbauer spectrum of a (μ-1,2-peroxo) bis(μ-carboxylato) diiron(III) model for the peroxo intermediate in the methane monooxygenase hydroxylase reaction cycle. J Am Chem Soc 118:4914-4915.
32. Kurtz DM Jr. 1990. Oxo and hydroxo-bridged diiron complexes: A chemical perspective on a biological unit. Chem Rev 90:585-606.
33. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. 1993. PROCHECK: A program to check stereochemical quality of protein structures. J Appl Crystallogr 26:283-291.
34. IV cluster. J Am Chem Soc 115:6450-6451.
35. Lee SK, Nesheim JC, Lipscomb JD. 1993b. Transient intermediates of the methane monooxygenase catalytic cycle. J Biol Chem 268:21569-21577.
36. Lipscomb JD. 1994. Biochemistry of the soluble methane monooxygenase. Annu Rev Microbiol 48:371-399.
37. Liu KE, Valentine AM, Qiu D, Edmondson DE, Appelman EH, Spiro TG, Lippard SJ. 1995a. Characterization of a diiron(III) peroxo intermediate in the reaction cycle of methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath). J Am Chem Soc 117:4997-4998.
38. Liu KE, Valentine AM, Wang DL, Huynh BH, Edmondson DE, Salifoglou A, Lippard SJ. 1995b. Kinetic and spectroscopic characterization of intermediates and component interactions in reactions of methane monooxygenase from Methylococcus capsulatus (Bath). J Am Chem Soc 117:10174-10185.
39. Liu KE, Wang D, Huynh BH, Edmondson DE, Salifoglou A, Lippard SJ. 1994. Spectroscopic detection of intermediates in the reaction of dioxygen with the reduced methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath). J Am Chem Soc 116:7465-7466.
40. Liu Y, Nesheim JC, Lee SK, Lipscomb JD. 1995c. Gating effects of component B on oxygen activation by the methane monooxygenase hydroxylase component. J Biol Chem 270:24662-24665.
41. Martinis SM, Atkins WM, Stayton PS, Sligar SG. 1989. A conserved residue of cytochrome P-450 is involved in heme-oxygen stability and activation. J Am Chem Soc 111:9252-9253.
42. McMurry TJ, Groves JT. 1986. Metalloporphyrin models for cytochrome P-450. In: Ortiz de Montellano PR, ed. Cytochrome P-450 structure, mechanism, and biochemistry. New York: Plenum. pp 1-28.
43. Nesheim JC, Lipscomb JD. 1996. Large isotope effects in methane oxidation catalyzed by methane monooxygenase: Evidence for C-H bond cleavage in a reaction cycle intermediate. Biochemistry 35:10240-10247.
44. Nicholls A, Sharp KA, Honig B. 1991. Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct Funct Genet 11:281-296.
45. Nordlund P, Dalton H, Eklund H. 1992. The active site structure of methane monooxygenase is closely related to the binuclear iron center of ribonucleotide reductase. FEBS Lett 307:257-262.
46. Nordlund P, Sjöberg BM, Eklund H. 1990. Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345:593-598.
47. Ohlendorf DH. 1994. Accuracy of refined protein structures. II. Comparison of four independently refined models of human interleukin 1β. Acta Crystallogr D 50:808-812.
48. Ortiz de Montellano PR. 1986. Oxygen activation and transfer. In: Ortiz de Montellano PR, ed. Cytochrome P-450 structure, mechanism, and biochemistry. New York: Plenum Press. pp 217-271.
49. Otwinowski Z. 1993. An oscillation data processing suite for macromolecular crystallography. New Haven, Connecticut: Yale University.
50. Patel RN, Savas JC. 1987. Purification and properties of the hydroxylase component of methane monooxygenase. J Bacteriol 169:2313-2317.
51. Paulsen KE, Liu Y, Fox BG, Lipscomb JD, Münck E, Stankovich MT. 1994. Oxidation-reduction potentials of the methane monooxygenase hydroxylase component from Methylosinus tricosporium OB3b. Biochemistry 33:713-722.
52. Pilkington SJ, Dalton H. 1990. Soluble methane monooxygenase from Methylococcus capsulatus Bath. Methods Enzymol 188:181-190.
53. Poulos TL, Finzel BC, Gunsalus IC, Wagner GC, Kraut J. 1985. The 2.6-Å crystal structure of Pseudomonas putida cytochrome P-450*. J Biol Chem 260:16122-16130.
54. Priestley ND, Floss HG, Froland WA, Lipscomb JD, Williams PG, Morimoto H. 1992. Cryptic stereospecificity of methane monooxygenase. J Am Chem Soc 114:7561-7562.
55. Que L Jr, Dong Y. 1996. Modeling the oxygen activation chemistry of methane monooxygenase and ribonucleotide reductase. Acc Chem Res 29:190-196.
56. Rataj MJ, Kauth JE, Donnelly MI. 1991. Oxidation of deuterated compounds by high specific activity methane monooxygenase from Methylosinus trichosporium: Mechanistic implications. J Biol Chem 266:18684-18690.
57. Rosenzweig AC, Frederick CA, Lippard SJ. 1992. Crystallization and preliminary X-ray analysis of the methane monooxygenase hydroxylase protein from Methylococcus capsulatus (Bath). J Mol Biol 227:583-585.
58. Rosenzweig AC, Frederick CA, Lippard SJ, Nordlund P. 1993. Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane. Nature 366:537-543.
59. Rosenzweig AC, Nordlund P, Takahara PM, Frederick CA, Lippard SJ. 1995. Geometry of the methane monooxygenase catalytic diiron center in two oxidation states. Chem & Biol 2:409-418.
60. Shu L, Liu Y, Lipscomb JD, Que L Jr. 1996a. EXAFS studies of the methane monooxygenase hydroxylase component from Methylosinus trichosporium OB3b. J Biol Inorg Chem 1:297-304.
61. 2 diamond core structure for the key intermediate Q of the methane monooxygenase. Science 275:515-518.
62. Stainthorpe AC, Lees V, Salmond GP, Dalton H, Murrell JC. 1990. The methane monooxygenase gene cluster of Methylococcus capsulatus (Bath). Gene 91:27-34.
63. Stainthorpe AC, Murrell JC, Salmond GP, Dalton H, Lees V. 1989. Molecular analysis of methane monooxygenase from Methylococcus capsulatus (Bath). Arch Microbiol 152:154-159.
64. Sturgeon BE, Burdi D, Chen S, Huynh BH, Edmondson DE, Stubbe J, Hoffman BM. 1996. Reconsideration of X, the diiron intermediate formed during cofactor assembly in E. coli ribonucleotide reductase. J Am Chem Soc 118:7551-7557.
65. Thich JA, Ou CC, Powers D, Vasiliou B, Mastropaolo D, Potenza JA, Schugar HJ. 1976. Molecular structure and magnetic properties of μ-dihydroxo-bis[2,6-pyridinedicarboxylatoaquoiron(III)] and μ-dihydroxo-bis[4-hydroxo-2,6-pyridinedicarboxylato-aquoiron(III)] tetrahydrate. J Am Chem Soc 98:1425-1433.
66. Thomann H, Bernardo M, McCormick JM, Pulver S, Andersson KK, Lipscomb JD, Solomon EI. 1993. Pulsed EPR studies of mixed valence [Fe(II)Fe(III)] forms of hemerythrin and methane monooxygenase: Evidence for a hydroxide bridge. J Am Chem Soc 115:8881-8882.
67. Tsien HC, Brusseau GA, Hanson RS, Wackett LP. 1989. Biodegradation of trichloroethylene by Methylosinus trichosporium OB3b. Appl Environ Microbiol 55:3155-3161.
68. Wallar BJ, Lipscomb JD. 1996. Dioxygen activation by enzymes containing binuclear non-heme iron clusters. Chem Rev 96(7):2625-2657.
69. Woodland MP, Dalton H. 1984. Purification and characterization of component A of the methane monooxygenase from Methylococcus capsulatus Bath. J Biol Chem 259:53-59.
70. 3. J Am Chem Soc 116:3653-3654.