Structures of the flavocytochrome p-cresol methylhydroxylase and its enzyme-substrate complex: Gated substrate entry and proton relays support the proposed catalytic mechanism

Journal of Molecular Biology

Volumn 295, Issue 2, 2000, Pages 357-374

  Cunane, Louise M ^a   Chen, Zhi Wei ^a   Shamala, N ^a   Mathews, F Scott ^a   Cronin, Ciarán N ^b   Mcintire, William S ^b,c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Electron transfer; Enzyme catalysis; FAD; Heme; Oxidation reduction

Indexed keywords

CRESOL; CYTOCHROME C OXIDASE; FLAVOCYTOCHROME P CRESOL METHYLHYDROXYLASE; HEME; OXYGEN; PROTOCATECHUIC ACID; QUERCETIN; UNCLASSIFIED DRUG; WATER;

ARTICLE; BIODEGRADATION; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; GENE SEQUENCE; HYDROGEN BOND; METABOLISM; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTON TRANSPORT; PSEUDOMONAS PUTIDA;

PSEUDOMONAS; PSEUDOMONAS PUTIDA;

EID: 0034645779     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3290     Document Type: Article

References (45)

1. Benson T. E., Walsh C. T., Hogle J. M. The structure of the substrate-free form of MurB, an essential enzyme for the synthesis of bacterial cell walls. Structure. 4:1996;47-54.
2. Bethge P. H. VAX adaptation of the ROCKS crystallographic program system. J. Appl. Crystallog. 17:1984;215.
3. Brünger A. T. X-PLOR Version 3.1: A System for X-Ray Crystallography and NMR. 1992;Yale University Press, New Haven and London.
4. Brünger A. T., Adams P. D., Clore G. M., DeLano W. L., Gros P., Grosse-Kunstleve R. W., Jiang J. S., Kuszewski J., Nilges M., Pannu N. S., Read R. J., Rice L. M., Simonson T., Warren G. L. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
5. Bugg T. D., Walsh C. T. Intracellular steps of bacterial cell wall peptidoglycan biosynthesis: enzymology, antibiotics, and antibiotic resistance. Nature Prod. Rep. 9:1992;199-215.
6. Carson M. Ribbons. Methods Enzymol. 277:1997;493-505.
7. 5 at 2. 5 Å resolution. J. Mol. Biol. 184:1985;279-295.
8. Causer M. J., Hopper D. J., McIntire W. S., Singer T. P. Azurin from Pseudomonas putida: an electron acceptor from p-cresol methylhydroxylase. Biochem. Soc. Trans. 12:1984;1131-1132.
9. Cronin C. N., McIntire W. S. pUCP-Nco and pUCP-Nde: Escherichia-Pseudomonas shuttle vectors for recombinant protein expression in Pseudomonas. Anal. Biochem. in the press:1999.
10. Cronin C. N., Kim J., Fuller J. H., Zhang X., McIntire W. S. Organization and sequences of p-hydroxybenzaldehyde dehydrogenase and other plasmid encoded genes for early enzymes of the p-cresol degradative pathway in Pseudomonas putida NCIMB 9866 and 9869. DNA Seq. 10:1999;7-17.
11. Dickerson R. E. Cytochrome c and the evolution of energy metabolism. Sci. Am. 242:1980;137-153.
12. Engst S., Kuusk V., Efimov I., Cronin C., McIntire W. S. Properties of p-cresol methylhydroxylase flavoprotein overproduced by E. coli. Biochemistry. 1999.
13. Evans S. V. SETOR: hardware lighted three-dimensional solid model representation of macromolecules. J. Mol. Graph. 11:1993;134-138.
14. Fraaije M. W., van Berkel W. J. H., Benen J. A. E., Visser J., Mattevi A. A novel oxidoreductase family sharing a conserved FAD-binding domain. Trends Biochem. Sci. 23:1998;206-207.
15. Gatti D. L., Entsch B., Ballou D. P., Ludwig M. L. pH-dependent structural changes in the active site of p-hydroxybenzoate hydroxylase point to the importance of proton and water movements during catalysis. Biochemistry. 35:1996;567-578.
16. Hamlin R. Multiwire area X-ray diffractometers. Methods Enzymol. 114:1985;416-452.
17. Hodel A., Kim S.-H., Brünger A. T. Model bias in macromolecular crystal structures. Acta Crystallog. sect. A. 48:1992;851-858.
18. Hopper D. J. The hydroxylation of p-cresol and its conversion to p-hydroxybenzaldehyde in Pseudomonas putida. Biochem. Biophys. Res. Commun. 69:1976;462-468.
19. Hopper D. J. Redox potential of the cytochrome c in the flavoprotein p-cresol methylhydroxylase. FEBS Letters. 161:1983;100-102.
20. Hopper D. J., Taylor D. G. The purification and properties of p-cresol-(acceptor) oxidoreductase (hydroxylating), a flavocytochrome from Pseudomonas putida. Biochem. J. 167:1977;155-162.
21. Howard A. J., Nielsen C., Xuong N. H. Software for a diffractometer with multiwire area detector. Methods Enzymol. 114:1985;452-472.
22. Keat M. J., Hopper D. J. p-Cresol and 3,5-xylenol methylhydroxylases in Pseudomonas putida N.C.I.B. 9869. Biochem. J. 175:1978;649-658.
23. Kim J. J., Wu J. Structure of the medium-chain acyl-CoA dehydrogenase from pig liver mitochondria at 3-Å resolution. Proc. Natl Acad. Sci. USA. 85:1988;6677-6681.
24. Kim J., Fuller J. H., Cecchini G., McIntire W. S. Cloning, sequencing and expression of the structural genes for the cytochrome and flavoprotein subunits of p-cresol methylhydroxylase from two strains of Pseudomonas putida. J. Bacteriol. 176:1994;6349-6361.
25. Kim J., Fuller J. H., Kuusk V., Cunane L., Chen Z.-W., Mathews F. S., McIntire W. S. The cytochrome subunit is necessary for covalent FAD attachment to the flavoprotein subunit of p-cresol methylhydroxylase. J. Biol. Chem. 270:1995;31202-31209.
26. Kleywegt G. J., Jones T. A. Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallog. sect. D. 50:1994;178-185.
27. Koerber S. C., McIntire W. S., Bohmont C., Singer T. P. Resolution of the flavocytochrome p-cresol methylhydroxylase into subunits and reconstitution of the enzyme. Biochemistry. 24:1985a;5276-5280.
28. Koerber S. C., Hopper D. J., McIntire W. S., Singer T. P. Formation and properties of flavoprotein-cytochrome hybrids by recombination of subunits from different species. Biochem. J. 231:1985b;383-387.
29. Laskowski R. A., MacArthur M. W., Moss D. S., Thornton J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
30. Mathews F. S., Chen Z.-W., Bellamy H. D., McIntire W. S. The 3-dimensional structure of p-cresol methylhydroxylase (flavocytochrome c) at 3.0 Å resolution. Biochemistry. 30:1991;238-247.
31. 551 from Pseudomonas aeruginosa refined at 1.6 Å resolution and comparison of the two redox forms. J. Mol. Biol. 156:1982;389-409.
32. Mattevi A., Fraaije M. W., Mozzarelli A., Olivi L., Coda A., van Berkel W. J. H. Crystal structures and inhibitor binding in the octameric flavoenzyme vanillyl-alcohol oxidase: the shape of the active-site cavity controls substrate specificity. Structure. 5:1997;907-920.
33. McIntire W., Edmondson D. E., Hopper D. J., Singer T. P. 8 alpha-(O-tyrosyl)flavin adenine dinucleotide, the prosthetic group of bacterial p-cresol methylhydroxylase. Biochemistry. 20:1981;3068-3075.
34. McIntire W. S., Koerber S. C., Bohmont C. W., Singer T. P. Unusual properties of the flavocytochrome p-cresol methylhydroxylase. Bray R. C., Engel P. C., Mayhew S. G. Flavins and Flavoproteins. 1984;643-656 Walter de Gruyter, Berlin, New York.
35. McIntire W., Singer T. P., Smith A. J., Mathews F. S. Amino acid and sequence analysis of the cytochrome and flavoprotein subunits of p-cresol methylhydroxylase. Biochemistry. 25:1986;5975-5981.
36. McIntire W. S., Hopper D. J., Singer T. P. Steady-state and stopped-flow kinetic measurements of the primary deuterium isotope effect in the reaction catalyzed by p-cresol methylhydroxylase. Biochemistry. 26:1987;4107-4117.
37. Mewies M., McIntire W. S., Scrutton N. S. Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Protein Sci. 7:1998;7-20.
38. Murzin A. Structural classification of proteins: new superfamilies. Curr. Opin. Struct. Biol. 6:1996;386-394.
39. Ramachandran G. N., Sasisekharan V. Conformation of polypeptides and proteins. Advan. Protein Chem. 23:1968;283-437.
40. Reeke G. N. The ROCKS system of computer programs for macromolecular crystallography. J. Appl. Crystallog. 17:1984;125-130.
41. Reeve C. D., Carver M. A., Hopper D. J. The purification and characterization of 4-ethylphenol methylenehydroxylase, a flavocytochrome from Pseudomonas putida JD1. Biochem J. 263:1989;431-437.
42. Regan J. J. GREENPATH Version 0.97. 1994.
43. Roussel A., Cambillau C. The TURBO-FRODO graphics package. Silicon Graphics Geometry Partners Directory. 1991.
44. Schreuder H. A., Mattevi A., Obmolova G., Kalk K. H., Hol W. G. J., van der Bolt F. J. T., van Berkel W. J. H. Crystal structures of wild-type p-hydroxybenzoate hydroxylase complexed with 4-aminobenzoate, 2,4-dihydroxybenzoate, and 2-hydroxy-4-aminobenzoate and of the Tyr222Ala mutant complexed with 2-hydroxy-4-aminobenzoate. Evidence for a proton channel and a new binding mode of the flavin ring. Biochemistry. 33:1994;10161-10170.
45. Shamala N., Lim L. W., Mathews F. S., McIntire W., Singer T. P., Hopper D. J. Structure of an intermolecular electron transfer complex: p-cresol methylhydroxylase at 6.0 Å resolution. Proc. Natl Acad. Sci. USA. 83:1986;4626-4630.