What's in a covalent bond?: On the role and formation of covalently bound flavin cofactors

FEBS Journal

Volumn 276, Issue 13, 2009, Pages 3405-3427

  Heuts, Dominic P H M ^a   Scrutton, Nigel S ^b   McIntire, William S ^c,d   Fraaije, Marco W ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

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

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Covalent flavinylation; Flavin; Post translational; Redox potential; Self catalytic

Indexed keywords

6 HYDROXY DEXTRO NICOTINE OXIDASE; ACLACINOMYCIN OXIDASE; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; BIOTIN; CHOLINE OXIDASE; CYTOKININ DEHYDROGENASE; DIMETHYLGLYCINE DEHYDROGENASE; FLAVOPROTEIN; FUMARATE REDUCTASE; GLUCOOLIGOSACCHARIDE OXIDASE; GLUCOSE OXIDASE; HEME; HISTIDINE; MONOMERIC SARCOSINE OXIDASE; QUERCETIN; SARCOSINE DEHYDROGENASE; SARCOSINE OXIDASE; SUCCINATE DEHYDROGENASE; TRIMETHYLAMINE DEHYDROGENASE; UNCLASSIFIED DRUG; VANILLYL ALCOHOL OXIDASE;

AMINO ACID SEQUENCE; CATALYSIS; COVALENT BOND; CRYSTAL STRUCTURE; HUMAN; NECTARINE; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

BACTERIAL PROTEINS; COENZYMES; CRYSTALLOGRAPHY, X-RAY; FLAVINS; FLAVOPROTEINS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 67650480250     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07053.x     Document Type: Review

References (170)

1. Reche P Perham RN (1999) Structure and selectivity in post-translational modification: attaching the biotinyl-lysine and lipoyl-lysine swinging arms in multifunctional enzymes. EMBO J 18, 2673 2682. (Pubitemid 29233940)
2. Argyrou A Blanchard JS (2004) Flavoprotein disulfide reductases: advances in chemistry and function. Prog Nucleic Acid Res Mol Biol 78, 89 142. (Pubitemid 39752478)
3. Xie L van der Donk WA (2001) Homemade cofactors: self-processing in galactose oxidase. Proc Natl Acad Sci USA 98, 12863 12865. (Pubitemid 33051280)
4. McIntire WS (1998) Newly discovered redox cofactors: possible nutritional medical and pharmacological relevance to higher animals. Annu Rev Nutr 18, 145 177. (Pubitemid 28366864)
5. Mure M (2004) Tyrosine-derived quinone cofactors. Acc Chem Res 37, 131 139.
6. Povolotskaia KL (1953) New form of riboflavin bound with proteins. Biokhimia 18, 638 643.
7. Boukine VN (1955) Proceedings of the 3rd International Congress of Biochemistry (Brussels 1955; New York 1956), p. 260.
8. Green DE, Mii S Kohout PM (1955) Studies on the terminal electron transport system I. Succinic dehydrogenase. J Biol Chem 217, 551 568.
9. Kearney EB Singer TP (1955) On the prosthetic group of succinic dehydrogenase. Biochim Biophys Acta 17, 596 597.
10. Kearney EB (1960) Studies on succinic dehydrogenase XII. Flavin component of the mammalian enzyme. J Biol Chem 235, 865 877.
11. Salach J, Walker WH, Singer TP, Ehrenberg A, Hemmerich P, Ghisla S Hartmann U (1972) Studies on succinate dehydrogenase. Site of attachment of the covalently-bound flavin to the peptide chain. Eur J Biochem 26, 267 278.
12. Walker WH, Singer TP, Ghisla S Hemmerich P (1972) Studies on succinate dehydrogenase 8-histidyl-FAD as the active center of succinate dehydrogenase. Eur J Biochem 26, 279 289.
13. Reeve CD, Carver MA Hopper DJ (1990) Stereochemical aspects of the oxidation of 4-ethylphenol by the bacterial enzyme 4-ethylphenol methylenehydroxylase. Biochem J 269, 815 819. (Pubitemid 20236096)
14. Mewies M, McIntire WS Scrutton NS (1998) Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Prot Science 7, 7 20. (Pubitemid 28133742)
15. 1-histidyl FAD. J Biol Chem 280, 38831 38838. (Pubitemid 43853786)
16. Alexeev I, Sultana A, Mäntsälä P, Niemi J Schneider G (2007) Aclacinomycin oxidoreductase (AknOx) from the biosynthetic pathway of the antibiotic aclacinomycin is an unusual flavoenzyme with a dual active site. Proc Natl Acad Sci USA 104, 6170 6175. (Pubitemid 47186067)
17. Winkler A, Hartner F, Kutchan TM, Glieder A Macheroux P (2006) Biochemical evidence that berberine bridge enzyme belongs to a novel family of flavoproteins containing a bi-covalently attached FAD cofactor. J Biol Chem 281, 21276 21285. (Pubitemid 44115467)
18. Rand T, Qvist KB, Walter CP Poulsen CH (2006) Characterization of the flavin association in hexose oxidase from Chondrus crispus. FEBS J 273, 2693 2703. (Pubitemid 43920249)
19. Li YS, Ho JY, Huang CC, Lyu SY, Lee CY, Huang YT, Wu CJ, Chan HC, Huang CJ, Hsu NS et al. (2007) A unique flavin mononucleotide-linked primary alcohol oxidase for glycopeptide A40926 maturation. J Am Chem Soc 129, 13384 13385.
20. Taura F, Sirikantaramas S, Shoyama Y, Shoyama Y Morimoto S (2007) Phytocannabinoids in Cannabis sativa: recent studies on biosynthetic enzymes. Chem Biodivers 4, 1649 1663. (Pubitemid 47377198)
21. Heuts DPHM, Janssen DB Fraaije MW (2007) Changing the substrate specificity of a chitooligosaccharide oxidase from Fusarium graminearum by model-inspired site-directed mutagenesis. FEBS Lett 581, 4905 4909. (Pubitemid 47531760)
22. +-translocating NADH-quinone reductase from Vibrio alginolyticus. FEBS Lett 488, 5 8. (Pubitemid 32332796)
23. Juárez O, Nilges MJ, Gillespie P, Cotton J Barquera B (2008) Riboflavin is an active redox cofactor in the Na+-pumping NADH:quinone oxidoreductase (Na+-NQR) from Vibrio cholerae. J Biol Chem 283, 33162 33167.
24. Barquera B, Häse CC Gennis RB (2001) Expression and mutagenesis of the NqrC subunit of the NQR respiratory Na+ pump from Vibrio cholerae with covalently attached FMN. FEBS Lett 492, 45 49. (Pubitemid 32206717)
25. Fraaije MW, Van Berkel WJH, Benen JA, Visser J Mattevi A (1998) A novel oxidoreductase family sharing a conserved FAD-binding domain. Trends Biochem Sci 23, 206 207. (Pubitemid 28302616)
26. Leferink NG, Heuts DPHM, Fraaije MW van Berkel WJH (2008) The growing VAO flavoprotein family. Arch Biochem Biophys 474, 292 301.
27. Hatzinikolaou DG, Hansen OC, Macris BJ, Tingey A, Kekos D, Goodenough P Stougaard P (1996) A new glucose oxidase from Aspergillus niger: characterization and regulation studies of enzyme and gene. Appl Microbiol Biotechnol 46, 371 381. (Pubitemid 26390836)
28. Gadda G, Wels G, Pollegioni L, Zucchelli S, Ambrosius D, Pilone MS Ghisla S (1997) Characterization of cholesterol oxidase from Streptomyces hygroscopicus and Brevibacterium sterolicum. Eur J Biochem 250, 369 376. (Pubitemid 28012676)
29. Motteran L, Pilone MS, Molla G, Ghisla S Pollegioni L (2001) Cholesterol oxidase from Brevibacterium sterolicum. J Biol Chem 276, 18024 18030.
30. Kranz R, Lill R, Goldman B, Bonnard G Merchant S (1998) Molecular mechanisms of cytochrome c biogenesis: three distinct systems. Mol Microbiol 29, 383 396. (Pubitemid 28330775)
31. Denis L, Grossemy M, Douce R Alban C (2002) Molecular characterization of a second copy of holocarboxylase synthetase gene (hcs2) in Arabidopsis thaliana. J Biol Chem 277, 10435 10444. (Pubitemid 34968164)
32. Walsh C (1978) Enzymatic Reaction Mechanisms. WH Freeman & Company, San Francisco.
33. Walsh C (1980) Flavin coenzymes: at the crossroads of biological redox chemistry. Acc Chem Res 13, 148 155.
34. Bullock FJ Jardetzkey O (1965) An experimental demonstration of the nuclear magnetic resonance assignments in the 67-dimethylisoalloxazine nucleus. J Org Chem 30, 2056 2057.
35. Frost JW Rastetter WH (1980) Biomemetic 8α functionalization of riboflavin. J Am Chem Soc 102, 7157 7159.
36. Wagner MA, Khanna P Jorns MS (1999) Structure of the flavocoenzyme of two homologous amine oxidases: monomeric sarcosine oxidase and N-methyltryptophan oxidase. Biochemistry 38, 5588 5595.
37. Hassan-Abdallah A, Bruckner RC, Zhao G Jorns MS (2005) Biosynthesis of covalently bound flavin: isolation and in vitro flavinylation of the monomeric sarcosine oxidase apoprotein. Biochemistry 44, 6452 6462. (Pubitemid 40593796)
38. Kim J, Fuller JH, Kuusk V, Canane L, Chen ZW, Mathews FS McIntire WS (1995) The cytochrome subunit is necessary for covalent FAD attachment to the flavoprotein subunit of p-cresol methylhydroxylase. J Biol Chem 270, 31202 31209. (Pubitemid 26018399)
39. Cunane LM, Chen Z-W, McIntire WS Mathews FS (2005) p-Cresol methylhydroxylase: alteration of the structure of the flavoprotein subunit upon its binding to the cytochrome subunit. Biochemistry 44, 2963 2973. (Pubitemid 40293671)
40. Efimov I McIntire WS (2008) The redox potentials of the bound FAD analogs correlate with the covalent flavinylation rates for the flavoprotein subunit of p-cresol methylhydroxylase. In Flavins & Flavoproteins 2008. Proceedings from the 16th International Symposium Jaca Spain (Frago S, Gomez-Moreno C Medina M, eds pp. 57 62. Prensas Universitarias de Zaragossa, Zaragossa.
41. Brandsch R Bichler V (1987) Covalent flavinylation of 6-hydroxy-d-nicotine oxidase involves an energy-requiring process. FEBS Lett 224, 121 124.
42. Brandsch R, Bichler V Krauss B (1989) Binding of FAD to 6-hydroxy-d-nicotine oxidase apoenzyme prevents degradation of the holoenzyme. Biochem J 258, 187 192. (Pubitemid 19062268)
43. Mauch L, Bichler V Brandsch R (1989) Site-directed mutagenesis of the FAD-binding histidine of 6-hydroxy-d-nicotine oxidase. Consequences on flavinylation and enzyme activity. FEBS Lett 257, 86 88. (Pubitemid 19261768)
44. Brandsch R Bichler V (1991) Autoflavinylation of apo 6-hydroxy-d-nicotine oxidase. J Biol Chem 266, 19056 19062.
45. Koetter JWA Schulz GE (2005) Crystal structure of 6-hydroxy-d-nicotine oxidase from Arthrobacter nicotinovorans. J Mol Biol 352, 418 428. (Pubitemid 41207792)
46. Möhler H, Brühmüller M Decker K (1972) Covalently bound flavin in D-6-hydroxynicotine oxidase from Arthrobacte oxidans. Identification of the 8-(N-3-histidyl)-riboflavin-linkage between FAD and apoenzyme. Eur J Biochem 29, 152 155.
47. Fraaije MW, Van den Heuvel RHH, Van Berkel WJH Mattevi A (2000) Structural analysis of flavinylation in vanillyl-alcohol oxidase. J Biol Chem 275, 38654 38658. (Pubitemid 32009196)
48. Jin J, Mazon H, van den Heuvel RHH, Heck AJ, Janssen DB Fraaije MW (2008) Covalent flavinylation of vanillyl-alcohol oxidase is an autocatalytic process. FEBS J 275, 5191 5200.
49. Brizio C, Brandsch R, Douka M, Wait R Barile M (2008) The purified recombinant precursor of rat mitochondrial dimethylglycine dehydrogenase binds FAD via an autocatalytic reaction. Int J Biol Macromol 42, 455 462.
50. Scrutton NS, Packman LC, Mathews FS, Rohlfs RJ Hille R (1994) Assembly of redox centers in the trimethylamine dehydrogenase of bacterium W3A1: properties of the wild-type enzyme and a C30A mutant expressed from a cloned gene in Escherichia coli. J Biol Chem 269, 13942 13950.
51. Trickey P, Wagner MA, Jorns MS Mathews FS (1999) Monomeric sarcosine oxidase: structure of a covalently flavinylated amine oxidizing enzyme. Structure 7, 331 345. (Pubitemid 29159692)
52. Efimov I, Cronin CN, Bergmann DJ, Kuusk V McIntire WS (2004) Insight into covalent flavinylation and catalysis from redox spectral and kinetic analysis of the R474K mutant of the flavoprotein subunit of p-cresol methylhydroxylase. Biochemistry 43, 6138 6148. (Pubitemid 38669482)
53. Van den Heuvel RHH, Fraaije MW, Mattevi A van Berkel WJH (2000) Asp-170 is crucial for the redox properties of vanillyl-alcohol oxidase. J Biol Chem 275, 14799 14808. (Pubitemid 30337191)
54. Ferri S, Miura S, Sakaguchi A, Ishimura F, Tsugawa W Sode K (2004) Cloning and expression of fructosyl-amine oxidase from marine yeast Pichia species N1-1. Biotechnology (NY) 6, 625 632. (Pubitemid 40747857)
55. Liaw S, Lee DY, Chow LP, Lau GX Su SN (2001) Structural characterization of the 60-kDa bermuda grass pollen isoallergens, a covalent flavoprotein. Biochem Biophys Res Commun 280, 738 743. (Pubitemid 32924492)
56. Otto A, Stähle I, Klein R, Berg PA, Pankuweit S Brandsch R (1998) Anti-mitochondrial antibodies in patients with dilated cardiomyopathy (anti-M7) are directed against flavoenzymes with covalently bound FAD. Clin Exp Immunol 111, 541 547. (Pubitemid 28160898)
57. Williamson G Edmondson DE (1985) Effect of pH on oxidation-reduction potentials of 8a-N-imidazole-substituted flavins. Biochemistry 24, 7790 7797. (Pubitemid 16140516)
58. Ghisla S, Kenney WC, Knappe WR, McIntire WS Singer TP (1980) Chemical synthesis and some properties of 6-substituted flavins. Biochemistry 19, 2537 2544.
59. McIntire WS, Edmondson DE, Hopper DJ Singer TP (1981) 8α-(O-Tyrosyl) flavin adenine dinucleotide: the prosthetic group of bacterial p-cresol methylhydroxylase. Biochemistry 20, 3068 3075.
60. Edmondson DE De Francesco R (1991) Structure synthesis and physical properties of covalently bound flavins and 6- and 8-hydroxyflavins. In Chemistry and Biochemistry of Flavoenzymes (Müller F, ed pp. 73 103. CRC Press, Boca Raton, FL.
61. Edmondson DE Ghisla S (1999) Electronic effects of 7 and 8 ring substituents as predictors of flavin oxidation-reduction potentials. In Flavins and Flavoproteins (Ghisla S, Kroneck P, Macheroux P Sund H, eds pp. 71 76. Rudolf Weber Agency for Scientific Publications, Berlin.
62. Fraaije MW, Van den Heuvel RHH, Van Berkel WJH Mattevi A (1999) Covalent flavinylation is essential for efficient redox catalysis in vanillyl-alcohol oxidase. J Biol Chem 274, 35514 35520. (Pubitemid 129512845)
63. Efimov I, Cronin CN McIntire WS (2001) Effects of non-covalent and covalent FAD binding on the redox and catalytic properties of p-cresol methylhydroxylase. Biochemistry 40, 2155 2166. (Pubitemid 32165686)
64. Thiemer B, Andreesen JR Schräder T (2001) The NADH-dependent reductase of a putative multicomponent tetrahydrofuran mono-oxygenase contains a covalently bound FAD. Eur J Biochem 268, 3774 3782. (Pubitemid 32862917)
65. Lim L, Molla G, Guinn N, Ghisla S, Pollegioni L Vrielink A (2006) Structural and kinetic analyses of the H121A mutant of cholesterol oxidase. Biochem J 400, 13 22. (Pubitemid 44763815)
66. Kujawa M, Ebner H, Leitner C, Hallberg BM, Prongjit M, Sucharitakul J, Ludwig R, Rudsander U, Peterbauer C, Chaiyen P et al. (2006) Structural basis for substrate binding and regioselective oxidation of monosaccharides at C3 by pyranose-2-oxidase. J Biol Chem 281, 35104 35115. (Pubitemid 46036550)
67. Hassan-Abdallah A, Zhao G Jorns MS (2006) Role of the covalent flavin linkage in monomeric sarcosine oxidase. Biochemistry 45, 9454 9462. (Pubitemid 44223249)
68. Winkler A, Kutchan TM Macheroux P (2007) 6-S-cysteinylation of bi-covalently attached FAD in berberine bridge enzyme tunes the redox potential for optimal activity. J Biol Chem 282, 24437 24443. (Pubitemid 47328015)
69. Winkler A, Lyskowski A, Riedl S, Puhl M, Kutchan TM, Macheroux P Gruber K (2008) A concerted mechanism for berberine bridge enzyme. Nat Chem Biol 4, 739 741.
70. Heuts DPHM, Winter RT, Damsma GE, Janssen DB Fraaije MW (2008) The role of double covalent flavinylation in chitooligosaccharide oxidase. Biochem J 413, 175 183.
71. Heuts DPHM, Van Hellemond EW, Janssen DB Fraaije MW (2007) Discovery, characterization and kinetic analysis of an alditol oxidase from Streptomyces coelicolor. J Biol Chem 282, 20283 20291. (Pubitemid 47100003)
72. Nandigama RK Edmondson DE (2000) Influence of FAD structure on its binding and activity with the C406A mutant of recombinant human liver monoamine oxidase A. J Biol Chem 275, 20527 20532. (Pubitemid 30457634)
73. Van Hellemond EW, Mazon H, Heck AJ, van den Heuvel RHH, Heuts DPHM, Janssen DB Fraaije MW (2008) ADP competes with FAD binding in putrescine oxidase. J Biol Chem 283, 28259 28264.
74. Caldinelli L, Iametti S, Barbiroli A, Bonomi F, Fessas D, Molla G, Pilone MS Pollegioni L (2005) Dissecting the structural determinants of the stability of cholesterol oxidase containing covalently bound flavin. J Biol Chem 280, 22572 22581. (Pubitemid 40853160)
75. Eschenbrenner M, Chlumsky LJ, Khanna P, Strasser F Jorns MS (2001) Organization of the multiple coenzymes and subunits and role of the covalent flavin link in the complex heterotetrameric sarcosine oxidase. Biochemistry 40, 5352 5367. (Pubitemid 32458235)
76. Cecchini G (2003) Function and structure of complex II of the respiratory chain. Annu Rev Biochem 72, 77 109. (Pubitemid 36930442)
77. Steenkamp DJ Mallinson J (1976) Trimethylamine dehydrogenase from a methylotrophic bacterium I. Isolation and steady-state kinetics. Biochim Biophys Acta 429, 705 719.
78. Huang L, Scrutton NS Hille RJ (1996) Reaction of the C30A mutant of trimethylamine dehydrogenase with diethylmethylamine. J Biol Chem 271, 13401 13406. (Pubitemid 26185380)
79. Lu X, Nikolic D, Mitchell DJ, Van Breemen RB, Mersfelder JA, Hille R Silverman RB (2003) A mechanism for substrate-induced formation of 6-hydroxyflavin mononucleotide catalyzed by C30A trimethylamine dehydrogenase. Bioorg Med Chem Lett 13, 4129 4132. (Pubitemid 37338461)
80. Massey V Husain H (1978) Reversible resolution of flavoproteins into apoproteins and free flavins. Methods Enzymol 53, 429 437.
81. Hefti MH, Vervoort J van Berkel WJ (2003) Deflavination and reconstitution of flavoproteins. Eur J Biochem 270, 4227 4242.
82. Ghisla S Massey V (1986) New flavins for old: artificial flavins as active site probes of flavoproteins. Biochem J 239, 1 12.
83. Efimov I McIntire WS (2004) A study of the spectral and redox properties and covalent flavinylation of the flavoprotein component of p-cresol methylhydroxylase reconstituted with FAD analogues. Biochemistry 43, 10532 10546. (Pubitemid 39079324)
84. Efimov I McIntire WS (2005) Relationship between charge-transfer interactions, redox potentials and catalysis for different forms of the flavoprotein component of p-cresol methylhydroxylase. J Am Chem Soc 127, 732 741. (Pubitemid 40174398)
85. Moore EG, Cardemil E Massey V (1978) Production of a covalent flavin linkage in lipoamide dehydrogenase. Reaction with 8-Cl-FAD. J Biol Chem 253, 6413 6422. (Pubitemid 9025320)
86. Massey V Hemmerich P (1980) Active-site probes of flavoproteins. Biochem Soc Trans 8, 246 257.
87. Macheroux P, Plattner HJ, Romaguera A Diekmann H (1993) FAD and substrate analogs as probes for lysine N6-hydroxylase from Escherichia coli EN 222. Eur J Biochem 213, 995 1002. (Pubitemid 23152207)
88. Raibekas AA, Fukui K Massey V (1999) Design and properties of human d-amino acid oxidase with covalently attached flavin. Proc Natl Acad Sci USA 97, 3089 3093.
89. Negri A, Buckmann AF, Tedeschi G, Stocker A, Ceciliani F, Treu C Ronchi S (1999) Covalent flavinylation of l-aspartate oxidase from Escherichia coli using N6-(6-carboxy-hexyl)-FAD succinimidoester. J Prot Chem 18, 671 676. (Pubitemid 30010650)
90. DeLano WL (2002) The PyMOL molecular graphics system. http://www.pymol.org.
91. Byron CM, Stankovich MT, Husain M Davidson VL (1989) Unusual redox properties of electron-transfer flavoprotein from Methylophilus methylotrophus. Biochemistry 28, 8582 8587.
92. Pace C Stankovich M (1986) Oxidation-reduction properties of glycolate oxidase. Biochemistry 25, 2516 2522.
93. Husain M, Stankovich MT Fox BG (1984) Measurement of the oxidation-reduction potentials for one-electron and two-electron reduction of electron-transfer flavoprotein from pig liver. Biochem J 219, 1043 1047.
94. Meyer TE, Bartsch RG, Caffrey MS Cusanovich MA (1991) Redox potentials of flavocytochromes c from the phototrophic bacteria Chromatium vinosum and Chlorobium thiosulfatophilum. Arch Biochem Biophys 287, 128 134.
95. Kay CJ Lippay EW (1992) Mutation of the heme-binding crevice of flavocytochrome b2 from Saccharomyces cerevisiae: altered heme potential and absence of redox cooperativity between heme and FMN centers. Biochemistry 31, 11376 11382.
96. Gomes CM, Silva G, Oliveira S, LeGall J, Liu MY, Xavier AV, Rodrigues-Pousada C Teixeira M (1997) Studies on the redox centers of the terminal oxidase from Desulfovibrio gigas and evidence for its interaction with rubredoxin. J Biol Chem 272, 22502 22508. (Pubitemid 27386060)
97. Vinod MP, Bellur P Becker DF (2002) Electrochemical and functional characterization of the proline dehydrogenase domain of the PutA flavoprotein from Escherichia coli. Biochemistry 41, 6525 6532. (Pubitemid 34526020)
98. Sabaj KM Stankovich MT (1996) Exploring the redox properties of MCAD bound to two analogs acetoacetyl-CoA and hexadienoyl-CoA. In Flavins and Flavoproteins 1996 (Stevenson KJ, Massey V Willams CH Jr. eds pp. 645 648. University of Calgary Press, Calgary, AB, Canada.
99. Chaiyen P, Brissette P, Ballou DP Massey V (1997) Thermodynamics and reduction kinetics properties of 2-methyl-3-hydroxypyridine-5-carboxylic acid oxygenase. Biochemistry 36, 2612 2621. (Pubitemid 27106655)
100. Tegoni M, Silvestrini MC, Guigliarelli B, Asso M, Brunori M Bertrand P (1998) Temperature-jump and potentiometric studies on recombinant wild type and Y143F and Y254F mutants of Saccharomycescerevisiae flavocytochrome b2: role of the driving force in intramolecular electron transfer kinetics. Biochemistry 37, 12761 12771. (Pubitemid 28433507)
101. Wille G, Ritter M, Weiss MS, König S, Mäntele W Hübner G (2005) The role of Val-265 for flavin adenine dinucleotide (FAD) binding in pyruvate oxidase: FTIR kinetic and crystallographic studies on the enzyme variant V265A. Biochemistry 44, 5086 5094. (Pubitemid 40471224)
102. Negri A, Tedeschi G, Ceciliani F Ronchi S (1999) Purification of beef kidney d-aspartate oxidase overexpressed in Escherichia coli and characterization of its redox potentials and oxidative activity towards agonists and antagonists of excitatory amino acid receptors. Biochim Biophys Acta 1431, 212 222. (Pubitemid 29182736)
103. Van den Berghe-Snorek S Stankovich MT (1985) Thermodynamic control of D-amino acid oxidase by benzoate binding. J Biol Chem 260, 3373 3379.
104. Mancini-Samuelson GJ, Kieweg V, Sabaj KM, Ghisla S Stankovich MT (1998) Redox properties of human medium-chain acyl-CoA dehydrogenase modulation by charged active-site amino acid residues. Biochemistry 37, 14605 14612. (Pubitemid 28489069)
105. Parsonage D, Luba J, Mallett TC Claiborne A (1998) The soluble alpha-glycerophosphate oxidase from Enterococcus casseliflavus. Sequence homology with the membrane-associated dehydrogenase and kinetic analysis of the recombinant enzyme. J Biol Chem 273, 23812 23822. (Pubitemid 28435716)
106. Williamson G, Edmondson DE Müller F (1988) Oxidation-reduction potential studies on p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens. Biochim Biophys Acta 953, 258 262.
107. Krishnan N Becker DF (2005) Characterization of a bifunctional PutA homologue from Bradyrhizobiumjaponicum and identification of an active site residue that modulates proline reduction of the flavin adenine dinucleotide cofactor. Biochemistry 44, 9130 9139. (Pubitemid 40943228)
108. Stankovich M Fox B (1983) Redox potentials of the flavoprotein lactate oxidase. Biochemistry 22, 4466 4472.
109. Turner KL, Doherty MK, Heering HA, Armstrong FA, Reid GA Chapman SK (1999) Redox properties of flavocytochrome c3 from Shewanella frigidimarina NCIM. Biochemistry 38, 3302 3309.
110. Tedeschi G, Chen S Massey V (1995) DT-diaphorase: redox potential steady-state and rapid reaction studies. J Biol Chem 270, 1198 1204.
111. 2+/calmodulin of constitutive nitric-oxide synthases. J Biol Chem 281, 34246 34257. (Pubitemid 46036633)
112. Müh U, Cinkaya I, Albracht SP Buckel W (1996) 4-Hydroxybutyryl-CoA dehydratase from Clostridium aminobutyricum: characterization of FAD and iron-sulfur clusters involved in an overall non-redox reaction. Biochemistry 35, 11710 11718. (Pubitemid 26303689)
113. Navarro F, Martín-Figueroa E, Candau P Florencio FJ (2000) Ferredoxin-dependent iron-sulfur flavoprotein glutamate synthase (GlsF) from the Cyanobacterium Synechocystis sp. PCC 6803: expression and assembly in Escherichia coli. Arch Biochem Biophys 379, 267 276. (Pubitemid 30637463)
114. Lund J Dalton H (1985) Further characterisation of the FAD and Fe2S2 redox centres of component C of the NADH: acceptor reductase of the soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur J Biochem 147, 291 296.
115. Burns KD, Pieper PA, Liu HW Stankovich MT (1996) Studies of the redox properties of CDP-6-deoxy-l-threo-d-glycero-4-hexulose-3-dehydrase (E1) and CDP-6-deoxy-l-threo-d-glycero-4-hexulose-3-dehydrase reductase (E3): two important enzymes involved in the biosynthesis of ascarylose. Biochemistry 35, 7879 7889.
116. Tedeschi G, Zetta L, Negri A, Mortarino M, Ceciliani F Ronchi S (1997) Redox potentials and quinone reductase activity of l-aspartate oxidase from Escherichia coli. Biochemistry 36, 16221 16230. (Pubitemid 28065037)
117. Martínez-Júlvez M, Nogués I, Faro M, Hurley JK, Brodie TB, Mayoral T, Sanz-Aparicio J, Hermoso JA, Stankovich MT, Medina M et al. (2001) Role of a cluster of hydrophobic residues near the FAD cofactor in Anabaena PCC 7119 ferredoxin-NADP+ reductase for optimal complex formation and electron transfer to ferredoxin. J Biol Chem 276, 27498 27510.
118. Einarsdottir GH, Stankovich MT, Powlowski J, Ballou DP Massey V (1989) Regulation of oxidation-reduction potentials of anthranilate hydroxylase from Trichosporon cutaneum by substrate and effector binding. Biochemistry 28, 4161 4168.
119. Stewart RC Massey V (1985) Potentiometric studies of native and flavin-substituted old yellow enzyme. J Biol Chem 260, 13639 13647. (Pubitemid 16233215)
120. Coves J, Zeghouf M, Macherel D, Guigliarelli B, Asso M Fontecave M (1997) Flavin mononucleotide-binding domain of the flavoprotein component of the sulfite reductase from Escherichia coli. Biochemistry 36, 5921 5928. (Pubitemid 27214945)
121. Veine DM, Arscott LD Williams CH Jr. (1998) Redox potentials for yeast Escherichia coli and human glutathione reductase relative to the NAD+/NADH redox couple: enzyme forms active in catalysis. Biochemistry 37, 15575 15582. (Pubitemid 28516022)
122. Ludwig ML, Pattridge KA, Metzger AL Dixon MM (1997) Control of oxidation-reduction potentials in flavodoxin from Clostridium beijerinckii: the role of conformation changes. Biochemistry 36, 1259 1280. (Pubitemid 27074950)
123. Porras AG Palmer G (1982) The room temperature potentiometry of xanthine oxidase pH-dependent redox behavior of the flavin molybdenum and iron-sulfur centers. J Biol Chem 257, 11617 11626.
124. Davis CA Barber MJ (2004) Cytochrome b5 oxidoreductase: expression and characterization of the original familial ideopathic methemoglobinemia mutations E255- and G291D. Arch Biochem Biophys 425, 123 132. (Pubitemid 38542804)
125. Shaw JP Harayama S (1992) Purification and characterisation of the NADH: acceptor reductase component of xylene monooxygenase encoded by the TOL plasmid pWW0 of Pseudomonas putida mt-2. Eur J Biochem 209, 51 61.
126. Klopprogge K Schmitz RA (1999) NifL of Klebsiella pneumoniae: redox characterization in relation to the nitrogen source. Biochim Biophys Acta 1431, 462 470. (Pubitemid 29231999)
127. Becker DF, Leartsakulpanich U, Surerus KK, Ferry JG Ragsdale SW (1998) Electrochemical and spectroscopic properties of the iron-sulfur flavoprotein from Methanosarcina thermophila. J Biol Chem 273, 26462 26469. (Pubitemid 28471654)
128. Kay CJ, Barber MJ, Notton BA Solomonson LP (1989) Oxidation-reduction midpoint potentials of the flavin haem and Mo-pterin centres in spinach (Spinacia oleracea L.) nitrate reductase. Biochem J 263, 285 287.
129. Ukaegbu UE, Henery S Rosenzweig AC (2006) Biochemical characterization of MmoS, a sensor protein involved in copper-dependent regulation of soluble methane monooxygenase. Biochemistry 45, 10191 10198. (Pubitemid 44384794)
130. Hunt J, Massey V, Dunham WR Sands RH (1993) Redox potentials of milk xanthine dehydrogenase. Room temperature measurement of the FAD and 2Fe/2S center potentials. J Biol Chem 268, 18685 18691.
131. Pueyo JJ, Gomez-Moreno C Mayhew SG (1991) Oxidation-reduction potentials of ferredoxin-NADP+ reductase and flavodoxin from Anabaena PCC 7119 and their electrostatic and covalent complexes. Eur J Biochem 202, 1065 1071.
132. Gadda G Fitzpatrick PF (1998) Biochemical and physical characterization of the active FAD-containing form of nitroalkane oxidase from Fusarium oxysporum. Biochemistry 37, 6154 6164. (Pubitemid 28196773)
133. Bandeiras TM, Salgueiro CA, Huber H, Gomes CM Teixeira M (2003) The respiratory chain of the thermophilic archaeon Sulfolobus metallicus: studies on the type-II NADH dehydrogenase. Biochim Biophys Acta 1557, 13 19. (Pubitemid 36254730)
134. Gomes CM, Bandeiras TM Teixeira M (2001) A new type-II NADH dehydrogenase from the archaeon Acidianus ambivalens: characterization and in vitro reconstitution of the respiratory chain. J Bioenerg Biomembr 33, 1 8. (Pubitemid 32294787)
135. Gomez-Moreno C, Choy M Edmondson DE (1979) Purification and properties of the bacterial flavoprotein: thiamin dehydrogenase. J Biol Chem 254, 7630 7635.
136. Newton-Vinson P Edmondson DE (1999) High-level expression structural kinetic and redox characterization of recombinant human liver monoamine oxidase B. In Flavins and Flavoproteins 1999 (Ghisla S, Kroneck P, Macheroux P Sund H eds pp. 431 434. Rudolf Weber Agency for Scientific Publications, Berlin.
137. Frébortová J, Fraaije MW, Galuszka P, Sebela M, Pec P, Hrbác J, Novák O, Bilyeu KD, English JT Frébort I (2004) Catalytic reaction of cytokinin dehydrogenase: preference for quinones as electron acceptors. Biochem J 380, 121 130. (Pubitemid 38725736)
138. Wu X, Palfey BA, Mossine VV Monnier VM (2001) Kinetic studies: mechanism and substrate specificity of amadoriase I from Aspergillus sp. Biochemistry 40, 12886 12895. (Pubitemid 33026635)
139. Gutman M, Bonomi F, Pagani S, Cerletti P Kroneck P (1980) Modulation of the flavin redox potential as mode of regulation of succinate dehydrogenase activity. Biochim Biophys Acta 591, 400 408.
140. Huang CH, Winkler A, Chen CL, Lai WL, Tsai YC, Macheroux P Liaw SH (2008) Functional roles of the 6-S-cysteinyl 8alpha-N1-histidyl FAD in glucooligosaccharide oxidase from Acremonium strictum. J Biol Chem 283, 30990 30996.
141. Coulombe R, Yue KQ, Ghisla S Vrielink A (2001) Oxygen access to the active site of cholesterol oxidase through a narrow channel is gated by an Arg-Glu pair. J Biol Chem 276, 30435 30441.
142. Forneris F, Heuts DPHM, Delvecchio M, Rovida S, Fraaije MW Mattevi A (2008) Structural analysis of the catalytic mechanism and stereoselectivity in Streptomyces coelicolor alditol oxidase. Biochemistry 47, 978 985.
143. Malito E, Coda A, Bilyeu KD, Fraaije MW Mattevi A (2004) Structures of Michaelis and product complexes of plant cytokinin dehydrogenase: implications for flavoenzyme catalysis. J Mol Biol 341, 1237 1249. (Pubitemid 39092312)
144. Jin J, Mazon H, van den Heuvel RHH, Janssen DB Fraaije MW (2007) Discovery of a eugenol oxidase from Rhodococcus sp. strain RHA1. FEBS J 274, 2311 2321. (Pubitemid 46633459)
145. Kenney WC, Edmondson DE, Singer TP, Nakagawa H, Asano A Sato R (1976) Identification of the covalently bound flavin of l-gulono-gamma-lactone oxidase. Biochem Biophys Res Commun 71, 1194 1200.
146. Shimizu M, Murakawa S Takahashi T (1977) The covalently bound flavin prosthetic group of d-gluconolactone dehydrogenase of Penicillium cyaneo-fulvum. Agric Biol Chem 41, 2107 2108. (Pubitemid 8232289)
147. Kenney WC, Edmondson DE, Singer TP, Nishikimi M, Noguchi E Yagi K (1979) Identification of the covalently-bound flavin of l-galactonolactone oxidase from yeast. FEBS Lett 97, 40 42.
148. Huh WK, Kim ST, Yang KS, Seok YJ, Hah YC Kang SO (1994) Characterisation of d-arabinono-14-lactone oxidase from Candida albicans ATCC 10231. Eur J Biochem 225, 1073 1079. (Pubitemid 24342553)
149. Hiraga K, Kitazawa M, Kaneko N Oda K (1997) Isolation and some properties
150. Yamashita M, Omura H, Okamoto E, Furuya Y, Yabuuchi M, Fukahi K Murooka Y (2000) Isolation characterization and molecular cloning of a thermostable xylitol oxidase from Streptomyces sp IKD472. J Biosci Bioeng 89, 350 360. (Pubitemid 30318036)
151. Carter CJ Thornburg RW (2004) Tobacco nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiol 134, 460 469. (Pubitemid 38178717)
152. Decker KF (1991) Covalent flavoproteins. In Chemistry and Biochemistry of Flavoenzymes, vol II (Müller F ed pp. 343 375. CRC Press, Boca Raton, FL.
153. Halada P, Leitner C, Sedmera P, Haltrich D Volc J (2003) Identification of the covalent flavin adenine dinucleotide-binding region in pyranose 2-oxidase from Trametes multicolour. Anal Biochem 314, 235 242. (Pubitemid 36321813)
154. Kujawa M, Volc J, Halada P, Sedmera P, Divne C, Sygmund C, Leitner C, Peterbauer C Haltrich D (2007) Properties of pyranose dehydrogenase purified from the litter-degrading fungus Agaricus xanthoderma. FEBS J 274, 879 894. (Pubitemid 46144046)
155. Leys D, Basran J Scrutton NS (2003) Channelling and formation of 'active' formaldehyde in dimethylglycine oxidase. EMBO J 22, 4038 4048. (Pubitemid 37021733)
156. Chiribau CB, Sandu C, Fraaije M, Schiltz E Brandsch R (2004) A novel gamma-N-methylaminobutyrate demethylating oxidase involved in catabolism of the tobacco alkaloid nicotine by Arthrobacter nicotinovorans pAO1. Eur J Biochem 271, 4677 4684. (Pubitemid 40065571)
157. Mathews FS, Chen ZW, Bellamy HD McIntire WS (1991) Three-dimensional structure of p-cresol methylhydroxylase (flavocytochrome c) from Pseudomonas putida at 30-A resolution. Biochemistry 30, 238 247.
158. Edmondson DE, Binda C Mattevi A (2004) The FAD binding sites of human monoamine oxidases A and B. Neurotoxicology 25, 63 72. (Pubitemid 38044169)
159. Zhou BP, Lewis DA, Kwan SW Abell CW (1995) Flavinylation of monoamine oxidase B. J Biol Chem 270, 23653 23660.
160. Ilari A, Bonamore A, Franceschini S, Fiorillo A, Boffi A Colotti G (2008) The X-ray structure of N-methyltryptophan oxidase reveals the structural determinants of substrate specificity. Proteins 71, 2065 2075. (Pubitemid 351732956)
161. Goyer A, Johnson TL, Olsen LJ, Collakova E, Shachar-Hill Y, Rhodes D Hanson AD (2004) Characterization and metabolic function of a peroxisomal sarcosine and pipecolate oxidase from Arabidopsis. J Biol Chem 279, 16947 16953. (Pubitemid 38560447)
162. Carrell CJ, Bruckner RC, Venci D, Zhao G, Jorns MS Mathews FS (2007) NikD an unusual amino acid oxidase essential for nikkomycin biosynthesis: structures of closed and open forms at 115 and 190 A resolution. Structure 15, 928 941. (Pubitemid 47212748)
163. Chen ZW, Koh M, Van Driessche G, Van Beeumen JJ, Bartsch RG, Meyer TE, Cusanovich MA Mathews FS (1994) The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science 266, 430 432. (Pubitemid 24348961)
164. Van Driessche G, Koh M, Chen ZW, Mathews FS, Meyer TE, Bartsch RG, Cusanovich MA Van Beeumen JJ (1996) Covalent structure of the flavoprotein subunit of the flavocytochrome c: sulfide dehydrogenase from the purple phototrophic bacterium Chromatium vinosum. Protein Sci 5, 1753 1764. (Pubitemid 26303479)
165. Nandy A, Petersen A, Wald M, Suck R, Kahlert H, Weber B, Becker WM, Cromwell O Fiebig H (2005) Primary structure recombinant expression and molecular characterization of Phl p4, a major allergen of timothy grass (Phleum pratense). Biochem Biophys Res Commun 337, 563 570. (Pubitemid 41429322)
166. Willie A, Edmondson DE Jorns MS (1996) Sarcosine oxidase contains a novel covalently bound FMN. Biochemistry 35, 5292 5299. (Pubitemid 26129470)
167. Bandeiras TM, Salgueiro C, Kletzin A, Gomes CM Teixeira M (2002) Acidianus ambivalens type-II NADH dehydrogenase: genetic characterisation and identification of the flavin moiety as FMN. FEBS Lett 531, 273 277. (Pubitemid 35341207)
168. Steenkamp DJ, McIntire W Kenney WC (1978) Structure of the covalently bound coenzyme of trimethylamine dehydrogenase. Evidence for a 6-substituted flavin. J Biol Chem 253, 2818 2824. (Pubitemid 8326490)
169. Yang CC, Packman LC Scrutton NS (1995) The primary structure of Hyphomicrobium X dimethylamine dehydrogenase. Relationship to trimethylamine dehydrogenase and implications for substrate recognition. Eur J Biochem 232, 264 271.
170. Fujieda N, Tsuse N, Satoh A, Ikeda T Kano K (2005) Production of completely flavinylated histamine dehydrogenase, unique covalently bound flavin, and iron-sulfur cluster-containing enzyme of Nocardioides simplex in Escherichia coli, and its properties. Biosci Biotechnol Biochem 69, 2459 2462. (Pubitemid 43004368)