2gb0 Citations

Monomeric sarcosine oxidase: structure of a covalently flavinylated amine oxidizing enzyme.

Structure 7 331-45 (1999)
Cited: 65 times
EuropePMC logo PMID: 10368302

Abstract

Background

Monomeric sarcosine oxidases (MSOXs) are among the simplest members of a recently recognized family of eukaryotic and prokaryotic enzymes that catalyze similar oxidative reactions with various secondary or tertiary amino acids and contain covalently bound flavins. Other members of this family include heterotetrameric sarcosine oxidase, N-methyltryptophan oxidase and pipecolate oxidase. Mammalian sarcosine dehydrogenase and dimethylglycine dehydrogenase may be more distantly related family members.

Results

The X-ray crystal structure of MSOX from Bacillus sp. B-0618, expressed in Escherichia coli, has been solved at 2.0 A resolution by multiwavelength anomalous dispersion (MAD) from crystals of the selenomethionine-substituted enzyme. Fourteen selenium sites, belonging to two MSOX molecules in the asymmetric unit, were used for MAD phasing and to define the local twofold symmetry axis for electron-density averaging. The structures of the native enzyme and of two enzyme-inhibitor complexes were also determined.

Conclusion

MSOX is a two-domain protein with an overall topology most similar to that of D-amino acid oxidase, with which it shares 14% sequence identity. The flavin ring is located in a very basic environment, making contact with sidechains of arginine, lysine, histidine and the N-terminal end of a helix dipole. The flavin is covalently attached through an 8alpha-S-cysteinyl linkage to Cys315 of the catalytic domain. Covalent attachment is probably self-catalyzed through interactions with the positive sidechains and the helix dipole. Substrate binding is probably stabilized by hydrogen bonds between the substrate carboxylate and two basic sidechains, Arg52 and Lys348, located above the re face of the flavin ring.

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  2. Crystal structure of novel dye-linked L-proline dehydrogenase from hyperthermophilic archaeon Aeropyrum pernix. Sakuraba H, Satomura T, Kawakami R, Kim K, Hara Y, Yoneda K, Ohshima T. J. Biol. Chem. 287 20070-20080 (2012)


Reviews citing this publication (16)

  1. Sequence-structure analysis of FAD-containing proteins. Dym O, Eisenberg D. Protein Sci. 10 1712-1728 (2001)
  2. Oxidation of amines by flavoproteins. Fitzpatrick PF. Arch. Biochem. Biophys. 493 13-25 (2010)
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  10. Flavoprotein oxidases: classification and applications. Dijkman WP, de Gonzalo G, Mattevi A, Fraaije MW. Appl. Microbiol. Biotechnol. 97 5177-5188 (2013)
  11. Oxidation of amines by flavoproteins. Fitzpatrick PF. Arch. Biochem. Biophys. 493 13-25 (2010)
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  8. FOXRED1, encoding an FAD-dependent oxidoreductase complex-I-specific molecular chaperone, is mutated in infantile-onset mitochondrial encephalopathy. Fassone E, Duncan AJ, Taanman JW, Pagnamenta AT, Sadowski MI, Holand T, Qasim W, Rutland P, Calvo SE, Mootha VK, Bitner-Glindzicz M, Rahman S. Hum. Mol. Genet. 19 4837-4847 (2010)
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  18. Active site analysis of fructosyl amine oxidase using homology modeling and site-directed mutagenesis. Miura S, Ferri S, Tsugawa W, Kim S, Sode K. Biotechnol. Lett. 28 1895-1900 (2006)
  19. Spectral and kinetic characterization of the michaelis charge transfer complex in monomeric sarcosine oxidase. Zhao G, Jorns MS. Biochemistry 45 5985-5992 (2006)
  20. NikD, an unusual amino acid oxidase essential for nikkomycin biosynthesis: structures of closed and open forms at 1.15 and 1.90 A resolution. Carrell CJ, Bruckner RC, Venci D, Zhao G, Jorns MS, Mathews FS. Structure 15 928-941 (2007)
  21. Ionization of zwitterionic amine substrates bound to monomeric sarcosine oxidase. Zhao G, Jorns MS. Biochemistry 44 16866-16874 (2005)
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  23. Crystal structure analysis of free and substrate-bound 6-hydroxy-L-nicotine oxidase from Arthrobacter nicotinovorans. Kachalova GS, Bourenkov GP, Mengesdorf T, Schenk S, Maun HR, Burghammer M, Riekel C, Decker K, Bartunik HD. J. Mol. Biol. 396 785-799 (2010)
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  26. Probing oxygen activation sites in two flavoprotein oxidases using chloride as an oxygen surrogate. Kommoju PR, Chen ZW, Bruckner RC, Mathews FS, Jorns MS. Biochemistry 50 5521-5534 (2011)
  27. Characterization of a novel dye-linked L-proline dehydrogenase from an aerobic hyperthermophilic archaeon, Pyrobaculum calidifontis. Satomura T, Zhang XD, Hara Y, Doi K, Sakuraba H, Ohshima T. Appl. Microbiol. Biotechnol. 89 1075-1082 (2011)
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  30. Spectral and kinetic characterization of intermediates in the aromatization reaction catalyzed by NikD, an unusual amino acid oxidase. Bruckner RC, Jorns MS. Biochemistry 48 4455-4465 (2009)
  31. Cloning, expression and crystallization of heterotetrameric sarcosine oxidase from Pseudomonas maltophilia. Hassan-Abdallah A, Zhao G, Eschenbrenner M, Chen ZW, Mathews FS, Jorns MS. Protein Expr. Purif. 43 33-43 (2005)
  32. Mechanistic and structural analyses of the role of His67 in the yeast polyamine oxidase Fms1. Adachi MS, Taylor AB, Hart PJ, Fitzpatrick PF. Biochemistry 51 4888-4897 (2012)
  33. X-ray, ESR, and quantum mechanics studies unravel a spin well in the cofactor-less urate oxidase. Gabison L, Chopard C, Colloc'h N, Peyrot F, Castro B, El Hajji M, Altarsha M, Monard G, Chiadmi M, Prangé T. Proteins 79 1964-1976 (2011)
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  39. Structures of dimethylsulfoniopropionate-dependent demethylase from the marine organism Pelagabacter ubique. Schuller DJ, Reisch CR, Moran MA, Whitman WB, Lanzilotta WN. Protein Sci. 21 289-298 (2012)
  40. Pleiotropic impact of a single lysine mutation on biosynthesis of and catalysis by N-methyltryptophan oxidase. Bruckner RC, Winans J, Jorns MS. Biochemistry 50 4949-4962 (2011)
  41. FAD binding in glycine oxidase from Bacillus subtilis. Caldinelli L, Pedotti M, Motteran L, Molla G, Pollegioni L. Biochimie 91 1499-1508 (2009)
  42. Identification of a stable flavin-thiolate adduct in heterotetrameric sarcosine oxidase. Hynson RM, Mathews FS, Schuman Jorns M. J. Mol. Biol. 362 656-663 (2006)
  43. Probing the role of active site residues in NikD, an unusual amino acid oxidase that catalyzes an aromatization reaction important in nikkomycin biosynthesis. Kommoju PR, Bruckner RC, Ferreira P, Jorns MS. Biochemistry 48 6951-6962 (2009)
  44. The cation-π interaction between Lys53 and the flavin of fructosamine oxidase (FAOX-II) is critical for activity. Collard F, Fagan RL, Zhang J, Nemet I, Palfey BA, Monnier VM. Biochemistry 50 7977-7986 (2011)
  45. Deuterium kinetic isotope effects in heterotetrameric sarcosine oxidase from Corynebacterium sp. U-96: the anionic form of the substrate in the enzyme-substrate complex is a reactive species. Saito M, Itoh A, Suzuki H. J. Biochem. 151 633-642 (2012)
  46. Turning a monocovalent flavoprotein into a bicovalent flavoprotein by structure-inspired mutagenesis. Kopacz MM, Fraaije MW. Bioorg. Med. Chem. 22 5621-5627 (2014)
  47. Kinetic mechanism of putrescine oxidase from Rhodococcus erythropolis. Kopacz MM, Heuts DP, Fraaije MW. FEBS J. 281 4384-4393 (2014)