Deletional studies to investigate the functional role of a dynamic loop region of alkanesulfonate monooxygenase

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1824, Issue 7, 2012, Pages 898-906

  Xiong, Jingyuan ^a   Ellis, Holly R ^a  

^a AUBURN UNIVERSITY   (United States)

Author keywords

Alkanesulfonate monooxygenase; FMN; Mobile loop; SsuD; Sulfur; TIM barrel fold

Indexed keywords

ALKANESULFONATE MONOOXYGENASE; ENZYME VARIANT; MUTANT PROTEIN; QUERCETIN; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DELETION MUTANT; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME STABILITY; ENZYME STRUCTURE; FLUOROMETRY; MOLECULAR DYNAMICS; OXIDATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SULFONATION; TITRIMETRY; WILD TYPE;

ALKANESULFONATES; AMINO ACID SEQUENCE; BIOCATALYSIS; CATALYSIS; CATALYTIC DOMAIN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLAVINS; FMN REDUCTASE; KINETICS; MIXED FUNCTION OXYGENASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS);

EID: 84861566184     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2012.04.005     Document Type: Article

References (50)

1. M. Kertesz, Riding the sulfur cycle-metabolism of sulfonates and sulfate esters in Gram-negative bacteria, FEMS Microbiol. Rev. 24 (2000) 135-175. (Pubitemid 30136440)
2. M. Kertesz, T. Leisinger, A.M. Cook, Proteins induced by sulfate limitation in Escherichia coli, Pseudomonas putida, or Staphylococcus aureus, J. Bacteriol. 175 (1993) 1187-1190. (Pubitemid 23060159)
3. E. Eichhorn, J.R. van der Ploeg, T. Leisinger, Characterization of a two-component alkanesulfonate monooxygenase from Escherichia coli, J. Biol. Chem. 274 (1999) 26639-26646.
4. J.R. van der Ploeg, E. Eichhorn, T. Leisinger, Sulfonate-sulfur metabolism and its regulation in Escherichia coli, Arch. Microbiol. 176 (2001) 1-8. (Pubitemid 32692638)
5. H.M. Abu-Soud, L.S. Mullins, T.O. Baldwin, F.M. Raushel, Stopped-flow kinetic analysis of the bacterial luciferase reaction, Biochemistry 31 (1992) 3807-3813.
6. W.A. Francisco, H.M. Abu-Soud, A.J. DelMonte, D.A. Singleton, T.O. Baldwin, F.M. Raushel, Deuterium kinetic isotope effects and the mechanism of the bacterial luciferase reaction, Biochemistry 37 (1998) 2596-2606. (Pubitemid 28119337)
7. J.W. Hastings, Q.H. Gibson, Intermediates in the bioluminescent oxidation of reduced flavin mononucleotide, J. Biol. Chem. 238 (1963) 2537-2554.
8. S.-C. Tu, Isolation and properties of bacterial luciferase-oxygenated flavin intermediate complexed with long-chain alcohols, Biochemistry 18 (1979) 5940-5945.
9. 2-dependent alkanesulfonate monooxygenase enzyme, Biochemistry 47 (2008) 2221-2230.
10. E. Eichhorn, C.A. Davey, D.F. Sargent, T. Leisinger, T.J. Richmond, Crystal structure of Escherichia coli alkanesulfonate monooxygenase SsuD, J. Mol. Biol. 324 (2002) 457-468. (Pubitemid 35430512)
11. G.K. Farber, G.A. Petsko, The evolution of α/β barrel enzymes, Trends Biochem. Sci. 15 (1990) 228-234.
12. R.K. Wierenga, The TIM-barrel fold: a versatile framework for efficient enzymes, FEBS Lett. 492 (2001) 193-198. (Pubitemid 32217827)
13. N.K. AbouKhair, M.M. Ziegler, T.O. Baldwin, Bacterial luciferase: demonstration of a catalytically competent altered conformational state following a single turnover, Biochemistry 24 (1985) 3942-3947. (Pubitemid 16239798)
14. Z.T. Campbell, T.O. Baldwin, Two lysine residues in the bacterial luciferase mobile loop stabilize reaction intermediates, J. Biol. Chem. 284 (2009) 32827-32834.
15. J.C. Low, S.-C. Tu, Functional roles of conserved residues in the unstructured loop of Vibrio harveyi bacterial luciferase, Biochemistry 41 (2002) 1724-1731. (Pubitemid 34132246)
16. 8 barrel structure of the bacterial luciferase α subunit, Biochemistry 40 (2001) 5436-5443.
17. R.A. Carpenter, J. Xiong, J.M. Robbins, H.R. Ellis, Functional role of a conserved arginine residue located on a mobile loop of alkanesulfonate monooxygenase, Biochemistry 50 (2011) 6469-6477.
18. B. Gao, H.R. Ellis, Altered mechanism of the alkanesulfonate FMN reductase with the monooxygenase enzyme, Biochem. Biophys. Res. Commun. 331 (2005) 1137-1145. (Pubitemid 40692477)
19. K. Abdurachim, H.R. Ellis, Detection of protein-protein interactions in the alkanesulfonate monooxygenase system from Escherichia coli, J. Bacteriol. 188 (2006) 8153-8159. (Pubitemid 44845686)
20. S.-C. Tu, D.B. McCormick, Conformation of porcine D-amino acid oxidase as studied by protein fluorescence and optical rotatory dispersion, Biochemistry 13 (1974) 893-899.
21. 2 with dihydroflavins. 1. N3,5-dimethyl-1,5-dihydrolumiflavin and 1,5- dihydroisoalloxazines, J. Am. Chem. Soc. 99 (1977) 7272-7286.
22. T.C. Bruice, Oxygen-flavin chemistry, Isr. J. Chem. 24 (1984) 54-61.
23. V. Massey, Activation of molecular oxygen by flavins and flavoproteins, J. Biol. Chem. 269 (1994) 22459-22462. (Pubitemid 24273342)
24. J. Sucharitakul, T. Phongsak, B. Entsch, J. Svasti, P. Chaiyen, D.P. Ballou, Kinetics of a two-component p-hydroxyphenylacetate hydroxylase explain how reduced flavin is transferred from the reductase to the oxygenase, Biochemistry 46 (2007) 8611-8623. (Pubitemid 47106112)
25. 2 by NAD(P)H-flavin oxidoreductase and 4-hydroxyphenylacetate 3-monooxygenase, Biochemistry 42 (2003) 7509-7517.
26. A. Kantz, F. Chin, N. Nallamothu, T. Nguyen, G.T. Gassner, Mechanism of flavin transfer and oxygen activation by the two-component flavoenzyme styrene monooxygenase, Arch. Biochem. Biophys. 442 (2005) 102-106.
27. J. Valton, C. Mathevon, M. Fontecave, V. Nivière, D.P. Ballou, Mechanism and regulation of the two-component FMN-dependent monooxygenase ActVA-ActVB from Streptomyces coelicolor, J. Biol. Chem. 283 (2008) 10287-10296.
28. B. Lei, S.-C. Tu, Mechanism of reduced flavin transfer from Vibrio harveyi NADPH-FMN oxidoreductase to luciferase, Biochemistry 37 (1998) 14623-14629. (Pubitemid 28489071)
29. C.E. Jeffers, S.-C. Tu, Differential transfers of reduced flavin cofactor and product by bacterial flavin reductase to luciferase, Biochemistry 40 (2001) 1749-1754. (Pubitemid 32144046)
30. S.-C. Tu, Reduced flavin: donor and acceptor enzymes and mechanisms of channeling, Antioxid. Redox Signal. 3 (2001) 881-897. (Pubitemid 33131276)
31. C.E. Jeffers, J.C. Nichols, S.-C. Tu, Complex formation between Vibrio harveyi luciferase and monomeric NADPH:FMN oxidoreductase, Biochemistry 42 (2003) 529-534. (Pubitemid 36105772)
32. H.R. Ellis, The FMN-dependent two-component monooxygenase systems, Arch. Biochem. Biophys. 497 (2010) 1-12.
33. N. Jawanda, K. Ahmed, S.-C. Tu, Vibrio harveyi flavin reductase-luciferase fusion protein mimics a single-component bifunctional monooxygenase, Biochemistry 47 (2008) 368-377.
34. T.C. Bruice, A progress report on studies of the activation of molecular oxygen by dihydroflavins, in: V. Massey, C.H. Williams (Eds.), Flavins and flavoproteins, Elsevier North-Holland, Inc., New York, 1982, pp. 265-277.
35. Z.T. Campbell, A. Weichsel, W.R. Montfort, T.O. Baldwin, Crystal structure of the bacteria luciferase/flavin complex provides insight into the function of the β subunit, Biochemistry 48 (2009) 6085-6094.
36. A.J. Fisher, T.B. Thompson, J.B. Thoden, T.O. Baldwin, The 1.5-Å resolution crystal structure of bacterial luciferase in low salt conditions, J. Biol. Chem. 271 (1996) 21956-21968. (Pubitemid 26303821)
37. L. Li, X. Liu, W. Yang, F. Xu, W. Wang, L. Feng, M. Bartlam, L. Wang, Z. Rao, Crystal structure of long-chain alkane monooxygenase (LadA) in complex with coenzyme FMN: unveiling the long-chain alkane hydroxylase, J. Mol. Biol. 376 (2008) 453-465.
38. B.V. Norledge, A.M. Lambeir, R.A. Abagyan, A. Rottmann, A.M. Fernandez, V.V. Filimonov, M.G. Peter, R.K. Wierenga, Modeling, mutagenesis, and structural studies on the fully conserved phosphate-binding loop (Loop 8) of triosephosphate isomerase: toward a new substrate specificity, Proteins 42 (2001) 383-389. (Pubitemid 32107762)
39. C.-H. Li, S.-C. Tu, Active site hydrophobicity is critical to the bioluminescence activity of Vibrio harveyi luciferase, Biochemistry 44 (2005) 12970-12977. (Pubitemid 41377277)
40. M. Alahuhta, R.K. Wierenga, Atomic resolution crystallography of a complex of triosephosphate isomerase with a reaction-intermediate analog: new insight in the proton transfer reaction mechanism, Proteins 78 (2010) 1878-1888.
41. 8 barrels: implications for the evolution of metabolic pathways, J. Mol. Biol. 303 (2000) 627-640.
42. M.K. Go, A. Koudelka, T.L. Amyes, J.P. Richard, Role of lys-12 in catalysis by triosephosphate isomerase: a two-part substrate approach, Biochemistry 49 (2010) 5377-5389.
43. +, and pyruvate, Biochemistry 33 (1994) 6301-6309.
44. D.L. Pompliano, A. Peyman, J.R. Knowles, Stabilization of a reaction intermediate as a catalytic device: definition of the functional role of the flexible loop in triosephosphate isomerase, Biochemistry 29 (1990) 3186-3194. (Pubitemid 20131455)
45. 13C chemical shift assignments and conformational change upon ligand binding by magic-angle spinning solid-state NMR spectroscopy, J. Mol. Biol. 397 (2010) 233-248.
46. T.F. Holzman, T.O. Baldwin, Proteolytic inactivation of luciferases from three species of luminous marine bacteria, Beneckea harveyi, Photobacterium fischeri, and Photobacterium phosphoreum: evidence of a conserved structural feature, Proc. Natl. Acad. Sci. 77 (1980) 6363-6367.
47. C.A. Leja, E.U. Woehl, M.F. Dunn, Allosteric linkage between beta-site covalent transformations and alpha-site activation and deactivation in the tryptophan synthase bienzyme complex, Biochemistry 34 (1995) 6552-6561.
48. K.S. Anderson, E.W. Miles, K.A. Johnson, Serine modulates substrate channeling in tryptophan synthase: a novel intersubunit triggering mechanism, J. Biol. Chem. 266 (1991) 8020-8033. (Pubitemid 21906469)
49. B.W. Miles, F.M. Raushel, Synchronization of the three reaction center within carbamoyl phosphate synthetase, Biochemistry 39 (2000) 5051-5056. (Pubitemid 30241625)
50. M.M. Malabanan, T.L. Amyes, J.P. Richard, A role for flexible loops in enzyme catalysis, Curr. Opin. Struct. Biol. 20 (2010) 702-710.