Mechanism-Based Inhibitors of Cytokinin Oxidase/Dehydrogenase Attack FAD Cofactor

Journal of Molecular Biology

Volumn 380, Issue 5, 2008, Pages 886-899

  Kopečný, David ^a,b   Šebela, Marek ^b   Briozzo, Pierre ^c   Spíchal, Lukáš ^b   Houba Hérin, Nicole ^a   Mašek, Vlastimil ^b   Joly, Nathalie ^c   Madzak, Catherine ^a   Anzenbacher, Pavel ^b   Laloue, Michel ^a  

^a CEMAGREF   (France)

^b PALACKÝ UNIVERSITY   (Czech Republic)

^c AGROPARISTECH   (France)

Author keywords

cytokinin oxidase dehydrogenase; cytokinin signaling; maize; mechanism based inhibitor; protein structure

Indexed keywords

ADENINE DERIVATIVE; CYTOKININ; ENZYME INHIBITOR; FLAVINE ADENINE NUCLEOTIDE; N 6 (BUTA 2,3 DINEYL)ADENINE; N 6 (PENTA 2,3 DIENYL)ADENINE; OXIDOREDUCTASE;

ARABIDOPSIS; ARTICLE; CATABOLISM; CHEMICAL BOND; CHEMICAL STRUCTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MAIZE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; RAMAN SPECTROMETRY;

AMARANTHUS; ARABIDOPSIS; BACTERIA (MICROORGANISMS); ZEA MAYS;

EID: 45949096039     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.05.044     Document Type: Article

References (44)

1. Mok D.W.S., and Mok M.C. Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52 (2001) 89-118
2. Inoue T., Higushi M., Hashimoto Y., Seki M., Kobayashi M., Kato T., et al. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409 (2001) 1060-1063
3. Suzuki T., Miwa K., Ishikawa K., Yamada H., Aiba H., and Mizuno T. The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol. 42 (2001) 107-113
4. Yamada H., Suzuki T., Terada K., Takei K., Ishikawa K., Miwa K., et al. The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42 (2001) 1017-1023
5. Brownlee B.G., Hall R.H., and Whitty C.D. 3-Methyl-2-butenal: an enzymatic degradation product of the cytokinin, N-6-(delta-2 isopentenyl) adenine. Can. J. Biochem. 53 (1975) 37-41
6. Morris R.O., Bilyeu K.D., Laskey J.G., and Cheikh N.N. Isolation of a gene encoding a glycosylated cytokinin oxidase from maize. Biochem. Biophys. Res. Commun. 255 (1999) 328-333
7. Houba-Hérin N., Pethe C., d'Alayer J., and Laloue M. Cytokinin oxidase from Zea mays: purification, cDNA cloning and expression in moss protoplasts. Plant J. 17 (1999) 615-626
8. Massonneau A., Houba-Hérin N., Pethe C., Madzak C., Falque M., Mercy M., et al. Maize cytokinin oxidase genes: differential expression and cloning of two new cDNAs. J. Exp. Bot. 55 (2004) 2549-2557
9. Laloue M., and Fox J.E. Characterization of an imine intermediate in the degradation of isopentenylated cytokinins by a cytokinin oxidase from wheat. In: Bopp M. (Ed). Abstracts of the 12th International Conference on Plant Growth Substances (1985), Springer-Verlag, Berlin 23
10. Kopečný D., Pethe C., Šebela M., Houba-Hérin N., Madzak C., Majira A., and Laloue M. High-level expression and characterization of Zea mays cytokinin oxidase/dehydrogenase in Yarrowia lipolytica. Biochimie 87 (2005) 1011-1022
11. Frébortová J., Fraaije M.W., Galuszka P., Šebela M., Peč P., Hrbáč J., et al. Catalytic reaction of cytokinin dehydrogenase: preference for quinones as electron acceptors. Biochem. J. 380 (2004) 121-130
12. Malito E., Coda A., Bilyeu K.D., Fraaije M.W., and Mattevi A. Structures of Michaelis and product complexes of plant cytokinin dehydrogenase: implications for flavoenzyme catalysis. J. Mol. Biol. 341 (2004) 1237-1249
13. Suttle J.C., and Mornet R. Mechanism-based irreversible inhibitors of cytokinin dehydrogenase. J. Plant. Physiol. 162 (2005) 1189-1196
14. Lamplot Z., Šebela M., Maloň M., Lenobel R., Lemr K., Havliš J., et al. 1,5-Diamino-2-pentyne is both a substrate and inactivator of plant copper amine oxidases. Eur. J. Biochem. 271 (2004) 4696-4708
15. Walsh C. Suicide substrates: mechanism-based enzyme inactivators. Tetrahedron 38 (1982) 871-909
16. Bilyeu K.D., Cole J.L., Laskey J.G., Riekhof W.R., Esparza T.J., Kramer M.D., and Morris R.O. Molecular and biochemical characterization of a cytokinin oxidase from maize. Plant Physiol. 125 (2001) 378-386
17. Frébort I., Šebela M., Galuszka P., Werner T., Schmülling T., and Peč P. Cytokinin oxidase/cytokinin dehydrogenase assay: optimized procedures and applications. Anal. Biochem. 306 (2002) 1-7
18. Halada P., Leitner C., Sedmera P., Haltrich D., and Volc J. Identification of the covalent flavin adenine dinucleotide-binding region in pyranose 2-oxidase from Trametes multicolor. Anal. Biochem. 314 (2003) 235-242
19. Bowman W.D., and Spiro T.G. Normal mode analysis of lumiflavin and interpretation of resonance Raman spectra of flavoproteins. Biochemistry 20 (1981) 3313-3318
20. Tegoni M., Gervais M., and Desbois A. Resonance Raman study on the oxidized and anionic semiquinone forms of flavocytochrome b2 and l-lactate monooxygenase. Influence of the structure and environment of the isoalloxazine ring on the flavin function. Biochemistry 36 (1997) 8932-8946
21. DeLano W. The PyMOL Molecular Graphics System (2002), DeLano Scientific, Palo Alto, CA. http://www.pymol.org http://www.pymol.org
22. Popelková H., Fraaije M.W., Novák O., Frébortová J., Bilyeu K.D., and Frébort I. Kinetic and chemical analyses of the cytokinin dehydrogenase-catalysed reaction: correlations with the crystal structure. Biochem J. 398 (2006) 113-124
23. Silverman R.B. The potential use of mechanism-based enzyme inactivators in medicine. J. Enzyme Inhib. 2 (1988) 73-90
24. Zheng Y., Dong J., Palfey B.A., and Carey P.R. Using Raman spectroscopy to monitor the solvent-exposed and "buried" forms of flavin in p-hydroxybenzoate hydroxylase. Biochemistry 38 (1999) 16727-16732
25. Desbois A., Tegoni M., Gervais M., and Lutz M. Flavin and heme structures in lactate:cytochrome c oxidoreductase: a resonance Raman study. Biochemistry 28 (1989) 8011-8022
26. Nagy J., Kenney W.C., and Singer T.P. The reaction of phenylhydrazine with trimethylamine dehydrogenase and with free flavins. J. Biol. Chem. 254 (1979) 2684-2688
27. Gärtner B., Hemmerich P., and Zeller E.A. Structure of flavin adducts with acetylenic substrates. Chemistry of monoamine oxidase and lactate oxidase inhibition. Eur. J. Biochem. 63 (1976) 211-221
28. Maycock A.L., Abeles R.H., Salach J.I., and Singer T.P. The structure of the covalent adduct formed by the interaction of 3-dimethylamino-1-propyne and the flavine of mitochondrial amine oxidase. Biochemistry 15 (1976) 114-125
29. Mitchell D.J., Nikolic D., Rivera E., Sablin S.O., Choi S., Breemen R.B., et al. Spectrometric evidence for the flavin-1-phenylcyclopropylamine inactivator adduct with monoamine oxidase N. Biochemistry 40 (2001) 5447-5456
30. McCann A., and Sampson N.S. A C6-FAD adduct is formed upon irreversible inactivation of cholesterol oxidase by 2a,3a-cyclopropano-5-cholestan-3b-ol. J. Am. Chem. Soc. 122 (2000) 35-39
31. Hou B., Lim E.K., Higgins G.S., and Bowles D.J. N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. J. Biol. Chem. 279 (2004) 47822-47832
32. Haidoune, M. (1989). Chimie des Cytokinines. Etude du Comportement de la trans-Zéatin en Milieu Acide: Synthèses de Nouvelles Adénines N6-Substituées Analogues des Cytokinines Naturelles et d'un Nouveau Métabolite. PhD thesis, University of Angers, France.
33. Kent U.M., Yanev S., and Hollenberg P.F. Mechanism-based inactivation of cytochromes P450 2B1 and P450 2B6 by n-propylxanthate. Chem. Res. Toxicol. 12 (1999) 317-322
34. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150 (1985) 76-85
35. Laloue M., and Fox J.E. Cytokinin oxidase from wheat. Partial purification and general properties. Plant Physiol. 90 (1989) 899-906
36. Šebela M., Štosová T., Havliš J., Wielsch N., Thomas H., Zdráhal Z., and Shevchenko A. Thermostable trypsin conjugates for high throughput proteomics: synthesis and performance evaluation. Proteomics 6 (2006) 2959-2963
37. Dostál L., Khare D., Bok J., Heinemann U., Lanka E., and Welfle H. RP4 repressor protein KorB binds to the major groove of the operator DNA: a Raman study. Biochemistry 42 (2003) 14476-14482
38. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
39. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26 (1993) 795-800
40. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
41. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
42. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 24 (1993) 946-950
43. Spíchal L., Rakova N.Y., Riefler M., Mizuno T., Romanov G.A., Strnad M., and Schmülling T. Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant Cell Physiol. 45 (2004) 1299-1305
44. Holub J., Hanuš J., Hanke D.E., and Strnad M. Biological activity of cytokinins derived from ortho- and meta-hydroxybenzyladenine. Plant. Growth Regul. 26 (1998) 109-115