Aurone synthase is a catechol oxidase with hydroxylase activity and provides insights into the mechanism of plant polyphenol oxidases

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 13, 2016, Pages E1806-E1815

  Molitor, Christian ^a   Mauracher, Stephan Gerhard ^a   Rompel, Annette ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

Catechol oxidase; Crystal structure; Type III copper protein mechanism; Tyrosinase

Indexed keywords

AURONE SYNTHASE; CATECHOL OXIDASE; COPPER; HISTIDINE; ISOLIQUIRITIGENIN; OXYGENASE; TYRAMINE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; AURONE; BENZOFURAN DERIVATIVE; BUTEIN; CHALCONE DERIVATIVE; PLANT PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; CRYPTOSTEGIA GRANDIFLORA; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME INACTIVATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SULFATION; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; COREOPSIS; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; BENZOFURANS; BINDING SITES; CATALYTIC DOMAIN; CATECHOL OXIDASE; CHALCONES; COPPER; COREOPSIS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY; TYRAMINE;

EID: 84962195829     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1523575113     Document Type: Article

References (64)

1. Mayer AM (2006) Polyphenol oxidases in plants and fungi: Going places? A review. Phytochemistry 67(21):2318-2331.
2. Tran LT, Taylor JS, Constabel CP (2012) The polyphenol oxidase gene family in land plants: Lineage-specific duplication and expansion. BMC Genomics 13:395.
3. Dirks-Hofmeister ME, Singh R, Leufken C.M., Inlow JK, Moerschbacher BM (2014) Structural diversity in the dandelion (Taraxacum officinale) polyphenol oxidase family results in different responses to model substrates. PLoS One 9(6):e99759.
4. King RS, Flurkey WH (1987) Effects of limited proteolysis on broad bean polyphenoloxidase. J Sci Food Agric 41(3):231-240.
5. Marusek CM, Trobaugh NM, Flurkey W.H., Inlow JK (2006) Comparative analysis of polyphenol oxidase from plant and fungal species. J Inorg Biochem 100(1):108-123.
6. Yoruk R, Marshall MR (2003) Physicochemical properties and function of plant polyphenol oxidase: A review1. J Food Biochem 27(5):361-422.
7. Sullivan ML (2014) Beyond brown: Polyphenol oxidases as enzymes of plant specialized metabolism. Front Plant Sci 5:783.
8. Wahler D, et al. (2009) Polyphenoloxidase silencing affects latex coagulation in Taraxacum species. Plant Physiol 151(1):334-346.
9. Richter C, Dirks ME, Gronover C.S., Prüfer D, Moerschbacher BM (2012) Silencing and heterologous expression of ppo-2 indicate a specific function of a single polyphenol oxidase isoform in resistance of dandelion (Taraxacum officinale) against Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 25(2):200-210.
10. Araji S, et al. (2014) Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut. Plant Physiol 164(3):1191-1203.
11. Cho MH, et al. (2003) (+)-Larreatricin hydroxylase, an enantio-specific polyphenol oxidase from the creosote bush (Larrea tridentata). Proc Natl Acad Sci USA 100(19): 10641-10646.
12. Nakayama T, et al. (2000) Aureusidin synthase: A polyphenol oxidase homolog responsible for flower coloration. Science 290 (5494):1163-1166.
13. Ono E, et al. (2006) Localization of a flavonoid biosynthetic polyphenol oxidase in vacuoles. Plant J 45(2):133-143.
14. Miosic S, et al. (2013) 4-Deoxyaurone formation in Bidens ferulifolia (Jacq.) DC. PLoS One 8(5):e61766.
15. Molitor C, et al. (2015) Latent and active aurone synthase from pet als of C. grandiflora: A polyphenol oxidase with unique characteristics. Planta 242(3):519-537.
16. Kaintz C, et al. (2014) Cloning and functional expression in E. coli of a polyphenol oxidase transcript from Coreopsis grandiflora involved in aurone formation. FEBS Lett 588(18):3417-3426.
17. Klabunde T, Eicken C, Sacchettini J.C., Krebs B (1998) Crystal structure of a plant catechol oxidase containing a dicopper center. Nat Struct Biol 5(12):1084-1090.
18. Virador VM, et al. (2010) Cloning, sequencing, purification, and crystal structure of Grenache (Vitis vinifera) polyphenol oxidase. J Agric Food Chem 58(2):1189-1201.
19. Sendovski M, Kanteev M, Ben-Yosef VS, Adir N., Fishman A (2011) First structures of an active bacterial tyrosinase reveal copper plasticity. J Mol Biol 405(1):227-237.
20. Goldfeder M, Kanteev M, Isaschar-Ovdat S, Adir N., Fishman A (2014) Determination of tyrosinase substrate-binding modes reveals mechanistic differences between type-3 copper proteins. Nat Commun 5:4505.
21. Fujieda N, et al. (2013) Crystal structures of copper-depleted and copper-bound fungal pro-tyrosinase: Insights into endogenous cysteine-dependent copper incorporation. J Biol Chem 288(30):22128-22140.
22. Ismaya WT, et al. (2011) Crystal structure of Agaricus bisporus mushroom tyrosinase: Identity of the tetramersubunits and interaction with tropolone. Biochemistry 50(24): 5477-5486.
23. Bijelic A, Pretzler M, Molitor C., Zekiri F, Rompel A (2015) The structure of a plant tyrosinase from walnut leaves reveals the importance of "substrate-guiding residues" for enzymatic specificity. Angew Chem Int Ed Engl 54(49):14677-14680.
24. Molitor C, Mauracher SG, Rompel A (2015) Crystallization and preliminary crystallographic analysis of latent, active and recombinantly expressed aurone synthase, a polyphenol oxidase, from Coreopsis grandiflora. Acta Crystallogr F Struct Biol Commun 71 (Pt 6):746-751.
25. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774-797.
26. Wise O, Coskuner O (2014) New force field parameters for met alloproteins I: Divalent copper ion centers including three histidine residues and an oxygen-ligated amino acid residue. J Comput Chem 35(17):1278-1289.
27. Mauracher SG, Molitor C, Al-Oweini R, Kortz U., Rompel A (2014) Latent and active abPPO4 mushroom tyrosinase cocrystallized with hexatungstotellurate(VI) in a single crystal. Acta Crystallogr D Biol Crystallogr 70(Pt 9):2301-2315.
28. Masuda T, Momoji K, Hirata T., Mikami B (2014) The crystal structure of a crustacean prophenoloxidase provides a clue to understanding the functionality of the type 3 copper proteins. FEBS J 281(11):2659-2673.
29. Li Y, Wang Y, Jiang H., Deng J (2009) Crystal structure of Manduca sexta prophenoloxidase provides insights into the mechanism of type 3 copper enzymes. Proc Natl Acad Sci USA 106(40):17002-17006.
30. Leufken CM, Moerschbacher BM, Dirks-Hofmeister ME (2015) Dandelion PPO-1/PPO-2 domain-swaps: The C-terminal domain modulates the pH optimum and the linker affects SDS-mediated activation and stability. Biochim Biophys Acta 1854(2):178-186.
31. Matoba Y, Kumagai T, Yamamoto A., Yoshitsu H, Sugiyama M (2006) Crystallographic evidence that the dinuclear copper center of tyrosinase is flexible during catalysis. J Biol Chem 281(13):8981-8990.
32. Deeth RJ, Diedrich C (2010) Structural and mechanistic insights into the oxy form of tyrosinase from molecular dynamics simulations. J Biol Inorg Chem 15(2):117-129.
33. Kuijpers TF, Gruppen H, Sforza S., van Berkel WJ, Vincken JP (2013) The antibrowning agent sulfite inactivates Agaricus bisporus tyrosinase through covalent modification of the copper-B site. FEBS J 280(23):6184-6195.
34. Zekiri F, et al. (2014) Purification and characterization of tyrosinase from walnut leaves (Juglans regia). Phytochemistry 101:5-15.
35. Mauracher SG, et al. (2014) High level protein-purification allows the unambiguous polypeptide determination of latent isoform PPO4 of mushroom tyrosinase. Phytochemistry 99:14-25.
36. Gidda SK, Varin L (2006) Biochemical and molecular characterization of flavonoid 7-sulfotransferase from Arabidopsis thaliana. Plant Physiol Biochem 44(11-12):628-636.
37. Varin L, Ibrahim RK (1989) Partial purification and characterization of three flavonol-specific sulfotransferases from Flaveria chloraefolia. Plant Physiol 90(3): 977-981.
38. Varin L, Ibrahim RK (1991) Partial purification and some properties of flavonol 7-sulfotransferase from Flaveria bidentis. Plant Physiol 95(4):1254-1258.
39. Malojcic G, et al. (2008) A structural and biochemical basis for PAPS-independent sulfuryl transfer by aryl sulfotransferase from uropathogenic Escherichia coli. Proc Natl Acad Sci USA 105(49):19217-19222.
40. Hakulinen N, Gasparetti C, Kaljunen H., Kruus K, Rouvinen J (2013) The crystal structure of an extracellular catechol oxidase from the ascomycete fungus Aspergillus oryzae. J Biol Inorg Chem 18(8):917-929.
41. García-Molina M.o., et al. (2013) Hydrogen peroxide helps in the identification of monophenols as possible substrates of tyrosinase. Biosci Biotechnol Biochem 77(12): 2383-2388.
42. Ortiz-Ruiz CV, Garcia-Molina Mdel M, Serrano JT, Tomas-Martinez V, Garcia-Canovas F (2015) Discrimination between alternative substrates and inhibitors of tyrosinase. J Agric Food Chem 63(8):2162-2171.
43. Ortiz-Ruiz CV, et al. (2015) Identification of p-hydroxybenzyl alcohol, tyrosol, phloretin and its derivate phloridzin as tyrosinase substrates. Bioorg Med Chem 23(13): 3738-3746.
44. Escobar MA, Shilling A, Higgins P., Uratsu SL, Dandekar AM (2008) Characterization of polyphenol oxidase from walnut. J Am Soc Hortic Sci 133(6):852-858.
45. Zekiri F, Bijelic A, Molitor C., Rompel A (2014) Crystallization and preliminary X-ray crystallographic analysis of polyphenol oxidase from Juglans regia (jrPPO1). Acta Crystallogr F Struct Biol Commun 70(Pt 6):832-834.
46. Fronk P, et al. (2015) Polyphenoloxidase from Riesling and Dornfelder wine grapes (Vitis vinifera) is a tyrosinase. Food Chem 183:49-57.
47. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
48. Emsley P, Lohkamp B, Scott W.G., Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
49. Long F, Vagin AA, Young P, Murshudov GN (2008) BALBES: A molecular-replacement pipeline. Acta Crystallogr D Biol Crystallogr 64(Pt 1):125-132.
50. Bijelic A, Rompel A (2015) The use of polyoxomet alates in protein crystallography - An attempt to widen a well-known bottleneck. Coord Chem Rev 299(0):22-38.
51. Bijelic A, et al. (2015) Hen egg-white lysozyme crystallisation: Protein stacking and structure stability enhanced by a Tellurium(VI)-centred polyoxotungstate. Chem Bio Chem 16(2):233-241.
52. Mauracher SG, Molitor C, Al-Oweini R, Kortz U., Rompel A (2014) Crystallization and preliminary X-ray crystallographic analysis of latent isoform PPO4 mushroom (Agaricus bisporus) tyrosinase. Acta Crystallogr F Struct Biol Commun 70(Pt 2):263-266.
53. Schmidt KJ, Schrobilgen GJ, Sawyer JF (1986) Hexasodium hexatungstotellurate(VI) 22-hydrate. Acta Crystallogr C 42(9):1115-1118.
54. Chen VB, et al. (2010) MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66(Pt 1):12-21.
55. Trott O, Olson AJ (2010) AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31(2):455-461.
56. Pronk S, et al. (2013) GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29(7):845-854.
57. Sorin EJ, Pande VS (2005) Exploring the helix-coil transition via all-atom equilibrium ensemble simulations. Biophys J 88(4):2472-2493.
58. Zoete V, Cuendet MA, Grosdidier A, Michielin O (2011) SwissParam: A fast force field generation tool for small organic molecules. J Comput Chem 32(11):2359-2368.
59. Vanquelef E, et al. (2011) R.E.D. Server: A web service for deriving RESP and ESP charges and building force field libraries for new molecules and molecular fragments. Nucleic Acids Res 39(Web Server issue):W511-W517.
60. Bochot C, et al. (2013) Unsymmetrical binding modes of the HOPNO inhibitor of tyrosinase: From model complexes to the enzyme. Chemistry 19(11):3655-3664.
61. Laskowski RA, Swindells MB (2011) LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model 51(10):2778-2786.
62. Salentin S, Schreiber S, Haupt V.J., Adasme MF, Schroeder M (2015) PLIP: Fully automated protein-ligand interaction profiler. Nucleic Acids Res 43(W1):W443-W447.
63. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graph 14(1):33-38, 27-28.
64. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22(12):2577-2637.