The rutin catabolic pathway with special emphasis on quercetinase

Biodegradation

Volumn 21, Issue 6, 2010, Pages 833-859

  Tranchimand, Sylvain ^a   Brouant, Pierre ^a   Iacazio, Gilles ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Flavonol; Flavonol biodegradation; Quercetinase; Rutin catabolic pathway

Indexed keywords

CATABOLIC PATHWAY; FLAVONOIDS; FLAVONOL; FLAVONOL BIODEGRADATION; METABOLIC CAPACITIES; NEW CENTURIES; OXIDATIVE MICROBIAL DEGRADATION; QUERCETINASE; RESEARCH GROUPS; SECONDARY METABOLITES;

BIODEGRADATION; CATALYSTS; DEGRADATION; ENZYMES; FATTY ACIDS; MACHINERY; METABOLISM; METABOLITES; MICROORGANISMS; PHENOLS;

ALCOHOLS;

DIOXYGENASE; QUERCETIN 2,3 DIOXYGENASE; QUERCETIN 2,3-DIOXYGENASE; RUTOSIDE;

ANTIOXIDANT; BIOCHEMISTRY; BIODEGRADATION; CATABOLISM; ENZYME ACTIVITY; GENETIC ANALYSIS; GENOMICS; MICROBIAL ACTIVITY; MICROBIOLOGY; OXIDATION; PHENOLIC COMPOUND; SECONDARY METABOLITE;

AMINO ACID SEQUENCE; BIOREMEDIATION; CHEMISTRY; ENZYMOLOGY; FUNGUS; METABOLISM; MOLECULAR GENETICS; REVIEW;

AMINO ACID SEQUENCE; BIODEGRADATION, ENVIRONMENTAL; DIOXYGENASES; FUNGI; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; RUTIN;

EID: 78649325896     PISSN: 09239820     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10532-010-9359-7     Document Type: Review

References (87)

1. Adams M, Jia Z (2005) Structural and biochemical analysis reveal pirins to possess quercetinase activity. J Biol Chem 280: 28675-28682.
2. Agarwall G, Rajavel M, Gopal B, Srinivasan N (2009) Structure-based phylogeny as a diagnostic for functional characterization of proteins with a cupin fold. PLoS ONE 4: e5736.
3. Antonczak S, Fiorucci S, Golebiowski J, Cabrol-Bass D (2009) Theorical investigations of the role played by quercetinase enzymes upon the flavonoids oxygenolysis mechanism. Phys Chem Chem Phys 11: 1491-1501.
4. Armand-Fraysse D, Lebreton P (1969) Recherches physiologiques sur les champignons III. Transformation métabolique de la rutine par les champignons lignivores. Bull Soc Chim Biol 51: 563-578.
5. Barney BM, Schaab MR, LoBrutto R, Francisco WA (2004) Evidence for a new metal in a known active site: purification and characterization of an iron-containing quercetin 2, 3-dioxygenase from Bacillus subtilis. Protein Expr Purif 35: 131-141.
6. Barz W (1971) Uber den abbau aromatisher verbindungen durch Fusarium oxysporum Schlecht. Arch Mikrobiol 78: 341-352.
7. Bowater L, Fairhurst SA, Just VJ, Bornemann S (2004) Bacillus subtilis YxaG is a novel Fe-containing quercetin 2, 3-dioxygenase. FEBS Lett 557: 45-48.
8. Braune A, Gutschow M, Engst W, Blaut M (2001) Degradation of quercetin and luteolin by Eubacterium ramulus. Appl Environ Microbiol 62: 5558-5567.
9. 18O labelling. Biochem J 205: 239-244.
10. Child JJ, Simpson FJ, Westlake DWS (1963) Degradation of rutin by Aspergillus flavus. Factors affecting production of the enzyme system. Can J Microbiol 9: 653-664.
11. Child JJ, Oka T, Simpson FJ, Krishnamurty HG (1971) Purification and properties of a phenol carboxylic acid esterase from Aspergillus flavus. Can J Microbiol 17: 1455-1463.
12. 2β. Trends Biochem Sci 26: 7-9.
13. Das S, Rosazza JPN (2006) Microbial and enzymatic transformations of flavonoids. J Nat Prod 69: 499-508.
14. Dunwell JM (1998) Cupins: a new superfamily of functionally-diverse proteins that include germins and plant seed storage proteins. Biotechnol Genet Eng 15: 1-32.
15. Dunwell JM, Gane PJ (1998) Microbial relatives of the seed storage proteins of higher plants: conservation of motifs in a functionally diverse superfamilly of enzymes. J Mol Evol 46: 147-154.
16. Dunwell JM, Khuri S, Gane PJ (2000) Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiol Mol Biol Rev 64: 153-179.
17. Dunwell JM, Culham A, Carter CE, Sosa-Aguirre CR, Goodenough PW (2001) Evolution of functional diversity in the cupin superfamily. Trends Biochem Sci 26: 740-746.
18. Dunwell JM, Purvis A, Khuri S (2004) Cupins: the most functionally diverse protein superfamily? Phytochemistry 65: 1-17.
19. Fiorucci S, Golebiowski J, Cabrol-Bass D, Antonczak S (2004) Oxygenolysis of flavonoid compounds: DFT description of the mechanism for quercetin. ChemPhysChem 5: 1726-1733.
20. Fiorucci S, Golebiowski J, Cabrol-Bass D, Antonczak S (2006) Molecular simulations reveal a new entry site in quercetin 2, 3-dioxygenase. A pathway for dioxygen. Proteins 64: 845-850.
21. Fiorucci S, Golebiowski J, Cabrol-Bass D, Antonczak S (2007) Molecular simulations bring new insights into flavonoid/quercetinase interaction mode. Proteins 67: 961-970.
22. Fittipaldi M, Steiner RA, Matsushita M, Dijkstra BW, Groenen EJJ, Huber M (2003) Single-crystal EPR study at 95 Hz of the type 2 copper site of the inhibitor-bound quercetin 2, 3-dioxygenase. Biophys J 85: 4047-4054.
23. Fusetti F, Schröter KH, Steiner RA, van Noort PI, Pijning T, Rozeboom HJ, Kalk KH, Egmond MR, Dijkstra BW (2002) Crystal structure of the copper-containing quercetin 2, 3-dioxygenase from Aspergillus japonicus. Structure 10: 259-268.
24. Gallego MV, Pinaga F, Ramon D, Valles S (2001) Purification and characterization of an α-L-rhamnosidase from Aspergillus terreus of interest in wine making. J Food Sci 65: 204-209.
25. Gopal B, Madan LL, Betz SF, Kossiakoff AA (2005) The crystal structure of a quercetin 2, 3-dioxygenase from Bacillus subtilis suggests modulation of enzyme activity by a change in the metal ion at the active site(s). Biochemistry 44: 193-201.
26. Haluk JP, Metche M (1970) Transformation microbiologique de la quercetine par Aspergillus niger van Tieghem. Bull Soc Chim Biol 52: 667-676.
27. Hattori S, Noguchi I (1959) Microbial degradation of rutin. Nature 184: 1145-1146.
28. Hay GW, Westlake DWS, Simpson FJ (1961) Microbial decomposition of rutin. Can J Microbiol 7: 921-931.
29. Hirooka K, Kunikane S, Matsuoka H, Yoshida K-I, Kunamoto K, Tojo S, Fujita Y (2007) Dual regulation of the Bacillus subtilis regulon comprising the lmrAB and yxaGH operons and yxaF gene by two transcriptional repressors, LmrA and YxaF, in response to flavonoids. J Bacteriol 189: 5170-5182.
30. Hund H-K, Breuer J, Lingans F, Hüttermann J, Kappel R, Fetzner S (1999) Flavonol 2, 4-dioxygenase from Aspergillus niger DSM 821, a type 2 CuII-containing glycoprotein. Eur J Biochem 263: 871-878.
31. Iacazio G (2005) Increased quercetinase production by Penicillium olsonii using fractional factorial design. Process Biochem 40: 379-384.
32. Kaizer J, Balogh-Hergovich E, Czaun M, Csay T, Speier G (2006) Redox and non-redox metal assisted model systems with relevance to flavonol and 3-hydroxyquinolin-4(1H)-one 2, 4-dioxygenase. Coord Chem Rev 250: 2222-2233.
33. Kooter IM, Steiner RA, Dijkstra BW, van Noort PI, Egmond MR, Huber M (2002) EPR characterization of the mononuclear Cu-containing Aspergillus japonicus quercetin 2, 3-dioxygenase reveals dramatic changes upon anaerobic binding of substrates. Eur J Biochem 269: 2971-2979.
34. Krishnamachari V, Levine LH, Paré PW (2002) Flavonoid oxidation by the radical generator AIBN: a unified mechanism for quercetin radical scavenging. J Agric Food Chem 50: 4357-4363.
35. Krishnamurty HG, Simpson FJ (1970) Degradation of rutin by Aspergillus flavus. Studies with oxygen 18 on the action of a dioxygenase on quercetin. J Biol Chem 245: 1467-1471.
36. Kurosawa Y, Ikeda K, Igami F (1973) Alpha-L-rhamnosidase of the liver of Turbo cornutus and Aspergillus niger. J Biochem 73: 31-37.
37. Mamma D, Kalogeris E, Hatzinikolaou DG, Lekanidou A, Kekos D, Macris BJ, Christakopoulos P (2004) Biochemical characterization of the multi-enzyme system produced by Penicillium decumbens grown on rutin. Food Biotechnol 18: 1-18.
38. Manzanares P, de Graaf LH, Visser J (1997) Purification and characterization of an a-L-rhamnosidase from Aspergillus niger. FEMS Microbiol Lett 157: 279-283.
39. Manzanares P, Orejas M, Ibanez E, Valles S, Ramon D (2000) Purification and characterization of an α-L-rhamnosidase from Aspergillus nidulans. Lett Appl Microbiol 31: 198-202.
40. Manzanares P, van den Broeck HC, de Graaf LH, Visser J (2001) Purification and characterization of two different α-L-rhamnosidases, RhaA and RhaB, from Aspergillus aculeatus. Appl Environ Microbiol 67: 2230-2234.
41. Medina ML, Kiernan VA, Francisco WA (2004) Proteomic analysis of rutin-induced secreted proteins from Aspergillus flavus. Fungal Genet Biol 41: 327-335.
42. Medina ML, Haynes PA, Breci L, Francisco WA (2005) Analysis of secreted proteins from Aspergillus flavus. Proteomics 5: 3153-3161.
43. Merkens H, Fetzner S (2008) Transcriptional analysis of the queD gene coding for quercetinase of Streptomyces sp. FLA. FEMS Microbiol Lett 287: 100-107.
44. Merkens H, Sielker S, Rose K, Fetzner S (2007) A new monocupin quercetinase of Streptomyces sp. FLA: identification and heterologous expression of the queD gene and activity of the recombinant enzyme towards different flavonols. Arch Microbiol 187: 475-487.
45. Merkens H, Kappl R, Jakob RP, Schmid FX, Fetzner S (2008) Quercetinase QueD of Streptomyces sp. FLA, a monocupin dioxygenase with a preference for nickel and cobalt. Biochemistry 47: 12185-12196.
46. Mills ENC, Jenkins J, Marigheto N, Belton PS, Gunning AP, Morris VJ (2002) Allergens of the cupin superfamily. Biochem Soc Trans 30: 925-929.
47. Monti D, Pisvejcova A, Kren V, Lama M, Riva S (2004) Generation of an a-L-rhamnosidases library and its application for the selective derhamnosylation of natural products. Biotechnol Bioeng 87: 763-771.
48. Narikawa T, Karaki Y, Shinoyama H, Fujii T (1998) Rutin degradation by culture filtrates from Penicillia. Nippon Nogeik Kaishi 72: 473-479.
49. Narikawa T, Shinoyama H, Fujii T (2000) A β-rutinosidase from Penicillium rugulosum IFO 7242 that is a peculiar flavonoid glycosidase. Biosci Biotechnol Biochem 64: 1317-1319.
50. Neznanov N, Kondratova A, Chumakov KM, Neznanova L, Kondratov R, Banerjee AK, Gudkov AV (2008) Quercetinase pirin makes poliovirus replication resistant to flavonoid quercetin. DNA Cell Biol 27: 191-198.
51. Noguchi I (1963) The degradation of flavonols by Pullularia fermentans var. candida. Bot Mag Tokyo 76: 191-198.
52. Oka T, Simpson FJ (1971) Quercetinase: a dioxygenase containing copper. Biochem Biophys Res Commun 43: 1-5.
53. Oka T, Simpson FJ (1972) Degradation of rutin by Aspergillus flavus. Quercetinase: isolation of a low molecular weight form containing less carbohydrate. Can J Microbiol 18: 1171-1175.
54. Oka T, Simpson FJ, Child JJ, Mills SC (1971) Degradation of rutin by Aspergillus flavus. Purification of the dioxygenase, quercetinase. Can J Microbiol 17: 111-118.
55. Oka T, Simpson FJ, Krishnamurty HG (1972) Degradation of rutin by Aspergillus flavus. Studies on specificity, inhibition and possible reaction mechanism of quercetinase. Can J Microbiol 18: 493-508.
56. Omori T, Shiozawa K, Sekiya M, Minoda Y (1986) Formation of 2, 4, 6-trihydroxy-carboxylic acid and 2-protocatechuoylphloroglucinol carboxylic acid from rutin by bacteria. Agric Biol Chem Tokyo 50: 779-780.
57. Padrn J, Grist KL, Clark JB, Wender SH (1960) Specificity studies on an extracellular enzyme preparation obtained from quercetin grown cells of Aspergillus. Biochem Biophys Res Commun 3: 412-416.
58. Pang H, Bartlam M, Zeng Q, Miyatake H, Hisano T, Miki K, Wong L, Gao GF, Rao Z (2004) Crystal structure of human pirin. J Biol Chem 279: 1491-1498.
59. Pietta P-G (2000) Flavonoids as antioxidants. J Nat Prod 63: 1035-1042.
60. Pillai BVS, Swarup S (2002) Elucidation of the flavonoid catabolism pathway in Pseudomonas putida PML2 by comparative metabolic profiling. Appl Environ Microbiol 68: 143-151.
61. Puti M, Kalra S (2005) Purification and characterization of naringinase from a newly isolated strain of Aspergillus niger 1344 for the transformation of flavonoids. World J Microbiol Biotechnol 21: 753-758.
62. Rajavel M, Kulkarni NN, Gopal B (2008) Conformational studies suggest that the double stranded β helix scaffold provides an optimal balance between protein stability and function. Protein Pept Lett 15: 244-249.
63. Rao JR, Cooper JE (1994) Rhizobia catabolize nod gene-inducing flavonoids via C-ring fission mechanisms. J Bacteriol 176: 5409-5413.
64. Rao KV, Weisner NT (1981) Microbial transformation of quercetin by Bacillus cereus. Appl Environ Microbiol 42: 450-452.
65. Rao JR, Sharma ND, Hamilton JTG, Boyd DR, Cooper JE (1991) Biotransformation of the pentahydroxy flavone quercetin by Rhizobium loti and Bradyrhizobium stains (Lotus). Appl Environ Microbiol 57: 1563-1565.
66. T (DSM 43046). Plasmid 55: 249-254.
67. Schaab MR, Barney BM, Francisco WA (2006) Kinetic and spectroscopic studies on the quercetin 2, 3-dioxygenase from Bacillus subtilis. Biochemistry 45: 1009-1016.
68. Schneider H, Blaut M (2000) Anaerobic degradation of flavonoids by Eubacterium ramulus. Arch Microbiol 173: 71-75.
69. Schoefer L, Mohan R, Schwiertz A, Braune A, Blaut M (2003) Anaerobic degradation of flavonoids by Clostridium orbiscindens. Appl Environ Microbiol 69: 5849-5854.
70. Siegbahn PEM (2004) Hybrid DFT study of the mechanism of quercetin 2, 3-dioxygenase. Inorg Chem 43: 5944-5953.
71. Simpson FJ, Talbot G, Westlake DWS (1960) Production of carbon monoxide in the enzymatic degradation of rutin. Biochem Biophys Res Commun 2: 15-18.
72. Simpson FJ, Narasimhachari N, Westlake DWS (1963) Degradation of rutin by Aspergillus flavus. The carbon monoxide producing system. Can J Microbiol 9: 15-25.
73. Steiner RA, Kalk KH, Dijkstra BW (2002a) Anaerobic enzyme substrate structures provide insight into the reaction mechanism of the copper-dependent quercetin 2, 3-dioxygenase. Proc Natl Acad Sci USA 99: 16625-16630.
74. Steiner RA, Kooter IM, Dijkstra BW (2002b) Functional analysis of the copper-dependent quercetin 2, 3-dioxygenase. 1. Ligand-induced coordination changes probed by X-ray crystallography: inhibition, ordering effect, and mechanistic insights. Biochemistry 41: 7955-7962.
75. Steiner RA, Meyer-Klaucke W, Dijkstra BW (2002c) Functional analysis of the copper-dependent quercetin 2, 3-dioxygenase. 2. X-ray absorption studies of native enzyme and anaerobic complexes with the substrates quercetin and myricetin. Biochemistry 41: 7963-7968.
76. Tranchimand S, Tron T, Gaudin C, Iacazio G (2005) Evaluation of phenolics and sugars as inducers of quercetinase activity in Penicillium olsonii. FEMS Microbiol Lett 253: 289-294.
77. Tranchimand S, Tron T, Gaudin C, Iacazio G (2006) First chemical synthesis of three natural depsides involved in flavonoid catabolism and related to quercetinase catalysis. Synth Commun 36: 587-597.
78. Tranchimand S, Ertel G, Gaydou V, Gaudin C, Tron T, Iacazio G (2008) Biochemical and molecular characterization of a quercetinase from Penicillium olsonii. Biochimie 90: 781-789.
79. van den Bosch M, Swart M, van Gunsteren WN, Canters GW (2004) Simulation of the substrate cavity dynamics of quercetinase. J Mol Biol 344: 725-738.
80. van der Heiden M, Nondmann DH, van der Helm MJ, Verrips CT, Swarthoff T, Smits A (1998) WO1997EP07138 19971210.
81. Westlake DWS (1963) Microbial degradation of quercitrin. Can J Microbiol 9: 211-220.
82. Westlake DWS, Simpson FJ (1961) Degradation of rutin by Aspergillus flavus. Factors affecting production of the enzyme system. Can J Microbiol 7: 33-44.
83. Westlake DWS, Spencer JFT (1966) The utilisation of flavonoid compounds by yeast and yeast like fungi. Can J Microbiol 12: 165-174.
84. Westlake DWS, Talbot G, Blakley ER, Simpson FJ (1959) Microbial decomposition of rutin. Can J Microbiol 5: 621-629.
85. Westlake DWS, Roxburgh JM, Talbot G (1961) Microbial production of carbon monoxide from flavonoids. Nature 189: 510-511.
86. Winter J, Moore LH, Dowell VR Jr, Bokkenheuser VD (1989) C-ring cleavage of flavonoids by human intestinal bacteria. Appl Environ Microbiol 55: 1203-1208.
87. Yoshida K-I, Ohki Y-H, Murata M, Kinehara M, Matsuoka H, Satomura T, Ohki R, Kumano M, Yamane K, Kunamoto K, Fujita Y (2004) Bacillus subtilis LmrA is a repressor of the lmrAB and yxaGH operons: identification of its binding site and functional analysis of lmrB and yxaGH. J Bacteriol 186: 5640-5648.