1mpy › Citations

An archetypical extradiol-cleaving catecholic dioxygenase: the crystal structure of catechol 2,3-dioxygenase (metapyrocatechase) from Ppseudomonas putida mt-2.

Kita A, Kita S, Fujisawa I, Inaka K, Ishida T, Horiike K, Nozaki M, Miki K
Structure 7 25-34 (1999)
Cited: 74 times
EuropePMC logo PMID: 10368270

Abstract

Background

Catechol dioxygenases catalyze the ring cleavage of catechol and its derivatives in either an intradiol or extradiol manner. These enzymes have a key role in the degradation of aromatic molecules in the environment by soil bacteria. Catechol 2, 3-dioxygenase catalyzes the incorporation of dioxygen into catechol and the extradiol ring cleavage to form 2-hydroxymuconate semialdehyde. Catechol 2,3-dioxygenase (metapyrocatechase, MPC) from Pseudomonas putida mt-2 was the first extradiol dioxygenase to be obtained in a pure form and has been studied extensively. The lack of an MPC structure has hampered the understanding of the general mechanism of extradiol dioxygenases.

Results

The three-dimensional structure of MPC has been determined at 2.8 A resolution by the multiple isomorphous replacement method. The enzyme is a homotetramer with each subunit folded into two similar domains. The structure of the MPC subunit resembles that of 2,3-dihydroxybiphenyl 1,2-dioxygenase, although there is low amino acid sequence identity between these enzymes. The active-site structure reveals a distorted tetrahedral Fe(II) site with three endogenous ligands (His153, His214 and Glu265), and an additional molecule that is most probably acetone.

Conclusion

The present structure of MPC, combined with those of two 2,3-dihydroxybiphenyl 1,2-dioxygenases, reveals a conserved core region of the active site comprising three Fe(II) ligands (His153, His214 and Glu265), one tyrosine (Tyr255) and two histidine (His199 and His246) residues. The results suggest that extradiol dioxygenases employ a common mechanism to recognize the catechol ring moiety of various substrates and to activate dioxygen. One of the conserved histidine residues (His199) seems to have important roles in the catalytic cycle.

Articles - 1mpy mentioned but not cited (15)

  1. Crystallographic comparison of manganese- and iron-dependent homoprotocatechuate 2,3-dioxygenases. Vetting MW, Wackett LP, Que L, Lipscomb JD, Ohlendorf DH. J Bacteriol 186 1945-1958 (2004)
  2. Prediction of catalytic residues using Support Vector Machine with selected protein sequence and structural properties. Petrova NV, Wu CH. BMC Bioinformatics 7 312 (2006)
  3. Protein surface analysis for function annotation in high-throughput structural genomics pipeline. Binkowski TA, Joachimiak A, Liang J. Protein Sci 14 2972-2981 (2005)
  4. A measure of the promiscuity of proteins and characteristics of residues in the vicinity of the catalytic site that regulate promiscuity. Chakraborty S, Rao BJ. PLoS One 7 e32011 (2012)
  5. Functional annotation by identification of local surface similarities: a novel tool for structural genomics. Ferrè F, Ausiello G, Zanzoni A, Helmer-Citterich M. BMC Bioinformatics 6 194 (2005)
  6. Crystal structure and functional analysis of the extradiol dioxygenase LapB from a long-chain alkylphenol degradation pathway in Pseudomonas. Cho JH, Jung DK, Lee K, Rhee S. J Biol Chem 284 34321-34330 (2009)
  7. Expression of Xhdsi-1VOC, a novel member of the vicinal oxygen chelate (VOC) metalloenzyme superfamily, is up-regulated in leaves and roots during desiccation in the resurrection plant Xerophyta humilis (Bak) Dur and Schinz. Mulako I, Farrant JM, Collett H, Illing N. J Exp Bot 59 3885-3901 (2008)
  8. Toxoflavin lyase requires a novel 1-His-2-carboxylate facial triad. Fenwick MK, Philmus B, Begley TP, Ealick SE. Biochemistry 50 1091-1100 (2011)
  9. OPUS-Dom: applying the folding-based method VECFOLD to determine protein domain boundaries. Wu Y, Dousis AD, Chen M, Li J, Ma J. J Mol Biol 385 1314-1329 (2009)
  10. Accurate prediction of protein catalytic residues by side chain orientation and residue contact density. Chien YT, Huang SW. PLoS One 7 e47951 (2012)
  11. Isolation and characterization of two novel halotolerant Catechol 2, 3-dioxygenases from a halophilic bacterial consortium. Guo G, Fang T, Wang C, Huang Y, Tian F, Cui Q, Wang H. Sci Rep 5 17603 (2015)
  12. Origin of methyl torsional barrier in 1-methyl-2(1H)-pyridinimine and 3-methyl-2(1H)-pyridone: II. Ground state. Pradhan B, Sinha RK, Singh BP, Kundu T. J Chem Phys 126 114313 (2007)
  13. The Promiscuous sumA Missense Suppressor from Salmonella enterica Has an Intriguing Mechanism of Action. Cole AE, Hani FM, Altman R, Meservy M, Roth JR, Altman E. Genetics 205 577-588 (2017)
  14. The ability of salts to stabilize proteins in vivo or intracellularly correlates with the Hofmeister series of ions. Hani FM, Cole AE, Altman E. Int J Biochem Mol Biol 10 23-31 (2019)
  15. Activity of a carboxyl-terminal truncated form of catechol 2,3-dioxygenase from Planococcus sp. S5. Hupert-Kocurek K, Wojcieszyńska D, Guzik U. ScientificWorldJournal 2014 598518 (2014)


Reviews citing this publication (9)

  1. Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Gerlt JA, Babbitt PC. Annu Rev Biochem 70 209-246 (2001)
  2. Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes. Schofield CJ, Zhang Z. Curr Opin Struct Biol 9 722-731 (1999)
  3. Protein design: toward functional metalloenzymes. Yu F, Cangelosi VM, Zastrow ML, Tegoni M, Plegaria JS, Tebo AG, Mocny CS, Ruckthong L, Qayyum H, Pecoraro VL. Chem Rev 114 3495-3578 (2014)
  4. The ins and outs of ring-cleaving dioxygenases. Vaillancourt FH, Bolin JT, Eltis LD. Crit Rev Biochem Mol Biol 41 241-267 (2006)
  5. Immobilization as a strategy for improving enzyme properties-application to oxidoreductases. Guzik U, Hupert-Kocurek K, Wojcieszyńska D. Molecules 19 8995-9018 (2014)
  6. Non-heme iron oxygenases. Ryle MJ, Hausinger RP. Curr Opin Chem Biol 6 193-201 (2002)
  7. Recent advances in lignin valorization with bacterial cultures: microorganisms, metabolic pathways, and bio-products. Xu Z, Lei P, Zhai R, Wen Z, Jin M. Biotechnol Biofuels 12 32 (2019)
  8. Oxygenases: mechanisms and structural motifs for O(2) activation. Bugg TD. Curr Opin Chem Biol 5 550-555 (2001)
  9. Biophysical analyses of designed and selected mutants of protocatechuate 3,4-dioxygenase1. Brown CK, Vetting MW, Earhart CA, Ohlendorf DH. Annu Rev Microbiol 58 555-585 (2004)

Articles citing this publication (50)

  1. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VA, Fouts DE, Gill SR, Pop M, Holmes M, Brinkac L, Beanan M, DeBoy RT, Daugherty S, Kolonay J, Madupu R, Nelson W, White O, Peterson J, Khouri H, Hance I, Chris Lee P, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, Moestl D, Wedler H, Lauber J, Stjepandic D, Hoheisel J, Straetz M, Heim S, Kiewitz C, Eisen JA, Timmis KN, Düsterhöft A, Tümmler B, Fraser CM. Environ Microbiol 4 799-808 (2002)
  2. Using a library of structural templates to recognise catalytic sites and explore their evolution in homologous families. Torrance JW, Bartlett GJ, Porter CT, Thornton JM. J Mol Biol 347 565-581 (2005)
  3. Convergent evolution of enzyme active sites is not a rare phenomenon. Gherardini PF, Wass MN, Helmer-Citterich M, Sternberg MJ. J Mol Biol 372 817-845 (2007)
  4. Crystal structure of an aromatic ring opening dioxygenase LigAB, a protocatechuate 4,5-dioxygenase, under aerobic conditions. Sugimoto K, Senda T, Aoshima H, Masai E, Fukuda M, Mitsui Y. Structure 7 953-965 (1999)
  5. Crystal structure of Pseudomonas fluorescens 4-hydroxyphenylpyruvate dioxygenase: an enzyme involved in the tyrosine degradation pathway. Serre L, Sailland A, Sy D, Boudec P, Rolland A, Pebay-Peyroula E, Cohen-Addad C. Structure 7 977-988 (1999)
  6. The 1.8 A crystal structure of catechol 1,2-dioxygenase reveals a novel hydrophobic helical zipper as a subunit linker. Vetting MW, Ohlendorf DH. Structure 8 429-440 (2000)
  7. Crystal structures of the reaction intermediate and its homologue of an extradiol-cleaving catecholic dioxygenase. Sato N, Uragami Y, Nishizaki T, Takahashi Y, Sazaki G, Sugimoto K, Nonaka T, Masai E, Fukuda M, Senda T. J Mol Biol 321 621-636 (2002)
  8. O2 Activation by Non-Heme Iron Enzymes. Solomon EI, Goudarzi S, Sutherlin KD. Biochemistry 55 6363-6374 (2016)
  9. The crystal structures of Zea mays and Arabidopsis 4-hydroxyphenylpyruvate dioxygenase. Fritze IM, Linden L, Freigang J, Auerbach G, Huber R, Steinbacher S. Plant Physiol 134 1388-1400 (2004)
  10. Crystal structure of methylmalonyl-coenzyme A epimerase from P. shermanii: a novel enzymatic function on an ancient metal binding scaffold. McCarthy AA, Baker HM, Shewry SC, Patchett ML, Baker EN. Structure 9 637-646 (2001)
  11. The role of the conserved residues His-246, His-199, and Tyr-255 in the catalysis of catechol 2,3-dioxygenase from Pseudomonas stutzeri OX1. Viggiani A, Siani L, Notomista E, Birolo L, Pucci P, Di Donato A. J Biol Chem 279 48630-48639 (2004)
  12. Elucidation of the 4-hydroxyacetophenone catabolic pathway in Pseudomonas fluorescens ACB. Moonen MJ, Kamerbeek NM, Westphal AH, Boeren SA, Janssen DB, Fraaije MW, van Berkel WJ. J Bacteriol 190 5190-5198 (2008)
  13. Crystal structures of substrate free and complex forms of reactivated BphC, an extradiol type ring-cleavage dioxygenase. Uragami Y, Senda T, Sugimoto K, Sato N, Nagarajan V, Masai E, Fukuda M, Mitsu Y. J Inorg Biochem 83 269-279 (2001)
  14. Catechol 2,3-dioxygenase and other meta-cleavage catabolic pathway genes in the 'anaerobic' termite gut spirochete Treponema primitia. Lucey KS, Leadbetter JR. Mol Ecol 23 1531-1543 (2014)
  15. The role of histidine 200 in MndD, the Mn(II)-dependent 3,4-dihydroxyphenylacetate 2,3-dioxygenase from Arthrobacter globiformis CM-2, a site-directed mutagenesis study. Emerson JP, Wagner ML, Reynolds MF, Que L, Sadowsky MJ, Wackett LP. J Biol Inorg Chem 10 751-760 (2005)
  16. Characterization of three XylT-like [2Fe-2S] ferredoxins associated with catabolism of cresols or naphthalene: evidence for their involvement in catechol dioxygenase reactivation. Hugo N, Meyer C, Armengaud J, Gaillard J, Timmis KN, Jouanneau Y. J Bacteriol 182 5580-5585 (2000)
  17. Biochemical characterization of L-DOPA 2,3-dioxygenase, a single-domain type I extradiol dioxygenase from lincomycin biosynthesis. Colabroy KL, Hackett WT, Markham AJ, Rosenberg J, Cohen DE, Jacobson A. Arch Biochem Biophys 479 131-138 (2008)
  18. Molecular basis of mitomycin C resistance in streptomyces: structure and function of the MRD protein. Martin TW, Dauter Z, Devedjiev Y, Sheffield P, Jelen F, He M, Sherman DH, Otlewski J, Derewenda ZS, Derewenda U. Structure 10 933-942 (2002)
  19. Rational design of catechol-2, 3-dioxygenase for improving the enzyme characteristics. Wei J, Zhou Y, Xu T, Lu B. Appl Biochem Biotechnol 162 116-126 (2010)
  20. Tuning the Regiospecificity of Cleavage in FeIII Catecholate Complexes: Tridentate Facial versus Meridional Ligands. Jo DH, Que L. Angew Chem Int Ed Engl 39 4284-4287 (2000)
  21. Determination of the active site of Sphingobium chlorophenolicum 2,6-dichlorohydroquinone dioxygenase (PcpA). Machonkin TE, Holland PL, Smith KN, Liberman JS, Dinescu A, Cundari TR, Rocks SS. J Biol Inorg Chem 15 291-301 (2010)
  22. Intersubunit interaction and catalytic activity of catechol 2,3-dioxygenases. Okuta A, Ohnishi K, Yagame S, Harayama S. Biochem J 371 557-564 (2003)
  23. Defining a kinetic mechanism for l-DOPA 2,3 dioxygenase, a single-domain type I extradiol dioxygenase from Streptomyces lincolnensis. Colabroy KL, Smith IR, Vlahos AH, Markham AJ, Jakubik ME. Biochim Biophys Acta 1844 607-614 (2014)
  24. Mononuclear iron(III) complexes of 3N ligands in organized assemblies: spectral and redox properties and attainment of regioselective extradiol dioxygenase activity. Anitha N, Palaniandavar M. Dalton Trans 40 1888-1901 (2011)
  25. Site-directed mutagenesis of gentisate 1,2-dioxygenases from Klebsiella pneumoniae M5a1 and Ralstonia sp. strain U2. Luo S, Liu DQ, Liu H, Zhou NY. Microbiol Res 161 138-144 (2006)
  26. Synthesis, structure, spectra and reactivity of iron(III) complexes of facially coordinating and sterically hindering 3N ligands as models for catechol dioxygenases. Sundaravel K, Dhanalakshmi T, Suresh E, Palaniandavar M. Dalton Trans 7012-7025 (2008)
  27. The interactions in the carboxyl terminus of human 4-hydroxyphenylpyruvate dioxygenase are critical to mediate the conformation of the final helix and the tail to shield the active site for catalysis. Lin JF, Sheih YL, Chang TC, Chang NY, Chang CW, Shen CP, Lee HJ. PLoS One 8 e69733 (2013)
  28. Biodegradation of phenanthrene by Pseudomonas sp. strain PPD: purification and characterization of 1-hydroxy-2-naphthoic acid dioxygenase. Deveryshetty J, Phale PS. Microbiology (Reading) 155 3083-3091 (2009)
  29. Investigation of acid-base catalysis in the extradiol and intradiol catechol dioxygenase reactions using a broad specificity mutant enzyme and model chemistry. Brivio M, Schlosrich J, Ahmad M, Tolond C, Bugg TD. Org Biomol Chem 7 1368-1373 (2009)
  30. Iron(III) complexes of N2O and N3O donor ligands as functional models for catechol dioxygenase enzymes: ether oxygen coordination tunes the regioselectivity and reactivity. Sundaravel K, Suresh E, Saminathan K, Palaniandavar M. Dalton Trans 40 8092-8107 (2011)
  31. Molecular basis for the substrate selectivity of bicyclic and monocyclic extradiol dioxygenases. Vaillancourt FH, Fortin PD, Labbé G, Drouin NM, Karim Z, Agar NY, Eltis LD. Biochem Biophys Res Commun 338 215-222 (2005)
  32. Catalytic and regiospecific extradiol cleavage of catechol by a biomimetic iron complex. Chatterjee S, Sheet D, Paine TK. Chem Commun (Camb) 49 10251-10253 (2013)
  33. Purification and characterization of alkylcatechol 2,3-dioxygenase from butylphenol degradation pathway of Pseudomonas putida MT4. Takeo M, Nishimura M, Takahashi H, Kitamura C, Kato D, Negoro S. J Biosci Bioeng 104 309-314 (2007)
  34. Single-turnover kinetics of 2,3-dihydroxybiphenyl 1,2-dioxygenase reacting with 3-formylcatechol. Ishida T, Senda T, Tanaka H, Yamamoto A, Horiike K. Biochem Biophys Res Commun 338 223-229 (2005)
  35. Iron(III) complexes of tripodal tetradentate 4N ligands as functional models for catechol dioxygenases: the electronic vs. steric effect on extradiol cleavage. Balamurugan M, Vadivelu P, Palaniandavar M. Dalton Trans 43 14653-14668 (2014)
  36. The role of residue Thr249 in modulating the catalytic efficiency and substrate specificity of catechol-2,3-dioxygenase from Pseudomonas stutzeri OX1. Siani L, Viggiani A, Notomista E, Pezzella A, Di Donato A. FEBS J 273 2963-2976 (2006)
  37. A novel Bacillus ligniniphilus catechol 2,3-dioxygenase shows unique substrate preference and metal requirement. Adewale P, Lang A, Huang F, Zhu D, Sun J, Ngadi M, Yang TC. Sci Rep 11 23982 (2021)
  38. Conserved protein YecM from Escherichia coli shows structural homology to metal-binding isomerases and oxygenases. Zhang RG, Duke N, Laskowski R, Evdokimova E, Skarina T, Edwards A, Joachimiak A, Savchenko A. Proteins 51 311-314 (2003)
  39. Purification and partial characterization of the extradiol dioxygenase, 2'-carboxy-2,3-dihydroxybiphenyl 1,2-dioxygenase, in the fluorene degradation pathway from Rhodococcus sp. strain DFA3. Kotake T, Matsuzawa J, Suzuki-Minakuchi C, Okada K, Nojiri H, Iwata K. Biosci Biotechnol Biochem 80 719-725 (2016)
  40. Biomimetic iron(III) complexes of facially and meridionally coordinating tridentate 3N ligands: tuning of regioselective extradiol dioxygenase activity in organized assemblies. Sankaralingam M, Saravanan N, Anitha N, Suresh E, Palaniandavar M. Dalton Trans 43 6828-6841 (2014)
  41. Finding molecular dioxygen tunnels in homoprotocatechuate 2,3-dioxygenase: implications for different reactivity of identical subunits. Xu L, Zhao W, Wang X. Eur Biophys J 39 327-336 (2010)
  42. Homology modeling, simulation and molecular docking studies of catechol-2, 3-Dioxygenase from Burkholderia cepacia: Involved in degradation of Petroleum hydrocarbons. Ajao A, Kannan M, Yakubu S, Vj U, Jb A. Bioinformation 8 848-854 (2012)
  43. Modeling and analysis of the structure of the thermostable catechol 2,3-dioxygenase from Bacillus Stearothermophilus. Dai L, Ji C, Gao D, Wang J, Jiang T, Bi A, Sheng X, Mao Y. J Biomol Struct Dyn 19 75-83 (2001)
  44. Cloning and mutagenesis of catechol 2,3-dioxygenase gene from the gram-positive Planococcus sp. strain S5. Hupert-Kocurek K, Stawicka A, Wojcieszyńska D, Guzik U. J Mol Microbiol Biotechnol 23 381-390 (2013)
  45. Evaluation of the effect of cold atmospheric plasma on oxygenases' activities for application in water treatment technologies. Todorova Y, Yotinov I, Topalova Y, Benova E, Marinova P, Tsonev I, Bogdanov T. Environ Technol 40 3783-3792 (2019)
  46. Nonfunctional Missense Mutants in Two Well Characterized Cytosolic Enzymes Reveal Important Information About Protein Structure and Function. Cole AE, Hani FM, Allen BW, Kline PC, Altman E. Protein J 37 407-427 (2018)
  47. Structure Elucidation and Biochemical Characterization of Environmentally Relevant Novel Extradiol Dioxygenases Discovered by a Functional Metagenomics Approach. Sidhu C, Solanki V, Pinnaka AK, Thakur KG. mSystems 4 e00316-19 (2019)
  48. Bioconversion of 4-hydroxyestradiol by extradiol ring-cleavage dioxygenases from Novosphingobium sp. PP1Y. Mensitieri F, Bosso A, Dal Piaz F, Charlier B, Notomista E, Izzo V, Cafaro V. Sci Rep 13 1835 (2023)
  49. Correlation of thermostability and conformational changes of catechol 2, 3-dioxygenases from two disparate micro-organisms. Sokolova A, Huang SL, Duff A, Gilbert EP, Li WH. Biophys Chem 180-181 145-152 (2013)
  50. The role of halogen substituents and substrate pKa in defining the substrate specificity of 2,6-dichlorohydroquinone 1,2-dioxygenase (PcpA). Burrows JE, Paulson MQ, Altman ER, Vukovic I, Machonkin TE. J Biol Inorg Chem 24 575-589 (2019)


Related citations provided by authors (1)

  1. Crystallization and Preliminary X-Ray Diffraction Studies of Expressed Pseudomonas Putida Catechol 2,3-Dioxygenase. Kita A, Kita S, Inaka K, Ishida T, Horiike K, Nozaki M, Miki K J. Biochem. 122 201- (1997)

Quick links